Cutworm Moths

C Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) Beata GaBrys University of Zielona Gora, Poland, Zielona Gora Apterous females (called apterae) are green-yellow or greyish-green, with a dark head and two rows of dark spots dorsally on the thorax and abdomen. The body is covered with a thick greyish-white or bluish mealy wax (Fig. 1). The siphunculi (cornicles) are small and dark. The body is 1.6–2.6 mm long. Winged females (called alatae) are green, with the head and ventral side black, and black transverse bars on dorsal abdomen. The wax layer is thinner in the alatae than in the apterae. The body is 1.6–2.8 mm long. Males are winged. The number of chromosomes is 2n = 16. Cabbage aphid occurs throughout all the temperate and warm temperate parts of the world. B. brassicae lives in colonies that can contain hundreds to several thousand densely packed individuals. The type of cabbage aphid life cycle depends on the climatic conditions during winter. In colder regions it is holocyclic (sexual forms – winged males and apterous oviparous females (oviparae) – appear in autumn; females release a sex pheromone, nepetalactone, and after mating they lay overwintering eggs). Where the winter is mild, they are anholocyclic (aphids reproduce parthenogenetically the year round). Parthenogenetic females are viviparous (they give birth to nymphs). Depending on the temperature and humidity conditions, one cabbage aphid generation develops in 7–10 days. Cabbage aphid is monoecious, its host range consisting primarily of plants in the family Brassicaceae (=Cruciferae) in summer as well as in winter, including such important crops as oilseed rape and cabbage vegetables (head cabbage, Brussels sprouts, cauliflower, kale, collards). The host plants may be divided into three groups depending on their ability to support aphid populations: permanent, temporal, and accidental host plants. Permanent host plants support the cabbage aphid population throughout the whole vegetation period. A female may give birth to about 20 nymphs (larvae) in 10 days on these plants (e.g., Brassica napus L., B. oleracea L., Sinapis alba L.). Temporal host-plants support 2–3 aphid generations. A female feeding on temporal host plants produces about ten larvae in 10 days (such plants as Lepidium sativum L., Isatis tinctoria L.). On accidental host-plants, aphids may develop less than one generation (e.g., Thlaspi arvense L. (10 larvae/10 days/female), Capsella bursa-pastoris (L.) Med. (5 larvae/10 days/female), Lunaria annua L. (4 larvae/10 days/female), Erysimum cheiranthoides L. (0 larvae/10 days/female). Older nymphs and adult apterae leave plants in response to overcrowding and decline in plant quality; they move within a plant or between plants via touching stems or the soil. Winged morphs appear following overcrowding and decline in plant quality, or in reaction to environmental factors such as temperature (below 10–15°C for at 686 C Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae), Figure 1 Cabbage aphids on cabbage leaf. Note white waxy exudates on aphid bodies. least 24 h), and seasonal changes in day length (photoperiod). Overcrowding alone is not responsible for appearance of winged forms in cabbage aphid colonies. During flight, cabbage aphid responds to physical and chemical stimuli. Shape, size, and density of plants, as well as light of high intensity (especially wavelengths of 550–590 nm) are significant cues. Particularly important is the contrast between light reflected from bare soil and plants. Summer migrants do not respond to host plant volatiles from large distances; however, they do react positively to host plant volatiles in close proximity, especially the volatile products of glucosinolate breakdown. While on the plant surface, B. brassicae is relatively unaffected by mechanical barriers. However, exceptionally dense hairs can protect plant parts against aphid infestation. Epicuticular wax structure also is important; cabbage aphids drop off smooth surfaces. Glucosinolates typical of a given plant species, and n-alkane mixture in epicuticular waxes present on the plant surface, can be recognized by cabbage aphids. It is not clear whether these chemicals bear any importance in host selection. The existence of external contact chemoreceptors at the tips of aphid antennae is not well documented. It is assumed that aphids tend to initiate stylet probes into plant tissues regardless of the nature of surface chemicals. Landing on an Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) unsuitable plant motivates cabbage aphids for new flights. Flight muscle autolysis occurs several days after settling and the start of reproduction. When probing (i.e., inserting and moving the stylets within plant tissues), cabbage aphid selects for high turgor and high amino acid, sucrose, and glucosinolate content in young and growing plant parts of its host plants. When aphid stylets are in peripheral tissues (epidermis and mesophyll), the continuation of probing depends on detection of chemical stimulants – glucosinolates – in mesophyll cells. Aphids are able to sample mesophyll cell content during brief cell punctures along the stylet pathway. Feeding deterrents may impede stylet penetration at epidermis and parenchymatous tissues as well as at vascular tissue level. When aphid stylets are in vascular tissues (phloem and xylem), cabbage aphid responds positively to a high content of amino-acid nitrogen, and at the same time it is relatively resistant to its loss. High nitrogen fertilization of soil promotes cabbage aphid population development under field conditions. The development of B. brassicae is positively correlated with treonine, tyrosine, alanine, leucine, and glutamic acid content, and negatively correlated with phenylalanine content. A minimum of 15% sucrose content stimulates feeding by the cabbage aphid. Such concentrations occur in phloem sap of growing leaves. Among plant allelochemicals, the glucosinolates are very strong phagostimulants for the cabbage aphid. In phloem sap of young leaves, the glucosinolate concentration reaches 10 mM. However, most glucosinolates do not have direct effect on aphid performance. Cabbage aphid fecundity is positively correlated with some alkenyl glucosinolates (e.g., progoitrin, sinigrin) content, and a negative correlation is found for indole ones (e.g., glucobrassicanapin, neoglucobrassicin). Glucosinolate metabolism in the aphid is not known. Some amount of the ingested glucosinolates is sequestered in cabbage aphid hemolymph. The glucosinolates may also be hydrolyzed by endogenous aphid myrosinases (aphid myrosinases are not identical with plant myrosinases). High lectin content in the phloem sap causes high mortality of B. brassicae. The possible C mechanism for this toxicity may be binding of lectin to chitinous structures in the stylets and foregut. Cabbage aphid may reduce plant growth by 35%, the number of side branches by 43%, and the oil content by over 10%. Aphids may cause 85% yield loss and may induce the increase in glucosinolate content in rapeseed. Content of certain amino acids (e.g., methionine) increases in phloem sap due to cabbage aphid feeding. B. brassicae transmits about 20 plant viruses. The natural enemies of the cabbage aphid are primarily generalist insect predators such as Coccinellidae and Carabidae (Coleoptera), Syrphidae (Diptera), Chrysopidae (Neuroptera), and parasitoids. There is only one primary parasitoid species of B. brassicae – Diaeretiella rapae (Mc Intosh) (Hymenoptera, Aphidiidae). It may reduce aphid populations by 30–40% at the peak infestation.  Crucifer Pests and their Management References Gabrys B (1999) Semiochemicals in the biology and ecology of the cabbage aphid Brevicoryne brassicae (L.). Zeszyty Naukowe Akademii Rolniczej we Wroclawiu. Rozprawy. CLXIV. 356. 84 pp Hafez M (1961) Seasonal fluctuations of population density of the cabbage aphid, Brevicoryne brassicae (L.) in the Netherlands and the role of its parasite, Aphidius (Diaeretiella) rapae (Curtis).Tijdscrift vor Plantenziekten 67:445–548 Klingauf FA (1987) Host plant finding and acceptance. In: Minks AK, Harrewijn P (eds) Aphids, their biology, natural enemies and control, vol 2B. Elsevier, Amsterdam, pp 209–223 Markkula M (1953) Biologisch-ökologische Untersuchungen uber die Khlblattlaus, Brevicoryne brassicae. (L.) (Hem., Aphididae) Ann Soc Zool Bot Fenn Van 15:1–133 Nault LR, Styer WE (1972) Effect of sinigrin on host selection by aphids. Entomol Exp Appl 15:423–437 Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) The cabbage looper is found in many crucifergrowing areas of the world, including parts of 687 688 C Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) Africa, Asia, Europe and North America. However, overwintering occurs only in warm-winter regions. The cabbage looper is highly dispersive, and adults have sometimes found at high altitudes and far from shore. Flight ranges of approximately 200 km have been estimated. Description and Life Cycle The number of generations completed per year varies from two to three in cool-summer climates to several overlapping generations in warmer climates. Development time (egg to adult) requires 18–25 days when insects are held at 32–21°C, respectively, so at least one generation per month could be completed successfully under favorable weather conditions. There is no diapause present in this insect, and although it is capable of spending considerable time as a pupa, it does not tolerate prolonged cold weather. It reinvades most temperate regions annually after overwintering in warmer latitudes. In the eastern United States, overwintering regularly occurs only in the southern half of Florida. back to form a loop and then projecting the front section (Fig. 3) of the body forward. The mature larva is predominantly green, but is usually marked with a distinct white stripe on each side. The thoracic legs and head capsule are usually pale green or brown. Dorsally, the larva bears several narrow, faint white stripes clustered into two broad white bands. In some cases the mature larva is entirely green. The body is narrower at the anterior end, and broadens toward the posterior. It measures 3–4 cm in length at maturity. Head capsule width is 0.29, 0.47, 0.74, 1.15, and 1.79 mm, respectively, for instars one through five. Larval development generally requires 19–20 days. Pupa At pupation, a white, thin, fragile cocoon in formed on the underside of foliage, in plant debris, or among clods of soil. The pupa measures about 2 cm in length. Duration of the pupal stage is about 4, 6, and 13 days at 32, 27, and 20°C, respectively. Egg Adult Cabbage looper eggs are hemispherical in shape, with the flat side affixed to foliage. They are deposited singly on either the upper or lower surface of the leaf, although clusters of six to seven eggs are not uncommon. The eggs are yellowish white or greenish in color, bear longitudinal ridges, and measure about 0.6 mm in diameter and 0.4 mm in height. Eggs hatch in about 2–5 days. The forewings of the cabbage looper moth are mottled gray-brown in color; the hind wings are light brown at the base, with the distal portions dark brown (Fig. 2). The forewing bears silvery white spots centrally: a U-shaped mark and a circle or dot that are often connected. The forewing spots, although slightly variable, serve to distinguish cabbage looper from most other crop-feeding noctuid moths. The moths have a wingspan of 33–38 mm. During the adult stage, which averages 10–12 days, 300–600 eggs are produced by females. Moths are considered to be seminocturnal because feeding and oviposition sometimes occurs about dusk. They may become active on cloudy days or during cool weather, but are even more active during the nighttime hours. Larva Young larvae initially are dusky white, but become pale green as they feed on foliage. They are somewhat hairy initially, but the number of hairs decreases rapidly as larvae mature. Larvae have three pairs of prolegs, and crawl by arching their Cabbage Looper, Tricoplusia ni (Hübner) (Lepidoptera: Noctuidae) C dogbane, Apocynum spp.; sunflower, Helianthus spp.; and others. Damage Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), Figure 2 Adult of cabbage looper, Trichoplusia ni. Cabbage loopers are leaf feeders, and in the first three instars they confine their feeding to the lower leaf surface, leaving the upper surface intact. The fourth and fifth instars chew large holes, and usually do not feed at the leaf margin. In the case of cabbage, however, they feed not only on the wrapper leaves, but also may bore into the developing head. Natural Enemies Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), Figure 3 Cabbage looper larva. Host Plants The cabbage looper feeds on a wide variety of cultivated plants and weeds. As the common name implies, it feeds readily on crucifers, and has been reported damaging broccoli, cabbage, cauliflower, Chinese cabbage, collards, kale, mustard, radish, rutabaga, turnip, and watercress. Other vegetable crops injured include beet, cantaloupe, celery, cucumber, lima bean, lettuce, parsnip, pea, pepper, potato, snap bean, spinach, squash, sweetpotato, tomato, and watermelon. Additional hosts are flower crops such as chrysanthemum, hollyhock, snapdragon, and sweetpea, and field crops such as cotton and tobacco. Surprisingly few common agricultural weeds are frequent hosts. Adults feed on nectar from a wide range of flowering plants, including clover, Trifolium spp.; goldenrod, Solidago canadensis; The cabbage looper is attacked by numerous natural enemies, and the effectiveness of each seems to vary greatly. Most studies note the effectiveness of wasp and tachinid parasitoids, and a nuclear polyhedrosis virus (NPV). During the latter instars, Voria ruralis (Fallen) (Diptera: Tachinidae), a solitary or gregarious endoparasite attacking the medium or large size larvae, often is the dominant cause of death, accounting for an average of about 53% mortality. Trichoplusia ni NPV causes about 12% mortality, and undetermined fungi about 10%. Copidosoma truncatellum (Dalman) (Hymenoptera: Encyrtidae) is the other significant mortality factor, but accounted for only six to seven percent mortality. Other studies reported that egg parasitism of cabbage looper by Trichogramma (Hymenoptera: Trichogrammatidae), while variable, could reach about 35%. Despite the abundance of parasitoids, however, T. ni NPV is usually considered the key factor affecting populations. Early signs of larval infection by NPV are a faint mottling of the abdomen in the area of the third to the sixth abdominal segments. This is followed by a more generalized blotchy appearance, and the caterpillar eventually becomes creamy white in color, swollen, and limp. Caterpillars die within 5–7 days of contracting the disease. 689 690 C Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae) Management Blacklight traps and pheromone traps have been used in an attempt to predict looper population densities. Pheromone releasers and blacklight traps can be combined to increase moth catches. Insecticide resistance has become a problem in cabbage looper control, but susceptibility varies widely among populations. Bacillus thuringiensis has long been used for effective suppression of cabbage looper, and has the advantage of not disrupting populations of beneficial insects.  Crucifer Pests and their Management  Vegetable Pests and their Management References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, 729 pp Elsey KD, Rabb RL (1970) Analysis of the seasonal mortality of the cabbage looper in North Carolina. Ann Entomol Soc Am 63:1597–1604 McEwen FL, Hervey GER (1960) Mass-rearing the cabbage looper, Trichoplusia ni, with notes on its biology in the laboratory. Ann Entomol Soc Am 53:229–234 Oatman ER, Platner GR (1969) An ecological study of insect populations on cabbage in southern California. Hilgardia 40:1–40 Shorey HH (1963) The biology of Trichoplusia ni (Lepidoptera: Noctuidae). II. Factors affecting adult fecundity and longevity. Ann Entomol Soc Am 56:476–480 Shorey HH, Andres LA, Hale RL (1962) The biology of Trichoplusia ni (Lepidoptera: Noctuidae). I. Life history and behavior. Ann Entomol Soc Am 55:591–597 Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae) John L. Capinera University of Florida, Gainesville, FL, USA Cabbage maggot (cabbage root fly) is known as a pest throughout the northern hemisphere. It apparently was introduced accidentally from Europe to North America in the early 1800s. Cabbage maggot thrives under cool conditions, and rarely is reported to be a pest south of about latitude 45 degrees north, and when it is, it usually occurs at a high elevation. Quite cold tolerant, it is found in some of the northernmost agricultural regions. Life History The number of generations occurring annually varies from one in the far north to three in optimal climates, although there are occasional reports of four generations. The generations may overlap considerably. A developmental threshold of about 6°C has been determined for most life stages. The time required for a complete generation is estimated at 40–60 days. Eggs normally are laid in the soil around the stem of cruciferous plants, but sometimes eggs are deposited directly on the stem of plants. The elongate eggs are white in color, and taper markedly at both ends, but one end is more blunt than the other. One side of the egg is flattened or slightly concave, with the opposite side convex. Eggs measure about 1.1 mm long and 0.34 mm wide. The eggs are often laid in clumps of a few eggs, but sometimes hundreds of eggs are found at the same location, evidence that more than one female may oviposit at the same spot. Females commonly produce 300–400 eggs during their life span of 30–60 days. Eggs hatch in 3–5 days, averaging about 3.5 days at 20°C. There are three instars. The length of the mouthparts (cephalopharyngeal skeleton) can be used to differentiate instars, with mean lengths of 0.44, 0.80, and 1.24 mm, respectively. The larvae are white in color and attain lengths of about 1.5, 3.7, and up to 8 mm, respectively. The mouth hooks are black. Located immediately behind the head is a pair of brownish fan-like spiracles, each of which is divided into about 12 lobes. Larvae feed externally and internally on roots, and internally on stem tissue. The larval period requires about 18–22 days under field conditions, but development time may be altered by weather. Exposure of first and Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae) second instar larvae to cool temperatures or short photoperiods seems to induce diapause in the pupal stage. The puparium is oval, bluntly rounded at both ends, and brown in color. The average length is 5.5 mm, with a range of 3.5–6.5 mm. The duration of the prepupal stage is about 3–5 days, and the pupa requires 12–25 days during the summer. However, this is the overwintering stage, so it is prolonged for 5–8 months in the overwintering generation(s). Overwintering pupae require at least 22 weeks of temperatures < 6°C to complete diapause development. The puparia from the summer generations are usually found in the soil immediately adjacent to the root on which the larvae last fed. Sometimes they occur within the plant tissue, including the aboveground stem tissue. Aestivation occurs in response to warm temperatures, above 20°C, and especially in response to hot temperatures, 27–30°C. In preparation for overwintering, the larvae seem to disperse further from the plant, and deeper into the soil. Overwintering puparia may be found 12–15 cm from the plant, and commonly are found in the soil at a depth of 10 cm. The adults are dark with gray markings (Fig. 4). The male bears three blackish longitudinal bands Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae), Figure 4 Adult cabbage maggot (cabbage root fly), Delia radicum (Linnaeus). C on the thorax, but these markings are less distinct on the female. The flies are quite bristly, and measure 5–7 mm long. Adults feed on nectar from flowering plants. If they obtain adequate food they may persist for 2–4 weeks, whereas they perish in 2–3 days if denied food. Adults are highly attracted to crucifers for oviposition. The preoviposition period of adults is about 6 days. Cabbage maggot commonly attacks cruciferous vegetable crops, including broccoli, Brussels sprouts, cabbage, cauliflower, collard, kale, kohlrabi, mustard, radish, rutabaga, turnip, and watercress. It has been reported from noncrucifer crops on occasion, but these are misidentifications that stem from the difficulty in accurately identifying this fly. Cruciferous weeds apparently do not play a significant role in the biology of this insect; although some appear to be suitable hosts, they rarely are mentioned in the economic entomology literature. Important natural enemies include staphylinids of several genera, particularly Aleochara sp. (Coleoptera: Staphylinidae); a wasp, Trybliographa rapae (Westwood) (Hymenoptera: Eucoilidae); and a mite, Trombidium sp. (Acari: Trombidiidae). Aleochara sp. attack the pupal stage of cabbage maggot, Trybliographa attacks the larvae, and the mite destroys the eggs. Natural control has been studied extensively in both Europe and North America. Egg predation by staphylinids and carabids may reach 90–95% annually. Aleochara are very effective predators, but become active too late in the spring to have much effect on first generation cabbage maggot. Trybliographa is fairly effective at high host densities, often parasitizing in excess of 50% of available hosts. Other natural enemies of the immature cabbage maggot include numerous hymenopterous parasitoids of questionable economic importance, carabids (Coleoptera: Carabidae) and ants (Hymenoptera: Formicidae). General predators undoubtedly attack the adults, but they are not considered to be important. Fungi are commonly observed infecting flies. Entomophthora muscae and Strongwellsea castrans cause epizootics among adults during wet weather, 691 692 C Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae) and though impressive, act too late to prevent early season crop damage. The spring generation tends to appear consistently, but latter generations are greatly influenced by weather. Rain and cool weather may decrease egg production and egg predation, and cause starvation of flies, but optimal egg production is associated with temperatures of 18–21°C, which corresponds well with the weather occurring during most spring generations. Pupal development is particularly susceptible to delay caused by hot temperatures, which normally is associated with summer generations. Dry soil is lethal to eggs. damage results in severe crop loss, and in this case the autumn generation may be quite important. The summer generation causes little damage. Damage tends to be greater on loamy sand soil than on sand or clay soil, but as a general rule light soils are more problem prone. Although most eggs are laid on the soil, a small number are sometimes deposited on plant tissue, resulting in injury by larvae to leaflets, especially to Brussels sprout buttons. Occasionally the growing points of plants are attacked, resulting in multiple heads. Management Damage Larvae (Fig. 5) damage crucifers by feeding on the roots and, to a much lesser degree, the stems or petioles of plants. Damage to leaf crops such as cabbage is most evident in the late spring; signs of feeding damage are initially seen as drooping or wilting of a few leaves, and then perhaps the entire plant. Delayed maturity and stunting are common responses to root maggot injury. Plant death often coincides with drought or water stress, when the injury to roots is fully expressed. When plants are small, five to ten maggots are necessary to kill the seedling. However, later in the season densities of 100 maggots or more may be supported satisfactorily if the plant has adequate water. Cabbage maggot larvae feed on the rootlets or feeder roots, but invariably move to the main or tap root as they mature. They scar the surface and burrow into the root. In the case of crops that are harvested for their root, such as radish and turnip, Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae), Figure 5 Mature cabbage maggot (larva of cabbage root fly), Delia radicum (Linnaeus). Adult flight periods can be monitored by using cone screen traps baited with crucifers. Baits are more effective than yellow sticky traps, although sticky trap captures are correlated with egg deposition rates. Horizontal surfaces are more suitable than vertical surfaces for landing by flies. Dispensers that release isothiocyanates, naturally occurring odors released by crucifers, can be used as lures. Color, but not leaf pattern, also can influence host selection. Water traps baited with isothiocyanate can be used to monitor population, but trap catches do not predict egg numbers accurately. Flight activity can be predicted from thermal unit accumulations. The overwintering (partly developed) generation require about 300 daydegrees (above a base temperature of 43°F). Subsequent generations require about 1200 degree-days. With the introduction of chlorinated hydrocarbon insecticides, damage by cabbage maggot was greatly reduced. Long-lasting insecticides, applied to the soil at planting, protect the roots from larvae. This remains the principal method of plant protection in commercial crucifer production, but the insecticides have been changed over time as resistance to insecticides developed. Loss of insecticide efficacy is due not only to selection for insecticide resistant insects, but enhanced degradation of insecticide by soil microbes. Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae) Insecticides are typically applied as a granular formulation over the seed bed or incorporated into the soil, or as a liquid drench. Foliar applications are sometimes made to suppress adults. Foliar application of insecticides, timed according to temperature accumulations, can be superior to soil applications or calendar-based sprays. Seed treatment can be an effective method of providing protection to seedlings, but it does not work well for all insecticides. Naphthalene has been investigated in Europe for repellency to ovipositing flies; although good protection occurs for about 6 weeks, the cost of application is high. Modification of planting and tillage practices is often recommended for reduction in cabbage maggot damage. Delayed planting is reported to allow the young plants to escape oviposition by the spring adults. Sanitation also is quite important, as the roots and stems of crucifers left in the field can be very suitable for autumn and early spring generations of cabbage maggot. Crop residues should be deeply buried, or pulled and allowed to dry completely. High plant densities are more attractive than low densities to flies, but because there are more plants on which to distribute the eggs, yield may be equivalent at both plant densities. Introducing diversity into the landscape, as by undersowing portions of a crucifer crop with clover, will disturb the normal host orientation pattern and reduce oviposition. Similarly, single row intercropping of crucifers with unrelated plants will greatly reduce the oviposition rate on crucifers. Physical manipulations of the crop environment also assist pest suppression. Crops covered tightly with row covers escape injury by cabbage maggot. Tar paper or cardboard discs, or collars made of other weather-resistant material, placed around the stem of seedlings have long been recommended as a physical barrier to reduce the ability of females to deposit eggs at the soil-stem interface. A precise fit is required, however, or the flies will circumvent the barrier. Reliable biological control techniques have not yet been developed. Entomopathogenic nematodes (Nematoda: Steinernematidae and C Heterorhabditidae) have been evaluated for suppression of larvae. Although heterorhabditid nematodes are attracted to cabbage maggot larvae and pupae, under field conditions they have not been shown to be effective. Steinernematid nematodes provide some suppression of cabbage maggot larvae in pot and field trials, but very high densities of nematodes are needed, at least 100,000 nematodes per plant. This is not entirely surprising because fly larvae are less susceptible to nematodes than are many other insects. In Europe, the potential of using the predatory beetle Aleochara bilineata (Gyllenhal) (Coleoptera: Staphylinidae) to achieve biological suppression of cabbage maggot is being studied; while technically feasible, the costs thus far are high. Despite the common name, cabbage is less attractive to cabbage maggots than some other crucifer crops. Chinese cabbage, mustard, rutabaga, and turnip tend to be more severely injured than cabbage. There also is some variation within vegetable crops in resistance to attack; fast growing varieties seem most injured. Overall, not much progress has been made on finding cultivars resistant to cabbage maggot.  Crucifer Pests and their Management Vegetable Pests and their Management References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, 729 pp Finch S (1989) Ecological considerations in the management of Delia pest species in vegetable crops. Ann Rev Entomol 34:117–137 Finch S (1993) Integrated management of the cabbage root fly and the carrot fly. Crop Protection 12:423–430 Fulton BB (1943) The cabbage maggot in North Carolina. North Carolina. Agr Exp Stn Bull 335, 24 pp Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae) The cabbageworm occurs in temperate regions around the world, and is easily confused with other common cabbage white butterflies. In most 693 694 C Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae) temperate areas, it is a serious pest if insecticides are not used to protect cabbage. In North America, it is known as the imported cabbageworm because it is an invader; in Europe it is known as the small white cabbage butterfly. Life Cycle and Description The complete life cycle of this insect requires 3–6 weeks, depending on weather. The number of generations reported annually is two to three in cool climates such as Canada, increasing to six to eight in southern areas. Egg Eggs are laid singly, usually on the lower surface of outer leaves of plants. The egg measures 0.5 mm in width and 1.0 mm in length, and initially is pale white in color but eventually turns yellowish. The egg is laid on end, with the point of attachment flattened and the distal end tapering to a blunt point. The shape is sometimes described as resembling a bullet. about 15 days to complete its development during August. Average development times for each instar at 19°C was observed to be 4.5, 3.0, 3.3, 4.1, and 7.8 days, respectively. All larval stages except the first instar bear a narrow yellow line running along the center of the back; this stripe is sometimes incomplete on the early instars. A broken yellow line, or series of yellow spots, also occurs on each side. Pupa Pupation normally occurs on the food plant. The chrysalis is about 18–20 mm in length, and varies in color, usually yellow, gray, green and speckled brown. A sharply angled, keel-like projection is evident dorsally on the thorax, and dorsolaterally on each side of the abdomen. At pupation, the chrysalis is anchored by the tip of the abdomen to the silk pad, and a strand of silk is loosely spun around the thorax. Pupation during the summer generations lasts about 11 days. The chrysalis is the overwintering stage, however, so its duration may be prolonged for months. The proportion of pupae that diapause increases as autumn progresses, so that at the time of the final generation all pupae are in diapause. Larva Adult The larva is green, velvety in appearance (Fig. 6), and bears five pairs of prolegs. There are five instars. Head capsule widths are about 0.4, 0.6, 0.97, 1.5, and 2.2 mm, respectively. Body lengths at maturity of each instar averages 3.2, 8.8, 14.0, 20.2, and 30.1 mm, respectively. The larva requires Upon emergence from the chrysalis the butterfly has a wingspan of about 4.5–6.5 cm. It is white above with black at the tips of the forewings. The front wings are also marked with black dots: two in the central area of each forewing in the female, and one in case of males (Fig. 7). When viewed from below, the wings generally are yellowish, and the black spots usually show faintly through the wings. The hind wing of each sex also bears a black spot on the anterior edge. The body of the butterfly is covered with dense hair, which is colored white in females, but darker in males. The adult typically lives about 3 weeks. The female produces 300–400 eggs. The adult is very active during the daylight hours, often moving from the crop to flowering weeds to feed. Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae), Figure 6 Larva of cabbageworm, Pieris rapae. Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae) C Cabbageworms feed on foliage, and if left unchecked often will reduce mature plants to stems and large veins. Although they prefer leafy foliage, larvae may burrow into the heads of broccoli and cabbage, especially as they mature. Larvae are often immobile, and difficult to dislodge, and may be overlooked when cleaning produce. Larvae produce copious quantities of fecal material which also contaminate and stain produce. glomeratus (L.) (Hymenoptera: Braconidae) attacks the early instars, and emerges from the mature larva as it prepares to pupate. A. glomeratus is readily observed in the field, searching diligently on foliage for larvae. Dead cabbageworm larvae are often found with clusters of 20–30 A. glomeratus cocoons attached. In some areas tachinids (Diptera: Tachinidae) are more important than wasps. Virus and fungal diseases of imported cabbageworm have been reported, but the predominant natural disease in a granulosis virus (GV). P. rapae GV occurs most commonly under high density conditions, and often among late instar larvae after they have consumed the exterior foliage of plants and are forced into close contact. Over 90% mortality of larvae due to natural occurrence of this disease has been reported. In the early stages of infection, larvae are inactive and paler in color. As the disease progresses, the caterpillar body turns yellow, and tends to appear bloated. After death, the body blackens, the integument ruptures, and the liquefied body contents ooze on the plant foliage. Rainfall has a major roll in assisting the spread of the virus on the plant, and from the soil to the plant. Host Plants Management Larvae of this insect feed widely on plants in the family Cruciferae, but occasionally on a few other plant families that contain mustard oils. Commonly attacked are vegetable crops such as broccoli, Brussels sprouts, cabbage, cauliflower, collard, horseradish, kale, and kohlrabi. Also sometimes attacked are flowers such as nasturtium and sweet alyssum, and weeds in the family Cruciferae. Adults sip nectar from flowers, and are commonly seen feeding at a number of plants. Imported cabbageworm are readily killed by foliar application of insecticides, including the bacterial insecticide Bacillus thuringiensis. Crucifer crops differ is their susceptibility to attack by imported cabbageworm. Chinese cabbage, turnip, mustard, rutabaga, and kale are less preferred than cabbage, collards, Brussels sprouts, broccoli, and cauliflower. Some cultivars of certain crops also have moderate levels of resistance to infestation by imported cabbageworm. Cabbage butterflies avoid ovipositing on red cabbage varieties. However, larval survival is favored by red cabbage, so red varieties are not a satisfactory solution to the caterpillar problem.  Crucifer Pests and their Management  Vegetable Pests and their Management Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae), Figure 7 Adult of cabbageworm. Damage Natural Enemies The imported cabbageworm is subject to numerous predators, parasitoids, and diseases. Apanteles 695 696 C Cactus Flies References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, 729 pp Chittenden FH (1916) The common cabbage worm. USDA Farmers’ Bull 766, 16 pp Harcourt DG (1963) Biology of cabbage caterpillars in eastern Ontario. Proc Entomol Soc Ontario 93:61–75 Richards OW (1940) The biology of the small white butterfly (Pieris rapae. ), with special reference to the factors controlling its abundance. J Anim Ecol 9:243–288 Cactus Flies Members of the family Neriidae (order Diptera).  Flies Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) Jesusa C. LeGaspi, BenJamin C. LeGaspi Jr. USDA-ARS, FAMU-Center for Biological Control, Tallahassee, FL, USA USDA-ARS, FAMU-Center for Biological Control, Tallahassee, FL, USA The cactus moth became a textbook example of successful classical biological control after it was imported from Argentina into Australia in 1926 to control invasive Opuntia cacti. To date, the moth continues to play an active role in controlling Opuntia in Australia. In 1989, Cactoblastis was found in Florida (USA), subsequently spreading northward to South Carolina and westward to Alabama by 2004. The arrival of the moth in the United States was cause for concern in the cactus industry. In the United States, cacti are grown primarily as ornamentals in Arizona, California, Nevada, New Mexico, and Texas. Highest nursery production is in Arizona (wholesale and retail values of $4.5 million and $9.5 million, respectively), followed by southern California. Despite attempts to prevent migration to the valuable cactus growing regions in Mexico, Cactoblastis was found in Isla Mujeres, Mexico, in August 2006. Over 250,000 ha are cultivated in Mexico producing annual economic revenue of about $50 million (1990–1998). Although the importations into Australia and the invasion into the USA and Mexico occurred many years apart, the Cactoblastis moth has now become a cautionary example in the practice of biological control. Research on the moth has shifted from mass release to control. Here, we attempt to summarize the current state of knowledge on the biology, distribution and control methods against Cactoblastis. Biology Like other cactus-feeding moths, the Cactoblastis female lays its eggs (Fig. 8) on top of each other to form an “eggstick,” often averaging 60–100 eggs per eggstick. Young larvae burrow into the cactus cladode through a single entry hole, negating the effect of the cactus secretions. Larvae feed collectively within the cladode for about 2 months in the summer and four in the winter. Afterwards, the larvae exit the plant to pupate in the leaf litter or soil. Adult lifespan is short, about 9 days, or ranging from about 5 days at 34°C to about 12 days at 18°C in females. Sex ratios are typically 1:1. Depending on climate and season, Cactoblastis undergoes 2–3 generations per year. In South Africa, summer and winter generation times are 113–132 days and 234–256 days, respectively. In Australia, summer and winter generation times are 100–120 and 235–265 days, respectively. Under laboratory conditions, generation time ranges from 67 days at 30°C to 185 days at 18°C. Duration of lifestages is generally: egg (50 days); larval (130–180 days); pupal (40–70 days). Duration of immature life stages is affected by temperature Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Figure 8 Life cycle of Cactoblastis cactorum: (a) eggs deposited on a cactus spine, forming an “eggstick”; (b) larvae hatching from eggs; (c) mature larvae are strikingly colored orange and black; (d) pupae and a pupal case, with arrows pointing to the genital slit, a character that can be used to sex the pupae; (e) male (left) and female (right) moths; (f) a cactus pad hollowed out by feeding of the larvae. Note that the larvae are visible within the pad (photographs by Ignacio Baez). 697 698 C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) (Table 1, Fig. 9). At 30°C, development from eggs to pupae averages 64.8 days, increasing to 179.9 days at 18°C. Duration of immature life stages was used to generate a development rate curve (Fig. 9) and to calculate a theoretical development threshold temperature of 13.3°C. Lifetime fecundity is about 172 eggs on Opuntia ficus-indica, compared to 138 on O. aurantiaca for the summer generation. Respective values for the winter generation were 177 and 159. Total fecundity of winter generations ranges from 88–97 in South Africa, and 99–125 in Australia, although some estimates for total fecundity are as high as 200–300 eggs per female. Total lifetime fecundity changes with temperature, and ranges from about 12 at 34°C to about 100 at 26°C. The combined effects of insect age and temperature are shown using an Enkegaard oviposition rate surface using the equation: eggs = (−11.241 + 0.854T) d exp (−0.020Td); where T is temperature (°C) and d is time (days) (Fig. 10). The estimated parameters p and q describe how quickly maximal oviposition is reached as a function of temperature; and w how quickly it returns to zero. Net reproductive rate (R0), gross reproductive rate (GRR), generation time (T), intrinsic rate of increase (r), finite rate of increase (λ), and doubling time (DT) were 43.68 females/female, 44.02 females/ female, 67.14 days, 0.0562 females/female/day, 1.058 females/female/day, and 12.33 days, respectively, at 30°C. The life history parameters of Cactoblastis (Table 2) indicate an insect with relatively low reproductive potential and susceptibility to control measures at the egg stage that is exposed for periods of 20–48 days, depending on temperature. Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Table 1 Immature development of Cactoblastis cactorum (mean ± SE; days) Life stage Temperature (°C) 18 22 26 30 34 Eggs 47.90 ± 0.28 29.60 ± 0.22 22.50 ± 0.22 20.90 ± 0.23 22.90 ± 0.35 Larvae 78.39 ± 2.58 61.36 ± 2.77 33.52 ± 0.61 29.89 ± 0.80 30.08 ± 1.05 53.46 ± 1.52 24.91 ± 0.14 16.28 ± 0.51 13.88 ± 0.66 13.79 ± 0.67 179.86 ± 2.92 115.96 ± 2.84 72.22 ± 0.79 64.75 ± 0.88 67.04 ± 1.65 Pupae Complete Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Figure 9 Development rate for Cactoblastis cactorum immatures (eggs to pupae). Development rate was fitted to the logistic equation rate = 0.0165/(1 + (T/20.7093)−5.8823). The linear portion of the curve was used to estimate a lower development threshold temperature of 13.3°C. Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) Distribution After importation into Australia from Argentina in 1926, Cactoblastis moths dispersed throughout Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Figure 10 Enkegaard surface showing simultaneous effects of time and temperature on mean oviposition rate (female eggs). The estimated equation is: eggs = (−11.241 + 0.854T) d exp (−0.020Td) (F = 16.96; df = 3, 54: P < 0.001; R2 = 0.35). infested areas, exceeding all expectations of the Australian government and resulting in collapse of cactus stands at the original release sites by 1932. In 1956, Cactoblastis was shipped from South Africa to the Caribbean island of Nevis where it established and provided successful biological control against a complex of native prickly pear cacti. Successful introductions followed in Montserrat and Antigua in 1960. Through natural migration, intentional or unintentional human action, Cactoblastis has been reported throughout the Caribbean (or West Indies; including St. Kitts, the US Virgin Islands, Hispaniola [Haiti], Cuba, the Dominica Republic, the Bahamas, the Cayman Islands, Puerto Rico, Barbados), New Caledonia, Hawaii, Mauritius, St. Helena, and Ascension Island with varying degrees of establishment and success against Opuntia. The moth was imported into Pakistan and Kenya but apparently failed to establish. In 1989, the arrival of Cactoblastis in mainland North America was documented by reports in south Florida. Cactoblastis likely entered Florida Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Table 2 Life history parameters for Cactoblastis cactorum at different temperatures Parameter 22 Net Reproductive Rate (R0)a 8.550 Gross Reproductive Rate (GRR)b Generation Time (T)c 26 30 34 46.24 49.20 43.68 5.95 9.021 48.22 49.38 44.02 6.16 185.54 129.58 75.07 67.14 68.95 Intrinsic Rate of Increase (r)d 0.0116 0.0296 0.0519 0.0562 0.0258 Finite Rate of Increase (λ)e 1.0116 1.03 1.053 1.058 1.026 Doubling Time (DT)f a Temperature (°C) 18 59.90 23.41 13.32 12.33 R0 = ∑ lxmx expressed in units of female/female; egg numbers divided by 2 because of 1:1 sex ratio GRR = ∑ mx in female/female c T = (∑ xlxmx)/R0 in days d r = ln R0/T in female/female/day e λ = exp(r) in female/female/day f DT = ln (2)/r in days b C 26.86 699 700 C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) through commercial importations of Opuntia from the Dominican Republic into Miami. By 1999, Cactoblastis had spread northwards and was found throughout the eastern Florida coastline and as far north as Tampa on the western coast. By 2002, the moth had expanded westward to Pensacola, Florida and northward along the eastern coast to Charleston, South Carolina. In July, 2004, westward migration had reached Dauphin Island, Alabama and Bull Island, South Carolina (about 80 km north of Charleston). The westward migration of Cactoblastis in the southeastern United States is estimated at 160 km/year with arrival at the Texas border predicted to occur in 2007. The muchdreaded arrival of Cactoblastis in Mexico occurred in August 2006 on Isla Mujeres, a small island off the northeast coast of the Yucatan peninsula in Mexico. The method by which Cactoblastis migrated into Mexico is unknown, although speculation centers on winds and hurricanes, or accidental transport via tourists or commercial trade. The analysis of insect distributions may be assisted through the use of bioclimatic models such as CLIMEX. Bioclimatic models incorporate known ecological and climatic tolerances of organisms in their native habitats to predict potential distribution or densities in other geographical regions. The twofold process typically consists of replicating the known distribution of the target species in its native habitat by estimating biological and stress parameters using experimental data or estimates from the literature. Afterwards, the geographical area of interest is extended or a new area is chosen where the target species may be introduced intentionally, as in a biological control agent, or unintentionally, as in an invasive pest species. Temperature index parameters were estimated using the laboratory data on development time at different constant temperatures (Table 3). The moisture index parameters were based on those of the Mediterranean fruitfly, Ceratitis capitata (Diptera: Tephritidae), with a native South American distribution similar to that of Cactoblastis. The target area of distribution was the documented native habitat of Paraguay, Uruguay, southern Brazil and northern Argentina. Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Table 3 CLIMEX parameter file for Cactoblastis Parameter Description Value Temperature Index DV0 Lower temperature threshold= 9 DV1 Lower optimum temperature 25 DV2 Upper optimum temperature 30 DV3 Upper temperature threshold 36 Moisture Index SM0 Lower soil moisture threshold 0.1 SM1 Lower optimal soil moisture 0.2 SM2 Upper optimal soil moisture 0.8 SM3 Upper soil moisture threshold 1.0 Cold Stress TTCS Cold stress temperature threshold 9.0 THCS Cold stress temperature rate 0 DTCS Cold stress degree-day threshold 0 DHCS Cold stress degree-day rate −0.0001 TTCSA Cold stress temperature threshold (average) 9.0 THCSA Cold stress temperature rate (average) −1.0 Heat Stress SMDS Dry stress threshold 0.01 HDS Dry stress rate −0.1 Wet stress SMWS Wet stress threshold 1.2 HWS Wet stress rate 0.0015 PDD Degree days per generation 1500 Predicted and known worldwide distributions of Cactoblastis are shown together in the map. In its native distribution range of Uruguay, Paraguay, south Brazil and north Argentina, Cactoblastis appears to be limited by cold stress to the south and along the Andes mountain range, and Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) by wet stress to the north in parts of Brazil. Areas in eastern Brazil may be conducive to moth survival despite the absence of records in that area. The fact that no records of Cactoblastis exist in this area may be due to the absence of host Opuntia species, or the lack of efforts to find the moth. The model suggests potential distribution may occur in North America (from the Caribbean Islands to Florida, Texas and Mexico), Africa (South Africa, and parts of the eastern coast), southern India, parts of Southeast Asia and in the northeastern coast of Australia. As partial validation of these predictions, the moth was recorded in the Caribbean, including Cuba, Bahamas and Puerto Rico. Furthermore, the moth has been recorded in southern Africa and Australia. Cactoblastis was released, but apparently did not establish, in Kenya and Pakistan. Based on the model output, establishment might have been expected in Kenya, but not in Pakistan. New Caledonia, Hawaii and the islands of St. Helena and Ascension did not appear on the maps generated. Based on the current parameter values, the moth is close to its predicted northern range along the Atlantic coast. However, new data and revised parameter values could allow further expansion northwards. Therefore, the current projections are likely to be conservative estimates of Cactoblastis range in North America. Because the potential range is likely to be conservative, more problematic is that the predicted range already encompasses Florida, Texas, eastern Mexico, as well as a bridge of favorable climate linking Florida to Texas along the Gulf Coast. Therefore, even without human intervention such as contaminated shipments of cacti, climatic conditions may support natural migration of the moth from Florida into Texas, provided adequate Opuntia populations exist along the Gulf Coast. Other bioclimatic models yield results similar to those from CLIMEX. GARP (Genetic Algorithm for Rule set Prediction) was used to estimate distribution of host cacti. Flora Map predicted potential distribution of Cactoblastis. When the distribution maps of both host plant and cactus moth were overlaid, possible invasion routes into Mexico C were predicted to be along the northern border through Texas, or less likely, through southeastern Mexico. The validity and utility of bioclimatic models is controversial. Clearly, distribution of organisms is determined by factors other than climate. The problems encountered in collecting data to both calibrate and validate the CLIMEX model are likely to be typical for most scientists attempting similar studies. Detailed distribution records are difficult to obtain, despite the fact that Cactoblastis is a well-documented insect. There is a need to determine definitively whether the absence of records from large regions such as eastern Brazil is because sampling was performed, but no moths were collected, or simply because no sampling efforts were undertaken. Absence data is almost as important as presence data. In addition to problems with distribution record data, weather data may not be available for specific times and locations of interest. In an insect as cosmopolitan as Cactoblastis, a potentially significant complication is that strains of different geographical origins have differing bionomics, perhaps as adaptations to local climate. Despite numerous valid criticisms against the climate matching approach, in the absence of appropriate data, climate matching may be the only viable option to predict species distributions. Control Currently there are no consistently effective chemical or biological methods to control Cactoblastis. To limit Cactoblastis infestations, adequate surveillance and early detection are critical. Effective surveillance may require the use of specialized traps such as those baited with virgin female moths. In areas where Cactoblastis has established as a pest, the selection of a control agent is determined by considering the value of the crop, the size of the affected area, and if the moth is itself used as a control agent against invasive cactus species. Control methods may include management 701 702 C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) practices such as the collection and destruction of infested cacti. Systemic insecticides have not proven effective against Cactobastis, but selected contact insecticides may be used against early instars, before they penetrate the cactus. There are many potential biological control agents against Cactoblastis, but none appear to be specific. As discussed in the Biology section, the moth is characterized by a relatively low reproductive potential, which suggests that potential biological control agents need not possess extremely high reproductive rates. Candidate agents for evaluation might include egg parasitoids or predators that attack the vulnerable and exposed egg stage. Egg parasitoids belonging to the genus Trichogramma have been suggested as agents, possibly in augmentative biological control programs. In Australia, Trichogramma minutum Riley caused up to 32% egg parasitism. This egg parasitoid is commercially available. In South Africa and Australia, egg predation by ants is a significant regulatory factor in the Cactoblastis populations. Important ant predators include Crematogaster liengmei Forel, Pheidole sp., Tetramorium erectum Emery, T. bacchus Forel, Tetramorium sp., Monomorium albopilosum Emery, M. minutum Mayr, and Camponotus niveosetosus Mayr. Egg mortality due primarily to ant predation has been found to range from 55 to 78% depending on season and cactus species. Other ant species suspected of being egg predators on Cactoblastis are Technomyrmex albipes Smith, Monomorium delagoense Forel, Camponotus eugeniae Forel, and C. rufoglaucus (Jerdon). Alternatively, potential agents might be those specialized for searching and attacking the moth larvae within the cactus plant. Possible classical biological control agents from South America include one braconid larval parasitoid, five to six ichneumonid wasps, and a tachnid fly. Apanteles alexanderi Brethes (Hymenoptera: Braconidae) can cause parasitism levels over 30%. The ichneumonid Temelucha sp. caused 5–30% larval parasitism. The tachinid fly Epicoronimyia mundelli (Blanchard) also attacks other species of cactus moths. The braconid wasp, Bracon hebetor Say, parasitized up to 25% of the larvae in South Africa; this wasp can be mass reared on alternate hosts. Larval predators of Cactoblastis include ants (Pheidole sp. and Anoplolepis steingroeveri (Forel)) and a tachinid (Pseudoperichaeta sp.). Pupal predation by the ant species Dorylus helvolus (L.) has been measured at about 13–34%. Pupal parasitism by chalcid parasites Invreia sp. and Euchalcidia sp. was estimated at about 5%. In Florida, the chalcid parasite Brachymeria ovata Say, attacked 55% of Cactoblastis pupae at one site. Limited work has been done on evaluating insect pathogens as a control agent against Cactoblastis. Beauveria sp. caused high larval death rates in Australia and the species B. bassiana may have potential in inundative control programs. The protozoan Nosema cactoblastis has been reported from South Africa, but recorded infection levels are only 0–6%. The pathogen Bacillus thuringiensis Berliner has demonstrated efficacy against Lepidopteran pests but is not likely to be effective against Cactoblastis inside the cactus plant. The Sterile Insect Technique (SIT) method is being developed to study Cactoblastis populations, and possibly for eradication in colonization sites or for controlling dispersal and movement into new areas. SIT may have the most potential in the northern Gulf coast region where cacti are rare and Cactoblastis populations are low, although control will be expensive. Control measures against Cactoblastis infestations in the United States will probably be limited in most regions because Opuntia species are usually a low value crop. Life history data indicate that the moth does not display particularly high reproduction, so its pest status is due largely to the protection afforded by the cactus plant once the larvae have gained entry into the cactus tissue. The most vulnerable life stage appears to be the egg stage, both because it is exposed, and also because of its relatively long duration. Natural predation by ants may be encouraged. However, even after moth larvae have entered the plant, specialized natural enemies may be effective in seeking and attacking larvae inside the cactus plant. Effective Caddisflies (Trichoptera) integrated pest management of Cactoblastis will require an understanding of all the management options available to develop comprehensive, yet cost-effective strategies under different geographical and socio-economic situations, while limiting detrimental effects against non-target organisms.  Sterile Insect Technique  Area-Wide Insect Pest Management  Biological Control of Weeds  Foreign Exploration for Insects that Feed on Weeds References Legaspi JC, Legaspi BC Jr (2007) Life table analysis for Cactoblastis cactorum immatures and female adults under five constant temperatures: implications for pest management. Ann Entomol Soc Am 100:497–505 Mahr DL (2001) Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America: a workshop of assessment and planning. Fla Entomol 84:465–473 (and papers contained in this volume) Sutherst RW, Maywald GF, Bottomley W, Bourne A (2004) CLIMEX v2: user’s guide. CSIRO, Queensland Australia Zimmermann HG, Moran VC, Hoffmann JH (2000) The renowned cactus moth, Cactoblastis cactorum: its natural history and threat to native Opuntia floras in Mexico and the United States of America. Divers Distrib 6:259–269 Zimmermann HG, Bloem S, Klein H (2004) Biology, history, threat, surveillance and control of the cactus moth, Cactoblastis cactorum. International Atomic Energy Agency, Vienna, Austria, 46 pp Caddisflies (Trichoptera) Lewis s. LonG University of Florida, Gainesville, FL, USA The Trichoptera, or caddisflies, is an advanced order of aquatic insects that, as adults, are easily distinguished by the presence of two pairs of wings covered with hair and held in a roof like manner over the abdomen. They typically exhibit a rather dull appearance (some being distinctly patterned) with long, slender antennae. They possess chewing type mouthparts with reduced mandibles, but feed C mainly on liquid diets as adults and are detritivorous or predaceous as larvae. Adults are nocturnal and typically found alongside lakes and streams, but may also be encountered away from bodies of water. Larvae are found in a variety of aquatic habitats, mainly cool swift-flowing streams. Caddisflies are an important component in aquatic food chains and also are used as bioindicators of pollution. Caddisfly larvae can be distinguished from other aquatic insects by the presence of modified anal prolegs and a portable case or silken retreat that protects their delicate body. Larval cases are constructed from a variety of materials, ranging from stick and leaf fragments to small stones and grains of sand, and are held together by silk produced by labial silk glands. Larval caddisflies (Fig. 11) have a closed respiratory system marked by the absence of spiracles and the presence of abdominal gills in some members. Respiration of larvae occurs through the cuticle and gills (if present). Abdominal undulation and morphological adaptations, mainly humps on the anterior segments of the abdomen and lateral fringes of hair, allow for circulation of water through the case. Larvae go through five to seven instars before pupation. They cease feeding and become inactive for up to several weeks inside the silken pupal cases. Pharate adults use their sharp mandibles to cut away the case, and then float to the surface and emerge from the pupal integument. Adults live for approximately a month (up to three in some families). After mating, females enter the water to deposit eggs on the underside of rocks. Hairs on the body act as a water-proof layer, essentially allowing the adult to breathe underwater by preventing the spiracles from coming into contact with the surrounding water. The eggs of some species are surrounded by a gelatinous mass that swells to form a protective covering. Caddisflies are a product of their environment. One reason they are so diverse is their ability to occupy so many diverse habitats, from cool flowing streams to warm still waters. Morphology and behavior of the larvae allow a variety of means to collect food, in addition to several families 703 704 C Caddisflies (Trichoptera) Caddisflies (Trichoptera), Figure 11 Diagram of adult male and larval caddisflies. occupying different feeding guilds. For example, aperture size of the net-spinning caddisfly retreat is directly correlated to the size of their food item: a larger aperture for larger prey, and a smaller aperture for particulate material. Morphological modifications found in some families allow for a diet of diatoms by scraping the surface of rocks, while others are more suited for a filtering collecting lifestyle using forelegs or delicate nets and retreats. Nets, cases and tubes constructed by the larvae also allow for protection and concealment while feeding or during pupation. Cases match the habitat in which the larvae are found, from sand and pebble cases in sandy streams, to plant material found in many springs, lakes and ponds. Caddisflies are considered the sister group to butterflies and moths(Order Lepidoptera) and are unique in the fact that they are the only holometabolous group of insects that are considered aquatic. Some Trichoptera also share similar pheromone detection systems like these found in some primitive Lepidoptera. Currently, there are an estimated 1,400 species of caddisflies recognized from North America within 27 families, and approximately 7,000 species in 60 extant families worldwide. Weaver and Morse (1986) reviewed different phylogenies and examined feeding and case-making behavior to hypothesize that an ancestral tube-dwelling caddisfly gave rise to other forms. Keys to caddisfly larvae, pupae and adults of North American species can be found in the publications cited in the “References” section. A worldwide database and current higher classification is available at the website, http://entweb.clemson.edu/database/trichopt/ hierarch.htm. An overview of classification is: Order Trichopteralt Suborder Annulipalpia Superfamily: Hydropsychoidea Family: Dipseudopsidae Family: Arctopsychidae Family: Ecnomidae Family: Hydropsychidae Family: Polycentropodidae Family: Psychomyiidae Family: Xiphocentronidae Superfamily: Hydroptiloidea Family: Glossosomatidae Family: Hydroptilidae Superfamily: Philopotamoidea Family: Philopotamidae Superfamily: Rhyacophiloidea Family: Hydrobiosidae Family: Rhyacophilidae Suborder: Integripalpialt Superfamily: Limnephiloidea Caddisflies (Trichoptera) Family: Apataniidae Family: Brachycentridae Family: Goeridae Family: Lepidostomatidae Family: Limnephilidae Family: Rossianidae Family: Uenoidae Superfamily: Phayganeoidea Family: Phryganeidae Superfamily: Leptoceroidea Family: Calamoceratidae Family: Leptoceridae Family: Molannidae Family: Odontoceridae Superfamily: Sericostomatoidea Family: Beraeidae Family: Helicopsychidae Family: Sericostomatidae A brief synopsis of the more common families follows. Family: Brachycentridae (Humpless Caddisflies) The larval cases of this family range from pieces of plant material to small pebbles and grains of sand. Some members of this family are filter feeders, collecting food particles from the current with the use of their hairy forelegs, switching to a predaceous diet in later instars. The genera Brachycentrus and Micrasema are the two more common genera that are found throughout North America. Family: Glossosomatidae (Saddlecase Caddisflies) Larvae of this family form saddle-like cases that are similar to turtle shells. The upper portion of the case is comprised of large stones while the lower portion is generally made up of sand. They are usually found on the upper surface of stones in swift, cool streams. Two common genera are Glossoma and Agapetus. C Family: Helicopsychidae (Snail-case Cadisflies) This family is unique within the order with larvae constructing coiled cases similar in appearance to snail shells. They are found primarily in swift flowing waters with sandy substrates and the wave swept shores of lakes and also in springs. Helicopsyche is the only genus within the family. Family: Hydropsychidae (Net-spinning Caddisflies) These caddisflies are known for their cup-shaped nets that allow for both a secure place to reside and a means of collecting food. The net acts as a strainer and is permanently held in place with pupation occurring inside of the structure. Hydropsyche, Cheumatopsyche and Ceratopsyche are the more diverse and widely distributed genera within this family. Family: Hydroptilidae (Microcaddisflies) Microcaddisflies are unique in that the first four instars are free-living with later instars increasing in size and making a purse or flask-shaped case open at each end. Larval case material is varied, ranging from pure silk to plant material and grains of sand. Hydroptila, Ochrotrichia and Oxythira are the most diverse and widespread genera within the family. Family: Lepidostomatidae (Lepidostomatid Caddisflies) Generally found in cool headwater streams, these caddisflies are also known from springs. Larvae construct four sided cases or slender tubes of concentric rings, each made up of sticks, twigs and 705 706 C Caddisflies (Trichoptera) sand. Lepidostoma is a common genus, accounting for most of the diversity within the family. Family: Leptoceridae (Long-horned Caddisflies) Named for their long antennae in both the larval and adult stages, long-horned caddisflies are primarily detritivorous or predaceous with some members known to feed on freshwater sponges. Larval cases vary, with some resembling short, stout “log cabins” of twigs to slender tubes made of silk and plant material. Oecetis, Ceraclea and Triaenodes are three widespread genera found within this family. Family: Limnephilidae (Northern Caddisflies) This is the largest family of caddisflies in North America with more that 300 species, with the widespread genus Limnephilus accounting for almost a third of the diversity. Larvae are found in both lentic and lotic habitats and cases differ between young and older larvae. Family: Molanidae (Hood-case Caddisflies) much smaller lower opening, which results in the collection of food particles within the net. Pupation occurs in a silk lined pebble case. Three widespread genera, Chimarra, Doliphiloides and Wormalida, are found within this family. Family: Phyrganeidae (Large Caddisflies) As the name implies, these are larger than most caddisflies, found primarily in cold, lentic habitats and sometimes along the slow margins of streams. Larval cases consist of portions of grass stems arranged spirally. Representative genera within the family are Agrypina and Ptilostomis. Family: Polycentropodidae (Trumpet-net Caddisflies) These caddisflies are found in a variety of lentic and lotic habitats and within a variety of retreats and cases. Some members construct delicate trumpet-shaped retreats while others have rigid tubes strengthened with sand. Primarily collectors, members of this family are also known to be predaceous. Common genera include Neureclipsis and Polycentropus. This widespread family is only represented by a few species known mainly in eastern North America in lentic habitats. The case is distinctive in that it consists of a tapered tube of sand with a flattened hood, allowing the larvae to feed in the open under concealment. Molanna is the more common genus of this family. Family: Rhyacophilidae (Primitive Caddisflies) Family: Philopotamidae (Finger-net Caddisflies) References The larvae of this family are found primarily on rocks in swiftly flowing, cold streams. The finger shaped tubes have a large upper opening and a This family is caseless, or free-living, until pupation and is typically predaceous. The genus Rhyacophilia is a diverse group containing over 100 species and is typically found in swift mountain streams. McCafferty WP (1981) Aquatic entomology. Science book international, Boston, MA, 448 pp Merritt RW, Cummins KW (eds) (1996) An introduction to the aquatic insects of North America, 3rd edn. Kendall/ Hunt, Dubuque, IA Callow Weaver JS III, Morse JC (1986) Evolution of feeding and casemaking behavior in Trichoptera. J North Am Benthol Soc 5:150–158 Wiggins GB (1996) Larvae of North American caddisfly general Trichoptera, 2nd edn. University of Toronto Press, Toronto, Ontario, Canada Cadelle, Tenebroides mauritanicus (Linnaeus) (Coleoptera: Tenebrionidae) This is a grain and flower-infesting species.  Stored Grain and Flour Insects Caeciliidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Caecum (pl., caeca) A sac-like or tube-like structure, opened at one end only.  Gastric Caecum C application technology, calibration refers to adjustment of nozzles on a spray apparatus, or determination of the amount of pesticide that is produced by a sprayer when it is operated. California Red Scale, Aonidiella auranti (Maskell) (Hemiptera: Diaspidae) This is a major pest of citrus in California, USA.  Citrus Pests and their Management Calipharixenidae A family of insects in the order Strepsiptera.  Stylopids Callidulidae A family of moths (order Lepidoptera) also known as Old World butterfly moths.  Old World Butterfly Moths  Butterflies and Moths Caenidae A family of mayflies (order Ephemeroptera).  Mayflies Calamoceratidae A family of caddisflies (order Trichoptera).  Caddisflies Calcaria Moveable spurs at the tip of the tibia. Calibrate A process designed to standardize or correct the measuring devices on instruments. In pesticide Calliphoridae A family of flies (order Diptera). They commonly are known as blow flies, bluebottle flies, and greenbottle flies.  Flies Callirhipidae A family of beetles (order Coleoptera). They commonly are known as cedar beetles.  Beetles Callow Newly molted individuals whose exoskeleton is still relatively soft and lightly pigmented. 707 708 C Calophllidae Calophllidae A family of bugs (order Hemiptera, superfamily Psylloidea).  Bugs Rican natural history” followed his sabbatical leave in Costa Rica in 1909–1910. He was president of the American Entomological Society from 1901 to 1915, editor of Entomological News from 1911 to 1944, and one of the founders of the Entomological Society of America. He died on August 23, 1961. Calopsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Calopterygidae A family of damselflies (order Odonata). They commonly are known as broad-winged damselflies.  Dragonflies and Damselflies Calvert, Philip Powell Philip Calvert was born in Philadelphia on January 29, 1871, and grew up there, leaving school in 1888 and graduating from the University of Pennsylvania in 1892 with a certificate in biology, and in 1895 with a Ph.D. He then spent a year in Germany, at the universities of Berlin and Jena. In 1907 he began to teach zoology at the University of Pennsylvania, retiring in 1959 with the rank of Emeritus Professor. Teaching played a major role in his life. His research contribution was on Odonata, on which group he published over 300 papers, beginning in 1899. He wrote especially on taxonomy, but also on anatomy, distribution, paleontology, and ecology. Some of his major publications were (1893) “Catalogue of the Odonata (dragonflies) of the vicinity of Philadelphia with an introduction to the study of this group of insects,” (1901–1906) “Insecta Neuroptera Odonata” in Biologia Centrali-Americana, (1909) “Contribution to a knowledge of the Odonata of the Neotropical Region, exclusive of Mexico and Central America,” and (1944) “The rates of growth, larval development, and seasonal distribution of the genus Anax”. A book, “A year of Costa References *Mallis A (1971)Philip Powell Calvert. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 178–180 Rehn JAG (1962) Philip Powell Calvert (1871–1961). Entomol News 63:113–121 Schmieder RG (1962) Additions to the bibliography of Philip P Calvert, subsequent to 1950. Entomol News 63:121 Schmieder RG, Phillips ME (1951) Bibliography of Philip P Calvert. Entomol News 62:3–40 Calypter (pl., calypteres) A small fold or lobe in the hind margin of fly wings (Diptera) covering the haltere. Calyptodomous Pertaining to nests, particularly wasp nests, in which the combs are surrounded by an envelope. Camel Crickets A family of crickets (Rhaphidophoridae) in the order Orthoptera.  Grasshoppers, Katydids and Crickets Cameron, Malcolm Malcolm Cameron was born in London in 1873, and died there on October 24, 1954. He obtained Candeèze, Ernest Charles Auguste an M.D. degree at The London Hospital and entered the British navy as naval surgeon. He served in the British navy during the Boer War and in the first World War (campaigns in the Falklands and East Africa). He retired in 1920 and devoted the rest of his life to entomology, although he had about 40 publications before retirement. He went to India, where he collected Staphylinidae extensively, but returned in 1925 to London due to a lung illness. His five-volume contribution on Staphylinidae of British India was his major work, but 206 other papers on Staphylinidae worldwide together enabled him to describe 4,136 species and 195 genera in Staphylinidae, making him the most profuse describer of species of this family after Max Bernhauer. Like Bernhauer, he did not provide illustrations or keys for most of his works (the Fauna of British India was an exception), so identification of specimens of the species he described is not easy. His collection of some 55,000 specimens was bequeathed to the British Museum (Natural History), later called The Natural History Museum. References Herman LH (2001) Cameron, Malcolm. Bull Am Mus Nat Hist 265:51–52 Puthz V (1986) Bibliographie de Publikationen Malcolm Cameron’ s (1873–1954). Philippia 5:301–310 Cambrian Period A geological period of the Paleozoic era, extending from about 580 to 500 million years ago. Chelicerate arthropods date from this time.  Geological Time Camillid Flies Members of the family Camillidae (order Diptera).  Flies C Camillidae A family of flies (order Diptera). They commonly are known as camillid flies.  Flies Campestral Inhabiting open fields. Campodeidae A family of diplurans (order Diplura).  Diplurans Campodeiform Larva A term used to describe larvae that are elongate and flattened, with well-developed thoracic legs and antennae, and a prognathous head. Such larvae are usually active and predacious. It is named for Campodea, a dipluran. This body form is found in the orders Ephmeroptera, Odonata, Plecoptera, and Neuroptera. Canacidae A family of flies (order Diptera). They commonly are known as beach flies.  Flies Candeèze, Ernest Charles Auguste Ernest Candèze was born in Liège, Belgium, on February 27, 1827. He studied medicine in Paris and Liège, and became a physician and director in a hospital for the insane. In Liège he was a pupil of Lacordaire. His taxonomic interest was the study of Elateridae (Coleoptera), in which family he became a world authority, and 709 710 C Canine Babesiosis his most notable achievement (1857–1860) was a four-volume monograph on Elateridae supplemented by papers in Annales de la Société Entomologique de Belgique. Additionally, he published on insect pests of horticulture, was a member of the Academie de Belgique and of the Société Royale des Sciences de Liège, president of the Société Entomologique de Belgique in 1873 and 1874, one of the five commissioners of the Muséum d’ Histoire Naturelle of Brussels, and a member of several foreign entomological societies. One of his collections of Elateridae is in the Natural History Museum (London) and another in Brussels. His wife died in 1872; they had five children, of whom Léon Candèze became an entomologist. He died near Liège on June 30, 1898. References *EssigEO (1931) Candèze, Ernst Charles Auguste. In: A history of entomology. MacMillan, New York, pp 563–564 Lameere A (1898) Notice sur le Dr. Ernest Candèze. Ann Soc Entomol Belg 42:504–519 Canine Babesiosis This is a tick-transmitted protozoan disease. It is also known as canine piroplasmosis.  Piroplasmosis Canine Piroplasmosis This is a tick-transmitted protozoan disease. It is also known as canine babesiosis.  Piroplasmosis Cannibalism John L. Capinera University of Florida, Gainesville, FL, USA Cannibalism is intraspecific predation. It occurs widely among arthropods. It is best known in predatory species, though it also occurs among detritivores and herbivores. Cannibalism is often viewed as a population self-regulatory measure, acting to limit population size and suppress population outbreaks. Shortage of food, high density, or both of these factors contribute to cannibalism. Elimination of competition is considered by some to be the basis for such cannibalism. However, possibly of equal benefit is the fitness advantage resulting from improved nutrition by cannibalistic individuals. Cannibals can benefit from larger food supplies following the elimination of competition, but also from the higher nutritional quality of feeding on arthropod body tissues rather than plant tissues. Probably less important are the benefits derived from reduced predation and parasitism following cannibalism; lower host densities often result in less frequent attack by predators and parasitoids. Cannibalism may select for shorter egg development times, as eggs are a particularly vulnerable stage. Cannibalism likely has contributed to development of parental care. In eusocial insects, cannibalism can be used to adjust caste ratios or sex allocation ratios. Cannibalism is a normal phenomenon for many arthropods, not an anomaly. Cannibalism has been documented in many insect orders, including Odonata, Orthoptera, Thysanoptera, Hemiptera, Trichoptera, Lepidoptera, Diptera, Neuroptera, Coleoptera, and Hymenoptera. It occurs among predatory species and herbivores, and involves predation by the mobile adults and larvae or nymphs on each other, and on immobile eggs and pupae. Arthropods occurring at high densities, faced with inadequate food availability, or spatially constrained (e.g., limited to feeding within a fruit or stem) more commonly display cannibalism. Also, generalist species are more prone to display cannibalism than are specialist species, and females are more cannibalistic than males. The greater occurrence of cannibalism among females may simply be a manifestation of the greater size of females, allowing them to overpower prey more easily. Cannibalism is common among freshwater insects. Perhaps surprisingly, cannibalism is quite common among some groups of herbivorous insects. Cannibalism Some adaptations to deter cannibalism are evident. Deposition of eggs on long thin stalks by lacewings (Neuroptera: Chrysopidae) is often given as an example of evolution of a cannibalismdeterring behavior. Synchronous hatching of eggs is much more widespread, and similarly deters the early-hatching individuals from taking advantage of their late-hatching siblings. Dispersion of individuals, particularly of eggs, is another good way to reduce cannibalism. Population Regulation Cannibalism can reduce population size before resource (food) shortages occur, thereby averting physiological stress. This is not unlike other population regulation behaviors such as spacing, dispersion, and the benefits resulting from marking pheromones (which serve to deter insects from ovipositing repeatedly into a limited food resource). For many species, cannibalism is correlated with frequency of encounter, and higher levels of cannibalism occur if there is an abundance of susceptible prey. For example, ladybird beetle (Coleoptera: Coccinellidae) larvae often feed on nearby unhatched eggs, but if hatching is simultaneous there is no cannibalism. Cannibalism occurs among herbivorous insects even when normal food is plentiful, as in the ladybird beetle example mentioned above. Hatching Danaus spp. (Lepidoptera: Nymphalidae) caterpillars feed readily on their siblings (eggs), even while feeding on foliage. The importance of cannibalism in population regulation is generally poorly documented. Often such losses are simply attributed to disappearance, and it is unknown whether losses are due to intraspecific or interspecific predation, or dispersion. Cannibalism also is hard to measure because it may be restricted to a short period in time, and often is detectable only via direct observation. As noted above, ladybird beetle larvae often feed on eggs, but once hatch occurs, predation diminishes or disappears because eggs, not other larvae, are the preferred alternate food. It may be necessary to C actively seek out cannibalism data to document the relative importance of cannibalism. For example, studies of Gerris water striders (Hemiptera: Gerridae) have shown that the presence or absence of older water striders significantly influences survival of young Gerris. If broods overlap, the older bugs feed heavily on the younger, but if the older insects are artificially removed, survival of the young bugs is quite high. This effect of cannibalism is not easy to discern without the artificial manipulation of the older age class. After hatching, the predatory and cannibalistic Mormon cricket (Fig. 12), Anabrus simplex Haldeman (Orthoptera: Tettigoniidae), forms groups (called “bands”) that move each day, stopping only briefly to feed and to rest at night. The benefit of almost continuous movement is thought to be a mechanism to protect the defenseless molting individuals from being consumed by their siblings, as the molting crickets are left behind while the non-molting and aggressively cannibalistic individuals continue to seek food. If these highdensity aggregations were not moving the molting individuals would be easy prey and most would be killed. This may represent an unusual example of the significance of cannibalism, and the evolution of a novel defense against it. Cannibalism can also be important in maintaining populations during periods of food scarcity. From the perspective of population persistence, it is better to have a few well-fed cannibalistic individuals surviving than to have all individuals die from temporary lack of food. Physiological quality can be as important as abundance. Population stability and persistence is enhanced during periods of food deprivation if the few survivors are well fed and capable of reproduction; the alternative may be more but malnourished individuals incapable of reproducing. Nutrition Conflicting data exist on the nutritional benefits of being a cannibal. For example, a study of 711 712 C Cannibalism Cannibalism, Figure 12 Cannibalism by Mormon cricket, Anabrus simplex Haldeman (Orthoptera: Tettigoniidae). (i) Cannibalism of a cricket; this species attacks congeners whenever the opportunity arises. Perhaps because of this, it forms groups (called “bands”) that move each day, stopping only briefly to feed and to rest at night. The benefit of almost continuous movement is thought to be a mechanism to protect the defenseless molting individuals from being consumed by their siblings, as the inactive molting crickets are left behind while the non-molting and aggressively cannibalistic individuals continue to seek food. (ii) When cricket bands cross highways some are killed by the tires of passing vehicles. The other crickets are quick to take advantage of this food source and stop to feast on their killed or injured comrades. They, in turn will be killed by additional vehicular traffic. After several vehicles have passed by, the roadways are marked by slippery, greasy bands marking the paths of vehicle tires. predatory ladybird beetles showed that although individuals cannibalizing eggs did not benefit in terms of survival rates, they displayed more rapid development and (in the case of females) a higher final body weight. Both rapid development and higher body weight are considered favorable to population growth. Another study involving Harmonia axyridis ladybird beetles found that cannibalism allowed beetle larvae to supplement an otherwise inadequate diet of aphids and to survive Cannibalism to maturity. Cannibalistic willow leaf beetles, Plagiodera versicolora (Coleoptera: Chrysomelidae), gain a size advantage and are more successful at initiating feeding sites on tough vegetation as compared to non-cannibalistic individuals. Similarly, many aquatic detritivores supplement their diet with animal material obtained through cannibalism, and a study of caddisflies (Trichoptera) found that individuals with animal material in their diet had higher larval survival, shorter larval and pupal development times, earlier emergence dates, larger adult body mass (30–40%), and higher fecundity (30% more eggs). In contrast, a study of the herbivorous caterpillar Acsia monuste (Lepidoptera: Pieridae) found no benefit from cannibalism of eggs or larvae, and study of the caterpillar Spodoptera frugiperda (Lepidoptera: Noctuidae) found lower body rates and development times among cannibals. However, many studies do not separate the effects of density per se (higher density increases the rate of cannibalism but decreases fitness) from the effects of cannibalism (which sometimes benefits the cannibal). Herbivorous insects have greater difficulty in obtaining protein than many other insects, particularly predators and parasitoids, due to the relatively low levels of protein in their diet. Not surprisingly, many have evolved supplemental feeding behaviors that provide additional protein, including feeding on pollen, exuviae, and members of the same species (conspecifics). Early stages of development especially benefit from extra protein, and later in life it is not unusual for holometabolous insects to shift toward more carbohydrates in their diet. The level of cannibalism displayed by an herbivorous species can change according to dietary levels of protein. Addition of casein to a laboratory diet of pure cellulose greatly diminished cannibalistic behavior of the Pacific dampwood termite, Zootermopsis angusticollis (Isoptera: Hodotermitidae). The level of cannibalism by the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), was inversely related with the nitrogen level of the host plant. Thus, armyworm larvae C Cannibalism, Table 4 Levels of cannibalism and subsequent egg production by beet armyworm larvae fed on sugarbeet foliage grown in nutrient solution with nitrogen deficiency (0N), normal nitrogen (1N), or twice the normal level of nitrogen (2N) (adapted from Al-Zubaidi and Capinera (1983) Environ Entomol 12:1687–1689) Nutrient level (N) 0N 1N 2N 60 38 24 Foliage + pupae 467 512 615 Foliage only 382 481 512 Cannibalism (%) Mean no. eggs after fed: were able to compensate for poor quality diet by increasing cannibalism, with a subsequent boost (Table 4) in egg production. Trophic Eggs Trophic eggs ar e homologous to fertile eggs but they cannot develop into viable offspring and are normally eaten by siblings. Thus, in a sense, consumption of these eggs is an expression of cannibalism. They are most commonly found in eusocial (social) insects such as Isoptera (termites) and Hymenoptera (wasps, bees, ants) but sometimes in other, non-eusocial groups such as owlflies (Neuroptera), crickets (Orthoptera), ladybird beetles (Coleoptera), psocids (Psocoptera), and spiders (Aranea). Trophic eggs likely evolved due to the survival benefits of having viable or nonviable (sterile) eggs available for offspring to feed upon. Trophic eggs provide a uniform food for offspring, and in the case of colonial species, can be stored for use during unfavorable periods. Trophic eggs are most common among eusocial species due to the interdependency on the different castes and (usually) the ability of the queen to manipulate the members of the colony. 713 714 C Canopidae Sexual Cannibalism This is a special type of cannibalism wherein an insect (usually a female) consumes a conspecific, normally a male, in association with mating. Such cannibalism usually occurs after copulation, and is widespread among mantids (Mantodea) but uncommon in other taxa. In mantids, this has been documented to be a significant source of nutrition for the female. It is easy to understand the benefits of cannibalism to the female, and some have postulated that cannibalism pre-coitus is more likely with unsuitable males and post-coitus more likely with more suitable mates. What is less apparent, however, is why the male is successfully duped into becoming a food resource for his mate. With mantids, the larger size of females perhaps accounts for the female’s success; it is easy for her to overpower him. On the other hand, it can be argued that natural selection favors post-coitus sexual cannibalism because the male is making the “supreme” parental investment in his offspring. Perhaps this is consistent with other nuptial gifts such as the large proteinaceous sperm capsule (spermatophylax) provided to females by males of some katydids (Orthoptera: Tettigoniidae) such as the Mormon cricket, Anabrus simplex. If such sacrifice on the part of male mantids occurs willingly, it certainly represents an extreme form of paternal investment. Though not well understood, it appears that males are rather cautious with females, and strive to escape after mating. Costs of Cannibalism Cannibalism clearly is not always beneficial. Cannibals risk injury or death from the defensive responses of their prey. Typically, cannibals prey on smaller or younger conspecifics, minimizing their risk of injury. Cannibalism can also result in the transmission of microbial pathogens to the predatory individual. Infected individuals early in the disease cycle are sluggish, and are relatively easy prey, but they may harbor a lethal dose of pathogens if they are ingested. Thirdly, cannibalism often is particularly widespread among siblings because adults deposit clusters of eggs. This can result in reduction of inclusive fitness, because there is little opportunity to distinguish relatives from nonrelatives. Aggressive cannibals may also eliminate prospective mates if they consume all conspecifics. The genetic costs of destroying relatives and eliminating prospective mates are likely very important evolutionary factors in the selection against cannibalistic behavior. Finally, many insects benefit from living in groups. Although most apparent for social insects, even nonsocial insects enjoy benefits from group living such as easier exploitation of food resources or more effective deterrence of predation. Cannibalism works against the accrual of such group-derived benefits.  Facultative Predators  Nutrient Content of Insects  Praying Mantids (Mantodea)  Mormon Cricket, Anabrus simplex Haldeman  Katydids  Gregarious Behavior in insects References Bernays EA (1998) Evolution of feeding behavior in insect herbivores. Bioscience 48:35–44 Elgar MA, Crespi BJ (1992) Cannibalism. Ecology and evolution among diverse taxa. Oxford University Press, Oxford, UK, 361 pp Fox LR (1975) Cannibalism in natural populations. Ann Rev Ecol Syst 6:87–106 Joyner K, Gould F (1987) Conspecific tissues and secretions as sources of nutrition. In: Slansky F Jr, andRodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, NY, pp 697–719 Simpson SJ, Sword GA, Lorch PD, Couzin ID (2006) Cannibal crickets on a forced march for protein and salt. Proc Natl Acad Sci 103:4152–4156 Canopidae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs Cape Honey Bees, Apis mellifera capensis Escholtz Canopy C Cape Honey Bees, Apis mellifera capensis Escholtz The leafy part of plants or trees. Canthariasis Infestation of the organs of the body, including the alimentary canal, with beetle larvae. This is an unusual condition, and most often occurs by consuming flour or other grain products that are infested with grain beetles. Cantharidae A family of beetles (order Coleoptera). They commonly are known as soldier beetles.  Beetles Cantharidin A defensive chemical produced by blister beetles and found in their blood. It can cause blisters on the skin of humans if they crush the beetles. Blisters can also form in the mouth and digestive tract of animals that consume the beetles along with forage plants. Horses are more susceptible to injury and death than other livestock. In North America, alfalfa hay is the principal source of blister beetles, and it is contaminated when hay is crimped (crushed) to hasten drying, as beetles are also killed at this time and incorporated into the hay. Problems occur mostly during or following grasshopper outbreaks because Epicauta spp. blister beetle larvae develop on the eggs of grasshoppers, and the adults move to alfalfa blossoms to feed.  Blister Beetles  Multifunctional Semiochemicals Canthus A chitinous process that, in some insects, divides the eyes into an upper and lower half. Jamie eLLis University of Florida, Gainesville, FL, USA The Cape honey bee, Apis mellifera capensis Escholtz is a subspecies (or race) of western honey bee, A. mellifera Linnaeus, that occurs naturally in the Cape region of South Africa. Upon casual observation, Cape bees look very similar to another race of honey bee present in South Africa, Apis mellifera scutellata (the “African” honey bee of the Americas). Yet reproductively, Cape bees differ significantly from Apis mellifera scutellata and other honey bee races, making it perhaps the most distinctive race of A. mellifera worldwide. Identification Cape bees have been distinguished from scutellata and other African races of honey bees using morphometric techniques. Genetic analyses are used increasingly as complications with morphometric techniques arise. Most beekeepers in South Africa use other characteristics to identify Cape bees, namely (i) the ability of worker bees to produce female offspring, (ii) the highly developed ovaries in Cape laying-workers, and (iii) small, queenless swarms. Once these phenotypes can be detected, Cape bees usually are established already. Distribution The natural distribution of Cape bees mirrors that of the fynbos region in the southwestern section of South Africa. Part of the Cape Floral Kingdom (one of six floral kingdoms worldwide), the fynbos is a narrow strip of land stretching from the southwestern-most corner of South Africa, eastward to Port Elizabeth. Even though it is small, the fynbos region contains over 80% of the flower diversity 715 716 C Cape Honey Bees, Apis mellifera capensis Escholtz found in the Cape Floral Kingdom, and it has more plants species than any area in the world, including tropical rain forests. Because it is rich in plant biodiversity, the fynbos region is able to support a remarkable diversity of life, from insects to higher animals. Cape honey bees specialize in foraging on plant species found in the fynbos, and beekeepers in this area use Cape bees as their bee of choice. Like other western honey bee races, Cape bees can be managed readily for purposes of pollination and honey production. Because the fynbos region is limited climatically to the small belt stretching from southwestern South Africa eastward to Port Elizabeth, Cape bee distribution is limited to this area as well (Fig. 13). Here, one can find the “pure” race of Cape bee. However, Cape bees can hybridize with Apis mellifera scutellata, and they begin to do so just north of the fynbos belt. This zone of hybridization also encompasses a narrow stretch of land, running the entire length of area just north of the fynbos region. North of the zone of hybridization, one will find the “pure” race of Apis mellifera scutellata. Reproduction in Cape Bees Understanding reproduction in Cape bees is fundamental to understanding their biology and behavior. For the most part, reproduction in Cape bees follows that of other races of honey bees. Queens are the reproductive individuals in honey bee colonies. When queens emerge from the waxy cells in which they pupate, they spend the first 10–14 days of their lives maturing and mating. During this time, a queen bee will leave the colony in search of drones or male honey bees. Queens and drones mate in the air, following which the drones die. The queen will repeat this process over the course of a few days, mating with anywhere from 10–20 drones. Queens store all of the semen collected from the various drones in an organ called a spermatheca. Cape Honey Bees, Apis mellifera capensis Escholtz, Figure 13 The distribution of Cape honey bees in South Africa (shaded gray). The area shaded black represents where A.m. capensis and A.m. scutellata hybridize. The checkered area indicates the natural distribution of A.m. scutellata (modified from Hepburn and Radloff, 1998). Cape Honey Bees, Apis mellifera capensis Escholtz When a queen bee lays an egg, she can control whether or not the egg is fertilized. If she chooses not to fertilize the egg, the resulting offspring will be a male bee or drone. If she chooses to fertilize the egg, the resulting offspring will be a female bee, either a queen or a worker. This type of reproduction is referred to as haplodiploid reproduction because male honey bees (from unfertilized eggs) are haploid while female honey bees (from fertilized eggs) are diploid. Queen and worker bees both originate from the same type of egg. The quantity and quality of food they are fed while young determines whether the female larvae will become a queen or a worker. So it is correct to suggest that workers are underdeveloped queens (though, some rightly argue that the reciprocal is most true, at least behaviorally and physiologically) because they were fed less food while developing as larvae. Worker bees, despite being sexually immature, have ovaries but they are unable to mate. They can, however, lay eggs. Because the eggs cannot be fertilized, workers are able to produce only drone offspring. This leads to an interesting dynamic in honey bee colonies. The presence of a queen in a colony suppresses a worker’s desire to reproduce. As long as the colony has a functioning queen, worker bees typically do not oviposit. However, honey bee colonies may lose their queens for a number of reasons. This event usually results in the rearing of a new queen, a feat accomplished by worker bees that begin to nurture a young female larva originally produced by the now-deceased queen. Despite this safety mechanism, many colonies fail to requeen themselves before the female larvae in the colony become too old to become queens. Because of this, many colonies become hopelessly queenless and are destined to perish. Despite the fact that the colony will die without a queen, it does have one last chance to pass its genetics on to other honey bees in the area. When a colony has become hopelessly queenless for a period of time (usually > 2 weeks), some workers’ ovaries develop, and the workers begin to oviposit. The resulting, haploid offspring all become drones. C Drones produced from laying workers are sexually viable, thus they are able to mate with virgin queens from other colonies in the area. This is the point in the reproductive cycle where Cape bees differ from all other races of honey bees. When a Cape bee colony goes queenless, it attempts to rear a new queen. And if for whatever reason the colony becomes hopelessly queenless, some workers’ ovaries will develop and the workers will begin to oviposit. However, unlike eggs produced by laying workers in other honey bee races, eggs produced by Cape laying workers are usually diploid, even though Cape workers cannot mate. This means that Cape workers are fully capable of producing female offspring, both workers and queens. The process by which Cape workers produce diploid eggs is called thelytokous parthenogenesis – they can produce males and females parthenogenetically. In this system, the egg pronucleus fuses with one of the polar bodies that results from meiosis, thus forming a diploid nucleus that continues to develop normally into a female bee (either a queen or worker). Queenless colonies of Cape bees can survive for some period of time and even rear a new queen from one of the laying worker’s eggs. If, however, the colony fails to requeen itself, the population will dwindle and the colony will die. Even multiple laying workers present in a colony cannot maintain the reproductive output of a single queen. Thelytoky in Cape bees leads to a number of different important considerations. For example, worker offspring produced by Cape laying workers are a type of clone, being genetically identical to their mother (who provided both sets of chromosomes). Furthermore, the ability of workers to lay diploid eggs breeds a type of reproductive conflict not seen in colonies of other races of honey bees. For example, queenless Cape colonies have a number of options: (i) produce a new queen from a queen mother egg, (ii) produce a new queen from a worker-laid egg, (iii) proceed as a laying worker colony, or (iv) proceed as a laying worker colony and later produce a queen from a worker-laid egg. It is important to note that thelytoky is not unique to Cape bees. It is believed that workers 717 718 C Cape Honey Bees, Apis mellifera capensis Escholtz from most (if not all) races of honey bees are capable of laying diploid eggs. However, < 1% of worker-laid eggs are diploid in other honey bee races. So while it is the exception, rather than the rule, in other honey bee races, thelytoky is common and the predominant scenario in Cape bee colonies. A number of hypotheses have been proposed for the prevalence of thelytoky in Cape bees. Perhaps the leading hypothesis is that because the Cape region of South Africa is very windy, Cape colonies experience a significant queen loss when queens leave the colonies to mate. Colonies with thelytokous capabilities would not suffer the loss of a queen the same way as colonies without thelytokous capabilities, thus favoring the propagation of colonies with thelytokous workers. Biology and Behavior Behaviorally, Cape bees are not unlike other African races of honey bees. They are “flighty” on the comb (run on the comb when the colony is disturbed), abscond (completely abandon the nest) readily in response to nest disturbances or diseases/pests, have smaller colonies than European races (an artifact of being in a warmer climate), use copious amounts of propolis (resins collected from trees and plants, used as a weatherproofing agent and antibiotic in the colony), and are well-suited to warm climates. Unlike other African bee races (especially Apis mellifera scutellata), Cape bees are docile, at least usually. Yet, there is a key behavioral difference that separates them from all other races of honey bees. Cape bees are considered social parasites. Social parasitism in Cape bees is not understood fully. In instances of larger numbers of colonies per unit area (e.g., managed-colony situations), worker bees and drones will “drift” between colonies. When the drifting bees are Cape worker bees, the worker bees can takeover or parasitize the “host” colony. In this regard, the mother queen of the host colony is lost (a process not understood fully at this point) and the Cape worker becomes the reproductive individual in the colony. This process can be exacerbated when two or more Cape worker bees drift into the same colony. Laying workers not only possess the ability to produce female offspring, but their pheromonal bouquet changes from that of a worker to that of a queen. This is especially true with respect to the pheromones of the mandibular glands, which change to a very queen-like scent. This change in scent makes the Cape laying worker become adopted by the parasitized colony as its new queen. That is why it is difficult to requeen a laying worker colony. The bees in the colony think they have a queen. Any introduction of a new queen into a Cape laying worker colony almost always results in the new queen’s death. The ability of Cape workers to produce female offspring elicits another interesting behavior in Cape colonies – worker policing. In worker policing, workers produced from one Cape laying worker can detect eggs oviposited by other laying workers and destroy or eat those eggs. This establishes a dominance hierarchy within Cape laying worker colonies whereby females from the same mother police the colony and destroy their aunts’ offspring in favor of their own mother’s offspring (their sisters). Research has shown that this behavior has led to territory grabbing within Cape laying worker colonies. Because a Cape laying worker colony is composed of many laying workers, all whose offspring are working to ensure their mother is the dominant laying force in the colony, bees produced by the same laying worker may congregate in the same area of the colony. So within a colony, one might find smaller “sub-colonies,” each headed by a laying worker. This system is truly amazing and has advanced the study of the development of sociality and reproductive castes. Problems for Beekeepers Although the biology and behavior of Cape bees are fascinating, they present a problem for beekeepers in South Africa. Cape workers can parasitize colonies Carabid Beetles (Coleoptera: Carabidae) as Parasitoids of any race of A. mellifera. Migratory beekeepers managing scutellata in the northern part of South Africa have moved bees into the fynbos region of South Africa where the Cape bee is present (the reciprocal also happens). This has allowed Cape workers to drift into and parasitize Apis mellifera scutellata colonies. This action has been a significant problem for beekeepers because Cape-parasitized colonies often dwindle and die. Furthermore, Cape bees are specialist foragers in the fynbos region and they often perform poorly when taken outside of this region. So Apis mellifera scutellata colonies parasitized by Cape bees in the northern part of South Africa can become useless to beekeepers. Beekeepers in South Africa often consider Cape bees more of a serious threat to their colonies than varroa mites (Varroa destructor, the most prolific pest of honey bees). Because of this, researchers globally have taken notice of Cape bees. Many fear that if Cape bees ever spread outside of South Africa, they may be a significant problem for beekeepers worldwide. C Capsid The protein coat or shell of a virus particle; the capsid is a surface crystal, built of structure units. Capsids Some members of the family Miridae (order Hemiptera).  Plant Bugs  Bugs Capsomere A cluster of structure units arranged on the surface of the nucleocapsid, in viruses possessing cubic symmetry. Carabidae A family of beetles (order Coleoptera). They commonly are known as ground beetles. Beetles References Hepburn HR (2001) The enigmatic Cape honey bee, Apis mellifera capensis. Bee World 82:181–191 Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer-Verlag, Berlin, Germany, 370 pp Johannsmeier MF (ed) (2001) Beekeeping in South Africa. Plant protection handbook No. 14, Agricultural Research Council, Pretoria, South Africa, 288 pp Capitate Having an expanded tip or club-shaped, and usually used in reference to antennae.  Antennae of Hexapods Capniidae A family of stoneflies (order Plecoptera). They sometimes are called small winter stoneflies.  Stoneflies Carabid Beetles (Coleoptera: Carabidae) as Parasitoids donaLd C. weBer, paveL saska, CaroLine s. ChaBoo USDA Agricultural Research Service, Beltsville, MD, USA Crop Research Institute, Praha, Czech Republic University of Kansas, Lawrence, KS, USA Several genera of carabid beetles are ectoparasitoids as larvae. The parasitoid habit is uncommon in beetles; only eleven beetle families include parasitoid species, compared to a much wider diversity of parasitoids in the Diptera and Hymenoptera. The evolution and ecology of these parasitoid beetles is fascinating, but their host associations are poorly known. Carabid beetles have been stereotyped as ground-dwelling generalist predators, yet in recent 719 720 C Carabid Beetles (Coleoptera: Carabidae) as Parasitoids years many counter-examples have shown the Carabidae to be more diverse in form, habit, and trophic association. Many carabids, especially tropical species, are arboreal. Granivory, herbivory, and specialized predatory habits are widespread. Three of the 76 recognized tribes are known to have parasitoid species: Brachinini, Peleciini, and Lebiini. All of these are ectoparasitoids on pupae of other beetles or, in one Peleciine genus, on immature millipedes. In all known parasitoid carabids, the larva passes through three distinct development phases. First, the free-living first larval instar emerges from an egg laid in the host’s habitat, and locates a host. Then, the larva feeds on a single pupal or pre-pupal host, while it molts zero to four times. Third, after the host is consumed, the larva undergoes a nonfeeding larval stage (“pre-pupa”) with zero to two molts; it then pupates next to the remains of the host. The total number of larval instars often deviates from the three molts typical for Carabidae, ranging from one (Pelecium) to five instars (some Brachinus). The adults live in the host habitat and may have a narrow or broad range of prey, including the immature stages of the host. The best-known genera of parasitoid carabids are Brachinus, Lebia, and Lebistina. Brachinus, the celebrated bombardier beetle, emits a directed, explosive spray of boiling-hot quinone solution, which is considered the most highly evolved defensive secretion of the many types documented in the Carabidae. Studies by Eisner and colleagues have shown the elaborate mechanisms which allow the orchestration of this exothermic reaction while protecting the emitter and instantly repelling potential predators. They have also shown the chain of evolutionary developments leading to this impressive set of defensive organs. North American Brachinus are found in littoral habitats near fresh water, where the known beetle hosts in families Hydrophilidae, Dytiscidae, and Gyrinidae emerge to pupate from their larval aquatic habitats. Recently, dryland European Brachinus have been associated with carabid hosts of the genus Amara, broadening the known hosts to 11 species, for only nine of the approximately 300 Brachinus species described. On the basis of fragmentary observation, it appears that Pelecium sulcatum (Pelecinii) develop as parasitoids on chrysomelid pupae and immature millipedes, and have only one larval instar. Lebia species number over 450 and the genus is cosmopolitan, with 47 in North America. Adults typically seek prey in plant canopies, and all known larvae are ectoparasitoids of chrysomelid beetle pupae, yet only four species’ hosts have been documented. Many additional Lebia species are reported to be associated (often with adult mimicry) with specific chrysomelids, particularly flea beetles (Alticinae) and casebearers (Cryptocephalinae), implying a host-parasitoid relationship. Two species parasitize economically important hosts: L. scapularis on elm leaf beetle, Xanthogaleruca luteola in Europe, and L. grandis on (Fig. 14) Colorado potato beetle, Leptinotarsa decemlineata in North America. Although elm leaf beetle is a significant invasive pest of ornamental elms in North America and elsewhere, L. scapularis apparently has not been considered for classical biological control. In contrast, L. grandis was introduced to France in the 1930s, and its parasitoid life history discovered, as part of a USA-France Carabid Beetles (Coleoptera: Carabidae) as Parasitoids, Figure 14 Lebia grandis fed first instar larva (top) with its prepupal host, Colorado potato beetle, Leptinotarsa decemlineata (photo by Caroline Chaboo). Carayonemidae classical biocontrol program. Since the carabid was originally described from North Carolina in 1830, over 60 years before Colorado beetle arrived there, its putative original host was the false potato beetle, L. juncta, the only Leptinotarsa present. Although the introduction to Europe failed, there is interest in future classical biocontrol because of the apparent host specificity and the fact that the adults are the most voracious predators known on eggs and larvae of Colorado potato beetle. Lebia adults are typically found in close association with their host species, and females oviposit in close proximity to the host pupal habitat; in the case of L. grandis, this takes place in the soil below infested host plants. Lebistina, an African genus closely related to Lebia, shows adult mimicry of its chrysomelid hosts, a pattern shared with some Lebia species. Lebistina is one part of a complex anthro-ecological story involving the San indigenous tribe of Southern Africa. San tribe members dig underground for the pupae of chrysomelids and their carabid parasitoids, both associated with the aromatic shrub Commiphora in the incense tree family, Burseraceae. Pupae of both the chrysomelid Diamphidia, and especially its parasitoid Lebistina, are collected for their potent neurotoxic arrow-poisons, which allow San hunters to fell large prey such as giraffes with small bows and arrows, but usually only after several days of tracking the injured animal. Parasitoid carabids present some fascinating evolutionary questions, not the least of which is why both the impressive arrow-poisons and the explosive exocrine toxins are associated with these genera. Yet, at most, 1% of their hosts are known. In addition, the possible management of predator/parasitoid beetles may offer an interesting opportunity for “double control” of chrysomelid pest species. C Erwin TL (1979) A review of the natural history and evolution of ectoparasitoid relationships in carabid beetles. In: Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) Carabid Beetles: their evolution, natural history, and classification. Dr W Junk, The Hague, The Netherlands, pp 479–484 Robertson H (2004) How San hunters use beetles to poison their arrows. Iziko museum of Cape Town. Available at www.biodiversityexplorer.org/beetles/chrysomelidae/ alticinae/arrows.htm (accessed 26 March 2008) Saska P, Honek A (2004) Development of the beetle parasitoids, Brachinus explodens and B. crepitans (Coleoptera: Carabidae). J Zool (Lond) 262:29–36 Weber DC, Rowley DR, Greenstone MH, Athanas MM (2006) Prey preference and host suitability of the predatory and parasitoid carabid beetle, Lebia grandis, for several species of Leptinotarsa beetles. J Insect Sci 6:9. Available online at http://insectscience.org/6.09/ Carabiform Larva This is another term for campodeiform larva.  Campodeiform Larva Caraboid Larva A larval form that is similar to campodeiform, but usually more chitinized and with stronger mandibles and short antennae. It is found in the families Staphylinidae, Carabidae, Dytisidae, and Hydophylidae (all in the order Coleoptera).  Campodeiform Larva Carapace This is not a term used with insects (hexapods). It is used to describe the fused dorsal covering of crustaceans. References Carayonemidae Eggleton P, Belshaw R (1993) Comparisons of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biol J Linn Soc 48:213–226 Eisner T (2003) For love of insects. Belknap Press, Harvard University, Cambridge, MA, 464 pp A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs 721 722 C Carbamate Insecticide Carbamate Insecticide One of a class of cholinesterase inhibiting insecticides derived from carbamic acid.  Insecticides Carbohydrate cardo stipes palpifer lacinia A large class of carbon-hydrogen-oxygen compounds, including simple sugars (monosaccharides) such as glucose. Glucose is the major fuel for most organisms and is the basic building block of polysaccharides such as starch and cellulose. Carboniferous Period A geological period of the Paleozoic era, extending from about 360 to 300 million years ago. The oldest insect fossils date from this period.  Geological Periods Carcinogen A substance or agent capable of causing cancer. Carcinophoridae A family of earwigs (order Dermaptera). They sometimes are called seaside and ring-legged earwigs.  Earwigs Cardo A term that is used differently among orders (Fig. 15) and structures, but most commonly refers to the base or proximal section of a maxillary appendage.  Mouthparts of Hexapods subgalea galea palpus Cardo, Figure 15 External lateral aspect of the left maxilla in an adult grasshopper, showing some major elements. Careers in Entomology Linda wiener St. John’s College, Santa Fe, NM, USA Entomologists are lucky to have a wide range of career choices. These include research in a wide variety of contexts, from universities, to many government agencies, to private corporations. The following is a summary of the institutions which hire entomologists, the types of work available and the qualifications usually required. Faculty research, teaching, and extension positions almost always require a Ph.D. in entomology or a related field. Leadership positions in government agencies and heads of research groups in industry and government require a Ph.D. plus related administrative experience. Research assistant positions are available for most graduate students. These are funded positions to perform research which also include tuition and a stipend. Teaching assistant positions are also available to graduate students. These Careers in Entomology include helping professors teach lecture and laboratory classes and grade papers and projects. Post doctoral fellowships are available to people with a Ph.D. to perform research on funded projects. There are a wide variety of research technician jobs that require an M.S. or relevant work experience or a combination of education and work experience. Positions in county extension and many regulatory positions require a B.S. and/or relevant work experience. There are many part time and intern positions which are available to high school or college students without a degree. Jobs in the urban pest control industry rarely require any special education. C Regulatory Regulatory work involves inspection of plants and animals entering an area with the goal of detecting, excluding, containing, or eradicating pathogens, weeds, and other undesirable organisms. Industry Industry work may involve research, but also inventing, patenting, and marketing new products. This also involves service oriented skills such as advising clients and providing pest control services. Qualifications and Skills Opportunities Each job listing will have a list of desired qualifications and skills. Educational Institutions Research Land Grant Universities and Cooperative Extension Research requires skills in areas such as devising, setting up, and running experiments, taking data, analyzing and recording data using computer programs, writing up results for publication and presenting results in lectures and conferences. Teaching Teaching skills include knowledge of the field and the ability to help students learn through lecture and discussion as well as designing courses and putting together course materials for a class. Extension Extension usually requires a combination of research skills and facility interacting with the public and other government organizations. These institutions usually have a focus on agricultural research and teaching with a network of extension stations throughout the state. Faculty positions generally involve a combination of research and teaching, often, but not always, focusing on applied rather than “pure” research. The research portion of the work involves the design and implementation of research projects, identifying sources and applying for research funding, training of graduate students and other students who participate in the research, writing up papers for publications, delivering lectures at conferences, and (if extension) interacting with and advising farmers. These positions usually include teaching in an area of expertise as well as teaching entry level courses in entomology. Land grant universities have insect collections for reference and research. Positions are available in the museums for taxonomists and collections managers who help identify, sort, label, and collect specimens. Extension work involves research on agricultural and urban plant and animal husbandry. 723 724 C Careers in Entomology Extension positions are available and based in each county to advise people about raising and caring for plants and animals. Extension work involves research and survey work as well as considerable interaction with the public and other government agencies. Extension positions often focus on agriculture and animal husbandry, but increasingly focus on urban landscapes and other urban pests. Positions also are available in the extension research stations connected with the university, but located in agricultural areas. Other Public and Private Research Universities There are many other research universities that hire entomologists as part of biology departments or departments of entomology, ecology, behavior, or evolution. Medical and veterinary schools also hire entomologists to do research on insect transmitted diseases and other insect related illnesses. Duties and qualifications are similar to the above. and Plant Health Inspection Service (APHIS) and the Forest Service. They hire for research, extension, and regulatory positions. Armed Forces The Navy, Army, and Air Force hire entomologists to do research on insects which transmit vector borne diseases such as malaria, dengue fever, and encephalitis as well as pest control specialists who work on ships and bases. Other Agencies Other agencies hire specialists in mosquito control and to track and advise on other public health concerns such as bubonic plague. The National Park Service and other government agencies hire entomologists for implementing IPM programs and handling pest control problems. Industry Undergraduate Colleges and Universities with a Focus on Teaching There are many smaller universities and colleges where a professor’s primary duties are in teaching. In these institutions, teaching duties can be quite various and a person with training in entomology might find herself teaching human anatomy or animal physiology, as well as courses in her specialty. Many professors also have research projects, though these are not as central to advancement as in the aforementioned research universities. United States Government U.S. Department of Agriculture The principal agencies hiring entomologists include the Agricultural Research Service (ARS), Animal Urban Pest Control and Landscape Maintenance This is a large and diverse industry that services business and residential customers. They need entomologists to do identifications, advise customers, and apply pesticides and other pest controls. Pesticide and Pest Control Device Manufacturers These businesses need entomologists to design and run evaluation tests on the pesticides and devices that a company markets. They also need experts to identify areas of need in the pest control industry and to consult with distributors and customers. Careers in Entomology Food, Tobacco, and Drug Companies These industries hire entomologists to research methods of keeping insects out of their packaged products and out of their manufacturing and processing areas. They also hire entomologists to do pest control in processing and packaging areas. International Aid Organizations A variety of agencies such as the World Health Organization (WHO), the United States Agency for International Development (USAID), and the International Center for Tropical Agriculture (CIAT) hire entomologists to work on a variety of public health and agriculture projects overseas. There are many non-governmental organizations (NGOs) which hire entomologists for similar projects. These are research and extension positions, generally temporary, and may require foreign language skills. Independent Entomologists This section will focus on entomologists who choose not to work for an institution, but who go into business for themselves. It is anticipated that this section will give ideas, inspiration, and some caution to those who are thinking of working independently as an entomologist. The individuals consulted for this section chose the independent route for a great variety of reasons. Some did not have the formal education to get a job in a university or government following established routes. Others did not like being a part of a large institution, or preferred working by themselves. Others could not realize their ambitions or dreams at a university and so formed their own foundations and businesses. Circumstances of all sorts cause some aspiring entomologists to put together a career in a location that lacks universities or industries that fit their skills or their C family situations. Many independent entomologists got their start working at a university or in industry and later struck out on their own. The following are typical examples of the work of independent entomologists. Keep in mind that these categories are rather general and not mutually exclusive. Many independent entomologists work in several of these areas. This brief survey should show that there are numerous opportunities available to those who prefer to work independently. Undoubtedly, there are some possibilities left out or still to be invented. The benefits mentioned most frequently of doing independent work are the ability to do what you love all the time, making (more or less) your own hours, the diversity of contacts that are developed, and the ability to conceive of a dream and bring it to fruition, while offering a valuable service not otherwise available. Some, with a lifelong passion for entomology but little or no formal education, have found their way to satisfying careers via the independent route. A few of these people have eventually obtained traditional jobs in universities or industry. Naturally, there is a downside to such work. Difficulties include the lack of support staff and the necessity of doing everything yourself, including all the bookkeeping, hiring, firing, advertising, phone answering, etc. Also, there is a frequent necessity of looking for new work which may involve lots of phone calls, drawing up of proposals, and periods without much income. On the other hand, many people mentioned that getting started was difficult, but after a few years, the work just keeps coming in with very little necessity to go out and look for it. Many independent entomologists have second jobs on the side ranging from teaching to police officer. Research and Development of Products Entomologists working in this area often contract to test and develop products for pest control as well as helping the developers through the complex procedures for registering a new product. 725 726 C Caribbean Fruit Fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae) People doing this work generally started out with standard jobs in universities or industry where they received training and made the contacts necessary to run a business on their own. Lectures, Workshops and Other Courses Entomologists working in this area design and teach courses on a wide range of topics from parasitic insects to tropical biology to urban pest control to the design, building, and maintenance of insect zoos. Such courses may be for professionals, graduate or undergraduate students, or the general public. They may also develop and sell educational materials. Lectures and classes on insects are also popular with garden clubs, elementary schools, nature centers, museums, state and national parks, elder hostels, agricultural associations, and many others. traditional chemical control programs), advising about rearing and displaying live insects, and advising industry about development or marketing of products. Many entomologists contract with other organizations to do specific tasks such as curating a particular group of insects for a museum, surveying private or public land for butterflies and other insects, and scouting fields for pests and beneficial insects and making control recommendations. Non Profit Organizations These organizations usually are focused on conservation of particular insect groups or insect habitats. These organizations also may include insects and pest control in a larger context such as preserving traditional agricultural techniques. Retail or Wholesale Business Writing and Photography Many independent entomologists write field guides, children’s books, and other books about animals and insects. A passion for photography or art involving insects frequently is the driving force for those who pursue a career in publishing books on insects. Urban Pest Control Perform routine and specialized pest control for home owners and businesses. This involves diagnosing problems, applying pesticides or otherwise controlling pest populations. It may also involve doing home repairs and other preventive measures. At least one intrepid entomologist has a store specializing in insect toys, jewelry, food, books, and other products. Other businesses sell insect control devices and chemicals. Caribbean Fruit Fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae) This fly affects various fruits in the Caribbean region.  Citrus Pests and their Management  Tropical Fruit Pests and their Management Carina (pl., Carinae) Consultant and Contract Work Consultants are probably the largest category of independent entomologists. Consulting work can range from pest control in urban or agricultural settings (often involving IPM and other alternatives to A ridge or keel. This character is evident on many orthopterans, and both lateral and medial carinae occur on the pronotum of some grasshoppers. It has considerable diagnostic value at the species level in grasshoppers.  Thorax of Hexapods Carnivorous Plants Carnid Flies Members of the family Carnidae (order Diptera).  Flies Carnidae A family of flies (order Diptera). They commonly are known as carnid flies.  Flies Carnivore A flesh-eating organism (contrast with herbivore). Carnivore Fleas Members of the family Vermipsyllidae (order Siphonaptera).  Fleas Carnivorous Feeding on animals. Carnivorous Plants James CressweLL University of Exeter, Exeter, United Kingdom Carnivorous plants use entrapped animal tissues, mainly insects, as a source of nutrition. There are approximately 600 species of carnivorous plants in six angiosperm subclasses, which include both monocotyledons and eudicotyledons. The multiple, polyphyletic origins of the carnivorous plants suggest that the syndrome is an adaptation to the low nutrient, bright, waterlogged habitats that the plants typically inhabit. Carnivorous plants are found worldwide in varied climates that span C extremes of temperature and rainfall. All carnivorous plants are insectivorous except for the few species with aquatic traps. Among the insectivorous plants, there are three kinds of structures that are responsible for trapping insects: mucilage (sticky) traps (found among the Lentibulariaceae, Roridulaceae, Byblidaceae, Droseraceae and Dioncophyllaceae); pitfall (pitcher) traps (Sarraceniaceae, Nepenthaceae, Cephalotaceae and Bromeliaceae); and snap traps (Droseraceae). Stalked glands bearing a droplet of adhesive liquid are the basis of mucilage traps. The glands are borne on leaf surfaces, and insects become entangled in the mucilage when they alight on or walk onto the glandular surface. Enzymatic juices are released by the plant and digestion of the prey ensues. Pitcher traps are modified leaves that are formed into vase-like structures that are held erect with the aperture uppermost. The lip of the pitcher may bear nectaries and pigment patterns that serve to attract insect visitors. Below the nectaries, the interior surface of the pitcher is smooth and slippery, and may be covered with minute, downward-pointing projections that prevent insect feet from obtaining a firm grip on the surface. The hapless insect visitor falls into the fluid in the base of the pitcher and drowns. Pitcher plants have digestive glands, but the dissolution of the prey is further assisted by various pitcher inhabitants, including microbes and insect larvae. Plants with snap traps have a pair of lobed structures that are capable of movement at the end of certain leaves. The trap responds to stimulation of trigger hairs on the trap surface by rapidly closing the lobes, which have marginal spines that interdigitate and thereby enclose the insect visitor. The trap reopens after the prey is digested by secreted enzymes. The prey of insectivorous plants typically are small, mobile individuals from a diverse array of taxa: Collembola,Diptera,Hymenoptera,Coleoptera, Hemiptera, Thysanoptera; with less frequent representation from Lepidoptera, Odonata, Orthoptera and other orders. Spiders, mites and isopods are also caught. To attract insects, the traps of some carnivorous plants provide nectar rewards and some are 727 728 C Carnivory and Symbiosis in the Purple Pitcher Plant pigmented, scented or glisten in ways that may emulate the attributes of flowers or carrion. Other traps rely simply on the tendency of insects to alight on, or walk across, convenient surfaces. Insect tissues are particularly rich in nitrogenous compounds, and plants reportedly obtain 10–75% of their nitrogen from prey, depending on species and location. Prey capture promotes flower production and the reproductive success of the plant. All carnivorous plants are pollinated by insects and there is a potential conflict between prey capture and pollination. Many plants have a spatial or temporal separation between their flowers and their traps that promotes segregation of these processes, so evidence for the existence of this conflict is rare. Pitcher traps often support a “phytotelm,” which is a plant-borne pool that comprises an aquatic ecosystem. The volume of phytotelms ranges from a few milliliters in Sarracenia pitchers to approximately 2 L in Nepenthes rajah. The insect members of the phytotelm community are Dipteran larvae, and different species adopt various lifestyles, such as filter feeding (e.g., mosquito larvae), saprophagy and predation. These inhabitants are sometimes referred to as pitcher “inquilines” or the “infauna.” Phytotelms are much studied by community ecologists looking at patterns of coexistence and community structure. There are also non-aquatic associates of pitcher traps. Ants (e.g., genus Camponotus) inhabit pitchers in certain pitcher plants (Nepenthes bicalcarata) and scavenge from the pitcher fluid. Additionally, spiders occasionally spin webs across pitcher apertures, thus acting as resource parasites.  Insectivorous Plants References Cresswell JE (2000) Resource input and the community structure of larval infaunas of an eastern tropical pitcher plant. Ecol Entomol 25:19–25 Ellison AM, Gotelli NJ (2001) Evolutionary ecology of the carnivorous plants. Trends Ecol Evol 16:623–629 Juniper BE, Robins RJ, Joel DM (1989) The carnivorous plants. Academic Press, London, UK Carnivory and Symbiosis in the Purple Pitcher Plant donna GiBerson University of Prince Edward Island, Charlottetown, PE, Canada Pitcher plants are a widely recognized group of carnivorous plants, well known for capturing and digesting small animals to supplement more usual nutrient sources. Carnivorous plants have fascinated biologists for centuries, despite making up only a tiny percentage of the species of flowering plants. Only about 600 species occur in six angiosperm subclasses. They generally inhabit nutrient-poor habitats, and the captured and digested insects provide a source of nitrogen, phosphorus, and micronutrients. Pitcher plants make up a substantial proportion of the carnivorous flora, with known representatives in three unrelated families: the new world Sarraceniaceae (27 + species), the tropical Nepenthaceae (103 + species) and the Australian Cephalotaceae (one species). The pitcher plants have modified tubular leaves or “pitchers” that act as simple pitfall traps for insects and other small terrestrial animals. Insects are attracted to the plant by color patterns or production of extrafloral nectar, then may lose their footing and fall into the pitcher to drown in fluid retained in the pitchers. In many cases, slippery surfaces and/or downward pointing hairs prevent the insects from climbing out and escaping. Some pitchers exclude rainfall by hoods that cover the pitcher opening (e.g., Nepenthes, some Sarracenia) and secrete fluids that include digestive enzymes (including proteases, esterases, acid phosphatases, and amylases) that collect at the bottom of the pitcher. Other species (e.g., Heliamphora spp. and Sarracenia purpurea) collect rainwater and may or may not secrete digestive enzymes into the water. One reason for the fascination with these plants is that they represent a type of plant/insect interaction that falls outside of the more expected Carnivory and Symbiosis in the Purple Pitcher Plant interactions such as herbivory or pollination. Therefore, many studies have concentrated on aspects of carnivory, such as cost-benefit analyses (i.e., cost of attracting insect prey versus nutritional benefit from prey), prey species composition, digestive enzymes, etc. Other researchers have focused on pitcher plants as habitat for a wide variety of organisms. Pitcher plant inhabitants include aquatic taxa that live in the fluid in the pitcher (insects, mites, rotifers, protozoa, and bacteria), but may also include wasps that build nests in the pitchers, ants that live in specialized parts of the plants, and spiders that spin webs across the mouth of pitchers. Because the pitchers function as discrete habitats with clear boundaries between the internal and external environment, they have been the subject of many process-related studies, examining food-web, energy flow, and community questions within entire ecosystems. This is particularly true for the purple pitcher plant, Sarracenia C purpurea, which is the most widely distributed pitcher plant in North America, and which has relatively long-lived pitcher habitats. Sarracenia Species in North America The Sarraceniaceae includes three genera in the New World: Sarracenia (8–11 species, depending on taxonomic opinion), Darlontonia (a single species in California and Oregon) and Heliamphora (at least 15 species in South America). Sarracenia is North American, and is mainly a genus of the American southeast (Table 5). As many as five species may occur naturally at a single site along the Gulf coast, but pitcher plant habitat is declining dramatically in these areas, and many species and subspecies in the genus are threatened by habitat loss. One species, S. purpurea (the purple pitcher Carnivory and Symbiosis in the Purple Pitcher Plant, Table 5 Sarracenia species in North America Species S. alata S. flava S. leucophylla S. minor S. oreophila Common name pale pitcher plant, or winged pitcher plant yellow pitcher plant white-topped pitcher plant hooded pitcher plant green pitcher plant S. psittacina S. purpurea parrot pitcher plant purple pitcher plant S. purpurea var. burkii (or S. rosea) S. rubra S. rubra alabamensis (or S. alabamensis) S. rubra jonesii (or S. jonesii) Burke‘s variety Distribution US Gulf coastal plain; SW Alabama to Texas US southeastern coastal plain; SW Alabama to SE Virginia US Gulf coastal plain; Florida to E Mississippi Northern Florida to North Carolina rare in North Carolina, Georgia, and Alabama; protected status US southern Gulf coast; Georgia to Mississippi fragmented locations through the eastern US from Florida north to Maine and westward to Minnesota; widespread across Canada from the Atlantic coast to the northern prairie provinces and into northern British Columbia and southern Northwest Territories US Gulf coastal plain; some elevate this to species status as S. rosea sweet pitcher plant canebrake pitcher plant SE USA; North Carolina to Florida and Mississippi rare in Alabama; protected; some elevate this to species status as S. alabamensis mountain pitcher plant rare in North and South Carolina; protected; some elevate this subspecies to species status as S. jonesii 729 730 C Carnivory and Symbiosis in the Purple Pitcher Plant plant), ranges throughout much of North America, from Florida and Labrador in the east, and northwestward through Minnesota and the Canadian prairie provinces, into northern British Columbia and the southern Northwest Territories. Populations are generally stable in the northern parts of the range, especially in the less human-populated areas of the Canadian boreal zone. Species are perennial, and have tube-shaped leaves that form pitfall traps for small, mobile invertebrates. All species also produce photosynthetic non-tubular leaves in response to light intensity and nutrients. Sarracenia species interact with insects in four major ways, (i) carnivory, (ii) pollination, (iii) herbivory, and (iv) symbiosis. All pitcher plants are carnivorous and attract insects as prey. The plants can self-pollinate, but several insects, especially bumblebees, are important in providing cross-pollination for the plants. Several insects feed on different parts of pitcher plants, and some of them are obligate pitcher herbivores, especially noctuid moths in the genus Exyra. Finally, some insects live inside the pitchers, especially in S. purpurea, which provides a relatively long-lasting aquatic habitat. Some wasps and spiders may also build nests in pitchers, and block the capture of prey by the plant. Information on herbivory and pollination ecology of pitcher plants can be found in the excellent review of pitcher plant-arthropod interactions by Debbie Folkerts. Most Sarracenia species secrete a small amount of fluid that collects in the bottom of the pitcher, and prey collects in this moist zone rich in digestive enzymes. The types of prey that are attracted and retained by the plant vary with pitcher morphology, mainly relating to the height of the pitchers and the size of the pitcher opening, but ants are a frequent prey item in most pitcher species. Most species have a hood that covers the pitcher opening, preventing rain from diluting the digestive enzymes. In contrast, pitchers in S. purpurea lack this covering hood, so the pitcher fills up with rain, providing a larger and more complex aquatic habitat than other Sarracenia species. Most North American studies of carnivory and symbiosis have concentrated on S. purpurea because its wide distribution and ability to hold water for relatively long periods of time allow the development of a surprisingly complex community of inhabitants. The Purple Pitcher Plant, Sarracenia purpurea Sarracenia purpurea is a long-lived herbaceous perennial that is widespread over much of North America. Pitcher-shaped leaves are produced in a rosette, with new pitchers produced every 15 or 20 days. Soon after a new pitcher opens, it fills up with rainwater and begins attracting insect prey, and several new leaves may be produced over the summer. The purple pitcher plant is exposed to a wide variety of conditions throughout a range which encompasses 30° longitude and 70° latitude. In the south, the species grows year round in a variety of nutrient poor habitats, whereas in the north, it has a relatively short growing season and is strongly associated with peatlands. Unlike other pitcher plants, pitchers of S. purpurea provide a stable habitat for several months, including over the winter, before degrading and losing water in their second year. In the northern part of the range, the pitcher fluid may freeze during the winter, but the pitcher retains its integrity for at least a few weeks into the new season and continues to hold water. Like most carnivorous plants, purple pitcher plants are associated with habitats where nutrients are not generally available. Interestingly, the plants have been shown to be nutrient limited in localities even where nitrogen amounts do not appear limiting. In these cases, soil microbes and plants such as Sphagnum intercept the nutrients before angiosperms like the pitcher plants can assimilate them. The ability to capture and digest animal prey provides nitrogen, phosphorus, and some micronutrients, and though the plant can grow without prey, the added nutrients are thought to be important for plant processes like flowering. Carnivory and Symbiosis in the Purple Pitcher Plant Carnivory in Purple Pitcher Plants Insects are attracted to the pitchers by both visual and chemical cues. The plant produces extrafloral nectar containing both carbohydrates and amino acids, allowing it to attract a wide variety of insects and other small invertebrates. Nectar, which is most abundant in newer pitchers, is produced in nectaries around the pitcher rim, where it accumulates and entices insects to move downward on the plant. UV light guides and purple streaks are found at the top of the pitchers and these also direct insects into the plant and downward into the pitcher fluid. Downward pointing hairs prevent the insects from escaping, and they eventually drown and are digested by the plant. In most Sarracenia species, digestion occurs through the action of digestive enzymes (e.g., proteases, hydrolases) produced in glands in the epidermis. Digestive glands and plant-produced enzymes had not been shown conclusively in S. purpurea and digestion was believed to result from proteolytic activity from bacteria and autolytic enzymes from the drowned victims. However, recent study has shown that not only does S. purpurea produce digestive enzymes (hydrolases), but that enzyme induction relates to pitcher developmental stage and to the presence of prey. Newly opened pitchers produce hydrolases even before the pitcher fills with water and before any bacteria or prey are present, but hydrolase levels decline if no prey are captured. The production of hydrolases can be re-induced, though, if prey is attracted to the pitcher at a later time. This may be a strategy to minimize the “cost” of carnivory to the plant, since digestive enzymes are produced only during the time when the pitcher is most attractive to prey or when prey are actually present. Carnivory is usually examined by identifying the captured and decomposing prey found in pitchers. Ants generally make up the majority of the prey items, but flies, bees, wasps, moths, beetles, leafhoppers, grasshoppers, and spiders are also found. Despite all the adaptations that the pitcher shows to attract and retain prey, videotape of C actual pitcher plant-insect interactions show that many insects are able to escape from the pitchers and capture efficiency is really quite low. In one study, several thousand insects were recorded in and around the pitcher mouth, but only about 2% were captured, and some groups (e.g., ants) were quite successful in escaping the pitcher trap. Most pitchers that have been evaluated in this author’s lab, though, have had significant deposits of decomposing insect detritus in the bottom, and no pitchers were devoid of prey, so even if capture efficiency is low, it is likely still high enough to add nutrients to the plant. Young pitchers attract the most prey, possibly due to the relatively large amounts of nectar produced in new pitchers compared to old ones. Pitchers continue to accumulate prey throughout the summer, however, and the highest overall amounts of detritus are found in the older, overwintered pitchers. Limnological Characteristics in Pitchers of the Purple Pitcher Plant Individual pitchers on purple pitcher plants form temporary aquatic habitats that can hold up to about 60 ml of water (for large pitchers), but more typically hold between 20 and 40 ml. The plant maintains a clean water environment in pitchers through uptake of CO2 and ammonia, and infusion of oxygen during photosynthesis. Oxygen levels are usually maintained at or near saturation for given temperatures (usually 5–10 mg/L), and pitchers rarely go anoxic in the field, and only if prey volumes are unusually high. However, other conditions within pitchers are usually highly variable, on both short and longterm scales, with large fluctuations in pH, temperature, and nutrients. Reported pH levels range from highly acidic (pH of about 3.0) to near neutral, depending on the pH of rainwater that fills the pitchers, the pH of plant secretions, and the pattern of prey decomposition. Several researchers have reported that pitcher pH declines 731 732 C Carnivory and Symbiosis in the Purple Pitcher Plant over time as prey is captured, and have related the declines to the decomposition processes in the leaves. We have also found dramatic diurnal variations in pH within individual pitchers, due to low alkalinity conditions and the uptake and release of CO2 during photosynthesis and respiration by the plant. Temperature patterns within the pitcher can also be highly variable, both geographically (over the extremely large geographical range of the plant) and seasonally or diurnally within a site. Pitcher plants usually grow in open bogs in full sunlight, so can be exposed to a wide range of ambient temperatures. Conditions within the pitcher usually do not vary as much as in the surrounding bog. Nutrient levels in the fluid depend on the age of the leaf, mainly because of temporal differences in the amount of prey captured. Hydrolases are secreted as the leaf opens and begins attracting insect prey, and then these enzymes combine with bacterial action and prey-derived autolytic enzymes to release ammonia and other dissolved nutrients. A steady supply of soluble nitrogen is therefore supplied for the plant through the breakdown of prey. Nitrogen fixing bacteria are also found in pitcher fluid, and these provide a further source of nitrogen to the plant. Animals living within the pitchers (arthropods and rotifers) feed on bacteria, protozoa, and the decaying prey and they excrete ammonia, which prevents nutrients from becoming sequestered in the bacteria and protozoa. The ammonia does not accumulate to toxic levels since the plant actively takes it up, especially when temperatures and light are at high levels. Aquatic Pitcher Inhabitants All Sarracenia species are associated with a suite of organisms (arthropods, rotifers, protozoa, bacteria) that reside within the pitcher and form communities of varying levels of complexity. Since S. purpurea pitchers hold water and provide habitat for several months, they form surprisingly complex aquatic communities comprising several trophic levels. The inhabitants have sometimes been referred to as resource parasites, intercepting prey that has been captured by the plant and using it for their own growth and development. However, it is now clear that these species also free up nutrients and prevent them from becoming sequestered in bacteria or protozoa, and can actually enhance release of nutrients to the plant. In return, the pitcher provides habitat and maintains a clean water habitat by actively taking up the toxic ammonia and CO2 produced by the living organisms in the pitcher. Several species of aquatic insect have been recorded alive in S. purpurea pitchers, but many of these (including stoneflies, caddisflies, midges, etc.) are thought to wash into pitchers during bog flooding events, and survive to emerge but not to actively colonize new pitchers. Three Diptera species (the pitcher plant mosquito, Wyeomyia smithii; pitcher plant midge, Metriocnemus knabi; and pitcher plant fleshfly, Fletcherimyia fletcheri) are obligate inhabitants of S. purpurea, and have been widely studied across their range, which approximates the range of the plant. At least eight other sarcophagids are associated with Sarracenia spp. pitchers, including Sarcophaga sarraceniae, and the other species of Fletcherimyia, but these are not as well studied as Fletcherimyia fletcheri. Other organisms that have been reported from purple pitcher plants include mites (especially Sarraceniopus gibsoni), a rotifer (Habrotrocha rosa), and a suite of protozoa and bacteria species. Wyeomyia smithii (Coquillett) (Diptera: Culicidae): The Pitcher Plant Mosquito The pitcher plant mosquito is, without doubt, the best studied of the pitcher plant inhabitants. Its range is slightly smaller than that of the pitcher plant itself, but it still extends over a wide area of Carnivory and Symbiosis in the Purple Pitcher Plant North America. The life history patterns vary depending on latitude. The species is univoltine in the north and bivoltine or even multivoltine in the south. It is autogenous for its first ovarian cycle throughout its range, but will take a blood meal to mature additional egg batches. It is an obligate pitcher plant inhabitant and is restricted to the purple pitcher plant in the north, though it will oviposit in other Sarracenia species in the south. Adult females are attracted to the pitchers through chemical cues and oviposit preferentially into new pitchers, increasing the chance that the pitcher will retain water throughout the insect’s life cycle. In the more northerly parts of the range, adult emergence and oviposition correspond to the period when pitchers are just opening in spring. Adults desiccate easily, and do not travel far from their natal pitchers. In one study in Prince Edward Island, Canada, it took 6 years for mosquitoes to recolonize pitcher plants (Fig. 16) that had been transplanted from another bog, despite a rich supply of pitchers with mosquito inhabitants within a few meters of the transplanted plants. Wyeomyia smithii larvae (Fig. 17) overwinter as larvae throughout their range, but again, there are differences that relate to latitude. They overwinter as 4th instar larvae in the south, and as 3rd instar larvae in the north (often frozen in the pitcher fluid), and diapause is both initiated and terminated via photoperiod. Recent work has shown that the photoperiodic responses are changing in response to global warming, and that measurable changes in the required daylength to induce diapause have occurred over the last 30 years. Despite their ability to overwinter in the frozen pitcher fluid in northern locations, they are not very tolerant of low temperatures, and will die if winter temperatures are too cold, or if sufficient snow cover is not available for insulation. Therefore, at northern edges of the range, there are many plants, and even entire bogs, where the mosquito is absent. They also die if there isn’t enough aquatic habitat for survival, for example, if the fluid dries under drought conditions or if the pitcher develops a hole through which the water escapes. C The mosquitoes feed by filtering bacteria, protozoa, and fine detritus from the water column, and they obtain their oxygen directly from the air through a breathing siphon, and through their cuticle. They are tolerant to wide diurnal variations in temperature, oxygen, and pH. Metriocnemus knabi Coquillet (Diptera: Chironomidae): The Pitcher Plant Midge The pitcher plant midge has been less studied than the mosquito, but is found in pitchers throughout most of the range of the plant, and is often present in very high numbers in pitchers. Larvae (Fig. 17) can overwinter in more than one instar, depending upon the stage of development when daylength begins to shorten; for example, different cohorts may overwinter as 2nd or 3rd or 4th instar larvae. Life cycles may be univoltine or bivoltine, depending on the summer temperatures during development, and oviposition occurs in both young and older leaves. The midges are more tolerant to cold than the mosquito, and they are found in many northern bogs where the mosquitoes are absent. Similar to the mosquito, the midge requires enough water to maintain an aquatic environment, but if the pitcher loses water (common in older pitchers that can lose their integrity), the midge larva can crawl from one pitcher to another on the same plant. They pupate in a gelatinous mass on the sides of the pitchers, and adults emerge and mate, then search for oviposition sites. The midge lives in the wad of detritus that collects at the bottom of the pitcher, and feeds by chewing into the bodies of the drowned insects or scavenges on the decomposing particulate material. They respire cutaneously and are relatively intolerant of low oxygen, so will only be found in pitchers with sufficient oxygen for respiration. Few natural pitchers experience anoxia, however, so it is rare to find pitchers in northern peat bogs without a strong complement of pitcher plant midges. 733 734 C Carnivory and Symbiosis in the Purple Pitcher Plant Carnivory and Symbiosis in the Purple Pitcher Plant, Figure 16 Glenfinnan bog and pitcher plants, Prince Edward Island, Canada: (a) bog habitat; (b) purple pitcher plant, Sarracenia purpurea. Carnivory and Symbiosis in the Purple Pitcher Plant C Carnivory and Symbiosis in the Purple Pitcher Plant, Figure 17 (a) Larvae of pitcher plant midge, Metriocnemus knabi; (b) larva of pitcher plant flesh fly Fletcherimyia fletcheri; (c) larvae of pitcher plant mosquito, Wyeomyia smithii; (d) modified tubular leaves or “pitchers” that act as simple pitfall traps for insects and other small terrestrial animals, and serve as a home to the aforementioned flies. Fletcherimyia fletcheri (Aldrich) (Diptera: Sarcophagidae): The Pitcher Plant Flesh Fly Sarcophagid flies are usually not associated with aquatic habitats, but several species, particularly within the genus Fletcherimyia, are found in pitcher plants. Fletcherimyia fletcheri is the most aquatic of the suite of pitcher plant species, and is an obligate inhabitant of the purple pitcher plant. Larvae (Fig. 17) are deposited directly into pitcher plants, with larvipositing females preferring new pitchers at the height of their prey attractance. Usually only one larva is found per pitcher, since larvae are aggressive and territorial and will kill or chase away any additional larvae. Not all larvae die after territorial encounters, though, since they are capable of limited movements to other pitchers. They are usually considered to be univoltine in the northern part of the range, and multivoltine in 735 736 C Carnivory and Symbiosis in the Purple Pitcher Plant the south. Larvae develop in the pitchers, then crawl out to pupate in the surrounding moss. Larvae feed at the surface of the water on newly drowned prey items. They attach to the surface tension and breathe surface oxygen through posterior spiracles, so are tolerant to wide variations in oxygen in the water. Other Pitcher Plant Inhabitants Mites are often found in pitcher plants, and feed either on the captured prey or on other mite species. It isn’t clear how the mites disperse from pitcher to pitcher, but they may travel on the bodies of the adult insect inhabitants or be associated with some of the obligate herbivores of pitcher plants. A species of bdelloid rotifer, Habrotrocha rosa, is also common in purple pitcher plants, though it is rarely seen unless pitcher fluid is examined without preservation, since the rotifers don’t preserve well and are usually washed through sieves before examination. The rotifers are very active, however, and can be fascinating to watch, if a researcher is patient enough to look for them. The rotifers feed on bacteria and particulate organic matter in the water column, and may be critical in providing soluble nitrogen and other nutrients to the plant. Protozoan and bacterial species diversity have rarely been enumerated, but at least 40 Protozoa species and several bacterial types have been recorded from pitchers. Pitcher Plants as “Model Ecosystems” Purple pitcher plant leaves provide ideal systems for investigating a variety of ecological questions. The pitchers form small, discrete, aquatic systems that support complex aquatic communities consisting of at least three trophic levels. Although they are aquatic ecosystems, they are located within terrestrial ecosystems, and therefore provide small “islands” of habitat where colonization and dispersal patterns, as well as food webs and energetics, can be studied relatively easily, and with a degree of replication that is not possible in most habitats. They are also easily manipulated, since it is relatively simple to add or remove food materials or top predators, to monitor population effects. Since purple pitcher plants occur over a vast geographical area, it is also possible to study ecological processes in entire ecosystems over a wide latitudinal range. The pitcher ecosystem is mainly detritus based, with energy coming from the insects that are captured by the plant, then drown and decay in the pitcher fluid. The lowest level of the food web is therefore made up of detritivores, including bacteria, some mites, the pitcher plant midge, and when present, the flesh fly. The pitchers may also contain phytoplankton. Protozoans and rotifers feed on the bacteria and algae, then are themselves fed on by the top predator in the system, the pitcher plant mosquito. There are usually no predators for the midges and flesh flies, despite their low position in the food web. Manipulations of various food web components have shown that pitcher plant communities respond to a combination of “top-down” and “bottom-up” regulation. Generally, the lower trophic levels are resource limited with respect to both population size and taxonomic richness, so as resources (prey) are added to pitchers, abundance and richness increases. In contrast, predator limitation targets specific groups only, so that addition of mosquito larvae results in a decrease in rotifers, but increases in bacterial abundance and richness. Many other studies have concentrated on other aspects of community structure, especially the interactions among the pitcher macrofauna (midges, mosquitoes, flesh flies). Some studies have found that the feeding of the midges releases nutrients that support mosquito populations, in a processing chain commensalism. Others have not found relationships among the major insect groups, suggesting that these patterns may relate to food availability. A recent study which evaluated latitudinal trends in species richness across most of the range of the purple pitcher plant found Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus that species richness (mainly of the bacteria and protozoa) increases with increasing latitude, contrary to most predictions of latitudinal patterns. This may also be driven by food web patterns, since the top predator in the system, the mosquito, declines in abundance with increasing latitude. Summary The purple pitcher plant is a widespread carnivorous plant which interacts with insects through carnivory and by providing habitat, as well as through herbivory and pollination. The pitchers form discrete aquatic habitats within a terrestrial landscape, and provide a home to a surprisingly complex community of aquatic organisms. Because of the ease of studying and manipulating these habitats, considerable information is available on both the individual taxa and their interactions, over a wide geographical range.  Carnivorous Plants  Insectivorous Plants  Bromeliad Fauna  Phytotelmata References Bradshaw WE, Creelman RA (1984) Mutualism between the carnivorous purple pitcher plant and its inhabitants. Am Midl Nat 112:294–304 Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Natl Acad Sci 98:14509–14511 Buckley HL, Miller TE, Ellison AM, Gotelli NJ (2003) Reverse latitudinal trends in species richness of pitcher-plant food webs. Ecol Lett 6:825–829 Dahlem GA, Naczi RFC (2006) Flesh flies (Diptera: Sarcophagidae) associated with North American pitcher plants (Sarraceniaceae), with descriptions of three new species. Ann Entomol Soc Am 99:218–240 Dress WJ, Newell SJ, Nastase AJ, Ford JC (1997) Analysis of amino acids in nectar from pitchers of Sarracenia purpurea. (Sarraceniaceae) Am J Bot 84:1701–1706 Fish D, Hall DW (1978) Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant, Sarracenia purpurea. Am Midl Nat 99:172–183 C Folkerts D (1999) Pitcher plant wetlands of the Southeastern United States: arthropod associates. In: Batzer DP, Rader RB, Wissinger SA (eds) Invertebrates in freshwater wetlands of North America: ecology and management. Wiley, New York, pp 247–275 Gallie DR, Chang S-C (1997) Signal transduction in the carnivorous plant Sarracenia purpurea: regulation of secretory hydrolase expression during development and response to resources. Plant Physiol 115:1461–1471 Giberson DJ, Hardwick ML (1999) Pitcher plants (Sarracenia purpurea) in eastern Canadian peatlands: ecology and conservation of the invertebrate inquilines. In Batzer DP, Rader RB, Wissinger SA (eds) Invertebrates in freshwater wetlands of North America: ecology and management. Wiley, New York, pp 401–419 Heard SB (1994) Pitcher-plant midges and mosquitoes: a processing chain commensalism. Ecology 75:1647–1660 Juniper BE, Robins RJ, Joel DM (1989). The carnivorous plants. Academic Press, London, UK Kitching RL (2001) Food webs in phytotelmata: “bottom-up” and “top-down” explanations for community structure. Ann Rev Entomol 46:729–760 Rice BA (2007) Carnivorous plant FAQ v11.0. Available at (http://www.sarracenia.com/faq.html.) Accessed 2 May, 2007 Rymal DE, Folkerts GW (1982) Insects associated with pitcher plants (Sarracenia: Sarraceniaceae) and their relationship to pitcher plant conservation: a review. J Alabama Acad Sci 53:131–151 Van Breeman, N (1995) How Sphagnum bogs down other plants. Trends Ecol Evol 10:270–275 Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus GeorGe m. orphanides A Research Institute, Nicosia, Cyprus In Cyprus, a cecidomyiid complex, Asphondylia spp. attacks the pods of carob, Ceratonia siliqua, causing a fruit stunting deformation known as brachycarpia. This malformation is reported to have been noticed on the island for the first time around 1870. The adult female (Fig. 18) inserts the eggs with its ovipositor in the carob pods when these are about 0.5 cm long. Infestation becomes evident 7–10 days later with the pod swelling gradually as the midge larva grows. The pupa is formed in the infested pod in a rather hardened 737 738 C Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 18 Adult of the carob midge, Asphondylia sp. whitish niche. Upon completing its development the adult emerges leaving the pupal skins halfprotruding from the infested pod. Initially it was believed that the cecidomyiid responsible for brachycarpia was Asphondylia gennadii (Marchal) and that it attacked only carobs. Later biological studies in Cyprus, however, revealed that the midges from carob pods (Figs. 19–20) required an alternate host for the summer. The adults of the overwintering generation emerging from carob pods in April would not deposit their eggs in the few out-of-season young carob pods that could sometimes be available. No alternative points of attack on the carob tree could be found. Instead, they would search for secondary host-plants like caper (Capparis spinosa), pepper (Capsicum annuum), potato (Solanum tuberosum), garden rocket (Eruca sativa), mustard (Sinapis spp.), sea squill (Urginea maritima), asphodel (Asphodelus fistulosus), and St. Johnswort (Hypericum crispum). The successful development of the carob midge on all these host plants was proved experimentally in cages and supported by meticulous observations in isolated areas under natural conditions. On caper the females insert the eggs within the flower bud among the petals, the stamens and on the ovary. On pepper, squill, potato and St. Johnswort they insert their eggs in the ovary during the flowerbud stage (Fig. 21). As a result, infested flower buds harden and never bloom. Five or six generations develop on the secondary plants, which are available for infestation until September–October. At that time, the midges return to carobs to lay their eggs in the newly formed pods of the normal flowering season for the overwintering generation. The above findings stimulated a re-examination of the generic placement and the overall taxonomic status of the carob gall midge. Adults, larvae and pupae from all the mentioned host plants are anatomically identical, suggesting that all these midges may belong to one species. However, there is a differential host preference among adults from the various secondary hosts. For example, adult females from pepper readily attacked only pepper and garden rocket, rarely attacked caper and did not attack squill and St. Johnswort. Those from caper readily attacked caper, mustard, garden rocket, asphodel and St. Johnswort, rarely attacked Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus C Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 19 Normal (n) and midge-infested (i) carob pods. Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 20 Ovipositor of the carob midge, Asphondylia sp. 739 740 C Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus CYPRUS Squill Mustard Garden Rocket Asphodel St. Johnswort Pepper Caper Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 21 Differential host preference among carob midge adults from squill, pepper and caper. pepper and did not attack squill. Finally, midges from squill readily attacked squill, garden rocket and mustard but did not attack pepper and St. Johnswort. In an older survey (1970–1972) midge infestation on carobs and caper, in contrast with that on the other host plants, was widely distributed all over the island. A striking difference, however, was observed with the infestation on pepper that occurred only on the northern coast and the whole Karpasia peninsula (Fig. 22). The southern part of the island is still free from midge infestation on pepper. The northern part is now inaccessible to repeat the survey. This characteristic distribution of midge infestation on the different host plants and the midge behavior on host preference indicates that the carob midge complex consists of the overwintering generation of a morphologically homogenous but biologically heterogeneous population of Asphondylia. It is possible that there are three races or sibling species of this gall midge. Damage On carobs, the estimated loss of yield is significantly lower than the apparent one. The number Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 22 Distribution of carob midge infestation on pepper in Cyprus. of carob pods on each inflorescence is generally very large and certainly not all of them reach maturity. All the unfertilized pods drop at an early stage of their development unless the carob midge attacks them. Infested pods do not drop. The majority of the fertilized pods will also drop at their early growing stages because trees cannot bear to maturity all the pods produced. Consequently, it is misleading to calculate the damage by comparing the infested and normal pods because among the infested pods, a significant number would have dropped even in the absence of the carob midge. The relationship between the estimated loss of yield and the observed infestation was found to be described by a second-degree polynomial curve with the equation ŷ = - 0.12 + 0.177x + 0.00247x2. Mortality Factors The natural mortality factors recorded were: (i) the parasites – Eurytoma sp. A., Eurytoma sp. B., Pseudocatolaccus nitescens (Walker), Tetrastichus brevicornis (Panzer), Eupelmus urozonus Dalm., Adontomerus sp. and Paraholaspis sp.; (ii) predators – ants, earwigs, spiders; (iii) unidentified molds; and (iv) weather conditions. Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae) Molds appear in the interior part of the infested carob pods, causing the death of the midge larva. Subsequently, the pods drop. Ants have been observed cutting holes through the infested carob pods and earwigs would enlarge these holes. The midge larvae or pupae would then be destroyed either by these predators or by the development of molds or they would dry up. Spiders attack adult midges while the latter rest during the day. The midge mortality occurring from November to April is mainly due to abiotic factors (weather). The effectiveness of the biotic factors (parasites, predators and molds) becomes evident from April onwards. References Anon (1914) Entomological notes. Cyprus Agr J 35:805–807 Gagné RJ, Orphanides GM (1992) The pupa and larva of Asphondylia gennadii (Diptera: Cecidomyiidae) and taxonomic implications. Bull Entomol Res 82:313–316 Gennadius P (1902) The carob tree. Government Printing Office, Nicosia, Cyprus, 30 pp Harris KM (1975) The taxonomic status of the carob gall midge, Asphondylia gennadii (Marchal), comb. N. (Diptera, Cecidomyiidae), and of other Asphondylia species recorded from Cyprus. Bull Entomol Res 65:377–380 Morris HM (1930) Report of the entomologist for 1929. Report of the Director of Agriculture, Cyprus, pp 47–55 Orphanides GM (1975) Biology of the carob midge complex, Asphondylia spp. (Diptera, Cecidmyiidae), in Cyprus. Bull Entomol Res 65:381–390 Orphanides GM (1976) Damage assessment and natural control of the carob midge complex, Asphondylia spp. (Diptera, Cecidomyiidae) in Cyprus. Bollettino del Laboratorio di Entomologia Agraria “F. Silvestri” 33:80–98 Carotenoids Carotenoids are among the most common and important natural pigments. They are fat-soluble, and found principally in plants and photosynthetic bacteria, where they are abundant in chloroplasts and play a critical role in photosynthesis. They also C occur in some non-photosynthetic microbial organisms. Animals are incapable of carotenoid synthesis, but they obtain them from their diet where they serve as antioxidants, serve as a precursor to vitamin A, and impart bright coloration. Carotenoids are responsible for much of the red, orange, yellow, and brown color found in plants, as well as some of the coloration of animals, including insects. At least 600 different carotenoids are known. They are derived from a 40-carbon polyene chain, and display alternating single and double bonds. The specific end groups on these molecules affect polarity and help determine how they interact with membranes. The hydrocarbon carotenoids are known as carotenes. The oxygenated carotenoids are called xanthophylls. Beta-carotene is perhaps the best known carotenoid. In insects, carotenoids are responsible for the yellow color of such insects as pierid butterflies and the orange of ladybird beetles. Combined with blue pigment, carotenoids can produce green color. One of their most important functions is the production of the visual pigment retinene. Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae) John h. kLotz, LaureL d. hansen University of California, Riverside, Riverside, CA, USA Spokane Falls Community College, Spokane, WA, USA Carpenter ants play critical roles in forest ecosystems as predators of defoliating insects, decomposers of cellulose, and as vital links in food webs. They may become serious household pests, however, when they infest structures and damage wood. Carpenter ants belong to the highly diverse and cosmopolitan genus, Camponotus, in the 741 742 C Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae) subfamily Formicinae (Table 6). The formicines are characterized by their production of formic acid in the venom gland, a potent alarm pheromone and defensive compound that is sprayed on its victims. There are 19 other subfamilies in the family Formicidae. Of the 288 genera of ants, with approximately 11,800 species described so far, Camponotus is one of the most impressive with an estimated 1,000 species worldwide. In the United States and Canada there are approximately 50 species of Camponotus, of which 24 are considered to be structural or nuisance pests. Those causing the most damage belong to the subgenus Camponotus. Since the majority of species in this group nest in wood, they are commonly called carpenter ants. Two of the most common species that infest structures are black carpenter ants, C. modoc in western states, and C. pennsylvanicus in central and eastern states. Colony Development The claustral mode of colony founding, wherein the queen seals herself off in a chamber and rears her first brood in isolation, is typical for carpenter ants. After the spring mating flights, inseminated queens search for suitable nest sites in wood where they construct a cavity and lay a clutch of eggs. The queen does not leave the chamber to forage, instead metabolizing her fat bodies and wing muscles to provide nourishment for herself and the growing brood. Depending on temperature and species, complete metamorphosis (development of egg-larva-pupa and adult stages) takes from 6 to 10 weeks before the first workers emerge. These first workers are small due to the limited food supply and are therefore called minims. With their arrival, foraging commences and the colony begins to grow. The queen lays a second clutch of eggs in late summer but these do not complete development until after winter dormancy. After the first year, the queens of C. modoc and C. pennsylvanicus have two annual periods of oviposition, the first in late winter or early spring and the second in summer. Major (larger) and media (smaller than major, but larger than minim) workers are not produced until the third season, and reproductives only after several years. Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae), Table 6 Some common species of carpenter ants and their geographic distribution Camponotus species Geographical distribution C. americanus Mayr Eastern and central USA, SE Canada C. chromaiodes Bolton Eastern and central USA, SE Canada C. herculeanus (Linnaeus) Northern USA, Canada, Alaska, Europe C. ligniperdus (Latreille) Europe C. modoc Wheeler Western USA, southwestern Canada C. novaeboracensis (Fitch) Northern USA, southern Canada C. pennsylvanicus (DeGeer) Eastern and central USA, SE and S central Canada C. essigi Smith NW Mexico to S Canada C. nearcticus Emery Northern USA, eastern USA, S Canada C. sayi Emery Southwestern USA and Mexico C. floridanus (Buckley) Southeastern USA C. castaneus (Latreille) Eastern central USA C. variegatus (Smith) Hawaiian islands C. vicinus Mayr Western USA, Mexico to S Canada Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae) C Mature colonies are partitioned into a main or parent nest where the queen resides, and into satellite nests that contain workers, mature larvae, pupae, and winged reproductives. Generating satellite nests expands the territory of a colony, while a network of interconnecting trails maintains communication and flow of resources between the nests. The number of satellite nests per colony and their size varies. For example, ten nests were counted in a colony of Florida carpenter ants, C. floridanus, and 12,000 workers were found in a satellite nest (Fig. 23) of C. modoc. Thus, the total number of ants in a colony may attain over 50,000 in the case of C. modoc and more than 100,000 in C. vicinus. The difference in size may be attributed to the presence of multiple queens (polygyny) in C. vicinus colonies versus a single queen (monogyny) that is typically found in colonies of C. modoc and C. pennsylvanicus. Wood with high moisture content is selected for colony initiation by inseminated queens. Moisture is a requirement for the development of eggs and young larvae, and parent nests will often be located in areas outside structures where there is sufficient humidity. Satellite nests are typically found in drier areas because eggs and young larvae are not present. These nests are often found in structures under insulation, in attics, wall voids, and subfloors where higher temperatures and humidity occur. case of C. pennsylvanicus, for example, odor trails are the primary orientation cue, but workers are also capable of landmark and celestial orientation. As with other ants, tactile cues are also used for orientation, and edge-following is commonly observed in carpenter ants, particularly along structural guidelines in man-made environments. Home Range Trophallaxis The territory of a colony is determined by its daily activity range, which includes the network of trails connecting its various nests with resource sites. The area covered by a large mature colony may be considerable. For example, in the case of the Florida carpenter ant nest complex mentioned above, it spread over an area measuring 43 m across; and trails 200 m long have been reported for C. modoc. Many species of carpenter ants are nocturnal, and they have evolved special adaptations for finding their way in the environment at night. In the Honeydew is a favorite food of carpenter ants. Excreted by homopterans such as aphids, it contains sugars, amino acids, minerals, and vitamins. Carpenter ants have specialized digestive tracts for handling this liquid diet, and removing solids with a filtration mechanism in their mouthparts. The crop, also known as the social stomach, is a distensible sac located in the gaster of the ant which expands to hold liquids that are stored, transported, and finally regurgitated and shared via trophallaxis with other ants. This food-sharing Foraging Carpenter ants use group foraging to exploit ephemeral resources. The discovery of a food item too large to handle individually prompts a scout to deposit a chemical trail pheromone on the ground as she returns to the nest. The trail pheromone is produced in the hindgut and, in combination with formic acid, stimulates trail-following by other ants that the scout actively solicits when she arrives back at the nest. Established trails are used for more permanent resource sites such as aphid colonies that may remain in use from one season to the next. It is thought that the foraging population makes up no more than 10% of the colony population. Some of the larger species make prime targets for visual predators such as birds, so it is not surprising that their foraging is conducted primarily at night. The onset of foraging in C. pennsylvanicus and C. modoc is a dramatic event to observe, with large numbers of ants pouring out of the nest at dusk. 743 744 C Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae) Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae), Figure 23 Carpenter ants and damage: workers of Camponotus vicinus in a nest (above); satellite nest of Camponotus modoc under subfloor insulation (center); damage caused by Camponotus modoc to building timber (below) (photos by Laurel Hansen). Carpenter Bees (Hymenoptera: Apidae: Xylocopinae) behavior among workers, and from workers to larvae and the queen, is a fundamental bond in the social behavior of ants. Pest Management The structural pest management industry ranks carpenter ants as one of the most important economic pests. In certain regions of the United States, such as the Northeast and Pacific Northwest, carpenter ants outrank termites as wood-destroying organisms. They are also notoriously difficult to control. In order to be effective, a management program for a household infestation of carpenter ants must be based on a thorough inspection. Ideally, all of the nests on the property should be located, both inside and outside. Structural infestations are more commonly caused by satellite nests; however, the original source of the problem often results from a parent nest located outside. Locating nests is often difficult due to the cryptic behavior of carpenter ants. In this regard, a “feed and follow” technique can be helpful. Chopped insects such as crickets or mealworms are provided to the ants, which are then followed back to their nest. This technique is most effective when conducted at night when the majority of foragers are active. Outdoor nests may be located in live or dead trees, stumps or logs, landscape timbers, firewood piles, and buried wood. Indoors, common nest locations include crawl spaces and attics, often in or under insulation. In addition, satellite colonies will nest in exterior and interior wall voids, and hollow doors. Ant activity is often associated with moist conditions in and around sinks, dishwashers, bathtubs, showers, and toilets. Once the nests have been located, they can be treated with a contact insecticide appropriate for the situation (e.g., a dust formulation in a wall void, or spray for infested landscape timbers). If nests are not located, there are other treatment options offered by pest control companies. In what is known as a perimeter treatment, a band of insecticide is sprayed around the outside foundation C of a structure, along door and window frames, and under the lower edge of siding. Depending on the insecticide used, some act as barriers to the ants while others are non-repellent. In the latter case, the insecticide is picked up by the ant and carried back to the nest where it can be spread to other ants. Toxic baits may be effective if they are sufficiently attractive to the ants. Their recruitment and food-sharing behavior facilitates the distribution of a toxicant throughout the colony. References Cannon CA, Fell RD (1992) Cold hardiness of the overwintering black carpenter ant. Physiol Entomol 17:121–126 Hansen LD, Akre RD (1985) Biology of carpenter ants in Washington State (Hymenoptera: Formicidae: Camponotus). Melanderia 43:1–63 Hansen LD, Klotz JH (2005) Carpenter ants of the United States and Canada. Cornell University Press. Ithaca, New York, 224 pp Klotz JH, Greenberg L, Reid BL, Davis L Jr (1998) Spatial distribution of colonies of three carpenter ants, Camponotus pennsylvanicus, Camponotus floridanus, Camponotus laevigatus (Hymenoptera: Formicidae). Sociobiology 32:51–62 Hedges, SA (1998) Field guide for the management of structure-infesting ants. Franzak & Foster Co, Cleveland, OH, 155 pp Carpenter Bees (Hymenoptera: Apidae: Xylocopinae) John L. Capinera University of Florida, Gainesville, FL, USA The common name of these insects is derived from their nesting habits. Although small carpenter bees, Ceratina spp., excavate tunnels in pithy stems of various bushes, the large carpenter bees, Xylocopa spp., chew nesting galleries in solid wood or in stumps, logs, or dead branches of trees. Obviously, the wood-attacking species are the basis for the “carpenter bee” name designation. The latter bees may become economic pests if nesting takes 745 746 C Carpenter Bees (Hymenoptera: Apidae: Xylocopinae) place in structural timbers, fence posts, and other wood structures. It is Xylocopa that most people know about or are concerned about, at least in North America. The easiest method of separating Ceratina from Xylocopa is by size: Ceratina are < 8 mm in length, whereas Xylocopa are 20 mm or larger. At various times, carpenter bees have been placed in the families Anthophoridae, Xylocopidae, or Apidae, though the most recent placement is within the Apidae. This family is characterized, in part, by the jugal lobe of the hind wing being absent or shorter than the submedian cell and by the forewing having three submarginal cells. Within the family, carpenter bees are distinguished most easily by the triangular second submarginal cell, and by the lower margin of the eye almost in contact with the base of the mandible (i.e., the malar space is absent). Xylocopa spp. generally resemble bumble bees in size and color. They are black, metallic bluish or greenish black, or purplish blue. Some males have yellowish areas on the face. Both sexes may have pale or yellowish pubescence on the thorax, legs, or abdomen, but there tends to be less yellow color than in bumble bees. Sometimes they are unicolorous, ranging from entirely yellow to entirely black. Large carpenter bees are readily distinguished from bumble bees primarily by the absence of pubescence on the dorsum of the abdomen, which is somewhat shiny. They also lack a malar space (present in bumble bees), and the triangular second submarginal cell. Xylocopa virginica is the species of most concern in the USA, though locally other species can be abundant. Xylocopa virginica normally uses dry, coniferous woods as nesting sites, including Pinus, Juniperus, and Taxodium spp., but some deciduous woods used in fence railings are also used. Hardwood timber is usually avoided. Xylocopa virginica selects nesting sites in well-lighted areas where the wood is not painted (though they may not be deterred by stains) or covered with bark. In general, these bees are gregarious, often building several tunnels in the same location, and also tending to nest in the same areas for generations. Old nests are refurbished, but new nests are also constructed at old locations. In new nests, female bees chew their way into the wood, excavating a burrow about 15 mm in diameter. Boring proceeds more slowly against the grain (about 15 mm a day) than with the grain. The direction of galleries in the wood appeared to depend on the direction of the grain. If the grain is oriented vertically, the nests are vertical; if horizontally, then the nests tend to be horizontal with respect to the ground. Galleries extend about 30–45 cm in newly completed nests. New tunnels are smooth and uniform throughout, but older galleries show evidence of less uniformity with random depressions and irregularities. Apparently these older galleries are used by several generations of bees. Also, several bees may use a common entry hole connecting to different tunnels. After excavating the gallery, female bees gather pollen, which is mixed with regurgitated nectar. The pollen mass is placed at the end of a gallery, an egg is laid, and the female places a partition or cap over the cell composed of chewed wood pulp. This process is repeated until a linear complement of six to eight end-to-end cells is completed. Females apparently construct only one nest per year in northern locations, with bees emerging in the late summer and overwintering as adults, and with mating taking place in the spring. In warm-weather areas such as Florida, however, at least two generations are produced per year, with broods occurring in February-March and during the summer. In Florida, adult bees are active from November to January and from April to summer. Several types of “damage” are directly associated with carpenter bees: weakening of structural timbers in barns, sheds and other open structures where bees have ready entry; defacing of wood trim on structures, usually the eves of houses; gallery excavation in wood water tanks (much less a problem now that metal has replaced wood in most instances); and human annoyance. The last point is included because carpenter bee females may sting (rarely, and males do not sting), and male bees may hover or dart at humans who venture into the nesting area. In general, carpenter bees are Carpenter, Frank Morton not much of a threat to people, but this does not prevent people from becoming alarmed because these are large insects. Also, there sometimes is an indirect effect of carpenter bee colonization on structures. Occasionally woodpeckers are attracted to tunnels to feed on the brood. If the tunnels are in a structure, the damage resulting from the woodpecker can be significant. A buzzing or drilling sound is heard when a carpenter bee is boring into the wood. If the hole is not visible, as often is the case when the bee is boring under the eves of houses, their activities can be detected by the presence of sawdust on the ground under the hole. As noted previously, carpenter bees rarely attack painted or varnished wood. In areas frequented by these insects, damage to structures can often be prevented by painting. If this is not effective or desirable, a small amount of insecticide that is labeled for bees and wasps can be applied to the affected area, including the entryways of the tunnels. Also, the holes could be plugged with caulking, putty, or similar substance, or screened. A common approach is to spray or dust the tunnels with insecticide, allow the bees a day or two to contact the insecticide and move it around the tunnel, and then plug the hole. Alternatively, because the number of bees is usually not great, and because the bees are fairly docile, it is usually possible to capture them all with an insect net and freeze or crush them, thereby avoiding the cost and hazard of insecticides. Carpenter bees generally are not pests. Even those species considered to be occasional pests, such as X. virginica, offset their damage by pollination services, including pollination of economically important plants. Small carpenter bees are never pests because they excavate nests and provision only the hollowedout stems of twigs. Like the larger xylocopines, they excavate nests with their mandibles, and use these cavities for both nesting and overwintering sites. The female provisions the nest with pollen and nectar, deposits an egg, then caps the cell with masticated plant material. Typically she repeats the process again and again until several cells are C stacked within the hollowed stem. The last cell area is left incomplete, and she uses this area to rest and to defend her nest from intruders. She remains close to the nest until her offspring emerge. Interestingly, because the first laid eggs hatch first, and they are deepest within the hollow stem, the new adults (which do not chew their way laterally through the wall of the stem) must navigate around the younger, less developed siblings stacked above in order to escape. The new adults chew through the cell caps, moving the debris down but being careful not to damage any wasps still in the pupal stage, and moving the pupae up to rest on the new, elevated floor of the cell. It may take several days for the firsthatching wasp to dig its way out, and by this time other wasps likely have hatched, resulting in a trail of adults, all working in tandem to pass cell cap material down.  Bees (Apidae) References Balduf WV (1962) Life of the carpenter bee, Xylocopa virginica (Linn.). Ann Entomol Soc Am 55:263–271 Daly HV (1973) Bees of the genus Ceratina in America north of Mexico. UC Publ Entomol 74:1–113 Howard LO (1892) Note on the hibernation of carpenter bees. Proc Entomol Soc Washington 2:331–332 Hurd PD Jr (1955) The carpenter bees of California. Bulletin of the California Insect Survey 4:35–72 Hurd PD Jr (1958) Observations on the nesting habits of some new world carpenter bees with remarks on their importance in the problem of species formation. Ann Entomol Soc Am 51:365–375 Hurd PD Jr (1961) A synopsis of the carpenter bees belonging to the subgenus Xylocopoides Michener. Trans Am Entomol Soc 87:247–257 Hurd PD Jr, Moure JS (1963) A classification of the large carpenter bees (Xylocopini). UC Publ Entomol 29:1–365 Rau P (1928) The nesting habits of the little carpenterbee, Ceratina calcarata. Ann Entomol Soc Am 21:380–397 Carpenter, Frank Morton Frank Carpenter was born in Boston, USA, on September 6, 1902. His father, although an 747 748 C Carpenterworm Moths (Lepidoptera: Cossidae) employee of a business company, had a strong interest in natural history, and encouraged Frank’ s interest in insects. He entered Harvard University in 1922, and graduated with an A.B. degree in 1926, a master’ s degree in 1927, and a D.Sc. in 1929. His doctoral thesis on fossil ants was published in 1930, but was preceded by seven of his earlier papers on fossil insects. In 1928 he was appointed at Harvard University as research fellow in applied biology, in 1931 as associate in entomology, in 1932 as assistant curator of invertebrate paleontology, in 1935 as instructor in zoology, in 1936 as curator of fossil insects, in 1939 as assistant professor of entomology, in 1945 as Alexander Agassiz professor of zoology, in 1969 as Fisher professor of natural history, and in 1973 became emeritus professor. This is the man who built the fossil insect collections of Harvard University’ s Museum of Comparative Zoology. For nearly 40 years, he taught entomology and paleontology. He was chairman of the Department of Biology in 1952–1959 and had a heavy role in extension. His research in fossil insects spanned 70 years, and he specialized in the Paleozoic fauna. The fossil dragonfly that he described as Meganeuropsis americana, with a wingspan of 29 inches is the largest insect known. In addition to work on fossil insects, he worked on systematics of present-day Neuroptera, Raphidioidea and Mecoptera. After retirement in 1973, he continued voluntarily to curate the collection of fossil insects and to edit Psyche, the journal of the Cambridge [Massachusetts] Entomological Club (a job he held from 1947 to 1990). His wife Ruth, to whom he was married for 64 years, was a constant companion and helper. He died in Massachusetts on January 18, 1994. Reference Furth DG (1994) Frank Morton Carpenter (1902–1994): academic biography and list of publications. Psyche 101:126–144 Carpenterworm Moths (Lepidoptera: Cossidae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Carpenterworm moths, family Cossidae, total 682 species worldwide; actual fauna probably exceeds 750 species. The group is a relict family which has retained many primitive features and often is classified closer to Tineidae and Psychidae. There are five subfamilies, two of which are exclusively Neotropical (Chilecomadiinae and Hypoptinae): Chilecomadiinae, Cossulinae, Cossinae, Hypoptinae, and Zeuzerinae. The family is in the superfamily Cossoidea (series Cossiformes) in the section Cossina, subsection Cossina, of the division Ditrysia. Adults small to very large (9–240 mm wingspan), with head small and average or slightly rough scaling; labial palpi upcurved; maxillary palpi small, 1–2-segmented; antennae filiform or bipectinate (antennal tips usually thinner). Wings are elongated (Fig. 24) and hindwings often rather small and rounded; body very robust (the largest female cossids rival hawk moths in size and mass). Carpenterworm Moths (Lepidoptera: Cossidae), Figure 24 Example of carpenterworm moths (Cossidae), Stygia leucomelas Ochsenheimer from France. Carrion Beetles (Coleoptera: Silphidae) Maculation usually various dark shades of brown or gray, with various spots or markings; some lighter or colorful. Adults are nocturnal. Larvae are borers in trunks and limbs. Host plants are recorded in a large number of plant families, especially all those with larger tree species. A number of species are economic pests of forest trees. References Arora GS (1976) A taxonomic revision of the Indian species of the family Cossidae (Lepidoptera). Rec Zool Surv India 69:1–160 Barnes W, McDunnough JH (1911) Revision of the Cossidae of North America. Contr Nat Hist Lepidoptera North Am 1:(1)1–35, pl 1–7 Buser R, Huber W, Joos R (2000) Cossidae – Holzbohrer. In: Schmetterlinge und ihre Lebensräume: Arten-Gefährdung Pro-Schutz. Schweiz und angrenzenden Gebiete, 3:97–116, pl 2. Pro Natura-Schweizerische Bund fuer Naturschutz, Basel Schoorl JW Jr (1990) A phylogenetic study on Cossidae (Lepidoptera: Ditrysia) based on external adult morphology. Zoologische Verhandlingen 263:1–295, 1 pl Seitz A (ed) (1912–1937) Familie: Cossidae. In: Die GrossSchmetterlinge der Erde, 2:417–431, pl 52–55 (1912); 2(suppl):241–245 (1933); 287, pl 16 (1934); 6:1264–1287, pl 167, 169, 181–184 (1937); 10:807–824, pl 93, 96–99 (1933); 14:540–551, pl 79–80 (1929). A. Kernen, Stuttgart Carposinidae A family of moths (order Lepidoptera). They commonly are known as fruitworm moths.  Fruitworm Moths  Butterflies and Moths Carrion Beetles (Coleoptera: Silphidae) derek s. sikes University of Alaska Museum, Fairbanks, AK, USA Despite the association of silphids with carrion, which is often repugnant to humans, the biology C of these organisms includes a rich and complex array of fascinating evolutionary and ecological phenomena. Silphids (Fig. 26) have the largest bodies and are the most conspicuous of the staphylinoid beetles. However, the family is not very species rich by beetle standards, containing only 183 extant species. Commonly, they are known as “carrion beetles” due to their frequent association with vertebrate carcasses. They are sometimes referred to as “large carrion beetles” to distinguish them from other beetles associated with carrion, such as those in the family Leiodidae (which are sometimes called “small carrion beetles”). Most species eat carrion although many will also prey on carrion associated insects, such as maggots, or other carrion beetles. Some species are phytophagous, or exclusively predaceous, while at least one species has been found only in dung. The primary food source for the larvae of most species, however, is vertebrate carrion. A radical departure from this ancestral life history pattern is seen in the species Nicrophorus pustulatus which, although capable of breeding on carrion, has recently been discovered to be a parasitoid of snake eggs – perhaps the only known example of a parasite of a vertebrate that kills and consumes its host (in this case, snake embryos). The family contains two subfamilies, each of which specializes on a different size of carrion. Carrion feeding members of the subfamily Silphinae, which lack parental care, prefer large vertebrate carcasses (>300 g), and are often found on megafaunal carcasses, such as elk, moose, or bison. They must share these carcasses with vertebrate scavengers and a large suite of necrophilous insects such as the larvae of blow- and fleshflies, some of which become prey for the beetles. Adults of the subfamily Nicrophorinae, which display parental care and complex subsocial nesting behaviors, generally only breed by monopolization of a small carcasses (<300 g, usually <100 g) such as those of birds or rodents. These beetles remove small carcasses from the competitive arena of flies, ants, and other scavengers by burial into a subterranean nest – hence their common name of 749 750 C Carrion Beetles (Coleoptera: Silphidae) “burying beetles” or “sexton beetles.” This remarkable behavior attracted the attention of early naturalists and remains the focus of research today. Distinguishing Characteristics and Relationships The family as a whole has only one, somewhat ambiguous, synapomorphy (diagnostic character) – a bulge on the posterior quarter of each elytron. However, silphids can be easily recognized by a combination of characters including their necrophilous habits (most species), their size (usually 1–2 cm), their weakly to strongly clubbed antennae, their very large scutellum, which is sometimes as wide as their head, and their tricostate elytra. There is strong evidence indicating silphids are closely related to members of the family Staphylinidae. Some evidence suggests silphids may actually belong inside the family Staphylinidae (which would require changing the family Silphidae into a subfamily of the Staphylinidae). Members of the subfamily Nicrophorinae do possess an unambiguous synapomorphy – a pair of stridulatory files on the dorsal surface of abdominal segment 5 which are used for auditory communication between adults before mating (courtship songs) and between adults and larvae during development, and for defense when disturbed. The files are scraped by the underside of the elytral apices when the beetles pump their abdomens forward and backward. Paired stridulatory files are absent from the Silphinae but adults of the basal genera Ptomaphila (Australia) and Oxelytrum (Neotropics) possess stridulatory morphology – at least one species of Oxelytrum has been observed stridulating. These beetles have spines on the underside of the elytra that can be scraped by the abdominal intersegmental membrane when the beetles move their abdomens from side to side – a phenomenon that has yet to be studied in the silphines. Because silphines do not nest, presumably the only function of their stridulation would be defense. Morphology Adult Length 7–45 mm (usually 12–20 mm); ovate to moderately elongate, and slightly to strongly dorsoventrally flattened (Silphinae). Frontoclypeal (epistomal) suture absent (Silphinae), or present as fine line (Nicrophorinae). Antennae are 11-segmented but appear as 10-segmented in Nicrophorinae due to reduced second segment fused to third segment; ending in 3-segmented club, usually preceded by two or three enlarged but sparsely setose segments (Silphinae and basal Nicrophorinae) or antennomeres 9–11 forming a large club (Nicrophorus). Pronotum with lateral edges complete, sometimes explanate. Scutellum large – often as wide as head. Elytra truncate, exposing 1–5 abdominal tergites in Diamesus, Necrodes, and Nicrophorinae; not truncate in remaining Silphinae, covering abdomen; never striate; in Silphinae bearing 0–3 raised costae or carinae per elytron (present but indistinct in Nicrophorinae); with raised callus near posterior end of outermost costa; epipleura usually welldeveloped and with ridge complete almost to apex. The elytra of most Nicrophorus, Ptomascopus and Diamesus species usually have broad colored bands or spots (fascia and maculae) extending laterally to meet epipleura. Abdomen with sternite 2 not visible between hind coxae but visible laterally of metacoxae; sternites 3–8 visible in females, 3–9 visible in males. Legs with five tarsal segments per tarsus. Males usually with broadly expanded protarsal segments and longer protarsal setae (midtarsal also expanded in male Diamesus), proand midtarsi of female similar. Larvae Length 12–40 mm, campodeiform (most Silphinae) or eruciform (Nicrophorinae); elongate, more or less parallel-sided to ovate, slightly to strongly flattened, relatively straight or slightly curved Carrion Beetles (Coleoptera: Silphidae) ventrally. Body surfaces heavily pigmented and heavily sclerotized (Silphinae), or lightly pigmented and lightly sclerotized (Nicrophorinae). Stemmata 6 (Silphinae) or 1 (Nicrophorinae) on each side. Mandibles lacking mola. Thoracic terga and abdominal terga and sterna consisting of one or more sclerotized plates, without patches or rows of asperities, each tergum with 1 (Silphinae) or 2 (Ptomascopus) lateral tergal processes extending beyond edges of sterna or without such processes (Nicrophorus) but with four spinose projections along posterior margin of abdominal terga. One or two segmented, well developed urogomphi. Classification, Diversity, and Distribution In recent years there have been some changes to the classification and newly described species added, so a current classification, with updated species counts, and distributional information is provided below (Table 7). The family currently stands at 183 species. The distribution of an organism is the result of both ecology and evolutionary history. Silphids, especially the nicrophorines, are rare in warmer climates, such as lowland tropical forests, and virtually absent from dry climates like deserts – these ecological constraints certainly have limited their distribution in places like Africa, Australia, and Tibet. A few silphids in northern Africa survive in cooler, wetter mountainous regions but the Sahara presumably prevents southward dispersal. The family Silphidae is thought to have originated in the northern hemisphere on the paleocontinent of Laurasia. The subfamily Nicrophorinae best represents this with only three species in territory once part of the southern landmass of Gondwana. These three species are thought to have radiated down the Andes of South America, having survived in the cooler, montane climate. The nicrophorines are distributed in the northern hemisphere, with species radiations having occurred in the Malay Archipelago, resulting C in various endemic island species restricted to montane habitats, and into South America along the Andes. None are found in Africa south of the Sahara, in Australia (Fig. 25), or Antarctica. These beetles were once thought to be absent from the Indian subcontinent south of the Himalayas, but there may be a population of the recently described species Nicrophorus sausai in Meghalaya India, a mountainous region isolated from the Himalayas. This unusual, and perhaps relict, population begs additional study and confirmation. The silphines are more widespread than the nicrophorines, with greater representation on Gondwanan areas. This is thought to be related to their greater generic diversity (12 genera) and possible greater age. There are four species in Australia and New Guinea (Ptomaphila, 3 endemic species; Diamesus 1 species) and a larger radiation in South America than is seen in the nicrophorines (Oxelytrum, 8 species). It has been suggested that this radiation of the Silphinae into South America and consequently Australia (via Antarctica) took place 50–60 million years ago producing these, the only two silphid genera endemic to the southern Hemisphere. There are also three silphine species in South Africa (Thanatophilus, 2 species; Silpha, 1 species) and an entire silphine genus (Heterotemna, 3 species) endemic to the Canary Islands off the northwest coast of Africa. However, as with the nicrophorines, most species of the Silphinae are found in the northern hemisphere, although they seem to be somewhat more tolerant of warm habitats than are the nicrophorines. This tolerance is perhaps due to their preference for larger carcasses which they do not (and could not) defend from competitors. Nicrophorus species, probably due to their requirement for small carcasses that can be buried and defended, do not appear to compete well with the ants, flies and carrion-associated scarab beetles that are more abundant in warmer habitats. Together, the Silphidae show an amphitropical or amphipolar distribution, i.e. they are restricted to northern and southern temperate zones but 751 752 C Carrion Beetles (Coleoptera: Silphidae) Carrion Beetles (Coleoptera: Silphidae), Table 7 Carrion beetle classification, species counts, and distribution Order Coleoptera Superfamily Staphylinoidea Family Silphidae Latreille, 1807 Subfamily Silphinae Latreille, 1807 15 genera, 183 species 12 genera, 111 species Aclypea Reitter, 1884 13 species, Holarctic Dendroxena Motschulsky, 1858 2 species, Eurasia Diamesus Hope, 1840 2 species, Asia, Australia Heterosilpha Portevin, 1926 2 species, West Nearctic Heterotemna Wollaston, 1864 3 species, Africa: Canaries Necrodes Leach, 1815 3 species, Holarctic Necrophila Kirby and Spence, 1828 17 species, Holarctic subgenus Necrophila Kirby & Spence, 1828 subgenus Eusilpha SemenovTian-Shanskij, 1890 subgenus Calosilpha Portevin, 1920 subgenus Deutosilpha Portevin, 1920 subgenus Chrysosilpha Portevin, 1921 Oiceoptoma Leach, 1815 9 species, Holarctic Oxelytrum Gistel, 1848 8 species, SW Nearctic/Neotropical Ptomaphila Kirby & Spence, 1828 3 species, Australia, New Guinea Silpha Linnaeus, 1758 25 species, Eurasia, Africaa subgenus Silpha Linnaeus, 1758 subgenus Phosphuga Leach, 1817 subgenus Ablattaria Reitter, 1884 Thanatophilus Leach, 1815 Subfamily Nicrophorinae Kirby, 1837 a 24 species, Holarctic & Africa, Madagascar 3 genera, 72 species Eonecrophorus Kurosawa, 1985 1 species, Nepal Ptomascopus Kraatz, 1876 3 species, Asia Nicrophorus Fabricius, 1775 68 species, Holarctic, N Africa, S America, SE Asia One species of Europe, Silpha trisits Illiger, has been introduced and established in North America (southern Quebec) Carrion Beetles (Coleoptera: Silphidae) C Carrion Beetles (Coleoptera: Silphidae), Figure 25 Map of the subfamily Nicrophorinae (Silphidae). 6,736 localities from 17,250 specimens examined showing the known distribution (99% of records are Nicrophorus). The lack of records throughout much of Russia is almost certainly a collection artifact whereas the absence of records in Australia, sub-Saharan Africa, most of India and South America is not. A corresponding map for the subfamily Silphinae has not yet been prepared – see text for description of the distribution of the Silphinae. generally absent from the intervening tropics (with the exception of tropical montane habitats). The lesser generic diversity of the nicrophorines (3 genera) compared to the silphines, combined with their almost pure Laurasian distribution, supports preliminary estimates for a younger age of the main radiation in the Nicrophorinae (the genus Nicrophorus) based on fossil and molecular divergence dating methods. All known fossils of the genus Nicrophorus are Eocene or younger, less than 50 million years old, with the majority being known from the Pleistocene. Molecular dating methods provide a preliminary, and wide, range for the radiation of the genus having happened 50–24 million years ago. The transition to the Oligocene from the Eocene is thought to represent the most dramatic climatic change of the Cenozoic era, in which the Mesozoic “hot house” world was transformed into the Neogene “ice house” world that persists today. Given the absence of Nicrophorus from lowland tropical habitats and the preference of these organisms for cooler climates, it seems reasonable to infer these beetles may have radiated during this cooling event of the Oligocene. Roughly concurrent with this cooling event, many modern rodent families appeared and radiated – and these would have been ideal prey items for Nicrophorus beetles. In addition to a small-mammal radiation during this time, most modern bird orders and families appeared between the early Eocene and the late Oligocene-early Miocene, during a period of intense diversification. Small birds are also ideal prey items for Nicrophorus. The family is thought to have originated in the Old World, and the subfamily Nicrophorinae certainly shows this pattern in which all but one of the five genera/subgenera are endemic to Asia. The New World has the minority of world species for all groups that are also found in the Old World, and has only two endemic genera: Oxelytrum and Heterosilpha. One new species of Nicrophorus, 753 754 C Carrion Beetles (Coleoptera: Silphidae) Carrion Beetles (Coleoptera: Silphidae), Figure 26 Nicrophorus olidus Matthews, a silphid found in Honduras and Mexico; female, dorsal and lateral view. N. hispaniola, was recently discovered and described in the Dominican Republic. This was the first Nicrophorus described in the New World since 1925, bringing the total to 21 New World species of Nicrophorus. There are 25 species of Silphinae in the New World, combined with the 21 species of nicrophorines yielding 46 species of silphids in the New World. Ecology Silphids are most frequently encountered at vertebrate carrion but are sometimes found associated with dung or fungi, or at electric lights. Most species will prey on fly larvae or other insects present on carcasses or dung, in addition to eating the carcass itself. Some species are phytophagous (11 species of Aclypea) while others are predacious (Dendroxena, some Silpha and possibly Ptomascopus zhangla, a poorly known and recently discovered species from China). The silphine Necrodes surinamensis as an adult feeds primarily on fly larvae but can survive on carrion alone. The majority of silphids that have been studied are nocturnal or crepuscular (active at sundown and sunrise), which might help avoid predation by birds. Some species of the genus Nicrophorus have become model organisms for research in ecology, physiology, and behavior – particularly dealing with questions about parental care, the evolution of sociality, competition, and other behaviors of nesting organisms (e.g., brood parasitism). There have been over 150 behavioral ecology studies on these species in the past 25 years. Subjects of these studies include, for example, the ability of adults to regulate their brood size to match the size of the carrion resource via control of the number of eggs produced and subsequent parental culling of “extra” larvae by cannibalism. Other subjects investigated include adult competition and fights to win a carcass, pheromone emission, adult stridulatory communication (between parents and larvae, precopulatory, and defensive), duration and explanation for paternal care, and antimicrobial properties of anal and oral secretions, among many others. Biparental care, as seen in Nicrophorus, is rare in insects in general, and has been the focus of much investigation. The typical progression from discovery to new offspring for Nicrophorus species proceeds as follows: A small vertebrate carcass, like that of a mouse, is found soon after nightfall and often on the day of its death. If numerous Nicrophorus beetles find the carcass the beetles begin to fight to dominate the resource. Larger bodied beetles tend to win these competitions with losers retreating, sometimes with minor injuries (missing leg parts or cuts in their wing covers). The loser females sometimes lay eggs near the carcass and some of her offspring might enter and develop in the nest of the winning beetles. The beetles’ fights usually Carrion Beetles (Coleoptera: Silphidae) result in a single species remaining, with smaller bodied species having been excluded. Within the larger species the males fight the males and the females fight the females until the largest male and largest female remain in control of the carcass. Courtship stridulation occurs and can lead to rejection of the male by the female if he cannot stridulate as expected. This may help beetles identify conspecifics but no one has carefully investigated how this is accomplished. The mechanisms by which closely related species avoid hybridization are equally unstudied. The male and female pair work together to bury the carcass by digging beneath it. If the substrate is too tough the pair might move the carcass to more suitable ground by laying beneath it and moving it with their legs. If a male finds a carcass and no females are present he will emit a pheromone to attract a female. Sometimes males without carcasses will emit pheromone to attract females with whom they try to mate. Females, like all insects, can store sperm for later use and sometimes can find and bury carcasses alone, using sperm from prior mating to fertilize her eggs. It can take 5–24 h for a carcass to be secured below-ground (with smaller-bodied species tending to bury less deeply than larger bodied species). The carcass is rolled into a ball that minimizes its surface area. Fur or feathers are removed and a brood chamber is built that will house the carcass and the developing larvae. The carcass is treated with oral and anal secretions that help preserve the resource from microbial decay. The female will then lay eggs based on the mass of carcass (between 10 and 50 eggs is typical) although more eggs are typically laid than larvae that will be reared. Because body size is critical to winning contests for carcasses, larger bodied offspring will be more likely to successfully reproduce than smaller bodied offspring. A carcass resource can yield either many small burying beetle offspring, or fewer large burying beetle offspring. This selection pressure has resulted in a behavior known as filial cannibalism – the parents kill and consume “extra” larvae that would otherwise lower the average body size C of the resulting offspring. These beetles, therefore, regulate the size of their brood carefully – both by laying a clutch size appropriate to the mass of the carrion resource, and by later “fine-tuning” the clutch size if too many eggs hatch by eating the late arriving larvae. Parent beetles stay with the larvae during their approximate 2-week development period – defending them against possible usurpers (this being the major advantage of paternal care). The parents also tend the larvae, maintain the brood ball and regurgitate food for the larvae. The burying beetles are unusual among insects in having peak levels of juvenile hormone (normally considered a gonadotropic hormone in adult insects) during the early parental period when the ovaries are small. Parental regurgitations to young larvae increase larval growth rates, and in some species, are essential for molting from the first to second instar. The larvae molt between each of three instars and either pupate to adult and overwinter as adults or overwinter as a final larval instar “pre-pupa.” This life history of Nicrophorus species is based on finding, concealing and monopolizing small carcasses before their competitors. However, they cannot exclude all interested parties – in addition to a vigilance that prevents usurpation by other Nicrophorus adults, the parents must contend with both bacterial and fungal decay of the carcass. Recent studies in both North America and Japan have shown that the treatment of the carcass with oral and anal secretions by Nicrophorus adults greatly reduces the microbial decay, and a number of antimicrobial agents have been identified. Other animals that often accompany the beetles into their nest include both nematodes and mites (Acari). The nematode-beetle relationship is poorly known with considerable potential for future work. At least two nematode species, Rhabditis stammeri, and R. vespillonis, have been documented as associates of Nicrophorus vespilloides and N. vespillo, respectively, although it is certain that many more, probably undescribed, nematode species associate with silphids. The nematodes 755 756 C Carrion Beetles (Coleoptera: Silphidae) breed on the carrion and their offspring disperse to new carrion resources with the new generation of beetles – traveling in the gut of the beetle larvae and using the adult hindgut and/or genitalia for transport to a new carcass. Nematodes have been observed in laboratory settings to reach enormous population sizes – causing the beetles to abandon the carcass – but it is unknown if this happens in the wild. The new generation of nematodes will form large aggregations on the surface of the carcass, each will arch upwards and start to wave. They will also form small, living, waving towers by climbing on one another. This behavior brings the nematodes in contact with the beetles, onto which they climb. It is not known how or if the beetles have adapted to competitive pressure from these nematodes, nor is it known to what degree the nematodes reduce the beetles’ fitness. The mite-beetle relationship is better understood than that of the nematodes, but remains one of the more complex and rich areas for future research. It is not known how many species of silphids carry mites (phoretic associates) but most of the Nicrophorus species that have been studied ecologically carry them. Like the nematodes, the mites’ life cycle is tied to that of the beetles with the deuteronymphs (the last pre-adult stage) dispersing phoretically on the adult beetles. Mites present on silphine species probably are using them as alternate hosts opportunistically until they can transfer to a burying beetle. Many of the mites appear to be host-specific, and considerable taxonomic work remains to done with them. Over 14 species of mites from four families (Parasitidae, Macrochelidae, Uropodidae, and Histiomatidae) were found on Nicrophorus species in Michigan, USA. The most frequently encountered and wellstudied mites in this system are those in the genus Poecilochirus (Mesostigmata: Parasitidae). Initial work in the 1960s indicated an apparent mutualistic mite-beetle relationship resulting from the mites’ predation on fly eggs that would otherwise hatch and compete with beetle offspring. However, more thorough examination of this relationship has found much greater complexity – including examples of mutualism, commensalism, and parasitism, varying with species and conditions. What was once thought to be a single species of mite, Poecilochirus carabi, has since been discovered to be a species complex of several morphologically similar, but reproductively isolated species that are specific to their host beetle species. Only a few of these cryptic mite species have been described or examined in detail. It is likely that most of the 69 known Nicrophorus species have their own (probably undescribed) Poecilochirus species. An even more poorly-known symbiotic relationship involving the Silphidae awaits study: nematodes of the family Allantonematidae have been reported as parasites of the burying beetles’ Poecilochirus mites! Conservation In the USA, much attention has been focused recently on the American burying beetle, Nicrophorus americanus Olivier, a federally listed endangered species and one of five “giant” species in the genus. As recently as the 1930s, this species was considered to be common over most of the eastern half of the North American continent. However, it now occurs in <10% of its former range (populations are now restricted to a few islands offshore of Rhode Island and Massachusetts and the western periphery of the historic range). This species was first listed in 1989 and represents an unusual case of species endangerment in that there are no apparent causal factors for its decline that simultaneously explain why the eight other co-occurring Nicrophorus species have not declined. Many weakly supported hypotheses have been suggested, including DDT contamination, extinction of the passenger pigeon, deforestation, artificial lighting, loss of carrion availability, and an unknown, intrinsic, genetic effect. One important difference between N. americanus and its congeners is that this species requires larger carcasses (>80 g) than its congeners to maximize its reproductive success. Subsequent work and review of the literature points to a “best,” Carrion Beetles (Coleoptera: Silphidae) albeit provisional, explanation of this species’ decline based on (i) known population declines of optimally sized carrion “prey” species such as ground nesting birds and the passenger pigeon, and (ii) increased vertebrate scavenger and congener competition for the reduced carrion available. The greater pressure from vertebrate scavengers may have resulted from competitive release after the loss of larger predators (such as the gray wolf [Canis lupus] and the mountain lion [Felis concolor]) and an increase in habitat fragmentation and edge habitats. Nicrophorus americanus may have declined because it is experiencing greater vertebrate and congener competition for a reduced resource base. The species is being bred in captivity and work is underway to establish new populations. The attention it has received due to its federal protection has helped its prospects considerably. Given the well-documented and recent rise in mean global temperature, some conservationists are worried about montane island endemics that cannot survive in the warmer lowlands. As our climate changes, the size of these cooler, montane habitats will contract as they gradually move higher in elevation. There are at least ten Nicrophorus species endemic to the higher elevations of various islands in the Malay Archipelago. These species, among many other similarly adapted organisms, could become threatened with extinction if their cooler, montane habitats start to disappear. Some are already living at the highest elevations available to them. C mammals – and possibly caused by the key innovation of small carcass monopolization. From other recent research we have learned that females with a carcass will not attack males who have recently been in contact with a carcass and typically cared for a brood. These males are considered to have a “breeder’s badge”, a profile of cuticular hydrocarbons that identifies them as parental – and those males lacking this scent are attacked. This addresses questions of how these social beetles recognize each other. It had already been determined that adults cannot recognize their own larvae from those of other couples, nor even, of other species of nicrophorines (in Japan, Ptomascopus larvae are sometimes brood parasites, mixed into broods of Nicrophorus concolor larvae and raised by Nicrophorus parents). The mechanism by which parents can minimize such brood parasitism is temporal – they kill larvae that arrive too early or too late around the window of time that their own larvae appear. Our understanding of the biology and evolution of the Silphidae progresses, with continuing work on the phylogenetics, reproductive behaviors of basal lineages, brood parasitism, communal breeding, endocrinology, use of stable isotopes to determine larval diet, and host shifts, although many questions remain uninvestigated.  Decomposer Insects  Beetles (Coleoptera) References Recent Research Recent work on these beetles has resulted in some interesting discoveries. In addition to 11 newly described species since 1999, primarily from Asia, there has been phylogenetic work underway which has suggested that the relatively high species richness of the genus Nicrophorus may have resulted from a rapid radiation – a burst of evolution. This radiation was possibly coincident with the global cooling during the Oligocene and the subsequent radiation of small birds and Ratcliffe BC (1996) The carrion beetles (Coleoptera: Silphidae) of Nebraska. Bull Univ Nebraska State Mus 13:1–100 Peck SB (2001) Silphidae Latreille, 1807. In: Arnett RH, Thomas MC (eds) American beetles: archostemata, myxophaga, adephaga, polyphaga: staphyliniformia, vol 1. CRC Press, Boca Raton, FL, pp 268–271 Scott MP (1998) The ecology and behavior of burying beetles. Ann Rev Entomol 43:595–618 Sikes DS (2005) Silphidae. In: Kristensen NP, Beutel RG (eds) Handbook of zoology, vol IV Arthropoda: Insecta part 38, Coleoptera, Beetles, vol I: Morphology and systematics (Archostemmata, Adephaga, Myxophaga, Polyphaga partim) (RG Beutel RAB Leschen, eds) Walter de Gruyter, Berlin, NY, pp 288–296 757 758 C Carsidaridae Sikes DS, Newton AF, Madge RB (2002) A catalog of the Nicrophorinae (Coleoptera: Silphidae) of the world. Zootaxa 65:1–304 Carsidaridae A family of bugs (order Hemiptera, superfamily Psylloidea).  Bugs Carter, Herbert James References Carter HJ (1933) Gulliver in the bush – wanderings of an Australian entomologist. Angus & Robertson, Sydney, Australia, 234 pp Zimmerman EC (1993) Australian weevils, vol 3. CSIRO, East Melbourne, pp 493–494 Carthaeidae A family of moths (order Lepidoptera) also known as Australian silkworm moths.  Australian Silkworm Moths  Butterflies and Moths GeorGe hanGay Narrabeen, NSW, Australia Carton Herbert James Carter was born on the 23rd of April 1858 in Marlborough, Wiltshire, England. He was educated in England, receiving his Bachelor of Art Degree in Cambridge. At the age of 24 he migrated to Australia and took up the position of Mathematical Master at Sydney Grammar School. Later on, in 1902, he was appointed as Principal of Ascham Girls’ School in Sydney where he worked until his retirement in 1914. Although he was a devoted educator, his interest in entomology and his contribution to knowledge of the Australian insect fauna were very significant. He became interested in entomology soon after his arrival in Australia and produced his first paper on Australian Coleoptera in 1905. He traveled and collected extensively in New South Wales, Victoria, Tasmania, South Australia and Western Australia. He collaborated with A.M. Lea and a number of other entomologists of his era, including with K.G. Blair, the Coleopterist of the British Museum. During his long life he published 65 papers, including major works on Tenebrionidae, Buprestidae and Colydiidae. He described 55 genera and 1,234 species new to science. After retirement he continued his entomological work until his sudden death on the 16th of April 1940, in the Sydney suburb of Wahroonga. The paper manufactured by Hymenoptera for nest construction. Carrier An inert material serving to dilute a pesticide, and to carry it to its target. Carrying Capacity The theoretical maximum population size that an area can support indefinitely within defined set of conditions. Casebearer Moths (Lepidoptera: Coleophoridae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Casebearer moths, family Coleophoridae, comprise over 1,525 species worldwide, with most being Palearctic (1,082 sp.) and in the genus, Casey, Thomas Lincoln Casebearer Moths (Lepidoptera: Coleophoridae), Figure 27 Example of casebearer moths (Coleophoridae), Coleophora sp. from Florida, USA. Coleophora. Most are in subfamily Coleophorinae, while non-casebearers are in Batrachedrinae. The family is part of the superfamily Gelechioidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (5–24 mm wingspan), with head smooth-scaled; haustellum scaled; labial palpi recurved; maxillary palpi minute, 2-segmented. Wings usually very elongated and hindwings spindle-shaped with long fringes. Maculation shades of brown or gray, sometimes mostly white, and unicolorous or with various markings or stripes, but rarely more colorful and with iridescence. Adults may be mostly crepuscular but many are diurnal. Larvae make small cases (except for Batrachedrinae), often distinctly shaped for each species (Fig. 27), skeletonizing host leaves, but some are seed borers, leafminers, or stalk borers, or skeletonize leaves beneath frass webs. A few Batrachedrinae are predaceous on scale insects (Hemiptera). Various host plants are utilized. A few species are economic. Ovovivipary has been recorded for a few species. References Baldizzone G (1996) A taxonomic review of the Coleophoridae (Lepidoptera) of Australia. Tijdschrift voor Entomologie 139:97–144 C Hodges RW (1966) Review of the New World species of Batrachedra with descriptions of three new genera (Lepidoptera: Gelechioidea). Trans Am Entomol Soc 92:585–651 Landry J-F, Wright B (1993) Systematics of the nearctic species of metallic-green Coleophora (Lepidoptera: Coleophoridae). Can Entomol 125:549–618 Toll S (1962) Materialien zur kenntnis der paläarktischen arten der familie Coleophoridae (Lepidoptera). Acta Zool Cracoviensia 7:577–720, 133 pl Vives-Moreno A (1988) Catalogo mundial sistematico y de distribucion de la familia Coleophoridae Hübner, [1825] (Insecta: Lepidoptera). Boletin de Sanidad Vegetal 12:1–196 Casey, Thomas Lincoln Thomas Casey was born at West Point, New York state, on February 19, 1857. His father was a general of the U.S. army, and he graduated from the U.S. Military Academy in 1879. As a soldier, he traveled widely in the USA, and used every opportunity to collect beetles as well as building his collection by purchase from others. He also was interested in applied astronomy. He was a prolific describer of insect species, publishing 77 papers between 1884 and 1924, and in them describing more than 9,000 species. However, he has been widely criticized not only because his descriptions were brief and lacked illustrations, but because he often selected superficial differences between specimens as the basis of species separation. In other words, he failed to recognize that morphological characters may vary considerably within species. Consequently, many of the species names that he proposed have subsequently been sunk as synonyms. His collection of almost 117,000 specimens including 9,200 holotypes was bequeathed to the U.S. National Museum of Natural History. He died on February 3, 1925. Reference Herman LH (2001) Casey, Thomas Lincoln. Bull Am Mus Nat Hist 265:53–54 759 760 C Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) peter neuensChwander International Institute of Tropical Agriculture, Cotonou, Bénin, West Africa This is one of many insects that came to the attention of science only after it had been inadvertently transported and established on a new continent. In the early 1970s, mealybug infestations suddenly devastated cassava (in French: “manioc”) in the Congo and what is today the Democratic Republic of Congo, around the two capitals Brazzaville and Kinshasa, respectively. From there, this new plague spread rapidly, at a speed of over 100 km per year. It got new footholds in Nigeria, near the border to Benin, then on the border between Gambia and Senegal, and within a few years had covered the entire cassava growing area of Africa from Senegal to Ethiopia and to South Africa. By the mid-1990s, only the Indian Ocean Islands including Madagascar were still free of this pest, and they have remained so up to today (2001). Wherever this mealybug, which was newly described as Phenacoccus manihoti Matile-Ferrero, and belonging to the family Pseudoccocidae, turned up it became the most important cassava pest, threatening the supply of the main staple food for about 200 million Africans. Morphology and Biology This is a typical mealybug; pinkish, covered with white waxy dust, oval in shape (3–4 mm length) with no wings, weak legs, and long sucking mouth parts on the ventral side (Fig. 28). Yellowish eggs are laid in daily batches protected by wax filaments, mostly underneath the tip of the abdomen of the female. The tiny first instar larvae disperse all over the plants and can be transported by wind. The three nymphal instars resemble each other and the adult, except for the size increase. This species is parthenogenetic, which means that it reproduces without males. The life cycle is completed within 1 month and the mealybug reproduces throughout the year, without any resting stages. It attacks cassava, Manihot esculenta Crantz (Euphorbiaceae), the related Ceara rubber Manihot glaziovii Mull. Arg., as well as the interspecific hybrid of these two plants, which are of South American origin. At extreme outbreak levels the infestation spills over to many other plants of different species which happen to grow in the vicinity of infested cassava, but when infestations are low no other plant species are attacked. Damage Mealybugs suck preferentially in the growing tip and on the underside of leaves. During heavy attacks the undersides of leaves are covered with a white mass. Mealybugs eject surplus sugar water, which accumulates on the leaves below as a sticky cover of honeydew, which is subsequently attacked by fungi. The resulting black “sooty-mold” cover reduces photosynthesis, and sucking of the insect in the growing tips leads to stunting. In areas where cassava leaves are eaten as a vegetable, such use is made impossible by heavy mealybug infestation. Accumulation of carbohydrates in the storage tubers, which in cassava is a continuous process, is reduced, and quality is impaired. Tuber yield losses of up to 80% have been recorded. In addition, because of the stunting, planting sticks are of poor quality, which compromises the following year’s crop. Thus, cassava cultivation has disappeared from vast areas during the height of the cassava mealybug epidemic. Control Options Wherever this mealybug appeared for the first time, extension services tried to combat it with pesticides. As the mealybug is often hidden in the Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) C Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae), Figure 28 The cassava mealybug, Phenacoccus manihoti, on a cassava leaf (upper left); the exotic parasitoids Apoanagyrus lopezi (upper right) and A. diversicornis (middle left); one of the widespread and common indigenous coccinellids, Hyperaspis pumila (middle right); and cassava field devastated by cassava mealybug (lower) (from Neuenschwander (2005) In: Evaluating indirect ecological effects of biological control. CABI, Wallingford, UK). buds, insecticides are generally inefficient, all the more because they also preferentially kill the natural enemies. In fact, it was demonstrated that repeated insecticide applications led to an explosion of the mealybug population. Similarly, cassava varieties were tested in a quest to find and/or develop resistant varieties. As stand-alone component, resistant/tolerant varieties did, however, not give satisfactory results. 761 762 C Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) The Solution: Biological Control Cassava was brought to Africa from South America by Portuguese traders in the sixteenth century, though it acquired today’s importance only in the early twentieth century. It was therefore surmised that this new mealybug came from South America and that classical biological control, i.e., the transfer of natural enemies that keep this insect under control in its original home, could bring the solution. “Foreign exploration”, i.e., the search for natural enemies, in Latin America was undertaken by several international research organizations, including CAB International and the International Institute of Tropical Agriculture (IITA), but the cassava mealybug remained elusive. In the course of this exploration, another mealybug was discovered, Phenacoccus herreni Cox and Williams, but when its parasitoids were tested they did not attack the P. manihoti known from Africa. In 1981, a researcher from the Centro Internacional de Agricultura Tropical (CIAT) finally found P. manihoti in Paraguay. Under the leadership of IITA, “foreign exploration” was then concentrated and P. manihoti was found on cassava in a few sites in the Rio de la Plata valley in Paraguay, Brazil and Bolivia. The first natural enemy of P. manihoti to be discovered, the parasitic wasp Apoanagyrus (Epidinocarsis) lopezi de Santis (Hymenoptera, Encyrtidae), eventually also proved to be the best biological control agent. Mated females lay their eggs into mealybugs (second to fourth instars), where a larva develops freely floating in the coelom of the mealybug. Sometimes the host tries to mount a defense action by encapsulating the parasitic larva, but this is successful only in about 10% of cases (which might include larvae that died for other reasons). The larva pupates in the sausage-shaped dry remains of the mealybug, called a “mummy”, from where the adults emerge, after a total life cycle of about 2 weeks. Because the female determines the sex of its offspring by adding or withholding sperm during oviposition into the host, she can exploit the host to its best. Second instar hosts yield only male parasitoids, which though small are fully functional; fourth instars yield mostly females, which because of their large size can produce more eggs than small females. Several other natural enemies, among them the wasp A. diversicornis Howard and several predatory lady beetles, mainly Hyperaspis notata Mulsant and Diomus hennesseyi Fürsch (Coleoptera: Coccinellidae), were collected mostly in Paraguay and Brazil in the course of several years and shipped to CABI in the United Kingdom for quarantine. There, the insects were reared and checked to be: (i) free of diseases, (ii) not harmful to plants, (iii) not hyperparasitic, i.e., harmful to indigenous parasitoids, and (iv) not harmful to useful insects like bees and silkworms. They were then sent to IITA in Nigeria, with the necessary Nigerian import permits and under the umbrella approval of the Inter-African Phytosanitary Council of the Organization for African Unity. Further studies, mass rearing with specially developed equipment, and releases followed. In the early 1980s, on the strength of encouraging results in Nigeria, these exotic insects were sent to all African countries requesting them. Releases were executed mostly from the ground and, in a few instances, by aircraft using a specially developed apparatus. Thus, a total of about 150 releases was made by IITA, always in close collaboration with the quarantine authorities and scientists of the various African countries. By the mid-1990s, A. lopezi was established everywhere in Africa where P. manihoti occurred. It sometimes had dispersed long distances from the release sites (170 km within ten generations of A. lopezi was documented). The other parasitoid failed to establish (i.e., it could not be recovered after 1 year) and the two coccinellids (Fig. 28) established only locally in the Democratic Republic of Congo, Malawi, and perhaps some East African countries, where they had to compete with numerous common indigenous lady beetle species. A. lopezi became the target of extensive impact studies, using paired sleeve cages, chemical Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) exclusion experiments, simulation modelling on the basis of laboratory studies, and direct monitoring through field surveys in many countries. As a result, this is one of the best-researched examples of classical biological control of an exotic arthropod pest. Wherever A. lopezi had been present for about 2 years (3–4 years in the East African highlands), mealybug populations dropped tenfold to noneconomic levels, thus validating the model predictions. In local spots with exceedingly poor soils, such as pure sand without any mulch, mealybug populations, though lower than before, remained high enough to cause damage despite the presence of A. lopezi. For such conditions, any further release of A. lopezi is useless, but strengthening the plants by applying mulch successfully tipped the balance and reduced mealybug infestation considerably. The key features that made A. lopezi such a successful biological control agent (particularly in comparison to A. diversicornis) were: (i) an exceptional host finding capacity, higher than any of its exotic or local competitors; (ii) acceptance of a wide range of host stages; (iii) extensive host feeding, whereby the female wounds its host and sucks its hemolymph, thereby killing small hosts outright; (iv) fast development (almost two generations for one by its host; he same as for A. diversicornis). These advantages clearly outweighed the perceived low reproductive rate, low (but density dependent) parasitism rate, and the fact that A. lopezi was attacked by local hyperparasitoids. In fact, 16 species of wasps were found to have switched over to A. lopezi. They came from parasitoids, mostly Anagyrus spp. (Hymenoptera, Encyrtidae), that attack Phenacoccus madeirensis Green, a common mealybug on cassava. Except for an odd case, these Anagyrus spp. could not reproduce on P. manihoti. Though at the time of the release in the early 1980s no indigenous mealybug species had been tested and the whole concept of non-target effects was not yet prominent, food-web studies after the establishment showed that A. lopezi developed on P. manihoti only. Environmental effects of this biocontrol project were thus limited to the impact on a ecosystem that had been temporarily C disturbed by the invasion of P. manihoti, which offered numerous indigenous predators a new and ample food. With the collapse of this food source, the abundance of these general predators, as well as of hyperparasitoids, declined drastically, presumably back to pre-invasion levels. The population equilibrium of P. manihoti has remained low for the last 20 years, with an occasional short-term low peak in abundance. Ten to 15 years after the establishment of A. lopezi, extension services and governmental research organizations in most previously affected countries reclassified P. manihoti as an insect of minor importance. The stability of the system is only disturbed where insecticide interventions on neighboring crops like cotton, or against grasshoppers, disturb the balance by killing the wasps. This leads to an upsurge in P. manihoti populations, a situation well known to practitioners of integrated pest management. In field experiments, yields under conditions of biological control of P. manihoti were compared with those where mealybug infestations had been artificially boosted. In surveys, various factors affecting yield were quantified and their contribution to yield attributed. On the basis of these results, the savings due to biological control of P. manihoti were extrapolated to all affected countries and compared with the investment into this project. According to different scenarios of how farmers can cope with loss of cassava, returns for each dollar invested were between $200 and $740. For this evidently successful project, its former leader was honored with the World Food Prize.  Area-Wide Pest Management References Gutierrez AP, Neuenschwander P, Schulthess F, Herren HR, Baumgaertner JU, Wermelinger B, Loehr B, Ellis CK (1988) Analysis of biological control of cassava pests in Africa. II. Cassava mealybug Phenacoccus manihoti. J Appl Ecol 25:921–940 Hammond WNO, Neuenschwander P (1990) Sustained biological control of the cassava mealybug Phenacoccus manihoti (Hom.: Pseudococcidae) by Epidinocarsis lopezi (Hym.: Encyrtidae). Entomophaga 35:515–526 763 764 C Cassava Pests and their Management Herren HR, Neuenschwander P (1991) Biological control of cassava pests in Africa. Ann Rev Entomol 36:257–283 Neuenschwander P (1996) Evaluating the efficacy of biological control of three exotic homopteran pests in tropical Africa. Entomophaga 41:405–424 Neuenschwander P (2001) Biological control of cassava mealybug in Africa: a review. Biol Control 21:214–229 Neuenschwander P, Markham R (2001) Biological control in Africa and its possible effects on biodiversity. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control, CABI Publishing, Wallingford, UK, pp 127–146 Zeddies J, Schaab RP, Neuenschwander P, Herren HR (2001) Economics of biological control of cassava mealybug in Africa. Agric Econ 24:209–219 Cassava Pests and their Management anthony C. BeLLotti CIAT (International Center for Tropical Agriculture), Cali, Colombia The origin of cassava (Euphorbiaceae: Manihot esculenta Crantz) is the Neotropical Americas, where it is estimated that domestication occurred some 7,000–9,000 years ago. At present this perennial shrub is grown throughout the tropical regions of the world. The highest production is in Africa (ca. 55%); while Asia and Latin America account for 27 and 18%, respectively. In the case of yields on an average per-hectare basis, they are highest in Asia (14.1 t/ha) and the Americas (12.7 t/ha) and lowest in Africa (8.5 t/ha). Cassava is cultivated mainly for its starchy roots and is ranked as the sixth most important caloric source in the human diet and the fourth most important staple in the tropics. Cassava leaves may also be consumed and may be an important source of protein in some African countries and Northeast Brazil. Cassava is vegetatively propagated, has a long growth cycle (8–24 months), is drought tolerant, and is often intercropped with staggered planting dates so it is almost always present in farmers’ fields. Most cassava is grown by small-scale farmers in traditional farming systems, often on marginal or fragile soils under rain-fed conditions, using few purchased inputs such as fertilizers and pesticides. As yields are low in these systems, pest control is of low priority due to the high costs and the long crop cycle, which may require various applications. The dynamics of cassava production are changing, however, as trends in the food, feed and industrial sectors are leading to an increased demand for high-quality cassava starches. In Latin America, there are indications of a shift toward larger scale production units where cassava is grown as a plantation crop, and it is advantageous for farmers to employ a multiple planting and harvesting production system in order to meet the constant market demands of the processing industries. In this type of production system, the cassava crop will be found at several different growth stages in the same or surrounding fields. Evidence now indicates that pest problems will be compounded in these overlapping production systems. Populations of certain pests such as whiteflies, hornworms and mealybugs tend to increase when a constant food supply (e.g., young cassava foliage) is available. Given this trend, with the concomitant increase in pest populations and damage, there will be a greater tendency to apply pesticides to control pest outbreaks. The Consultative Group for International Agricultural Research (CGIAR) has two research centers – the International Center for Tropical Agriculture (CIAT, Cali, Colombia) and the International Institute of Tropical Agriculture (IITA, Ibadan, Nigeria) – with global and regional (Africa) mandates, respectively, for cassava, oriented toward resource-poor farmers. Today, there is a need to invest in cassava research in order to understand fully the role of pests and diseases in these multiple production systems, where different stages of the crop overlap, providing a constant source of nourishment. Following is an overview of the cassava arthropod complex, and the corresponding damage to the crop, aspects of biology, behavior, and management of the most important pests are explored for the following categories: foliage feeders, Cassava Pests and their Management stemborers/stem feeders, soil-borne pests and secondary pests. This is followed by a look at future trends. The Cassava Arthropod Pest Complex and Crop Damage Not surprisingly since cassava originated in the Neotropics, the greatest diversity of arthropods reported attacking the crop is from these regions (Table 8). More than 200 species have been reported, many of which are specific to cassava and have adapted in varying degrees to the array of natural biochemical defenses in the host, which include laticifers and cyanogenic compounds. The pest complex varies greatly among the major cassava-growing areas in the Americas, Africa and Asia. The crop, whose origin is in South America, was introduced into Africa in the 1500s and into Asia in the seventeenth century. In Asia, none of the major Neotropical pests has become established, and native arthropods that have adapted to cassava have not been reported as causing serious economic damage. In Africa, the whitefly Bemisia tabaci is presently considered to be the major pest of cassava because it is the vector of cassava mosaic disease (CMD). Moreover, recent reports indicate that B. tabaci is also causing root yield reductions due to direct feeding on the crop. There is also the possibility of the accidental introduction of pests via planting material, which can wreak havoc. The cassava green mite (Mononychellus tanajoa) and the cassava mealybug (Phenacoccus manihoti), which were introduced from South America, have caused considerable crop losses and have been the target of massive biological control efforts. Studies indicate that several arthropod species can cause considerable yield loss and that the pest complex is not geographically uniform. Two cassava mealybug species offer an example of the geographic influence on crop damage. Phenacoccus herreni, which has caused considerable damage in northeast Brazil, was probably introduced from northern South America (Venezuela or Colombia), C where mealybug populations are controlled by natural enemies not found in Brazil. Phenacoccus manihoti, which has caused severe crop damage in Africa, had, until recently, been reported only from Paraguay, the Mato Grosso area of Brazil, and the Santa Cruz area of Bolivia. In 2005, this species was collected from the states of Bahia and Pernambuco in northeastern Brazil. The spread of P. manihoti into the drier, hotter regions of Brazil is probably associated with the movement of cassava planting material (i.e., stem cuttings) from southern Brazil into the northeast. The cassava pest complex can be divided into two groups: those that have probably co-evolved with cassava, which is their primary or only host; and generalist feeders that may attack the cassava crop sporadically or opportunistically and are often limited in geographic distribution. The first group includes the Mononychellus mite complex, mealybugs, the hornworm Erinnyis ello, lacebugs, whiteflies, stemborers, fruit flies, shoot flies, scales, thrips and gall midges. The generalist feeders consist mainly of a complex of white grub species, termites, cutworms, grasshoppers, leaf-cutting ants, burrower bugs, crickets, Tetranychus mite species and other stemborers. The most serious pests of cassava – those causing economic damage or yield losses – are generally those that have co-evolved with the crop, including mites, hornworms, whiteflies, mealybugs, lacebugs and stemborers. Generalist feeders reported causing yield losses, often on a localized basis, include burrower bugs, white grubs, leafcutting ants and grasshoppers. Most cassava arthropod pests cause indirect plant damage because they are foliage or stem feeders, reducing leaf area, leaf life or photosynthetic rate. Those pests that can attack the crop over a prolonged period, especially during seasonally dry periods (3–6 months) can cause severe yield losses as a result of decreased photosynthesis, premature leaf drop and death of the apical meristem. Potential yield reduction by these pests can be greater than that by cyclical pests such as hornworms, leaf-cutter ants and grasshoppers, 765 766 C Cassava Pests and their Management Cassava Pests and their Management, Table 8 Global distribution of important arthropod pests of cassava Arthropod pest Major species Americas Mites Mononychellus caribbeanae x Mononychellus tanajoa x Tetranychus urticae x Oligonychus peruvianus x Chilomima clarkei x Coelosternus spp. x Lagochirus araneiformis x Lagochirus spp. x Vatiga illudens x Vatiga manihotae x Vatiga lunulata x Amblystira machalana x Cyrtomenus bergi x Pangaeus piceatus x Tominotus communis x Heterotermes tenuis x Coptotermes sp. x Phyllophaga menetriesi x Phyllophaga obsoleta x Phyllophaga sneblei x Stemborers Lacebugs Burrower bugs Termites White grubs Africa x x x x x x x Leucopholis rorada Hornworm Asia Erinnyis ello x Erinnyis alope x Tiger moth Phoenicoprocta sanguinea x Leaf-cutter ants Atta sexdens x Atta cephalotes x Acromyrmex landolti x Aonidomytilus albus x Parasaissetia nigra x Ceroplastes sp. x Saissetia miranda x Araecerus fasciculatus x x x Lasioderma serricorne x x x Rhyzopertha dominica x x x Tribolium castaneum x x x Sitophilus oryza x Scale insects Pests of dried cassava (stored) Cassava Pests and their Management C Cassava Pests and their Management, Table 8 Global distribution of important arthropod pests of cassava (Continued) Arthropod pest Major species Americas Africa Asia Sitophilus zeamais x x Prostephanus truncatus x x x x x x x x Gall midge Jatrophobia brasiliensis x Whiteflies Aleurotrachelus socialis x Aleurothrixus aepim x Aleurodicus dispersus x Bemisia afer Shootflies Fruit flies Mealybugs Root mealybugs Bemisia tuberculata x Bemisia tabaci x Trialeurodes variabilis x Neosilba perezi x Silba pendula x Anastrepha pickeli x Anastrepha manihoti x Phenacoccus manihoti x Phenacoccus herreni x Phenacoccus gossypii x Phenacoccus madeirensis x Ferrisia virgarta x Pseudococcus mandio x x Stictococcus vayssierei Leafhoppers Grasshoppers Thrips x Empoasca bispinata x Sacphytopius fuliginosus x Scaphytopius marginelineatus x Zonocerus elegans x Zonocerus variegatus x Frankliniella williamsi x Corynothrips stenopterus x Scirtothrips manihoti x Scolothrips sp. x which cause sporadic defoliation; however, these highly visible pests often induce cassava producers to apply pesticides. Few cassava pests damage cassava roots directly. Three exceptions are burrower bugs (Cyrtomenus bergi), white grubs (Scarabaeidae) and root mealybugs (e.g., Pseudococcus mandio). Cyrtomenus bergi x x causes root punctures during feeding that can introduce fungal pathogens that reduce root yield and quality. White grubs have been found feeding directly on cassava roots causing yield loss and severe root rot. Yield losses of 17% have been reported for P. mandio feeding on cassava roots in southern Brazil. 767 768 C Cassava Pests and their Management In general, arthropod pests are most damaging during the dry season, being less severe in areas of considerable and consistent rainfall; however, there are exceptions to this rule. Hornworm attacks will frequently occur at the onset of the rainy season when there is considerable new growth and young leaves. Severe whitefly attacks often coincide with the rainy season when young, succulent leaves are preferred for oviposition. Studies have also shown that burrower bugs and white grubs prefer soils with higher soil moisture content. The cassava plant is well adapted to long periods of limited water and responds to water shortage by reducing its evaporative (leaf) surface rapidly and efficiently and by partially closing the stomata, thereby increasing water-use efficiency. The crop has the potential to recover and compensate for yield losses from seasonally dry periods and pest attack due to the higher photosynthetic rate in newly formed leaves. Younger leaves play a key role in plant carbon nutrition. Most pests prefer the younger canopy leaves; thus, dry-season feeding tends to cause the greatest yield losses in cassava. Climate change predictions indicate that certain agricultural lands will receive less rainfall in the future. The cassava crop may have a comparative advantage in these extended seasonally drier regions; however, increased cassava production in the Neotropics and Africa could result in more severe pest outbreaks, reducing yields and/or increasing pesticide use. Management of Cassava Arthropod Pests Foliage Feeders Whiteflies Considered one of the world’s most damaging agricultural pest groups, both as direct feeders and virus vectors, whiteflies attack cassava-based agroecosystems in the Americas, Africa and, to a lesser extent, in Asia. Currently, they may be causing more crop damage and yield loss on cassava than any other pest attacking the crop. There is a large species complex associated with the crop, the importance of which can vary between regions or continents. The largest complex on cassava is in the Neotropics, where 11 species are reported, including Aleurotrachelus socialis, Trialeurodes variabilis, Aleurothrixus aepim, Bemisia tuberculata and Bemisia tabaci (=B. argentifolii). Aleurotrachelus socialis and T. variabilis cause considerable direct damage and yield losses in northern South America (Colombia, Venezuela and Ecuador) and in certain regions of Central America. Trialeurodes variabilis is observed primarily in the higher altitudes (over 1,000 m), while A. socialis is confined to lower altitudes (up to 1,200 m). Aleurothrixus aepim is found in high populations causing yield loss in Northeast Brazil. Bemisia tabaci, the vector of CMD, caused by several geminiviruses, has a pantropical distribution, feeding on cassava throughout most of Africa, several countries in Asia and more recently in the Neotropics. It has been speculated that the absence of CMD in the Americas may be related to the inability of its vector to colonize cassava effectively. Prior to the early 1990s, the B. tabaci biotypes found in the Americas did not feed on cassava. The B biotype of B. tabaci, regarded by some as a separate species (B. argentifolii), has been collected from cassava in several regions of the Neotropics. Although seldom observed in high populations, it is now considered that CMD poses a more serious threat to cassava production given that most traditional cultivars grown in the Neotropics are highly susceptible to the disease. Damage Whiteflies can cause direct damage to cassava by feeding on the phloem of leaves, inducing leaf curling, chlorosis and defoliation. High populations, combined with prolonged feeding, result in considerable reduction in root yield. Yield losses resulting from A. socialis and A. aepim activity are Cassava Pests and their Management common in Colombia and Brazil, respectively. With A. socialis feeding, there is a correlation between duration of attack and yield loss. Infestations of 1, 6 and 11 months resulted in a 5, 42 and 79% yield reduction, respectively. More recently, yield losses of 58% due to T. variabilis feeding have been recorded in the Andean region of northern South America. In several East African countries, yield losses due to direct feeding by B. tabaci have been recorded in recent years as a result of the higher populations observed. In Uganda, over 50% reductions in root yield have been recorded. Biology and Behavior Research with A. socialis and A. aepim indicates that populations of both species can occur throughout the growing cycle (1 year or more) but are usually highest during the rainy season when there is considerable new growth. Aleurotrachelus socialis females prefer ovipositing on the undersides of the young apical leaves, reaching a high of 244 eggs (avg. 181, min. 155) per female. The individually oviposited banana-shaped eggs hatch in about 10 days and pass through three feeding nymphal instars and a pupal stage (4th instar) before reaching the winged adult stage. During the third instar the body color changes from beige to black, surrounded by a waxy white cerosine, making this species easy to distinguish from other whitefly species feeding on cassava. Aleurotrachelus socialis egg-to-adult development was 32 days under growth chamber conditions (28 ± 1°C, 70% RH). Aleurotrachelus socialis may be specific to cassava as populations have not been observed on other plant species. Control Integrated management of cassava whiteflies depends on having effective, low-cost, environmentally sound technologies available for farmers. A successful whitefly control program requires continual research input to acquire the basic knowledge needed to develop the technologies and strategies for appropriate implementation. C A recent survey in an important cassava-growing region of Colombia showed that 34% of the farmers surveyed applied chemical pesticides for whitefly control versus only 4.6% applying biological products. Farmer field trials in the region revealed a 58% reduction in yield due to whitefly attack; however, 52% of the farmers surveyed employed no control measures. Pesticide applications have not provided adequate control, probably for lack of knowledge of whitefly biology, especially the immature stages (the presence of eggs and early-instar nymphs). Moreover, around 88% of the farmers had little or no knowledge of whitefly biology, behavior and management. This has resulted in inappropriate timing of applications and the misuse of chemical pesticides. Recent research and field observations on cassava whiteflies in the Neotropics indicate that control measures, especially pesticide applications, are compromised because of the whitefly’s capacity for rapid population increases and its ability to develop high levels of pesticide resistance. When A. socialis feeds on a susceptible cassava variety, it doubles its population every 4.2 days. When there are overlapping crop cycles (e.g., multiple plantings) and favorable rainfall patterns, the conditions are ideal for a rapid buildup in whitefly populations as a constant food supply of young cassava leaves are available for adult feeding, high oviposition and nymphal development. Field observations indicate that once whitefly populations begin this rapid increase, they are very difficult to control, requiring repeated pesticide applications that disrupt natural biological control and that are also uneconomical for small farmers. This capacity for rapid population buildup makes it urgent to introduce efficient management practices early in the plant growth cycle, possibly during the first month of plant growth and before the economic threshold is reached. Four methods of whitefly control in cassava are discussed: host plant resistance (HPR), biological, cultural and chemical. 769 770 C Cassava Pests and their Management Host Plant Resistance This form of resistance to whiteflies is rare in cultivated crops. HPR studies initiated at CIAT more than 20 years ago have systematically evaluated the accessions in the CIAT cassava germplasm bank for resistance to whiteflies, especially A. socialis. Of approximately 5,500 genotypes evaluated in the field in Colombia, about 75% are susceptible, with damage ratings above 3.5 (1 = no damage, 6 = severe damage). Emphasis is placed on those genotypes with damage ratings under 2.0 (about 8%). As there may be susceptible escapes due to insufficient selection pressure, they are reevaluated in subsequent trials. Several sources of resistance to A. socialis have now been identified: Genotype MEcu 72 has consistently expressed a high level of resistance, while MEcu 64, MPer 334, MPer 415 and MPer 273 express moderate to high levels. When feeding on resistant genotypes, A. socialis has less oviposition, a longer development period, smaller size and higher mortality than those feeding on susceptible genotypes. Aleurotrachelus socialis nymphal instars feeding on MEcu 72 and MPer 334 suffered 72.5 and 77.5% mortality, respectively, mostly in the early instars. A cross between MEcu 72 (female parent, whitefly resistant) and MBra 12 (male parent, high yielding, good plant type) resulted in 128 progeny, four of which were selected for whitefly resistance, yield and cooking quality. These four hybrids, along with susceptible genotypes and local farmer varieties, were evaluated at three sites in Tolima Province in Colombia by CORPOICAMADR (Colombian Corp. for Agricultural Research/Ministry of Agricultural and Rural Development) over a 4-year period. CG 489–31 was selected for high whitefly resistance, high yield and good cooking qualities. In 2003, it was officially released by MADR under the name of Nataima-31. It has attained yields of 33 t/ha, outyielding the regional farmers’ variety in Tolima by 34% with no pesticide applications. Nataima-31 is now being grown commercially in several areas of Colombia and has been introduced into Ecuador and Brazil. Given that B. tabaci is a pantropical species that is the vector of CMD, which causes severe cassava crop damage in Africa and India, several cassava genotypes were sent by CIAT to NRI (Natural Resources Institute-UK) to be evaluated for resistance to B. tabaci. Genotype MEcu 72 had the lowest rate of B. tabaci oviposition so it was introduced into Uganda during 2005 and will be included in a breeding program to develop whitefly-resistant varieties. Biological Control Numerous natural enemies are found associated with whiteflies on cassava in the Neotropics (Table 9). In recent field explorations in Colombia, Ecuador, Venezuela and Brazil, a complex of parasitoids, predators and entomopathogens were collected from several whitefly species. The most representative group is that of the microhymenopteran parasitoids. The richness of species in Colombia, Venezuela and Ecuador is primarily represented by the genera Encarsia, Eretmocerus and Amitus, frequently associated with A. socialis. Gaps in knowledge about this natural enemy complex have limited the determination of their effectiveness in biological control programs. There is little knowledge regarding levels and rates of parasitism by species or specification of the host and its effect on the regulation of whitefly populations. Eleven species of parasitoids (5 genera) were collected from the cassava-growing regions of Colombia; an additional five species were collected from Ecuador and seven from Venezuela. On the Caribbean Coast of Colombia, A. socialis was parasitized by eight species, with the genus Eretmocerus comprising 70% of the parasitoids. In Magdalena Province, 73% of A. socialis parasitism was by Amitus macgowni, followed by Encarsia sp. (26%). In the Andean region Eretmocerus spp. parasitized all whitefly species, but Encarsia pergandiella was the predominant parasitoid of T. variabilis. More than 20 species of entomopathogens have been reported infecting whiteflies on cassava, including Aschersonia sp., Lecanicillium (Verticillium) lecani, Beauveria bassiana and Paecilomyces Cassava Pests and their Management C Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests Principal species Parasitoids Predators Entomopathogens Aleurotrachelus socialis Amitus macgowni Delphastus sp. Beauveria bassiana Encarsia sp. D. quinculus Lecanicillium lecani Encarsia hispida D. pusillus Aschersonia aleyrodes E. bellotti Chrysopa sp. nr. cincta E. sofia Condylostylus sp. E. luteola E. americana E. cubensis Metaphycus sp. Euderomphale sp. Signiphora aleyrodis Eretmocerus spp. Aleurothrixus aepim Cladosporium sp. Encarsia porteri E. aleurothrixi Aleurodicus dispersus Encarsia sp. E. haitiensis Aleurotonus vittatus Eretmocerus sp. Bemisia tuberculata E. hispida Condylostylus sp. E. pergandiella Euderomphale sp. Encarsia sp. prob. variegata Metaphycus sp. Eretmocerus sp. Bemisia tabaci Encarsia sophia Delphastus pusillus E. lutea Condylostylus sp. E. formosa E. mineoi Eretmocerus mundus Trialeurodes variabilis Encarsia sp. Chrysopa sp. nr. cincta Aschersonia aleyrodes E. pergandiella Condylostylus sp. B. bassiana E. Sophia E. luteola E. strenua L. lecani 771 772 C Cassava Pests and their Management Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests (Continued) Principal species Parasitoids Predators Entomopathogens E. hispida E. bellotti E. nigricephala Eretmocerus spp. Aleuroglandulus malangae Encarsia guadeloupae, Encarsia desantisi Mononychellus tanajoa Nephaspis namolica Insects: Hirsutella thompsoni Stethorus tridens Neozygites floridana S. darwin N. tanajoae S. madecasus Oligota minuta O. gilvifrons O. centralis O. pigmaea Delphastus argentinicus Chrysopa sp. Mites/Phytoseiidae: Typhlodromalus manihoti T. aripo Neoseiulus idaeus Galendromus annectes Euseius concordis Euseius ho Phenacoccus manihoti Apoanagyrus lopezi Cleothera onerata Acerophagus sp. Hyperaspis sp. Nephus sp. Chrysopa sp. Sympherobius sp. Typhlodromalus aripo Phenacoccus herreni Acerophagus coccois Ocyptamus sp. Cladosporium sp. Apoanagyrus diversicornis Sympherobius sp. Neozygites fumosa Aenasius vexans Hyperaspis sp. Anagyrus insolitus Nephus sp. A. thyridopterygis Cleothera onerata A. pseudococci C. notata Cassava Pests and their Management Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests (Continued) Principal species Parasitoids Predators Anagyrus sp. nr. Greeni Diomus sp. Aenasius sp. nr. putonophylus Coccidophylus sp. Prochiloneurus dactylopii Scymnus sp. Chartocerus sp. Olla sp. Hexacnemus sp. Curinus colombianus Eusemion sp. Cycloneda sanguinea Entomopathogens Hippodamia convergens Azya sp. Chrysopa sp. K. coccidarum Zelus sp. Phenacoccus gossypii Anagyrus sp. Curinus colombianus Apoanagyrus sp. Cleothera onerata Aenasius masii Coccidophylus sp. Acerophagus coccois Scymnus sp. Hexacnemus sp. Olla sp. Eusemion sp. Hippodamia convergens Haltichella sp. Azya sp. Prospaltella sp. Chrysopa sp. Signiphora sp. K. coccidarum Cladosporium sp. Pentillia sp. Sympherobius sp. Ocyptamus sp. Kalodiplosis coccidarum Zelus sp. Emesaya sp. Frankliniella williamsi Orius sp. Scirtothrips manihoti T. aripo Vatiga illudens Zelus sp. Vatiga manihotae Zelus nugax Erinnyis ello Trichogramma spp. Chrysopa spp. Bacillus thuringiensis Telenomus sphingis Podisus nigrispinus baculovirus of E. ello Cotesia americana P. obscurus Metarhizium anisopliae Cotesia sp. Polistes carnifex Beauveria bassiana Euplectrus sp. P. erythrocephalus Paecylomices sp. C 773 774 C Cassava Pests and their Management Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests (Continued) Principal species Parasitoids Predators Entomopathogens Drino macarensis P. versicolor Nomuraea rileyi Drino sp. P. canadensis Cordyceps sp. Euphorocera sp. Polybia emaciata Sarcodexia innota P. sericea Thysanomia sp. Zelus nugax Belvosia sp. Zelus sp. Forciphomyia eriophora Calosoma sp. Cryptophion sp. Dolichoderus sp. Ooencyrtus sp. Alcaeorrhynchus grandis Chetogena scutellaris Spiders: Tomicidae Salticidae Erinnyis alope Trichogramma spp. Spiders: Telenomus sp. Tomicidae Salticidae Chrysopa sp. Chilomima clarkei Brachymeria sp. Metarhizium anisopliae Tetrastichus howardi Beauveria bassiana Trichogramma sp. undetermined virus Prodilis sp. Aonidomytilus albus Saissetia miranda Anagyrus sp. Metaphycus sp. Scutellista cyanea Anastrepha pickeli Opius sp. Anastrepha manihoti Opius sp. Cyrtomenus bergi Nerthra sp. Heterorhabditis sp. Metarhizium anisopliae Steinernema sp. Phyllophaga menetriesi Campsomeris dorsata Metarhizium anisopliae Beauveria bassiana Stictococcus vayssierei Zonocerus elegans Anoplolepis tenella Metarhizium anisopliae Cassava Pests and their Management C Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests (Continued) Principal species Parasitoids Predators Entomopathogens Beauveria bassiana Zonocerus variegatus Metarhizium anisopliae Beauveria bassiana Iatrophobia brasiliensis Torymoides sulcius fumosoroseus; however, there has to be a careful selection of the species, as well as the identification of native isolates of entomopathogenic fungi. Greenhouse experiments at CIAT with an isolate of L. lecani resulted in 58–72% A. socialis nymphal mortality and 82% egg mortality. The L. lecani isolate has been formulated into a commercial biopesticide BioCanii®. The commercial biopesticide Mycotrol®, (isolate of B. bassiana, a product of Laverlam S.A.), gave very effective control (over 90% mortality of the egg and first two nymphal instar stages) of A. socialis in greenhouse experiments at CIAT. Mycotrol®, which is also effective against B. tabaci and T. variabilis, is presently being evaluated in field trials. The most frequently observed predators feeding on cassava whiteflies are chrysopids (Neuroptera: Chrysopidae). These generalists feed on the eggs and immature stages of numerous arthropods. Chrysoperla carnea is frequently collected feeding on A. socialis in cassava fields. In lab studies at CIAT, A. socialis egg and nymphal consumption by C. carnea were measured by recording the time required for 50% consumption of the prey state being offered. Chrysoperla carnea adults required 80 h to consume 50% of the nymphal instars and pupae and 77 h to consume 50% of the eggs. Cultural Control In traditional cropping systems cassava is often intercropped, a practice that has been shown to reduce populations of certain pests. Intercropping cassava with cowpeas reduced egg populations of A. socialis and T. variabilis by 70% compared to those in monoculture. Yield losses in cassava/ maize, cassava monoculture and mixed cultivar systems were ca. 60% versus only 12% in cassava/ cowpea intercrops. When cassava is grown in overlapping cycles or multiple plantings, it is difficult to break the whitefly development cycle so rapid population buildups occur. Upon emerging from the pupal stage, adults migrate to feed and oviposit on recently germinated young plants in adjacent fields. A successful tactic for countering this situation is to implement a “closed season,” defined as an interdiction or prohibition when cassava cannot be present in the field. Field observations at CIAT have shown that a 1- to 2-month period with no cassava in the field decreases whitefly populations dramatically over a 4-year period. The success of this ban is enhanced by the fact that A. socialis does not appear to have efficient alternate hosts so their populations “crash” when adults cannot find an alternate host species to sustain or increase populations. Nevertheless, the economic practicality of this strategy for the producers is debatable. In many regions a constant supply of cassava roots is economically desirable for meeting the demands of local fresh and processing markets. This same tactic would not be as effective for a species such as B. tabaci, which has numerous alternate hosts where its populations can be sustained and multiply. Chemical Control Several products with new or novel active ingredients have been evaluated for controlling 775 776 C Cassava Pests and their Management A. socialis and T. variabilis. Foliar applications of theamethoxam and imidacloprid were most efficient in reducing whitefly populations. Best control was obtained when applied as a drench at a high doses (0.8 and 0.6 l/ha) on young plants. The treatment of cassava planting material (stem cuttings) with a 7-min emersion in a solution of theamethoxam (Actara®) (1 g/l H2O) is also giving promising results. More than two pesticide applications during the crop cycle should be avoided. Field experiments have shown that pesticides need not be applied after 6 months of crop growth as yield loss due to whitefly attack will not occur. A cost-benefit analysis indicates that chemical pesticide applications for whitefly control in cassava are generally uneconomical for small farmers and only slightly beneficial for large farmers who can generally receive a higher price for the product. Research is under way to evaluate the feasibility of substituting entomopathogens as biopesticides to replace chemical pesticide applications. losses of 21, 25 and 53%, respectively. Under high mite populations on the Colombian Atlantic Coast, yields were reduced by 15% in resistant cultivars compared with an average 67% loss in susceptible cultivars. In Africa, M. tanajoa was first reported from Uganda in 1971; within 15 years it had spread across most of the cassavagrowing belt, occurring in 27 countries and causing estimated root losses of 13–80%. CGM has been the objective of a major biological control effort since the early 1980s. Cassava Mites More than 40 species of mites have been reported feeding on cassava in the Americas, Africa and Asia. The most important are Mononychellus tanajoa (syn. = M. progresivus), Mononychellus caribbeanae, Tetranychus cinnabarinus and Tetranychus urticae (also reported as T. bimaculatus and T. telarius). Cassava is the major host for the Mononychellus spp., while the Tetranychus spp. have a wide host range. Mononychellus tanajoa, the cassava green mite (CGM), is the most important species, causing crop losses in the Americas and Africa. It is native to the Neotropics, first being reported from northeast Brazil in 1938. It is presently found in most cassava-growing regions in the Americas, especially in seasonally dry regions of the lowland tropics in Brazil, Colombia and Venezuela. Biology and Behavior Mites, especially the cassava green mite, are dryseason pests that can cause yield losses where there is a seasonally dry period of at least 3 months. At the onset of the rainy season, mite populations decrease and cassava plants produce new foliage. If the rains do not persist, cassava green mite populations will again increase, causing defoliation and more severe yield losses. This pattern has been observed in the semiarid cassava-growing regions of Northeast Brazil. Cassava green mite populations prefer to feed on the undersides of young emerging leaves, which develop a mottled whitish to yellow appearance and may become deformed or reduced in size. Heavy infestations will cause defoliations, beginning at the top of the plant, often killing apical and lateral buds and shoots. The adult is green in color with an average body length of about 350 µm. Females oviposit on the leaf undersurface; eggs hatch in 3–4 days (30°C and 70 ± 5% RH). At 15, 20, 25 and 30°C, the eggto-adult stage is 41.4, 19.5, 10.3 and 7.8 days, respectively. These data indicate that cassava green mite populations can increase rapidly in warm regions of the lowland tropics. At 30°C, each female oviposits 90–120 eggs; during the initial population buildup, mostly females are produced, adding to the rapid population increase. Damage In experimental fields in Colombia, M. tanajoa attacks of 3, 4 and 6 months resulted in yield Management Pesticide applications for controlling mites on a long-cycle crop such as cassava are not a feasible or Cassava Pests and their Management economic option for low-income farmers. Moreover, even low doses of pesticides have adverse effects on natural enemies. Cultural control methods have not been explored, and there is little mention of their use in the literature. Research into the control of M. tanajoa has followed two main thrusts: HPR and biological control. It is expected that these two complementary strategies can reduce cassava green mite populations below economic injury levels. Host Plant Resistance It is hypothesized that in the presence of efficacious natural enemies, only low-to-moderate levels of HPR are needed to reduce CGM populations below economic injury levels. A level of resistance that would hinder, delay or suppress the initial buildup of cassava green mite populations could provide sufficient opportunity for establishing effective natural enemy populations that would prevent an eruption of the cassava green mite population. Therefore an important objective of an HPR strategy is to develop cultivars that are not highly susceptible to the cassava green mite and that hopefully contain low-to-moderate levels of resistance. Immunity or even high levels of resistance do not appear to be available in M. esculenta germplasm. A considerable effort has been made to identify cassava green mite resistance in cultivated cassava. CIAT, IITA and several national research programs in the Americas and Africa have screened cassava germplasm for cassava green mite resistance. Of the more than 5,000 landrace cultivars in the CIAT cassava germplasm bank, only 6% (300 cultivars) were identified as having low-to-moderate levels of resistance. A select number of cultivars with moderate levels of resistance have been released to farmers after a considerable effort by plant breeders and entomologists. Two hybrids (ICA Costeña and Nataima 31), both with low levels of mite resistance, are being grown by cassava farmers in Colombia. Most mite-resistance field evaluations by CIAT have been carried out in the lowland tropics with a prolonged dry season (4–6 months) and high mite populations (Colombian Atlantic Coast). In Brazil, cassava green mite evaluations were C conducted by CNPMF/EMBRAPA, primarily in the semiarid regions of the northeast. Of the 300 cultivars identified by CIAT as promising for CGM resistance (over several years and 2–7 field cycles), 72 have consistently had damage ratings below 3.0. Low-to-moderate levels of resistance are indicated by 0–3.5 (0–6 damage scale). Mite resistance-mechanism studies indicate strong antixenosis (preference vs nonpreference) for oviposition, as well as moderate antibiosis. In lab studies, M. tanajoa displayed a strong ovipositional preference for susceptible varieties. When paired with the moderately resistant cultivars MEcu 72, MPer 611 and MEcu 64 in freechoice tests, 95, 91 and 88%, respectively, of the eggs were oviposited on the susceptible cultivar CMC 40. Antibiosis is expressed by mites having lower fecundity, a longer development time, a shorter adult life span, and higher larval and nymphal mortality when feeding on resistant versus susceptible cultivars. Biological Control Beginning in the early 1980s, extensive evaluations of the natural enemy complex associated with cassava mites were conducted at more than 2,400 sites in 14 countries of the Neotropics. The primary target in most of these field and lab studies was the cassava green mite. These ongoing extensive surveys indicate that the cassava green mite is present throughout much of the lowland Neotropics. High populations, which can cause significant yield loss, occur most frequently in Northeast Brazil and can be localized. Geographic regions of the Americas were identified and prioritized using GIS support to assist in targeting specific areas for exploration. Homologous maps based on agrometeorological data and microregional classification comparing Africa and the Neotropics were prepared as one of the major targets for biological control in those areas of Africa where the cassava green mite was causing economic damage. A total of 87 phytoseiid species were collected and stored: 25 are new or unrecorded species; 66 777 778 C Cassava Pests and their Management were collected from cassava. The current predator mite reference collection held at CIAT conserves primarily those related to phytophagous mites found on cassava. A taxonomic key on the species associated with cassava is being prepared with Brazilian colleagues. The CIAT-Brazil collection is a true reference collection with accompanying database and can be readily used for species description. Explorations also identified several insect predators of cassava green mite, especially the staphylinid Oligota minuta and the coccinellid Stethorus sp. After extensive lab and field studies of this cassava green mite predator complex, it was generally agreed that the phytoseiid predators offer the best potential for controlling mites, especially when occurring in low densities. The phytoseiid development cycle is shorter than that of the cassava green mite. In studies at CIAT with the species Neoseiulus anonymus, the egg-to-adult development period at 25 and 30°C was 4.7 and 4.0 days, respectively. This is approximately half the development period for the cassava green mite at those temperatures. Survey data also revealed that cassava green mite densities were much higher in northeast Brazil than in Colombia, but the richness of phytoseiid species was greater in Colombia. Field data from experiments in Colombia demonstrated that a rich phytoseiid species complex could reduce cassava green mite populations and prevent cassava yield loss. When natural enemies were eliminated by applying low doses of an acaricide that did not affect the cassava green mite population, cassava root yields were reduced by 33%. Application of an acaricide did not increase yields, indicating the effectiveness of biological control. A major objective of the surveys for cassava green mite natural enemies and the substantial research that followed was to identify the key phytoseiid species controlling cassava green mite populations and introduce them into Africa. This was a collaborative effort between CIAT and EMBRAPA in the Americas and IITA in Africa. Of the phytoseiid species identified as feeding on CGM, those most frequently collected were Typhlodromalus manihoti (found in over 50% of the fields surveyed), Neoseiulus idaeus, Typhlodromalus aripo, Galendromus annectens, Euseius concordis and Euseius ho. More than ten species of phytoseiids were shipped from Colombia and Brazil to Africa, via quarantine in England (IIBC-International Institute of Biological Control). None of the Colombian species became established, but three of the Brazilian species did (T. manihoti, T. aripo and N. idaeus). Typhlodromalus aripo, the most successful of the three species, has now spread and is found in more than 14 countries. Typhlodromalus aripo inhabits the apex of cassava plants during the day and forages on leaves at night; it can persist during periods of low cassava green mite densities by consuming alternative food sources (e.g., maize pollen). On-farm trials in Africa indicate that T. aripo reduces CGM populations by 35–60% and increases fresh root yield by 30–37%. Neozygites sp. is a fungal pathogen (Zygomycetes: Entomophthorales) found on mites throughout cassava-growing regions of the Neotropics. Isolates of Neozygites floridana from Brazil and Colombia, and from M. tanajoa from Brazil and Benin were evaluated on the cassava green mite in Africa. Laboratory and field studies indicate that the Brazilian strain of N. floridana was the most virulent. Although this fungus shows considerable promise for biological control of the cassava green mite, further research and field evaluations are needed. Exotic phytoseiid mite predators can play an important role in reducing CGM populations in Africa; however, field observations in the Neotropics indicate that they are very sensitive to disturbances in the agroecosystems, especially the use of pesticides. For example, when insecticides were applied at CIAT for controlling thrips, cassava green mite populations erupted, and few phytoseiid predators were detected in the fields. Studies in Colombia showed that low acaricide doses that did not cause mortality to cassava green mite were lethal to phytoseiids, causing a considerable increase in mite populations and cassava yield losses. In the Neotropics, Cassava Pests and their Management C especially on larger plantations, cassava farmers may use pesticides to control hornworm, whitefly or thrips outbreaks. This could result in mite outbreaks and yield losses if biological control is the only control measure, and highly susceptible cultivars are being grown. ranged from 68–88%, depending on cultivar susceptibility. Farmers in northeast Brazil estimated their losses to be over 80%, and cassava production decreased in the region during the 1980s. In Africa, yield losses due to P. manihoti feeding and damage were around 80%. Cassava Mealybugs Although more than 15 species are reported attacking the crop, only two are important economically, Phenacoccus herreni and P. manihoti, both of Neotropical origin. Phenacoccus manihoti was introduced inadvertently into Africa in the early 1970s, where it spread rapidly across the cassavagrowing regions of that continent, causing considerable yield loss. This species has been the object of a successful biological control program. In the Americas P. manihoti was first found in Paraguay in 1980 and later collected from certain areas of Bolivia and Mato Grosso do Sul state in Brazil, causing no economic damage. More recently (2005), P. manihoti was collected from two northeastern states, Bahia and Pernambuco. The origin of P. herreni is probably northern South America, where it was found in cassavagrowing regions of Colombia and Venezuela. It was first reported in northeast Brazil during the mid-1970s, where high populations caused considerable yield losses. Surveys in the region found few parasitoid natural enemies, suggesting that P. herreni is an exotic pest, probably coming from northern South America where parasitoids are frequently observed. Biology and Behavior Both species are morphologically similar and originally thought to be only one species. Phenacoccus manihoti is parthenogenic, whereas males are required for reproduction of P. herreni. The females deposit ovisacs containing hundreds of eggs on the undersides of leaves and around apical and lateral buds. Eggs hatch in 6–8 days, and there are four nymphal instars; the first instars are highly mobile and will spread over the plant or between plants. The fourth instar is the adult stage for females, while males have four nymphal instars plus the adult stage. The third and fourth instars occur in a cocoon, from which the winged male adults emerge, living only 2–4 days. The life cycle of the female is 49.5 days; that of the male, 29.5. The optimal temperature for female development is 25–30°C. Populations of both species peak during the dry season. The onset of rains reduces pest populations and plant damage, permitting some crop recovery. Mealybug dissemination between regions, countries or continents is probably through infested stem cuttings. The introduction of P. manihoti into northeast Brazil from southern Brazil can probably be traced to the movement of cassava varieties between these two regions. Damage Both species cause similar damage: adult and nymph feeding causes leaf yellowing, curling and cabbage-like malformation of the apical growing points. High populations lead to leaf necrosis, defoliation, stem distortion and shoot death. Reductions in photosynthetic rate, transpiration and mesophyll efficiency – together with moderate increases in water-pressure deficit, internal CO2 and leaf temperature – were found in infested plants. Yield losses in experimental fields at CIAT Management Cassava mealybug management is a welldocumented example of classical biological control, both in Africa and the Americas. In Africa, P. manihoti is being controlled successfully after introducing the parasitoid Anagyrus lopezi from the Neotropics. After several years of exploration in the Neotropics by scientists from IIBC, IITA and CIAT, the target species P. manihoti was finally located by a CIAT scientist (A.C. Bellotti) in Paraguay in 1980. IIBC collected natural enemies of P. manihoti that 779 780 C Cassava Pests and their Management were sent via quarantine in London to IITA in Benin for multiplication and release in Africa. The encyrtid parasitoid A. lopezi and the coccinellid predators Hyperaspis notata, Hyperaspis raynevali, and Diomus sp. became established in Africa. The parasitoid is credited with being the principal agent reducing the mealybug populations. Anagyrus lopezi became established in all ecological zones occupied by P. manihoti and is now found in 27 countries, covering an area of 2.7 million km2. Cassava losses have been reduced by 90–95% with an estimated savings of US$7.971–20.226 billion. Surveys in Colombia and Venezuela identified numerous parasitoids, predators and entomopathogens associated with P. herreni. Several parasitoids show a specificity or preference for P. herreni: Acerophagus coccois, Anagyrus diversicornis, Anagyrus putonophilus, Anagyrus isolitus, Anagyrus elegeri and Aenasius vexans. Based on numerous field and lab studies, three encyrtid parasitoids (A. diversicornis, A. coccois and A. vexans) were identified as effective in P. herreni infestations. Comparative life-cycle studies show that they completed two cycles for each cycle of P. herreni. This is a favorable ratio for biological control. Anagyrus diversicornis prefers third instar nymphs, where as the smaller A. coccois parasitizes male cocoons, adult females and second instar nymphs. Aenasius vexans prefers second and third instar nymphs. Field studies with natural populations of A. diversicornis and A. coccois estimated P. herreni mortality at 55% for their combined action. Through the combined efforts of CIAT and CNPMF/EMBRAPA, these three parasitoids were exported from CIAT to EMBRAPA, Brazil, where they were mass reared and released into P. herreniinfested cassava fields, primarily in the northeastern states of Bahia and Pernambuco from 1994 to 1996. More than 35,000 parasitoids were released, and all three species became established. Studies prior to release had determined that none of these species existed in this region. In Bahia, A. diversicornis dispersed 120 km in 6 months after release and 304 km in 21 months. A. coccois was recovered in high numbers 9 months later, 180 km from its release site. Aenasius vexans was consistently recaptured at its release site in Pernambuco, having dispersed only 40 km in 5 months. Personal observations in recent years indicate that P. herreni populations have decreased considerably as cassava farmers in the region have not reported severe outbreaks and cassava cultivation has returned to areas where it had been previously abandoned due to P. herreni damage. However, the recent introduction of P. manihoti into the region has resulted in reports of severe mealybug damage in Bahia, causing alarm among cassava producers. An effort by local institutions and researchers is needed to determine if key P. manihoti parasitoids are present or need to be introduced into the region. Thrips Several species of thrips are reported feeding on cassava, primarily in the Americas. The most important include Frankliniella williamsi, Corynothrips stenopterus, Scirtothrips manihoti, Caliothrips masculinus and Scolothrips sp. More recently a new species of thrips (Thrichinothrips strasser) associated with cassava was reported from Costa Rica. Frankliniella williamsi is reported feeding on cassava in Africa, and high populations of S. manihoti have recently been reported from central Brazil. Frankliniella williamsi appears to be the most important species and the only one reported causing yield losses. Damage Frankliniella williamsi larvae and adults feed on the growing points and young leaves of cassava, which do not develop normally; leaflets are deformed and show irregular chlorotic spots. The rasping-sucking stylet-like mouthparts damage leaf cells during expansion, causing deformation and distortion; and parts of the leaf lobes are missing. Brown wound tissue appears on the stems and petioles, and internodes are shortened. Growing points may die, causing growth of lateral buds, which may also be attacked, giving the plant a witches’-broom appearance that can be confused with viral disease symptoms. Cassava Pests and their Management Yield reductions induced by F. williamsi range from 5–28%, depending on varietal susceptibility. The average reduction for eight varieties in Colombia was 17.2%. Thrips damage and yield reduction are especially pronounced in the seasonally dry tropics where the dry season is at least 3 months. Plants recover with the onset of the rainy season. Management Frankliniella williamsi is not considered a major pest of cassava as it is not often reported causing yield losses in farmers’ fields. It can be controlled easily by using resistant pubescent cultivars. Approximately 50% of the CIAT cassava germplasm bank are pubescent, and resistant to F. williamsi. Resistance is based on leaf bud pilosity, and increasing pubescence of unexpanded leaves increases thrips resistance. Observations indicate that most landrace varieties grown by farmers in the seasonally dry lowland tropics are pubescent. It is hypothesized that cassava growers may have selected pubescent varieties over time for the absence of thrips damage. Cassava Lacebugs Reported as pests of cassava only in the Neotropics, five species of the genus Vatiga show a decided preference for feeding on cassava: Vatiga illudens, V. manihotae, V. pauxilla, V. varianta and V. cassiae. The first two are the most widely distributed and the most damaging to cassava. Vatiga illudens predominates in Brazil but also occurs throughout the Caribbean region and may be present in other areas. Vatiga manihotae, the most widespread lacebug, is consistently found on cassava in Colombia and Venezuela, but is also reported from Cuba, Trinidad, Peru, Ecuador, Paraguay, Argentina and Brazil. Vatiga spp. have also been reported feeding on wild species of Manihot. In 1985 the black lacebug, Amblystira machalana, was first observed causing damage to cassava in different regions of Colombia, Venezuela and Ecuador. Damage Lacebug adults and nymphs feed on the undersurface of lower and intermediate leaves, but can also C damage upper leaves. Feeding by Vatiga spp. causes leaves to form yellow spots that eventually turn reddish brown, resembling Tetranychus mite damage. Amblystira machalana feeding is characterized by white feeding spots that increase in area until leaf centers turn white and eventually darken. High lacebug populations will cause leaves to curl and die, often resulting in defoliation of lower leaves. Higher populations are observed on younger plants (4–5 months) but decline as plants age. The relationship between damage and population density and duration is not entirely understood. In recent field trials with natural populations of A. machalana at CIAT, yield losses ranged from 8.1–42.7%, depending on cultivar susceptibility and duration of lacebug attack. Populations of V. illudens in Brazil are endemic and appear to be causing yield losses, especially in the central Campo Cerrado regions, although high populations are also reported from the south and northeast. Biology and Behavior Prolonged dry periods favor high populations of V. illudens and V. manihotae. In contrast, A. machalana attack can occur during both wet and dry seasons, but is more likely during rainy periods. Observations in Colombia indicate shifts in lacebug populations. Vatiga manihotae was the predominant species in the Cauca Valley until the mid-1980s. By 1990, A. machalana populations dominated. More recently, V. manihotae increased and is once again the predominant species, while A. machalana is difficult to find. The cause for this shift in populations is unknown. In Ecuador, populations of A. machalana remain high. The egg stage of V. manihotae is 8–15 days, followed by five nymphal instars averaging 16–17 days; adult longevity was 40 days under field conditions. Laboratory studies with V. illudens in Brazil reported a nymphal duration of 13.5 days and an average adult longevity of 27 days. In lab studies with A. machalana, the egg stage averaged 8.2 days; the five nymphal instars, 14 days; average adult longevity was 22 days. 781 782 C Cassava Pests and their Management Management Lacebugs are the least studied of the important cassava pests, so considerable research is required before sound and efficient management practices can be recommended. These studies should be conducted in Brazil where V. illudens is endemic. Lacebug control appears difficult as few natural enemies have been identified, and chemical control should be avoided. In Colombia and Ecuador, observations indicate that V. manihotae or A. machalana populations are not high enough to warrant pesticide applications. Preliminary screening of cassava germplasm in Brazil and Colombia indicates that HPR may be available, but no germplasm development program is attempting to develop resistant cultivars. In insectary studies in Brazil using caged V. illudens-infested plants, isolates of the fungal entomopathogens Metarhizium anisopliae and Beauveria bassiana caused 100 and 74% mortality of the lacebugs, respectively, indicating the potential of these fungi for lacebug control. Cassava Hornworms Several lepidopterans feed on cassava, the most important being the cassava hornworm, Erinnyis ello, which causes serious damage to cassava in the Neotropics and has a broad geographic range, extending from southern Brazil, Argentina and Paraguay to the Caribbean Basin and southern USA. The migratory flight capacity of E. ello, its broad climatic adaptation, and wide host range probably account for its wide distribution. Several other species of Erinnyis (E. alope, and subspecies E. ello ello, E. ello encantado) are reported feeding on cassava in the Neotropics, but they appear to be of minor importance and do not cause economic damage to the crop. Damage Hornworm larvae feed on cassava leaves of all ages, and high populations will also consume young, tender stems and leaf buds. Severe attacks cause complete plant defoliation, bulk root loss and poor root quality. In farmers’ fields, natural attacks resulted in 18% yield loss; simulated damage studies resulted in 0–64% root loss, depending on number of attacks, plant age and edaphic conditions. Repeated attacks are more common when poorly timed pesticide applications fail to destroy fifth instar larvae or prepupae. Frequent attacks often occur on larger plantations (over 100 ha), where subsequent populations can oviposit and feed on areas not previously defoliated. Severe attacks and complete defoliation do not kill cassava because carbohydrates stored in the roots enable recovery, especially during the rainy season. Biology and Behavior Although hornworm outbreaks are sporadic, they mostly occur during the rainy season when foliage is abundant. The grey, nocturnal, migratory adult moths have strong flight abilities. Erinnyis ello females oviposit small, round, light green to yellow eggs individually on the upper surface of cassava leaves. In field cage studies, females oviposited an average of 450 eggs, although as many as 1,850 eggs/female were observed. This high level oviposition, combined with the mass migratory behavior of adults, helps explain the rapid buildup of hornworm populations and their sporadic occurrence. During the larval period, each hornworm consumes about 1,100 cm2 of foliage, about 75% of this during the fifth instar. At 15, 20, 25 and 30°C, the mean duration of the larval stage is 105, 52, 29 and 23 days, respectively, indicating that their peak activity may occur at lower altitudes or during the summer in the subtropics. When considerable leaf area is present, up to 600 eggs may be found on a single plant, and larval populations may exceed 100 per plant. It is estimated that 13 fifth instar larvae can defoliate a 3-month-old plant in 3–4 days, especially on low fertility soils. Given the foregoing, hornworm outbreaks must be controlled when populations are in the early larval stage. Management The migratory behavior of hornworm adults makes effective control difficult to achieve and Cassava Pests and their Management reduces the impact of natural biological control. Insect migration has been described as an evolved adaptation for survival and reproduction, and some researchers speculate that the hornworm’s migration evolved as a mechanism to survive low food availability, unfavorable environmental conditions and attack by natural enemies. It is important to detect hornworm outbreaks while in the early development stages. Successful control requires monitoring field populations to detect migrating adults, oviposition or larvae in the early instars. This can be done with black light traps for adults or by scouting fields for the presence of eggs and larvae. Pesticides give adequate control if applied when hornworm populations in the early larval instar stages are detected and treated. Larval populations in the fourth and fifth instars are difficult to control. Farmers often react only when considerable defoliation has occurred, with excessive, ill-timed costly applications that can lead to repeated or more severe attacks. Pesticide use may also disrupt natural enemy populations, leading to more frequent attacks, a common occurrence on larger plantations. More than 30 species of parasites, predators and pathogens of the egg, larval and pupal stages have been identified and reviewed extensively; however, their effectiveness is limited, most likely due to the migratory behavior of hornworm adults. Eight microhymenopteran species of the families Trichogrammatidae, Scelionidae and Encryrtidae are egg parasites, of which Trichogramma and Telenomus are the most important. In recent field surveys during a hornworm outbreak at CIAT, egg parasitism reached 68%, 57% due to Trichogramma sp. and 11% to Telenomus sp. Tachinid flies are important dipteran larval parasitoids and the Braconidae, especially Cotesia spp., are the most important hymenopteran. Chrysopa spp. are common egg predators while important larval predators include Polistes spp. (Hymenoptera: Vespidae) and several spider species. Important entomopathogens include Cordyceps sp. (Aconycites: Clavicipitaceae), a soil-borne fungus that invades hornworm pupae causing mortality. Recent lab C studies show that certain isolates of Beauveria sp. and Metarhizium sp. cause high larval mortality. Hornworm outbreaks can be controlled with timely (early instars) applications of commercial biopesticides of Bacillus thuringiensis. The effectiveness of biological control agents in a hornworm management strategy depends on the ability to synchronize the release of large numbers of predators or parasitoids to augment natural biological control. Predator and parasitic effectiveness in hornworm control is limited by poor functional response during outbreaks, which are of short duration (15 days). In the absence of a reliable commercial source of Trichogramma or other parasitoid or predator species, the cost of maintaining these natural enemies in continuous culture to guarantee availability when an E. ello outbreak occurs is economically prohibitive and impractical for most cassava farmers. The complexities of inundatory releases of parasitoid and predator species suggest the need for a cheap, storable biological pesticide. A granulosis virus of the family Baculoviridae was found attacking E. ello in cassava fields at CIAT in the early 1970s. Pathogenicity studies using virus material extracted from infected larvae collected in the field were carried out on cassava plants in the lab and field. Larval mortality reached 100% at 72 h after application. Studies on the effect of virus concentration on mortality of larval instars showed a sigmoidal relationship for the first, second and forth instars. LD50 studies show that progressively higher concentrations are needed for adequate control of each succeeding larval instar. Most fifth instar larvae reached the prepupal stage, but few female adults emerged and those that did had wing deformities and died without producing progeny. Although the baculovirus can be managed by small farmers, this technology has been most successful with larger producers or where research and extension services have provided access to it. Growers can collect and macerate diseased larvae and apply the virus suspension to cassava fields. The virus can be stored for several years under refrigeration, and for a few months at room 783 784 C Cassava Pests and their Management temperature. Hornworm management with the baculovirus was implemented in southern Brazil during the late 1980s and early 1990s. Researchers and extension workers trained farmers in the handling and use of the virus and distributed free samples. By 1991 the virus was being applied on about 34,000 ha in Paraná state at a cost of only about US$1/ha. In Santa Catarina state, virus applications to early instars resulted in almost complete control, and pesticide applications were reduced by 60%. In Venezuela, where the hornworm is endemic, the virus preparation was applied (70 ml/ha) to large cassava plantations (7,000 ha) via overhead sprinkler irrigation systems when larvae were in the first and second instars. This not only resulted in 100% control but also eliminated pesticides; the cost of gathering, processing, storing and applying the virus preparation was only US$4/ha. In Colombia, a baculovirus biopesticide was developed by a private company (Biotropical) in collaboration with CIAT. The product has been approved for commercial release by MADR and is available as a wettable powder. Field trials to evaluate the efficacy of this product (Bio Virus Yuca®) were carried out in two locations in Colombia: the provinces of Tolima and Risaralda. During natural hornworm attacks, the baculovirus applications (300 g/ha) resulted in 93% hornworm mortality in Tolima and 85% in Risaralda. The key to effective hornworm control is training farmers to detect outbreaks through light trapping of adults or field monitoring combined with the timely application of a biopesticide (or chemical insecticide) when larvae are in their early instars (1–3). Stemborers and Stem Feeders Numerous insect species can feed on and damage cassava stems and branches. Although some species are nearly worldwide in distribution, the most important are in the Neotropics. Four pests will be discussed in this section: stemborers, scale insects, fruit flies and shoot flies. Several other pests can also damage the stem (e.g., mites, thrips, mealybugs, hornworms and grasshoppers); however, they are primarily leaf feeders and are discussed elsewhere. Dipteran fruit flies (Anastrepha spp.) and shoot flies (Neosilba sp.) can also bore into the stem and are discussed here. Stemborers can damage cassava in two ways; they can (i) weaken the plant by tunneling in the stems, causing breakage that will reduce yields, and (ii) destroy or reduce the quality of stem cuttings, thereby affecting germination and vigor of the planting material. Stemborers A complex of arthropod stemborers that includes both lepidopteran and coleopteran species feed on and damage cassava. In the Neotropics stemborers are most important in Colombia, Venezuela and Brazil. Seven species of Coelosternus (Coleoptera: Curculionidae) can reduce cassava yields and quality of planting material in Brazil; however, the damage is generally sporadic and localized, and significant yield losses are not reported. Although stemborer species have been identified in Africa, there are no reports of severe damage or yield losses. Populations of the stemborer Chilomima clarkei (Lepidoptera: Pyralidae) have increased dramatically in Colombia and Venezuela in recent years, to the point where it is now considered an important pest of cassava, causing yield losses and damage to stem cuttings. On the Atlantic coast of Colombia (provinces of Magdalena and Cesar), C. clarkei damage was detected in 85% of the cassava plantations surveyed. Damage Chilomima clarkei populations can occur throughout the year but are higher during the rainy season. From 4–6 overlapping cycles can occur during the 1-year crop cycle, increasing potential damage and making control more difficult. Stem breakage can occur when there is extensive tunneling by larvae. When over 35% of the plants suffer stem breakage, yield losses range from 45–62%. Larval Cassava Pests and their Management tunneling can also lead to stem rot and a reduction in the quantity and quality of planting material. Attacks are easily detected by the presence of excreta, sawdust and exudates ejected from burrows made in infested stems. Biology and Behavior Adult females are nocturnal and oviposit in cassava stems, usually around the bud or node. The tancolored females can oviposit more than 200 eggs in a 5–6 day period. The egg stage averages 6 days (28°C). The highly mobile first instar larvae feed on the outer bark or stem epidermis. Upon finding an appropriate feeding site, usually around lateral buds, the larvae form a protective web, under which the first four instars feed, enlarging the web with each instar. Stem penetration occurs during the fifth instar larval stage. Extensive tunneling can occur as the larval cycle is completed (6–12 instars). Pupation occurs in the stem and winged adults emerge. The larval stage is 32–64 days, followed by the pupal stage (12–17 days). Female adults live 5–6 days; males, 4–5 days. Management Stemborer control is difficult once the larvae enter the stem and tunneling begins. In addition, the web formed by the early larval stages acts as a protective devise against natural enemies and pesticide applications. The mobile first instar larvae are vulnerable and more exposed to both natural enemies and pesticides. Biopesticides such as Bacillus thuringiensis (Bt) are recommended; however, with overlapping generations, several applications may be required, which would be too costly for small producers. Intercropping with maize will reduce C. clarkei populations, but only until the intercrop is harvested. Cultural practices such as selection of clean cuttings and burning plant residues, especially stems and branches, are recommended for reducing stemborer populations. Natural enemies such as hymenopteran parasitoids (Bracon sp., Apanteles sp., Brachymeria sp., Tetrastichus howardi and C Trichogramma sp.) have been identified, but their role in regulating stemborer populations has not been investigated. The fungal entomopathogens Metarhizium anisopliae and Beauveria bassiana have been identified as possible biological control agents. CIAT has worked on identifying cassava germplasm resistant to C. clarkei. More than 1,000 genotypes have been evaluated on the Colombian Caribbean coast, where C. clarkei populations are consistently high. Evaluations are based on the number of holes and tunnels and percent stem breakage. Genotypes with 0–1 holes/stem indicate varietal influence and the need for further evaluation. As natural field populations of C. clarkei are used in these evaluations, results may be misleading because genotypes exhibiting low infestation may be “escapes” (i.e., have avoided damage by chance). CIAT has initiated research to introduce insect-resistant Bt genes through Agrobacteriummediated transformation into cassava embryonic tissue to develop resistant cultivars. Scale Insects Several species of scales are reported attacking cassava stems and leaves in the Americas, Africa and Asia. Although reductions in yield due to scale attack have been reported, they are not considered to be serious pests of cassava. The most important species are Aonidonytilus albus and Saissetia miranda. Aonidonytilus albus has been reported on cassava throughout most of the cassava-growing regions in the world and is considered the most widely distributed cassava pest. It is easily disseminated from one region to another through stem cuttings, which probably accounts for its wide distribution. Damage Outbreaks are more severe during the dry season. Their incidence increases when scale-infested stem cuttings are used for planting material. High A. albus populations may cover the stem and lateral buds. Leaves on heavily infested stems yellow, and defoliation can occur. With severe 785 786 C Cassava Pests and their Management attacks the plants are stunted and stems can desiccate, leading to plant mortality. Some scale species can attack the leaves, but the greatest damage appears to be the loss of planting material. The germination of heavily infested cuttings is greatly reduced; when they do germinate, the roots are poorly developed, reducing plant vigor. Yield losses of 19% were recorded at CIAT on plants heavily infested with A. albus and there was a 50–60% loss in germination. Management The most effective means of control is through the use of clean, uninfested planting material and destroying infested plants to prevent the spread of infestation. Stem cuttings for vegetative propagation should be carefully selected from uninfested plants. The mussel-shaped A. albus grey to white female is difficult to detect, especially when populations are low and attached to stems around the lateral buds. Treating stem cuttings that have originated from fields with scale attack is highly recommended. Dipping the cuttings in a pesticide emulsion for 5 min is effective against light A. albus infestations. Heavily infested cuttings should not be sown as they will germinate poorly even if treated with a pesticide. Storing healthy cuttings with infested ones will increase dissemination and infestation as the first nymphal instars (crawlers) are highly mobile. Fruit Flies Two species of fruit flies, Anastrepha pickeli and Anastrepha manihoti (Diptera: Tephritidae:), whose origin is the Neotropics, are reported to attack cassava fruits from several regions of Central and South America. Anastrepha montei is reported infesting seed capsules in Costa Rica. Infestation of cassava fruits causes no economic damage and is of no concern to cassava producers. When oviposition occurs in the fruit, the larvae bore throughout the fruit, destroying the developing seed, which is a problem for plant breeders. With respect to damage, the tan to yellow colored females will oviposit in the tender upper portion of the cassava stem in certain areas during the rainy season. The developing larvae become stemborers, tunneling into the apical stem, which provides an entrance for soft rot bacteria such as Erwinia caratovora, resulting in severe rotting of stem tissue and apical dieback. Several larvae may be found in one stem; their presence can be noted by the white liquid exudate that flows from their tunnel. Damage is more severe on younger (2–5 months) plants. Nevertheless, the plants can recover from fruit fly damage. Yield losses have not been reported, but there is a reduction in the quality of stem cuttings for planting material. When there is severe damage to the pith region of the stem, there is a reduction in germination. Yield losses can occur if severely damaged cuttings are used as planting material. It is therefore important that only stem cuttings without damage to the pith regions be sown for vegetative propagation. Shoot Flies Damage has been observed in most of the cassavagrowing regions of the Americas but has not been reported from Africa or Asia. The most important species are Silba pendula and Neosilba perezi (Diptera: Lonchaeidae). Severe attacks have been reported from Cuba, southern Brazil and parts of Central America, especially Costa Rica. Damage Larval feeding damage is manifested by a white to brown exudate flowing from cassava growing points, which eventually die. This breaks apical dominance, retards plant growth, and causes germination of side buds which leads to excessive branching. The dark metallic blue S. pendula adults deposit eggs in the growing points between the unexpanded leaves, and the young larvae tunnel in the soft tissue, eventually killing the apical bud. Attacks may occur throughout the year but are more prevalent at the onset of the rainy seasons Cassava Pests and their Management C and on recently germinated or young plants, resulting in a reduction in growth of the stems used for planting material. Yield is seldom affected. increase were highest on peanuts and forage peanuts, followed by maize. Sweet cassava, sorghum and onions are not favorable hosts, and C. bergi could not complete its life cycle on bitter cassava. Management If plants are being grown for quality cuttings, the crop needs to be protected only during the first 3 months of growth. Usually one timely pesticide application suffices to protect the crop. Damage Cyrtomenus bergi nymphs and adults feed on cassava roots by penetrating the peel and parenchyma with their strong thin stylet, leaving fine lesions in the plant tissue. This feeding action permits the entrance of several soil-borne pathogens (e.g., Aspergillus, Diplodia, Fusarium, Genicularia, Phytophthora and Pythium spp.), causing local rot spots on the parenchyma. The brown to black lesions begin to develop within 24 h after feeding is initiated. In cassava, a quantitative scale to assess root damage was established, using a 1–5 rating based on the percentage of the parenchyma surface covered by rot lesions (1 = no damage, 2 = 1–25%, 3 = 26–50%, 4 = 51–75% and 5 = 75–100%). Studies show that even low C. bergi populations (close to zero) can cause more than 20% of the root to be covered with rot lesions. The darkened lesions on the white root parenchyma are not acceptable for the fresh consumption market; middlemen reject shipments of root with 20–30% damage, which translates into 100% loss for the farmers. Field trials in Colombia showed that damage can reach 70–80% of total roots, with more than a 50% reduction in starch content, thereby reducing the commercial value for the processing industry. As damage is not detected until roots are harvested and peeled, producers can lose the value of the crop as well as labor, time and land use. Soil-Borne Pests The majority of the arthropod pests of cassava are “source” pests, feeding on leaves and stems, which causes indirect damage by reducing root yield. Few are “sink” pests, which cause direct, irrevocable damage to the edible roots. The most important and damaging root feeders appear to be generalists, and there is a hypothesis that cyanogenic potential in cassava is a defense mechanism against them. All cassava varieties have a high cyanogenic potential in leaves, stems and root peel. It can also be theorized that the root peel acts as a protective device, especially in those varieties with low cyanogen levels in the root parenchyma. Three soil-borne pests are discussed here: the burrower bug, white grubs (several species) and root mealybugs. Cassava Burrower Bug First recorded as a pest of cassava in Colombia in 1980, Cyrtomenus bergi (Hemiptera-Heteroptera: Cydnidae) appears to be native to the Neotropics, is a polyphagous feeder that attacks a wide range of crops, and is one of the few arthropod pests that feeds on the tuberous root of cassava. Additional hosts include onions, peanuts, maize, potatoes, Arachis pintoi (forage peanuts), sorghum, sugarcane, coffee, asparagus, beans, peas, pastures and numerous weeds. It has also been reported feeding on cassava in Venezuela, Costa Rica, Panama and Brazil (states of São Paulo and Pará). Cassava is not the optimal host for C. bergi. Fecundity, survival and intrinsic rate of population Biology and Behavior Cyrtomenus bergi has five nymphal instars. It had a lifespan of 286–523 days when fed on slices of low-HCN cassava roots in the lab (23°C, 65 ± 5% RH). Egg eclosion averaged 13.5 days; mean development time of the five nymphal stages was 111 days; mean longevity for adults was 293 days. Cyrtomenus bergi is strongly attracted to moist soils, and populations can occur in the 787 788 C Cassava Pests and their Management soil throughout the crop cycle. It will migrate when soil moisture content is below 22% and is most persistent when it exceeds 31%. Thus, the rainy season greatly favors adult and nymphal survival, behavior and dispersal, whereas there is increased nymphal mortality during the dry season. Feeding preferences may be related to levels of cyanogenic glucosides in the cassava roots. Adults and nymphs that fed on high-HCN (>100 mg/kg) cultivars had longer nymphal development, reduced egg production and increased mortality. Oviposition on CMC 40 (43 mg HCN/kg) was 51 eggs/female versus only 1.3 on MCol 1684 (627 mg HCN/kg). Adult longevity on CMC 40 (235 days) was more than twice that on MCol 1684 (112 days). Additional studies indicate that the earliest instars are most susceptible to root cyanogenic potential (CNP). Due to the short length of the stylet, feeding during the first two instars is confined mainly to the root peel, whereas third to fifth instars can feed on the root parenchyma. CMC 40 has a low cyanogen level in the root parenchyma, but a high level in the root peel (707 mg HCN/kg). Feeding experiments in the lab resulted in 56% mortality of first and second instar nymphs feeding on CMC 40 and 82% for those feeding on MCol 1684. The high cyanogen level in the peel of CMC 40 is probably responsible for the high mortality. Feeding preference studies carried out in the field in Colombia show that low HCN cultivars suffer more damage than high-HCN ones. Three cassava varieties – MCol 1684 (high CPN), MMex 59 (intermediate CPN) and CMC 40 (low CPN) – were evaluated in field studies to determine the effect of CPN on C. bergi root damage. Ten months after planting, root damage on the low, intermediate and high CPN varieties was 85, 20 and 4%, respectively. These data indicate that CPN may act as a feeding deterrent and that C. bergi should not be a problem where cassava with high CNP is cultivated (i.e., northeast Brazil and many parts of Africa). However, in many cassava-producing regions, low CNP or “sweet” varieties are preferred, especially for fresh consumption or starch markets. Management Cyrtomenus bergi can be the target of extensive chemical control, given the nature of the damage it causes to cassava as well as other crops. For example, in Colombia, control of C. bergi on crops such as onions, peanuts and coriander requires considerable pesticide use, with only marginal results. In cassava, pesticide use can reduce populations and damage; however, frequent applications may be required and they are costly and often fail to reduce damage below economic injury levels. Cyrtomenus bergi control is difficult due to the polyphagous nature of the pest and its adaptation to the soil environment. As the initial damage can occur early in the crop cycle, control methods should be implemented either prior to or at planting, or during the first 2 months of crop growth. Intercropping cassava with Crotalaria sp. (sunn hemp) reduced root damage to 4% versus 61% damage in cassava monoculture. This practice also reduces cassava yields by 22%; because Crotalaria has little commercial value, this technology has not been readily adopted by producers. Recent research indicates that there is considerable potential for biological control of C. bergi. Isolates of native Colombian strains of the entomopathogenic fungi Metarhizium anisopliae and Paecilomyces sp. have been evaluated in the laboratory. An isolate of M. anisopliae infecting C. bergi in the field resulted in 61% mortality of fifth instar nymphs and an overall mortality of 33%. More recent studies with M. anisopliae strains CIAT 224 and CIAT 245 caused mortalities of 34.7% and 49.3%, respectively. Applications of M. anisopliae (Isolate CIAT 224), combined with a sublethal dose of the insecticide imidacloprid, were evaluated in the laboratory and greenhouse. Cyrtomenus bergi nymphal mortality was always significantly higher when M. anisopliae was applied in combination with imidacloprid, compared to applications of the fungus alone (80.3% vs. 34.2%). Thus, entomopathogens combined with sublethal doses of insecticides such as imidacloprid can be an effective tool in an IPM strategy for controlling C. bergi Cassava Pests and their Management or other soil-borne pests; however, field studies are required before acceptable technologies can be recommended. Several species of nematodes have been identified parasitizing C. bergi. Steinernema carpocapsae successfully infected C. bergi in the laboratory, resulting in 59% parasitism after 10 days. Strains of S. feltiae and a native species of Colombia, Heterorhabditis bacteriophora, were compared in greenhouse studies with C. bergi adults. The penetration rate for S. feltiae was 93.9%, compared to 72.1% for H. bacteriophora. However, H. bacteriophora caused higher mortality (42.2%) than S. feltiae (8.6%) after 15 days. Field studies are needed to evaluate the potential of H. bacteriophora and other nematode species in an IPM strategy. White Grubs A complex of rhizophagous white grubs (Coleoptera: Scarabaeidae) is associated with the cassava crop in many regions of the Americas, Africa and Asia. White grubs are classified as hemi-edaphic (along with ants and termites) as they spend only a portion of their life cycle in the soil. It is during their larval stages in the soil that they can damage the cassava crop; the adult scarab beetles are not reported feeding on the aboveground organs of the plant. Recent surveys in cassavagrowing regions of Colombia showed that white grubs were well represented in the edaphic communities associated with the crop. In Risaralda province, 1,858 white grubs (eight species) were collected from cassava plots. It is often difficult to distinguish the species actually causing damage to the crop. The genus commonly associated with damage to cassava in the Neotropics and Africa is Phyllophaga spp. Leucopholis rorida is reported causing damage to cassava in Indonesia and other countries in Asia. Damage Severe attacks of white grubs can destroy the stem cuttings used to establish new plantations. In one field study in Colombia there was a 95% loss in stem cutting germination due to white grub attack. C Grubs feed on the bark, pith and buds of stem cuttings, hindering germination. They also can cause plant death by feeding on the basal part of young stems. Recent studies in Colombia on Phyllophaga menetriesi with potted cassava plants under controlled conditions showed that one larva caused a 30% reduction in plant survival and three larvae per plant destroyed 50% of the plants in 56 days. White grub feeding damage has also been observed on the roots including the swollen tuberous root. Biology and Behavior Laboratory studies with P. menetriesi resulted in an average of 13 days for the egg stage and 19, 27 and 175 days for the first, second and third instars, respectively. After the third instar, the larvae entered a diapause stage averaging about 30 days, followed by a pupal stage averaging 34 days. Adults remained in the pupal chamber for about 73 days, followed by a 15-day flight period. The complete egg-to-adult cycle of P. menetriesi averaged 386 days. Phyllophaga menetriesi is mostly observed at altitudes between 1,000–1,600 m, and damage to cassava is primarily during the rainy months when the crop is planted and early growth occurs. Management White grubs populations can often be detected during land preparation prior to planting. Farmer surveys in a major cassava-growing region in Colombia (Risaralda and Quindio provinces) disclosed that 71% of the farmers applied pesticides to control soil pests, while only 14% used biological control. Biological control through the use of entomopathogenic nematodes and fungi offers promise for white grub control. A native Colombian strain of Heterorhabditis sp., when applied in high doses (10,000 infective juveniles/ml) to first and second instar larvae of P. menetriesi in lab studies, resulted in 88.3 and 83.4% mortality, respectively. In lab studies at CIAT, several isolates of M. anisopliae caused high levels of mortality of P. menetriesi. Two isolates (CIAT 515 and CIAT 418) caused 789 790 C Cassava Pests and their Management more than 60% white grub mortality. Isolate CIAT 515, in combination with a low rate of imidacloprid, resulted in 90% mortality of second instar larvae. The effectiveness of these biological control agents needs to be tested in farmers’ fields before they can be recommended as part of a white grub management strategy. Adequate control measures have not been determined for either species. Recommendations for management of S. vayssierei in the Cameroon include planting on ridges and monocropping cassava. Secondary Pests Cassava Root Mealybugs Two mealybug species have been reported feeding on and causing damage to cassava roots. In South America, Pseudococcus mandio (Hemiptera: Pseudococcidae) has been recorded from southern Brazil, Paraguay and Bolivia; it is reported as causing root damage only in Brazil. Stictococcus vayssierei (Hemiptera: Stictococcidae) is reported from the Cameroon and neighboring Central African countries. Stictococcus vayssierei is referred to in the literature as the root mealybug, the root scale or the brown root scale insect of cassava. Pseudococcus mandio can result in reduced quality of tuberous roots and cause some plant defoliation. Females have three nymphal instars, and adults oviposit an average of 300 eggs, indicating a capacity for rapid population increases. The life cycle from oviposition to adult was 25 days for females and 30 for males. Yields losses of 17% have been reported in southern Brazil. Stictococcus vayssierei larvae and adults attack young feeder roots on germinating stem cuttings, resulting in defoliation, wilting, tip dieback and plant death. Mature tuberous roots are often small, covered with mealybugs, and unattractive for the commercial market. Females (males are rare) are dark red in color, circular and flattened. Eggs are protected by wax threads secreted beneath the female body. Larvae are creamy white and mobile. Stictococcus vayssierei infestation is severest during the dry season and on unfertile, lateritic and clay soils. Infestations were more severe when cassava was planted on flat lands than when planted on ridges. Plant vigor and root yield improved by approximately 22% when planted on ridges. Intercropping favored higher mealybug infestations than cassava grown in monoculture. Numerous species of arthropods feed on cassava without causing major economic damage to the crop. These occasional or incidental pests may occur sporadically or at such low population levels that yield is not affected. If their populations increase or outbreaks occur in localized areas, some of these pests could cause yield losses. These secondary pests discussed briefly here include gall midge, termites, leaf hoppers, leaf-cutting ants and grasshoppers. Grasshoppers Zonocerus elegans and Zonocerus variegatus are potentially the most destructive of this group. They attack cassava primarily in Africa and are rarely reported feeding on cassava in the Neotropics (occasionally from Brazil). Several African countries including Nigeria, Congo, Benin, Uganda, Ivory Coast, Ghana and Central Africa report thousands of hectares of cassava defoliated in some years, probably causing yield reductions. Damage Grasshoppers feed on the leaves, causing defoliation, but during outbreaks the young tender bark can be stripped. Young plants are preferred and attacks are more severe during the dry season. Yield losses as high as 60% have been estimated. Biology and Behavior In Nigeria, grasshopper oviposition usually occurs at the onset of the rainy season; eggs hatch at the start of the dry season (6–7 months later). This population attacks cassava as the dry season progresses when other preferred herbaceous food plants become scarce. Experiments show that large Cassava Pests and their Management amounts of HCN in the leaves can act as a deterrent to grasshopper feeding. The early instars (1–4) will not consume growing cassava, while instars 5 and 6 will eat it only if deprived of other food sources. Wilted cassava leaves are readily consumed by all stages and result in a high grasshopper growth rate. Control Chemical control of grasshoppers is feasible but may not be financially or ecologically sustainable, especially for small, resource-limited farmers. It is not considered an effective mid- or long-term solution as pesticide applications may lead to a resurgence of other pests such as the cassava mealybug or the cassava green mite when their natural enemies are killed indiscriminately. Biological control with fungal entomopathogens offers a more effective long-term solution for grasshopper control. Metarhizium anisopliae var. acridum (also known as M. flavoviride), Beauveria bassiana and Entomophaga grylli have been identified infecting Z. variegatus. Efforts are currently underway to develop effective biopesticides for grasshopper control. Results with M. anisopliae have been encouraging. Gall Midges Iatrophobia brasiliensis (Diptera: Cecidomyiidae) has been recorded on cassava only in the Americas. They are considered of little economic importance and do not require control. However, the yellowish green or red galls on the upper leaf surface are highly visible to farmers, who may apply pesticides. A severe attack, especially on young plants, may cause leaf yellowing, and retarding of plant growth has been reported. Destruction of infested leaves is recommended to reduce midge populations. Leaf-cutter Ants Several species of leaf-cutter ants (genera Atta and Acromyrmex) are reported feeding on cassava in the Neotropics, especially in Brazil. Commonly reported species are Atta sexdens, Atta cephalotes C and Acromyrmex landolti. Ants cut semicircular pieces of leaves, which they carry to their underground nests. Cassava plants can be completely defoliated when a large number of worker ants attack a crop. Outbreaks occur most frequently during the early months of crop establishment, but plants usually recover from ant damage. Recent field trials in Venezuela resulted in a 55% reduction in root yield due to leaf-cutter ant defoliation. Ant nests are usually visible because of the mound of soil deposited around the hole. Control of leaf-cutter ants is difficult; toxic baits are recommended. Termites Termites are reported as pests in several cassavagrowing regions of the world, but primarily in Africa. They attack cassava mainly in the tropical lowlands, feeding on stem cuttings, feeder roots, swollen roots or growing plants. In Colombia, termites have been observed causing losses in germination as well as death of young plants, especially in regions with sandy soils. Feeding on swollen roots can lead to root rot (due to soil pathogens) damage. Losses in germination of 30% and 50% loss in stored planting material have been recorded. Control in the field is difficult, but stored planting material can be protected with an application of an insecticide dust. Leafhoppers Several species have been collected feeding on cassava. Several collections have been made by CIAT in Colombia, and numerous specimens from three families (Cicadellidae, Cixiidae and Delphacidae) are being identified. None is considered to be a pest causing yield losses, and all are usually observed in low populations. However, several of these species are being studied as possible vectors of cassava frog skin disease (CFSD), which probably originated in the Amazon regions of South America and has now spread to several countries in the region causing considerable crop loss. The disease has been described as a virus of the family Reoviridae and/or phytoplasm. Damage is characterized by the suberization and thickening of the 791 792 C Cassava Pests and their Management swollen root epidermis, resulting in low production of little commercial value. Several species have now been mass reared, and vector-transmission studies are being carried out. Future Trends and Considerations The success of an ecologically oriented IPM program for cassava requires the implementation of a strategy that minimizes or prevents chemical pesticide use. Given the increased emphasis on commercial-scale plantations, where the crop has a high commercial value, there is a tendency to apply pesticides when noticeable crop damage occurs. Pests that trigger pesticide application include the cassava hornworm, whiteflies, mites, white grubs, burrower bugs, mealybugs and thrips. Crop-protection technologies based on host plant resistance, microbial and arthropod biological control agents, together with appropriate agronomic practices, should be developed and implemented. This holistic approach has formed the basic philosophy for IPM research at international agricultural research centers such as CIAT and IITA, as well as in several national research programs such as EMBRAPA (Brazilian Agricultural Research Corp., Brasilia, Brazil), NARO (National Agricultural Research Organization, Uganda). CIAT, IITA and the Brazilian national program EMBRAPA maintain large germplasm banks that offer entomologists and breeders a potential pool for pest-resistance genes. Traditional farmers will adopt new varieties cautiously if they are adapted to local agroecological and socioeconomic conditions. New or introduced varieties should not be highly susceptible to major pests in a given region. In the Neotropics this is especially true for mites, whiteflies, thrips and mealybugs. Biological control agents have been identified for many of the cassava arthropod pests; however, the efficacy of naturally occurring biocontrol agents to maintain pests below economic damage levels has not been well documented. Classical biological control has been successful in Africa against two introduced pests from the Americas, the cassava mealybug (P. manihoti) and the green mite (M. tanajoa). Although natural biological control is probably effective in controlling some pests in the Neotropics, pest outbreaks and subsequent yield losses continue to occur. For example, the hornworm Erinnyis ello has a large complex of natural enemies including predators, parasites and pathogens; however, they are not effective in maintaining the hornworm below the economic injury level. The adult’s migratory abilities and sporadic attacks serve as a defense against the more than 30 natural enemies. The stemborer Chilomima clarkei causes considerable damage in certain regions of Colombia, but effective natural enemies have not been identified. In recent years whitefly populations and damage have increased in several regions of the Neotropics as well as in Africa, causing considerable yield reduction. Several natural enemies have been identified, but their role in a biological control program has not been determined. It should be kept in mind that in cropping systems where cassava is grown as a functional perennial, certain pests and their associated natural enemies may be in equilibrium. When cassava is grown year round in the tropics, often with overlapping cycles, pest species may be present throughout and thereby able to increase rapidly when environmental conditions become favorable to their dynamics. Natural enemy populations may not respond rapidly enough to suppress the increasing pest populations so outbreaks occur. Populations of mites, mealybugs, lacebugs and whiteflies, although present in the subtropics of the Americas, do not increase as rapidly or reach the levels of their counterparts in the tropical regions. During the “winter” months in subtropical regions, cassava will lose most or all its foliage. This can cause considerable reduction in pest populations so any increases may be retarded when warmer, more favorable, growing conditions return in the spring. Biotechnology tools offer the potential for developing improved pest-resistant cultivars and enhancing the effectiveness of natural control organisms including parasitoids and Cassava Pests and their Management entomopathogens. Wild Manihot species are a rich source of useful genes for the cultivated species M. esculenta and for resistance to pests and diseases. Their use in regular breeding programs is restricted by the long reproductive breeding cycle of cassava and “linkage drag” associated with the use of wild relatives in crop improvement. This source of resistance genes has been exploited for controlling CMD in Africa. CMD resistance was obtained by intercrossing cassava varieties with Manihot glaziovii, which resulted in interspecific hybrids that were backcrossed to cassava until CMD-resistant varieties were produced. Several wild Manihot species have been evaluated in the greenhouse and field for resistance to mites (M. tanajoa), mealybugs (P. herreni) and whiteflies (Aleurotrachelus socialis). Genotypes (accessions) of the wild species Manihot flabellifolia and Manihot peruviana displayed intermediate levels of resistance to M. tanajoa and P. herreni and high levels of resistance to A. socialis. In addition, M. tanajoa oviposition was greatly reduced when feeding on accessions of Manihot alutacea and Manihot tristis. Interspecific crosses between these wild Manihot species and M. esculenta landrace varieties have resulted in numerous interspecific progeny, which are being evaluated for pest resistance. Initial results indicate that the resistance is heritable as numerous progeny have been identified with resistance to M. tanajoa and A. socialis. Three polymorphic molecular markers for M. tanajoa that showed clear differences between resistant and susceptible individuals were identified in M. flabellifolia. A project is under way to develop low-cost tools for accelerated markeraided introgression of useful pest-resistance genes into cassava gene pools. It is predicted that cassava production in Africa, Asia and the Americas will increase considerably during the next decade. This growth will be market driven and influenced by the processing and private sectors. Cassava can provide the raw material for the animal feed, starch and bio-fuel industries, as well as remaining an important food for human consumption. Pest management will C continue to play an important role in sustaining high cassava-production levels. This will require continued research input to develop new integrated pest management (IPM) technologies. In order to meet the demand for increased cassava production, farmers will seek new higher yielding varieties. This will increase the movement of germplasm – usually vegetative stem cuttings – between regions, countries and even continents. Quarantine measures to prevent the movement of pests, especially into Asia, are an important issue. Cassava pests have shown the ability to disseminate great distances as shown by the introduction of the mite and mealybug into Africa from the Americas. There are several additional pests that could cause severe crop losses if introduced into Africa or Asia, including several mite species, lacebugs, whiteflies, stemborers, mealybugs and thrips. Moreover, what may be considered a secondary pest in the Neotropics could become a major pest outside its center of origin, as evidenced by the mealybug, P. manihoti. References Bellotti AC (2002) Arthropod pests. In: Hillocks RJ, Thresh JM, Bellotti AC (eds) Cassava: biology, production and utilization. CABI Publishing, Wallingford, Oxon, UK, pp 209–223 Bellotti AC, Arias B (2001) Host plant resistance to whiteflies with emphasis on cassava as a case study. Crop Protect 20:813–823 Bellotti AC, Riss L (1994) Cassava cyanogenic potential and resistance to pests and diseases. Acta Hortic 375:141–151 Bellotti AC, Arias B, Guzmán OL (1992) Biological control of the cassava hornworm Erinnyis ello (Lepidoptera: Sphingidae). Fla Entomol 75:506–515 Bellotti AC, Peña J, Arias B, Guerrero JM, Trujillo H, Holguín C, Ortega A (2005) Biological control of whiteflies by indigenous natural enemies for major food crops in the Neotropics. In: AndersonPK, Morales F (eds) Whitefly and whitefly-borne viruses in the tropics: building a knowledge base for global action. CIAT Publication No 341, Cali, Colombia, pp 313–323 Bellotti AC, Smith L, Lapointe SL (1999) Recent advances in cassava pest management. Ann Rev Entomol 44: 343–370 Braun AR, Bellotti AC, Guerrero JM, Wilson LT (1989) Effect of predator exclusion on cassava infested with tetranychid mites (Acari: Tetranychidae). Environ Entomol 18:711–714 793 794 C Caste Braun AR, Bellotti AC, Lozano JC (1993) Implementation of IPM for small-scale cassava farmers. In: Altieri MA (ed) Crop protection strategies for subsistence farmers. Westview, Boulder, Colorado, pp 103–115 El-Sharkawy MA (1993) Drought-tolerant cassava for Africa, Asia, and Latin America. BioScience 43:441–451 Herren HR, Neuenschwander P (1991) Biological control of cassava pests in Africa. Ann Rev Entomol 36:257–283 Holguin CM, Bellotti AC (2004) Efecto de la aplicación de insecticidas químicos en el control de la mosca blanca Aleurotrachelus socialis Bondar en el cultivo de yuca Manihot esculenta Crantz. Rev Colomb Entomol 30:37–42 Melo EL, Ortega-Ojeda CA, Gaigl A, Ehlers RV, Bellotti AC (2006) Evaluación de dos cepas comerciales de entomonematodes como agentes de control de Cyrtomenus bergi Froeschner (Hemiptera: Cydnidae). Rev Colomb Entomol 32:31–38 Neuenschwander, P (2004) Cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). In: Capinera JL (ed) Encyclopedia of entomology. Kluwer, Dordrecht, The Netherlands, pp 464–467 Ngeve JM (2003) The cassava root mealybug (Stictococcus vayssierei Richard) [Hom: Stictococcidae]: present status and future priorities in Cameroon. Afr J Root Tuber Crops 5:47–51 Onzo A, Hanna R, Sabelis MW (2005) Biological control of the cassava green mite in Africa: Impact of the predatory mite Typhlodromalus aripo. Entomol Beric 65:2–7 Yaninek JS, Onzo A, Ojo JB (1993) Continent-wide releases of Neotropical phytoseiids against the exotic cassava green mite in Africa. Exp Appl Acarol 17:145–160 Caste A form or type of individuals in social insects. Castes may be distinguished by different morphology and behavior. Castes John L. Capinera University of Florida, Gainesville, FL, USA Castes can be defined as subsets of individuals within a species that are morphologically or biologically distinct. Although “polymorphism” usually is understood to mean the occurrence of discretely different morphotypes and biologies within a species, and therefore overlaps with this definition of castes, within the social insects the term “castes” is always used to describe this condition. In social insects, there may or may not be marked differences in appearance of the subsets, but they definitely display differences in behavior and biology. An alternate term for describing the discretely different (lacking intermediate forms) intraspecific variation occurring within insects is “polyphenism.” (In contrast, phenotypes that show gradual change in response to environmental variation, without producing discretely different subsets, are called “reaction norms.”) Regulation of caste is determined by hormones, which trigger different patterns of gene expression, leading to alternative phenotypes. Ultimately, however, it is the environment, acting through hormone intermediaries, that promotes development of polyphenisms such as castes. In social insects, the castes cooperate with each other in a nest to accomplish tasks benefiting the entire colony. Some of the castes are sterile, serving as workers or soldiers to facilitate reproduction by a small number of reproductives. The sterile castes presumably have evolved through the process of kin selection. Phenotypic plasticity occurs in all organisms, and the phenotype that is expressed depends on environmental conditions. Interestingly, the environment to which the alternative phenotype is an adaptation is often not the same as the environment that induces the development of that phenotype. As noted above, some phenotypes display incremental changes in response to environmental variables. Others display discrete changes, resulting in two or more discrete alternative phenotypes. In either event, it can be advantageous to an organism to have the ability to develop multiple phenotypes without requiring genetic polymorphism. The developmental switch that leads to production of alternative phenotypes is regulated by hormones. For morphological expression of polyphenism, a molt is normally required. Thus, the developmental trigger typically is in the instar preceding the expression. Within that sensitive period when change can be triggered, often there Castes is only a brief period when hormones can alter developmental pathways. The relevant hormones generally are juvenile hormone and ecdysone, but sometimes other hormones are involved. Ants Among the ants, female castes are usually expressed as worker, soldier and queen castes. Males do not display different castes. Soldiers are often referred to as major workers, with the coexisting smaller members called minor workers. Not all castes occur in all species. Castes are determined by a number of factors, including larval nutrition, winter chilling, post-hibernation temperature, egg size, queen age, and queen influence. The function of castes or “caste polyethism” is well described by the aforementioned designations. Queens are mostly concerned with production of eggs, though early in the life of the colony the queen may perform various tasks, and some grooming of workers may occur indefinitely. Soldiers are specialized for colony defense, and often bear a large head and oversized mandibles to aid in this task. Workers repair the nest, gather food, and tend larvae and pupae, and the other colony members. Workers may also be involved in colony defense, especially the larger workers. Males exist only to fertilize queens. Temporal changes also occur over the course of the ant’s lifespan; this is called “age polyethism.” For example, young workers tend to work inside the nest, whereas older workers tend to forage outside. Over the years, some authors have recognized variants, phases, or anomalies within castes in an attempt to recognize small differences in behavior and morphology, and this has led to confusion. Castes can be defined by both morphological and behavioral characteristics, of course, and E.O. Wilson has proposed a system of caste naming that integrates both types of characters: The males play no direct role in colony maintenance, being only sperm donors. The queen or “gyne” is the principal reproductive, although “gyne” sometimes is used to include all reproductive females. She is C anatomically distinctive due to an enlarged abdomen. The worker ordinarily is a sterile female. Such females have reduced ovarioles and lack spermathecae for sperm storage. So if they eventually become reproductives, they can only reproduce parthenogenetically. The worker caste is often subdivided into subcastes such as “minor,” “media,” and “major,” and is based on size. When workers are specialized for defense, they are called soldiers. The ergatogyne is a reproductive caste intermediate between worker and queen. It can be subdivided into “intercaste” which is anatomically intermediate between workers and queens, but lacks a spermatheca so cannot mate, and “ergatoid queen” which also is intermediate but possesses a spermatheca and can replace the queen. The gamergate is not common, but occurs in a few groups of ants, and is strictly a physiological caste. In this case, the reproductive is morphologically indistinguishable from the worker, but can be inseminated and produce eggs. The most distinguishing feature of the dichthadiiform ergatogyne is that it possesses an extremely enlarged gaster, but this reproductive also has some additional minor morphological modifications. The final caste would be considered to be the temporal caste. In the temporal caste, differentiation is based solely on behavior and age. Social Bees and Wasps Among social bees and wasps, the more primitively eusocial groups lack mophological differences but display different behaviors. More interesting is the general lack of the worker subcastes such as those that are found in ants and termites. This is despite the fact that bees and wasps, at least the species with very large colonies, display a sophisticated division of labor (polyethism). In bees and wasps, however, the division of labor is based less on production of castes, and more on temporal polyethism. In temporal polyethism the same individual passes through different stages of specialization as it grows older. Some differences 795 796 C Castes exist based on size, however, with larger individuals tending to forage more and smaller individuals tending to conduct nest work and brood care. In social bees and wasps, there is a correlation between caste evolution and colony size. E.O. Wilson divides this into four steps: 1. 2. 3. 4. Colony size of 2–50 adults – the females are semisocial or begin life as workers and later become egg layers. Colony size of 10–400 adults – externally, the queen is still identical to the worker caste, but there is functional differentiation of the worker caste from the queen. The egg-laying females maintain the workers in a subordinate position by aggressive dominance behavior. This can be expressed by the stealing and eating of eggs laid by rivals. Temporal poyethism is weakly developed among workers. Colony size of 100–5,000 adults – some external differentiation of queens and workers is evident, and this is under the control of nurse workers that feed larvae differently. Queens do not display dominance behavior. Temporal polyethism is weak among workers. Colony size of 300–80,000 adults – queen and worker dimorphism is strong. Queen dominance is absent and queens maintain control with pheromones. Temporal polyethism is strongly developed among workers. Termites Superficially, termites and ants have similar caste systems. However, these taxa are phylogenetically remote from each other, and careful examination shows some important differences, so it is clear that sociality and caste systems evolved separately in Hymenoptera and in Isoptera. Both ants and termites have evolved a soldier caste with specialized head structure and behavior, and both are populated primarily by similarlooking but behaviorally versatile workers. Their systems of temporal polyethism also are similar. Termites differ, however, in that males do not exist solely for fertilization. Termite workers can be either sex, whereas in the holometabolous social insects (ants, bees, wasps) the workers are always female. Also, termite immatures are workers, whereas immatures of the other social insects require continual care by adult workers. Termite castes have some unique features. In the lower termites, the reproductives secrete sexspecific pheromones that inhibit metamorphosis of the immatures into additional reproductives. Termites also are capable of producing “supplementary reproductives.” If the primary reproductives are removed, fertile but wingless individuals of both sexes develop in the colony. Thus, termite colonies display “immortality”; they may never completely perish because reproductives can be generated as necessary. Termite soldiers seem to be capable of suppressing the development of workers into soldiers, maintaining a larger number of termites arrested in the worker stage, probably to the benefit of the colony. The classification of termite castes is as follows: The larva (a wingless nymph, as these are hemimetabolous insects) lacks evidence of wings and of the features that characterize soldiers. The nymph (brachypterous nymphs) develops from the larval stage but possesses wing buds initially, and wing pads after some molts. Eye differentiation also occurs at this stage. A worker stage occurs in the higher termites, but not the lower. Workers lack wings, and eyes are reduced or lacking. The head and mandibles are well developed. Lacking the worker stage, the lower termites have instead a stage called pseudergate. Pseudergates develop from nymphal stages or larvae. Soldiers have morphological features that are specialized for defense. This includes large mandibles, large heads, and glands capable of discharging defensive secretion. Primary reproductives are derived from colony-founding queens and males. If the primary reproductives are removed from the colony, often supplementary reproductives can appear. The supplementary reproductives take three forms: (i) the adultoid reproductive, found in the higher termites only, which appears identical to the primary reproductive and may already exist but changes behavior in the absence of the primary reproductive; (ii) the nymphoid reproductive is a Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) supplementary male or female derived from a nymph and retaining wing buds; (iii) the ergatoid reproductive is also a supplementary male or female, but is larval in form and lacks wing buds. The primary reproductives construct an initial cell and rear the first brood, providing them not only with food but the protozoans necessary for independent feeding on cellulose. The first brood workers (or worker-like pseudergates or nymphs) soon take over responsibilities for foraging, nest construction and nursing. The queen and male become specialized reproductive organisms. Interestingly, the worker caste is morphologically uniform but behaviorally diverse when species are compared. The soldier caste is morphologically diverse but behaviorally uniform. Soldiers can use their mandibles effectively in defense against insects their own size, or in the case of those practicing chemical defense, their glands can secrete or spray a number of bioactive substances to deter intruders.  Polyphenism  Termites  Bees  Ants C Nijhout HF (1999) Control mechanisms of polyphenic development insects. Bioscience 49:181–192 Wilson EO (1971) The insect societies. Belknap Press, Cambridge, MA, 548 pp Zhou X, Oi FM, Scharf ME (2006) Social exploitation of hexamermin: RNAi reveals a major cast-regulatory factor in termites. Proc Natl Acad Sci 103:4499–4504 Castniidae A family of moths (order Lepidoptera) also known as giant butterfly moths.  Giant Butterfly Moths  Butterflies and Moths Caterpillar The larva of a butterfly, moth (Fig. 29), sawfly, and some scorpionflies. Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) nanCy C. hinkLe1, phiLip G. koehLer2 1 University of Georgia, Athens, GA, USA 2 University of Florida, Gainesville, FL, USA References Ananthakrishnan TN, Whitman D (eds) (2005) Insect phenotypic plasticity. Diversity of responses. Science Publishers, Enfield, New Hampshire, 213 pp Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Cambridge, MA, 732 pp Miura T (2004) Proximate mechanisms and evolution of caste polyphenism in social insects: from sociality to genes. Ecol Res 19:141–148 Miura T (2005) Developmental regulation of caste-specific characters in social insect polyphenism. Evol Dev 7:122–129 Cat fleas are the most common ectoparasite on both dogs and cats in North America. These small (2 mm), reddish brown, wingless insects have bodies that are laterally compressed (i.e., flattened side-to-side) and covered with many backwardprojecting spines, making them, like a cocklebur, difficult to remove from the animal’s coat. Their anal spine head thoracic legs prolegs Caterpillar, Figure 29 Lateral view of a moth caterpillar (Lepidoptera: Sphingidae). 797 798 C Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) hind legs are long and well adapted for jumping. Adult fleas feed exclusively on blood and their mouthparts are equipped for sucking blood from the host. Cat fleas attack a variety of warm-blooded hosts, including humans and pets, making them both a veterinary problem and household pest. Although cat fleas have been collected from more than 30 species of urban and suburban wildlife, most of these animals are not satisfactory hosts. Cat fleas do not commonly serve as disease agent vectors. However, they are capable of transmitting the causative agents of flea-borne typhus (Rickettsia typhi) and cat scratch disease (Bartonella henselae). The cat flea is the intermediate host for the dog tapeworm, Dipylidium caninum, which can affect small children as well as dogs and cats. It is supposedly capable of transmitting plague (Yersinia pestis), but has been important in epidemic situations only outside the U.S. Probably the most common flea symptom is that pets bite and scratch themselves repeatedly. Severely flea-infested puppies and kittens risk lifethreatening anemia. Sensitized people suffer pruritus stimulated by antigens in flea saliva, and resultant scratching opens the skin to infection. Flea saliva has been described as one of the most irritating substances known to man, and very small amounts cause great irritation and itching. Flea allergy dermatitis (FAD) is a severe condition found primarily in dogs, but also occasionally seen in cats. In a flea-allergic animal, flea salivary antigens stimulate intense itching that results in self-inflicted trauma such as scratching and biting. Affected animals display obsessive grooming behavior, hair loss, and weeping sores with secondary infection. Until successful FAD immunotherapy is developed, treatment involves flea elimination from the animal’s environment and flea bite prevention. But only one bite can stimulate a full cascade of symptoms in sensitive animals. Fleas and their associated diseases can constitute over half a veterinary practice’s caseload in some regions. More energy and money are spent battling these insects than any other problem in veterinary medicine. The cat flea is a cosmopolitan, eclectic species, having been recorded from over three dozen species, including opossums, raccoons, skunks, coyotes, and even birds. Infested wildlife can move flea infestations from infested premises to previously noninfested areas. The combination of wide host range and movement of fleas by urban wildlife explain the fleas’ ability to repopulate domestic animals following suppression efforts. Because it lacks host specificity and tends to feed on humans, the cat flea is a pest of both companion animals and their homes. Once adult cat fleas locate a host, they tend to remain on that animal unless dislodged. They feed readily, taking several blood meals every day. They not only feed, but mate and lay eggs while on the host, unlike rat fleas that hide in rodent burrows between blood meals. Flea eggs (Fig. 30) are not sticky so they readily fall off into the host’s environment, with large numbers accumulating in areas frequented by the animal. Scratching caused by saliva in flea bites speeds the drop of eggs from the host. Once the adult flea finds a host, it begins to feed. The female mates and begins oviposition within a couple of days. On the host, a female flea averages about one egg per hour and, as a female flea can live on the host for several weeks, potential production can amount to hundreds of eggs in her lifetime. Only the adult stage is parasitic; all other life stages develop off the host. Cat flea eggs are approximately one mm in length, with little surface structure. Typically eggs hatch within 24–48 h following oviposition, with more rapid hatching at warm temperatures. Small, white, eyeless, legless larvae emerge from the eggs with chewing mouthparts. They graze through their habitat, feeding on organic debris and adult flea feces (partially digested blood). As they seldom travel far from where they hatch, cat flea larvae are usually found in furniture, carpeting, or outside in areas frequented by host animals. In efforts to avoid light, flea larvae typically burrow deep into carpet or, outdoors, into duff. Flea larvae are highly subject to desiccation and dry out rapidly. Humidity over 50% in the larval environment is essential for development, Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) C Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae), Figure 30 The cat flea life cycle: (left) a flea egg is not sticky so readily falls from the host and hatches a few days later; (second from left) flea larvae coil when disturbed; (third from left) within the cocoon the larva completes development through the pupal stage to an adult flea; (right) adult fleas feed exclusively on blood. and this susceptibility to heat and desiccation makes it unlikely that flea larvae survive outdoors in sun-exposed areas. Because hosts prefer shaded areas, flea eggs are more likely to be deposited in shade, and flea larvae develop where the ground is shaded and moist. Likewise, indoors flea larvae are protected under the carpet canopy where air movement is minimized and humidity is highest. Most flea larvae, therefore, tend to be located in areas where pets spend most of their time. Under favorable conditions, flea larvae can complete development in as little as 10 days. Cool temperatures, food shortages, or other unsuitable environmental conditions may extend larval developmental time to several weeks or a month. In areas like south to central Florida, flea larvae can develop outdoors from egg to pupal stage, even during the winter months of November to March, due to the mild temperatures and high humidity. When mature, the larva locates an appropriate site for pupation and spins a silk cocoon to which adheres environmental debris, making the cocoon appear as a small dirt clod or lint ball. Within its cocoon, the larva molts to the pupa and continues metamorphosis, becoming an adult flea within about 4 days under favorable conditions. The pre-emerged adult stadium has the most variable length of any stage in the flea life cycle, ranging from days to several months (or perhaps over a year). The pre-emerged adult flea within the cocoon is more resistant to desiccation than either eggs or larvae. Stimuli such as pressure, carbon dioxide, and warmth (triggers associated with mammalian hosts) cause adult fleas to emerge from their cocoons. This emergence from the cocoon causes many problems in homes and apartments where infested pets previously lived. When the hosts are removed from a residence, the eggs and larvae all develop to the pre-emerged adult stage, waiting for a host. As soon as a new resident occupies the house, thousands of fleas emerge at once, stimulated by the movement, warmth, and carbon dioxide. Emergence of these adults from their protective cocoons may persist for 3–6 weeks despite all efforts to control them. Most fleas emerge within a couple of weeks following cocoon formation. Upon emergence, the flea can survive for approximately 7–10 days (or longer under high humidity and low temperature conditions) if it does not locate a host. Because fleas must have blood from a mammal host to survive, treating host animals to use them as “bait” is the most efficient and successful suppression tactic. There are several on-animal products that are effective for flea control. Many contain pyrethrins, which are safe, effective products but kill only fleas on the animal at time 799 800 C Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae), Figure 31 Fleas are ornamented with spines and combs that help anchor them in the host’s coat. of treatment and do not provide residual control. Other over-the-counter compounds include spot-on permethrin products, which are limited to canine use as they can be lethal to cats. Veterinarians can prescribe products that provide several weeks of control with a single application. These are applied in a small volume (a few milliliters) on the back of the animal’s neck and distribute over the body surface in skin oils. In addition to spot-on formulations, some products are available as sprays. These adulticides kill fleas on the animal within a few hours, then provide residual flea suppression for several weeks. After pets are treated, fleas will continue to emerge and hop onto the animal; the host will “harvest” fleas from the surrounding environment until they have been killed and no more are emerging. Because it will take a while for fleas in the Caudate environment to die off, some fleas may be seen on the animals for up to a month following treatment, but that does not indicate product ineffectiveness. When used prior to flea population build up, insect growth regulators can break the flea life cycle. While these compounds do not kill adult fleas, they do prevent eggs and larvae from completing development, ensuring that any fleas brought into the area will not establish a sustaining population. Due to their wide host range, fleas can continually move into homes and reinfest. Homes without pets can develop severe cat flea problems if wild or feral animals (raccoons, opossums, skunks, etc.) nest in the crawl space or attic and share their fleas. Typically migrants den under the structure in the spring; as their young abandon the nest, fleas left behind climb up through subflooring, seeking a blood meal from any warm-blooded host. Excluding potential carriers from the property will reduce opportunities for reinfestation. Sanitation is an important flea suppression tactic; by eliminating larval development sites and destroying immature stages before they develop to the pestiferous adult stage (Fig. 31), pets and people can be protected from fleas. Areas frequented by pets accumulate flea eggs and larval food, so these microhabitats should be vacuumed and treated with insect growth regulators or borate products to prevent flea infestations. Such areas include under furniture, animal bedding and sleeping quarters, and utility rooms or other locations where the pet spends time.  Fleas C Cattle Grub, Hypoderma spp. (Diptera: Oestridae) Livestock-infesting flies that migrate through the host’s body.  Myiasis  Veterinary Pests and their Management Cattle Ticks Several ticks can be important parasites of cattle.  Ticks  Area-Wide Pest Management Cauda The pointed tip of the abdomen, the modified ninth abdominal tergum, in aphids. It is sometimes called the “tail.”  Abdomen of Hexapods Caudal Pertaining to the anal end of the body. Caudal Filaments Thread-like processes at the tip of the abdomen (Fig. 32), often referred to as “tails” by nonentomologists.  Abdomen of Hexapods References Durden LA, Traub R (2002) Fleas (Siphonaptera). In: Mullen GR, Durden LA (eds) Medical and veterinary entomology. Academic Press, San Diego, CA Dryden MW, Broce AB, Cawthra J, Gnad D (1995) Urban wildlife as reservoirs of cat fleas, Ctenocephalides felis. In: American Association of Veterinary Parasitologists, 40th Annual Meeting. Pittsburgh, PA, p 65 Holland GP (1964) Evolution, classification, and host relationships of Siphonaptera. Ann Rev Entomol 9:123–146 Rust MK, Dryden MW (1997) The biology, ecology, and management of the cat flea. Ann Rev Entomol 42:451–473 Caudal Lamellae The caudal gills of damselflies. Caudate Having a tail-like process at the anal end of the body. 801 802 C Caudell, Andrew Nelson Maxillary palpus Antenna Compound eye Median ocellus Labrum Maxilla Labial palpus Labium Pronotum Mesonotum Metanotum Style Coxa Trochanter Femur Tibia Tarsus Pretarsus Abdominal appendage II Eversible sac Lateral caudal filament (cercus) Median caudal filament Caudal Filaments, Figure 32 Dorsal (left) and ventral (right) view of a silverfish (Collembola). Caudell, Andrew Nelson Andrew Caudell was born in Indianapolis on August 18, 1872, and moved with his parents to a farm in Oklahoma where he grew up. He became interested in insects and later studied at Oklahoma Agricultural College. After a brief employment in Massachusetts with the Gypsy Moth Project, in 1898 he joined the U.S. Department of Agriculture, studied Orthoptera, and became custodian of Orthoptera at the U.S. National Museum. Study of this group of insects, but including Zoraptera, became his life’s work, and he published numerous papers on it. His other accomplishments included being president of the Entomological Society of Washington in 1915, and publishing with Nathan Banks “The Entomological Code. A code of nomenclature for use in entomology”. Married, and with one daughter, he died on March 1, 1936. Reference Mallis A (1971)Andrew Nelson Caudell. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 198–200 Cave Adapted Insects C Cave Adapted Insects steven J. tayLor Illinois Natural History Survey, Champaign, IL, USA Insects inhabit nearly every conceivable habitat on earth and often exhibit unique adaptations corresponding to these environments. Caves are certainly among the more unusual and fascinating of these habitats. Insects and other organisms living in caves have evolved to deal with a set of unique environmental conditions, and the species of cave inhabiting insects vary in the degree to which they are limited to life in caves. Species that must spend their entire lives within caves are called troglobites. Environmental conditions typical of habitat deep within caves include: · · · · Complete absence of light Stable and usually very high (>95%) humidity Relatively low levels of available nutrients Nearly constant temperature Troglobites are among the most interesting of the cave-adapted species. Because they live in the absence of light, many troglobitic insects have non-functional eyes. Most commonly, this is evidenced by the reduction or even complete loss of the compound eyes. Instead, troglobitic insects may have greatly elongated antennae and legs (Fig. 33) relative to their nearest epigean (aboveground) relatives. Equipped with elongate setae, these appendages allow the insects to detect nearby potential prey or predators in the absence of light. Troglobitic insects also may be particularly attuned to detecting vibrations and chemosensory cues. There is little selective pressure for elaborate coloration (camouflage, warning coloration) in the absence of light, and, as a result, many troglobitic insects are whitish or pale brown in coloration. The high humidity of the caves, often in excess of 98%, means that moisture retention is less of a problem than in many epigean habitats. Consequently, many cave insects have a thinner, less waxy cuticle Cave Adapted Insects, Figure 33 Haedonoecus subterraneus (Orthoptera: Rhaphidophoridae), adult female. Note extremely long legs, palps, and antennae – adaptations that are advantageous in a cave. (Source: Packard AS (1888) Cave fauna of North America. Memoirs Natl Acad Sci 4:1–156 + 27 plates.) than their nearest surface relatives, further enhancing the often pale appearance we associate with cave-adapted animals. Perhaps the most important aspect of cave life relating to the absence of light is its effect on the availability of energy. In the dark zone of caves there are no primary producers – no photosynthesizing plants. Interesting exceptions to this do occur, but by and large, cave communities depend on organic debris that falls or washes into caves, the bodies of organisms that accidentally fall or wander into caves, and fecal material and sometimes the bodies, eggs, or young of trogloxenes (species that live in caves but must leave the cave for part of their life cycle) that bring in energy from outside the caves, such as bats and cave crickets. The cave community, then, is basically a decomposer community. In many caves, insects play important roles in this community. The relatively low levels of energy available in many caves means that life is sparse, and, consequently, predators are rare. In comparison to their surface kin, troglobitic insects often move more slowly, live longer, and produce fewer and larger eggs, all adaptations to deal with the lower energy levels of the cave environment. For example, the European catopid cave beetle, Speonomus longicornis, may live more than 3 years. 803 804 C Cave Adapted Insects The near constant conditions in the cave usually mean that troglobites do not have very pronounced circadian rhythms of activity. This does not, however, mean that there are no environmental cues to indicate the passing of days or seasons. Many caves “breathe,” taking in air or releasing it as the barometric pressure changes or as the temperature above ground rises and falls. The movements of trogloxenes, such as cave crickets and bats, also may be informative to the cavelimited species. Seasonal flooding of cave streams also can provide information about seasons (as well as provide an influx of new nutrients). What specific organisms, then, live under the above environmental conditions and exhibit these sorts of adaptations? The hexapod order Collembola (Springtails) contains many troglobites; a few of the genera with cave-inhabiting species include Pseudosinella, Onychiurus, and Folsomia. These tiny organisms feed on minute organic debris and the ubiquitous fungi that break down leaf litter, twigs, and fecal material. Springtails sometimes are found on the surface film of drip pools on cave floors (e.g., some Arrhopalites species). Troglobitic springtails are sometimes present in large numbers, visible to us as tiny white flecks moving about on the substrate. Trogloxenic cave or camel crickets of the genus Ceuthophilus are one of the more prominent insect inhabitants of many Nearctic caves. These orthopterans roost in caves, usually high on walls or on ceilings where they are less susceptible to predation by cave visitors such as mice and raccoons. At night, some portion of the cave’s population of Ceuthophilus sp. will emerge from the cave (often about dusk) to forage for food above ground. Most cave-inhabiting Ceuthophilus species exhibit adaptations that suit them both for their nighttime excursions (mottled brown and black coloration, large powerful legs for jumping out of harm’s way) and for life in the cave (most notably, their long, attenuated appendages, especially the antennae). Other genera of Rhaphidophoridae occur in caves in the United States (e.g., Haedonoecus), in Europe (e.g., Troglophilus), in Australia and New Zealand (where cave-dwelling species of Gymnoplectron and other genera are known as “cave wetas”) and elsewhere. The feces of the roosting crickets provide food for other cave organisms, and the adult female crickets typically deposit their eggs in the protection of the cave, inserting their ovipositor into the soft sandy cave soils. These eggs, of course, are a dense source of nutrients, and in some areas there are troblobitic beetles of the family Carabidae. In the United States, common beetle genera that are cave cricket (Ceuthophilus, and the more caveadapted but less widespread Haedonoecus) egg predators include ground beetles of the genera Rhadine and Neaphaenops (Fig. 34). Troglobitic carabid beetles are often a pale rusty red in color, and the more cave-adapted species have no eyes, or compound eyes reduced to only a few facets. Some cave-adapted carabid predators of cricket eggs have a narrowed and elongated head and Cave Adapted Insects, Figure 34 Neaphaenops tellkampfi, a cave cricket egg predator found in some Kentucky, USA, caves. (Source: Packard AS (1888) Cave fauna of North America. Memoirs Natl Acad Sci 4:1–156 + 27 plates.) Cave Adapted Insects thorax, which presumably facilitate reaching deep into holes where cricket eggs may be found. The Coleoptera are one of the most successful insect orders in caves, especially the families Carabide, Leiodidae, and Staphylinidae. The first cave invertebrate to be described (in 1832) was a carabid beetle, Leptodirus hohenwarti (Fig. 35), in Europe. Many of the troglobitic carabids (ground beetles) are predators. The North American carabid genera Rhadine and Neaphaenops contain troglobitic species that may spend many hours searching for the eggs, which they extract from the ground and consume. Psudanophthalmus is another carabid beetle genus frequently found in caves of the eastern United States, where they feed on a variety of different things. Southern European caves harbor an unusually diverse cave carabid fauna. Another group of beetles with some success in the cave environment is the rove beetles (Staphylinidae). While significantly fewer species of staphylinids are troglobites, they commonly are Cave Adapted Insects, Figure 35 Leptodirus hohenwarti Schmidt, 1832. (Source: Jeannel (1949) Reprinted in Vandel, A (1965) Biospeloeology: the biology of caverniculous animals. Pergamon Press, New York, NY, 524 pp) C found in caves, especially in the Mediterranean region. In the United States, the staphylinid Quedius spelaeus frequently is encountered, especially in association with cave stream riparian zones and leaf litter. One rather distinctive looking group of rove beetles, the Pselaphinae (mold beetles), contains a number of very small, narrowly endemic troglobitic species of Batrisodes, found in caves of south-central Texas. Round fungus beetles (Leiodidae) of the genus Ptomophagus include several troglobitic species in North America. A surprising number of flies are found in caves. Most famously, the larvae of the New Zealand cave glow-worm (Arachnocampa luminosa, Mycetophilidae) are found on the ceilings of sometimes spacious caverns. They are bioluminescent, and dangle sticky threads down from the ceiling which capture prey items attracted to the light. In the United States, the predatory larva of the mycetophilid Macrocera nobilis, commonly known as the “monorail worm,” also makes sticky, web-like structures on walls and floors of caves and moves effectively both forward and backward along these narrow strands. In temperate North American caves, adults of several species of troglophilic heleomyzid flies commonly are found on cave walls and ceilings. Another common cave fly in the eastern United States is Megaselia cavernicola (Phoridae). In the winter, it is not unusual to encounter large numbers of mosquitoes (Culicidae) overwintering in the relatively stable and moderate conditions of a cave. This brief look at cave insects certainly does not represent the true diversity of taxa and interesting adaptations that exist. While some of the more common inhabitants of temperate North American caves are emphasized here, the fauna of tropical caves has been short-changed, as have the incredible faunas of the lava tubes of the Canary and Hawaiian islands, where pale, stilt-legged emisine reduviids stalk their prey and cixid hemipterans feed on tree roots and produce vibratory signals intended for potential mates. Nor have the other arthropods found in caves been discussed. These include an amazing array of 805 806 C Cave Habitat Colonization arachnids (spiders, mites, opilionids, ricinuliids, etc.) and, especially in aquatic habitats, crustaceans (copepods, crabs, crayfish, isopods, amphipods, etc.). The citations below serve as an introduction to the large body of literature on cave invertebrates.  Cave Habitat Colonization References Camacho AI (ed) (1992) The natural history of biospeleology. Monografias Museo Nacional de Ciencias Naturales, Madrid, Spain, 680 pp Chapman P (1993) Caves and cave life. HarperCollins, London, UK, 224 pp Culver DC (1982) Cave life evolution and ecology. Harvard University Press, Cambridge, MA, 189 pp Mohr CE, Poulson TL (1966) The life of the cave. McGrawHill, New York, NY, 232 pp Vandel A (1965) Biospeloeology: the biology of caverniculous animals. Pergamon Press, New York, NY, 524 pp Cave Habitat Colonization david sLaney, phiLip weinstein Wellington School of Medicine and Health Sciences, Wellington, New Zealand Over the centuries people have keenly studied the animals found in the sea, in rivers, and on the land, but little attention has focused on animals that inhabit caves. The ancient Greeks believed that caves were the abode of the dead, and this may have led to the belief that caves could not possibly harbor life. However, large numbers of cave dwelling animals representing a wide diversity of groups, such as insects, millipedes, amphipods, isopods, fish, and spiders, have been described over the last 200 years. The first published work on biospeleology appeared in 1845, by the Danish zoologist, J.C. Schiödte, describing animals he collected from caves in Italy. Thereafter, biospeleological research began in earnest, focusing on European and North American temperate caves. One of the key questions that researchers have debated over the last 150 years is how animals came to live in caves, and how they have subsequently evolved. These two processes, cave colonization and speciation, are frequently confused in the literature. Here we describe models of cave colonization, and refer the reader to Taylor (this volume) and references below for further details on speciation. One of the first modern hypotheses for the origin of cave organisms was that of Vandel (1965), who put forward the “Pleistocene-effect” model for the evolution of terrestrial troglobites (obligate cave dwellers) in temperate regions. This model has also been termed the “relictual,” “isolation,” “refugium” or “climate-relict” model. Vandel proposed that troglobites evolved allopatrically from epigean (surface dwelling) species, which had adapted to the cool climatic conditions of the Pleistocene ice ages (1.5 million–10,000 years ago). When the glaciers retreated, these organisms were subsequently restricted to more favorable climatic habitats, such as deep wooded ravines, cool and moist forest floors and caves. Over time, with continued climatic variability and subsequent surface habitat changes, the epigean populations became extinct. Under this model the resulting geographic isolation of cave populations leads to the allopatric speciation of cave dwelling organisms. Vandel’s model has been the traditional view for the origin of cave populations, especially in temperate regions such as Europe and North America where major climatic changes during the Pleistocene have occurred. But what about tropical caves? Biological investigation of the worlds’ tropical caves did not receive much attention until the 1970s. Before this, scientists working in the Pleistocene-effect paradigm believed that troglobites were virtually nonexistent in tropical caves. The paucity of troglobites in these regions was explained by the lack of past climatic extremes required to restrict epigean populations to cave habitats. However, since the 70s both the discovery of large numbers of terrestrial troglobites in tropical regions such as Australia, the Canary and Galápagos Islands, Hawaii, and Cave Habitat Colonization Jamaica, combined with the mounting evidence that significant past climatic fluctuations occurred in much of the world during the Pleistocene, has made biologists reconsider the evolutionary origins of troglobites in the tropics. For example, it is postulated that cavernicolous species of cockroaches in North Queensland have arisen as a result of isolation in moist refugia during periods of increasing aridity in Australia in the late Cenozoic. In 1973 Howarth proposed the “adaptive-shift” model to account for the origin of tropical troglobites in lava tubes of the Hawaiian Islands where epigean congeners of the cave dwelling species have been found. This model has also been termed the “local habitat shift” or “invasion” model. Howarth proposed that pre-adapted species move into newly developed cave habitats to exploit the resources not otherwise available on the surface, with troglobites evolving parapatrically or sympatrically through an adaptive-shift rather than by isolation induced by climatic change. Under this model caves do not act as refugia from episodic climatic changes, instead their colonization is a continuing process. Speciation follows as a result of isolation of organisms brought about by an adaptive-shift, and does not relate directly to climate change. As with Vandel’s model, Howarth’s model incorporates both processes of colonization and of speciation. A related model to the adaptive-shift model is the “active colonization” model put forward by members of the Laboratoire Souterrain du CNRS in France, which applies to temperate as well as tropical caves. In addition to cave habitats, the researchers have studied the colonization of interstitial voids found in soil and screes (termed the “milieu souterrain superficiel” or superficial hypogean compartment). They suggest that climatic events may not be the primary factors of cave colonization, but that colonization is an active phenomenon in new biotypes. Climatic changes are considered as a localized model, with organisms colonizing caves as a result of a number of biological interactions. This model is a C variant of Howarth’s adaptive-shift theory, but includes the possibility of subsequent events, including climatic changes, leading to speciation. The biological interactions that lead to colonization may include invasion as an immediate refuge from surface abiotic stresses, opportunism (caves as new niches to be colonized) or a result of competition or predation pressure in surface habitats. Hypotheses for the evolution of subterranean organisms are still debated today, with a regular re-elaboration of the fundamental scenarios described above. To date research evidence has failed to falsify any alternative models, and no generalized single theory has been put forward. The origin of a particular cave dwelling organism should perhaps best be interpreted based on the evidence that explains the origin of that organism, and may invoke a combination of biological and or abiotic factors leading to colonization (and speciation) in those individual circumstances.  Cave Adapted Insects References Barr TC Jr (1968) Cave ecology and the evolution of troglobites. Evol Biol 2:35–102 Culver DC (1982) Cave life: evolution and ecology. Harvard University Press, Cambridge, MA Howarth FG (1973) The cavernicolous fauna of Hawaiian lava tubes. Pacific J Insects 15:139–151 Howarth FG (1987) The evolution of non-relictual tropical troglobites. Int J Speleology 16:1–16 Rouch R, Danielopol DL (1987) L’ origine de la faune aquatique souterraine, entre le paradigme du refuge et le modéle de la colonisation active. Stygologia 3:345–372 Slaney DP (2001) New species of Australian cockroaches in the genus Paratemnopteryx Saussure (Blattaria, Blattellidae, Blattellinae), and a discussion of some behavioural observations with respect to the evolution and ecology of cave life. J Nat Hist 35:1001–1012 Vandel A (1965) Biospeleology: the biology of cavernicolous animals (translated by Freeman BE). Pergamon Press, Oxford, UK, 524 pp Weinstein P (1994) Behavioural ecology of tropical cave cockroaches: preliminary field studies with evolutionary implications. J Aust Entomol Soc 33:367–370 807 808 C Cayenne Tick, Amblyomma cajennense Fabricius (Ixodida: Ixodidae) Cayenne Tick, Amblyomma cajennense Fabricius (Ixodida: Ixodidae) This disease vector is found throughout the Americas.  Ticks cDNA The double-stranded DNA copy of a eukaryotic messenger RNA molecule, produced in vitro by enzymatic synthesis and used for production of cDNA libraries or probes for isolating genes in genomic libraries. cDNA Library A collection of clones containing dsDNA that is complementary to the mRNA. Such clones lack introns and regulatory regions of eukaryotic genes. Once cDNA molecules are transcribed, they are inserted into a vector and amplified in E. coli. Cecidomyiidae A family of flies (order Diptera). They commonly are known as gall midges.  Flies  Gall Midges (Diptera: Cecidomyiidae) Cecidosidae A family of moths (order Lepidoptera). They also are known as gall moths.  Gall Moths  Butterflies and Moths Cedar Beetles Members of the family Callirhipidae (order Coleoptera).  Beetles Cell The fundamental unit of life. Each multicelled organism is composed of cells. Cells may be organized into organs that are relatively autonomous but cooperate in the functioning of the organism. This term also is used to describe any area of a wing that is between or bounded by veins. Wing cells are named after the vein forming the upper margin, and are numbered from the base outward. Cell Culture The growing of cells in vitro, or in an artificial container rather than in an organism. Cell Culture of Insects Jun mitsuhashi Tokyo University of Agriculture, Tokyo, Japan Insect tissue culture was initiated by R. Goldschmidt in 1915. He cultured spermatocytes of Hyalophora cecropia (Lepidoptera: Saturniidae) in hemolymph of the same species. He could maintain the spermatocytes for more than 3 weeks, and observed spermatogenesis in vitro. His culture may be taken as organ culture, because he did not aim to proliferate cultured cells. Later, W. Trager (1935) established standard methods for insect cell culture. He devised media proper for insect cell culture, and with it he successively cultured Bombyx mori (Lepidoptera: Bombycidae) ovarian cells for several weeks. In 1956, Wyatt formulated a synthetic medium based on the chemical composition of insect hemolymph. The composition of her medium is still used at present as the base of formulation of new media. In 1962, the first insect continuous cell line (a cell population which continues to proliferate unlimitedly) was established by Grace. He obtained permanently growing cells from the culture of the Cell Culture of Insects ovarian cells of Antheraea eucalypti (Lepidoptera: Saturniidae). Since then, more than 400 insect cell lines have been established. They include 172 dipteran cell lines (115 from Drosophila melanogaster and 47 from 22 mosquito species), 147 lepidopteran cell lines, 16 coleopteran cell lines, 15 hemipteran cell lines, 13 hymenopteran cell lines, 11 blattarian cell lines, and 1 orthopteran cell line. The history of insect tissue culture development before 1962 was reviewed by Day and Grace (1959). Standard methods to initiate primary culture of insect tissues are as follows: The insects used should be aseptic or surface-sterilized. Tissues or organs to be cultured are excised under sterile conditions. The excised tissues or organs are washed in saline, and cut into small pieces. The resulting tissue fragments are washed again, and transferred into culture flasks with culture medium (explant culture). In some cases, especially D. melanogaster cell culture, excised tissues are often dissociated further into single cells by means of partial digestion with an enzyme, and are seeded as separated single cells. Generally, explant culture is common in insect cell culture, and gives better results. At present, techniques for insect cell culture are far from one which enables scientists to make cell culture from any tissue of any species, and improvement of the techniques continues. In explant culture, cell migration from explants begins soon after the culture is established. These migrated cells generally consist of epithelial-like, fibroblast-like and hemocyte-like cells. The epithelial-like cells and fibroblast-like cells often form cell sheets and cellular networks, respectively, while the hemocyte-like cells do not form any structure. The migrated cells may proliferate by mitoses, and subculture may become possible, if the culture conditions are appropriate. However, usually it takes several months or even years for the cells to proliferate enough to be subcultured. By repeating subcultures, a cell line may become a permanently growing cell population, which is called a continuous cell line. C Physical Conditions Culture conditions may be divided into physical conditions and chemical conditions. As the former, temperature, pH, osmotic pressure and illumination will be considered. The insect cells are usually cultured. Between 20 and 30°C, the growth rate increases with the rise of temperature. Most of insect cells, however, deteriorate above 30°C. Usually insect cells are not affected by the change in the pH of the culture media between 6.0 and 7.5, and are rather resistant to the change of osmotic pressure. Most insect cell culture media have osmotic pressure between 300 and 400 mOsmol/kg. However, cells may survive even in the medium diluted to half strength. Illumination does not affect on cell survival or growth, although UV or sunlight is harmful to the cells. Photoperiodism has no effect on insect cells either, i.e., long night photoperiod does not induce arrest of cell growth. Chemical Conditions For chemical conditions, composition of culture media and gaseous phase will be considered. Cells require inorganic salts for maintaining ion balance, sugars as energy source, amino acids for protein synthesis, vitamins and some growth factors for survival and proliferation. Usually approximately six inorganic salts are used. Na+, K+, Ca++, Mg++, PO4–, and Cl– will be required. As energy sources, glucose satisfies the requirement. Usually 20 amino acids, which are constituents of proteins, are incorporated into a medium, although the essential amino acids are arginine, cystine, glutamine, glycine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, proline, serine, threonine, tryptophan, tyrosine, and valine. As vitamins, water-soluble B group vitamins are commonly used. They are, in most media, thiamine, riboflavin, calcium pantothenate, niacin, pyridoxine, biotin, folic acid, p-aminobenzoic acid, isoinositol and choline chloride. However, some of them are not essential. For example, the flesh fly 809 810 C Cell Culture of Insects (Diptera: Sarcophagidae) embryonic cell line, NIH-SaPe-4, requires only thiamine, riboflavin, calcium pantothenate and either of niacin or niacinamide. The vitamin requirement by insect cells in culture may depend on cell line species. Most insect cells do not require added lipid-soluble vitamins, such as vitamin A, D, E, and K. Instead of using individual chemicals, natural substances, which contain necessary substances for cell growth, may be used. Seawater may be used instead of mixtures of inorganic salts. Some protein hydrolysates, such as lactalbumin hydrolysate, casein hydrolysate, egg albumin digest and so on, are used in lieu of mixture of 20 or 21 individual amino acids. Water-soluble yeast extract products contain usually sorts and amounts of vitamins for insect cell growth, and are used instead of the mixture of individual vitamins. The media containing natural substances are called “natural media” whereas those contain only known chemicals are called as “synthetic media”. However, both types of media need to be fortified by addition of sera or some other growth-promoting substances. As sera, heat-treated insect hemolymph or fetal bovine serum (FBS) is used. Among commercially available vertebrate sera, only FBS is markedly growth-promotive. Other sera, such as calf serum bovine serum, horse serum, turkey serum and sheep serum are either ineffective or even detrimental. Other than sera, growth factors or some other growth-promoting substances are used as an additive. As growth factors, only one insect growth factor has been isolated from the flesh fly cell line, so far, NIH-SaPe-4. This growth factor is a polypeptide and acts in autocrine manner, and seems to be species specific, or to have narrow spectrum. Vertebrate growth factors are ineffective on insect cells, except insulin, which is reported to be growth stimulative for D. melanogaster cells. For the gas composition in gaseous phase as well as in media, oxygen is required in large-scale culture of cells. In small-scale culture, insect cells do not consume much oxygen, and the cells can be cultured in tightly capped flasks. For large-scale culture (several liters to several 100 L), however, oxygen supply is necessary, and it is performed by oxygen sparger directly into the media. The control of CO2 concentration in gaseous phase is not necessary for insect cells, because insect cells are insensitive to the change in the pH of the culture media. Characteristics of Cells The structure of the cultured cells varies even in a cell line. The shape and the size of the cells are not uniform. Also, karyotype of the cells varies. Tetraploid cell lines are common among lepidopteran cell lines. The karyotype may change by repeating subculture. Some insect cell lines are substratedependent, and form cell sheets. Others are substrate-independent and can grow in suspension. Growth rate is different in different cell lines. The population doubling time distributes from 20 h to several days. Insect cell lines cannot be distinguished morphologically from each other. However, they can be distinguished each other by analyses of karyotype, isozyme pattern, PCR, DNA finger printing, and the combination of these techniques. Insect cell culture is a good tool for basic studies in various fields. Established cell lines are more or less different from cells in intact insects. The cell lines, however, retain many characteristics that they had when they were in insect bodies. Therefore, cell lines can be used as excellent experimental materials, if one keeps the difference of cells in vivo and in vitro in mind. Insect cell lines have been used in various fields, such as cell physiology, cytogenetics, biochemistry, endocrinology, toxicology, gene technology and pathology. Among them insect cell cultures have been used frequently in the studies of insect pathology, especially virus diseases, for a long time. Practical Applications For practical use, insect cell culture is being used in combination with insect viruses for production of foreign protein, and viral insecticides. In the former Centipedes (Class Chilopoda) case, baculovirus vector systems are now widely used to produce proteins not originating from insects. For example, gene encoding human interferon-β is inserted into the polyhedrin gene sequence of NPV, which is previously inserted into an Escherichia coli plasmid. The resulting plasmid is transfected with wild virus genome to the NPV-sensitive insect cell line. In this way, recombinant NPV, which contains the human interferon-β gene in the sequence of polyhedrin gene, is obtained. The human interferon-β can be produced by inoculating the recombinant virus to the NPV-sensitive cell culture. For the production of viral insecticides, the process of cell culture, preparation of inoculum, inoculation, maintenance of infected cells, and harvest of replicated viruses have been almost established. However, when one tries to increase the scale of culture, various problems arise, and the production of viruses by means of large scale culture of insect cells and viruses has not yet been industrialized. The problems to be solved include oxygen supply, avoidance of shear force, and cost of culture media. The insect cell lines may be used for toxicity tests. In the screening tests for insecticides, cultured cells are good materials for screening chemicals, which act on metabolic pathways. Drugs for human such as anti-cancer drugs may be tested at the screening level by the use of insect cells. Insect cells can be cultured without a CO2 incubator, and are tolerant to the change in pH, osmotic pressure and temperature. These are advantages of using insect cell culture over mammalian cell culture. C Celyphidae A family of flies (order Diptera).  Flies Cement This is a very thin lipid or shellac-like layer of integument outside the wax layer. It serves to protect the wax layer from disruption.  Integument: Structure and Function Cenchrus (pl., Cenchri) A roughened section of the metanotum in sawflies; it serves to hold the wings in place when they are folded over the body. Census Complete enumeration of every individual within a defined sample universe. (contrast with sample).  Sampling Arthropods Centipedes (Class Chilopoda) The centipedes are not numerous, numbering about 3,000 species around the world. However, they are widely distributed in both temperate and tropical regions, where they are found in soil, under litter, and beneath stones and bark. References Day MF, Grace TDC (1959) Culture of insect tissues. Ann Rev Entomol 4:17–38 Goldschmidt R (1915) Some experiments on spermatogenesis in vitro. Proc Natl Acad Sci USA 1:220–222 Grace TDC (1962) Establishment of four strains of cells from insect tissues grown in vitro. Nature 195:788–789 Trager W (1935) Cultivation of the virus of grasserie in silkworm tissue cultures. J Exp Med 61:501–513 Wyatt SS (1956) Culture in vitro of tissue from the silkworm, Bombyx mori. LJ Gen Physiol 39:841–852 Characteristics Centipedes usually are 1–10 cm in length, but may be larger in the tropics, where they can attain a length of up to 26 cm. They possess but one pair of legs per segment, a feature that allows them to be easily distinguished from the superficially similar millipedes (Diplopoda). Like many other 811 812 C Centipedes (Class Chilopoda) arthropods (millipedes, pauropods, symphylans), but unlike insects, the centipedes bear a head and a long trunk with many leg-bearing segments. The head bears a pair of antennae, and sometimes ocelli, but not compound eyes. The mouthparts are ventral, and positioned to move forward. Gas exchange is through a tracheal system in which the spiracles cannot be closed. Excretion takes place through malpighian tubules, and unlike insects and arachnids, centipedes excrete ammonia.. The heart is a dorsal tube with paired ostia at each segment. The ventral nerve cord has a ganglion for each body segment. Sperm transfer is indirect, using a spermatophore. Structures called Tömösváry organs are found at the base of the antennae in some centipedes. Apparently it is used to detect vibrations. The orders Geophilomorpha and Scolopendromorpha exhibit epimorphic development; the young have the full complement of segments when they hatch. Development of the other orders is anamorphic; the young have only a portion of their eventual complement of segments upon hatching, and add them as they grow. Covering the mouthparts of centipedes is a pair of structures called maxillipeds or poison claws. They are derived from the first pair of trunk appendages, but are involved in feeding. Each claw consists of four segments and is curved inward toward the midventral line. A poison gland is found within the base of the claw. Centipedes are well known for their poison claws, but they have other defenses as well. In some, the posterior-most legs may be used for pinching, and repugnatorial glands on the last four legs are common. As with millipedes, defensive secretions may include hydrocyanic acid. Except for the geophilomorphs, centipedes are adapted for running. Interestingly, the legs of some longlegged centipedes are progressively longer toward the posterior of the body, which helps to prevent interference with leg movement. The soil dwelling geophilomorphs do not use their legs for running, and these animals move through the soil using extension and contraction of the body trunk, much the same as earthworms. Classification As is the case with many taxa of arthropods, the classification of centipedes is subject to debate. Following is a recent classification system: Phylum: Arthropoda Subphylum: Atelocerata Class: Chilopoda Subclass: Epimorpha Order: Geophilomorpha Family: Himantariidae Family: Schendylidae Family: Oryidae Family: Mecistocephalidae Family: Geophilidae Family: Chilenophilidae Family: Eriphantidae Family: Dignathodontidae Family: Aphilodontidae Family: Gonibregmatidae Family: Neogeophilidae Order: Scolopendromorpha Family: Scolopendridae Family: Cryptopidae Subclass: Anamorpha Order: Lithobiomorpha Family: Lithobiidae Family: Ethopolidae Family: Watobiidae Family: Gosibiidae Family: Pseudolithobiidae Family: Pterygotergidae Family: Henicopidae Order: Craterostigmomorha Order: Scutigeromorpha Family: Scutigeridae The Epimorpha are longer centipedes, usually consisting of at least 21 leg-bearing segments. Young epimorphs, upon hatching, bear a full complement of long or short legs. Tömösváry organs are absent. In contrast, the Anamorpha are shorter, usually with 15 leg-bearing segments. Young anamorphs, when the hatch, bear 4–7 pairs of long or very long legs. Tömösváry organs are present. The order Geophilomorpha consists of Central Nervous System (CNS) about 1,000 species, order Scolopendromorpha of a bout 550 species, Lithobiomorpha of about 1,100 species, order Craterostigmomorpha only two species, and Scutigeromorpha about 130 species. The geophilomorphs are long worm-like animals, highly specialized, dwelling in soil, and not primitive, whereas the scutigeromorphs are long-legged forms, commonly found around human habitations, and clearly are primitive. The Scolopendromorpha and Lithobiomorpha both consist of heavy-bodied animals that live beneath stone, bark and logs. Ecology Life histories of centipedes are poorly known, but 5–6 instars occur in many species. Longevity is often 3–6 years, and it commonly takes more than a year to attain maturity. It is difficult to separate instars, but head capsule width is most reliable. The centipedes are predaceous. Most feed on arthropods, snails, earthworms and nematodes, but even toads and snakes are consumed by some. The antennae and legs are used to detect prey. The poison claws are used to stun or kill the prey. Though painful, the bite of centipedes is normally not lethal to humans, resembling the pain associated with a wasp sting. Centipedes require a humid environment. Their integument is not waxy, and their spiracles do not close. Hence, they are found belowground, in sheltered environments, or active above-ground principally at night. Some centipedes have adapted to a marine existence, living among algae stones and shells in the intertidal zone. Apparently they can retain sufficient air during high tides, or capture a sufficiently bubble of air to allow submersion. Some centipedes (scolopendromorphs and geophilomorphs) produce a cavity in soil or decayed wood in which to brood their egg clutch, which often numbers 15–35 eggs. The female guards the eggs until the young hatch. Inte remaining taxa, the eggs are deposited singly in the soil. C Reference Lewis JGE (1981) The biology of centipedes. Cambridge University Press, Cambridge, UK, 476 pp Central Body A region in the center of the protocerebrum that serves as an integration point for different types of information, and for activation of body movements associated with the thoracic region. The central body is located between the bases of the stalks of the mushroom bodies. It receives input from both sides of the brain, and from the optic lobes.  Central Body Central Dogma The Central Dogma was proposed by F. Crick in 1958. It states that the genetic information is contained in DNA, which is transcribed into RNA, which is translated into polypeptides. The transfer of information was proposed to be unidirectional from DNA to polypeptides: polypeptides are unable to direct synthesis of RNA, and RNA is unable to direct synthesis of DNA. The Central Dogma was modified in 1970 when RNA viruses were found to transfer information from RNA to DNA. Central Nervous System (CNS) In insects, the central nervous system consists of the brain, ventral ganglia, and the ventral nerve cord. The ventral ganglia and connecting nerve cord usually lie close to the cuticle on the ventral side of the body. The brain occurs on top of the esophagus, and is sometimes called the supraesophageal ganglion.  Nervous System 813 814 C Centromere Centromere A region of a chromosome to which spindle fibers attach during mitosis and meiosis. The position of the centromere determines whether the chromosome will appear as a rod, a J, or a V during migration of the chromosome to the poles in anaphase. In some insects, the spindle fibers attach throughout the length of the chromosome and such chromosomes are called holocentric. Centromeres are usually bordered by heterochromatin containing repetitive DNA. Ceraphronidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies Ceratocanthid Scarab Beetles Members of the family Ceratocanthidae (order Coleoptera).  Beetles Ceratocanthidae Cephalothorax The fused head and thorax of Arachnida and Crustacea, and of coccids. A family of beetles (order Coleoptera). They commonly are known as ceratocanthid scarab beetles.  Beetles Ceratocombidae Cephidae A family of sawflies (order Hymenoptera, suborder Symphyta). They commonly are known as stem sawflies.  Wasps, Ants, Bees and Sawflies Cerambycidae A family of beetles (order Coleoptera). They commonly are known as longhorned beetles.  Beetles  Longicorn, Longhorned, or Round-headed Beetles (Coleoptera: Cerambycidae) Cerambycoid Larva A larval body form that is straight, somewhat flattened or cylindrical, smooth or naked, and distinctly segmented. They tend to be found in wood or soil, and occur in the families Cerambycidae, Buprestidae, and Elateridae (all in order Coleoptera). A family of bugs (order Hemiptera).  Bugs Ceratophyllidae A family of fleas (order Siphonaptera). They sometimes are called bird and rodent fleas.  Fleas Ceratopogonidae A family of flies (order Diptera). They commonly are known as biting midges, punkies or no-see-ums midges.  Flies  Biting Midges, Culicoides sp. (Diptera: Ceratopogonidae) Cercoccidae A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs Cereal Stem Moths (Lepidoptera: Ochsenheimeriidae) Cercophanidae C Cercus A family of moths (order Lepidoptera) also known as Andean moon moths.  Andean Moon Moths  Butterflies and Moths Cercus Cercopidae A family of insects in the order Hemiptera. They sometimes are called froghoppers or spittlebugs.  Bugs Cercus Cercus (pl., cerci) A sensory appendage (Fig. 36) located near the tip of the abdomen, usually on abdominal segment ten. In many insects the c erci are antenna-like in shape, paired and jointed.  Abdomen of Hexapods Cereal Leaf Beetle, Oulema melanopus (Linnaeus) (Coleoptera: Chrysomelidae) This leaf-feeding beetle is a pest of small grain crops.  Wheat Pests and their Management Cereal Stem Moths (Lepidoptera: Ochsenheimeriidae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Cereal stem moths, family Ochsenheimeriidae, include only 17 species from the Palearctic (one sp. is from Kashmir), with one sp. introduced into North America. The family is part of the Cercus Cercus, (pl., cerci) Figure 36 Diagrams of the tip of the abdomen in various hexapods, showing various forms of the cercus. Top left, earwig; top right grasshopper, lower left, scorpionfly; lower right silverfish. superfamily Yponomeutoidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (9–17 mm wingspan), with head very roughened; eyes large; haustellum short and naked; labial palpi tufted; maxillary palpi 2-segmented; antennae often basally swollen in males. Wings rather elongated but fringes average. Maculation somber hues of brown or gray, with indistinct markings. Adults are diurnal. Larvae are leafminers, but become stem borers in later instars, primarily on grasses (Gramineae), sedges (Cyperaceae) and rushes (Juncaceae). The common name for the family is derived from the single economic species, the cereal stem moth. Some place the family as a subfamily of what is grouped as the “family” Ypsolophidae (the latter actually a subfamily 815 816 C Cerebellum of Plutellidae). The family and nominate genus Ochsenheimeria are named after the German lepidopterist Ferdinand Ochsenheimer (1767–1822). References Davis DR (1975) Review of Ochsenheimeriidae and the introduction of the cereal stem moth Ochsenheimeria vacculella into the United States (Lepidoptera: Tineoidea). Smithsonian Contrib Zool 192:1–20 Davis DR (1998) Ochsenheimeriidae. In Lepidopterorum Catalogus, (n.s.). Fasc 48. Association for Tropical Lepidoptera, Gainesville, FL, 12 pp Karsholt O, Nielsen ES (1984) A taxonomic review of the stem moths, Ochsenheimeria Hübner, of northern Europe (Lepidoptera: Ochsenheimeriidae). Entomol Scand 15:233–247 Réal P (1966) Famille des Ochsenheimeriidae. In: Balachowsky AS (ed) Entomologie Appliquée à l’ Agriculture. Tome 2: Lépidoptères, 254–255. Paris, 1057 pp Zagulajev AK (1988) Family Ochsenheimeriidae. In: Fauna SSSR. 4. Lepidoptera, 7: 70–177. Acad. Nauk. [in Russian], St. Petersburg Cerumen A brown mixture of wax and propolis used by social bees for nest construction. Cervical Shield A plate on the dorsal surface of caterpillars just behind the head. It is also known as the prothoracic plate or shield. Cervix The membranous region between the head and thorax (Fig. 37). The cervix is analogous to the neck in vertebrates. Cervical Sclerites Cerebellum The subesophageal ganglion, a portion of the visceral nervous system that innervates many of the appendages associated with feeding.  Nervous System Cerebrum The portion of the brain above the esophagus; the region before the subesophageal ganglion. There are three recognized portions, the proto-, deuteroand tritocerebrum.  Nervous System Cerococcidae A family of insects in the superfamily Coccoidae (order Hemiptera). They sometimes are called ornate pit scales.  Bugs Small chitinous plates on the membrane between the head and the thorax. Cerylonidae A family of beetles (order Coleoptera). They commonly are known as minute bark beetles.  Beetles Cestodes or Tapeworms hiLary hurd Keele University, Keele, Staffordshire, United Kingdom The majority of tapeworms (phylum Platyhelminthes, order Cestoda) that have terrestrial life cycles utilize two hosts. The adult worms are found in the gut lumen of the final, or definitive host, where they undergo sexual reproduction and produce eggs that contain a developing embryo protected Cestodes or Tapeworms lateral ocellus C compound eye postocular area cervix gena antenna clypeus labrum cervical sclerites tentorial suture basimandibular sclerite maxilla labium labial palpus mandible maxillary palpus Cervix, Figure 37 Side view of the head of an adult grasshopper, showing some major elements. by several membranes. These eggs are shed into the environment with the host feces, either still contained within the tapeworm segment, or proglottis, in which they developed, or free from it. The life cycle continues when eggs are ingested by an intermediate host, often a coprophagous insect or other arthropod. They hatch within the insect gut and burrow through the gut wall with the help of 3 pairs of curved hooks and the lytic contents of a pair of glands. In the hemocoel, they transform into a metacestode and, once mature, will be transmitted and the life cycle completed if their intermediate host falls prey to another definitive host. Fecal material from infected definitive hosts may be more attractive to insects than that from uninfected hosts, as is the case for feces from rats infected with a rate tapeworm, Hymenolepis diminuta. This enhances the chances of the cestode’s life cycle being completed. Another rat tapeworm, Raillietina celebensis (also an occasional parasite of humans), provides an example of the means whereby a non-coprophagous insect becomes an intermediate host. Gravid proglottides, detached from the main tape and remaining intact, are picked up from the fecal material by ants, carried to the nest and fed to the ant larvae. Some larval fleas also ingest tapeworm eggs when feeding on host feces. The immature worms develop with the larval flea and are ingested by the definitive host when the adult flea is accidentally eaten during grooming. Dogs become infected with the dog tapeworm, Dipylidium caninum, in this way and, for the latter species, so do cats and occasionally humans. Prevalence of cestode infection in the definitive host may be linked with seasonal changes in feeding patterns. Thus, a study of the shrew Sorex araneus araneus in Poland demonstrated that a spring and summer diet including the coprophagous beetle, Geotrupes stercorosus, gave rise to infections with Ditestolepis diaphana and Staphylocystis furcata in the summer and autumn. Whereas in the winter and spring, the predominance of Pseudodiorchis prolifer infections in the shrew reflected a change of diet in the autumn and winter to the myriopod intermediate host of this latter cestode, as beetles were difficult to find. Due to the trophic nature of tapeworm transmission, definitive hosts of cestodes associated with insects are partially or entirely insectivorous. Thus, with the possible exception of cestode infections in the poultry industry, tapeworms that 817 818 C Cestodes or Tapeworms utilize insect intermediate hosts are of no medical or veterinary importance and have, therefore, attracted little research attention. The exception is the rat tapeworm, H. diminuta, which has been the doyen of cestode laboratory research models due to the ease with which its life cycle can be maintained. Several insects act as intermediate hosts for the rat tapeworm including fleas and cockroaches (Fig. 38), but laboratory studies have focused upon the effect of infection on the flour beetles, Tribolium spp. and Tenebrio molitor. Long-term studies have revealed that infection results in a 50% depression in the equilibrium population of T. confusum as a result of fecundity reduction in the females. The mechanism underlying fecundity reduction has been extensively studied in T. molitor, and appears to result both from the host response to the presence of the parasite and to the direct action of a factor(s) produced by the early developmental stages of the parasite. Several aspects of the process of vitellogenesis or the production and uptake of yolk protein are affected. In the ovary, yolk uptake by developing follicles is retarded and they contain less protein than their equivalents from uninfected beetles. The presence of a competitive inhibitor of Adult worm infects the rat gut Metacestode in the insect hemocoel the binding site of juvenile hormone to the follicular epithelium results in a retardation in the development of patency in the follicular epithelium, thereby affecting yolk uptake. Synthesis of yolk protein in the fat body also is inhibited but, in this case, by a factor of parasite origin that is peptidergic in nature. The effect of infection on male reproductive physiology is not as well studied. An increase in the size, protein and trehalose content of the beanshaped accessory glands has been reported and this may account for an increase in protein and trehalose content of spermatophores produced by infected males. In contrast, male response to female sex pheromone is decreased by infection. The effect of these changes on the number of offspring produced by females mated with infected males is yet to be established unequivocally. Although cestodes cause a reduction in the reproductive fitness of beetles, it has been demonstrated that the life span of infected female T. molitor is increased by 40% and males by 25%. This may be due to changes in resource management such that longevity is increased when fewer resources are devoted to reproduction. The production of aggregation pheromones is down-regulated by infection, and several aspects of behavioral response to environmental cues are altered, although this does not appear to increase the chance of host predation by rats. However, defensive glands are everted less frequently, and toluquinone and m-cresol production are reduced, possibly accounting for the greater likelihood that infected beetles will be eaten by rats. This may thus represent an example of host manipulation that will enhance transmission prospects. Eggs shed with feces References Intermediate host, Tenebrio molitor Cestodes or Tapeworms, Figure 38 The life cycle of Hymenolepis diminuta, an example of an insect-associated cestode. Blankespoor CL, Pappas PW, Eisner T (1997) Impairment of the chemical defence of the beetle, Tenebrio molitor, by metacestodes (cysticercoids) of the tapeworm, Hymenolepis diminuta. Parasitology 115:105–110 Carver FJ, Gilman JL, Hurd H (1999) Spermatophore production and spermatheca content in Tenebrio molitor infected with Hymenolepis diminuta. Insect Physiol 45:565–569 Chagas, Carlos Justiniano Ribeiro Hurd H (2001)Parasite regulation of insect reproduction: similar strategies, different mechanisms? In: EdwardsJP, Weaver RJ (eds) Endocrine interactions of parasites and pathogens. Bios Scientific Publishers, Oxford, UK Kisielewska K (1961) Circulation of tapeworms of Sorex araneus araneus L. in biocenosis of Bialowieza National Park. Acta Parasitol Pol 9:31–369 Webb TJ, Hurd H (1999) Direct manipulation of insect reproduction by agents of parasite origin. Proc R Soc Lond B Biol Sci 266:1537–1541 Chaeta (pl., chaetae) An outgrowth of the cuticle originating in a pit. It is an articulated spine-like process. Chaeteessidae A family of praying mantids (Mantodea).  Praying Mantids Chaetotaxy The arrangement and nomenclature of chaetae (setae). This is used to create a setal map. Chaff Scale, Oulema melanopus (Linnaeus) (Coleoptera: Chrysomelidae This is an occasional pest of citrus trees.  Citrus Pests and their Management Chafers Members of the subfamily Melolonthinae, family Scarabaeidae (order Coleoptera).  Beetles Chagas, Carlos Justiniano Ribeiro Carlos Chagas was a Brazilian physician who discovered Chagas disease (Chagas’ disease), or C American trypanosomiasis. Chagas disease is an endemic insect-borne disease found in Central and South America from Mexico to Argentina. It is caused by the protozoan Trypanosoma cruzi. In discovering this malady, he became the only individual investigator so far who described completely all elements of the disease: the pathogen, vector, host, clinical manifestations, and epidemiology. He also developed a new and effective approach to malaria control, a technique that remains the principal method for malaria suppression around the world. Chagas was born on July 9, 1879 in Oliveira, in the state of Minas Gerais, Brazil. He was the son of upper-class parents who owned a small coffee plantation. His ancestors had come to Brazil in the seventeenth century. His father died when Carlos was only 4 years old, and at the age of seven he was sent to a Jesuit boarding school. There he was befriended by a priest who instilled in him a love of natural history. Following his mother’s wishes that he should become an engineer, at the age of 14 he enrolled in the School of Mining Engineering in Oro Pieto, Minas Gerais. However, at the age of 16 he was afflicted with beri-beri and spent some time with his uncle Carlos Ribeiro de Castro, an M.D. who had just established a new hospital. Brazil at this time was struggling to develop because it had so many endemic diseases. For example, many European ships refused to dock in Brazil for fear of their crews contracting yellow fever, bubonic plague, smallpox and other diseases. Chagas’ uncle convinced him that through the practice of medicine he could perform important national service. Influenced by his uncle, in 1897 Chagas abandoned the plan to become an engineer and entered the Faculty of Medicine of Rio de Janeiro where he received his M.D. in 1903. Chagas had opportunity early in his career to conduct research, but was attracted by clinical practice in a hospital in Jurujuba. Following financial problems, in 1905 Chagas accepted a position with a company in the interior of the state of São Paulo, where malaria was a serious problem for workers. Studying the transmission cycle closely, 819 820 C Chagas, Carlos Justiniano Ribeiro he realized that workers were being bitten while sleeping. Up to this time, the only known effective preventative approach for malaria control was destruction of larvae in breeding areas (swamps). As this was not effective, he began to use the insecticide pyrethrum to disinfect houses. This approach proved to be very successful. Chagas moved to the Oswaldo Cruz Institute in 1906, which became his base of operations for the remainder of his career. In 1909, Cruz asked Chagas to undertake an antimalaria campaign in Lassance, Brazil, where railroad construction was stalled because so many workers had succumbed to malaria. There he remained for 2 years, living and working in a railroad car. He soon noticed disease symptoms that were not consistent with malaria, and later some locals pointed out to him a blood-sucking bug called “vinchuca” that commonly were found in the huts of workers. This blood-sucking insect, an assassin bug or kissing bug (Hemiptera: Reduviidae), was later determined to be in the genus Triatoma, several species of which transmit a disease later named Chagas disease. Chagas dissected the Triatoma bugs and found within them a trypanosome (Protozoa). Allowing the bugs to feed on marmoset monkeys, he found that the trypanosome could be transmitted. He identified the trypanosome and named it Schizotrypaum cruzi after his mentor and friend Oswaldo Cruz. Later it became known as Trypanosoma cruzi. Suspecting that these bugs could be transmitting the trypanosome to people due to their great abundance in rural homes, and their blood-feeding habits, Chagas soon found tryanosomes in the blood of a young girl. He also conducted autopsies of workers dying with acute and chronic forms of the disease, and found brain and myocardium abnormalities accounting for the involvement of these organs in the new disease. He conducted surveys of animals in the area, and determined that armadillos were the likely reservoir of the trypanosomes. The acute phase of Chagas disease occurs in the first few weeks or months of infection. Often it is symptom-free or exhibits only mild symptoms and signs that are not unique to Chagas disease. The symptoms noted by the infected individual may include fever, fatigue, aches of the head or body, rash, loss of appetite, diarrhea, and vomiting. The signs of infection include mild enlargement of the liver or spleen, swollen glands, and local swelling (a chagoma). The most easily recognized indication of acute Chagas disease is called Romaña’s sign, which includes swelling of the eyelids on the side of the face near the bite wound or where the bug feces were deposited or accidentally rubbed into the eye. Symptoms, if present, usually fade away after a few weeks or months. However, if untreated, the disease persists. Occasionally young children die from severe inflammation of the heart muscle or brain. The acute phase is more severe in immuno-compromised people. The chronic phase of infection may result in no signs of infection for decades or even for life. However, some people develop heart problems including an enlarged heart, heart failure, altered heart rate or rhythm, and cardiac arrest. Also, intestinal problems can occur, including an enlarged esophagus or colon, which can lead to difficulties with eating or defecation. Chagas was widely recognized for his noteworthy achievements. He was elected to the National Academy of Medicine in 1910, and in 1912 he received the Schaudinn Prize for outstanding work in protozoology and tropical medicine. He was twice nominated for the Nobel Prize, but never received the award. In 1922, Chagas was recognized with the Great Prize of the Pasteur Centenary Commemorative Exposition in Strasbourg. He was awarded honorary doctorate degrees from Harvard University and the University of Paris. Chagas took over direction of the Institute in 1917 following the death of Oswaldo Cruz, and remained in this position until 1934. During this period the Brazilian government asked him to organize a campaign against Spanish influenza, which was devastating Rio de Janeiro, and also to reorganize the Department of Health in Brazil (he also served as director from 1920–1924). There he Chagas Disease: Biochemistry of the Vector C introduced many innovations and created centers of preventative medicine. He died in Rio de Janeiro from a heart attack on November 8, 1934.  Chagas Disease or American Trypanosomiasis  Trypanosomes References Lewinsohn R (1979) Carlos Chagas (1879–1934): the discovery of Trypanosoma cruzi and of American trypanosomiasis (foot-notes to the history of Chagas’s disease). Trans R Soc Trop Med Hyg 73:513–523 Lewinsohn R (2003) Prophet in his own country: Carlos Chagas and the Nobel Prize. Perspect Biol Med 46:532–549 Chagas Disease: Biochemistry of the Vector m. patriCia Juárez National University of La Plata, La Plata, Argentina Chagas disease is caused by the parasitic protozoan Trypanosoma cruzi, which is transmitted by blood-feeding insects in the subfamily Triatominae (Hemiptera: Reduviidae), with 130 species forming five tribes, among them only the tribes Triatomini and Rhodniini possess relevant vector capacity. Triatoma infestans (Klug) (Fig. 39) and Rhodnius prolixus (Stål) are representative examples of each tribe, and the most thoroughly studied, as they are the major ones responsible for Chagas disease transmission. Triatomins are called kissing bugs or assassin bugs; local names are vinchuca, chinche or picudo. Trypanosoma cruzi infects some 16–18 million people, with another 90 million at risk in regions of South and Central America. There is neither a vaccine against it, nor a safe and effective drug to cure it. Fundamental research in insect physiology was pioneered by V.B. Wigglesworth using R. prolixus. Most biochemical studies in Triatominae are focused on blood intake, digestion, fat body and integumental lipid metabolism and transport, and molting. Chagas Disease: Biochemistry of the Vector, Figure 39 Triatoma infestans, a major vector of Chagas disease in South America. Feeding Insect blood feeding impacts directly on human and animal health. When a blood meal is taken, the pathogen T. cruzi might be transmitted via excreta deposited on the host skin. Rhodnius prolixus is capable of ingesting 300 mg of blood in 15 min. Such highly efficient blood intake is made possible by a special mouthpart developed to avoid blood coagulation and platelet aggregation. Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of R. prolixus was recently reported. Serotonin and other major biogenic amines in insects, dopamine and octopamine, have been reported to modulate a variety of physiological and behavioral functions, including the control of feeding behavior in insects. Feeding was found 821 822 C Chagas Disease: Biochemistry of the Vector to be a natural stimulus for the release of serotonin into the hemolymph of R. prolixus, and serotonin depletion led to a reduced blood meal size in this insect. Triatomins produce bioactive molecules in their salivary glands that are inoculated into host skin via saliva during feeding. Four closely related proteins found in Rhodnius saliva behave as immunomodulators, countering their host’s haemostatic, inflammatory and immune responses to facilitate blood feeding, exhibiting vasodilator, anticoagulant and antiplatelet aggregation activity. Because they bind nitric oxide, and act as a storage and delivery system for it, they are named nitrophorins. As a consequence of hematophagia, triatomins feed on a protein- and lipid- rich diet, with fatty acids as the major source for energy production. This results in a much larger yield in the amounts of ATP produced, as compared to that of insects consuming carbohydrate. The fat body is the major metabolic factory, as well as the main storage depot of fat, glycogen and protein. Its metabolites are transported to target organs via hemolymph. Protein Metabolism Many of the proteins that are crucial in the life of insects are biosynthesized in the fat body. Protein synthesis is often under control of juvenile hormone (JH). Complete hydrolysis of blood-meal proteins is mediated by exo- and endo-peptidases. Endoproteinases cleave proteins to smaller segments that are finally completely degraded to amino acids by exopeptidases. Triatominae midgut also contains endopeptidases B and D, involved in hemoglobin hydrolysis. Salivary glands have acid phosphatase activity with anticoagulant properties to destroy hemoglobin; large amounts of sialidase activity are also detected after a blood meal, rich in sialic acids. Hemoglobin digestion and detoxification of the free haem by its sequestration into an insoluble pigment known as haemozoin (Hz) were recently detected in the midgut of R. prolixus. Blood meals trigger the onset of diuresis after the diuretic hormone is released by the neurosecretory cells of the mesothoracic ganglionic mass. Insects then undergo a rapid elimination of urine during which time the insect may lose 40% of the weight of the meal. Multiple diuretic peptide factors have been suggested, and the serotonin role is well described. Uric acid is the most important nitrogenous waste material excreted by triatomins. It is formed through the uricotelic pathway by de novo synthesis from protein. Reproduction Egg production is under hormonal and nutritional control; a blood meal is required to start vitellogenesis, and juvenile hormone (JH) secretion by the corpora allata (CA) regulates oocyte development. The amount of blood required for oviposition varies from 5 to 8 mg/egg for R. prolixus to 16–25 mg/egg for T. infestans. Vitellogenins (VG) are high molecular weight lipoproteins synthesized in the fat body of adult females. They enter the oocytes by pinocytosis to be converted into vitellins (VN). A molecular weight around 4 × 105 was estimated for different species, after characterization by immunodiffusion (ID), immunoelectrophoresis (IEP), and electrophoresis in polyacrylamide gel (PAGE). Vitellogenin synthesis also has been detected in R. prolixus ovaries. Lipid Composition, Metabolism, and Transport A high lipid content (7–8%) is characteristic of eggs, and remains high through the first instar in T. infestans. It is close to 1.5% throughout the whole nymphal cycle to adult stage. Major insect and egg lipids are triacylglycerols (85%) with energy storage function; phospholipids (4–8%), mainly phosphatidylethanolamine and phosphaditylcholine, are involved in cell membrane formation and metabolic events; and the major sterol Chagas Disease: Biochemistry of the Vector component is cholesterol, sequestrated from host blood and stored as cholesterol esters or free (5–8%), which contributes to lipid bilayer fluidity regulation. Small amounts of saturated hydrocarbons (straight and multiple methylbranched chains of 27 to >41 carbons), primary fatty alcohols (straight chains of 24–34 carbons) and wax esters (44–48 carbons) confer water-proofing properties to the cuticular surface, also preventing chemicals and microorganism penetration. The major whole-body insect fatty acid components are oleic (18:1) and palmitic (16:0), with minor amounts of linoleic (18:2), stearic (18:0), palmitoleic (16:1) and arachidonic (20:4) acids. Minor components play specific functions; for example, volatile fatty acids of short chains (VFA) formed in the Brindley glands, are released upon disturbance and serve as defensive secretion, with isobutyric acid accounting for most of their characteristic stink odor. Very long chain fatty acids (VLCFA), up to 34 total carbons, are also present in the triatomin integument, and are detectable precursors to hydrocarbon and fatty alcohol formation. Specific fatty acids precursors to cuticular waxes formation are detected in minute amounts in the integument: methyl-branched fatty acids of 16 and 18 carbons in the straight carbon chain are intermediates in methyl-branched hydrocarbon synthesis. Dietary lipids are the only source of 18:2 and 20:4 acids in Triatominae, which lack both ∆ 5 and ∆ 6 desaturating enzymes. These polyunsaturated components contribute to membrane fluidity and they are precursors to the eicosanoids prostaglandins, molecules of significance in reproduction. Large amounts of 20:4 acids are stored in male testes. They are metabolized into prostaglandins (PG) and transferred to females via spermatophores during copulation. Eicosanids also participate in the immune response, i.e., to help clear bacteria from contaminated hemolymph, and to regulate fluid balance. Fatty acid biosynthesis was extensively studied in the whole insect, the fat body, the integument and reproductive organs, both in tissue slices and C after subcellular fractionation. De novo fatty acid assays employed radioactive precursors such as [14C]acetate or [14C]propionate by injection into the hemolymph for in vivo or tissue slice assays; [14C]acetyl-CoA or [14C]malonyl-CoA were used in cell-free assays. Whole insect, fat body or integumental tissue mostly metabolize [14C]acetate into triacylglycerols (ca. 80%) and phospholipids (>10%). The major fatty acids formed are 16:0, 18:1, 18:0 and 16:1, produced by a cytosolic fatty acid synthetase (FAS) and a ∆ 9 desaturase. Metabolites are incorporated into hemolymph lipoproteins (Lp) that serve multiple functions in insect development and reproduction. They transport nutrients from the site of absorption or the site of synthesis to the site of utilization and storage in target tissues. Other than vitellogenin, three lipoproteins have been identified in triatomins, a high density lipoprotein (HDL) also named lipophorin, and two very high density lipoproteins, VHDL-1 and VHDL-2. Their apo-proteins are polypeptides from 17 to 210 kdaltons (kDa), with a 86 kDa common component. Lipid transport is mediated by lipophorin, an ubiquitous lipoprotein, that is widely distributed among insects. It functions as a reusable shuttle for neutral and polar lipid transport in Triatominae. HDL from the hemolymph of T. infestans has an apparent molecular weight of 670 kDa, with an isoelectric point of 7.0 and a density (δ) of 1.10 g/ml. It contains 53% protein and 47% lipid. The protein moiety consists of two apoproteins: apoLp-I (255 kDa) and apoLp-II (70–80 kDa), rich in the amino acids aspartic acid, glutamic acid, and leucine. Diacylglycerols constitute 41% of the total lipids, and satisfy the major energy requirement in insects. HDL is also the vehicle for transport of phospholipids, hydrocarbons, and cholesterol. It also behaves as a free fatty acid donor to VHDL, a hexameric storage protein (δ = 1.27 g/ml) with a putative role related to amino acid and free fatty acid supply involved in molting, metamorphosis and reproduction events. Lipophorin binding sites located on the surface of the oocyte, mainly at the microvilli, mediate phospholipid transfer from the hemolymph to the oocytes. 823 824 C Chagas Disease or American Trypanosomiasis The Integument References The bulk of triatomins cuticular proteins are soluble in urea 7 M, with eight major bands separated by electrophoresis. They contain large amounts of hydrophobic and polar uncharged amino acids. The abdominal cuticle is extensible through the fifth instar, and chitin accounts for <20% (w/w). When Rhodnius takes a blood meal, a plasticizing factor is secreted which lowers the pH of the cuticle, and this changes the degree of bonding between cuticular proteins. Therefore, the cuticle becomes more flexible and the abdomen is dramatically expanded up to nearly four times, with the cuticle becoming very thin. Chitin synthesis is started by depletion of glycogen and trehalose from storage sites for conversion to UDP-N-acetylglucosamine units, which are further polymerized to chitin, an aminopolysaccharide. Chitin synthesis occurs mostly in the fat body; its formation is under ecdysteroid regulation. Chitin is not responsible for the hardness of the integument; instead this attribute is associated with tanned proteins, their degree of sclerotization and their distribution among the polysaccharide matrix. Molting evokes major biochemical changes in the cuticle of Triatominae. In preparation for molting, chitinase and proteinase are secreted to digest the less sclerotized cuticle, but have no effect either on exocuticle or on the surface lipids. The oenocytes, modified epidermal cells, are the site of integumental lipid synthesis. They transfer newly formed hydrocarbons to hemolymph, which functions as a selective shuttle, storing methylbranched chains while releasing to the site of deposition, the epicuticular surface, straight and methylbranched chains in a 1:1 ratio. Inhibition of cuticular lipid synthesis in T. infestans was shown to raise detrimental effects on hatch and insect development, water barrier properties, and to enhance chemical and microbial insecticide penetration; complete degradation of T. infestans hydrocarbons by fungal pathogens was recently shown.  Assassin Bugs  Area-Wide Pest Management  Chagas Disease or American Trypanosomiasis Brenner RR (1987) Chagas disease vectors. Lipid composition and metabolism. In: Brenner RR, Stoka AM (eds) Chagas disease vectors. Biochemical aspects and control, vol 3. CRC Press, Boca Raton, FL, USA, pp 9–35 Juárez MP (1994) Hydrocarbon biosynthesis in Triatoma infestans eggs. Arch Insect Biochem Physiol 25:193–206 Champagne DE, Nussenzveig RH, Ribeiro JM (1995) Purification, partial characterization, and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus. J Biol Chem 270:8691–8695 Rimoldi OJ, Córsico B, Gonzalez MS, Brenner RR (1996) Detection and quantification of a very high density lipoprotein in different tissues of Triatoma infestans during the last nymphal and adult stages. Insect Biochem Mol Biol 26:705–713 Wigglesworth VB (1933) The physiology of the cuticle and of ecdysis in Rhodnius prolixus. Q J Microsc Sci 76:269–318 Chagas Disease or American Trypanosomiasis John L. Capinera University of Florida, Gainesville, FL, USA Chagas (or Chagas’) disease is named after its discoverer, the Brazilian physician Carlos Chagas. It is caused by the trypanosome (protozoan) parasite Trypanosoma cruzi. This pathogen is transmitted to animals and people by kissing bugs (Hemiptera: Reduviidae: Triatominae) (Table 10). The disease occurs in the western hemisphere from Mexico to Argentina (Fig. 40), primarily in rural areas where poverty is widespread. It is estimated that as many as 18 million people in Mexico, Central America, and South America have Chagas disease. Interestingly, most of these victims do not know they are infected because the acute symptoms fade away. If the disease remains unrecognized and untreated, however, there can be serious consequences later in life and the disease ultimately can be life threatening. About 50,000 people die each year from complications caused by Chagas disease. Chagas Disease or American Trypanosomiasis C Chagas Disease or American Trypanosomiasis, Table 10 The major vectors of Chagas disease and their distribution Species Geographic distribution Panstrongylus herreri northern Peru Panstrongylus megistus Brazil, Paraguay, Argentina, Uruguay Rhodnius prolixus southern Mexico south to Colombia and Venezuela Rhodnius pallescens Panama, Colombia Triatoma infestans Peru, Bolivia, Brazil, Paraguay, Argentina, Uruguay, Chile Triatoma dimidiata Mexico south to Ecuador and Peru Triatoma pallidipennis Mexico Triatoma phyllosoma Mexico Triatoma maculata Colombia, Venezuela, Guyana, Suriname Triatoma brasiliensis Brazil Triatoma guasayana Bolivia, Paraguay, Argentina Triatoma sordida Bolivia, Brazil, Paraguay, Uruguay, Argentina Chagas Disease or American Trypanosomiasis, Figure 40 The distribution of Chagas disease in Latin America; shaded areas indicate regions where Chagas disease is most likely to occur. The acute phase of Chagas disease occurs in the first few weeks or months of infection. Often it is symptom-free, or exhibits only mild symptoms and signs that are not unique to Chagas disease. The symptoms noted by the infected individual may include fever, fatigue, aches of the head or body, rash, loss of appetite, diarrhea, and vomiting. The signs of infection include mild enlargement of the liver or spleen, swollen glands, and local swelling. The most easily recognized indication of acute Chagas disease is called Romaña’s sign, which includes swelling of the eyelids on the side of the face near the bite wound or where the bug feces were deposited or accidentally rubbed into the eye. Symptoms, if present, usually fade away after a few weeks or months. However, if untreated, the disease persists. Occasionally young children die from severe inflammation of the heart muscle or brain. The acute phase is more severe in immunocompromised people. The chronic phase of infection may result in no signs of infection for decades or even for life. However, some people develop heart problems including an enlarged heart, heart failure, altered heart rate or rhythm, and cardiac arrest. Also, intestinal problems can occur, including an 825 826 C Chagas Disease or American Trypanosomiasis enlarged esophagus or colon, which can lead to difficulties with eating or defecation. A toxin is responsible for the destruction of tissues. Although Chagas disease occurs primarily in the rural areas in Latin America, the movement of large numbers of people from rural to urban areas of Latin America, and to other regions of the world, has increased its geographic distribution. It is a growing threat in the United States and the Caribbean region, where Chagas disease is not endemic; it is estimated that about 500,000 unknowingly infected immigrants now live in these more northern countries. In these areas, where kissing bugs are not common or not likely to bite humans, Chagas management should focus on preventing transmission from blood transfusion, organ transplantation, and mother-to-baby (congenital) transmission. Nevertheless, there are Triatomine bug stages Triatomine bug takes a blood meal (passes metacyclic trypastigotes in feces, tryposmastigotes enter bite wound or mucosal membranes, such as the conjunctiva) ominous reports of Trypanosoma cruzi occurring in wild animal (raccoon, opossum) populations as far north as North Carolina. The triatomine bugs indigenous to North America are capable of transmitting Chagas disease (Fig. 41). The failure of Chagas to be a problem in the USA is attributed to the low incidence of infected bugs (6%) and vertebrate hosts (15%), but also to the habit of the northern species not to defecate immediately after feeding, so even if humans are bitten the bugs are less likely to defecate on humans in North America than in Central and South America. In Chagas-endemic areas, the principal route of infection is by being bitten by triatomine bugs, primarily Triatoma spp., and especially T. infestans. The bugs contract the typanosomes by feeding on infected animals or people. The bite of kissing bugs typically produces little or no pain, so the Vertebrate host stages Metacyclic trypomastigotes penetrate various cells at bite wound site. Inside cells they transform into amastigotes. Metacyclic trypomastigotes in hindgut Multiply in midgut Epimastigotes in midgut Triatomine bug takes a blood meal (trypomastigotes ingested) Trypomastigotes can infect other cells and transform into intracellular amastigotes in new infection sites. Amastigotes multiply by binary fission in cells of infected tissues. Intracelluar amastigotes transform into trypomastigotes, then burst out of cells and enter the bloodstream. Chagas Disease or American Trypanosomiasis, Figure 41 The Chagas disease cycle in triatomine bugs and animal hosts (adapted from CDC). Chagas Disease or American Trypanosomiasis sleeping host is usually unaware of the bloodfeeding episode. Once infected, the bugs pass T. cruzi parasites in their feces. The bugs frequently aggregate in barns, sheds or houses if they are not insect-proof. In rural areas, many houses are made from materials such as mud, adobe, straw, and palm thatch, and lack window screening and in some cases, doors. Thus, there is nothing to prevent entry of the bugs. During the day, the bugs hide in crevices in the walls and roofs. If the roof is straw or another material with cracks and crevices, the bugs can hide easily and are not readily detected. Then, during the night, when the inhabitants are sleeping, the bugs emerge to feed. (Bugs may feed during the day if their hosts are nocturnal, such as bats.) Because they tend to feed on people’s faces, triatomine bugs have also come to be known as “kissing bugs.” After they bite and ingest blood, they commonly defecate on the person. The person becomes infected if T. cruzi parasites in the bug feces enter the victim’s body through mucous membranes or breaks in the skin. The unsuspecting, sleeping person may accidentally scratch or rub the feces into the bite wound, eyes, or mouth, facilitating entry of the trypanosomes. This is the principal form of T. cruzi entry into humans, but disease transmission also occurs through consumption of uncooked food contaminated with feces from infected bugs, congenital transmission (from a pregnant woman to her baby), blood transfusion, organ transplantation, and (rarely) accidental laboratory exposure. Animals can contract the disease by consuming infected prey, as in consumption of mice by household cats. The natural reservoirs of Trypanosoma cruzi are wild animals such as monkeys, opossums, amphibians, lizards, armadillos, sloths, bats, porcupines and ground squirrels. These natural hosts do not develop pathologies. However, T. cruzi is also harbored in infected humans, and domestic animals like cats, dogs, rabbits, and guinea pigs. Canine trypanosomiasis is of veterinary importance in Latin America. In nature, kissing bugs are found in hiding places such as caves, tree holes, C hollow trees, fallen logs, palm fronds and epiphytes. Though kissing bugs feed on birds, and the bugs can be quite numerous in chicken houses on farms, birds seem to be immune against infection and therefore are not considered to be a T. cruzi reservoir. The different vectors of Chagas disease have differing host preferences, so the disease transmission cycle varies accordingly. The generalized infection cycle is as follows: The infected triatomine bug ingests blood and defecates feces containing trypomastigotes near the feeding site. The victim, irritated by the bite, scratches the area, thereby rubbing the trypomastigote-containing feces into the wound or into intact but susceptible mucosal membranes, such as the conjunctiva. Once inside the host, the trypomastigotes invade cells, where they differentiate into intracellular amastigotes. The amastigotes multiply by binary fission and differentiate into trypomastigotes, which are released into the bloodstream. Cells from a number of different tissues are susceptible to infection by the trypomastigotes, and once inside, they transform into intracellular amastigotes at new infection sites. Intracellular amastigotes destroy tissues such as the intramural neurons of the autonomic nervous system in the intestine and heart, leading to digestive and heart problems, respectively. Replication resumes only when the parasites enter another cell or are ingested by another vector. The final step in the cycle is infection of the vector, which occurs when the bug feeds on an infected host containing trypomastigotes. Once ingested by the bug, the ingested trypomastigotes multiply and differentiate (amastigote and epimastigote forms) in the midgut and transform into infective metacyclic trypomastigotes in the hindgut. The feces may contain thousands of metacyclic tryptomastigotes. Management of bugs to disrupt disease transmission is possible. In many areas of Latin America, the interiors of houses are treated with pyrethroid insecticides to eliminate kissing (Triatoma) bugs. At least two South American countries have rid themselves of the problem in this manner. However, complete control is difficult 827 828 C Chalaza (pl., chalazae) to accomplish, and houses are often reinfested because some bugs escape the insecticide within the homes by hiding, or because the homes are reinvaded from nearby, untreated areas. Animal shelters are often good harborages for Triatoma, and if they are not adequately treated and are near homes, the bugs quickly disperse to the treated home. A distance of at least 1,500 m is considered necessary as a buffer zone between untreated and treated harborages. An economic and effective alternative to chemical control is bed nets, though the edges of the net must be tucked beneath the mattress to assure that bugs cannot enter. Also, the net and mattress must be large enough that the human sleeping beneath the net does not come into contact with the bed netting, because there is risk that bugs will feed through the netting if the human is immediately adjacent. The logistics and cost of meeting these requirements often prove daunting to poor people, so insecticide treatment is more practical. Likewise, improved housing and sanitation would virtually eliminate this problem, but achieving this is presently not possible due to the cost. Detection of infection is often done by examining the patient’s blood to look for trypanosomes or T. cruzi-specific antibodies. However, a procedure called “xenodiagnosis” is sometimes used, wherein laboratory-reared bugs free of trypanosomes are fed on patients, incubated, and then examined for presence of trypanosomes in the alimentary tract. Xenodiagnosis is very sensitive because the trypanosomes, even if few in number in the human host, build up to large numbers in the bug and are easily detected. Treatment of infected people is difficult because medication is usually effective only if administered during the acute phase, and many victims are unaware of their condition. This issue is compounded by the resistance of the trypanosome to medication is some regions, and by the toxicity and side effects of the drugs. During the chronic phase of infection, treatment consists mostly of treating the symptoms, and both heart replacement and intestinal surgery are practiced. Treatment in either the acute or chronic phase does not guarantee a cure. A vaccine was developed in the 1970s and it proved fairly successful, but implementation is constrained by the high cost of production. The effect of Chagas disease is measured less by mortality and more by morbidity. Chronically infected people often suffer decades of weakness and fatigue that effectively removes them from the workplace and prevents them from enjoying a normal life. This results in considerable social disruption and economic loss. A survey of the incidence of Chagas disease found that about 12% of the residents of Chile and Paraguay were infected, and in Argentina and Bolivia the rate was 8%.  Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)  Chagas  Chagas Disease: Biochemistry of the Vector  Trypanosomes  Area-Wide Pest Management References Beard CB, Gordon-Rosales C, Durvasula RV (2002) Bacterial symbionts of the Triatominae and their potential use in control of Chagas disease transmission. Ann Rev Entomol 47:123–141 Brenner RR, Stoka AM (eds) Chagas disease vectors, vols 1–3. CRC Press, Boca Raton, FL Dias JCP, Schofield CJ (1999) The evolution of Chagas disease (American Trypanosomiasis) control after 90 years since Carl Chagas discovery. Memorias do Instituto Oswaldo Cruz 94:103–121 Kirchhoff LV (1993) American trypanosomiasis (Chagas disease) – a tropical disease now in the United States. N Engl J Med 329:639–644 Zeledón R, Rabinovich JE (1981) Chagas’ disease: an ecological appraisal with special emphasis on its insect vectors. Ann Rev Entomol 26:101–133 Chalaza (pl., chalazae) A pimple-like protuberance of the body wall bearing a seta. Chalazae are commonly found on larvae. Chaudoir, Maximilien Stanislavovitch De Chalcididae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies C Chamaemyiidae A family of flies (order Diptera). They commonly are known as aphid flies.  Flies Chalkbrood A fungus disease of honey bee larvae caused by Ascosphaera apis. The disease causes the larvae to become mummified, and usually to take on chalky white appearance, but sometimes gray or black. Early in the infection process the larvae are covered with a fluffy white growth of mycelia, but later they shrink and acquire the chalky appearance. Though not usually considered serious, occasionally it can be damaging. It occurs widely, though often going unnoticed. Young bees are susceptible to infection, and normally are infected after being fed spores and then exposed to cool weather. Because the chilling is necessary, it is usually the cells at the periphery of the hive that are infected. Bees usually acquire the disease by ingestion of honey or pollen, and the spores successfully overwinter and remain infective for many years. Poor ventilation and excessive precipitation and humidity are associated with greater expression of this disease. Poor nutrition is also a factor, as is colony weakening due to other diseases, mites, and poor beekeeping practices. The pathogen can also be acquired from native bees. Management is usually accomplished by reversing the conditions that bring about expression of the disease: improved ventilation, better nutrition, keeping the hives closed during winter, and better sanitation. Destruction of infected hives is helpful. Antibiotics are not usually suggested.  Ascosphaera API  Honey Bees  Apiculture Reference Morse RA, Nowogrodzki R (1990) Honey bee pests, predators and diseases, 2nd edn. Cornell University Press, Ithaca, NY, 474 pp Chaoboridae A family of flies (order Diptera). They commonly are known as phantom midges.  Flies  Aphids Charipidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies Chaudoir, Maximilien Stanislavovitch De Maximilien de Chaudoir was born on September 12, 1816, at Ivnitza, a village in the Ukraine. He inherited the title of Baron which had been conferred on his grandfather by King Maximilien Joseph of Bavaria, and had later been made hereditary by Czar Nicholas I of Russia. His private tutor was Jean Wavre, who interested him in natural history. In 1831 he was sent to study law to Dorpat (Tartu), but there spent most of his time working on the insect collections assembled by J.F. Eschholtz. In 1834 he was made a member of the Société Entomologique de France, and the following year (at the age of 18) presented his first entomological paper at one of its meetings. After his return to the Ukraine, his entomological collection, especially of Carabidae, grew by purchase from collectors and dealers and from his own collecting expeditions in the Ukraine and other Russian territories in the Caucasus. He published frequently in the Bulletin de la Société Imperiale des Naturalistes de Moscou. In 1863 he moved to 829 830 C Champion, George Charles France, later transporting his worldwide collection of Carabidae there and working on it until his death on May 6, 1881. His publications include 108 works on Carabidae including major taxonomic revisions, and are written mainly in French, although he knew Russian, German, English, and Italian. His collection was acquired in 1952 by the Muséum National d’ Histoire Naturelle of Paris. References Ball GE, Erwin TL (1982) The Baron Maximilien de Chaudoir: inheritance, associates, travels, work, and legacy. Coleopt Bull 36:475–501 Basilewsky P (1982) Baron Maximilien de Chaudoir (1816–1881) [including a bibliography]. Coleopt Bull 36:462–474 Champion, George Charles George Champion was born in London on April 29, 1859. He became interested in beetles early in his life, and was employed in his late twenties by Frederick Godman and Osbert Salvin to collect beetles for the Biologia Centrali-Americana project in Central America. Later, he wrote for the project and assisted in editing its publications. His taxonomic work on beetles then continued, and he wrote many publications on specimens collected by his son H.G.C. Champion in India, eventually publishing more than 420 papers. He died in Woking, England, on August 8, 1927. Reference Herman LH (2001) Champion, George Charles. Bull Am Mus Nat Hist 265:54–55 Chapman, Reginald Frederick eLizaBeth a. Bernays University of Arizona, Tucson, AZ, USA Reg Chapman was born at London, England on July 2, 1930. He obtained a bachelor’s degree in zoology in 1951 at Queen Mary College of London University, United Kingdom. Then, with a scholarship from the Anti-Locust Research Centre he studied factors governing roosting behavior in locusts, first in the laboratory in London and later in Africa. Chapman lived and worked in a locust outbreak area in one of the smaller valleys of the East African rift system from 1953 to 1957. There was no town, electricity, phone or radio. He was one of the first to make quantitative observations on insect behavior in the field, and one of few combining field and lab work (he built his own house and lab). He soon learned that the locusts did not sundown, and if he really wanted to understand what was governing their behavior he needed to work as they demanded – a lesson he passed on to many. In this remote place Reg Chapman made his first contributions to behavior of locusts and grasshoppers (and lizards), including relationships between hemolymph potassium levels and feeding activity. He was strongly influenced by three extremely rigorous scientists who guided his PhD – Boris Uvarov, Donald Gunn, and John Kennedy. At the University of Ghana he studied hostfinding by tsetse flies for 2 years. In 1959, Reg was appointed to a faculty position at Birkbeck College (another college of the University of London). His main responsibility was to teach invertebrate zoology and advanced entomology. Subsequently, he developed a masters course which he taught single-handed, and this led to what he is best known for – The Insects – Structure and Function. First published in 1969, this book with its various revisions and finally a total rewrite (1998) has been a major resource for students, teachers, and researchers round the world. At Birkbeck, Chapman extended his interests in insect feeding to include the sensory system, with locusts and grasshoppers as models with a small, but quite productive, research group including Liz Bernays who was to become his wife. One finding, that insects can differentiate Chelating Agent between plants on the basis of the surface wax on the leaves, was quite novel at the time, and his interest in the plant surface continued. He initiated work on chemoreceptor physiology with another student, Wally Blaney, and on the significance of receptor numbers among other things. He was successively, lecturer, University Reader and University Professor in the University of London. In 1970, Chapman became Director of the Research Division at the Anti-Locust Research Centre and as well as continuing research, directed studies on other topics such as insect flight, plant chemistry and insects and crop plant resistance. As the Centre increased its coverage of insect pests in developing countries, he developed and was responsible for, a wide range of research programs in many parts of the world – groups in the Philippines working on brown planthopper of rice, in India on varietal resistance of sorghum to pests, in Botswana on sorghum pests, in Nigeria on a pest grasshopper, the impact of soil termites on grasslands, and the impact of pesticide use on non-target organisms, and in Mali a radar group studying grasshopper migration. He spent a week at a time with each, examining data and discussing the next steps. As well as revising The Insects at that time, he wrote a small book on locust biology. When Liz Bernays was offered a position in Berkeley in 1983, Reg Chapman, in his usual way of putting others first, went with her to an unsalaried situation. However, in 1987, the University of Arizona made irresistible offers to both, and Chapman was a professor of insect neurobiology until his retirement in 2001. In Arizona, his work on taste physiology was productive, with the help of several postdocs and students. Besides The Insects, and A Biology of Locusts, Reg wrote Host-plant Selection by Phytophagous Insects with Liz, edited four books, and wrote 20 critical reviews, ten book chapters, 110 research papers, and twenty entries for encyclopedias and other popular books. Reg’s research accomplishments and reviews, especially in the C area of feeding behavior and physiology, are a major contribution, but much of the work he did is under the authorship of others – he always wanted his students and coworkers to get the credit. Similarly, he was a major influence on hundreds of graduate students; he loved to help them, and constructively criticize all who came to him, not just the 37 he formally guided. His breadth of knowledge and his ability to quickly see to the heart of a problem was legendary. He cared deeply about getting it right and doing it properly. He will be remembered as one of the most modest, yet broadly knowledgeable and critical entomologists, and a great classroom teacher. Reg Chapman died at Tucson, Arizona on May 2, 2003. Checkered Beetles Members of Coleoptera).  Beetles the family Cleridae (order Cheek The lateral part of the head between the compound eye and the mouth. Chela The terminal portion of a limb that bears a clawlike structure. This term is sometimes used to describe the forelegs of mantids, which effectively grasp prey. Chelating Agent A molecule capable of binding metal atoms; one example is EDTA, which binds Mg++. 831 832 C Chelicera (pl. chelicerae) Chelicera (pl. chelicerae) The pincer-like first pair of mouthpart appendages in arachnids. Chelisochidae A family of earwigs (order Dermaptera). They sometimes are called black earwigs.  Earwigs Chelonariidae A family of beetles (order Coleoptera). They commonly are known as turtle beetles.  Beetles Cheloniform Larva A larva that is oval or circular, strongly flattened, and with a concealed head; resembling a turtle. Chemical Ecology of Insects heather J. mCausLane University of Florida, Gainesville, FL, USA Ecology is the study of the effects on organisms of their biotic (i.e., living) and abiotic (i.e., nonliving) environments. Chemical ecology is simply the study of the effects on organisms of chemicals produced by living organisms in their environment (i.e., their biotic environment). Thus, chemical ecology is a sub-discipline of ecology, emphasizing interactions within and among species that are mediated by chemicals. The behavior and/or physiology of all major groups of organisms examined to date, from bacteria to plants to insects to humans, are to some extent influenced by chemicals produced and released into the environment by other organisms. Chemical ecology as a recognized scientific discipline came into being in the early 1970s. At this time there was increasing interest in nonpesticidal methods of insect control because of the growing awareness of environmental problems caused by persistent, toxic pesticides. Simultaneous rapid advances in the instrumentation required to analyze minute amounts of chemicals found in nature (i.e., gas chromatographs, mass spectrometers and nuclear magnetic resonance spectroscopes) spurred the development of chemical ecology. Over the last 30 years, the breadth of insect chemical ecology has increased from the study of insects interacting within one trophic level to two-trophic level interactions involving insects and their food organisms to multitrophic-level interactions. Chemical ecologists work on problems ranging from applied to basic in nature. For many chemical ecologists, the primary goal of their research is to find ways to reduce insect populations to acceptable levels without using broad-spectrum insecticides by changing the insects’ behavior so that they inflict less harm on our food, our livestock and us. Other chemical ecologists study the chemical ecology of insects to understand better the more basic aspects of their species of interest; who is related to whom, why they eat a particular food plant and not others, how they defend themselves, etc… The chemicals that mediate interactions between organisms in nature are termed semiochemicals. This comes from the Greek word “semeon” which means a mark or a signal. The semiochemicals that mediate interactions between organisms of the same species (intraspecific interactions) are pheromones whereas semiochemicals that mediate interactions occurring between different species (interspecific interactions) are allelochemicals. Pheromones were the first semiochemicals that received intense scientific study and to date, well over 500 have been identified, most of these being sex attractant pheromones of Lepidoptera. Insects use pheromones to communicate with members of their species to facilitate reproduction (sex pheromones), locate food sources (trail Chemical Ecology of Insects pheromones), warn of danger (alarm pheromones) and maintain the function and cohesion of large colonies (many pheromones of social insects). We can use pheromones to disrupt communication among members of a pest species so that they do less damage to our crops and animals. We can also use pheromones to detect the presence of insect pests, monitor their changes in population size, and time applications of insecticides or other control measures. Interspecific interactions, involving insects and other insects, plants or other organisms, are mediated by allelochemicals. These chemicals are significant to organisms of a species different from their source, for reasons other than food. Three types of allelochemicals are recognized: allomones, kairomones, and synomones. The designation of a particular chemical depends on which species in the interaction benefits and which, if any, is harmed after perceiving the chemical. For example, an allomone is a chemical that is produced or acquired by one organism that causes a behavioral or physiological response in the receiver of another species that is beneficial to the emitter but not to the receiver. The organism, either plant or insect, releasing the allomone is benefited by preventing a potential predator from eating it. The receiver of the allomone is harmed because it is denied what would otherwise be a suitable meal. Many plants produce allomones that repel herbivorous insects and protect their tissues from herbivore damage. Ecologists, such as Gottfried Fraenkel, Paul Erhlich and Peter Raven, in the 1950s and 1960s suggested that the huge diversity of insectrepellent and deterrent chemicals found within angiosperm plants might actually have evolved in response to the selection pressure of feeding by herbivorous insects. Today, most ecologists believe that these secondary plant compounds, so named because they did not appear to have a function in the primary metabolism of plants as nutrients or structural compounds, probably arose as defenses against plant pathogens and to help in plant-plant competition rather than as defenses against insects; however, their effects on insects are undisputed. C Allomones in the cabbage plant family (the Brassicaceae) are the reason that relatively few insects feed on these plants. Most members of this plant family produce sulfur-containing compounds called glucosinolates that deter feeding of herbivores. These chemicals give mustard, collard and turnip greens their distinct taste (which many humans consider an “acquired” taste). Volatile breakdown products of the glucosinolates, the isothiocyanates and other compounds, which repel most insects, give the condiment mustard its pungent aroma. Plants in the squash, pumpkin and melon family (the Cucurbitaceae) are well defended with exceedingly bitter large steroidtype molecules called cucurbitacins. Most insects will not feed on wild species of the Cucurbitaceae because of the bitter cucurbitacins. However, when humans began domesticating these crops for human consumption, they selectively bred out the bitter taste and reduced the levels of the allomones that the plants use to defend themselves. Thus, cucurbit species grown for human consumption are non-bitter and are readily attacked by many pest insects. Chemical ecologists can apply their knowledge of plant-produced allomones for pest management by developing them as biopesticides or by increasing their levels in non-edible portions of a crop with the help of plant breeders. Azadirachtin from the Indian neem tree Azadirachta indica, oils of various herbs such as mint, rosemary, and thyme, pyrethrum from chrysanthemums, and rotenone from the roots of the legume Derris, among others, have all been developed as botanical insecticides or plant protectants because of their toxic or repellent effects on insects. Many insect species produce allomones, often surprisingly similar in structure to those of plants, which repel or deter predators that may try to eat them. For example, Heliconius butterflies and Zygaena moths release the cyanogenic glycosides, linamarin and lotaustralin, which break down to release hydrogen cyanide, when predators threaten them. Coincidently, clover and birdsfoot trefoil also rely on the same cyanogenic glycosides to 833 834 C Chemical Ecology of Insects deter herbivores and grazers. The venoms of wasps, bees and ants are allomones that are highly deterrent to predators, including the human variety. The list of allomones synthesized or acquired by insects to defend themselves is lengthy and is reviewed elsewhere. A second group of allelochemicals is the kairomones. A kairomone is a semiochemical that is produced or acquired by an organism that causes a behavioral or physiological response in the receiver of a different species that is beneficial to the receiver but not to the emitter. We know that many species of predators and parasitoids are attracted to their hosts or prey by volatile chemicals (kairomones) released by the prey or from by-products of the prey (e.g., pheromones and excretory products such as frass and honeydew). For example, some species of ant-decapitating flies in the genus Pseudacteon (family Phoridae) are attracted to their hosts, worker fire ants in the genus Solenopsis (family Formicidae), by the odor of the ants’ alarm pheromone. Specialist herbivorous insects (those that oviposit on and whose larvae feed on only a narrow range of plant species) use distinct chemicals produced by their host plants as signposts or guides to their plants. For example, moths that specialize on plants in the cabbage family, such as the cabbage white butterfly Pieris rapae, are attracted to the volatile isothiocyanates, which are allomones for most other insects that do not feed on cabbage. Thus a kairomone can be a chemical cue that the emitter legitimately uses as a pheromone or an allomone but that an illegitimate receiver turns to its advantage. A single chemical compound could be called a pheromone, a kairomone or an allomone, depending on who benefits, the emitter or the receiver. The last class of semiochemicals that is recognized today is the synomones. This term was proposed for chemicals that mediate mutualistic interactions in which both the emitter and the receiver benefit. For example, the blend of chemicals released by plants when under attack by herbivorous insects may properly be called a synomone when it attracts parasitoids or predators that then parasitize the insect herbivore, thus reducing the damage to the plant. The receiving organism, the parasitoid, benefits by being provided an additional source of cues with which to help it locate a potential host. For example, the braconid parasitoid, Cardiochiles nigriceps, is attracted to tobacco, cotton and corn plants that have been damaged by larvae of its host, the tobacco budworm Heliothis virescens (Noctuidae), by volatile chemicals that are released by the damaged plants. Interestingly, the synomonal blend released by the plant is specific to the herbivorous insect that is feeding on it; the parasitoid ignores plants that have been damaged by larvae of a closely related noctuid, the corn earworm Helicoverpa zea, which is not a viable host for this parasitoid. The odor of flowers that attracts pollinating insects can also be considered synomonal because it is beneficial to both the flower whose pollination is ensured and, usually, to the receiving insect, which is guided to a necessary resource – nectar, pollen, or some other reward. However, some plants have turned their synomones into allomones, by attracting insects and then providing them with nothing in return. For example, many species of orchids in the Mediterranean and other places in the world attract male bees and wasps of certain species with floral odors that mimic the sex pheromone of their own species. The males are attracted to the flower and attempt to mate with it. During this “pseudocopulation”, the flower is pollinated but the male insect gains nothing, and is perhaps even harmed by wasting its time and energy on an activity that will not increase its genetic fitness.  Alarm Pheromones  Allelochemicals  Attraction of Insects to Organic Sulfur Compounds in Plants  Host Location in Parasitic Wasps  Host Marking Pheromones  Host Plant Selection by Insects  Natural Enemy Attraction to Plant Volatiles  Pheromones  Plant Secondary Compounds and Phytophagous Insects Chestnut Gall Wasp Classical Biological Control in Japan  Pyrrolizidine Alkaloids and Tiger Moths  Sex Attractant Pheromones  Social Insect Pheromones  Tritrophic Interactions References Bell WJ, Cardé RT (eds) (1995) Chemical ecology of insects 2. Chapman & Hall, New York. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573 Dicke M, Grostal P (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Ann Rev Ecol Syst 32:1–23 Harborne JB (2001) Twenty-five years of chemical ecology. Nat Prod Rep 18:361–379 Haynes KF, Yeargan KV (1999) Exploitation of intraspecific communication systems: illicit signallers and receivers. Ann Entomol Soc Am 92:960–970 Morehead SA, Feener DH Jr (2000) Visual and chemical cues used in host location and acceptance by a dipteran parasitoid. J Insect Behav 13:613–625 Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422 Chemigation C Chestnut Gall Wasp Classical Biological Control in Japan seiiChi moriya National Agricultural Research Center, Tsukuba, Japan The chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), is one of the most serious chestnut-tree pests. It is thelytokous and univoltine. This wasp is now thought to have originated in China and to have been accidentally introduced from there into Japan around 1940. Chestnut gall wasp was also introduced into South Korea and Georgia, in the southeastern United States, in 1958 and 1974, respectively, probably via Japan. The adult emerges from the gall during a relatively brief part of the early summer, and immediately lays eggs inside chestnut buds (Fig. 42) When the buds start to develop the following spring, immature larvae that hatched in the previous year resume their growth, and the galls begin to swell rapidly. Consequently, in heavily infested trees, the yields of chestnuts are diminished, and the trees themselves may die. Application of agricultural chemicals, including insecticides, through the irrigation system. Chemokinesis A kinesis response with respect to a chemical gradient. Chemoreceptor A sense organ that perceives chemical stimuli. Chemotaxis A taxis with reference to a chemical gradient (taste, odor). Chestnut Gall Wasp Classical Biological Control in Japan, Figure 42 Dryocosmus kuriphilus ovipositing on the bud of a chestnut tree (photo by S. Moriya). 835 836 C Chestnut Gall Wasp Classical Biological Control in Japan After entering Japan, the pest spread so fast that it was distributed throughout most of Japan by the end of the 1950s, seriously damaging chestnut production. Because the larva of chestnut gall wasp is protected by the thick wall of the gall, no method of chemical control was feasible. But chestnut gall wasp could be controlled very effectively at first by using resistant chestnut varieties. Therefore, all of the susceptible varieties of chestnut trees were rapidly replaced by resistant ones. However, a stronger strain of chestnut gall wasp emerged, and the galls began to appear again around 1960, even on the highly resistant varieties. The breakdown of resistance alarmed chestnut growers, because the use of resistant varieties was the only available method of controlling the pest. After diplomatic relations between Japan and China were re-established in 1972, a Japanese entomologist found that chestnut gall wasp had been recorded on a Chinese chestnut, Castanea mollissima Blume, much earlier in China than in Japan. Furthermore, it was found that chestnut gall wasp had not been a serious pest in China even though Chinese chestnut varieties were highly susceptible to chestnut gall wasp. Thus, a Chinese parasitoid, Torymus sinensis Kamijo (Hymenoptera: Torymidae), was selected for introduction to Japan. In the spring of 1982, a mere 260 mated females were released onto Japanese chestnut trees, C. crenata Sieb. et Zucc., growing on the grounds of the National Institute of Fruit Tree Science (NIFTS), Tsukuba, about 50 km northeast of Tokyo. Like chestnut gall wasp, the parasitoid is univoltine, and yet the population of T. sinensis in Japan increased steadily year after year. The density of T. sinensis females in 1989 was more than 25 times higher than that in 1983. T. sinensis is now completely dominant among the native parasitoids of chestnut gall wasp at NIFTS. The effect of the 1982 release of T. sinensis on the chestnut gall wasp population was evaluated by observing gall formation ratios (Fig. 43) on chestnut trees. Infestation of chestnut gall wasp steadily decreased after the release until it reached a level of about 3% in 1988, then decreased to < 1% in the early 1990s. Chestnut Gall Wasp Classical Biological Control in Japan, Figure 43 Torymus sinensis attacking a gall of Dryocosmus kuriphilus (photo by S. Moriya). Thus, the single release of T. sinensis at NIFTS ultimately reduced chestnut gall wasp infestation to a level far below that which chestnut trees can tolerate (the tolerable injury limit is about 30% infestation of current shoots). The rate at which T. sinensis expanded its distribution range was also determined. The parasitoid spread gradually during the first few years, at a rate of <1 km/year, followed by more rapid and accelerated spreading in the next few years. In the spring of 1989, T. sinensis was detected in an area more than 12 km from NIFTS. Since then, a steady expansion, at a constant rate of about 60 km per year (=per generation), has been observed. Consequently, the parasitoids seem to have dispersed by themselves several hundred kilometers from the point of release by the mid1990s. In Kumamoto Prefecture, in southwestern Japan, T. sinensis was also released in 1982 and was later confirmed to have become established there. However, unlike the case in Tsukuba, the population density did not increase significantly. This Chewing and Sucking Lice (Phthiraptera) delay in population increase might be attributable to the high mortality of T. sinensis associated with the activity of native facultative hyperparasitoids. A native Japanese parasitoid, T. beneficus Yasumatsu et Kamijo, which is closely related to T. sinensis, consists of at least two strains that differ from each other only in the time of the adult emergence period. The female of either strain of T. beneficus has a shorter ovipositor sheath than does the female of T. sinensis, whereas the male T. beneficus cannot be distinguished morphologically from the male T. sinensis. The emergence period of T. sinensis is in between those of the two strains of T. beneficus and more or less overlaps them. Thus, it should be noted that crossing between T. sinensis and T. beneficus occurs under natural conditions. When these two torymids were artificially crossed, morphologically intermediate females were observed among the offspring, and they were fertile. Although there was no evidence of direct competition between T. sinensis and T. beneficus, the number of T. beneficus apparently decreased after T. sinensis was introduced into the chestnut groves at NIFTS. References Moriya S, Inoue K, Mabuchi M (1989) The use of Torymus sinensis to control chestnut gall wasp, Dryocosmus kuriphilus, in Japan. Food Fertilizer Technology Center Technical Bull 118:1–12 Moriya S, Inoue K, Shiga M, Mabuchi M (1992) Interspecific relationship between an introduced parasitoid, Torymus sinensis Kamijo, as a biological control agent of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu, and an endemic parasitoid, T. beneficus Yasumatsu et Kamijo. Acta Phytopathol Entomol Hung 27:479–483 Murakami Y (1997) Natural enemies of the chestnut gall wasp: approaches to biological control. Kyushu University Press, Fukuoka, Japan, 308 pp (in Japanese) Murakami Y, Gyoutoku Y (1995) A delayed increase in the population of an imported parasitoid, Torymus (Syntomaspis) sinensis (Hymenoptera: Torymidae) in Kumamoto, southwestern Japan. Appl Entomol Zool 30:215–224 Shiga M (1997) Classical biological control of the chestnut gall wasp, Dryocosmus kuriphilus: present status and interactions between an introduced parasitoid, Torymus C sinensis, and native parasitoids. In: Yano E, Matsuo K, Shiyomi M, Andow DA (eds) Biological invasions of ecosystem by pests and beneficial organisms. National Institute of Agro-Environmental Sciences, Tsukuba, Japan, pp 175–188 Chevrolat, Louis Alexandre Auguste Auguste Chevrolat was born in Paris on March 29, 1799. He had numerous sisters, and was brought up not by his parents but by his grandmother and a maternal aunt in the town of Melun. He showed an early interest in natural history, collecting birds and all sorts of insects, but decided to specialize in beetles. He made friends with notable entomologists (Latreille, Duméril, Dejean, and Guérin) and began to publish descriptions of new species of insects, the first being Doryphora 21-punctata published in Magasin de Zoologie. He was charged by Duponchel to edit the section on chrysomelids for the dictionary directed by d’ Orbigny. In 1832 he was a founding member of the Société Entomologique de France, and in 1875 was elected an honorary member of it. He published more than 180 papers during his lifetime, his two most frequent outlets were Annales de la Société Entomologique de France, and Magasin Zoologique, and he published more on Curculionidae (in the broad sense) than on any other insect family. He died on December 16, 1884. Reference Reiche L (1884) Notice necrologique sur Auguste Chevrolat. Ann Soc Entomol Fr (6) 4:357–360 Chewing and Sucking Lice (Phthiraptera) This order of wingless ectoparasitic insects is thought to have evolved from barklice (Psocoptera). 837 838 C Chewing and Sucking Lice (Phthiraptera) Certainly it is not difficult to imagine insects dwelling in animal nests (many Psocoptera) evolving into insects that dwell on birds and mammals (Phthiraptera), and morphologically they are similar. Traditionally, the order Phthiraptera has been treated as two separate orders (or two suborders), the chewing lice (Mallophaga) and the sucking lice (Anoplura). However, modern treatment of this group has Mallophaga divided into three suborders (Amblycera, Rhyncophthirina, Ischnocera), with Anoplura the fourth suborder. Both chewing and sucking lice are obligate parasites, and cannot survive long off their hosts. They are the only truly parasitic group among the exopterygote insects. They display remarkable host specificity, and most individuals spend their entire life cycle on a single host. They relocate opportunistically only when individuals are in close proximity, and so they have developed diverse morphology due to their high degree of isolation. Their basic specializations are based on feeding on skin debris, fur, feathers, and blood. The order name (Phthiraptera) is derived from the Greek words “phtheir” (louse), plus “a” (without), and “pteron” (wing). Classification About 3,000 species of chewing lice from around the world are distributed in three suborders, and often associated with specific bird hosts, but sometimes mammals. There are about 15 families of sucking lice, containing only about 500 species, though many species probably remain to be described. Most species of lice are quite host specific. Some families have common names that reflect their hosts. Class Insecta Order Phthiraptera Suborder Amblycera Family Menoponidae – poultry lice Family Trinotonidae Family Laemobothriidae – hawk lice Family Ricinidae – hummingbird lice Family Trochiliphagidae Family Boopidae – marsupial chewing lice Family Gryropidae – guinea pig lice Family Trimenoponidae – marsupial lice Family Abrocomophagidae Suborder Ischnocera Family Trichodectidae – mammal chewing lice Family Philopteridae – bird lice Family Heptapsogasteridae Suborder Rhyncophthirina Family Haematomyzidae Suborder Anoplura Family Polyplacidae – spiny rat lice Family Linognathidae – pale lice Family Enderleinellidae – squirrel lice Family Hoplopleuridae Family Neolinognathidae Family Hamophthiriidae Family Ratemiidae Family Microthoraciidae Family Echinophthiriidae – seal lice Family Pthiridae – pubic lice Family Pedicinidae Family Pecaroecidae – peccary lice Family Hybothiridae Family Haematopinidae – ungulate lice Family Pediculidae – body lice The hosts of the chewing lice, other than those suggested by the aforementioned common names, are hummingbirds for trochiliphagids; ducks, geese and swans for trinotonids; a rodent for the only known abrocomophagid; many birds for heptapsogasterids; and elephants and warthogs for haematomyzids. The sucking lice feed on mammals. Interestingly, although humans have domesticated animals for thousands of years, they have rarely acquired lice from them. Instead, the lice associated with humans are in the genera Pthirus and Pediculus, which they share with the higher primates, particularly the apes. Characteristics Chewing lice are small ectoparasites, generally measuring 0.5–6 mm long, and wingless. The head Chewing and Sucking Lice (Phthiraptera) is wide, or at least wider than the thorax (Fig. 44), and bears small eyes and short antennae(3–5 segments). The form of the antenna varies; in the suborder Amblycera they normally are capitate, whereas in the suborder Ischnocera they are filiform. Ocelli are absent. The mouthparts, as suggested by the common name, are the chewing type. The body is flattened and has six or fewer spiracles. The legs have one or two claws. Cerci are lacking. The metamorphosis is incomplete (hemimetabolous development). These hemimetabolous insects have three nymphal instars. C Sucking lice also are small ectoparasites, measuring only 0.5–5 mm in length, and oval in shape. Their head is narrow, a distinguishing character relative to the chewing lice (Fig. 45). Their eyes are reduced or absent; ocelli are absent. The antennae are short, and 3–5 segmented. The mouthparts, which are about as long as the head, are highly modified and are adapted for piercing and sucking. The mouthparts are retracted into the head when not in use. The body is dorsoventrally flattened. The segments of the thorax are fused, and the thoracic spiracles located dorsally. The abdominal Labrum Mandible Labium Maxillary palp Ventral ledge of antennal groove Antenna Antenna groove Temple Gula Clypeus Preocular slit Antenna Eye Transverse suture Pleural ridge Longitudinal suture Pronotum Spiracle Mesonotum Pleural ridge Metanotum 1 Pleural ridge 2 Spiracle of 3rd Abdominal segment 3 4 5 6 Episternum Pleural ridge Sternal apophysis Sternum Coxa Sternum Pleural ridge Antecoxal sclerite Coxa Trochanter Femur Tibia Tarsus Pretarsus 7 8 9 10th abdominal Segment Anus Gonopore Chewing and Sucking Lice (Phthiraptera), Figure 44 A diagram of a chewing louse showing a dorsal view (left) and a ventral view (right). 839 840 C Chewing and Sucking Lice (Phthiraptera) Labrum Clypeus Clypeofrontal suture Frons Postfrontal suture Ocular lobe Prothoracic pleural ridge Mesothoracic pleural ridge Antenna Tibia Eye Femur Trochanter Coxa Thoracic sternum Tergal pit Metathoracic pleural ridge Median tergites Spiracle Paratergites Chewing and Sucking Lice (Phthiraptera), Figure 45 A diagram of a sucking louse showing a dorsal view (left) and a ventral view (right). segments are distinct. The tarsi consist of only one segment, and there is only one large claw on each tarsus. Cerci are absent. Metamorphosis is incomplete, as with the chewing lice. Biology Probably all species of birds are affected by chewing lice, but only about 20% of mammals host these lice. The eggs are attached to the feathers or hairs of the host with glue. The nymphs and adults feed on feathers, hair, skin, blood, and the oils produced by the skin. Blood feeding seems to be of minor importance, and substantial infestations can occur with little ill effect, though the common behavior among birds of taking a “dust bath” is probably an attempt to rid themselves of lice. However, when populations are very high, they can be of veterinary importance, especially to young fowl. They are not important in disease transmission. They spread from animal to animal by body contact, and often leave their host soon after it perishes. Sucking lice feed only on blood of mammals. Two (or three, depending on how Pediculus humanus is treated) species affect humans, and about 12 species affect domestic animals. The families tend to contain lice with very similar feeding habits. For example, the echinophthiriids feed on seals, sea lions, walruses and river otter; the enderleinellids on squirrels; the haematopinids on ungulates such as pigs, cattle, horses and deer; the hoplopleurids on rodents and insectivores; the linognathids on even-toed ungulates such as cattle, sheep, goats, reindeer and deer, and on canids such as dogs, foxes and wolves; the pecaroecids on peccaries; the pediculids on the head and body of humans; the polyplacids on rodents and insectivores; and pthirids on gorillas and humans. The eggs generally are cemented to the hairs of the host. There are three nymphal instars in nearly all species. Because lice are co-evolved (co-speciated) with their specific hosts, the extinction of hosts results in extinction of lice species as well. Due to pervasive host extinction (for example, about 67% of the genera of mammals are thought to be extinct), many species of lice likely have disappeared. However, lice Chikungunya do not preserve well, and are virtually absent from the fossil record, so their history is not well known.  Human Lice References Arnett RH Jr, (2000) American insects, 2nd edn. CRC Press, Boca Raton, FL, 1003 pp Ash JS (1960) A study of the Mallophaga of birds with particular reference to their ecology. Ibis 102:93–110 Durden LA, Musser GG (1994) The sucking lice (Insecta, Anoplura) of the world; a taxonomic checklist with records of mammalian hosts and geographical distributions. Bull Br Mus Nat Hist 218:1–90 Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge, UK, 755 pp Hopkins GHE (1949) The host-associations of the lice of mammals. Proc Zool Soc Lond 119:387–605 Kim KC, Ludwig HW (1978) The family classification of Anoplura. Syst Entomol 3:249–284 Kim KC (1987) Order Anoplura. In: Stehr FW (ed) Immature insects, vol 1 Kendall/Hunt Publishing, Dubuque, IA, pp 224–245 Kim KC, Pratt HD, Stpjanovich CJ (1986) The sucking lice of North America. An illustrated manual for identification. Pennsylvania State University Press, University Park, Pennsylvania. Price MA, Graham OH (1997) Chewing and sucking lice as parasites of mammals and birds. U.S. Department of Agriculture Technical Bulletin 1849, 309 pp Price RD (1987) Mallophaga. In: Stehr FW (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA, pp 215–223 C he relocated to the Temporary University in Ghangsha, Hunan, and then to Southwestern Associated University in Kunming, Yunan. The latter involved an incredible 68-day overland trek by Chiang and his fellow students. After graduating, he joined the Agricultural Research Institute in Kunming. Kunming was the terminus of the Allied Forces air supply route from India, and Chiang interacted with a military anti-malaria unit, which allowed him to make important contacts and to improve his English. Chiang contacted the University of Minnesota and enrolled in 1945. He completed his graduate studies in 1948, and accepted a temporary position studying European corn borer. This, and a temporary stint as an instructor of entomology at Minnesota, led to a permanent faculty position where he worked until retiring in 1984. Huai Chiang is best known for his work on corn pests, and he authored about 250 publications, including two articles in the Annual Review of Entomology. He was considered an expert in biological control and insect ecology. He was active in international and government agencies and programs, and was honored by several universities and countries for his research and service. He died on March 30, 2005, in Ithaca, New York. Reference Radcliffe T (2005) Huai C. Chiang. Am Entomol 51:126–127 Chewing Mouthparts Mouthparts that consist of opposable, non-sucking structures; biting mouthparts.  Mouthparts of Hexapods Chiang, Huai C. Huai Chiang was born February 15, 1915, in Sunjiang County, Jiansu Province, China. He attended Tsinghua University in Beijing, where he was first exposed to entomology. During the Sino-Japanese war of 1937–1945, his studies were disrupted and Chigger A mite of the family Trombiculidae.  Mites Chikungunya keLLy roe, kenneth w. mCCravy Western Illinois University, Macomb, IL, USA Chikungunya is an Alphavirus in the family Togaviridae. It is an arthropod-borne virus (arbovirus) 841 842 C Chikungunya transmitted to humans primarily by Aedes aegypti, the yellow fever mosquito. Togaviruses replicate in the cytoplasm and mature by budding out from the cell membrane. They are not very stable in the environment and are easily destroyed or inactivated by disinfectants. The genus Alphavirus has 27 member viruses, all of which are mosquitoborne. Eleven of these viruses cause disease in humans, and eight of them produce significant epidemics: Chikungunya, Ross River virus, eastern, western, and Venezuelan equine encephalitis, O’nyong-nyong, Mayaro, and Sindbis. Chikungunya virus is widespread throughout Africa, India, and Southeast Asia, including the Philippines. Devastating epidemics, sometimes lasting for months or years, have occurred and reoccurred in Africa and Asia. A majority of an urban population can be infected within a few months. Under these circumstances A. aegypti can maintain the virus in a human-mosquito-human cycle. Symptoms, Treatment, and Prevention Chikungunya received its name from a Swahili or Makonde term meaning “that which bends up,” referring to the stooped posture of patients afflicted with severe joint pain associated with this disease. Chikungunya is a debilitating but generally selflimiting febrile viral disease. It is characterized by arthralgia or arthritis, typically in the small joints of the extremities, such as ankles, knees, toes, wrists, and fingers. Other symptoms include high fever, headache, nausea, vomiting, photophobia, maculopapular rash, buccal and palatal enanthema, myalgia, chills, flushed face, lymphadenopathy, stooped posture, and, in some cases, bleeding from the nose and mild hemorrhaging. The incubation period can range from 2–12 days, but is usually 3–7 days. The onset of this disease is sudden, and is marked by a rapid increase in body temperature followed by severe pain in the limbs and spine. These symptoms usually last 3–5 days followed by recovery in 5–7 days. However, the virus has shown signs of greater virulence in the recent Indian Ocean epidemic. Occasionally joint pain can reoccur intermittently for months or even years. Unapparent Chikungunya infections do occur, but how commonly this occurs is unknown. It is thought that life-long immunity is conferred through clinical or unapparent infection with the Chikungunya virus. Chikungunya is diagnosed based on symptoms and serological testing. At this time there is no cure for the disease. Vaccine trials were carried out in 2000, but funding for the project was eliminated and the project was discontinued. There is no vaccine or antiviral treatment available for Chikungunya fever. The illness is generally selflimiting and the symptoms usually resolve over time. Symptomatic treatments are recommended after excluding other more dangerous diseases, such as dengue and yellow fever. These treatments include rest, plenty of fluids, and acetaminophen, naproxen, ibuprofen, or paracetamol to relieve fever and aching. Aspirin should not be taken to treat Chikungunya fever. An infected person should stay indoors to protect against further mosquito exposure and transmission of the disease to other people during the first few days of illness. Other measures to reduce the spread of Chikungunya fever include use of insecticides to kill adult and larval mosquitoes. Measures that can be taken by individuals include elimination of standing water where mosquitoes can breed, use of insect repellents containing permethrin or DEET, wearing long pants and long-sleeved shirts, and use of screens on windows and doors to prevent entry by mosquitoes. The present strain of the Chikungunya virus in the Indian Ocean region appears to be more virulent than those causing previous epidemics. A number of patients have developed complications and died. The death of a 10 year old boy had no other plausible explanation; Chikungunya virus was the only pathogen present in his blood. The death toll from the Chikungunya virus continues to increase. In the Indian Ocean region, 77 death certificates issued in January through March 2006 state Chikungunya Chikungunya as the cause of death, although for most cases co-morbidity played a significant role. Epidemiology Aedes aegypti is the most important vector of the viruses of Chikungunya, dengue, and yellow fever. This mosquito is widely distributed between 40°N and 40°S latitude. Aedes aegypti does not thrive in hot dry climates and is vulnerable to extreme temperatures. The primary food source for female A. aegypti is blood from a vertebrate host; male mosquitoes do not suck blood. The blood meal for A. aegypti is commonly human blood, but they will also feed on other mammals and birds. Aedes aegypti has been recognized as the chief vector of Chikungunya for approximately 50 years, although other species of Aedes (see below) and Culex have also been implicated. In the 1950s an aggressive mosquito control campaign greatly reduced A. aegypti on the island of Réunion, east of Madagascar in the Indian Ocean. Reducing the primary vector of Chikungunya should have reduced or eliminated the spread of this disease. This proved not to be the case. Aedes albopictus, the Asian tiger mosquito, was not viewed as a significant threat, and remained abundant due to lack of control measures. This mosquito is of Asian origin, and is usually found far away from human habitation. Aedes albopictus feeds readily on many species of mammals and birds. It was assumed to be an inefficient vector of Chikungunya in nature because of its habit of feeding on non-susceptible hosts that do not contribute to the transmission cycle. However, the recent outbreak and epidemic of Chikungunya on Réunion, with roughly 265,000 people infected (34% of the total population of the island), indicates that A. albopictus can be an effective vector of Chikungunya. The Chikungunya virus was first isolated from the blood serum of a febrile human by R.W. Ross in 1953 in the Newala district of Tanzania. It was later recovered in Bangkok in 1958, and C has more recently caused massive epidemics in many countries. The Chikungunya virus is geographically distributed in Africa, India, and Southeast Asia. The virus is maintained in Africa through a sylvatic transmission cycle between Aedes luteocephalus, Aedes furcifer, or Aedes taylori mosquitoes and wild primates. The Chikungunya virus is transmitted among baboons and humans by A. furcifer. In Africa, baboons are the primary vertebrate host from which the virus extends into the human population. In Asia, the Chikungunya virus is transmitted from human to human by A. aegypti through an urban transmission cycle. Because neither a vertebrate reservoir nor a sylvan transmission cycle has been identified outside of Africa, it is thought that the Chikungunya virus originated in Africa and was later introduced into Asia and other parts of the world. The Chikungunya virus has caused outbreaks and epidemics in East Africa (Tanzania and Uganda), Austral Africa (Zimbabwe and South Africa), West Africa (Senegal and Nigeria), and Central Africa (Central African Republic and Democratic Republic of the Congo) since its discovery in 1953. Chikungunya virus in the Indian Ocean region has recently caused one of the largest epidemics reported in the last 40 years, involving hundreds of thousands of people. The severity and magnitude of the epidemic has surprised public health specialists and the governments. Chikungunya virus infection has steadily increased within the human population. In 2005 there were an estimated 12,400 cases reported, whereas in 2006 there were over 200,000 cases reported through April alone. These numbers do not include cases that are misdiagnosed or unreported. It has been suggested that many cases of Chikungunya fever are misdiagnosed as dengue fever. The clinical symptoms of Chikungunya infection often mimic those of dengue fever, and Chikungunya virus is present in regions where dengue virus is endemic. There have been documented cases of simultaneous co-infection with dengue and Chikungunya viruses. A human-mosquito-human 843 844 C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) cycle has sustained urban epidemics involving A. aegypti as the vector, and Chikungunya-dengue and Chikungunya-yellow fever outbreaks have been described. The association of Chikungunya, dengue, and yellow fever is likely due to transmission by the same vector species, A. aegypti. Aedes aegypti is not limited to Africa and Asia, so there is the possibility that the Chikungunya virus could spread elsewhere. In 2006, six complete genome sequences of selected Chikungunya viral isolates were studied. Results of this study suggest that the Chikungunya virus can adapt to new environmental conditions, and can evolve the ability to survive in vectors that it was incapable of surviving in previously. These results underscore the possibility that the Chikungunya virus can spread to other parts of the world. The Chikungunya virus continues to be a growing problem since its discovery in 1953. References Enserink M (2006) Massive outbreak draws fresh attention to little-known virus. Science 311:1085 Effler PV, Pang L, Kitsutani P, Vorndam V, Nakata M, Ayers T, Elm J, Tom T, Reiter P, Rigau-Perez JG, Hayes JM, Mills K, Napier M, Clark GG, Gubler DJ (2005) Dengue fever, Hawaii, 2001–2002. Emerg Infect Dis 11:742–749 Higgs S (2006) The 2005–2006 Chikungunya epidemic in the Indian Ocean. Vector Borne Zoonotic Dis 6:115–116 Jupp PG, McIntosh BM (1988) Chikungunya disease. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, FL, pp 137–157 Kettle D (1995) Medical and veterinary entomology, 2nd edn. CABI Publishing, New York. McIntosh BM, Jupp PG, Dos Santos I (1977) Rural epidemic of Chikungunya in South Africa with involvement of Aedes furcifer and baboons. S Afr J Sci 73:267–269 Myers RM, Carey DE (1967) Concurrent isolation from patient of two arboviruses, Chikungunya and dengue type 2. Science 157:1307–1308 Reiter P, Fontenille D, Paupy C (2006) Aedes albopictus as an epidemic vector of Chikungunya virus: another emerging problem? Lancet Infect Dis 6:463–464 Ross RW (1956) The Newala epidemic. III. The virus: isolation, pathogenic properties and relationship to the epidemic. J Hyg 54:177–191 Salvan M, Mouchet J (1994) Aedes albopictus and Aedes aegypti at Ile de la Réunion. Ann Soc Belg Med Trop 74:323–326 Tesh RB, Gubler DJ, Rosen L (1976) Variation among geographic strains of Aedes albopictus in susceptibility to infection with Chikungunya virus. Am J Trop Med Hyg 25:326–335 World Health Organization. Chikungunya and dengue in the south west Indian Ocean. Available at http://www. WHO.int/csr/don/2006_03_17/en. Accessed 25 May 2007 Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) dakshina r. seaL, waLdemar kLassen University of Florida, Homestead, FL, USA The common names of Scirtothrips dorsalis are chilli thrips, chili thrips, castor thrips, Assam thrips, strawberry thrips and yellow tea thrips. Taxonomists now regard Neophysopus fragariae Girault, Heliothrips minutissimus Bagnall, Anaphothrips andreae Karny and S. dorsalis var. padmae Ramakrishna as synonyms of S. dorsalis Hood. Economic Importance Scirtothrips dorsalis has long been a pernicious pest of various vegetable crops, cotton, citrus and other fruit and ornamental crops in its principal range in southern Asia, where it may kill newly emerged seedlings, severely distort leaves and scar the surface of fruits of its favored hosts. In India, S. dorsalis is a serious pest of castor bean (Ricinus communis L.), chilli pepper (Capsicum annum L. var. annum), peanut (Arachis hypogaea L.), cotton (Gossypium spp.), onion (Allium cepa L.), rose (Rosa spp.) and other flowers. In Taiwan, S. dorsalis is a significant pest of citrus, especially satsuma mandarin (Citrus unshui Marc), tea (Camellia sinensis [L.] O. Kuntze), and the rubber tree (Hevea brasiliensis Müll. Arg.). In Japan, S. dorsalis is notorious for its damage to citrus, tea, and grapevine (Vitis vinifera L.). In Côte d’Ivoire, it is a serious pest of cotton. In Indonesia, S. dorsalis is a serious pest of soybean (Glycine max Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) [L.] Merr.). In Queensland, Australia. S. dorsalis is a significant pest of strawberry (Fragaria ananassa Duchesne X F. virginiana Duchesne). Scirtothrips dorsalis has spread to South Africa, Côte d’Ivoire, Kenya, Oceania, Australia (Queensland), Papua New Guinea, Indonesia, and the Solomon Islands; in 2003 it was found to be established on St. Vincent, an island in the Caribbean Sea. Since 2003, S. dorsalis has emerged as a major pest in certain Caribbean islands, Suriname, Venezuela, Florida and southern Texas. The pest is still absent from the European and the Mediterranean Region. In the New World, S. dorsalis is now damaging crops as follows – St. Vincent and St. Lucia: commercial fields of chili pepper; Barbados: sea island cotton (Gossypium barbadense L.), and carrot (Daucus carota L.); Florida: Celosia argentea L., coleus (Plectranthus scutellaroides [L.] R. Br.), Coreopsis spp., geranium (Pelargonium x hortorum Bailey), Gerber daisy (Gerbera jamesonii H. Bolus ex hook f.), “Knockout” rose, pepper transplants (Rosa spp.), impatiens (Impatiens spp.), Japanese privet (Lagustrum japonicum), lisianthus (Eustoma russellianum), pentas (Pentas lanceolata [Förrsk.] Deflers), petunia (Petunia x hybrida), pittosporum (Pittosporum spp.), plumbago (Plumbago auriculata), snapdragon (Antirrhinum majus), verbena (Grandualaria x hybrida [Gönland & Rűmpler] Neson & Pruski), Victoria blue (Salivia farinacea), pansy Viola x wittrockiana Gams, zinnia (Zinnia elegans) and many other ornamental plants. Lawn care operators and other landscape management firms in Florida regard S. dorsalis to be nearly as threatening as insecticide-resistant western flower thrips, Frankliniella occidentalis (Pergande). Thus, where the two species both occur, it is important that measures taken against one species do not exacerbate the difficulty of suppressing the other. Also in Florida, S. dorsalis has been found frequently on pepper seedlings in retail outlets, but it has not yet become problematic in the commercial production of pepper or any other vegetable crop. C Scirtothrips dorsalis is a vector of various viral and bacterial diseases, including peanut bud necrosis virus (PBNV), peanut chlorotic fan virus (PCFV), tobacco streak virus (TSV) and tomato spotted wilt virus (TSWV). Recognizing S. dorsalis Infestations Scirtothrips dorsalis feeds on the meristems of host plants’ terminals and on other tender above-ground parts, and creates damaging feeding scars, distortions of leaves and discolorations of buds, flowers and young fruits (Fig. 46). It does not feed on mature tissue. Scirtothrips dorsalis causes damage by sucking the contents out of individual epidermal cells, which leads to necrosis of the tissue. Initially such tissue has a silvery sheen, but soon the damaged areas turn brown or black. In heavily infested pepper fields the appearance of the plants is known as “chilli leaf curl.” Heavy feeding causes the tender leaves and buds to become brittle, so that total defoliation and severe crop loss may occur. Usually, S. dorsalis adults are no longer than 1.2 mm and have pale bodies and dark wings. Dark spots are found dorsally on the abdomen, forming an incomplete stripe. Typically, the first instar larvae, second instar larvae and pupae are 0.37–0.39, 0.68–0.71 and 0.78–0.80 mm long, respectively, and all have pale bodies. The presence of distorted or discolored plant parts is suggestive of presence of S. dorsalis. Larvae feed on the undersides of young tender pepper leaves, and cause the leaf edges to curl upwards and brownish areas to develop between the veins. Corky tissue develops on infested fruits. Scirtothrips dorsalis larvae and adults tend to aggregate along the midvein or at the borders of damaged leaf tissues. In some instances, S. dorsalis infested plants superficially resemble broad mite infested plants, but broad mites cause pepper leaves to curl downwards and become narrow. On the other hand, when S. dorsalis populations become dense, the pest then feeds on the upper sides of the leaves of a number of host plants. 845 846 C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), Figure 46 Chilli thrips and damage: (a) adult of chilli thrips (photo by L. Mound), (b) larva of chilli thrips (photo by C. Sabines), (c) chilli thrips-infested rose plants (photo by C. Sabines), (d) chilli thrips damage on a pepper plant (photo by I. Maguire) (e) chilli thrips damage on a cotton plant (photo by I. Maguire). Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) Scirtothrips dorsalis individuals can be dislodged onto a white or black paper or plastic sheet on which they are readily visible. Samples can be taken by rinsing these thrips from plant material using 70% ethanol. The ethanol solution is then poured onto a fine sieve, and the specimens can be removed from the latter with a camel hair brush and mounted on slides for examination under a microscope. Adults are attracted to yellow sticky cards and perhaps to a lesser extent to yellowishgreen, green or white surfaces. In Japan sticky suction traps above the canopies of tea plants are used to monitor the flight of S. dorsalis and other thrips. Life History The life cycle stages of S. dorsalis are egg, first instar larva, second instar larva, prepupa, pupa and adult. The microscopic eggs are creamy white, kidney shaped and about 0.075 mm long and 0.070 mm wide. They are deposited inside plant tissue above the ground, and they hatch in 2–5 days. Larvae and adults tend to aggregate along the midvein or at the borders of damaged leaf tissues. Usually the pupae are found in the axils of the leaves, in curled leaves, under calyces of flowers and fruits, although they may also be found in the leaf litter or soil. Larval development requires 8–10 days and prepupal and pupal development together require 2.6–3.3 days. At about 28°C, the period spanning the first instar to the adult ranged from 11.0 days on pepper to 13.3 days on squash. S. dorsalis adults lived 13.6 days on tomato and 15.8 days on eggplant. The base and upper development temperatures of S. dorsalis are 9.7°C and 33.0°C, respectively. The species has a thermal requirement of 265 degree days from egg to adult and 281 degree days from egg to egg. Thus, the species is believed to undergo up to 18 generations per year in warm subtropical and tropical areas and about eight generations per year in warm temperate areas. It is believed that S. dorsalis cannot overwinter outdoors in areas where the minimum temperature reaches −4°C for 5 or more days. Scirtothrips dorsalis tends to become more abundant during prolonged C dry periods than during rainy periods, and its abundance is negatively affected by torrential rainfall events. The flight activity of S. dorsalis is greatest between noon and 2 p.m. Not all eggs are fertilized as a result of mating. Fertilized eggs develop into females, and unfertilized eggs develop into males. The sex ratio is often shifted in favor of female progeny. Host Plants Before S. dorsalis became established in the Western Hemisphere, it was already known to attack a wide range of hosts belonging to 112 plant taxa in about 40 families; as the pest invades new territory it attacks many additional taxa of plants. Economically important hosts of S. dorsalis, include the following: banana (Musa spp.), bean (Phaseolus vulgaris L.), cashew (Anacardium occidentale L.), castor (Ricinus communis L), Chinese bitter cucumber (Momordica charantia L.), citrus (Citrus spp.), corn (Zea mays L.), cocoa (Theobroma cacoa L.), cotton (Gossypium spp.), eggplant (Solanum melongena L.), golden dew drop (Duranta erecta Lindl.), grape (Vitis spp.), kiwi (Actinidia chinensis Planch), litchi (Litchi chinensis Sonn.), longan (Dimocarpus longan Lour.), mango (Mangifera indica L), melon (Cucumis melo L.), onion (Allium cepa L.), passionfruit (Passiflora edulis Sims), peach (Prunus persica L. Batsch), peanut, (Arachis hypogaea L.), pepper (Capsicum spp.), poplar (Populus spp.), sacara (Sacara spp.), sacred lotus, (Nelumbo nuciferae Gaertn.), soybean (Glycine max L.), strawberry (Fragaria ananassa Duchesne X F. virginiana Duchesne), sweet potato (Ipomoea batatas L.), tea (Camellia sinesis L.), tobacco (Nicotianum spp.), tomato (Lycopersicon esculentum L.), viburnum (Viburnum suspensum Lindl.), wild yam (Discorea spp.), and yedda hawthorn (Rhaphiolepis umbellata (Thunb.). Monitoring and Management Host crops such as bean, corn and cotton, are produced from seed and should be monitored as 847 848 C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) soon as the seedlings emerge, because the seedlings are especially attractive and very susceptible to severe damage by S. dorsalis. Hosts that appear to serve as preferred, such as pepper, “Knockout” rose, lisianthus, etc., should be monitored for symptoms of S. dorsalis infestation at least twice per week. Samples of symptomatic plant tissues should be sent to a professional for confirmation. The development of systems for managing S. dorsalis is still in its infancy. The World Vegetable Center (AVRDC) recommends the removal of any weeds that may serve as hosts, rotation of crops, fostering the activities of predators and parasites, and rotating insecticides. In Japan the use of reflective synthetic films to cover the ground between rows of citrus trees is fairly effective. Thrips are attacked by an array of predators, parasitoids and pathogens. Practical use in managing thrips populations in the field has been made of minute pirate bugs, Orius spp. (Hemiptera: Anthocoridae) and of the entomopathogenic nematodes, Thripinema spp. (Tylenchida: Allantonematidae). Orius adults and nymphs eat all stages of thrips, and suppress rapidly growing thrips populations. Since Orius also feed on aphids, spider mites, moth eggs, and pollen, Orius populations tend to persist long after thrips populations have been decimated. Thripinema are tiny parasitic worms, which render parasitized female thrips incapable of laying eggs. Male and female thrips parasitized with Thripinema tend to feed sparingly, cause little feeding damage and spread pathogens weakly. Whether releases of Orius or Thripinema should be made will depend on the value of the plant material to be protected. Also since releases may be less effective outdoors than in greenhouses and shadehouses, the cost of releases outdoors may be prohibitive. Nevertheless every effort should be made to conserve valuable natural enemies in field situations. Other predators of thrips, which have not been adequately studied to determine their practical suppression value, include lacewings, Chrysoperla spp., several mired bugs, ladybird beetles, and a number of predatory thrips including Franklinothrips vespiformis, the black hunter thrips, the six spotted thrips (Leptothrips mali), Scolothrips sexmaculatus, the banded wing thrips (Aeolothrips spp.), and the predatory phytoseiid mites, Amblyseius spp., Euseius hibisci and Euseius tularensis. In India the known predators of both larvae and adults of S. dorsalis are Carayonocoris indicus, Erythrothrips asiaticus, Franklinothrips megalops, Geocoris ochropterus, Mymarothrips garuda, Orius maxidentex, and Scolothrips indicus. Most of the known parasitoids of thrips are in the genera Ceranisus, Goetheana, Thripobius, and Entedonastichus. Under experimental conditions, S. dorsalis can be suppressed with several entomopathogens including Beauveria bassiana, Metarhizium anisopliae and Fusar ium semitectum. The first two of these pathogens have been used for insect control for several decades, whereas the latter was recently found to be effective in the laboratory studies in India. The advent of S. dorsalis into the Caribbean and Florida stimulated research on its biology and management. Notably the pyrethroid insecticides proved to be only weakly effective. The most effective materials evaluated to date (Table 11) are shown in the table. In order to forestall the development of resistance to any insecticide, materials belonging to different classes should be used in a rotation. Formulations of imidacloprid applied to the soil as a drench are effective, and they do not kill predators and parasites. In instances where another pest, such as the western flower thrips in Florida, has already developed incipient resistance to a given insecticide, great care must be exercised in choosing an insecticide to suppress S. dorsalis. Possibly this problem may be avoided by the application of entomopathogenic fungi, such as Beauveria bassiana, and Metarhizium anisopliae, but the efficacy of these preparations still requires field evaluation. The insecticide data in the table does not constitute control recommendations. All materials Chimaeropsyllidae C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), Table 11 Recently developed insecticides with high effectiveness against Scirtothrips dorsalis Class of material Trade name Common name Approximate % control Method of application Neonicotinoid Actara thiamethoxama 70 Foliar imidacloprid a 70–80 Foliar Admire imidacloprid a >90 Soil Organophosphate Orthene acephatea >80 Foliar Pyrrole Pylon Chlorofenapyra >90 Spinosyn A + Ba >90 Foliar Spinetoram >90 Foliar Fermentation product: Agrimek; Avid GABA inhibitor Abamectina 70–80 Foliar Entomopathogenic Fungi BotaniGard Beauveria bassiana >80 Foliar Tick EX Metarhizium anisoplae 70–80 Foliar Provado; Marathon; Fermentation product: Spintor; Conserve nicotinic acetylcholine receptor activator Radiant a This indicates that efficacy was measured in field trials; absence of “a” indicates that efficacy was measured in laboratory or greenhouse trials must be used in strict accordance with the registration label. Use of biologically based preparations such as spinosyn A + B, spinetoram and abamectin will allow continuation of the activity of naturally occurring predators and parasites.  Thrips (Thysanoptera) References Ananthakrishnan TN (1984) Bioecology of thrips. Indira Pub House, West Bloomfield, MI, 233 pp Ananthakrishnan TN (1993) Bionomics of thrips. Ann Rev Entomol 38:71–92 CABI/EPPO (1997) Quarantine pests for Europe, 2nd edn. CAB International, Wallingford, UK, 1440 pp CABI (2003). Crop protection compendium: global module. Commonwealth Agricultural Bureau International, Wallingford, UK Chang NT (1995) Major pest thrips in Taiwan. In: Parker BL, Skinner M, Lewis T (eds) Thrips biology and management. Plenum Press, New York, NY, pp 105–108 Moritz G, Morris D, Mound L (2001) Thrips ID. Pest thrips of the world. An interactive identification and information system. CSIRO Publishing, Australia Mound LA, Palmer JM (1981) Identification, distribution and host plants of the pest species of Scirtothrips (Thysanoptera: Thripidae). Bull Entomol Res 71:467–479 Seal DR, Ciomperlik M, Richards ML, Klassen W (2006) Distribution of the chilli thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), within pepper plants and within pepper fields on St. Vincent. Fla Entomol 89:311–320 Chimaeropsyllidae A family of fleas (order Siphonaptera).  Fleas 849 850 C Chinaberry, Melia azedarach L., A Biopesticidal Tree Chinaberry, Melia azedarach L., A Biopesticidal Tree efat aBou fakhr hammad American University of Beirut, Beirut, Lebanon Biopesticides are chemicals derived from a biological source. They are described as agents that include natural plant metabolites, microbial pest control agents such as entomopathogens, insect growth regulators and behavior-modifying chemicals. Biopesticides are generally nontoxic to vertebrates and plants and are called biorational insecticides in Integrated Pest Management programs. Biorationals are based on natural products and synthetic analogues of naturally occurring biochemicals and are more acceptable than conventional insecticides because they are environmentally less hazardous to humans and other non-target organisms. Botanical insecticides are plant-derived chemicals used in insect control. Plants synthesize secondary compounds that act as a defense against pests and diseases. The plant family Meliaceae was identified as one of the most promising sources of compounds with insect-control properties. In particular, some members of the generas Melia and Azadirachta were outstandingly effective against insects, and their components also were useful in many other respects. These components are considered important from economical, environmental and ecotoxicological standpoints because, in general, only 20–50 g of the active principle is sufficient to treat one hectare of area to achieve a satisfactory reduction in pest populations, and also because the products are readily biodegradable. The non-conventional effects of these preparations can include: partial reduction or complete inhibition of fecundity and sometimes egg hatchability, reduction of adult life span, oviposition deterrence, direct ovicidal effects, antifeedant and repellent effects against larvae, nymphs and adults, and action as an insect growth regulator. Insecticidal active ingredients from the neem tree, Azadirachta indica A. Juss, a member of the mahogany family (Meliaceae) and other related trees, specifically Melia azedarach L., fulfill most of the strict requirements for modern pesticides. These ingredients are non-toxic to mammals and are readily degraded on plants and in the soil. The high efficacy of these substances and their rapid biodegradability completely fulfill the requirements of toxicological and environmental safety. Classification The name Melia is the Greek name for the ash-tree Fraxinus ornus L. It belongs to the family Meliaceae, subfamily Meloideae, and tribe Melieae. Melia azedarach also is called Persian lilac, lilac, chinaberry, paradise tree, white cedar, umbrella tree, bead tree, syringa, hoop tree, China tree, pride of India, etc. In India, the most common name is Dharek. The names azadirachtin and azedarach are said to be derived from Persian azadirakht, which means “the tree azadirachtin” (azadirachtin = ash), similar to the derivatization of Melia from the Greek name for ash (μ ε λ κ). Its common names in the Mediterranean region are Zinzalakht and Azadarakht (Day). “Species”/forms/variations/cultivars of the Melia complex in Asia and the Pacific region were all considered to be M. azedarach. Consequently, Melia dubia CAV, M. australasica A. Juss, M. toosendan Sieb. and Zucc., M. volkensii Gürke, M. conchinchinensis M.J. Roem., M. superba Roxb., M. floribunda Morr., M. azedarach var. sempervirens Sw., M. azedarach var. japonica Don., and numerous others are synonyms of M. azedarach. The Texas umbrella tree, M. azedarach var. umbraculiformis, Berkmans which grows in the southern USA, is considered a mutation of M. azedarach. In contrast to all other M. azedarach variations/forms, it has a flattened crown of branches. Geographic Distribution The origin of Melia azedarach L., the chinaberry tree, is from northwestern India, where it is found Chinaberry, Melia azedarach L., A Biopesticidal Tree up to approximately 1,800 m above sea level. It is indigenous to Baluchistan and the Jhelum valley in Kashmir. However, it is cultivated and naturalized throughout India, Burma, and the Malay Peninsula. It occurs also in Persia and China. It is a deciduous tree often grown for shade or ornament on roadsides, parks and other open places. It is found in nearly all warm climatic areas. Due to its relatively low temperature requirements, it grows in southern Europe and in the Mediterranean region as well as southern France, northern Italy, and Croatia. It can be found as an avenue tree in Algeria, Cyprus, Greece, India, Lebanon, Palestine, Syria, Tunisia, etc. In northern Argentina, it is planted for firewood and timber production. In Uganda, Kenya, and South and West Africa, it is planted as a drought resistant ornamental and shade tree. Although the chinaberry tree is a native to tropical Asia, it is now widely distributed in dry regions of the southern and western United States. In some parts of the southern USA, M. azedarach is regarded as an “invasive” plant because its seeds are rapidly spread by birds. Botanical Characteristics Melia azedarach L. is a tree reaching up to 30 m (about 90 ft), with a thick trunk, spreading branches and furrowed bark. Chinese and Indian cultivars usually attain a height of 8–15 m whereas in certain areas in the Southern Hemisphere, such as Sri Lanka, Malaysia and Indonesia, the tree may reach 25–30 m. The blossoming time is MarchMay in the Northern Hemisphere, but some “forms” blossom throughout the summer or even the whole year round. The flowers are fragrant, are purplish or lilac, in long peduncles and axillary panicles which are shorter than the leaves and are glabrous or sparsely puberulent. The bi- to tri-pinnate alternate leaves are usually up to 45 cm (1–3 ft) long, while in young trees often longer (< 1 m). The leaflets are ovate and elliptic to lanceolate, acute, sharply serrate or lobed or have a crenate to serrate margin and are 1.2–5 cm (1–2 in) long. Leaf shedding C takes place in the Mediterranean region during October and November. Some ecotypes in the wet tropics (Malaysia) do not regularly shed their leaves. The girth can reach more than 3.2 m. The bark is relatively smooth and the heartwood is reddish. Fruits are nearly globular, yellow and smooth. The ripe yellow fruits, or drupes, are about the size of a cherry, globular to oval, 1/2– 3/4 in. in diameter, and are enclosed in a very hard endocarp, which contains 3–5 elongate-oval seed kernels. The ripe fruits can remain for several months on the trees. The kernels have an oil content of approximately 40%. The number of chromosomes is the same as in the neem tree, n = 14. Phytochemical Properties More than 280 limonoids have been isolated and identified from Meliacae plants. The most active constituents of M. azedarach are classified as azadirachtin-type C-seco limonoids and apo-euphol limonoids as trichilins with a 14,15-epoxide and a C-19/C-29 lactol bridge. The limonoid azadirachtin is absent from M. azedarach; it exists only in Azadirachta sp. The toxic tetranortriterpenoids (meliatoxins A1, A2, B1, B2) were isolated from the fruit of M. azedarach. Meliatoxin A2 was found to be identical to A1 except that ester moiety at C-28 is 2-methylpropionyl in place of the 2-methylbutanoyl group in A1. Meliatoxins B1 and B2 are isomeric with A1 and A2, respectively except the epoxide ring in B1 and B2 is replaced by a 5-member ring ketone at C-15. The chemical structure of the meliatoxins differs from trichilin, only in the lack of the hydroxyl substituent at C-12. Using bioassay guided fractionation and isolation technique, the principal insecticidal constituents of M. azedarach were isolated from methanolic extracts of green chinaberry fruits and were found to be two very potent insecticidal tetranortriterpenoids. These terpenoids include novel meliacin, called 1-cinnamoyl melianone, and a new derivative of meliacarpine called 1-cinnamoyl-3, 851 852 C Chinaberry, Melia azedarach L., A Biopesticidal Tree 11-dihydroxymeliacarpin. Azadirachtin analogs were found in M. azedarach fruit extracts. These isolated compounds were 1-cinnamoyl-3-feruloyl11-hydroxymeliacarpin, 1-cinnamoyl-3-feruloyl-11hydroxy 22, 23-dihydro-23-β-methoxymeliacarpin, and 1-tigloyl-11-methoxy-20-acetylmeliacarpine. Other limonoids that have been found in M. azedarach are: azedarchol, nimbin, santonum, sandolactone, ochinal and ochinine actetate, sandanol, melianone, mellanin, melianol and many others such as flavonoids, melianoninol, meliandiol, vanillic acid, vanillin and toosendanin. It was found that saponification of the oil from green berries of M. azedararch yielded 65% linoleic acid and approximately 20% oleic acid. Apart from palmitic and stearic acid, only very low quantities of other fatty acids, saturated or unsaturated, were also detected. The limonoids salanin and volkensin were isolated from the fruits of M. volkensii. Salanin, meldenin and a limonoid glycoside, established as 6-acetoxy-11-hydroxy-7-oxo-14epoxymeliacin-1,5-diene-3-O-L-rhamnopyraside, were isolated from 5 kg of powdered M. azedarach seeds extracted in 30 l of ethanol. M. azedarach leaves were also found to contain santonum, melianone, sandolactone, ochinal and ochinine acetate and 1-cinnamoyl melianone. Rutin and 3-O-L rhamnoside were isolated from M. azedarach in India. The two flavonol diglycosides, rutin and kaempferol-3-O-β rutinoside, were also isolated in high yields from the leaves of M. azedarach in Spain. Three trichilin type limonoids with the three known limonoids, trichilins B and D and meliatoxin A2, were isolated from ether-extracted root bark of the Chinese M. azedarach L., namely trichilin H, 12-acetyltrichlin B, and 7,12 diacetyltrichilin B. A biogenetically interesting ring-C seco limonoid, salannal, and a potent insect antifeedant, meliacarpine E, were also isolated from the root bark of the Chinese M. azedarach, along with four other seco-limonoids, salanin, deacetyl salanin, nimbolinin B, and nimbolidin B. Sandanol, melianol, mellanine A, and meldenin were isolated from the seeds. Production of Meliaceous Trees The trees are easily propagated both sexually and vegetatively. They can be reproduced using seeds, seedlings, saplings, root suckers or cuttings. Clean seeds, without the pulp, are planted in nurseries in prepared plastic sacks. Germination takes place after 8–15 days, depending on temperature and water supply. Shade usually is not required, but a partially shaded nursery may be advantageous. Ordinary seeds are ready for transplanting in 12 weeks, when they reach a height of 7.5–10 cm and their taproot is approximately 15 cm long. Transplanting is done during the rainy season with a high survival rate. It has been reported that trees produced through seed germination exhibit considerable variation. Hence, tissue culture technology was adopted to raise uniform plantation permitting multiplication of superior genotypes. Medicinal and Other Uses Melia azedarch is a medicinal plant used in Eastern medicine. It has been used in many places for the treatment of a variety of human disorders. On the Island of Maritius and in China, an extract of the bark is used as an antihelminthic. In Algeria, the plant is used as a tonic and antipyretic, and in South Africa, it is used for the treatment of leprosy, eczema and the relief of asthmatic attacks. In Asia, leaves are used as an antipyretic while the leaves, fruits and bark are used as an antihelminthic, however, certain “forms” are known to be poisonous to humans and livestock. The oil of M. azedarach is also used as an antihelminthic and antiseptic. Ripe fruits are known to be more toxic to mammals than green ones. Leaves seem to be less toxic, as they are used as fodder for goats in India. It was reported that children have died after eating six to eight ripe fruits. Records also show that M. azedarach is toxic to livestock, commonly affecting pigs, but the poisoning of cattle, sheep, goats and poultry has been reported with symptoms of Chinaberry, Melia azedarach L., A Biopesticidal Tree nausea, vomiting, constipation or scouring, often with blood. It was found that the approximate oral LD50 values of purified ethanolic solutions of the meliatoxins attributed to be the cause of high toxicity to pigs, was 6.4 mg/kg. Meliatoxins A1, A2, B1 and B2 have been shown to be responsible for the acute nervous system dysfunction and death in pigs. Toxicity may vary with location and stage of growth and may be entirely absent in some trees. Melia azedarach provides a multipurpose, termite-resistant heartwood which is used for teaboxes, furniture, ceilings and other building purposes. The “white cedar” leaves in Australia are used by aborigines as a fish poison. Bioactivity of the Melia azedarach Tree Against Insects Persian lilac trees remained unharmed during severe invasion by the desert locust Schistocera gregaria both in Palestine in 1915 and during the locust plague in India in 1926–27. It was proposed that M. azedarach does not kill acridids but repels them for several days and is unpalatable to Schistocerca gregaria. In Punjab, leaves of M. azedarach used as soil treatment at a rate of 7 tons/acre reduced the termite attack on wheat to 0.7% as compared with 8% in untreated plots. M. azedarach is not a good host for the sweetpotato whitefly, Bemisia tabaci (Gennadius). Host preference bioassays indicated a significantly lower number of live whiteflies on the leaves of the chinaberry tree versus the leaves of beans, cucumbers, and tomatoes after 24 h. Bioactivity of Extracts of Melia azedarach Leaf extracts of M. azedarach protected plants against locust feeding and the activity was found to be higher in these extracts than in pulp and the very small seed kernels. Chloroform extracts of C M. azedarach leaves were found to retard the growth of first instar larvae of the corn earworm Heliothis zea and the fall armyworm Spodoptera frugiperda. At a concentration of 30 mg-eq/g diet fed to test larvae, 100% mortality occurred and larvae died before pupation, retarding development in both insect species. Significant weight reduction in larvae was observed due to feeding deterrence of the extract. Aqueous extracts of M. azedarach applied on bean plant leaves interfere with the longevity and development of adults and immature stages of B. tabaci. The interference of the extract, in a field test, reduced transmission of viruses by 45–60% compared to control plants. This was attributed to the phago-deterrent effect of the plant extract against adults. Toxicity of aqueous emulsions of M. azedarach fruits prepared from 5% solutions in acetone containing also Triton X-100 (0.5%) against adults of Sitotroga cerealella was approximately 0.2% that of malathion, and activity of 4-day-old residues was 20–40%. The extract lost its toxicity nearly totally by the 8th day after the spray. Fruit and leaf extracts of M. azedarach showed a comparable and potential repellent effect against B. tabaci adults. Fruit and leaf aqueous extracts caused a significantly lower number of live adult whiteflies to be encountered on treated bean leaves than the control after 24 h, regardless of whether these plant parts were crushed or boiled in water. M. azedarach aqueous extracts at the rate of 1:5 (w/v) caused a possible antifeedant action against adult B. tabaci as indicated by fewer eggs laid by treated adults and fewer pupae produced. The growth of 2nd and 4th larval instars of the oak processionary caterpillar Thaumetopoea processionea, was retarded after being sprayed by an enriched M. azedarach fruit extract; and after 4 days of spraying, the larvae became quite lethargic. Even with lower concentrations of 0.01%, mortality of 100% was attained within a period of 1–2 weeks. Death was mainly caused by moult disruption because the larvae were not able to shed the old exuviae. Younger larvae were more sensitive to the plant extracts than older ones. 853 854 C Chinaberry, Melia azedarach L., A Biopesticidal Tree The Melia fruit aqueous extract significantly lowered the number of larvae of the pea leafminer, Liriomyza huidobrensis (Blanchard), per Swiss chard plant as compared to the control, at 15 days after first spray when two consecutive sprays were performed under field conditions. The Melia fruit extract significantly decreased the number of live larvae per cucumber leaf compared to the control, 10 days after each spray under greenhouse conditions. Melia fruit extracts and cyromazine caused the formation of deformed larvae which were partially brown rotted and oozing. This indicates that the fruit extract may have a growth-regulating activity similar to that of cyromazine, a triazine insect growth regulator selective to the genus Liriomyza. The aqueous leaf extract was found to keep the number of live larvae per leaf at a significantly lower density than the control only at 20 days after the second treatment application. This indicates that the leaf extract might need a longer period of time to reveal its effect. Increasing the number of consecutive sprays enhances the activity of these extracts under field conditions due to the known ultraviolet degradation of botanical extracts. The activity of mixed function oxidases in the midgut of 5th-instar larvae of Pieris rapae was reduced to half its value after feeding on toosendanin, an extract from the bark of M. azedarach or M. toosendan. Esterase activity in the midgut was also markedly reduced, but not in the hemolymph. Simple preparations from M. azedarach include: drying of the fruit, milling of the seeds, preparation of aqueous extracts, and of a seed dust diluted with 25% zeolite. The main pests controlled by these preparations were: S. frugiperda, Spodoptera sp., B. tabaci, Plutella xylostella, Mocis latipes, Diaphania sp., Herse cingulata, H. virescens, Sitophibus oryzae, Cyclas formicarius elegantulus, Aphis gossypii and Myzus persicae. Methanolic extracts of M. azedarach of high concentrations (25% and 12.5%) caused about 100% mortality of A. fabae nymphs within 4 days. Extracts of 25%, 12.5%, and 1.25% also deterred alates in choice experiments from ovipositing on treated Vicia faba plants. Adults of B. tabaci were significantly more repelled from tomato plants treated by the undiluted methanol, acetone or water extracts when compared to the control after 72 h. There were significant differences in percent mortality (23.0– 48.9%) of nymphal instars when exposed to the undiluted extracts compared to the other diluted extracts and the control. M. azedarach leaf and fruit extracts were found to be repellent to the whitefly adults, while the fruit extracts specifically have shown a significant detrimental effect against early nymphal instars. The undiluted methanol extracts caused a very low number of live adult whiteflies on treated plants in comparison to the undiluted water and acetone extracts. This indicates that methanol seems to extract more of the bioactive components from Melia compared to that of acetone or water. Similarly, aqueous and methanol extracts of leaves, fruits and callus of M. azedarach have shown significant repellent activity of 58.9–67.7% and have decreased significantly the oviposition rate of the insect without affecting the adult whitefly emergence compared to the control. Extracts of frozen samples were found to be as effective against the pest as fresh samples, thus allowing storage of Melia parts to be used in case of shortage. The antifeedant action of the M. azedarach extract was observed and it was found that the rate of adult mortality of B. tabaci on plants sprayed with M. azedarach leaf or fruit extracts (1:5, w/v) were not significantly different from the mortality rate when B. tabaci were kept unfed. The two highest concentrations: 10,000 and 2,000 ppm of the ethanol extract of fruits of M. azedarach were incorporated into artificial diet of the fall armyworm, S. frugiperda. This caused 100% mortality of the insect before pupation, but the hexane extracts tended to be less effective. Treated larvae showed significant weight loss and delay in the time needed for pupation. Ethanol extracts of the fruits of M. azedarach containing 32mg/100ml caused 97%–98% mortality of the cabbage aphid, Chinaberry, Melia azedarach L., A Biopesticidal Tree Bervicoryne brassicae in 48 h. Ethanol seed kernel extract of M. azedarach inhibited feeding of the rice noctuid Spodoptera abyssina by 99.8%. Petroleum ether extracts of M. azedarach fruits are strong antifeedants against nymphs of the brown planthopper, Nilaparvata lugens. Rice plants treated with a hexane extract of M. azedarach were not only repellent to adults of the green rice leafhopper, Nephetettix nigropictus, and the macropterous brown planthopper in choice test against control plants, but they also reduced the feeding time of the insects. Petroleum-ether extract (2%) of both Melia toosendan and M. azedarach caused respectively 100% and 89.5% feeding deterrence of third-instar larvae of Spodoptera litura. The petroleum-ether, ethanol and methanol extracts of M. azedarach and M. toosendan seed kernels have bioactivity against several insect pests such as the rice yellow stem borer Schirpophaga incertulas, the fifth instar of the cabbage butterfly Pieris rapae, the female rice gall midge Orseolia oryzae, the citrus leafminer Phyllocnystis citrella, the polyphagous beetle Anomala cupripes, and the Asiatic corn borer Ostrinia furnacalis. High oviposition deterrence and reduction of adult emergence of the rice hispa and the pulse beetle was detected when exposed to leaf or seed extracts of Chinaberry. The food intake of newly emerged females of the brown planthopper, and the whitebacked planthopper, Sogatella furcifera, on rice plants sprayed with M. azedarach seed oil, was reduced starting from the dosage of 5 mg/plant. The 32P isotope tracer technique was used to verify the antifeedant effect of M. azedarach seed oil emulsion against the citrus aphid, Aphis citricola. The nymphal period of the cicadellid Nephotettix nigropictus was prolonged and mortality was obtained when the insects were fed on seedlings treated with the oil extract. The 0.5% emulsified seed oil extract of M. azedarach gave good control of the orange spiny whitefly, Alevrocanthus spiniferus (Quaintance), and its efficacy was comparable to that of the potent acaricides amitraz or cyhexatin in controlling the C citrus red mite, Panonychus ulmi on citrus. The chinaberry seed oil is also highly toxic to the Formosan subterranean termite. Bioactivity of Melia azedarach components against insects Meliatoxins and trichilin type limonoids were found to be antifeedants against certain insect pests. Meliatriol isolated from fruits of M. azedarach showed strong antifeedant properties against 5th instar of the desert locust Schistocerca gregaria Forsk. Meliatine, an exceedingly bitter substance isolated from the leaves of M. azedarach, was found to effectively protect crop leaves against the locust attack. The steroid, estrer azaderachol, isolated from the ether extract of the root bark of M. azedarach var. japonica, showed antifeedant activity against larvae of Agrotis segetum. The antifeedant properties of M. azedarach constituents: salannal, meliacarpine E, salanin, deacetyl salanin, nimbolinin B and nimbolidin B were examined with the larvae of Spodoptera eridania. Meliacarpinin E showed the most potent activity at 50 ppm, similar to meliacarpinins A-D. Other C-seco limonoids showed only weak activities at 500– 1000 ppm. Three trichilin type limonoids from the ether extract of the root bark of the Chinese M. azedarach L., namely trichilin H, 12-acetyl, and 7,12 diacetyltrichilin B. were found to be antifeedants active against the Japanese pest Spodoptera exigua. Meliatoxin A2 isolated from the fruit of M. azedarach induced a significant level of antifeedant activity against Spodoptera lituralis larvae, while the meliatoxin B1, lacking the epoxide ring, was much less active. The salannins and salannols isolated from M. azedarach have shown antifeedant activity toward the Mexican bean beetle. The two tetranortriterpenoids: 1-cinnamoyl melianone and 1-cinnamoyl-3, 11-dihydroxymeliacarpin were found to have growth inhibitory 855 856 C Chinaberry, Melia azedarach L., A Biopesticidal Tree effects for first instar larvae of the Lepidoptera Heliothis viriscens and S. frugiperda. Other highly oxidized tetranorterpenoids that are azadirachtin analogs have impaired metamorphosis of the Mexican bean beetle, Epilachna varivestis. Integration With Natural Enemies Adults of the predator Coccinella septempunctata showed no mortality after being allowed to consume adults of the mustard aphid, Lipaphis erysimi, that had been exposed for 5 h to mustard leaves treated with 1.5% alcoholic extract of the drupe of M. azedarach. Leaves infested with Epilachna vigintioctopunctata, and treated with a petroleum ether extract of the drupes of M. azedarach, were less parasitized by Pediobius foveolatus than the control. However, on exposure to parasitization 24 h after treatment, larvae were parasitized normally and the parasites that emerged from treated hosts were normal. M. azedarach oil did not affect the survival and behavior of the larvae of Coccinella undecimpunctata, but there was prolongation of the fourth larval instar while the Aphis gossypii aphid consumption was unchanged. The oil of M. azedarach seeds was found to be only slightly toxic against the predatory mirid bug Cyrtorhinus lividipennis and non-toxic against the spider L. pseudoannulata, natural enemy of the whitebacked planthopper, Sogatella furcifera, the brown planthopper, N. lugens, and the green leafhopper, Nophotettix virescens. A massive dosage of the seed oil of M. azedarach applied topically to the wolf spider Lycosa pseudoannulata, a natural enemy of the brown planthopper, Nilaparvata lugens, had no effect on the spider. Potentials in Sustainable Systems Extracts of tissue culture of Melia have shown repellency to different insect species similar to extracts of Melia leaf or fruit. The synthesis of secondary plant compound(s) in such undifferentiated cells of Melia is clearly occurring. It may be possible to enhance production of meliaceous allelochemicals in tissue cultures to the extent that culture extracts could eventually be used for production of botanical insecticides. As an alternative to harvesting an ecologically important tree, cell-culture systems can be used to provide a continuous supply of those biopesticidal extracts through the propagation of Melia all year round and using them easily and conveniently. The different ecotypes of M. azedarach are a potential natural resource that can be utilized, as raw material and extracts, in low-input agroecosystems. Cultivation of this meliaceous tree is an economically feasible practice, as it is usually planted as a common shade tree. The efficacy of M. azedarach extracts might be enhanced by investigating the timing and frequency of application of the plant extracts on crops for management of major economical agricultural pests. These extracts could provide a relatively inexpensive and readily available insecticide to combat the pest resistance to insecticides.  Botanical Insecticides References Abou-Fakhr Hammad EM, Zournajian H, Talhouk S (2001) Efficacy of extracts of Melia azedarach L. callus, leaves and fruits against adults of the sweetpotato whitefly Bemisia tabaci (Hom. Aleyrodidae). J Appl Entomol 125:425–488 Ascher KRS, Shmutterer H, Zebitz CPW, Nagvi SNH (1995) The Persian lilac chinaberry tree: Melia azedarach L. In: Schmutterer H (ed) The neem tree. VHC Publishers, New York, NY, pp 602–642 Kraus HS, Baumann M, Bokel U, Klenk A, Klingele S, Pohnl M, Schwinger M (1987) Control of insect feeding and development by constituents of Melia azedarach and Azadirachta indica. In: Schmutterer H, Ascher KRS (eds) Natural pesticides from the neem tree and other tropical plants. Proceedings of the Third International Neem Conference, Rauiscchholzhausen, Germany, pp 111–125 Lee MS, Klocke JA, Barnby MA, Yamasaki RB, Balandrin MF (1991) Insecticidal constituents of Azadirachta indica Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae) and Melia azedarach (Meliaceae). In: Hedin PA (ed) Naturally occurring pest bioregulators, ACS Symposium Series 449, pp 293–304 Nakatani M, Huang RC, Okamura H, Naoki H, Iwagana T (1994) Limonoid antifeedant from Chinese Melia azedarach.Phytochemistry 36:39–41 Nardo EAB, De Costa AS, Lourencao AL (1997) Melia azedarach extract as an antifeedant to Bemisia tabaci (Homoptera: Aleyrodida). Fla Entomol 80:92–94 Oelrichs PB, Hill MW, Valley OJ, Macleod JK, Molinski TF (1983) Toxic tetranortriterpenes of the fruit of Melia azedarach. Phytochemistry 22:531–534 Tewari GC, Moorthy PNK (1985) Plant extracts as antifeedants against Henosepilachna vigintioctopunctata (Fabricius) and their effect on its parasite. Indian J Agr Sci 55:120–124 China, William Edward William China was born in London on December 7, 1895. His university education was in London and Cambridge, but was interrupted by World War I. In that war, he served in France, first in the British army, later in the Royal Air Force. He returned to Cambridge University and earned a degree in zoology. In January 1922, he was appointed assistant in the Department of Entomology of the British Museum (Natural History), in 1930 assistant keeper, and eventually in 1955, keeper. His subject of research was the taxonomy of Hemiptera, in which he eventually published 265 papers, describing 98 new genera and 248 species. During World War II, he was deeply involved in temporarily moving the national insect collections out of London to prevent damage or loss. His research resulted in his award in 1948 of a D.Sc. degree by Cambridge University. He retired in 1970 to a little fishing village in the county of Cornwall, where he died on September 17, 1979, survived by his wife Lita and three children. Reference Knight WJ (1980) Obituary and bibliography. Entomologist’s Monthly Magazine 115:164–175 C Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae) John L. Capinera University of Florida, Gainesville, FL, USA The chinch bug, Blissus leucopterus, is found through much of the eastern United States and southern Canada, west to about the Rocky Mountains. However, it is absent from the Gulf Coast region, where it is replaced by a closely related species, the southern chinch bug, Blissus insularis Barber. The two species have overlapping ranges in portions of the southern states from North and South Carolina through central Georgia and west to Texas. Southern chinch bug feeds only on lawn and forage grasses, particularly St. Augustine grass, and is not a food crop pest. Other species of Blissus occur in both eastern and western states but they are of little consequence. The Blissus spp. may have dispersed northwards from South America, but if so they apparently dispersed in precolonial times, as there is no record of their introduction. The range of B. leucopterus can be subdivided because two discrete subspecies exist; B. leucopterus hirtus Montandon in the northeast, and B. leucopterus leucopterus (Say) in the central region of the eastern states. In eastern Canada, the New England states, and south to about northern Virginia and eastern Ohio, the northeastern form, B. leucopterus hirtus, is a pest of lawn grasses, but not of food crops. This subspecies is also called “hairy chinch bug” to distinguish it from the food crop-attacking subspecies, B. leucopterus leucopterus, which is known simply as “chinch bug.” Chinch bug occurs from Virginia to Georgia in the east, extending to South Dakota and Texas in the west. Chinch bug generally is not damaging throughout its entire range, and is considered to be a pest mostly in the midwestern and southwestern states from Ohio in the east to South Dakota and Texas in the west. 857 858 C Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae) Life History There are at least two generations per year throughout the range of B. leucopterus leucopterus. The first generation commences in the spring with oviposition by overwintering adults, usually in April or May. The second generation begins in June–August. Second generation adults overwinter, often in the shelter of clump-forming wild grasses, dispersing in the spring to earlyseason crops, and then in early summer to laterdeveloping crops where the second generation develops. Generations overlap considerably due to prolonged oviposition, and in the southwestern states there is some evidence of a third generation. A complete life cycle can occur in 30–60 days. The elongate-oval eggs are rounded at one end, truncate at the other, and measure about 0.85 mm long and 0.31 mm wide. The truncate end bears three to five minute tubercles, 0.1 mm in length. The eggs are whitish initially, turning yellowish brown after a few days and reddish before hatching. Eggs are deposited in short rows at the base of the plant on roots, on the lower leaf sheaths and stems, and on the soil near the plant. Females deposit eggs at a rate of 15–20 per day over a 2–3 week period, producing up to 500 eggs. Duration of the egg stage is about 16 days at 27°C and 8 days at 31°C. There are five instars. Duration of the instars is about 5, 6, 5, 4, and 6 days for instars 1–5, respectively, when reared at 29°C. Under field conditions, the development time may be extended, with a developmental period of about 30–40 days normal, and 60 days not unusual. During the early instars, the head and thorax are brown, the legs pale. These structures become darker as the nymphs mature, so that the mature nymph is blackish. The first two segments of the abdomen are yellowish or whitish, the remainder red except for the tip of the abdomen, which is black. The reddish abdomen becomes progressively darker, however, appearing almost black at nymphal maturity. The wing pads become visible in the third instar, but are difficult to discern. In the fourth instar the wing pads extend about half the width (Fig. 47) of the first abdominal segment. In the fifth instar the wing pads extend to the third abdominal segment. The nymphal body lengths are about 0.9, 1.3, 1.6, 2.1, and 2.9 mm for instars 1–5, respectively. Nymphs prefer to feed in sheltered locations such as curled leaves and on roots, but are often found aggregated on the stem near the base of the plants. When not feeding they may hide under clods of soil and rubbish, or in loose soil. The body and legs of the adult are blackish in color (Fig. 48). The wings of B. leucopterus leucopterus nearly attain the tip of the abdomen, and are white in color with a pronounced blackish spot found near the center and outer margin of the Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae), Figure 47 Adult of chinch bug, Blissus leucopterus (Say). Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae), Figure 48 Fourth instar of chinch bug, Blissus leucopterus (Say). Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae) forewings. The adult measures 3.5–4.5 mm in length. In the related form called hairy chinch bug, the wings generally are abbreviated, usually not extending beyond the middle of the abdomen. Hosts of chinch bug consist solely of plants in the family Gramineae, but include both wild and cultivated grasses. It is known principally as a pest of such grain crops as barley, corn, millet, oat, rye, sorghum, and wheat, but oat is only marginally suitable. However, it also damages forage grasses including sudangrass and timothy, and feeds on wild grasses such as foxtail, Setaria spp.; crabgrass, Digitaria spp.; and goosegrass, Elusine indica. Females select sorghum for oviposition over wheat and corn; barley is intermediate in preference. Crop suitability, as measured by development time, is similar to oviposition preference. Numerous natural enemies have been observed. Among avian predators feeding on chinch bugs are common birds as barn swallow, Hirundo erythrogastra Boddaert; horned lark, Otocoris alpestris (Linnaeus); meadowlark, Sturnella magna (Linnaeus); redwinged blackbird, Agelaius phoeniceus (Linnaeus); and kingbird, Tyrannus tyrannus (Linnaeus). Insect predators of special importance are insidious flower bug, Orius insidious (Say) (Hemiptera: Anthocoridae), an assassin bug, Pselliopus cinctus (Fabricius) (Hemiptera: Reuviidae), and various ants (Formicidae). Ladybird beetles (Coleoptera: Coccinellidae) and lacewings (Neuroptera: Chrysopidae) frequently have been observed on plants infested with chinch bugs, but their effects are uncertain. Parasitoids are sometimes found in these small insects, but rarely are they considered to be significant mortality factors. An egg parasite, Eumicrosoma benefica Gahan (Hymenoptera: Scelionidae), the nymphal or adult parasite Phorocera occidentalis (Walker) (Diptera: Tachinidae), and an unspecified, naturally occurring nematode have been reported. The egg parasitoid, which is found throughout most of the range of the chinch bug and is active during much of the season when chinch bug occurs, was reported to parasitize up to 46% of the eggs in Nebraska, so it may be of considerable value in biological control. C The most important natural mortality factor is fungal disease, particularly Beauveria bassiana. Interestingly, this fungus was intensively redistributed, particularly in Kansas, during the late 1880s in an effort to increase suppression. However, it eventually became apparent that the disease spread naturally, and that the effectiveness of the fungus was related more to weather than to the efforts of agriculturalists and entomologists to foster epizootics. The fungus is invasive and pathogenic at relative humidities of at least 30–100%, but fungal replication and conidia production require humidities of at least 75%. Clumps of such bunch grasses as little bluestem, Andropogon scoparius, serve to harbor not only overwintering bugs, but Beauveria as well, and may be important in initiating fungal epizootics. The food plant of the chinch bug affects susceptibility to B. bassiana, with a diet of corn and sorghum suppressing fungus development and bug mortality. Weather has significant impact on chinch bugs. The overwintering period is moderately critical. Adults seek shelter in stubble and debris, but one of the most favorable locations is among the stems of bunch grasses. Bunch grasses provide food in the autumn before the onset of winter temperatures, and again in the spring before it is consistently warm and the bugs disperse. Bunch grasses also serve to break the wind by reducing desiccation and the severity of the wind, and by keeping excessive rainfall from the insects. Thus, in the absence of bunch grasses or similar shelter, survival can be poor. Heavy snow cover is favorable, keeping the bugs warmer and sheltered from the drying wind. Summertime weather is perhaps even more critical. Chinch bugs thrive in warm, dry conditions, at least in the midwestern states. Heavy rainfall can kill many bugs, and wet, humid weather fosters epizootics of fungal disease. In the southwest the situation is different because dry weather is usually assured, but the absence of summer rain causes premature senescence of plants, depriving bugs of green food late in the summer. 859 860 C Chironomidae Damage Chinch bug is a plant sap-feeding insect, causing a reddish discoloration at the site of feeding and death of that portion of the plant. Plant growth can be stunted, or plants killed when fed upon by large numbers of bugs. Their destructiveness is attributable, in part, to their gregarious nature. Not only do large numbers aggregate on certain plants, but they also disperse in tremendous numbers from field to field. When plants are infested while young, they suffer more damage than if infested later in growth. Management Granular and liquid insecticides are used to protect plants, particularly plants that are invaded by nymphs or adults dispersing from senescent earlyseason crops. Systemic insecticides can be applied at planting time, and either contact or systemic materials after the crop has emerged from the soil. Liquid insecticides should be directed to the base of the plants, a location favored by the insects. Historically, most damage occurred when early-season small grain crops matured, and large numbers of first generation nymphs dispersed by walking to adjacent crops, usually corn. This was combated by erecting barriers, usually in the form of a ditch, between crops. Also, some destruction of overwintering bugs in wild grasses was accomplished by burning, though it was rarely more than 50% effective. These practices are largely obsolete, and insecticides are now used effectively. However, it remains advisable to rotate among susceptible and nonsusceptible crops, and to grow susceptible crops in isolation from alternate hosts. Because the combination of small grains and corn leads to damage by chinch bugs, it may be desirable to eliminate one of these crops and thereby eliminate an important food from the chinch bug life cycle. In southern states the crop sequence is different, with both wheat and corn invaded by overwintering bugs early in the season. Cultural practices that promote dense growth and shade will increase humidity and decrease chinch bug numbers. Thus, fertilization and irrigation can be detrimental to chinch bug survival. There is considerable difference among crops in susceptibility to injury, and within crops the level of resistance also is variable. Measurable levels of difference in bug longevity and development occur when they feed on different varieties of wheat, though there is not a practical level of resistance. In contrast, a resistant variety of sorghum has been identified, and there is considerable resistance in grain corn.  Turfgrass Insects and their Management  Vegetable Pests and their Management References Leonard DE (1968) A revision of the genus Blissus (Heteroptera: Lygaeidae) in eastern North America. Ann Entomol Soc Am 61:239–250 Swenk MH (1925) The chinch bug and its control. Nebraska agricultural experiment station circular 28, 34 pp Chironomidae A family of flies (order Diptera). They commonly are known as midges.  Flies Chironomids as a Nuisance and of Medical Importance meir Broza University of Haifa, Haifa, Israel Chironomids, the “non-biting midges” (Diptera: Chironomidae) are one of the most important groups of insects worldwide in freshwater, aquatic ecosystems. Chironomids can be found on all continents, including Antarctica. They are abundant in terms of the number of species that are known to exist (estimated number between 15,000 and 20,000), their relative biomass or both. They play an important role in the decomposition process. Chironomids as a Nuisance and of Medical Importance Large populations of midges with densities amounting to several thousand larvae/m2 (usually on the floor of freshwater habitats) have been reported. They are a source of economic burden, nuisance, and health problems. Large midge population densities create conflict with nearby human settlements. This phenomenon is recognized worldwide, in the United Kingdom, United States, Japan, Italy, Spain, Israel, New Zealand and Sudan. Chironomidae (particularly Chironomus) emerging from polluted natural and man-made aquatic habitats, near or in urban districts, can become intolerable (Fig. 49). During the spring and midsummer, evening breezes carry large swarms of adult midges to nearby cities and communities where they can become a severe nuisance to the residents. Adult midges are most active during the evening and they may enter the mouth, eyes and ears, thus limiting evening activities outdoors and indoors. In 1998, a population estimated at 40–50 billion individuals/night emerged from 200 acres of waste stabilization ponds near Tel Aviv, Israel. Such swarms may be economically important due to the damage they can cause to vessels, pumps and aeroplane engines. Chironomid larval populations (“red-worms”) contaminate municipal drinking water supply systems. This problem has been reported in the United Kingdom since the 1970s, in the U.S.A., Israel and elsewhere. In both the U.K. and U.S.A., the chironomid inhabiting the water systems was identified as the parthenogenetic species Paratanytarsus grimmi. After entering the pipe system, the pupal stage circulates in the water and may produce egg masses without emerging as airborne adults. Because pesticides cannot be used in a water supply, a food-grade coagulant and water disinfectant were suggested as control agents. Besides the unacceptable appearance of redworms in the water supply, the larvae also may cause technical problems by blocking water filtration systems. In countries where recycled water is used for irrigation, the larvae may adhere to the inner surface of pipes and contribute to the build-up of biofilm on these surfaces. As a result of C Chironomids as a Nuisance and of Medical Importance, Figure 49 Nuisance midges: above, Chironomus sp. female (left) and male (right); below, accumulation of midges on an automobile after only a few minutes of travel. such accumulations, greater amounts of energy may be needed for water transport. Many insect vectors of serious human diseases are flies. This includes nematoceran flies in which the females feed on a vertebrate blood meal. Chironomids are non-biting midges, and it may seem surprising to find that they are of medical significance. However, they are now recognized as causing severe allergic reactions in humans. The most thoroughly investigated case of an allergic 861 862 C Chitin disease associated with chironomids comes from the Sudan. People living south of the Aswan Dam suffer from the mass emergence of chironomids from Lake Nasser. In the dry winds, large numbers of dead insects are blown into the air, causing allergic reactions such as asthma and rhinitis. The town of Wadi Halfa located near Lake Nasser has been particularly plagued since the building of the dam on the Nile. A few cases also have been reported from the U.S.A. For example, an employee at a hydroelectric plant in Alabama developed seasonal hay fever in response to the mass emergence of chironomids from the dam. It has been shown that chironomid larval hemoglobin, which contaminates adults during metamorphosis, is a potent human allergen. It is believed that midges are potentially the cause of many allergic reactions worldwide. As well as causing allergies, midges may play a role in the maintenance and transmission of infectious diseases. Chironomid egg masses have been reported to serve as a natural reservoir for the cholera bacterium, possibly raising the chironomid problem from a nuisance level to a lifethreatening hazard. Cholera is a severe diarrheal disease that kills thousands of people each year and affects the lives of millions of others. The disease is caused by the bacteria Vibrio cholerae, which is pathogenic to humans only. At present, the disease is most common in the Indian subcontinent and less developed countries in Asia, Africa and South America. References Ali A (1994) Pestiferous Chironomidae (Diptera) and their management. In: Rosen D, Bennett FD, Capinera JL (eds) Pest management in the subtropics: biological control – a Florida perspective, Intercept Ltd, Andover, UK, pp 487–513 Armitage P, Cranston PS, Pinder LCV (eds) (1995)The Chironomidae: the biology and ecology of non-biting midges. Chapman & Hall, London, UK, 572 pp Benke AC (1998) Production dynamics of riverine chironomids: extremely high biomass turnover rates of primary consumers. Ecology 79:899–910 Broza M, Halpern M, Teltsch B, Porat R, Gasith A (1998) Shock chloramination: a potential treatment for Chironomidae (Diptera) larvae nuisance abatement in water supply systems. J Econ Entomol 91:834–840 Broza M, Halpern M (2001) Chironomids egg masses and Vibrio cholerae. Nature 412:40 Chitin A tough insoluble structural polysaccharide material that comprises variable portions of the insect cuticle. It is a water-insoluble polysaccharide that forms the exoskeletons of arthropods, and is one of the most widely occurring polysaccharides in nature. Chitin molecules are long-chain sugars consisting of N-acetyl-glucosamines attached together with beta-glucosidic linkages. Chitinase An enzyme that degrades chitin. Chitinous Consisting of, or containing, chitin. Chittenden, Frank Hurlbut Frank Chittenden was born in Ohio on November 3, 1858, and grew up in a small town there. He studied entomology at Cornell University. Next, he worked at the Brooklyn Museum and was one of the founders of the Brooklyn Entomological Society and an editor of Entomologica Americana. In 1891 he was hired by the U.S. Department of Agriculture (Fig. 50) and embarked on his life’s work as an applied entomologist, contributing greatly to the knowledge of pests of vegetables and stored products. In 1904 he was awarded an honorary degree of doctor of sciences by Western University of Pennsylvania. He died in Washington, DC, on September 15, 1929. Chordotonal Sensory Organs C Chlorosis Yellowing or bleaching of normal green plant tissue, usually caused by the loss of chlorophyll. Choreutidae A family of moths (order Lepidoptera). They are commonly known as metalmark moths.  Metalmark Moths  Butterflies and Moths Cholinesterase Chittenden, Frank Hurlbut, Figure 50 Frank H. Chittenden. Reference *Mallis A (1971)Frank Hurlbut Chittenden. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 100–102 Chlorinated Hydrocarbons A class of synthetic insecticides containing chlorine as one of the constituents. Chlorinated hydrocarbon insecticides are typically very persistent and formerly were used widely for soil and seed treatments. These chemicals also are known as organochlorines.  Insecticides Chloroperlidae A family of stoneflies (order Plecoptera). They sometimes are called green stoneflies.  Stoneflies Chloropidae A family of flies (order Diptera). They commonly are known as frit flies or grass flies.  Flies An enzyme that is present in the synapse region of nervous tissue, and which is necessary for normal functioning of nerves in animals. Cholinesterase inhibiting chemicals such as insecticides of the organophosphate and carbamate classes disrupt nerve transmission in insects. Chordotonal Sensory Organs James L. nation University of Florida, Gainesville, FL, USA Insects have a plethora of sensory organs scattered over and within their body. Many of the sensory structures are mechanical sensors that bend, indicating contact with a surface or wind and air movement over the structure. Other mechanoreceptors detect stress in the exoskeleton, the cuticle, caused by movement of legs, wings, or antennae, and enable insects to know the position of their body and limbs. Still others detect vibrations in the substrate on which the insects may be resting, and vibrations in the air, which we usually call sound. Sound detectors are typically called tympanal organs. The simplest of mechanoreceptors may consist of a single hair or seta that projects from the cuticle surface. Such a simple receptor, usually with only one sensory neuron connecting it to the central nervous system (CNS) is called a sensillum. 863 864 C Chordotonal Sensory Organs More complex sensory organs are composed of many sensilla, i.e., they have many sensory neurons connecting to the CNS. Although there are numerous morphological variations in a mechanoreceptor, from the simple, single hair receptor to very complex receptors such as Johnston’s organ on the antennae of most insects, they tend to have certain common features. Whether one or many, each sensory neuron is enclosed in one to several sheath cells, and connected by a relatively long axon to the central nervous system. In mechanoreceptors the dendrites, that part of the sensory neuron nearest the site of the stimulus, typically are enclosed within a sclerotized cap cell, called the scolopale. The scolopale is attached to, or in contact with, the site where stimulation will occur, usually some internal structure or the cuticular surface. Any stretching or movement of the structure to which the scolopale is attached will stimulate the dendrites of the sensory neuron and may set up a series of nerve impulses going into the CNS. If only one sensory neuron and scolopale is present, the single unit is called a scolopodium, or chordotonal sensillum. These terms are used interchangeably. More complex mechanoreceptors contain many scolopidia or multiple scolopale units, or chrodotonal sensilla, again terms that refer to the same things. The subgenual organ is a complex chordotonal organ composed of multiple scolopidia. The name “subgenual” means below the knee, from Latin for knee (genu), and this complex chordotonal organ usually is located near the joint between the femur and tibia. Subgenual organs may contain as few as three scolopidia in some earwigs (Forficula spp.), but in most insects usually contains more scolopidia. It acts as a proprioceptor (a receptor of internal stimuli) and detects vibrations of the substrate on which the insect rests. The subgenual organ is especially well developed in crickets (Gryllidae) and katydids (Tettigonidae) and is closely associated with a tympanal organ, with both organs located on the tibia. The two organs have separate sensory innervation, however, and probably have separate functions. In some insects, the scolopidia in the subgenual organ vary in length, suggesting that different scolopidia might respond to vibrations of different amplitude according to length. The subgenual organ of the American cockroach Periplaneta americana is sensitive to vibrations that would displace the foot of the insect by as little as 10−9–10−7 cm. The subgenual organ generally is less well developed in Lepidoptera, Hymenoptera, and Hemiptera than in the Orthoptera, and some Hemiptera, Coleoptera, and Diptera do not have subgenual organs. Those without a subgenual organ display only low sensitivity to high frequency vibrations. Probably all insects have, in addition to the subgenual organ, additional more simple chordotonal sensilla on the legs, particularly at or near the leg joints, and some insects lacking a subgenual organ have a similar organ at the distal end of the tibia that may serve much the same function as the subgenual organ. Johnston’s organ is another large complex chordotonal organ that typically consists of many scolopidia. Johnston’s organ is located between the second (the pedicel) and third joints of each antenna of most adult insects. Some hexapods (Collembola and Diplura) do not have a Johnston’s organ. A simplified form of the organ occurs in some larvae. Johnston’s organ responds to several kinds of stimuli in different insects, including acting as a proprioceptor to indicate movement of the antennae, monitoring wing-beat frequency in relation to flight speed in some Diptera, serving as a gravity indicator, indicating ripples at the water surface in gyrinid beetles, and functioning as a sound reception in mosquitoes and perhaps other insects. With its location in the second antennal segment, Johnston’s organ is positioned to monitor movements of the antennal flagellum, whether due to muscles controlled by the insect, or displacements of the antennae by wind and flight. Radially arranged scolopidia are attached to the wall of the pedicel at one end and to the intersegmental membrane between the pedicel and flagellum. Johnston’s organ seems to have reached its apex of development in Chironomidae and Culicidae (Diptera), in which the pedicel is much enlarged and filled with scolopidia. It seems to function in successful Choriogenesis swarming and mating. Male mosquitoes detect the sound of the female in flight when the arista on the male antenna vibrates in resonance to the wing beats. Long hairs on the antennae of males also vibrate, causing the flagellum (the major portion of the antenna) to resonate in response to the flight sounds of females. Males of the mosquito Aedes aegypti are most sensitive to frequencies from 400 to 650 Hz, corresponding closely to the natural wing-beat frequency of females. Johnston’s organ functions as a flight speed indicator in adult Calliphora erythrocephala, and probably also in some other insects such as the housefly, honeybee, and related insects. It is probably an important gravity indicator for most insects, enabling them to have a sense of their body in relation to horizontal and vertical planes because the weight of the antenna excites scolopidia depending upon the pull of gravity relative to the body. Many insects produce sounds, are sensitive to sounds, and utilize sounds in courtship, mating, prey location, and predator avoidance. Detection of high frequency sound waves in the air is accomplished by a tympanum, a chordotonal organ containing scolopidia. Tympanal organs are located at various places on the body of insects, including near the sternum of the first abdominal segment of Acrididae (grasshoppers) and Cicadidae (cicadas), on the tibia of Tettigoniidae (long-horn grasshoppers) and Gryllidae (crickets), on the thorax of Notonectidae (water beetles), and on the thorax or abdomen of some Lepidoptera. Tympanal organs are specialized for air-borne sound pressure waves, and permit sound detection over a relatively long distance. They are sensitive to a wide range of frequencies from 2 kHz up to about 100 kHz. Typically in insects, as well as in other animals, tympanal organs are paired. A single pressure receptor is not very efficient at detecting the directionality of the sound source, but two receptors, preferably well separated from each other, can detect directionality by differences in reception at the two locations. Tympanal ears typically have a minimum of three components, (i) a thin cuticular tympanum on the cuticular surface, C (ii) an air sac or other tracheal structure behind the tympanum, and (iii) sensory neurons organized in scolopidia attached to the tympanal membrane or attached near it, so that they vibrate in response to the vibrations of the tympanum. Airborne sound waves cause the tympanum to vibrate, and sensory neurons enclosed in the scolopale cells detect the vibrations and respond by sending nerve signals to the CNS. The air cavity or tracheal sac plays an important role as a resonating chamber. Some insects have a tympanum that can respond to sound waves striking it from the inside of the air chamber as well as from outside; such tympanal organs are pressure-difference receivers, and they are especially sensitive to directionality of the sound. Some tympanal organs have scolopidia of different length, suggesting sensitivity to various frequencies, but function is unproven. Tympanal organs probably evolved from some early form of mechanoreceptor, probably a stretchregistering proprioceptor, but they evolved independently among the seven orders of insects having tympanal hearing. In addition to tympanal organs, some insects also may hear some sounds with other organs including Johnston’s organ, subgenual organs, scattered simple chordotonal sensilla, and simple hair sensilla. References Bailey WJ (1991) Acoustic behaviour of insects: an evolutionary perspective. Chapman & Hall, London, 225 pp Hoy RR, Robert D (1996) Tympanal hearing in insects. Ann Rev Entomol 41:433–450 Nation JL (2002) Insect physiology and biochemistry. CRC Press, Boca Raton, FL, 485 pp Yack JE, Fullard JH (1993) What is an insect ear? Ann Entomol Soc Am 86:677–682 Choriogenesis Production of a thin vitelline membrane and chorion by the follicle cell, the last step in production of the egg. 865 866 C Chorion Chorion The outer layer of an insect egg. The egg “shell.” Chromatids Chromosome components that have duplicated during interphase and become visible during the prophase stage of mitosis. Chromatids are held together at the centromere. Choristidae A family of insects in the order Mecoptera.  Scorpionflies Christophers, (Sir) Samuel Rickard Rickard Christophers was born in Liverpool on November 27, 1873. He graduated in medicine in 1896, and then spent some time on the Amazon. In 1898 he joined the Malaria Commission, which had been established jointly by The Royal Society and the (British) Colonial Office; that was the year in which final proof was obtained of transmission of malaria by Anopheles mosquitoes. In West Africa, he concluded quickly that people who survive malaria are the main reservoirs of the disease, allowing it to be transmitted by mosquitoes to uninfected people. After that, he worked in India, on malaria and the various Anopheles species that transmit it, showing that successful control requires knowledge of the habits and larval habitat of each implicated Anopheles species. He developed standards for malarial surveys. He investigated the anatomy and behavior of mosquitoes, including the development of mosquito eggs. Later he worked at the London School of Tropical Medicine and Hygiene, and then at Cambridge University. His landmark book (1960) “Aedes aegypti (L.), the yellow fever mosquito” was published when he was 87. At the age of 90 he retired and moved to the county of Dorset in the west of England. He died on February 19, 1978. Chromomere A region on a chromosome of densely packed chromatid fibers that produce a dark band. Chromomeres are readily visualized on polytene chromosomes. Chromosome Imprinting The mechanisms involved in chromosomal imprinting, or labeling of DNA, is associated with methylation of DNA in many organisms. Imprinting is a reversible, differential marking of genes or chromosomes that is determined by the sex of the parent from whom the genetic material is inherited. Chromosome Puffs A localized swelling of a region of a polytene chromosome due to synthesis of DNA or RNA. Puffing is readily seen in polytene salivary gland chromosomes of dipteran insects. Chromosomes Units of the genome with many genes, consisting of histone proteins and a very long DNA molecule; found in the nucleus of every eukaryote. Chronic Reference Gillett JD (1978) Sir Rickard Christophers. Antenna 2:33 In pathology, of long duration; not acute. This is usually used to describe a debilitating disease that Chronotoxicology slowly infects a population as opposed to one that quickly and dramatically infects the population. Chronic Bee Paralysis A disease of bees caused by a RNA virus (but not a picornavirus). Symptoms include flightlessness and a distended abdomen. (contrast with acute bee paralysis) Chronic Toxicity The toxic effect of a chemical following long-term or repeated sublethal exposures. Chronotoxicology maCieJ a. pszCzoLkowski Missouri State University and State Fruit Experiment Station, Mountain Grove, MO, USA All eukaryotic organisms, including insects, have developed rhythmic behavioral, physiological or biochemical patterns synchronized with particular periods of the day, to adapt to their ecological niches in the most optimal manner. Those oscillations, circadian rhythms, have evolved with a periodicity approximating 24 h, are of endogenous nature and may be adjusted to lighting stimuli. Chronotoxicology is the study of the adverse effects of chemicals on living organisms in relation to their circadian rhythms. In particular, it examines toxicants’ chronotoxicity, i.e., periodic changes in sensitivity of living organisms to toxicants. Historical Perspective Circadian changes in sensitivity to toxicants were first reported in mice by Halberg and Stephens as early as 1958. Five years later, Stanley Beck showed that the German cockroach, Blatella germanica (L.) exhibits a 24-h susceptibility rhythm when C administered a standard dose of potassium cyanide at different times of the day. Within a little more than a year of Beck’s report, two papers on insecticide chronotoxicity appeared in the prominent journal Science. Cole and Adkisson reported diurnal variations in mortality from a standard dose of trichlorfon applied to the beetle, Anthonomus grandis, and Polcik and colleagues, in a paper on dichlorvos chronotoxicity to the mite, Tetranychus urticae (Koch) posed an important and novel concept that “the findings of a marked sensitivity pattern should emphasize the importance of considering circadian organization [of the pest] in the evaluation and interpretation of toxicological experiments with insecticides.” Soon, Nowosielski et al. reported daily changes in susceptibility of the house cricket, Acheta domesticus (L.) and T. urticae to anesthetics (ethyl ether, chloroform and carbon tetrachloride). These pioneering papers demonstrated that susceptibility to toxicants fluctuate during the day, and are dependent not only on properties of the toxicant, but also on endogenous rhythmic changes in pest physiology. One might have predicted that by now, monitoring the diurnal susceptibility to toxicants (and, in particular, to insecticides) would be an experimental routine for establishing toxicity parameters. However, recent inquiry suggests that papers on the chronotoxicity of insecticides are rarities. Forty years after pioneering publications of Beck, Polcik and colleagues and Cole and Adkisson, Pszczolkowski and associates inspected representative databases (Medline, Toxline, Agricola, and Internet Database Service-Biological Sciences) in search of papers on pesticide chronotoxicity to insects. The search, followed by paperto-paper inquiry yielded only 16 reports referring to diurnal or circadian changes in insecticide toxicity in insects. Four more were found more recently. Ten of them examined difference between the highest and the lowest mortality percent after application of a standard dose of insecticide at various times of the day, in the remaining reports diurnal variations in LD50 were reported. However, even these scanty data show that insect mortality 867 868 C Chronotoxicology can be as much as nine times higher than if the same, standard dose is applied at some other time or times, and that, depending on the time of testing, the highest LD50 may be up to 7.5 times higher than the lowest LD50 for the same toxicant. Coincidence of Insecticide Susceptibility Rhythms and Other Biological Rhythms Theoretically, periodic changes in insecticide sensitivity should reflect periodic changes in ratios of penetration, ratios of detoxification (including metabolism, elimination from hemolymph and excretion of a given toxicant), periodic alterations at the site of action (for instance, periodic over- or underexpression of target receptors) or their combinations. This assumption was reiterated in publications devoted to physiological and behavioral aspects of insect biological rhythms, e.g., in fundamental “Insect clocks.” Unfortunately, this hypothesis did not attract attention of many researchers. Perhaps the most extensive analysis of physiological and biochemical events that underlie circadian sensitivity to an insecticide was research on house fly, Musca domestica (L.). Mean LD50 values for DDT were established as a function of application time in the house fly, kept in a specific photoperiodic regimen. Flies tested topically with DDT had a significantly lower LD50 value when treated at the end of the dark phase, and increased tolerance to DDT during the early part of the dark phase. This distribution was apparently caused by some endogenous oscillations, because the flies kept in total darkness exhibited similar pattern of DDT susceptibility. This rhythmic response was not caused by changes in cuticle permeability to the insecticide, for regardless of the time of application, about 40% of DDT was absorbed within 2 h. However, comparison of DDT susceptibility rhythm and rhythmic changes in respiration and DDT breakdown to DDE do not support the hypothesis that elevation of DDT toxicity (Fig. 51) was caused by decrease in dynamics of detoxification mechanisms. The data Chronotoxicology, Figure 51 Diurnal distributions of LD50 from DDT versus diurnal changes in respiration and DDT breakdown in WHO strain of the house fly Musca domestica. Generally, low respiratory rates and low DDT metabolism correspond with high tolerance to DDT, and high levels of detoxification correspond with high susceptibility to DDT, which is an unexpected correlation. For the sake of clarity, the original measurements are normalized and expressed as percent of the maximum value obtained for diurnal toxicity, respiration and DDT breakdown pattern, respectively. Shaded areas mark the dark phase of the photoperiod. (Collated and modified from Shipp E, Otton J (1976) Circadian rhythms of sensitivity to insecticides in Musca domestica (Diptera, Muscidae). Entomol Exp Appl 19:163–171; Shipp E, Otton J (1976) Diel changes in DDT absorption and breakdown rates and respiratory rhythm in the housefly, Musca domestica. Entomol Exp Appl 19:235–242.) show an opposite trend: relatively low ratios of DDT breakdown and respiration correspond with relatively high ratios of DDT tolerance, and vice versa. Only at 15:00 p.m. high tolerance to DDT is correlated with high levels of respiration and DDT breakdown. Thus, circadian changes in susceptibility of Musca domestica to DDT were generally independent of ability to detoxify DDT. Perhaps the oscillations in this insecticide tolerance were caused by some alterations at the target site. Time-dependent events in insect systems involved in insecticide toxicity and metabolism Chronotoxicology may be even more complex, given the mode of action of insecticide studied. Research on metabolism of di-syston (0,0-diethyl S-2 (ethylthio) ethyl phosphoditioate) in larvae of Heliothis zea (Boddie) is a good example. Di-syston requires biological oxidation to become active; thus, in addition to periodic changes in ratios of insecticide penetration, detoxification, or periodic alterations at the site of action one must consider periodic changes in activity of oxidative enzymes which are necessary to activate the insecticide. In this study, the experimental insects were maintained in a specific photoperiodic regimen (14 h of light- and 10 h of dark phase) and controls were exposed to constant light. The treatments aimed to synchronize larval biochemical processes to photoperiod, or keep them de-synchronized, respectively. In both groups, the larvae were injected with standard dose of isotopelabeled insecticide in various times of the day. Radioactivity of hydrolytic or oxidative metabolites of di-syston was determined in larval tissues and excreta, 4 h after injection, revealing three distinct rhythms. Oxidation (and therefore toxicity) of disyston (Fig. 52) reached the highest ratios at the end of the light phase and at the end of the dark phase of the photoperiod, and dropped to the lowest values soon after lights on and after lights off. The rhythm of hydrolase activity was bimodal too, with peaks in the middle of either dark or light phase of the photoperiod. The latter rhythm roughly corresponded with the rhythm of di-syston metabolite excretion. Control larvae, maintained in desynchronizing lighting conditions, did not show rhythmic patterns of di-syston metabolism. This work has two important implications. First it shows that sometimes a researcher should consider at least one more rhythmic organismal event influencing toxic potential of an insecticide administered at various times of the day; in this case time dependent changes in activation of toxic properties of the insecticide. Second, it shows that lighting conditions may influence periodic responses to insecticide toxicity (in their study, periodic changes in di-syston activation and degradation were abolished in constant light). It is a C Chronotoxicology, Figure 52 Diurnal changes in oxidation and hydrolysis of isotope-labeled Di-syston by Heliothis zea last instar larvae. Standard doses of this insecticide were applied at various times of the day. Di-syston requires biological oxidation to become insecticidally active, thus diurnal changes in its oxidation reflect its actual toxic potential. Changes in hydrolysis reflect dynamics of detoxification. B. Diurnal changes in concentrations of Di-syston metabolites in excreta of Heliothis zea last instar larvae. High activity of hydrolytic enzymes is correlated with low concentrations of toxic products of Di-syston oxidation (A) and products of Di-syston detoxification are excreted immediately (B), showing bimodal diurnal pattern of detoxification. Shaded areas mark the dark phase of the photoperiod. (Modified from Bull DL, Lindquist DA (1965) A comparative study of insecticide metabolism in photoperiod-entrained and unentrained boll-worm larvae Heliothis zea (Boddie). Comp Biochem Physiol 16:321–325.) pity that they did not provide information about diurnal changes in mortality of H. zea larvae due to di-syston. I am not aware of this information being available in literature. 869 870 C Chronotoxicology Because periodic changes in physiological or biochemical processes are difficult to monitor, a number of reports have suggested that circadian rhythms in insect sensitivity to toxicants could be correlated to locomotor activity rhythms, which are relatively easy to record. For example, it has been noted by several investigators that there is a general trend of a time of greatest susceptibility occurring at about the time of onset of increased activity. However, the scanty data published on coincidence of daily changes in susceptibility to insecticide treatment and rhythms of locomotor activity do not support this assumption. There is no universal rule that would allow predicting the time of the greatest sensitivity to insecticides by monitoring circadian patterns of locomotor activity. It seems that the time of greatest sensitivity depends on the species, mode of treatment and the insecticide tested rather than a specific moment in the insect’s activity pattern. Biological Rhythms and Measuring Toxicity Parameters Thus, it appears that insect toxicologists should concern themselves with not only the usual parameters of insecticide toxicity, but also with diurnal distribution of toxicity. At the very least, circadian time of treatment should be indicated in reports on mortality tests, particularly if toxicity parameters are used for comparative study of insecticide resistance. For example, in one study two samples of the beetle Diabrotica virgifera virgifera (LeConte) were collected, one in August 1967 and the other 12 months later, from the same location, which was meanwhile exposed to routine sprays with diazinon. Daily distributions of LD50 (Fig. 53) were established for either population of the beetles. If the author had limited himself to one toxicity assay at 7:00 a.m. in 1967, and one toxicity assay at 11:00 a.m. in 1968, he would have probably concluded that no resistance has been built up between 1967 and 1968. In fact, the field populations of Diabrotica increased resistance to diazinon by about 70% Chronotoxicology, Figure 53 Diurnal patterns of Diazinon toxicity to field populations of adult Diabrotica virgifera virgifera. The photoperiod shown is the naturally occurring photoperiod under which the beetles were living when collected. Upper curve shows LD50 distribution for the population collected in 1968. The lower curve reflects susceptibility of the population collected 12 months earlier. Only determination of diurnal LD50 distributions and maintaining the same photoperiodic regimen and similar timing of insecticide treatment allowed demonstration of increased resistance to Diazinon (further explanations in text). Shaded areas mark the dark phase of the photoperiod. (Modified from Ball HJ (1969) Diurnal rhythm of sensitivity to diazinon in adult western corn rootworms. J Econ Entomol 62:1097–1098.) during that period of time, and only investigation of diurnal pattern of susceptibility revealed increase in resistance against this insecticide. Precautionary measures should also be taken if insecticide resistance is compared between populations of the same age, and the same history of toxicant exposure, but kept under different breeding or testing regimens. Because insects are known to synchronize their endogenous rhythms to exogenous stimuli such as photo- or thermoperiod (a phenomenon called “entraining to a rhythm” in chronobiological nomenclature) the diurnal distribution of insecticide sensitivity may be synchronized to external conditions too. This was observed when house flies were reared through multiple generations, each experimental population in a different photoperiod. Seven different photoperiods were used, including Chronotoxicology constant light throughout 24-h cycle. In the first set of experiments the flies were treated with standard doses of trichlorfon at various times of the day. Next, the flies were returned to their respective photoperiodic regimens and percent mortality was recorded 48 h later. Mortality depended both upon the time of treatment commencement and the photoperiodic regimen the insects were kept in. For instance, mortality from trichlorfon administered at 10:00 a.m. almost did not vary, oscillating between 96 and 93 % regardless of the photoperiod to which the flies were synchronized, and maintained in, during the exposure (Fig. 54) to the insecticide. However, in the Chronotoxicology, Figure 54 Susceptibility of house flies to standard dose of trichlorfon at various times of the day as a function of the length of the light phase of the photoperiod. The flies were reared in specific photoperiod for several generations before and during exposure to the insecticide. The light in each experimental group came on at the same time (7:00 A.M.), trichlorfon was administered in various times of the day. The flies tested at 10:00 A.M. exhibited almost the same mortality ratios regardless of photoperiod they were reared and tested under. The flies tested at 4:00 P.M. or 9:00 P.M. showed marked variations in mortality from standard dose of trichlorfon, dependent on the photoperiod they had experienced prior to the tests and during exposure to the insecticide. (Modified from Fernandez AT, Randolph NM (1967) Photoperiodic effect on the daily susceptibility of the house fly to trichlorfon. J Econ Entomol 60:1633–1635.) C groups treated with trichlorfon in other times of the day, marked differences in mortality were observed. For instance, in group treated at 4:00 p.m., the mortality varied from 78 to 95%, depending on the length of the light phase of the photoperiodic regimen used. When the flies were exposed to the insecticide at 9:00 p.m. the differences were even greater. In another experiment, the flies were similarly reared in various photoperiodic regimens, and therefore their endogenous rhythms had synchronized to external light:dark oscillations of their specific photoperiodic regimens. Next, the flies were treated with various doses of trichlorfon at a fixed time of the day, corresponding not only to a fixed time of their own photoperiodic regimen (for instance 9 h after the onset of light) but also to a fixed time of the astronomical day (in this case 4:00 p.m.). Subsequently the flies were transferred to constant lighting conditions, where no oscillating stimuli could have influenced insects’ endogenous rhythms. After 48 h of exposure to trichlorfon (Fig. 55), the LD50 Chronotoxicology, Figure 55 Variability of LD50 from trichlorfon administered at fixed time of the day to the flies that had been synchronized to various photoperiods before the testing took place. The flies were kept in various photoperiods for several generations, and then exposed to the insecticide for 48 h under constant lighting conditions. Beginning of insecticide treatment commenced 9 h after lights on (4:00 P.M.), in each group. The flies that had experienced photoperiod light:dark 14:10 prior to the test were markedly more resistant to trichlorfon than those that had been kept in photoperiod light:dark 13:11. (Drawn on the basis of data by Fernandez and Randolph, 1967.) 871 872 C Chronotoxicology was calculated. The flies entrained to the photoperiod consisting of 13 h of light phase and 11 h of dark phase were three times more susceptible to trichlorfon than the flies entrained to only slightly different photoperiod (14 h of light phase and 10 h of dark phase). Analogous experiments with DDT, endrin and dieldrin yielded similar results. These remarkable results show that some insects entrained to a photoperiod maintain their characteristic rhythmicity of detoxification under constant lighting conditions, and their diurnal distribution of susceptibility to toxicants are determined by synchronizing stimuli from the past. Entraining, as a feature of circadian organization of insect physiology and behavior, clearly should be taken into consideration while planning toxicity tests, but many insect toxicologists do not realize how sensitive to entraining insect physiological systems can be. Insect populations do not need to be exposed to certain photoperiodic conditions for several successive generations to synchronize their organismal oscillations to external lighting regimen. For instance, short-lasting exposures to light during the dark phase of the rhythm also effectively synchronize rhythms in adult insects of some species (e.g., many dipterans). Such a stimulus may shift the insect endogenous rhythms by several hours in comparison to original pattern of physiological oscillations,inducing a response (so-called phase response) that lasts for days if not weeks under continuous lighting conditions. Even temporary changes in insect breeding conditions may have profound effects on detoxification rhythms and, consequently, diurnal distribution of mortality in toxicity tests. Concluding Remarks An entomologist aware of time-dependent changes in toxicity of insecticides, toxicants or narcotic agents finds himself in a frustrating situation. On one hand, it is reasonable to propose that circadian organization of mechanisms that underlie insecticide uptake, detoxification, action on the target sites or at least diurnal distribution of mortality should be carefully studied before ultimate toxicity parameters are established and released as a basis for further use. On the other hand, chronotoxicological experiments are labor expensive and time intensive. The scarcity of published data does not allow any generalization as to methodology of experimenting: there is no universal correlation of susceptibility patterns with daily distribution of locomotor activity. Dynamic detoxification processes sometimes do not correlate with toxicity changes in an expected manner; the same photoperiodic conditions may abolish cyclic changes in insecticide metabolism (and, presumably, toxicity) in one species, such as H. zea larvae, or permit changes in susceptibility to occur in another, such as adult house flies. Research in insecticide chronotoxicology apparently does not attract funding, and its results are not easy to interpret, discuss and publish, since there is not much literature on this topic. Nor has monitoring the diurnal distribution of pest susceptibility to insecticides become an experimental routine for establishing insecticide toxicity parameters. Impressive progress in knowledge of insect toxicology, insecticide resistance mechanisms and insect chronobiology has been made, but these disciplines need integration. Perhaps younger generations of entomologists will charge themselves with such a task.  Rhythms in Insects  Insecticides  Insecticide Toxicity  Insecticide Bioassays References Bainbridge CA, Margham P, Michael T (1982) Diurnal fluctuations in susceptibility to insecticides in several strains of the yellow fever mosquito (Aedes egypti L.). Pest Sci 13:92–96 Ball HJ (1969) Diurnal rhythm of sensitivity to diazinon in adult western corn rootworms. J Econ Entomol 62:1097–1098 Beck SD (1963) Physiology and ecology of photoperiodism. Bull Entomol Soc Am 9:8–16 Bull DL, Lindquist DA (1965) A comparative study of insecticide metabolism in photoperiod-entrained and unentrained boll-worm larvae Heliothis zea (Boddie). Comp Biochem Physiol 16:321–325 Cibarium Cole CL, Adkisson PL (1964) Daily rhythm in the susceptibility of an insect to a toxic agent. Science 144:1148–1149 Crystal MM (1969) Changes in susceptibility of screw-worm flies to the chemosterilant Nʹ, Nʹ-tetramethylenebis (1-aziridinecarboxamide), with time of administration. J Econ Entomol 62:275–276 Eesa NM, Cutkomp LK (1995) Pesticide chronotoxicity to insects and mites: an overview. J Islam Acad Sci 8 (1):21–28 Fernandez AT, Randolph NM (1967) Photoperiodic effect on the daily susceptibility of the house fly to trichlorfon. J Econ Entomol 60:1633–1635 Halberg F, Stephens AN (1958) 24-hour periodicity in mortality of C mice from E. coli lipopolysaccharide. Fed Proc17:439 Halberg J, Halberg F, Lee JK, Cutcomp LK, Sullivan WK, Hayes DK, Cawley BM, Rosenthal J (1974) Similar timing of circadian rhythms in sensitivity to pyrethrum of several insects. Int J Chronobiol 2:291–296 Kermarrec A, Abud-Autun A (1978) Variations de la sensibilité au parathion selon l’heure chez Acromyrmex octospinosus Reich (Formicidae, Attini). Ann Zool Ecol Anim 10:29–35 Nowosielski JW, Patton RL, Naegele JA (1964) Daily rhythm of narcotic sensitivity in the house cricket, Gryllus domesticus L., and the two-spotted spider mite, Tetranychus urticae Koch. J Cell Comp Physiol 63:393–398 Polcik B, Nowosielski JW, Naegele JA (1964). Daily sensitivity rhythm of the twospotted spider mite, Tetranychus urticae, to DDVP. Science 145:405–406 Pszczolkowski MA, Dobrowolski M, Spencer C (2004) When did you last test your insects? The forgotten importance of chronotoxicology. Am Entomol 50:72–74 Saunders DS (1982) Insect clocks, 2nd edn. Pergamon Press, New York, NY, 408 pp Shipp E, Otton J (1976a) Circadian rhythms of sensitivity to insecticides in Musca domestica (Diptera, Muscidae). Entomol Exp Appl 19:163–171 Shipp E, Otton J (1976b) Diel changes in DDT absorption and breakdown rates and respiratory rhythm in the housefly, Musca domestica. Entomol Exp Appl 19:235–242 C Chrysomelidae A family of beetles (order Coleoptera). They commonly are known as leaf beetles.  Beetles  Leaf Beetles (Coleoptera: Chrysomelidae) Chrysopidae A family of insects in the order Neuroptera. They commonly are known as green lacewings.  Lacewings, Antlions and Mantidflies  Natural Enemies Important is Biological Control Chrysopolomidae A family of moths (order Lepidoptera) also known as African slug caterpillar moths.  African Slug Caterpillar Moths  Butterflies and Moths Chyromyid Flies Members of the family Chyromyidae (order Diptera).  Flies Chyromyidae Chrysalis The pupal stage of a butterfly. Chrysididae A family of wasps (order Hymenoptera). They commonly are known as cuckoo wasps.  Wasps, Ants, Bees and Sawflies A family of flies (order Diptera). They commonly are known as chyromyid flies.  Flies Cibarium The preoral cavity; an external space in front of the head that is surrounded by the mouthparts but in front of the true mouth or stomodeum. 873 874 C Cicada Parasite Beetles Cicada Parasite Beetles Members of the family Rhipiceridae (order Coleoptera).  Beetles Cicadas (Hemiptera: Cicadoidea) aLLen sanBorn Barry University, Miami Shores, FL, USA The members of the superfamily Cicadoidea Westwood are four-winged insects with sucking mouthparts that possess three ocelli and a rostrum that arises from the base of the head. Family Tettigarctidae White Contains two species in the genus Tettigarcta White (Fig. 56). The extant members of this family are restricted in their distribution to Australia. The Tettigarctidae exhibit ancestral morphology showing many similarities in their structure to fossil cicadas. They have a expanded pronotum that lacks paramedial and lateral fissures and a pronotal collar and conceals much of the mesonotum along with peculiar wing venation. The mesonotum lacks a cruciform elevation. The hind coxae overhang the abdomen. In addition, both sexes of the Tettigarctidae have a timbal apparatus but the structures are poorly developed and they lack tympana. Males lack an acoustic resonating chamber in the abdomen. They have recently been shown to communicate through vibrational rather than airborne signals. Classification The classification within the superfamily has had a varied history. There have been as many as six families described within the superfamily. The major characters used to separate these families are structures of the sound production system, e.g., the timbal covers and stridulatory apparatuses. The separation of the two major historical families was based primarily on the presence or absence of timbal covers. However, the variation in the timbal cover anatomy is not related to a monophyletic ancestry within the groups. Similarly, the stridulatory structures have evolved as a means to isolate species reproductively and, therefore, appear to have evolved independently more than once. As a result, the structures of the sound apparati were a poor choice of characters on which the higher taxonomy should be based. The recent analysis of the higher taxonomy of the Cicadoidea suggests only two families are justified within the Cicadoidea, the Tettigarctidae and the Cicadidae. Order: Hemiptera Infraorder: Cicadomorpha Superfamily: Cicadoidea Family Cicadidae Latreille Members of this family (Fig. 57) represent the vast majority of extant cicadas. Characters that separate members of the family include: a pronotum that includes a pronotal collar, paramedial and lateral fissures and is smaller than the mesonotum; the mesonotal scutellum forms a cruciform elevation; timbals if present only found in males; males have an abdominal resonating chamber; both sexes have tympana. The extant genera have been divided into three subfamilies based on the Cicadas (Hemiptera: Cicadoidea), Figure 56 Tettigarcta crinita Distant, 1883, a member of the family Tettigarctidae. Cicadas (Hemiptera: Cicadoidea) Cicadas (Hemiptera: Cicadoidea), Figure 57 Cicada orni Linnaeus, 1758, a representative of the family Cicadidae. structure of the male genitalia, wing venation, timbal covers, and opercula. It includes the members of all previously described families except the Tettigarctidae. Chararacteristics Adults Cicadas show a large range in adult body size. The smallest species have body lengths of 1 cm and wingspans of <2 cm while the largest species have body lengths of 7 cm and wingspans of almost 20 cm. The body coloration varies from a uniform reddish, green, brown, or black to a mixture of colors. The coloration pattern of the pronotum and mesonotum is especially useful in determining species. The head is dominated by the two compound eyes. Three ocelli form a triangle on the dorsal surface of the head between the compound eyes. This arrangement of the ocelli is one of the distinguishing characteristics separating cicadas from other bugs. The antennae are short and are located between the postclypeus and the compound eyes. The mouthparts form a needlelike rostrum that is inserted into plants to obtain xylem fluid. The postclypeus houses the pumping musculature. The thorax is divided into the three segments characteristic of insects. Each thoracic segment has a pair of legs and wings are attached C to the mesothorax and metathorax. The wings can be hyaline, they may be infuscated, or they may be opaque or pigmented. Wing venation is another significant character used in taxonomy. The opercula are another diagnostic character that originate on the ventral metathorax but extend toward and often cover large portions of the abdomen. The abdomen is clearly segmented with the terminal segments modified to form the reproductive organs. The genitalia are one of the most important structures in identifying species. The abdomen of male cicadas is generally hollow and acts as a resonating organ to increase the song intensity. In addition, the timbal covers may be found covering the timbal organ of the male. Immature Stages Documented life cycles of cicadas range from 1 to 17 years. The life cycle can be variable within a species and emergence may be determined by the quality of the food source for the nymph, or all the individuals of a population may emerge synchronously as in the periodic cicadas (Magicicada spp.). Eggs are laid in twigs or stems of the host plants. The nymphs will crawl out of the egg and fall to the ground after hatching. The nymph will then burrow into the ground and attach to a root to obtain nourishment. The nymph will construct a chamber around the root in which it will grow and proceed through its hemimetabolous development. When it is mature, the nymph will emerge from the soil, find a vertical surface on which it can attach and then the adult encloses from it. Natural History Cicadas are found on all continents except Antarctica. They have a broad distribution in the tropical and temperate latitudes and can be found wherever permafrost is absent. As is common in the animal kingdom, the tropics are rich with species diversity. There is a correlation between the described cicada 875 876 C Cicadas (Hemiptera: Cicadoidea) diversity for particular geographic regions and where cicada taxonomists have concentrated their efforts during their individual careers either through repeated expeditions or by living in a particular region. One of the most distinguishing characteristics of cicadas is their acoustic behavior. The sounds produced by cicadas are species specific and are becoming useful tools in species identification. The sounds are generally produced by males but females have evolved acoustic responses to male signals. The major male sound production system is a timbal organ. The timbal organ is a ribstrengthened, chitinous membrane located in the first abdominal segment that is buckled by contraction of a timbal muscle. Structures such as the abdominal air sacs, opercula, and timbal covers can modify the sound emitted by the cicada. Stridulatory apparati have evolved in several genera as an accessory sound production system. The stridulatory systems are generally associated with the wings and the mesothorax but a genital system has also been described. Finally, crepitation is used as the primary communication signal by two genera of North American cicadas. The stridulatory and crepitation systems permit two way communication between the sexes in contrast to the unidirectional timbal system. Birds are major predators of adult cicadas. Emergences of periodical cicadas represent a superabundant food source and many animals (e.g., fish, amphibians, reptiles, birds and mammals) change their foraging habits to include the cicadas. Cicada killers (family Sphecidae) are natural parasites that provision their nests with adult cicadas as food for their offspring. Nymphs burrowing into the ground are prey for ants whereas underground nymphs are prey for animals like moles and boars. Predators such as spiders, mantids, robber flies, and bats also take adult cicadas as prey. There are also several genera of entomopathogenic fungi that use cicadas as hosts. Some fungi grow on nymphs (e.g., Cordyceps spp.) while others grow on the adults (e.g., Massospora spp.). Agricultural Importance The main source of agricultural damage occurs when the females oviposit in their host plants. Large emergences of cicadas (i.e., periodic cicadas) and their corresponding oviposition can cause small trees to wilt and small branches to break off trees. In addition, the loss of nutrients to the host tree in supporting a heavy infestation on its roots can lead to decreased growth and fruit production. These effects have been well documented in apple orchards located near old growth forests that support a large cicada population. There are several contact insecticides that can kill the adults but they cannot be relied upon to protect the trees completely. The slow action of the pesticides makes controlling the damage caused by the adults difficult. Pruning trees prior to cicada emergence decreases the availability of preferred oviposition sites. Covering small trees with cheesecloth or some form of netting to prevent access has been a successful strategy to protect trees particularly susceptible to damage. Several species around the world have moved from natural grasses as their host plant to sugarcane. These species decrease the yield of the sugarcane fields they infest. A successful control strategy has been to till the soil which kills the nymphs. Adults can also be controlled with contact insecticides. There have been reports of cicadas ovipositing in other food crops such as dates, asparagus, citrus trees, cotton, grapevines, etc. These reports are generally isolated, and cicadas do not appear to be major agricultural pests with the exceptions noted above.  Sound Production in the Cicadoidea References Boulard M (2001) Higher taxonomy and nomenclature of the Cicadoidea or true cicadas: history, problems and solutions (Rhynchota Auchenorhyncha Cicadomorpha). Ecole Pratique des Hautes Etudes, Travaux du Laboratoire Biologie et Evolution des Insectes Hemipteroidea 14:1–48 Citricola Scale, Coccus pseudomagnoliarum (Kuwana) (Hemiptera: Coccidae) Duffels JP (1993) The systematic position of Moana expansa (Homoptera: Cicadidae), with reference to sound organs and the higher classification of the superfamily Cicadoidea. J Nat Hist 27:1223–1237 Moulds MS (1990) A guide to Australian cicadas. New South Wales University Press, Kensington, Australia, 217 pp Moulds MS (2005) An appraisal of the higher classification of cicadas (Hemiptera: Cicadoidea) with special reference to the Australian fauna. Rec Aust Mus 57:375–446 Myers JG (1929) Insect singers: a natural history of the cicadas. George Routledge and Sons, Limited, London, UK, 304 pp Cicadellidae A family of bugs (order Hemiptera). They commonly are known as leafhoppers.  Leafhoppers  Bugs C Cimicidae A family of bugs (order Hemiptera). They sometimes are called bed bugs.  Bugs  Bedbugs (Hemiptera: Cimicidae) Circadian Rhythm An endogenous biological rhythm with a recurrence of about 24 h. Changes in biological or metabolic functions that show periodic peaks or lows of activity based on or approximating a 24-h cycle. This also is known as a circadian clock.  Biological Clock of the German Cockroach, Blatella germanica (L.) Cicindelidae A group of beetles (order Coleoptera), sometimes treated as a separate family, here considered part of Carabidae. They commonly are known as tiger beetles.  Beetles  Tiger Beetles Cigarette Beetle  Stored Grain and Flour Insects Ciidae A family of beetles (order Coleoptera). They commonly are known as minute tree-fungus beetles.  Beetles Cimbicidae A family of sawflies (order Hymenoptera, suborder Symphyta).  Wasps, Ants, Bees and Sawflies Circulative Virus A virus that systemically infects its insect vector and usually is transmitted for the remainder of the vector’s life. Circumesophageal Connective The bilateral neural connective between the tritocerebrum and the subesophageal ganglion. Usually the alimentary canal passes between the circumesophageal connectives.  Nervous System Citricola Scale, Coccus pseudomagnoliarum (Kuwana) (Hemiptera: Coccidae) This species is a citrus pest in California, USA.  Citrus Pests and Their Management 877 878 C Citrus Blackfly, Aleurocanthus woglumi (Ashby) (Hempitera: Aleyrodidae) Citrus Blackfly, Aleurocanthus woglumi (Ashby) (Hempitera: Aleyrodidae) This citrus pest is a black-colored whitefly.  Citrus Pests and Their Management Citrus Greening Disease This psyllid-transmitted disease is a serious hazard to citrus crops.  Transmission of Plant Diseases by Insects Citrus Leafminer, Phyllocnistis citrella (Stainton) (Lepidoptera: Gracillaridae)” This leaf-mining caterpillar is a pest of young trees.  Citrus Pests and Their Management Citrus Mealybug, Planococcus citri (Risso) (Hempitera: Pseudococcidae) This mealybug threatens citrus crops in USA.  Citrus Pests and Their Management Citrus Peelminer, Marmara gulosa (Guillen and Davis) (Lepidoptera: Gracillaridae) This is a minor citrus pest in USA.  Citrus Pests and Their Management Citrus Pests and their Management roBert meaGher USDA, Agricultural Research Service, Gainesville, FL, USA Botanically, the genus Citrus L. is an evergreen tree in the family Rutaceae. As a commercial tree, it is composed of a scion (the variety) and the rootstock. These two parts are budded or grafted together, with the goal of combining the best properties of each to make a tree that produces plenty of quality fruit. The genus Citrus contains many species and hybrids. Some of the more common fruits are citron (C. medica L.), sour orange (C. aurantium L.), pummelo (C. maxima Merril), lemon (C. limon (L.) Burm. f.), mandarin or tangerine (types with red-orange skin) (C. reticulata Blanco), common, Mexican, West Indian, or Key lime (C. aurantifolia (Christm. et Panz.) Swingle, Tahiti lime (C. latisfolia Tanaka), sweet lime (C. limettioides Tanaka), grapefruit (C. maxima var. racemosa, formerly C. paradisi MacFayden), and orange or sweet orange (C. sinensis (L.) Osbeck). Species in Citrus can readily interbreed or hybridize. Many combinations are commercially available, such as tangelo (mandarin X grapefruit), mandarin lime (lemon X mandarin), and tangor (mandarin X sweet orange). Other species or hybrids of Citrus are used as rootstocks. History of Citrus Citrus species probably originated in southeast Asia and India. Various citrus fruits, such as lemons, limes, and oranges, were cultured in the Indus Valley over 4,000 years ago. The modern citrus varieties most likely came from China. Conquering armies, traders, and explorers from the Romans to the Arabs to the western Europeans transported citrus fruits and seeds from Asia through southern Europe, northern Africa and to the New World. Christopher Columbus brought sour orange, lemon, and citron seeds when he established colonies in Haiti and the Caribbean. Spanish explorers brought oranges to St. Augustine, Florida, from 1513 to 1565, and Ponce de Leon brought seeds and ordered sailors to plant them wherever they landed. Grapefruit arrived in Florida much later, when a grove was planted near Tampa in 1823. Spanish missionaries introduced citrus to California in 1769. Citrus Pests and their Management Pest Descriptions This section includes the important mite and insect species (Table 12, Figs. 58–60) that attack citrus in the continental United States (Arizona, California, Florida, and Texas), though many are cosmopolitan. Pest management considerations are discussed at the end of this section. Acari Citrus is infested by several groups of mites including rust and bud mites (Eriophyidae), spider mites (Tetranychidae), false spider mites (Tenuipalpidae) and broad mites (Tarsonemidae). Mites have piercing-sucking mouthparts that physically injure leaves and fruit by removing cell contents and by injecting plant toxins and viruses. Mite management depends principally on protecting biological control agents, secondarily on application of horticultural oils to foliage, and as a last resort applications of miticides. Eriophyidae Citrus rust mites, Phyllocoptruta oleivora (Ashmead), are small, light yellow, and elongated mites. They are serious pests in Florida, Texas, and California coastal districts. These mites injure leaves by penetrating the lower epidermal layer of cells promoting dry necrotic areas called mesophyll collapse. This “russeting” results in leaf drop, especially during dry periods. Feeding in fruit destroys rind cells and on oranges this injury is also referred to as russeting. Injury to grapefruit, lemons, and limes during early fruit growth causes “silvering” of the peel and, if severe, results in a condition called “shark skin.” These blemishes lower the grade of fresh fruit, reduce fruit size, and increase fruit drop. There are several natural enemies of citrus rust mites including the parasitic fungus Hirsutela thompsonii Fisher. C Pink citrus rust mite, Aculops pelekassi (Keifer), is similar to citrus rust mites in feeding and injury. They can coexist on the same leaves, but A. pelekassi can develop larger, more damaging populations earlier in the season. Pink citrus rust mites are usually pink and are narrower than citrus rust mites. Citrus bud mite, Eriophyes sheldoni Ewing, is primarily a pest of coastal lemons in California. They feed within leaf axil buds and developing blossoms, causing formation of multiple buds and abnormal growth of subsequent leaf foliage or flowers. Several other eriophyid mites are pests in other world citrus areas, the citrus grey mite, Calacarus citrifolii Keifer, in southern Africa, and the brown citrus mite, Tegolophus australis Keifer, in coastal New South Wales and Queensland, Australia. Tetranychidae Citrus red mite, Panonychus citri (McGregor), was recognized as a pest in Florida in 1885, but was not identified in Texas until the early 1980s. In California, it was initially a pest in coastal areas, but by the 1930s spread to more inland districts. It is considered a sporadic pest, and occurs mostly on lemons and grapefruit. Adult mites are red or purple with large pink to white hairs (setae) on the body. Adults and immatures feed on leaves, fruit, and green twigs, but prefer the upper surface of young leaves. Injury to leaves and fruit is caused by extraction of chlorophyll. This “stippling” causes a grayish or silvery appearance, and severe stippling can lead to mesophyll collapse. High populations may cause leaf drop and twig dieback, and fruit sunburn in summer. During dry, cold, windy conditions, high mite populations may cause a condition known as “firing,” “blasting,” or “burning” of the foliage. There are many natural enemies of citrus red mites including lady beetles (species of Stethorus) and predaceous mites (species in the genera Galendromus, Typhlodromalus, and Euseius). 879 880 C Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury Taxa scientific/Common name Geographic area Site of injury Phyllocoptruta oleivora (Ashmead) citrus rust mite world (humid areas) twigs, leaves, fruit Aculops pelekassi (Keifer) pink citrus rust mite world (humid areas) twigs, leaves, fruit Eriophyes sheldoni (Ewing) citrus bud mite world blossoms, fruit Panonychus citri (McGregor) citrus red mite world leaves, fruit, green Eutetranychus banksi (McGregor) Texas citrus mite western hemisphere leaves Eotetranychus sexmaculatus (Riley) sixspotted mite western hemisphere, Asia leaves E. lewisi (McGregor) Lewis spider mite southern California fruit E. yumensis (McGregor) Yuma spider mite southern California, Arizona leaves, fruit, green twigs Tetranychus urticae (Koch) twospotted spider mite world leaves T. pacificus (McGregor) Pacific spider mite western U.S. leaves, fruit, green twigs Arachnida Acari Eriophyidae Tetranychidae T. tumidus (Banks) tumid spider mite southeastern U.S. leaves T. mexicanus (McGregor) Mexican spider mite southern North America to South America leaves Brevipalpus phoenicis (Geijskes) red & black flat mite world fruit, leaves, twigs B. obovatus (Donnadieu) privet mite world fruit, leaves, twigs B. californicus (Banks) false spider mite world fruit, leaves, twigs B. lewisi (McGregor) citrus flat mite California, Japan fruit, leaves, twigs world leaves, fruit Romalea guttata (Houttuyn) eastern lubber grasshopper southern U.S. leaves, fruit Schistocerca americana (Drury) American grasshopper North America leaves, fruit Tenuipalpidae Tarsonemidae Polyphagotarsonemus latus (Banks) broad mite Hexapoda Orthoptera Acrididae Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury Scudderia furcata (Brunner von Wattenwyl) North America leaves, fruit peel Microcentrum retinerve (Burmeister) angularwinged (lesser angle-wing) katydid eastern U.S. leaves, fruit peel M. rhombifolium (Saussure) broadwinged (greater angle-wing) katydid North America leaves, fruit peel Hapithus agitator (Uhler) restless bush cricket eastern U.S. leaves, small fruit Orocharis luteolira (Walker) false jumping bush cricket southeastern U.S. leaves, small fruit Reticulitermes flavipes (Kollar) eastern subterranean termite eastern North America roots, tree bark R. hesperus (Banks) western subterranean termite western North America roots, tree bark Heterotermes aureus (Snyder) desert subterranean termite southwestern U.S., Mexico roots, tree bark Paraneotermes simplicicornis (Banks) desert dampwood termite southwestern U.S. roots, tree bark Kalotermes minor (Hagen) common drywood termite southwestern U.S., Mexico roots, tree bark southwestern U.S., Mexico roots, tree bark western North America tree bark Leptoglossus gonagra (F.) citron bug western hemisphere fruit L. phyllopus (L.) leaffooted bug North America fruit L. zonatus (Dal.) western leaffooted bug North America fruit Tettigoniidae Gryllidae Isoptera Rhinotermitidae Kalotermitidae Termitidae Gnathamitermes perplexus (Banks) desert termite Termopsidae Zootermopsis angusticollis (Hagen) common dampwood termite Hemiptera Coreidae Lygaeidae Nysius ericae (Schillling) false chinch bug North America, Europe young stems C 881 882 C Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury N. raphanus (Howard) false chinch bug North America young stems world young stems and fruit Homalodisca coagulata (Say) glassy-winged sharpshooter U.S., French Polynesia green stems Empoasca fabae (Harris) potato leafhopper world fruit world twigs Asia, South America, Florida young leaves Asia, western hemisphere, world leaves Pentatomidae Nezara viridula (L.) southern green stink bug Cicadellidae Flatidae Metcalfa prunivora (Say) flatid planthopper Psyllidae Diaphorina citri (Kuwayama) Asiatic citrus psyllid Aleyrodidae Aleurocanthus woglumi (Ashby) citrus blackfly Dialeurodes citri (Ashmead) citrus whitefly D. citrifolii (Morgan) cloudywinged whitefly leaves Asia, western hemisphere, world Aleurothrixus floccosus (Maskell) woolly whitefly leaves leaves Parabemisia myricae (Kuwana) bayberry whitefly Asia, Israel, Venezuela, Califor- leaves nia, Florida Siphoninus phillyreae (Haliday) ash whitefly world, Arizona, California, Nevada leaves Toxoptera citricida (Kirkaldy) brown citrus aphid world (not Mediterranean), Florida leaves T. aurantii (Boyer de Fonscolombe) black citrus aphid world leaves Aphis spiraecola (Patch) spirea aphid world leaves A. gossypii (Glover) melon or cotton aphid world leaves A. craccivora (Koch) cowpea aphid world leaves world leaves, twigs, branches Aphididae Margarodidae Icerya purchasi (Maskell) cottonycushion scale Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury Coccus hesperidum (L.) brown soft scale world twigs, leaves C. pseudomagnoliarum (Kuwana) citricola scale world, California leaves, twigs Saissetia neglecta (De Lotto) Caribbean black scale world, Florida leaves, twigs, fruit S. miranda (Cockerell & Parrott) Mexican black scale world leaves, twigs S. oleae (Olivier) black scale world leaves, twigs Parasaissetia coffeae (Walker) hemispherical scale world leaves, twigs P. nigra (Nietner) nigra scale world leaves, twigs Ceroplastes floridensis (Comstock) Florida wax scale world leaves, twigs C. cirripediformis (Comstock) barnacle scale western hemisphere leaves, twigs Aonidiella aurantii (Maskell) California red scale world leaves, fruit, branches A. citrina (Coquillett) yellow scale world leaves, fruit Parlatoria ziziphi (Lucas) black parlatoria scale world leaves, twigs, fruit P. pergandii (Comstock) chaff scale world leaves, fruit, branches Cornuaspis (=Lepidosaphes) beckii (Newman) Purple scale world leaves, fruit, branches Lepidosaphes gloveri (Packard) glover scale world leaves, fruit, branches Unaspis citri (Comstock) citrus snow scale world branches, leaves, fruit Chrysomphalus aonidum (L.) Florida red scale world leaves, green twigs, Pinnaspis aspidistrae (Signoret) fern scale world leaves, fruit Planococcus citri (Risso) citrus mealybug world fruit, leaves, twigs Pseudococcus calceolariae (Maskell) citrophilus mealybug world fruit, leaves, twigs P. comstocki (Kuwana) Comstock mealybug world fruit, leaves, twigs P. longispinus (Targioni-Tozzetti) longtailed mealybug world fruit, leaves, twigs Maconellicoccus hirsutus (Green) pink hibiscus mealybug Africa, Asia, Australia, Caribbean, Florida fruit, leaves, twigs Coccidae Diaspididae Pseudococcidae C 883 884 C Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury Frankliniella bispinosa (Morgan) flower thrips southeastern U.S. flowers F. kelliae (Sakimura) flower thrips southeastern U.S. flowers Scirtothrips citri (Moulton) citrus thrips California, Arizona flowers S. auranti (Faure) citrus thrips southern Africa flowers S. dorsalis (Hood) citrus thrips Japan, Africa, Florida flowers S. perseae (Nakahara) avocado thrips California flowers Heliothrips haemorrhoidalis (Bouché) greenhouse thrips world leaves, fruit Chaetanaphothrips orchidii (Moulton) orchid thrips tropics, Florida leaves, fruit Danothrips trifasciatus (Sakimura) orchid thrips tropics, Florida leaves, fruit Diaprepes abbreviatus (L.) diaprepes root weevil Caribbean, Florida roots, leaves Pachnaeus litus (Germar) southern bluegreen citrus root weevil Caribbean, Florida leaves, roots, fruit P. opalus (Oliver) northern blue-green citrus root weevil Caribbean, Florida leaves, roots, fruit Artipus floridanus (Horn) little leaf notcher Caribbean, Florida leaves, roots Asynonychus godmani (Crotch) Fuller rose beetle world buds, leaves, roots Florida, Caribbean, South America flowers Anastrepha suspensa (Loew) Caribbean fruit fly Florida, Caribbean fruit A. ludens (Loew) Mexican fruit fly southwestern U.S., Mexico to South America fruit A. obliqua (Macquart) West Indian fruit fly Caribbean, Texas, Central and South America fruit A. fraterculus (Wiedemann) South American fruit fly Texas south to Chile and Argentina fruit Thysanoptera Thripidae Coleoptera Curculionidae Diptera Cecidomyiidae Prodiplosis longifila (Gagné) citrus gall midge Tephritidae Citrus Pests and their Management C Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury A. serpentina (Wiedemann) sapote fruit fly Texas south to Argentina fruit Bactrocera correcta (Bezzi) guava fruit fly southern Asia fruit B. dorsalis (Hendel) oriental fruit fly Asia and the Pacific fruit B. tryoni (Froggatt) Queensland fruit fly Australia fruit B. tsuneonis (Miyake) Japanese orange fly eastern Asia fruit Ceratitis capitata (Wiedemann) Mediterranean fruit fly world fruit C. rosa (Karsch) Natal fruit fly throughout Africa fruit Phyllocnistis citrella (Stainton) citrus leafminer world leaves Marmara gulosa (Guillen & Davis) citrus peelminer California, Mexico fruit Archips argyrospilus (Walker) fruittree leafroller North America fruit, leaves Argyrotaenia citrana (Fernald) orange tortrix North America, Europe fruit, leaves North America leaves, nuisance Papilio cresphontes (Cramer) orangedog western hemisphere leaves P. zelicaon (Lucas) California orangedog western North America leaves Atta texana (Buckley) Texas leafcutting ant western hemisphere leaves Solenopsis invicta (Buren) red imported fire ant western hemisphere twigs, bark S. geminata (F.) fire ant western hemisphere twigs, bark S. xyloni (McCook) southern fire ant southern U.S. twigs, bark Linepithema humile (Mayr) Argentine ant western hemisphere leaves (interferes with biological control) Lepidoptera Gracillariidae Tortricidae Megalopygidae Megalopyge opercularis (J. E. Smith) puss caterpillar Papilionidae Hymenoptera Formicidae Formica aerata (Francouer) native gray ant western U.S. leaves (interferes with biological control) 885 886 C Citrus Pests and their Management Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and site of injury (Continued) Taxa scientific/Common name Geographic area Site of injury world fruit, leaves, bark Gastropoda Pulmonata Helicidae Helix aspersa (Müller) Texas citrus mite, Eutetranychus banksi (McGregor), occurs throughout the Western hemisphere. It has been a pest in Texas citrus for many years, but was first detected on citrus in Florida in 1951. Since 1955 it has increased in abundance to where it is the dominant spider mite species. Adults are tan to brownish-green with dark green to black spots on the sides. Unlike citrus red mites, Texas citrus mites have short, stout setae on their upper surface. This species is abundant during periods of prolonged dry weather. They feed on upper leaf surfaces, rarely on the fruit and never on twigs, and their injury is similar to that of citrus red mites. Sixspotted spider mite, Eotetranychus sexmaculatus (Riley), was first mentioned as a sporadic pest in Florida in 1886 and continues as a spring season pest particularly on grapefruit and orange. In California, these mites occur in coastal growing areas. Adults are pale yellow to green with one to three pairs of dark spots on the upper surface which can sometimes be indistinct or missing. Sixspotted spider mites differ from citrus red mites and Texas citrus mites in that they feed on the lower leaf surface. They initially infest the petiole and midvein area, causing a slight depression. At higher densities, raised yellow areas develop on the upper leaf surface opposite that of the established lower leaf surface colonies, and severe defoliation can follow. Two other Eotetranychus species, Lewis spider mite, E. lewisi (McGregor), and Yuma spider mite, E. yumensis (McGregor), occur on grapefruit and lemon in California and Arizona. Lewis spider mite was found on navel oranges in southern California in 1942 and continues to be a pest in the southern citrus districts except in desert areas. Adults are various shades of pale amber or green with black spots along the lateral margin. Lewis spider mite generally damages fruit. Yuma spider mite is distributed in the Coachella and Imperial valleys of California and the Yuma citrus district of Arizona. Adults are light straw to dark pink and are most numerous in winter and late spring. These mites feed on leaves, fruit and green twigs. Twospotted spider mite, Tetranychus urticae Koch, is a serious pest of many crops but is only an occasional pest of citrus, particularly in the San Joaquin Valley of California. It first appears on the underside of the leaves, but as populations increase, can be found infesting the upper leaf surface and fruit. Conspicuous webbing similar to that of Eotetranychus species can occur in areas of heavy infestation. As with all spider mites, damage potential of T. urticae varies from citrus species to citrus species, from year to year, and is related to weather conditions such as heat and to water stress. Several other Tetranychus species rarely attack citrus in the U.S. Pacific spider mite, T. pacificus McGregor, is more of a pest of deciduous tree fruits, but has caused damage in the central valleys of California. Tumid spider mite, T. tumidus Banks, is present in the southeastern U.S. and T. mexicanus (McGregor) is occasionally a pest of citrus in Texas. Worldwide, other members of Tetranychidae are citrus pests. This list includes four Eutetranychus species: oriental red mite, E. orientalis (Klein), occurring in the Mideast and Asia, and three African species, lowveld citrus mite, E. anneckei Meyer, E. africanus Klein, and E. sudanicus Elb., Eotetranychus cendanci Rimando from southeast Asia, and Schizotetranychus hindustanicus (Hirst) from southern India. Citrus Pests and their Management C Citrus Pests and their Management, Figure 58 Some common insect and mite pests of citrus. Top left, scanning electron micrograph of citrus rust mite (photo, J. C. Allen); top right, feeding injury (dark areas where surface temperatures did not inhibit mite feeding) by citrus rust mite (photo, J. C. Allen); second row left, sixspotted spider mites (photo, J. Knapp); second row right, Texas citrus mite (photo, J. Knapp); third row left, Diaprepes (citrus root) weevil (photo, J. L. Capinera); third row right, blue-green citrus weevil (photo, P. M. Choate); bottom left, southern green stink bug (photo, J. L. Capinera); bottom right, brown soft scale (photo, L. J. Buss). 887 888 C Citrus Pests and their Management Citrus Pests and their Management, Figure 59 Some common insect and mite pests of citrus. Top left, Florida red scale (photo, J. L. Castner); top right, cottony cushion scale adults (on stem) and immatures (on leaf) (photo, L. J. Buss); second row left, citrus mealybug (photo, J. Knapp); second row right, adult citrus blackflies (photo, J. Knapp); third row left, immature citrus blackflies (photo, J. Knapp); third row right, citrus whitefly (photo, J. Knapp); bottom left, brown citrus aphid (photo, P. M. Choate); bottom right, spirea aphid (photo, J. L. Capinera). Citrus Pests and their Management C Citrus Pests and their Management, Figure 60 Some common insect and mite pests of citrus. Top left, giant swallowtail, adult form of orange dog (photo, J. L. Castner); top right, orange dog, larval form of giant swallowtail (photo, J. Knapp); second row left, adult citrus leaf miner (photo, J. L. Castner); second row right, leaf mines caused by citrus leaf miner larvae (photo, J. L. Castner); third row left, Asian cockroach (photo, J. L. Castner); third row right, eastern lubber grasshopper (photo, J. L. Capinera); bottom left, American grasshopper (photo, J. L. Capinera); bottom right, Mediterranean fruit fly (photo, J. Knapp). 889 890 C Citrus Pests and their Management Tenuipalpidae Orthoptera Four species of false spider mites in the genus Brevipalpus attack citrus in the United States. Three of these, phoenicis (Geijskes), obovatus Donnadieu, and californicus (Banks), are cosmopolitan and occur on citrus in most parts of the world. Infestations usually begin in the interior of the tree canopy on the underside of leaves near the midrib, but false spider mites are also found on fruit and woody tissue (twigs and branches). Brevipalpus mites are flat, reddish, and difficult to notice because they are small and slow moving. They have a relatively long life cycle compared with other phytophagous mites. Brevipalpus mites are economically important because they vector a bacilliform virus that causes leprosis. This disease can be found on fruit, leaves, and tree branches, and is commonly referred to as nailhead rust. The fourth species, B. lewisi McGregor, is found in the desert and interior valleys of California’s citrus growing region. It is a secondary invader that feeds on rind tissue damaged by other insects. B. phoenicis mites have gained fame lately when it was discovered that they only exist in the haploid state (one copy of chromosomes). Several species of grasshopper, katydid, and cricket cause minor damage to citrus due to feeding with their chewing mouthparts. These species rarely warrant control actions, but when they do foliar insecticides are employed. Tarsonemidae Broad mite, Polyphagotarsonemus latus (Banks), is a very important pest of “Tahiti” lime in Florida and an infrequent pest of coastal lemons in California. They are distributed across the world and feed on many horticultural plants. Adult females are light yellow, amber, or green with an indistinct white median stripe on the back, and males are similar in color but without the stripe. Broad mites are found on newly formed leaves or on young fruit. Heavy infestations on leaves cause distortion, curling, or stunting, but the most important damage is russeting on young fruit. Fruit that are severely russeted are not available for the fresh market and must be used for processing. Natural enemies include several predatory mite species. Acrididae Two grasshopper species, eastern lubber grasshopper, Romalea guttata (Houttuyn), and American grasshopper, Schistocerca americana (Drury), are sporadic pests in citrus groves. Lubber grasshopper adults are yellow with red and black markings and American grasshoppers are light brown with black markings. Injury is caused by nearly full grown nymphs which feed on foliage and occasionally fruit and the most serious damage occurs when young citrus trees are defoliated. Tettigoniidae Three species of katydid attack citrus. In Florida, only broadwinged katydid, Microcentrum rhombifolium (Saussure), causes economic damage. In California, forktailed katydid, Scudderia furcata Brunner von Wattenwyl, is the species that causes damage, although angularwinged katydid, M. retinerve (Burmeister), is also present. Katydid feeding resembles that of grasshoppers and is mostly restricted to foliage. When fruit rinds are attacked, large, smooth, sunken areas on the fruit surface result. Gryllidae Two species of bush cricket, restless bush cricket, Hapithus agitator Uhler, and false jumping bush cricket, Orocharis luteolira Walker, may be present in large numbers in Florida citrus groves. Both species feed on small fruit, leaves, and twigs in the Citrus Pests and their Management lower canopy. Fruit drop and peel blemishes may result in economic damage. Isoptera C cover of groves, protection of predators and parasitoids, application of horticultural oils, and foliar insecticide applications. Coreidae Rhinotermitidae The only termite species in Florida that attacks citrus is eastern subterranean termite, Reticulitermes flavipes (Kollar). Attack starts below ground where they feed on bark and cambium of young trees. They can become serious pests of citrus in groves where nearby pine woods support large populations. Two other species, desert subterranean termite, Heterotermes aureus (Snyder), and western subterranean termite, R. hesperus Banks, have damaged citrus in California. Kalotermitidae Desert dampwood termite, Paraneotermes simplicicornis (Banks), has damaged grapefruit trees in the Coachella Valley of California by feeding on the taproot and lateral roots. This species has also damaged young trees in Texas. Common drywood termite, Kalotermes minor Hagen, has damaged citrus in California by feeding either below ground or above ground by gaining entry through wounds or crevices. Two other termite species, desert termite, Gnathamitermes perplexus (Banks) (Termitidae), and common dampwood termite, Zootermopsis angusticollis (Hagen) (Termopsidae), occasionally damage citrus in California. Citron bug, Leptoglossus gonagra F., leaffooted bug, L. phyllopus (L.), and western leaffooted bug, L. zonatus (Dal.), are three plant bug species that puncture the fruit rind and suck the juices from underlying vesicles. Citron bug (Figs. 58–60) is dark brown to black with the front margin of the thorax yellow. Populations build on nearby melons and weeds in the grove during spring and summer, and injury to citrus usually occurs by fall. Leaffooted bug occurs in Arizona, the Gulf states, and Florida, where its principle host plants are thistles (Cirsium spp.). It is dark brown with a pale yellow line across the wings. Damage by plant bug feeding can cause fruit drop and also may provide access for various pathogens. Damage is more common on citrus fruit with thinner rinds. Western leaffooted bug is primarily a pest of pomegranates in California, although they will occasionally attack tangerines, oranges, and grapefruit. Lygaeidae Two false chinch bug species, Nysius ericae (Schil.) and N. raphanus Howard, occasionally are very destructive to young trees in California. Adults are small and light to dark gray. Nymphs and adults sometimes congregate in large numbers on younger wood. Hemiptera Pentatomidae At least 12 families have been documented to occasionally cause economic damage on citrus, and some of the most important pests are found in this group. All Hemiptera have piercing-sucking mouthparts, and are usually controlled by improved management of plants in the ground Southern green stink bug, Nezara viridula (L.), is green and is abundant in the fall and early winter. Although other species of stink bugs attack citrus, this species is usually the only one found in high numbers. Most stink bugs breed on a variety of 891 892 C Citrus Pests and their Management weed plants. In Florida, this insect is most destructive to tangerines. Cicadellidae Glassy-winged sharpshooter, Homalodisca coagulata (Say), is native to the southeastern United States, but recently has invaded California. Specimens from a citrus grove in Ventura County were identified in 1989. This large leafhopper is dark brown to black with yellowish spots on its head and back. Glassy-winged sharpshooters vector the bacterium Xylella fastidiosa which causes many plant diseases. Infections affect the xylem of the plant and is known as Pierce’s disease (grape), almond leaf scorch, phony peach disease, alfalfa dwarf, and oleander leaf scorch. Citrus variegated chlorosis, a serious disease of oranges in South America vectored by H. coagulata, is not currently present in the U.S. In California, the major concern is transmission of Pierce’s disease in vineyards. Although the disease has been present in California for many years, glassy-winged sharpshooter is a more efficient vector than the native sharpshooters because of higher mobility and the ability to occupy a wide range of new habitats and host plants. Potato leafhopper, Empoasca fabae (Harris), is a common insect that attacks over 100 crop plants throughout the U.S. It is an occasional pest of citrus in California, especially in groves near tomato or cotton fields in the San Joaquin Valley. Adults are small, greenish, and very active insects. Potato leafhopper feeds on fruit by puncturing rind cells, causing yellowish to light brown scars. Flatidae One flatid planthopper species, Metcalfa prunivora (Say), is an occasional pest of citrus in Texas. It is grayish-white and feeds on twigs. This insect only completes one generation per season. Grapefruit trees appear to be favored over orange trees. Psyllidae Asiatic citrus psyllid, Diaphorina citri Kuwayama, was found in southeastern Florida in 1998 and in southern Texas in 2001. Its native range includes much of southern Asia, although it has been found in Brazil and Honduras. African citrus psyllid, Trioza erytreae (Del Guercio), is the only other psyllid worldwide that is an economic pest of citrus. D. citri is a small active insect with a brown, mottled appearance and is found on the lower sides of new flush leaves. Damage caused by this insect is either direct feeding injury resulting from the withdrawal of fluids from the foliage, development of sooty mold on leaves, and/or transmission of organisms that cause citrus greening disease, though this disease is not yet known from American populations. Greening symptoms include mottling and yellowing of leaf veins, irregular leaf and flower production, abnormal fruit drop, and an unpleasant flavor in the juice. Asiatic citrus psyllid management in Florida is being conducted using classical biological control, wherein parasitoids from Asia are collected and released. Aleyrodidae There are eight whitefly species that are considered citrus pests. Whitefly nymphs extract phloem sap from leaf tissues causing leaves to wilt and drop if there are large populations. Feeding on such a sugary liquid diet means that the waste product, honeydew, is also a very sugary liquid substance. The creation of honeydew provides a food source for sooty mold fungus which “blackens” the leaves and interferes with the tree’s ability to make food through photosynthesis. Honeydew also attracts ants, which sometimes interfere with biological control. The combined effects of feeding by nymphs and associated sooty mold can result in death of young trees and serious fruit yield reductions for producing trees. Fruit that has sooty mold on it ripens later than normal fruit and is also discolored. Many of these whitefly species that attack Citrus Pests and their Management citrus are also pests of horticultural crops in greenhouses in northern states. Citrus blackfly, Aleurocanthus woglumi Ashby, is of Asian origin that was first detected in the Western Hemisphere in Jamaica in 1913 and then in Key West, Florida, in 1935. It was rediscovered in Ft. Lauderdale, Florida, in 1976 and spread to neighboring citrus-producing counties. It first invaded the lower Rio Grande Valley of Texas in 1955 on residential citrus, and again in Brownsville in 1971 in both residential and commercial groves. Adults are slate-blue with a median white band; the abdomen and head are bright red. Females lay eggs on the underside of leaves in a characteristic spiral pattern. This insect has over 300 host plants, but citrus is one of its favorites. There is a very successful history of both classical and augmentative biological control of citrus blackfly through release of two parasitic wasps in many areas of the Western Hemisphere including Mexico, Florida, and Texas. Citrus whitefly, Dialeurodes citri (Ashmead), and cloudywinged whitefly, D. citrifolii (Morgan), are two other Asian pests that invaded Florida in the late 1800s. In the 1920s, whiteflies were considered the most serious pests of citrus in Florida. They can still be a serious pest, although not at the same level that they once were. Both species are found in Texas citrus, and citrus whitefly also is found in California. Both citrus and cloudywinged whitefly adults are small and white, although cloudywinged adults have a darkened area at the end of each wing. Many natural enemies are used in biological control of both whitefly species, including fungi, predators, and parasitoids. Woolly whitefly, Aleurothrixus floccosus (Maskell), was first found in Florida in the early 1900s and also is found in Texas and California. Adults are yellowish-white and seldom fly. The last nymphal stage (pupa) is surrounded by waxy filaments. Adult females lay eggs in a circle on mature leaves. Like other whiteflies on citrus, they are mostly controlled by natural enemies. Barberry whitefly, Parabemisia myricae (Kuwana), is an Asian species first discovered in C California in 1978 and Florida in 1984. Like other whiteflies, they have several hosts other than citrus. Adults are small, whitish-yellow insects. Females prefer to lay eggs on young, tender foliage. Several natural enemies attack barberry whitefly, and the first populations found in Florida were already under natural biological control, apparently because the parasitoids were introduced with the whitefly. Ash whitefly, Siphoninus phillyreae (Haliday), is a species from temperate and subtropical regions of Europe, northern Asia and north Africa. It was first collected in southern California in 1988, and is now present in Arizona and Nevada. It has arboreal hosts, including several fruit trees, and in Europe this pest causes severe damage to pear and apple. Adults are small, whitish insects with a light dusting of wax. Natural enemies from Israel and Italy were imported to California for biological control. Aphididae Aphids comprise a large and diverse group of small, fragile insects that are economically important because of direct damage and transmission of plant diseases. Many species are winged (alate) and wingless (apterae), depending on the season. Their biologies are complex because a species may contain both sexual and parthenogenetic (able to reproduce without fertilization by males) forms at different times of the season or on different host plants. Brown citrus aphid, Toxoptera citricida (Kirkaldy), is one of the world’s most serious pests of citrus. It is found in southeast Asia, southern Africa, Australia and New Zealand, South America, the Caribbean, and since November 1995, in Florida. These aphids are larger than other species on citrus and have slender antennae. Wingless adults are shiny black, while nymphs are dark reddish-brown and reproduce parthenogenetically by producing nymphs, thus, there are no males and no eggs. They damage citrus by producing copious amounts of honeydew so that leaves and fruit become black 893 894 C Citrus Pests and their Management with sooty mold. However, their most serious damage to trees is by vectoring a phloem-limited virus called citrus tristeza closterovirus. This virus causes tristeza stem pitting disease. One of the most devastating citrus crop losses ever reported followed the introduction of this aphid into Brazil and Argentina, where 16 million trees on sour orange rootstock were killed. Several different management measures are being studied in Florida, including cultural control through rootstock improvement, biological control, and chemical control. Black citrus aphid, Toxoptera aurantii (Boyer de Fonscolombe), is a related species and is found throughout the world where citrus is grown. It is found in all citrus areas of the U.S. It is smaller than brown citrus aphid, with the adult apterae dull black. The antennae and legs appear to be striped. Black citrus aphid is not a serious pest of citrus and is either a poor or nonvector of citrus tristeza. Spirea aphid, Aphis spiraecola Patch (formerly known as A. citricola Van der Goot), is a small green aphid that originated in eastern Asia. It was found in Florida and California in the 1920s, and now is present in Texas. Aphids attack new growth leaves, causing them to curl or roll, and cause damage by retarding the growth of young trees, reducing fruit set, and production of sooty mold. Winged forms develop when the aphid colony becomes crowded or when leaves mature. Spirea aphid reproduces parthenogenetically throughout the season, and may spend the summer on alternate (non-citrus) host plants. Melon or cotton aphid, Aphis gossypii Glover, is a cosmopolitan pest that feeds upon and injures many horticultural and agronomic crops. It is about the same size as spirea aphid, but on citrus is generally dark gray or dull black. It infests citrus during the spring flush of growth. Melon aphid can transmit citrus tristeza virus, but apparently is not an efficient vector. Several other aphid species occasionally are found on citrus in Florida, including cowpea aphid, Aphis craccivora Koch, oleander aphid, A. nerii (Boyer de Fonscolombe), potato aphid, Macrosiphum euphorbiae (Thomas), and green peach aphid, Myzus persicae (Sulzer). Margarodidae Only one member of this family is a pest on citrus. Cottony cushion scale, Icerya purchasi Maskell, is a large scale insect originally from Australia but that has now dispersed throughout the world wherever citrus is grown. It was first discovered in California in 1868 and by the late 1880s was severely damaging citrus in the southern part of the state. A coccinellid predator from Australia, vedalia beetle [Rodolia cardinalis (Mulsant)], was imported to the Los Angeles area and released in 1888–1889. The beetle multiplied quickly and the cottony cushion scale was brought under control. This was the first successful use of a classical biological control agent in the U.S. Cottony cushion scale was accidentally sent to Florida in a shipment of vedalia beetles in 1893. Vedalia beetle provides effective control nearly everywhere. Mature female scales have bright orange-red, yellow, or brown bodies that are partially covered by wax. The body is also covered by a large, fluted egg sac filled with red eggs. Females are actually hermaphrodites, having the sex organs of both males and females. Males are rare and are winged. When females self-fertilize, only hermaphrodites are produced, whereas if a hermaphrodite mates with a male, more males and hermaphrodites are produced. Cottony cushion scales congregate along the midrib of leaves and on trees. They damage citrus by decreasing tree vitality, increasing fruit drop and defoliation. Coccidae Unarmored or soft scales are represented by several species on citrus. They have no protective covering like armored scales but do secrete a wax-like substance which protects them. Female soft scales do not have wings, but are mobile until eggs start to form. Adult males usually have one pair of wings, and don’t Citrus Pests and their Management live very long. Young scales are called crawlers, and they either hatch from eggs or are born alive. Later stages produce large amounts of honeydew upon which sooty mold fungus grows and, along with armored scales, are among the most serious pests of citrus in the world. Many parasitoid species attack and control soft scales, but ants will protect scale populations from their natural enemies. Two species of Coccus are citrus pests. Brown soft scale, Coccus hesperidum L., has a worldwide distribution on a variety of plants. In Florida, it is not a pest of concern, but is the most serious soft scale pest in Texas. The scale body is flat and oval, light brown to yellowish. Females give birth to pale yellow crawlers. Brown soft scale is a more serious problem on young trees due to feeding and honeydew production. Mature trees suffer from reduced vigor, twig dieback, and reduced fruit yields. There are several parasitic wasps that attack brown soft scale. Citricola scale, C. pseudomagnoliarum (Kuwana), is found in California. It is more of a serious pest in the San Joaquin Valley than other citrus districts. Young citricola scale are very flat and more transparent looking than young brown soft scale, while mature citricola scales are gray. Crawlers appear in late April and settle on the underside of leaves. By November, they migrate to twigs, where their development speeds up. By the next spring, mature female scales lay eggs which hatch into crawlers. Damage to citrus is similar to that of brown soft scale. Three species of black scale, Saissetia, are citrus pests. Caribbean black scale, S. neglecta De Lotto, is a pest in Florida. Adult females are brown to black and have a tough circular or hemispherical shell. Two lateral ridges and one longitudinal ridge create an “H” shaped pattern. Crawlers move from leaves to small twigs and fruit stems. Females lay eggs and usually reproduce without fertilization by males (parthenogenesis). Mexican black scale, S. miranda (Cockerell & Parrott), is found in the southern U.S. and Mexico on a wide variety of plants. It is seldom found in Florida. Black scale, S. oleae (Olivier), a pest of olive trees and oleander, C is found in the southern citrus districts of California and in Florida. This scale’s appearance is similar to that of other black scales. Excreted honeydew supports growth of sooty mold and feeding reduces tree vigor and causes leaf and fruit drop. Four other species of soft scales are occasional pests in the U.S. Hemispherical scale, Parasaissetia coffeae (Walker), is widely distributed across the world and is found in the coastal sections of southern California. Nigra scale, P. nigra (Nietner), is a tropical species that is found rarely in California. Florida wax scale, Ceroplastes floridensis Comstock, is an important pest of citrus in the Mideast and Asia, and is occasionally a problem in Florida. Adults are highly convex, somewhat angular, and oval. Males have not been reported. Barnacle scale, C. cirripediformis (Comstock), is an occasional pest of citrus in California, Texas, Florida, and Mexico. The thick wax coat is dirty white and is divided into distinct plates, one on top and six on the side. Diaspididae Armored scales are represented by several species on citrus. Females and immature males are covered by coatings of wax and cast skins (exuviae) of earlier instars. As crawlers, females insert their mouthparts into the plant and never move again. They will lay either eggs or live young under the armor (cover), depending on species. Armored scales injure citrus by feeding, not by production of honeydew and resulting sooty mold. The level of damage varies greatly among armored scale species. California red scale, Aonidiella aurantii (Maskell), and yellow scale, A. citrina (Coquillett), are two armored scales that are major pests in the citrusgrowing districts of California. California red scale is found also in Texas, while yellow scale is found in Florida. Adult females have circular covers. Immature male covers are more elongated, and adults are small, two-winged insects that live for only a few hours. Females give birth to live young (crawlers), which search for locations to settle. California red scale infest all parts of the tree, including leaves, twigs, 895 896 C Citrus Pests and their Management branches, and fruit. Yellow scale is found rarely on twigs and branches. Plant tissue is injured as a result of plant fluid removal and injection of toxic substances. Damage is caused by leaf yellowing, leaf drop, and fruit drop, and serious damage to trees occurs when twigs and branches are killed. Biological control is an important management tactic used against these scales, with Aphytis and Comperiella parasitoids mass reared and released. Black parlatoria or ebony scale, Parlatoria ziziphi (Lucas), was discovered infesting citrus in southern Florida in 1985. It is considered a major pest in countries bordering the Mediterranean, tropical Asia, parts of South America, and the Caribbean. The female covering is black, rectangular, and with a fluted surface while the male covering is white, except at one end, flat, and elongate. The armor is almost impossible to remove from host tissues. Scales infest leaves, twigs, and fruit, and because they adhere so strongly, cause rejection of fresh fruit in markets. Large populations cause chlorosis and early drop of leaves, dieback of twigs and branches, and distortion of fruit. Chaff scale, Parlatoria pergandii Comstock, has a similar distribution as black parlatoria scale, except that it is also found in the Gulf states. This is the most common armored scale in Texas. The scale covering is circular to elongated, thin, and brown to gray. The female body, eggs and crawlers are purplish. Chaff scales often are found in depressions on fruit or along midribs on leaves, and are also found on tree bark. When fruit mature, areas around the scale remain green, rendering the fruit unsuitable for the fresh market. Purple scale, Cornuaspis (=Lepidosaphes) beckii (Newman), was the most common and damaging armored scale in Florida prior to 1960 and the introduction of a parasitoid (Aphytis lepidosaphes Compere). It is found in Texas and in more humid areas of California. Adult females are curved and oyster-shaped (broad and tapering), with a purplish-brown cover and a white scale body color. Immature male covers are shorter and more slender than those of the female. Adult males are small winged insects. Females lays eggs under her scale cover. Purple scales prefer trees with a dense canopy and infest leaves, wood, and fruit. On leaves, they cause yellow chlorotic spots which lead to defoliation. Fruit quality is affected because fruit infested with scales do not change color. Glover scale, Lepidosaphes gloveri (Packard), also known as “long” scale, is found in association with purple scale. It is found in Florida, Texas, and limited areas in California. Adult female covers are long and narrow, purplish-brown, with white to purple colored scale bodies. They infest leaves, twigs, bark, and fruit, and when on woody bark, orient with the grain of the bark. Parasitic wasps generally keep this species under biological control. Citrus snow scale, Unaspis citri (Comstock), was known to infest citrus since 1880, but became an important pest in Florida in the early 1960s. Replacement of trees after a severe freeze in 1962 brought thousands of infested nursery stock to groves. Female covers are oyster-shaped with a longitudinal ridge, and are purplish-brown with a gray border. Immature male covers are white with a center ridge and fainter ridges on either side. Adult males are winged and yellowish. Although they infest all parts of a tree, citrus snow scales primarily attack the trunk and large branches. Declining tree vigor and lower fruit production result from high populations. Florida red scale, Chrysomphalus aonidum (L.), affects citrus in Florida and Texas, but is seldom found in groves in California. It was introduced into Florida from Cuba in 1874 and was a major pest until release of the parasitoid Aphytis holoxanthus DeBach in 1960. In Texas, California red scale and Florida red scale can be misidentified. Florida red scale female covers are more circular, are dark reddish-brown, and have a conspicuous light brown nipple. The female’s body is yellow, and the female’s cover is more easily removed than those of California red scale. Adult males are winged insects that fertilize adult females. Females lay eggs which hatch into very active, bright yellow crawlers. Unlike other Citrus Pests and their Management armored scales, Florida red scales attack only leaves and fruit. On leaves, they cause yellow chlorotic spots which lead to defoliation. They also cause yellow spots on fruit which render it unmarketable as fresh fruit. Fern scale, Pinnaspis aspidistrae (Signoret), is found in Florida, South America, and Japan. Female scale covers are pale brown, flat, and pear-shaped. Immature males are white and elongated, resembling male citrus snow scale. They are found only on leaves and fruit. They have a wide host range and never cause economic damage to citrus. Pseudococcidae Mealybugs are soft, oval, flat, distinctly segmented insects covered with a white, mealy wax that extends into spines (filaments) along the body margin and the posterior end. Unlike scales, mealybugs remain motile throughout their life cycle. Species differ in external appearance by the waxy covering and the thickness and length of filaments. Mealybugs injure plants by extracting sap from trees and secreting large amounts of honeydew, which serves as a food source for sooty mold. Feeding on foliage and twigs reduces the vigor of trees and may result in defoliation. Feeding on fruit results in distortions and scars which lower the grade of the produce. Citrus mealybug, Planococcus citri (Risso), occurs in Florida, Texas, and in the coastal citrus districts in California. They have pinkish bodies that are visible under the powdery wax. Adult males are winged insects. Eggs are laid in a white cottony mass, and nymphs are light yellow. Citrus mealybugs prefer protected areas such as the calyx of fruit or along the stem. Feeding along the stem usually results in fruit drop. There are several natural enemies including pathogens, parasitoids, and the ladybird beetle, Cryptolaemus montrouzieri (Mulsant). This predator was imported from Australia to California in 1891. Three species of Pseudococcus are citrus pests. Comstock mealybug, P. comstocki (Kuwana), a C native of Asia, is primarily a pest on lemons in the San Joaquin Valley of California. It differs from citrus mealybug by having a thicker wax cover and two spines at the posterior end. The citrophilus mealybug, P. calceolariae (Maskell), and longtailed mealybug, P. longispinus (Targioni-Tozzetti), are present in California. Longtailed mealybugs differ from other species because young are born as active nymphs. They are usually not a problem on citrus because of the work of natural enemies. An exotic species, pink hibiscus mealybug, Maconellicoccus hirsutus (Green), is a serious pest of citrus and other plants in Africa (Egypt), southeast Asia and northern Australia. It was found in the Caribbean in 1994, in southern California in August 1999, and just recently in Florida in June 2002. It has a high reproductive rate and infests many horticultural, ornamental, and agronomic crops. This mealybug feeds on soft tissues of plants and injects a toxin which causes leaf curling and distortion. Feeding also promotes growth of sooty mold because of honeydew excretion. Thysanoptera Thrips are a group of small, elongated insects with fringed wings. Their mouthparts have been described as “rasping-sucking,” but it is likely that certain parts pierce rather than rasp leaf and flower tissue. The majority of thrips species feed on plants, but some feed on fungus and others are predaceous on small arthropods. Life cycles consist of an egg stage, two larval stages that feed, one prepupal stage that doesn’t feed, one non-feeding pupal stage, and an adult stage that feeds. Several species are pests on citrus. Thripidae Two species of flower thrips are found on citrus in Florida. Frankliniella bispinosa (Morgan) occurs throughout the state, while F. kelliae Sakimura is found in central and southern growing areas. Both 897 898 C Citrus Pests and their Management species have wide host ranges, but on citrus have been shown to injure navel and “Valencia” oranges. Flower thrips migrate aerially during the flowering cycle from January through April. They have been documented to feed, oviposit, and develop on various flower parts, such as the ovary, style, petals, anthers, pistil, and calyx. Resulting damage is by reducing fruit set. Recently a relationship between thrips feeding and the fungal pathogen Colletotrichum acutatum J. H. Simmonds was associated with post bloom fruit drop. Three Scirtothrips species are recognized as citrus pests, S. auranti Faure in South Africa, S. dorsalis Hood in Japan and Africa, and citrus thrips, S. citri (Moulton), in California and Arizona. Citrus thrips is an important pest on navel oranges in the San Joaquin Valley, on desert citrus including grapefruit and tangerine, and on lemons grown in the coastal districts. They are small, yellowish-orange, and have fringed wings. They feed on leaves, young fruit (especially under the sepals), and green twigs. Leaf injury is along the midrib or leaf margins, causing leaf deformities, and injury to fruit is by puncturing epidermal cells, leaving uniform scars. Scars in young fruit form a ring around the stem, and as the fruit grows, the ring increases and is found further from the stem. Natural enemies include several predators including mites (Eusieus tularensis Congdon). A fourth species, S. perseae Nakahara, recently was found infesting avocado in southern California. It is not known if this Central American native will attack citrus. Greenhouse thrips, Heliothrips haemorrhoidalis (Bouché), is a New World species that is also found in Europe, the Mideast and north Africa. In the U.S. it is found in central and southern Florida and southern California along the coast. Adult females are black with a reticulated body surface and yellow-white legs. Greenhouse thrips develop parthenogenetically. They injure rind tissue by feeding on epidermal cells, which may cause ring spotting or irregular russeting. Injury occurs where fruits, fruits and leaves, or fruits and twigs are in contact. In Florida economic loss to growers is restricted to red grapefruit varieties, but in California greenhouse thrips attack “Valencia” oranges, lemons, and avocados. Feeding from fruit epidermal cells removes pigment. No scars or deformities develop, but fruit may be downgraded. Two other thrips species occur in Florida citrus. Chaetanaphothrips orchidii (Moulton) females are yellow with distinctive dark banding on the wings. They are most common on grapefruit and are present throughout the year. Fruit injury resembles that of greenhouse thrips. Danothrips trifasciatus Sakimura is present in low numbers in association with C. orchidii. Coleoptera Beetles represent the largest order of insects in number of species. As might be expected, this is an extremely diverse group with species that specialize in phytophagy (plant feeding), zoophagy or carnivory (feeding on animals, usually as predators or parasitoids), fungivory (fungus-feeding), and saprophagy (feeding on dead material). However, relatively few species specialize or infest citrus. The primary family of beetles that attack citrus is Curculionidae, the weevils. Diaprepes weevil, Diaprepes abbreviatus (L.), has several other common names such as “Apopka weevil” and “sugarcane rootstalk borer weevil.” It is native to the Caribbean, and is only found in the U.S. in Florida and Texas. It was first reported in central Florida (Apopka) in 1964 and since has spread over the southern two-thirds of the state. Adults are black with white, reddish, or yellowish scales on the wing covers (elytra). This is the largest weevil species that infests citrus in Florida. Eggs are laid on new flush leaves that have been clustered or glued together by females using an adhesive material. Young larvae fall to the soil and begin feeding on roots. During the course of its development, which can last anywhere between 6 and 24 months, larvae may consume any part of the tree’s root system. Diaprepes pupate in the soil Citrus Pests and their Management and then emerge to find mates. Although adults fly, they do not disperse far from their emergence site. Adults may nibble or “notch” the margin of leaves, but important injury is caused by larval feeding. Young trees can be killed by a single larva and older trees suffer when major roots or the taproot is girdled. Feeding on roots also allows for the introduction of plant pathogens, which injure an already stressed tree. There is a considerable amount of research being conducted by federal and state entomologists in Florida in detecting, controlling, and preventing damage by this insect. Two species of blue-green citrus root weevils are found in Florida. Pachnaeus litus (Germar) is found in south-central to southern Florida; P. opalus (Oliver) is commonly found in north and north-central Florida. At least two Pachnaeus species also occur in Texas citrus groves. Adults of both species are gray-green to aqua and can be separated by structures on the wing covers. Larvae are root feeders and will attack all root parts except the crown. Adults feed by notching the leaf margins. As with other citrus root weevils, many other plant species can be used as hosts. Fuller rose beetle, Asynonychus godmani Crotch, is found in Florida, Texas and California. It was reported in Florida in 1916 and has been known as Pantomorus cervinus (Boheman) and A. cervinus (Boheman). Its distribution in Florida ranges from the southern tip to north-central areas. Adults are brownish-gray, flightless, and are all females that develop parthenogenetically. Eggs are usually laid under the calyx of the fruit. Larvae take from 9 to 12 months to develop and feed on all root parts except for the crown. Fuller rose beetle is not a serious economic pest by itself, but because eggs are laid on fruit, they are a quarantine pest when fruit is to be exported. One management tactic developed in California is the use of parasitic nematodes [Steinernema carpocapse (Weiser)] for biological control. The smallest root weevil in Florida is the little leaf notcher, Artipus floridanus Horn. This insect was reported as early as 1876 and is found mostly along the east coast. Adults are grayish-white, C flightless, and are all female. Unlike the other species discussed in this group, A. floridanus has a much shorter life cycle. Larvae can complete development in as little as 35 days. Also unlike the other species, larvae feed only on smaller root parts such as pioneer and fibrous sections. Diptera This large, diverse order contains two families that attack citrus. Gall midges (Cecidomyiidae) are infrequent pests of citrus buds and flowers. Fruit flies (Tephritidae) from the genera Anastrepha, Bactrocera, and Ceratitis attack fruits and vegetables. Females insert eggs under the skin of fruit and larvae feed within, causing direct injury and decay. Fruit fly species are also quarantine pests, where whole loads or even a season’s worth of produce may be denied entry within regions of a country or among countries because of the threat of infestation. Cecidomyiidae The citrus gall midge, Prodiplosis longifila Gagné, is a small black-yellowish fly that attacks citrus, tomatoes, potatoes, and cotton in Florida, the Caribbean, and South America. Large populations developed in 1984 on limes in southern Florida. Eggs are laid in flower buds and larvae feed on flowers, injuring several flower structures. Larvae complete development, drop to the ground, and pupate in the soil. Damage occurs when flowers are killed and drop from the tree. Tephritidae Three genera, Anastrepha, Bactrocera, and Ceratitis, contain fruit fly species that are considered serious citrus pests. Eggs are inserted under the skin of various fruits, berries, nuts, and vegetables. Larvae then mine the host, promoting decay and causing 899 900 C Citrus Pests and their Management the fruit to be unmarketable. Fruit flies are direct pests in countries where they are established, but are also regulatory or quarantine pests in countries where particular species are not established. There has been much research worldwide into detection or monitoring of adults, and management tactics other than insecticide sprays, such as bait stations, sterile insect technique (releasing sterile flies to mate with wild flies) and biological control. Species in the genus Anastrepha are New World flies that attack tropical and subtropical fruits. The Mexican fruit fly, A. ludens (Loew), is important in the United States because it is subtropical rather than tropical. It is found in southern Texas, California and Arizona, where continuous detection and eradication programs, such as sterile insect technique, are in place. It was detected in Florida in 1934 and again in 1972, but did not become established. This relatively large yellow-brown fly is native to Mexico but can be found as far south as northern South America. In Texas, grapefruit appears to be the preferred host, and several deciduous hosts such as peach, pear and apple also can be attacked. The Caribbean fruit fly, A. suspensa (Loew), is a yellow-brown fly that is native to the West Indies. This species has an interesting history in Florida. It was documented in Key West in 1931, although was believed to have been established for many years. This “strain” attacked guavas (Psidium guajava L.) and noneconomic fruits but did not infest citrus. This strain differed from populations found in Puerto Rico that did feed on citrus. The Key West populations apparently were eradicated through fruit removal and insecticide sprays and died out sometime after 1936. Since 1965, a new introduction into Florida spread from southern areas to central Florida groves. It attacks mature and overripe citrus, and its seriousness as a pest is still being investigated. Exports require an elaborate fly-free zone system that requires several million dollars a year to maintain. Even so, in some years up to 16,000 hectares (40,000 acres) of grapefruit have been lost to export markets because of fly captures within protocol areas. Three other Anastrepha species are pests in the Western Hemisphere and are potential pests in Florida if they become established. The West Indian fruit fly, A. obliqua (Macquart), is nearly identical to A. suspensa and occurs throughout the Caribbean, southern Texas, and south to Argentina. It was found in Key West in the 1930s during surveys for A. suspensa. It was also eradicated and hasn’t been found in Florida since 1935. This species has a long host list, but mangos (Mangifera indica L.) and guavas can be economically damaged. It rarely attacks citrus. The South American fruit fly, A. fraterculus (Wiedemann), is economically the most important species in South America (Brazil, Argentina, Peru), but is also found in Central America northward to southern Texas. However, this species may be part of a species complex since specimens identified as A. fraterculus vary widely from populations in Brazil, Mexico, and Texas. It also has a wide host range that includes tropical, subtropical and temperate fruits including sweet orange and peach. The sapote or serpentine fruit fly, A. serpentina (Wiedemann), is a brown fly that is common from southern Texas to Mexico, Central America and South America. It can be a severe pest of ripened sapote (Calocarpum spp.) and sapodilla (Manilkara zapota L.) in Mexico. Although many flies are trapped in south Texas, there is only one record of an infestation in grapefruit. Species in the genus Bactrocera (formerly Dacus) are flies native to Africa, the Mediterranean, Asia and the Pacific. None of the citrus-infesting species are currently established on the mainland United States, but several are occasionally trapped in California and Florida. The oriental fruit fly, B. dorsalis (Hendel), is a variably colored medium-sized fly that infests fruits and vegetables throughout Asia (Pakistan, India, Vietnam, Philippines, Japan, etc.) and the Pacific, including Hawaii. It was introduced into Hawaii in the mid-1940s by returning servicemen that were stationed on several Pacific islands, but has become partially under control through the introduction of parasitoids. In Japan, several management tactics including the use of attractant baits and sterile male release has Citrus Pests and their Management been successful. Guava fruit fly, B. correcta (Bezzi), is a small, brightly colored, predominately black fly that occurs in southern and southeastern Asia. Adults have been trapped in California and Florida but it hasn’t established. It is a potential pest of citrus, peach, and other subtropical and tropical fruits. Queensland fruit fly, B. tryoni (Froggatt), is a small brown-yellow fly that is wasplike in appearance. The distribution of this species includes the eastern half of Australia, although flies have been trapped in Western Australia, New Guinea, and several Pacific islands. It is a pest of pome and stone fruits as well as citrus. Biologically, this species is more temperate in distribution and does not breed continuously but overwinters as an adult. Japanese orange fly, B. tsuneonis (Miyake), infests orange, grapefruit and mandarin orange in Japan, southwestern China and probably Taiwan. There have been no interceptions of this fly in the U.S., mostly because of an embargo of citrus from infested areas. Changes to the embargo laws may increase the chances of introducing this pest. Species in the genus Ceratitis are originally from sub-Saharan Africa, but now some have a worldwide distribution. Mediterranean fruit fly, “Medfly,” C. capitata (Wiedemann), is a yellowish brown fly that is one of the world’s most destructive fruit pests. It has been established in Hawaii since 1910, and has been detected at different times in California, Florida, and Texas. For instance, Medfly has been detected in Florida 16 times since 1929, and only massive and expensive eradication programs have kept it from becoming established in the continental U.S. As with other tephritid fruit flies, eggs are laid slightly beneath the fruit’s surface. Larvae feed within the fruit, and generally the fruit drops to the ground and larvae move into the soil to pupate. Over 260 species of hosts have been recorded, with peach, nectarine, orange, grapefruit, apricot, and pear being some of the Medfly’s favorites. In addition to the reduction in citrus yield, infested areas have the additional expense of control measures and costly sorting for fresh and processing fruit. Detection and control of the Medfly has included trapping, C quarantines, cultural control (waste removal and disposal of culls), release of sterile males, and biological control. Much research has been completed designing traps and lures for detection of Medfly. Two other Ceratitis species are pests in Africa. The Natal fruit fly, C. rosa Karsch, is slightly larger than the Medfly and similar in appearance. It is distributed throughout sub-Saharan Africa and on the Indian Ocean islands of Mauritius and Réunion. This fly overwinters in the adult stage and can withstand below-freezing temperatures. It attacks many temperate stone and pome fruits including peach, nectarine, apricot, apple and pear. Although the Natal fruit fly has been intercepted in the United States in produce, it has never been captured as an escapee. If accidentally introduced, it could prove to be a serious pest. C. malagassa Munro damages citrus fruit on the island of Madagascar. It has a smaller geographical distribution than the other two Ceratitis species discussed. Lepidoptera There are several families of moths and butterflies that attack the fruit or foliage of citrus. Fruitpiercing moths (Noctuidae) are pests in southern Africa, Australia, and east Asia. They include species in the genera Achaea, Calpe, Emaenas, Ercheia, Gonodonta, Othreis, and Serrodes. None of these are apparently established in the U.S. Other noctuids, such as cabbage looper, Trichoplusia ni (Hübner) and beet armyworm, Spodoptera exigua (Hübner) can cause considerable damage to nursery stock and young citrus. Bollworm, Helicoverpa zea (Boddie), is a pest of citrus in Africa in areas when cotton is planted nearby, but is seldom a problem on citrus. Gracillariidae Two species in this family are pests of citrus in the U.S. Citrus leafminer, Phyllocnistis citrella Stainton, 901 902 C Citrus Pests and their Management is an Asian species that has recently spread to northern Africa, Central America and the United States. It was found in late May 1993 in Dade County, Florida, late August 1994 in the Rio Grande Valley of Texas, and in 2000 in Imperial County, California. Hosts include citrus and related species within the plant family Rutaceae. Eggs are laid on the underside of leaves and green-yellow larvae enter leaves and begin forming mines. Pupation is within the mine and white and silver-colored adults emerge during the morning. Injury to foliage and fruit can be extensive with large populations, and damage is more serious to nursery trees or newly planted groves. This pest appears to be able to be controlled through the use of natural enemies. Several Asian parasitoid species have been collected from Australia and released in the United States, but native natural enemies also show promise in reducing populations. Citrus peelminer, Marmara gulosa Guillen Davis, has seriously damaged citrus in several areas in California including the Coachella and San Joaquin valleys and Kern County. Larvae burrow within the epidermal surface of the fruit causing serpentine mines. It often attacks fruit located near alternate hosts such as oleander and willows. Although it seldom affects more than 5% of the fruit, in 2000 citrus peelminer infested almost 70% of the fruit in some groves. It also expanded its geographic and host ranges in California. Research is now being conducted to see if infested fruit imported from Mexico during 1998 included a new biotype or species of peelminer. Tortricidae Two species can cause extensive injury to citrus. Fruittree leafroller, Archips argyrospilus Walker, has been a pest of citrus in California for many years. This species is widespread across the United States feeding on a wide variety of hosts. It has damaged apples in Michigan, New York and Pennsylvania, and bald cypress in Louisiana. On citrus, it feeds on spring flush growth of leaves, flowers, newly set fruit, and later on mature fruit. Unlike many tortricids, eggs are generally laid on woody tissue. Orange tortrix, Argyrotaenia citrana (Fernald), is primarily a pest of “Valencia” and navel oranges in southern California. Eggs are laid on stems, fruit and upper leaf surfaces, and larvae primarily feed on new growth leaves and fruit. Fruit feeding is around the sepals and holes can be eaten in the peel. Several other tortricid species occasionally can attack citrus in the United States. These include garden tortrix, Ptycholama peritana (Clemens), variegated leafroller, Platynota flavedana Clemens, omnivorous leafroller, Platynota stultana Walsingham, and western avocado leafroller, Amorbia cuneana (Walsingham). These species are not specific to citrus and attack several other crops and ornamentals. Tortricids found in other citrus-producing countries include Archips occidentalis (Walsingham) and Tortrix capensana Walker, pests in South Africa, Archips rosanus (L.) in Greece, and Epiphyas postvittana (Walker) in Australia. Like the other leafrollers, these species have relatively wide host plant ranges. Megalopygidae Puss caterpillars, Megalopyge opercularis (J. E. Smith) are pests more because of their medical importance than through defoliation. This caterpillar is the larval form of the southern flannel moth, which is found throughout the southeast and into Texas. Human disease from puss caterpillars usually arises from direct contact to their urticating hairs. Field workers pruning or harvesting fruit are usually the people who come in contact with these insects. Papilionidae A large number of species of swallowtail butterfly larvae (orangedogs) feed on citrus foliage throughout the world. Orangedogs are named Citrus Pests and their Management because when disturbed, larvae stick out orangecolored osmeteria (scent organs located behind the head) and give off a strong, disagreeable odor. Two species are common in the U.S. Giant swallowtail, Papilio cresphontes Cramer, is distributed throughout the U.S. except in the far west. It is an occasional pest of citrus in Florida and Texas, where young trees in groves or nurseries can be quickly defoliated. Adults are large dark butterflies with diagonal yellow bars on the forewings. Adults can be attracted to plants in butterfly gardens. Citrus California orangedog or black anise swallowtail, P. zelicaon Lucas, is a native butterfly that feeds on perennial anise (sweet fennel) and citrus. Like other Papilio larvae, these larvae are more damaging to young trees. Hymenoptera This order contains ants, wasps, and bees. Wasps and bees can be pests when fruit workers contact colonies in the field. Formicidae In the Rio Grande Valley, the Texas leafcutting ant, Atta texana (Buckley), is the most serious ant pest. These reddish-brown ants remove leaves from trees to culture fungus for food. In areas of large colonies, single trees may be defoliated in a single night. Large areas underground are excavated and may present problems for farm machinery. Multiple defoliation of young trees can slow growth or cause tree death. Fire ant species in the United States can be citrus pests and include red imported fire ant, Solenopsis invicta Buren, native fire ant, S. geminata (F.), and southern fire ant, S. xyloni McCook. Fire ants injure trees by attacking twigs, bark, and leaves, and young trees can be completely girdled. Young trees also can be damaged when bark beneath tree wraps are injured and provide a point of entry for fungi. C Several ant species are problems on citrus because of their interference in the development of biological control programs. Argentine ants, Linepithema humile (Mayr) (formerly known as Iridomyrmex humilis), and native gray ants, Formica aerata Francouer, feed on honeydew excreted by soft scales, mealybugs, whiteflies, and aphids. In this relationship, they protect these species from natural enemies. They even protect other scales species that don’t produce honeydew, such as California red scale, from potential biological control agents. Gastropoda: Pulmonata Helicidae Although snails are not insects, they can be serious pests of citrus by feeding on leaves, buds, flowers, fruit and bark. The brown garden snail, Helix aspersa Müller, is a European species that is found in California and in most southeastern states. However, it is not established in Florida. This species is hermaphroditic (having both male and female organs), so during mating mutual fertilization can occur. Large populations can be found in citrus groves where extensive damage to leaves and fruit may occur. At one time, snails were only found in California’s humid and cool coastal areas, but because of drip irrigation and no-till weed control, snails are now found in several citrus-growing districts. Citrus Pest Management Fresh or Processing Market One of the most important decisions citrus growers make at the beginning of a season is whether to market their fruit for the fresh market or processed market. For maximum profitability of fresh market fruit, a high level of pest control is needed to reduce the number of external blemishes. This level of quality is not needed for fruit destined for the processing market. Several factors are involved in the decision-making process for market destination: 903 904 C Citrus Pests and their Management grove location and accessibility of markets, fruit variety grown, grove history for pests, and profitability desired. Growers may decide that their fruit will be managed for the fresh market, but after spring bloom several abiotic (weather-related) or biotic (tree health, disease pressure, high pest densities) factors may change that decision. Therefore, the market decision that growers make impact the management input in groves. Sampling and Thresholds Citrus growers need to be able to identify and provide estimates of the numbers of pests and natural enemies present in their groves. The frequency and methods used to sample or monitor for pests and natural enemies varies depending on the pest being sampled and the time invested. For instance, it is suggested that sampling for citrus rust mites be every 2 weeks during the season because their populations can expand quickly. Most other pests are monitored on a monthly basis. Sampling may involve trees randomly selected for each period or permanently designated station trees. Trees that are randomly selected should be dispersed sufficiently to be representative of the grove. Station trees are representative trees that are flagged and visited each sampling period. In both cases, accurate and descriptive records should be kept. Action thresholds are pest population densities that, when reached, signal to the grower that some type of corrective action is needed. Thresholds for a certain pest species will vary depending on the fruit market destination, time of season, and abundance of appropriate natural enemies. Thresholds have been developed by entomologists for many of the important citrus pests, and are designed to provide enough time for growers to take corrective action. Management Strategies Growers use three general approaches for control of citrus pests. Cultural control is defined as using horticultural techniques to reduce the likelihood of pest problems. Several cultural control techniques may be completed before or during grove establishment, such as site selection, rootstock choice, and the use of virus-free budwood. Techniques accomplished after grove establishment include tree nutrition, irrigation, plant waste removal, pruning practices, and harvesting practices. The second management strategy that growers may employ is biological control, which is the use of naturally occurring or imported parasitoids, predators, or pathogens to reduce pest populations. The citrus industry historically has encouraged the use of natural enemies, therefore, many citrus pests are partially or fully under biological control. However, biological control systems are easily disturbed by pesticide use. The third management strategy used by citrus growers is chemical control. The products that are used include synthetic chemicals such as insecticides, acaricides, and horticultural oils, which have different ways of killing arthropods (mode of action). Biological products such as bacteria, fungi, or viruses also are available and can be used in a similar fashion as chemicals. Before chemical control is used, several factors must be considered. Is the pesticide labeled for use against the target pest and is it efficacious? What is the cost effectiveness of the product and what are the hazards to natural enemies, the environment, the fruit, and the applicators? Finally, what is the impact of the intended product on the development of pest resistance. All citrus-producing states have guides available each season for growers. These guides contain lists of labeled products and directions on how to use them against the important pests in those areas. Each state also has entomologists who compare the efficacy of new and existing products under the conditions of the local growing areas. References Hui S (1999) Sweet oranges: the biogeography of Citrus sinensis. Available at http://www.aquapulse.net/knowledge/ orange.html. Accessed 4 April, 1999 Cladogram Morton JF (1987) Fruits of warm climates, Media Incorp, Miami, FL. Available at http://www.hort.purdue.edu/ newcrop/morton/index.html Reuther W, Calavan EC, Carman GE (eds) (1989) The citrus industry, vol 5: crop protection, postharvest technology, and early history of citrus research in California. Division of Agriculture and Natural Resources, University of California, 374 pp Texas A&M University. Available at http://aggie-horticulture. tamu.edu/citrus/industry.htm University of California. UC pest management guidelines – pests of Citrus. Available at http://axp.ipm.ucdavis.edu/ PMG/selectnewpest.citrus.html University of Florida. Available at http://creatures.ifas.ufl. edu/ and http://edis.ifas.ufl.edu/MENU_CH5A for Insect Pests of Citrus and /MENU_CG for Pest Management Guides C Cixiidae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs Cladistic Analysis A technique that groups taxa based on the relative recency of common ancestry. Clade Citrus Rust Mites (Acari: Eriophyidae) Several mites cause russeting of citrus.  Citrus Pests and Their Management A monophyletic group of taxa that share a closer common ancestry with one another than with members of any other group. Cladiopsocidae Citrus Snow Scale, Unaspis citri (Comstock) (Hemiptera: Diaspididae) This is an important citrus pest in Florida, USA.  Citrus Pests and Their Management Citrus Stubborn Disease This is a leafhopper-transmitted disease of citrus.  Transmission of Plant Diseases by Insects A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Cladistics A school of thought that uses only evolutionary relatedness (phylogenetics) in assigning taxonomic groupings in classification systems. Cladogenic Speciation Branching evolution of new species. Citrus Whitefly, Dialeurodes citri (Ashmead) (Hemiptera: Aleyrodidae) This was once a very serious pest of citrus, but is now considered a minor pest.  Citrus Pests and Their Management Cladogram A term used two ways by different authors. Either a dendrogram (tree) produced using the principle of parsimony, or a tree that depicts inferred historical relationships between organisms. 905 906 C Clambidae Clambidae A family of beetles (order Coleoptera). They commonly are known as fringe-winged beetles.  Beetles Class A major subdivision of a phylum, and containing a group of orders.  Classification Classical Biological Control marJorie a. hoy University of Florida, Gainesville, FL, USA Biological control is a method of pest control that employs parasitoids, predators, microbial pathogens and, sometimes, nematodes to reduce pest populations. Pests that are targets of biological control include insects, mites, and weeds. [See the section on Natural Enemies for a description of natural enemies used in biological control programs.] Biological control is part of natural control, which maintains populations within more or less regular upper and lower limits over time. Natural control factors may be biotic (living) or abiotic (nonliving). Biotic control factors include the effects of natural enemies, food quantity and quality, interspecific and intraspecific competition for resources, and requirements for space or territory. All insects and mites have a diverse array of natural enemies. Microorganisms, invertebrates, and vertebrates all affect them, causing debilitation or death. Pathogens attacking arthropods include viruses, bacteria and fungi. Many vertebrates (including birds, lizards, fish and frogs) feed on pest arthropods. Nematodes belonging to several families attack insects. However, by far insects are the most numerous and diverse natural enemies of other insects, with hundreds of thousands of species feeding on other insects. Abiotic factors that affect insect and mite populations include weather (heat, cold, rain, drought) and other physical factors. Biotic and abiotic control factors usually act together to limit population growth by reducing birth rates or increasing mortality or dispersal, although one may be more important than the other in certain situations. Most organisms produce more progeny than the environment can sustain, yet many natural populations maintain characteristic densities over long periods of time. This state of dynamic equilibrium is achieved by an interaction between the biotic potential of the species and the resistance of biotic and abiotic factors in the environment. Some ecologists have focused on the importance of natural population regulation by biotic factors (particularly natural enemies), while others have emphasized the importance of abiotic factors (especially weather). Still other ecologists have emphasized the importance of interspecific competition in regulating population densities. The relative importance of these factors continues to be debated, but it is likely that each is important and potentially capable of regulating population densities in specific situations. Under most circumstances both biotic and abiotic factors together influence population densities, and it is the degree to which any one factor affects natural control in specific situations that differs. Physical factors generally influence populations in a density-independent manner. This means that the intensity of the effect of physical factors is not related to the target population’s density. Thus, a severe freeze usually will kill approximately the same proportion of large populations as of small populations. By contrast, biotic factors may influence population densities in a more density-dependent manner, with their effect increasing in intensity as populations become larger and decreasing in intensity as populations decrease. Density-dependent population regulation acts as a negative feedback process between population density and rate of increase. For example, the availability of plant hosts may exert density-dependent pressure on insect populations, with a small number of plants being sufficient for a small population but inadequate for a large one. Classical Biological Control Parasitoids, predators and pathogens potentially are capable of affecting pest populations in a density-dependent fashion because they can respond to changes in host population density. Some natural enemies may increase their activities and reproductive rates as the density of their insect host increases, and reduce these activities as the density of their hosts declines. If natural enemies increase their numbers with increasing pest/host population densities, this is termed a numerical response. Numerical responses occur because prey or hosts are readily available so that the reproductive rates of natural enemies are enhanced. A functional response is another important component of a density-dependent response by parasitoids and predators. A functional response is the change in number of prey or hosts consumed or parasitized per natural enemy in response to changing prey or host density. Functional responses are influenced by several factors, including: (i) rate of successful search, (ii) the amount of time the natural enemy and target pest are exposed to each other, and (iii) the time spent by the natural enemy handling each prey or host. If pest populations increase and, as a consequence, are more aggregated, natural enemies may not have to spend as much time searching for prey or hosts. Natural enemies also can increase their functional response by consuming only part of their prey at high densities, thus killing more prey per unit time. C Classical Biological Control This approach involves importing and establishing natural enemies in order to assist in the long-term control of newly introduced, foreign pests. Classical biological control involves a series of steps and usually takes a number of years. Most programs require more than 10 years of effort. Classical biological control in the U.S.A. was demonstrated to be a useful pest management tool over 100 years ago after two natural enemies were introduced and established in 1888 against the cottony cushion scale, Icerya purchasi, in California’s citrus industry. The cottony cushion scale was accidentally introduced into California. It rapidly established, spread and multiplied. The severe effects of its feeding on citrus trees threatened the survival of the citrus industry. In one of the more dramatic classical biological control programs ever recorded, the Vedalia lady beetle Rodolia cardinalis and a fly Cryptochetum iceryae were imported and released. Within 2 years, these natural enemies had established, multiplied, and spread to reduce populations of the cottony cushion scale (Fig. 61) to an insignificant level. These natural enemies have continued to provide effective control in California ever since unless disrupted by applications of pesticides. Furthermore, these natural enemies have been distributed to more than 25 additional countries, where they have established and provided excellent control of the cottony cushion scale. Naturally Occurring Biological Control Many insects or mites are not pests because native natural enemies keep them suppressed with no assistance from humans. Naturally occurring biological control often is discovered only after natural enemy populations have been disrupted and insect or mite populations have increased dramatically to become pests. Biological control also includes an applied technology through which humans attempt to restore, enhance, or mimic a natural phenomenon by three basic tactics: classical biological control, augmentation, or conservation. Assumptions of Classical Biological Control Insects or mites that establish in a new environment often are much more serious pests than they are in their native range where they are suppressed by a complex of natural enemies. If a foreign pest arthropod evades regulatory and quarantine barriers to become established in a new environment and cannot be eradicated, the feasibility of classical biological control should be evaluated immediately. 907 C Classical Biological Control Cryptochaetum iceryae and Rodolia cardinalis introduced Resurgence induced by DDT Icerya purchasi density 908 Economic injury level Economic threshold General equilibrium position 1868 1888-89 1892 1947 Classical Biological Control, Figure 61 The cottony cushion scale, Icerya purchasi, increased its population dramatically after its introduction in 1868 into California citrus groves. In 1888, the parasite Cryptochetum iceryae and the predator Rodolia cardinalis were introduced. Within a year after their establishment, they reduced the scale populations below the economic injury level, where it fluctuated around a general equilibrium position until DDT applications were made in the 1940s, which allowed a resurgence because the natural enemies were disrupted. The assumptions of classical biological control are: (i) pest populations are suppressed by natural enemies in their native land, (ii) pest populations have escaped suppression after their introduction without their natural enemies into a new environment, and (iii) introduced natural enemies may be more effective in a new location if introduced free of their own natural enemies (e.g., predators and parasitoids may have their own natural enemies that reduce their effectiveness against the target pest). Another assumption is that the existing natural enemies present in the new geographic environment will be generalists, and therefore less effective than natural enemies that have specialized on the target pest in their original environment. Classical biological control programs typically require a number of years to execute, and there are no guarantees that the pest populations will be suppressed to a satisfactory level in the new environment. However, if classical biological control is successful, it can provide cost-effective and environmentally benign pest management for a long time. Steps in Classical Biological Control Classical biological control involves a series of steps, beginning with identifying the pest as native or foreign in origin. If foreign, it is important to identify the origin of the pest, because this area may provide the most extensive array of natural enemies for evaluation and possible importation. Once the biology and behavior of the pest have been reviewed, specific natural enemies are identified as potential targets of a collecting trip. Sometimes, a long list of natural enemies is available; sometimes, only a few natural enemy species Classical Biological Control C Classical Biological Control, Figure 62 Endoparasitoid female, Trioxys pallidus (Hymenoptera: Aphelinidae), inserting an egg into the walnut aphid, Chromaphis juglandicola. (Photo provided by J. K. Clark.) are known. Typically, only a few species are collected, shipped and evaluated further. Once the natural enemies are obtained and shipped to a quarantine facility, their identity is verified by taxonomic specialists and the colonies are screened to eliminate undesirable hyperparasitoids (parasitoids of the primary parasitoid) or pathogens. Permission to release the natural enemies must be obtained from state and or federal regulatory agencies after a risk analysis has been conducted. Natural enemies are then mass reared and released (Figs. 62 and 63) with the goal of permanently establishing them in the new environment to provide continuing control of the target pest. Classical biological control programs are dependent upon having taxonomic specialists to correctly identify immigrant pests, provide information on their geographic distribution, and identify natural enemies in the country of origin. Correct identification (Fig. 64) of pests and their origins is important when planning collection trips. Natural enemies also must be correctly identified before they can be released from quarantine into the new environment. Some effective biological control programs have been delayed because taxonomic information was lacking or incorrect. Because financial support for systematics is declining, fewer such specialists are being trained which could lead to delays or failures in future classical biological control programs. Taxonomic specialists also can provide information on the host or prey range of the natural enemy, which is important when risk assessments are being conducted prior to releasing the natural enemies. Classical biological control is an important component of pest management programs because foreign pests invade new environments on a continuing basis. For example, by 1971 at least 1,683 species of insects or mites found in North American forests, rangelands, or agricultural fields were illegal aliens. Some were pests, some were beneficial, and some had no known economic importance. At least 235 major pests in the U.S.A. are foreign, coming from nearly all geographic regions of the world. Another 630 foreign arthropod species are listed as lesser pests. In Florida, at least 209 species of foreign insects have been found since 1970; approximately 20 are major pests, including the Mexican fruit fly, Anastrepha ludens, Mediterranean fruit fly, Ceratitis capitata, Asian tiger mosquito, Aedes albopictus, citrus blackfly, Aleurocanthus woglumi, citrus leafminer, Phyllocnistis citrella, Asian citrus psylla, Diaphorina citri, brown citrus aphid, Diaphorina citri, and the melon thrips, Thrips palmi. 909 910 C Classical Biological Control Classical Biological Control, Figure 63 Endoparasitoid female, Cardiochiles diaphaniae (Hymenoptera: Braconidae), inserting an egg into the melonworm, Hyalinata hyalinata. This parasitoid was introduced from Colombia, South America into Puerto Rico and Florida, successfully establishing in the former location. Based on past history, foreign insect and mite species will continue to immigrate to the U.S.A. at the rate of about eleven species per year. Of the eleven, seven are likely to be pests of some importance and about every third year a pest of major significance will be discovered. Assuming that few of these pests can be eradicated, classical biological control remains a potentially effective method for providing cost-effective pest suppression. Classical biological control can be effective against different types of pests. For example, in the continental U.S.A. and Hawaii insects in the orders Lepidoptera, Coleoptera, Hemiptera, Hymenoptera, Diptera and Orthoptera have been suppressed by arthropod natural enemies in classical biological control programs. Nearly complete control was obtained in some cases, while in others only partial control was achieved. Sometimes a single natural enemy provided substantial control; in other circumstances several natural enemy species were required. Effective biological control can be achieved with a specific natural enemy in the entire geographic region that the pest inhabits in some cases, or this natural enemy may be effective only in a limited part of the new geographic distribution. Some classical biological control programs can be accomplished without a collecting trip; if a natural enemy has been established in one region, scientists there can collect it and ship it to a new region where the pest has invaded. Once the natural enemy has been processed through quarantine, reared and released, it may provide relatively rapid and inexpensive control (Table 13). Cooperation Between Scientists Aids in Citrus Blackfly Project Classical biological control of the citrus blackfly, Aleurocanthus woglumi, in Texas and Florida provides an example of highly successful projects that benefited from cooperation between scientists in different regions. The citrus blackfly invaded Texas in the late 1960s and caused serious damage in citrus groves there. Eradication efforts began in 1971, but were unsuccessful. Joint efforts between scientists in Texas and Mexico resulted in the importation, evaluation and release of two parasitoids, Amitus hesperidum and Encarsia opulenta, that provided complete biological control of the citrus blackfly. Classical Biological Control C Identify pest as native or foreign If pest is exotic, determine geographic origin Evaluate information on pest’s biology & behavior and natural enemies to define search area Obtain natural enemies by collaboration & exchange or foreign exploration Import natural enemies into quarantine; evaluate biology & risks; maintain voucher specimens Once out of quarantine, evaluate natural enemy in laboratory, greenhouse & field cages; develop mass rearing methods Release into environment; determine if establishment occurred Evaluate efficacy & benefits : costs Classical Biological Control, Figure 64 Classical biological control involves a series of steps before a foreign pest can be controlled by the introduction and establishment of one or more natural enemies. From start to finish, classical biological control programs require sustained funding and personnel over several years. The citrus blackfly subsequently invaded Florida in 1976, and huge populations developed rapidly. The honeydew produced by the blackflies caused entire citrus groves to become blackened by sooty mold growth. Again, eradication of the pest was attempted, but after $15 million dollars had been spent, the blackfly was still present and increasing its distribution. 911 912 C Classical Biological Control Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by imported arthropod natural enemies in the Continental USA and Hawaii Pesta control Crop or host Principal natural enemiesa (P) = parasitoid (Pred) = predator Project resultsb C = complete S = substantial P = partial Oriental mole cricket, Gryllotalpa orientalis Sugarcane Larra polita (P) P alfalfa weevil, Hypera postica Alfalfa Bathyplectes curculionis (P) P-S Microctonus aethiops (P) P-S Tetrastichus incertus (P) P-S American cockroach, Periplaneta americana Household pest Ampulex compressa (P) P armyworm, Pseudaletia unipuncta Sugarcane Apanteles militaris (P) C Archytas cirphis (P) S Asiatic rice borer, Chilo suppressalis Rice Amyosoma chilonis (P) P Dioctes chilonis (P) P Trichogramma japonicum (P) P asparagus beetle, Crioceris asparagi Asparagus Tetrastichus asparagi (P) P-S Australian cockroach, Periplaneta australasiae Household pest Ampulex compressa (P) P barnacle scale, Ceroplastes cirripediformis Passion fruit Coccidoxenus mexicanus (P) S birch leaf-mining sawfly, Heterarthrus nemoratus Birch, Alder Chrysocharis laricinellae (P) C Phanomeris phyllotomae (P) C black scale, Saissetia oleae Citrus, Olive, Ornamentals Metaphycus helvolus (P) S Diversinervus elegans (P) S Encyrtus infelix (P) S Metaphycus luteolus (P) S Coccophagus capensis (P) P-S Coccophagus cowperi (P) S Apanteles lacteicolor (P) S browntail moth, Euproctis chysorrhoea Forest, shade trees California red scale, Aonidiella aurantii Citrus Chinese grasshopper, Oxya chinensi Townsendiellomyia nidicolor (P) S ? and others Sugarcane Aphytis lingnanensis (P) P Aphytis melinus (P) P Comperiella bifasciata (P) P Scelio pembertoni (P) S Classical Biological Control Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by imported arthropod natural enemies in the Continental USA and Hawaii (Continued) Pesta control Crop or host Principal natural enemiesa (P) = parasitoid (Pred) = predator Project resultsb C = complete S = substantial P = partial Chinese rose beetle, Adoretus sinicus Vegetables, ornamentals Campsomeris marginella modesta (P) P Tiphia segregata (P) P citrophilus mealybug, Pseudococcus fragilis Citrus, Acacia citrus blackfly, Aleurocanthus woglumii Citrus citrus mealybug, Planococcus citri Citrus citrus leafminer, Phyllocnistis citrella Citrus Florida Coconut palm Coccophagus gurneyi (P) C Hungariella pretiosa (P) C Amitus hesperidum (P) C Encarsia opulenta coconut scale, Pinnaspis buxi Cryptolaemus montrouzieri (Pred) P Leptomastidea abnormis (P) P Ageniaspis citricola (P) S Telsimia nitida (Pred) S Allotropa burrelli (P) C Pseudaphycus malinus (P) C Cryptochetum iceryae (P) S-C Rodolia (=Vedalia) cardinalis (Pred) C Comstock mealybug, Pseudococcus comstocki Apple cottony cushion scale, Icerya purchasi Citrus Egyptian alfalfa weevil, Hypera brunneipennis Alfalfa Bathyplectes curculionis (P) P European corn borer, OIstrinia nubilalis Corn Lydella thompsoni (P) P Macrocentrus gifuensis (P) and others P European earwig, Forficula auricularia Gardens Bigonicheta setipennis (P) P fern weevil, Syagrius fulvitarsis Native Hawaiian Tree ferns Doryctes syagrii (P) P Florida red scale, Chrysomphalus aonidum Citrus Aphytis holoxanthus (P) C gypsy moth, Lymantria dispar Forest, shade trees complex of parasitoids, predators and pathogens P Japanese beetle, Popillia japonica Turf, pasture, fruits, ornamentals Tiphia vernalis (P) P longtailed mealybug, Pseudococcus adonidum Citrus, Avocado Anarhopus sydneyensis (P) P Cryptolaemus montrouzieri (Pred.) P Hungariella peregrina (P) P C 913 914 C Classical Biological Control Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by imported arthropod natural enemies in the Continental USA and Hawaii (Continued) Pesta control Crop or host Principal natural enemiesa (P) = parasitoid (Pred) = predator Project resultsb C = complete S = substantial P = partial Mediterranean fruit fly, Ceratitis capitata Fruits, Coffee Opius tryoni (P) P Opius fullawayi (P) P melon fly, Dacus cucurbitae Melons Cucumber Opius fletcheri (P) P New Guinea sugarcane weevil, Rhabdoscelus obscurus Sugarcane Lixophaga sphenophori (P) S-C nigra scale, Saissetia nigra Ornamentals Metaphycus helvolus (P) S nutgrass armyworm, Spodoptera exempta Sugarcane, pasture a complex of parasitoids P-C olive scale, Parlatoria oleae Olive, ornamentals, deciduous fruit Aphytis maculicornis (P) Coccophagoides utilis (P) S S-C oriental beetle, Anomala orientalis Sugarcane Campsomeris marginella modesta (P) P-S Tiphia segregata (P) oriental fruit fly, Dacus dorsalis Fruits oriental fruit moth, Grapholitha molesta Peach, pome fruits Opius oophilus (P) S-C Opius vandenboschi (P) S Macrocentrus ancylivorus (P) P oriental moth, Cnidocampa Shade trees, fruit trees Chaetexorista javana (P) flavescens S pea aphid, Acyrthosiphon pisum Alfalfa Aphidius smithi (P) S pine tip moth, Rhyacionia frustrana bushnelli Pine trees Campoplex frustranae (P) P pink sugar cane, mealybug Trionymus sacchari Sugarcane Anagyrus saccharicola (P) S purple scale, Lepidosaphes beckii Citrus Aphytis lepidosaphes (P) S-C Rhodesgrass scale, Antonina graminis Orange grasses Neodusmetia sangwani (P) S San Jose scale, Quadraspidiotus perniciosus Deciduous fruit Prospaltella perniciosi (P) P Classical Biological Control C Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by imported arthropod natural enemies in the Continental USA and Hawaii (Continued) a Pesta control Crop or host Principal natural enemiesa (P) = parasitoid (Pred) = predator Project resultsb C = complete S = substantial P = partial satin moth, Stilpnotia salicis Forest trees Apanteles solitarius (P) S-C Meteorus versicolor (P) S-C spotted alfalfa aphid, Therioaphis maculata Alfalfa Aphelinus semiflavus (P) S Praon palitans (P) S Trioxys utilus (P) S southern green stink bug, Nezara viridula Vegetables, fruits, ornamentals Trissolcus basilis (P) S-C sugarcane aphid, Aphis sacchari Sugarcane complex of parasitoids and predators S sugarcane borer, Diatraea saccharalis Sugarcane Lixophaga diatraeae (P) P Agathis stigmaterus (P) P sugarcane leafhopper, Perkinsiella saccharacida Sugarcane and others Tytthus mundulus (Pred) C sweet potato leaf miner, Bedellia orchilella Sweet potato Apanteles bedelliae (P) P-C taro leafhopper, Tarophagus proserpina Taro Cyrtorhinus fulvus (Pred) S torpedo bug planthopper, Siphanta acuta Coffee, Mango, Citrus Aphanomerus pusillus (P) S-C walnut aphid, Chromaphis juglandicola Walnuts Trioxys pallidus (P) P-C western grape leaf skeletonizer, Harrisina brillians Grape Apanteles harrisinae (P) S wooly apple aphid, Eriosoma lanigerum Apple Aphelinus mali (P) S-C wooly whitefly, Aleurothrixus floccosus Citrus Amitus spiniferus (P) S-C Eretmocerus paulistus (P) C yellow scale, Aonidiella citrina Citrus Comperiella bifasciata (P) S-C Sturmia harrisinae (P) Not all examples are cited; success ratings and scientific names of pests and natural enemies vary in different lists. Complete successes (C) refer to complete biological control obtained and maintained against a pest over an extensive area so that pesticide applications rarely are necessary. Substantial (S) successes include cases in which insecticidal control is sometimes required. Partial successes (P) are those in which chemical controls are applied, but the intervals between applications or lengthened or the outbreaks occur less often. ? refers to situations in which the results are unknown or controversial. b 915 916 C Classical Biological Control As the result of cooperation between scientists from Texas and Mexico, A. hesperidum, E. opulenta, E. clypealis and E. smithi were introduced into Florida in 1976. Both A. hesperidum and E. opulenta became established. Amitus hesperidum provided rapid control of blackfly populations, but E. opulenta eventually replaced A. hesperidum as the dominant parasitoid after citrus blackfly populations had been reduced. Both parasitoids are given credit for providing complete biological control of the blackfly in Florida by 1981. The program cost approximately $US 2.2 million dollars, but the benefits continue to accrue, and were estimated to be $9.3 million in 1980 alone. Effective classical biological control depends upon the establishment of one or more foreign natural enemies in a new environment. Establishment of natural enemies in new environments is not guaranteed, with estimates of successful establishment ranging from 16 to 34%. There is intense interest in learning how to increase establishment rates and the use of climate-matching computer programs may allow scientists to increase the establishment rate. After release, the introduced natural enemy must find adequate hosts and other resources as well as suitable climatic conditions in the new environment. Natural enemies must be released in adequate numbers, in a healthy condition, at an appropriate time, and in the presence of suitable hosts or prey if establishment is to succeed. In some cases, different populations (biotypes) of a particular species have different biological attributes that make them more or less likely to establish and be effective in the new environment. For example, a parasitoid called Trioxys pallidus originally was collected in France and released in California to control the walnut aphid Chromaphis juglandicola. The French biotype established, but was only effective in the cooler, more humid coastal areas of California. A biotype of T. pallidus from Iran was subsequently established and provided highly effective control of the walnut aphid in the hot, dry Central Valley of California. Although classical biological control can yield complete and lasting pest population suppression in a many situations, many past efforts have been only casual or have involved use of an unsuitable natural enemy. In general, relatively little classical biological control has been directed against pests of range, forage, grain crops or row crops. For example, of 110 pest species under partial to complete control by classical biological control, only 13 involved pests of row crops. This relatively poor record has been attributed to the instability of the row crop environment. Row crops persist only for weeks or months, during which time the natural enemy must discover and move into the crop, find, attack, and build up numbers on the pest, then be subjected to abrupt disruption at the end of the crop season. A large number (ca. 40%) of the pests targeted in classical biological control programs have been scales (Hemiptera), and about 20% have been Lepidoptera, Coleoptera, or Hemiptera other than coccids. Many of the successes have been achieved in warmer climates, particularly in Hawaii and California, although it is likely that these successes are due to the extensive efforts employed in classical biological control. Other trends include an emphasis on employing parasitoids rather than predators, with a majority of successful classical biological control programs involving highly host-specific natural enemies. Establishment of host-specific parasitoids is considered to be lower risk than release of natural enemies with a broad host or prey range. Such host specificity is important in alleviating concerns about unintended effects of these natural enemies on nontarget native species. Successful classical biological control is dependent on two critical elements: (i) establishing the natural enemy in the new environment, and (ii) the efficacy of the natural enemy in the new environment. Usually, a particular pest will have more natural enemies attacking it than are feasible to evaluate and release. Some guidelines have been suggested for choosing between different natural enemy species to evaluate and release. Classical Biological Control Potentially effective natural enemies generally exhibit as many of the following attributes as possible: · · · · · · Fitness and adaptability in the target environment High searching capacity for the target species High reproductive rate relative to that of the host or prey Synchronization with the host or prey and its habitat Host or prey specificity An ability to increase its effectiveness as the host or prey density increases (density-dependent response to the pest) A natural enemy that behaves in a densitydependent manner can respond to changes in the population density of its host or prey, leading to an increasing percentage of kill with increasing host or prey density and a decreasing percentage of kill with decreasing host or prey density. It is difficult to document experimentally that, in fact, a natural enemy is behaving in a density-dependent manner because it is likely that most natural enemypest interactions exhibit a time lag, and thus are behaving in a delayed density-dependent manner. Delayed density dependence occurs when the response of natural enemies to the pest population is delayed for some reason. In many situations classical biological control programs result in substantial pest population reductions. However, some large, lengthy, and expensive projects have been unsuccessful for unknown reasons. As an example, a classical biological control project directed against the gypsy moth, Lymantria dispar, has been slow to result in adequate pest population suppression despite extensive and long-term efforts involving the importation and release of predators, parasitoids and pathogens. Gypsy moth populations are preyed on by native natural enemies, including vertebrate predators. Despite the effects of native and imported natural enemies, suppression of gypsy moth populations in North America to levels that are considered acceptable has been slow in coming. C Classical Biological Control and the Gypsy Moth The gypsy moth is an important forest defoliator that was introduced into North America in 1869. Large classical biological control projects were initiated during three different intervals, with the first beginning in 1905 after efforts to eradicate the gypsy moth were abandoned. That project continued through 1914 and the second ran from 1922 until 1933. Efforts intensified again in 1963. During these three intervals, more than 40 species of parasitoids were introduced into North America against the gypsy moth; ten established, including two that attack eggs, two that attack small larvae, four that attack larger larvae, and two that attack pupae. In addition, the predaceous ground beetle, Calosoma sycophanta, and a nuclear polyhedrosis virus (a virus specific to the gypsy moth) were established. Despite the effects of these parasitoids, predators and pathogens, and the depredations of a variety of native natural enemies such as mice, shrews, birds, spiders, stink bugs, hornets, preying mantids, ants and bacterial and fungal diseases, the gypsy moth continued to expand its range in North America and cause periodic defoliations over thousands of acres of forest and shade trees. Recently, a fungus native to Japan, Entomophaga maimaiga, was found causing dramatic and unexpectedly high levels of mortality to gypsy moth larvae in the northeastern United States. The mortality was unanticipated because the fungus is believed to have been introduced into North America nearly 80 years ago, but was not discovered until 1989. No one knows why it apparently was ineffective until recently; some speculate that the fungus was introduced recently, although the introduction was not conducted with an established program and did not go through risk evaluation. Despite the pleasant surprise of discovering another microbial disease agent, it is unclear 917 918 C Classical Biological Control whether E. maimaiga, in combination with the other exotic and native natural enemies, can provide adequate suppression of gypsy moth populations in North America. Gypsy moth populations apparently are influenced by both biotic and abiotic factors, including vertebrate and invertebrate natural enemies, weather, host tree species, foliage chemistry and plant quality. Because gypsy moth populations synchronously reach outbreak densities over large areas, it is possible that a combination of weather and other mortality factors is responsible for the onset of periodic outbreaks. There is considerable debate over the degree and type of control exerted by various vertebrate and invertebrate natural enemies, and it is unclear whether establishment of additional foreign natural enemies would contribute significantly to suppressing the stillexpanding distribution of the gypsy moth in North America. Even in southern Europe, where an extensive array of natural enemies occur and the gypsy moth is a native, gypsy moth populations reach damaging levels periodically. Thus, the gypsy moth appears to represent a foreign pest that may be managed only by a multi-tactic pest management program. Sometimes, classical biological control programs can reduce the pest population to a level that can be lived with over a very large area. The cassava mealybug classical biological control program is one of the most successful and large scale programs ever conducted. This program has gone through all the steps involved, including an economic analysis of the costs and benefits. Continent-Wide Control of the Cassava Mealybug in Africa Cassava, Manihot esculenta, was brought to Africa about 300 years ago from South America. Cassava serves as a subsistence crop for 200 million people because it is hardy, and adapted to a variety of farming systems and to sub-Saharan climatic conditions. Cassava is estimated to provide up to 50% of the daily caloric intake of 200 million people in Africa and, because cassava roots can remain in the ground for up to 2 years, provides an even higher proportion of the diet when other crops fail. Cassava is an insurance crop against famine. In the early 1970s, the cassava mealybug Phenacoccus manihoti was accidentally introduced into Africa, probably because quarantines were ignored and planting material was introduced illegally. The cassava mealybug spread rapidly across much of the sub-Saharan region of Africa and caused devastating losses (10–100%) by the early 1980s, estimated to be at least $2 billion per year. Chemical control was not ecologically, economically, or logistically feasible. Famine was possible if control was not achieved. A breeding program was initiated to develop resistant varieties, but this was recognized to be a potential solution that would take at least 10–20 years. At the same time as the breeding program was initiated, a classical biological control program was begun. Surveys in Central and South America were conducted for natural enemies of the cassava mealybug and an encyrtid parasitoid Apoanagyrus lopezi was introduced, reared and released by the Africa-Wide Biological Control Programme of the International Institute for Tropical Agriculture and by national agencies of many African countries. Subsequent to its first release in 1981 and 1982, A. lopezi has established in at least 19 countries and is providing effective control of the mealybug throughout most of its distribution in Africa. The economic benefits of this classical biological control program were estimated from 1977 through 2002, using the following very conservative assumptions: that cassava has a value of US $60/ton; production would remain stable at 1980 levels; an average yield loss of 20% would occur due to mealybug; and A. lopezi would reduce losses due to mealybugs by only 60%; by 2002 other Classical Biological Control control methods (plant resistance, integrated pest management programs) would provide effective control. An estimated $2,205,000,000 are estimated to have been saved by the introduction of A. lopezi, as compared to the classical biological control program which cost $14,800,000. This produced a benefit to cost ratio of 149:1, which is unusually high. The benefits are so high because the program was developed quickly, was unusually effective across a wide geographic region, and cassava is a very important crop. This estimate demonstrates how well classical biological control can work and has encouraged its use against another pest of cassava introduced into Africa, the cassava green mite. Conservation of Natural Enemies Conservation of natural enemies involves protecting and maintaining natural enemy populations. Conservation is crucial if either native or introduced natural enemies are to be maintained in agricultural crops. Conservation most often involves modifying pesticide applications. As a general principle, pesticide applications should be made only when pest populations exceed specified levels and when no other control tactic is available. In some cases, changing the active ingredients, rates, formulations, timing, and/or location of pesticide applications can allow natural enemies to remain effective. Maintaining untreated refuges also protects natural enemy populations; for example, alternate rows are treated with pesticides so that the lady beetle Stethorus punctum can survive to control European red mites, Panonychus ulmi, in Pennsylvania apple orchards. Effective Natural Enemies The effectiveness of natural enemies in controlling pest populations depends on the characteristics of C the specific system. However, as a general rule, the most effective natural enemies: · · · Exhibit a high degree of prey or host specificity Have a high relative reproductive rate compared to their prey or host, and Exhibit a tolerance of abiotic factors similar to that of the host or prey The host or prey searching ability of arthropod natural enemies has been studied rarely in the field. What we know about their behavior usually comes from observations in the laboratory or other artificial situations. Arthropod natural enemies respond to physical and chemical cues from the host or prey itself, from its host plant, and from an interaction of the two. Prey/host selection has been divided into four steps: (i) habitat selection, seeking a particular environment where an appropriate host plant occurs; (ii) prey or host finding, identifying prey or host individuals on the plant; (iii) prey or host acceptance, examining individual hosts or prey in the environment to determine whether to feed on or parasitize it; and (iv) prey or host suitability, the ability of the parasitoid to develop on or within the host or the predator to feed on the prey. Biological Control in Relation to Other Pest Management Approaches The goal in pest management is to reduce a pest’s density to a lower density than would otherwise occur. Fluctuations in density are expected to occur over time, which may be either small or large. Ideally, the average density remains below the level that causes economic injury. However, the degree of biological control achieved is not always sufficient to provide economic pest suppression. The term strategy describes the long-term plan or theoretical framework of an operation. The term tactics describes the methods used to 919 920 C Classical Biological Control attain or fulfill that strategy. There are several strategies for managing pests, including: exclusion or quarantine of foreign pests, eradication, suppression of pest populations by plant resistance, biological control or chemical control, and integrated pest management (IPM). Within each strategy, there are various methods or tactics employed. Exclusion or quarantines can prevent or delay the introduction of foreign pests into a new geographic region. Eradication of foreign pests by means of pesticide applications, release of sterile males, or removal of suitable host plants is feasible in some circumstances. Plant resistance can provide substantial to partial suppression of many insect or mite pests, but resistant plant varieties are not available for all pests. Furthermore, insects and mites can evolve resistance to plant resistance mechanisms. Thus, each strategy is valuable but may be limited in scope. Classical biological control can provide effective suppression of many invasive insects, mites and weeds. However, it is rare that all invasive pests can be controlled by the importation and release of natural enemies in classical biological control programs. Nor is chemical control able to suppress all pests because resistance to pesticides and concerns about damage to the environment and health hazards are increasing. As a result, integrated pest management is an increasingly important approach; it involves deploying several approaches, perhaps including the use of transgenic (pest resistant) plants, releases of sterile male insects, cultural controls, and release of pheromones (chemicals used to communicate between individuals within a species, such as mating pheromones), in a harmonious manner to control pests. Classical biological control should always be considered when a new pest invades because classical biological control generally is compatible with nonchemical management tactics in IPM such as plant resistance, cultural controls, and a variety of biorational methods. Biorational pest management methods include tactics such as pest mating disruption by release of pheromones, disruption of normal development of pests after application of insect hormones, or applications of antifeedant materials. Techniques that are compatible with the use of biological control, or have little impact on natural enemies, are often considered biorational. Under many circumstances, pest managers will need to employ multiple tactics to achieve economic suppression of all the pest populations. Tactics used in IPM programs include plant resistance, biological control, chemical control, cultural controls, or biorational controls. How should the pest manager prioritize the pest management tactics to be evaluated and employed? One principle should be that all tactics considered should be examined for their effects on natural enemies. The conceptual basis for organizing an IPM program with biological control as a key component was spelled out over 45 years ago. That project, designed for California alfalfa, demonstrates some of the concepts and complexities of creating such programs. The spotted alfalfa aphid, Therioaphis maculata, invaded California and was detected in 1954. The aphid spread rapidly throughout the state, causing millions of dollars of crop loss damage. Shortly after the aphid became established, research was initiated to find or develop varieties of alfalfa resistant to the aphids; to develop a classical biological control project; and to identify pesticides that would control this pest at a reasonable cost. An important component of the IPM program included the introduction and establishment of the spotted alfalfa aphid parasitoids Praon pallitans and Trioxys utilis in a classical biological control project. However, classical biological control was combined with other tactics to achieve effective pest management in alfalfa. A variety of alfalfa was identified that was able to tolerate feeding by the aphid and several pesticides were found that controlled the aphids. Analysis of the effects of insecticide treatments on a complex of native predators, as well as the introduced parasitoids Praon pallitans and Trioxys Classical Biological Control utilis, indicated that parasitoids of the spotted alfalfa aphid could survive many pesticides if the parasitoids were in the pupal stage when treated. Importantly, because the aphid was not the only alfalfa pest and the alfalfa caterpillar Colias eurytheme had to be controlled as well, a polyhedrosis virus was found to be effective in controlling the alfalfa caterpillar either alone or in combination with a selective chemical insecticide. Monitoring was recognized to be a key component in the program. Population levels of the alfalfa caterpillar and its parasitoid, Apanteles medicaginis, were monitored regularly and chemical control was recommended only if the pest: parasitoid ratio was unfavorable. Thus, both the aphid and the caterpillar could be controlled without disrupting control of the aphid by natural enemies. This project laid out a number of concepts that remain central to designing an effective IPM program in which biological control is a central component. This study defined integrated control as “…applied pest control which combines and integrates biological and chemical control…,” and emphasized that chemical control should be used only as necessary and in a manner which is least disruptive to biological control, cautioning that when “…chemicals are used, the damage from the pest species must be sufficiently great to cover not only the cost of the insecticidal treatment but also the possible deleterious effects, such as the harmful influence of the chemical on the ecosystem,” thereby introducing economic and ecological considerations into the pest management equation. Thus, biological control and chemical control were shown to be potentially complementary or, with adequate understanding, made to augment one another. This project also articulated an important principle: the ideal pest suppression tactic is not one that eliminates all individuals of the pest while leaving all of the natural enemies. Pest elimination would force the host- or prey-specific natural enemies to leave the treated area or starve. The goal should be to suppress pest populations rather than eliminate them. C Evaluating Classical Biological Control Programs The degree and quality of evaluations of classical biological control programs vary dramatically. In some cases, detailed documentation has been provided (for example, the cassava mealybug project), but in other cases few records were kept. Classical biological control programs can be difficult to evaluate; sometimes the results are so spectacular that assessment appears to be unnecessary. At the least, however, assessments of pest status “before” and “after” need to be made, although such evaluations provide only circumstantial evidence that natural enemies are effective. Designing controlled experiments to document the effectiveness of classical biological control is particularly difficult when there are no untreated plots because natural enemies have dispersed rapidly. Also, low pest populations are difficult to monitor. When no reduction in pest populations occurs, it is easy to assume that the natural enemies were ineffective, although the natural enemies may, in fact, be providing some degree of suppression. Partial suppression is even more difficult to evaluate; natural enemies often behave differently at high and low host or prey densities. Identifying the reasons for changes in pest population density is difficult because natural enemies are but one of the mortality factors influencing populations of pests. Both biotic and abiotic factors influence pests and in many crops several to many species of natural enemies influence pest populations, but unraveling the impact of each is difficult. Even the simplest ecosystem is sufficiently complicated that population models developed to describe them are not easily tested in the field. Two questions are often asked when evaluating natural enemies: (i) are natural enemies controlling a pest, and (ii) how is the control achieved? Three major approaches are employed to answer the first question. These may be used either singly or in combination. Research efforts to answer the second question are more complex. 921 922 C Classical Biological Control Exclude, Eliminate, or Reduce Natural Enemies Several exclusion techniques have been employed to demonstrate that one or more natural enemies can control a pest population. A branch, tree, or other whole plant can be isolated to prevent movement of natural enemies into the system. Isolation can be achieved by hand picking, providing sticky barriers for nonflying natural enemies, or by cages. The size of mesh on cages can be modified to exclude different natural enemies based on size. Evaluation of natural enemies by exclusion has been most useful when combined with other evaluation methods such as behavioral observations or population sampling. Unfortunately, none of these techniques is completely satisfactory. Cages may alter the microclimate (light intensity, temperature, humidity and wind speed) and this change can influence the effects of the natural enemies. For example, cooler temperatures can reduce the growth and activity rates of pests or natural enemies. Few have the time and patience to hand pick natural enemies, and the area which can be manipulated by this method is relatively small. Most natural enemies are able to fly over sticky barriers. It is usually difficult to identify which members of the predator or parasitoid complex are essential for the suppression of the pest population unless the complex consists of one or a few easily segregated species. Natural enemies can be eliminated by application of pesticides that are nontoxic to the pest and, if an outbreak occurs subsequently the natural enemy or natural enemies can be assumed to have been controlling the pest. This approach was accidentally employed when effective control of the cottony cushion scale by the Vedalia beetle was disrupted by application of DDT; this pest has been under excellent control for nearly a century and the control agents have been effective when introduced elsewhere. However, relatively few pesticides are nontoxic to pests, and subtle sublethal effects can alter the pest’s response. Natural enemies can be added to one plot and not to another and changes in pest density in the release site can be attributed to the effects of the natural enemies. Likewise, prey or hosts can be added to a field plot and the efficiency of natural enemies can be estimated by changes in pest density. Direct observation of predation is useful in identifying prey and predator species; observations reveal where and when a predator searches, which is useful in designing a sampling scheme. Direct observation requires no manipulation of the environment and pests or natural enemies can be added or removed to determine the responses of the natural enemy to changes in pest density. Unfortunately, this method is time consuming and difficult to employ if the natural enemy is cryptic, active only at night, or easily disturbed. A variety of biochemical methods also have been employed to determine whether predators are preying on specific prey, including the enzymelinked immunosorbent assay (ELISA), precipitin tests, polyacrylamide gradient gel electrophoresis, and prey marking by labels. Correlation Another approach is to correlate the damage exerted by the pest, or the crop yield, with natural enemy population levels. If high natural enemy populations are correlated with low damage levels or high crop yields, the natural enemies may be providing effective pest suppression. However, correlation is not causation and other changes in crop management practices such as crop cultivar or cultural methods may influence the amount of damage inflicted or the amount of crop yield. Ideally, blocks with the natural enemies of interest are compared to blocks lacking them. However, if the natural enemies are highly mobile, such comparisons may be possible only for a very short period of time. Modeling There are many kinds of models (including mathematical, statistical, simulation, and analytic), and Classification many uses to which models can be put. Computer models have been developed which attempt to forecast and understand pest and natural enemy populations. Some models include crop-pest-natural enemy interactions with the goal of understanding the role of natural enemies in regulating pest densities. C classical biological control programs directed against invasive insect, mite and weed pests could result in reduced pesticide use, reduced ground water contamination by pesticides, reduced negative effects on nontarget organisms from pesticides, reduced pesticide residues on food, reduced crop production costs, improved control of pests, and increased farm worker safety due to reduced pesticide use. Risk Assessments Classical biological control in recent years is receiving increased scrutiny regarding possible environmental risks associated with the importation and release of foreign natural enemies. Claims have been made that parasitoids and predators released into Hawaii have had a detrimental effect on native butterflies and moths. Unfortunately, it is not clear that the observed changes in native insect populations can be attributed to classical biological control because the critics failed to discriminate between the effects of habitat destruction, pesticide use, and the possible negative effects of released arthropod natural enemies. The release of the tachinid parasitoid Compsilura concinnata in the classical biological control program directed against the gypsy moth is thought to have had negative effects on native populations of Lepidoptera, including the beautiful native silk moths. Because C. concinnata is known to attack over 200 species of Lepidoptera, it is unlikely to be considered suitable for release under current risk assessments in classical biological control programs. Practitioners of biological control are convinced that classical biological control of arthropod pests or weeds is environmentally safe and low risk if carried out by trained biological control specialists. Concerns about preservation of native flora and fauna have led some to recommend restrictions on the importation of all foreign species. During the debate on the potential negative effects of classical biological control, it should be remembered that the use of natural enemies in References Clausen CP (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. Agricultural handbook 480. U.S. Department of Agriculture, Washington, DC DeBach P (ed) (1964) Biological control of insect pests and weeds. Reinhold, New York, NY DeBach P, Rosen D (1991) Biological control by natural enemies, 2nd edn. Cambridge University Press, Cambridge, UK Frank JH, McCoy ED (1992) The immigration of insects to Florida, with a tabulation of records published since 1970. Fla Entomol 75:1–28 Herren HR, Neuenschwander P (1991) Biological control of cassava pests in Africa. Ann Rev Entomol 36:257–283 Huffaker CB (ed) (1971) Biological control. Plenum Press, New York, NY Sailer RI (1983) History of insect introductions. In: Wilson CL, Graham CL (eds) Exotic plant pests and North American agriculture. Academic Press, New York, NY, pp 15–38 van Driesche RG, Bellows TS Jr (1996) Biological control. Chapman & Hall, New York, NY Classification In sampling, this refers to a sampling plan that classifies population density as being either above or below some predetermined level (e.g., economic threshold), or belonging within some density class (e.g., low, medium, high). Commonly used in pest management decision making application (contrast with estimation). In systematics, a natural arrangement of taxa that organizes like organisms into categories. Membership in groups traditionally has been based on structural features, but also biological 923 924 C Classification features, and increasingly on molecular features. Sometimes classification is considered “artificial,” because the classification is based on features that are convenient to see or to score, but have no phylogenetic significance. In contrast, “natural” classifications systems rely on features that are shared due to common evolutionary descent. The principal categories used in classification of insects, in descending (most inclusive to least) order, are: Phylum Class Subclass Infraclass Series Superorder Order Suborder Infraorder Family Subfamily Tribe Genus Species In practice, all these categories are not often used; the most commonly used taxa are class, order, family, genus and species. Other categories also exist; for example, the class Insecta is sometimes placed in the superclass Hexapoda and the superphylum Ecdysozoa, and related families are often grouped into superfamilies. The subclass Pterygota is sometimes divided into two divisions, consisting of the hemimetabolous orders and the holometabolous orders. Possibly the only level that can be assessed objectively is the species. Species are grouped into genera, genera into families, and so forth, but taxonomists differ in the importance of characters used to cluster the taxa, so different arrangements are possible. The names of most orders end in – ptera; of families in – idea; of subfamilies in -inae, and of tribes in – ini. The classification of insects is often debated, but a common arrangement and the derivation (from Greek or Latin) for the class Insecta follows. The order names generally are logical if you consider the appearance of the insects in that group. Perhaps the only obscure name is Zygentoma, which was introduced by Carl Börner, in 1904. He viewed these insects to be an evolutionary “bridge” or connection between the apterygote (wingless) and pterygote (winged) insects, hence the name. Subclass Apterygota: Greek a (without) = pteron (wings) Order Archeognatha: Greek archaios (primitive) + gnathos (jaw) Order Zygentoma: Greek zyg (bridge) + entoma (insect) Subclass Pterygota: Greek pteron (wing) Infraclass Paleoptera: Greek palaios (ancient) + pteron (wing) Order Ephemeroptera: Greek ephermeros (shortlived) + pteron (wing) Order Odonata: Greek odon (tooth) (referring to the mandibles) Infraclass Neoptera: Greek neos (new) + pteron (wing) Series Exopterygota: Greek exo (outside) + pteron (wing) Superorder Plecopteroidea Order Plecoptera: Greek plecos (plaited) + pteron (wing) Order Embiidina: Latin embios (lively) Superorder Orthopteroidea Order Phasmatodea: Latin phasma (apparition or specter) Order Mantodea: Greek mantos (soothsayer) Order Mantophasmatodea: from Mantodea + Phasmatodea Order Blattodea: Latin blatta (cockroach) Order Isoptera: Greek iso (equal) + pteron (wing) Order Grylloblattodea: Latin gryllus (cricket) + blatta (cockroach) Order Orthoptera: Greek orthos (straight) + pteron (wing) Order Dermaptera: Greek derma (skin) + pteron (wing) Order Zoraptera: Greek zoros (pure) + a (without) + pteron (wing) Superorder Hemipteroidea Order Psocoptera: Latin psocos (book louse) + Greek pteron (wing) Order Hemiptera: Greek hemi (half) + pteron (wing) Classification Order Thysanoptera: Greek thysanos (fringed) + pteron (wing) Order Phthiraptera: Greek phtheir (louse) + a (without) + pteron (wing) Series Endopterygota: Greek endo (inside) + pteron (wing) Superorder Neuropteroidea Order Megaloptera: Greek megalo (large) + pteron (wing) Order: Raphidioptera: Greek raphio (a needle; referring to the ovipositor) + pteron (wing) Order Neuroptera: Greek neuron (nerve) + pteron (wing) Superorder Coleopteroidea Order Coleoptera: Greek coleos (sheath) + pteron (wing) Order Strepsiptera: Greek strepti (twisted) + pteron (wing) Superorder Panorpoidea Order Mecoptera: Greek mecos (length) + pteron (wing) Order Trichoptera: Greek trichos (hair) + pteron (wing) Order Lepidoptera: Greek lepido (scale) + pteron (wing) Order Diptera: Greek di (two) + pteron (wing) Order Siphonaptera: Greek siphon (tube) + a (without) + pteron (wing) Superorder Hymenopteroidea Order Hymenoptera: Greek hymen (membrane) + pteron (wing) Variations on this System of Classification Among the principal variations on this system of classification are the grouping of Phasmatodea and Mantodea into a single order, Dictyoptera; the grouping of Megaloptera, Raphidioptera and Neuroptera into Neuroptera; the splitting of Hemiptera into two orders, Hemiptera and Homoptera; the grouping of Mallophaga and Siphunculata into Phthiraptera; and the grouping of Strepsiptera with Coleoptera. Also, some additional C groups of arthropods such as the Collembola, Diplura and Protura are sometimes considered to be insects. Classification systems (Figs. 65 and 66) are based on morphological similarities (phenetics) and evolutionary relatedness (phylogenetics), as well as comparative anatomy, physiology, and behavior. Increasingly, the genetic component of insects is being used to establish relatedness. Characteristics of the Major Groups The major groups are characterized by a number of fundamental differences. The members of subclass Apterygota lack wings, possess rudimentary abdominal appendages, practice indirect insemination, and molt throughout their life, whereas the subclass Pterygota possess wings (or did at one time), generally lack abdominal appendages, practice direct insemination via copulation, and molt only until sexual maturity is attained. Infraclass Paleoptera consists of primitive insects. The wings cannot be flexed over the back when the insect is at rest. The immature stages of existing paleopterans live in aquatic habitats. The Neoptera, on the other hand, are a diverse group of relatively modern insects. They can flex their wings over the body. They display development in which the immatures are similar to the mature form (Exopterygota), or the immatures differ markedly in appearance from the adults (Endopterygota). Superorder Plecopteroidea, consisting of Plecoptera and Embiidina, is closely related to superorder Orthopteroidea. Both suborders have chewing mouthparts; complex wing venation, with the hindwings larger than the forewings; and cerci. They differ, however, in that the forewings are not thickened, and external male genitalia are lacking. The members of superorder Orthopteroidea (Polyneoptera) have chewing mouthparts, long antennae, complex wing venation, large hindwings, thickened forewings, large cerci, and nymphs with ocelli. Several orders are considered to be orthopteroids: Phasmatodea, Mantodea, 925 926 C Classification Classification, Figure 65 Diagram of the possible phylogeny of the hexapods, showing relationships among the major groups (principally insect orders) and the temporal occurrence of major evolutionary steps in insect structure and development. Mantophasmatodea, Blattodea, Isoptera, Grylloblattodea, Orthoptera, Dermaptera, and Zoraptera. In many older classification systems, they were all considered to be part of the order Orthoptera. This is a relatively primitive group. Superorder Hemipteroidea (Paraneoptera) is also a large group, consisting of the orders Psocoptera, Hemiptera, Thysanoptera, and Phthiraptera. Unlike the Orthopteroidea, they lack cerci, and have stylet-like structures associated with their mouthparts (though in Psocoptera, chewing mouthparts are preserved). Some groups are well designed for piercing the host and sucking liquids. Though this and the preceding superorders are considered to be hemimetabolous, a few members of Thysanoptera and Hemiptera are physiologically holometabolous. The superorder Neuropteroidea is holometabolous, and consists of the orders Megaloptera, Raphidioptera, and Neuroptera. Both aquatic and terrestrial forms occur in this superorder. The wings tend to bear numerous cells. Superorder Coleopteroidea consists of the orders Coleoptera and Strepsiptera. They are similar in that the metathorax is developed for flight, and bears functional wings. The forewings of the Coleoptera are reduced to hard wing coverings, and even more reduced in the Strepsiptera, to small club-like appendages. They contrast strongly in that the Coleoptera is the largest order, and Strepsiptera one of the smaller orders. Panorpoidea is another large superorder, consisting of the orders Mecoptera, Trichoptera, Lepidoptera, Diptera, and Siphonaptera. They share few common characters, however, such as a tendency for a reduced meso- and metasternum, the media and cubitus of the hind wing arise from a common stem, and the terminal abdominal segments tend to function as an ovipositor. Lastly, the superorder Hymenopteroidea consists only of the order Hymenoptera, though Classification Classification, Figure 66 A recent assessment of phylogenetic relationships within Hexapoda based on both morphological and some molecular characters (adapted from Wheeler et al., 2001, Cladistics 17:113–169). this is a very divergent, complex group. They bear numerous Malpighian tubules, unlike all other endopterygotes, which have only four to six tubules. Also, their wing venation is often greatly reduced.  Each Individual Order  Phylum  Orders  Sampling Arthropods C 927 928 C Clastopteridae Clastopteridae A family of bugs (order Hemiptera, suborder Cicadomorpha).  Bugs Claustral Colony Founding A process of colony founding in which the initial reproductives seal themselves of in cells, and proceed to rear the initial brood using nutrients obtained from their own tissues. Clavate Thickening toward the tip. This term is usually used to describe antennae with expanded tips.  Antennae of Hexapods Clavate Larva This term is sometimes used to describe a larva with an enlarged thoracic region, particularly buprestid, cerambycid, and eucnemid larvae. Clavola The antenna beyond the pedicel. The flagellum.  Antennae of Hexapods Clavus This term has several meanings, including the angular hind margin of the hemelytra in Hemiptera (Fig. 67); the club of an antenna; the knob at the end of the stigmal or radial wing veins in Hymenoptera; and the rounded or finger-like process in the male genitalia of Lepidoptera. Claw A hollow, sharp, curved organ, located at the tip of the tarsus (foot).  Legs of Hexapods Clearwing Moths (Lepidoptera: Sesiidae) danieL potter University of Kentucky, Lexington, KY, USA Adults of the family Sesiidae(formerly Aegeriidae) are called clearwing mothsbecause a part of the wings, especially the hindwings, lacks overlapping scales and is therefore transparent. The body typically is dark-colored, but most species have contrasting yellow, orange, or reddish bands or markings on the abdomen, legs, or both. Males and females often differ in coloration, and in some Clavus, Figure 67 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and membranous distally. Clearwing Moths (Lepidoptera: Sesiidae) cases the amount of clear area in the wings. Virtually all species are day-flying. The moths may be seen sipping nectar from flowers or resting on foliage on sunny days. Many adult sesiids bear a striking resemblance to wasps, especially paper wasps (Polistes spp.) or yellow jackets. Being moths, they cannot sting; however, this mimicry doubtless discourages insectivorous birds and other vertebrate predators. The moths’ hovering flight and tendency for some species to move the abdomen in a wasplike posture contributes to the deception. Sesiid larvae tunnel in living branches, trunks, root collars, or roots of trees and shrubs, and in canes and vines of woody and some herbaceous plants. Granular, sawdust-like frass usually is expelled from the site of attack. Damage to the inner bark and cambium can contribute to the decline and death of host plants. Some species are economically important pests of forest and landscape trees, or fruit crops. The squash vine borer, Melittia cucurbitae, is a pest of squash, gourds, and pumpkins. A few species induce plant galls, or feed as inquilines within galls of other insects. Most clearwing species exploit only a few closely-related species of trees, shrubs, or vines as hosts. A few, such as the dogwood borer, Synathedon scitula, attack a broad range of plants. The family Sesiidae belongs to the order Lepidoptera, suborder Ditrysia (Frenatae), and superfamily Sesioidea. Clearwing moths have a world wide distribution with about 170 genera containing more than 1000 described species. Nineteen genera and 155 species of sesiids are known from North America, including such important pests as the raspberry crown borer, Pennisetia marginata; grape root borer, Vitacea polistiformis; squash vine borer, Melittia cucurbitae; lesser peachtree borer, Synanthedon pictipes; peachtree borer, Synanthedon exitiosa; dogwood borer, Synanthedonscitula; and lilac borer, Podosesia syringae. Adult clearwings are slender-bodied, small to medium-sized moths, wingspan 1.4 to 4.6 cm. The forewings are narrow, at least four times as long as wide, with anal veins reduced. The hind wings are shorter and somewhat more broad, with all three anal veins present. The forewings fold downward C along their inner, rear margin, with a row of tiny curved spines that interlock with the fold; similar spines along the hindwing costa help to hold the wings together. The antennae are simple to bipectinate, widening gradually and then narrowing again to the tip. The larvae are ivory white or cream-colored except for a brownish, sclerotized head and lighter thoracic shield. Each thoracic segment has one pair of small jointed legs. Abdominal segments 3 to 6, and 10, have fleshy lobes (prolegs), each ending in two transverse bands of tiny hooklike crochets. Many clearwing species have a 1-year life cycle. Others require two years to complete a generation, whereas a few species have two generations per year. Winter is spent as a partially grown larva within a gallery under the bark of the host plant, or within stems, canes, or roots. Several sizes of larvae may overwinter, reflecting the fact that the eggs from which they eclosed were laid by different females over a number of weeks. Active feeding resumes in early spring. Some species pupate in late winter or spring, whereas others feed longer and pupate later in the growing season. Before pupating, the larva extends its tunnel to the bark surface except for a paper-thin cover. Pupation occurs within a cocoon made from frass and bits of bark or soil held together with silken strands. The pupal stage lasts about 3 weeks. Empty pupal skins often are left partially protruding from exit holes in the bark after the moths have emerged. Flight activity, mating, and egg-laying by a particular species usually are finished within 4 to 6 weeks after initial emergence. Adults of different species emerge at certain times during the growing season, and their flight activity often is restricted to a specific time of day. These temporal differences likely are important for reproductive isolation, especially since females of a number of species emit chemically-similar sex pheromones to attract males. After mating, females deposit eggs singly in bark crevices, often around wounds, cankers, or old larval feeding galleries. They seem to be attracted to plants that are injured or weakened by root pruning, transplant shock, insect or disease injury, 929 930 C Cleptobiosis drought, or other stress factors. Individual females typically live only about a week, during which they may lay several hundred eggs. Eggs hatch in about 2 weeks, and larvae then bore into the bark and mine in the phloem and cambium, lengthening and enlarging the tunnel as they grow. Many species later enter the sapwood. Branch dieback, limb and trunk swellings, moist sap spots on the bark, gum exudates, expulsion of larval frass, or protruding pupal skins all may indicate that borers are present. Woodpeckers are important in natural control. Ants, and in some cases field mice, moles and skunks, prey upon the pupae. Eggs, larvae, and pupae are attacked by various parasitic wasps or flies. A fungus, Beauveria sp., sometimes infects and kills the larvae. In the early 1970s, scientists identified and synthesized two major isomeric pheromone components, the Z, Z- and E, Z- isomers of 3,13octadecadien- 1-ol-acetate, from the peach tree borer and lesser peach tree borer, respectively. Subsequent field testing soon revealed cross-attraction of other clearwing species to these pure isomers, their corresponding alcohols, or to various blends of these compounds. This breakthrough allowed entomologists to learn more about the flight periods of a number of clearwing moth species, to survey local sesiid fauna, and to develop effective attractants for some of the key pest species. Traps baited with commercial synthetic pheromones are used by nursery operators and landscape managers to monitor clearwing moth activity. This helps them to fine-tune timing of control actions. Entomologists also are evaluating use of such attractants for mass trapping or mating disruption of pests such as peachtree borer in orchards. The most important management strategy is to minimize plant stress, because healthy trees, shrubs, and vines are less likely to be attacked by borers. References Eichlin TD, Duckworth WD (1988) Sesioidea: Sesiidae. In RB Dominick et al (eds) The moths of America north of Mexico. Fasicle 5.1. 176 pp Englehardt GP (1946) The North American clearwing moths of the family Aegeriidae. Bulletin 190. U.S. National Museum, Washington, DC Johnson WT, Lyon HH (1988). Insects that feed on trees and shrubs, 2nd ed. Cornell University Press, Ithaca, New York Solomon JD (1995) Guide to insect borers of North American broadleaf trees and shrubs. Agricultural Handbook 706. USDA Forest Service, Washington, DC. 735 pp Taft WH, Smitley D, Snow JW (1991) A guide to the clearwing borers (Sesiidae) of the north central United States. USDA North Central Regional Publication 394 Cleptobiosis A relationship in which one species robs the food stores, or scavenges in the refuse piles, of another species – but does not nest in association with the host. Cleptoparasite An organism that consumes the stored food of another from its nest. Cleridae A family of beetles (order Coleoptera). They commonly are known as checkered beetles.  Beetles Click Beetles Members of Coleoptera).  Beetles the family Elateridae (order Clicking by Caterpillars Although acoustic communication is well known among certain moths (mostly in the context of detecting ultrasonic cries of insectivorous bats), C Clover Mite, Bryobia praetiosa Koch (Acari: Tetranychidae) acoustic communication is widespread in Lepidoptera. Vibrational signals are used by some butterfly and moth larvae in communication with mutualistic ants, conspecifics, and predators. However, sounds made by at least 12 families, including Tortricidae, Oecophorida, Notodontidae, Saturniiidae, and Sphingidae, may be involved in defense. Saturniid and sphingid larvae produce audible (to the human ear) clicks that have been described as “cracking” or “crackling.” Closure of the mandibles produces the “click” sounds, and it follows disturbance of the larvae as may occur when the insects are grasped or pecked by birds. The clicking sound often precedes regurgitation by the larvae, and regurgitation is known to be repellent to both vertebrate and invertebrate predators.  Vibrational Communication  Acoustic Communication in Insects  Acoustic Aposematism (Clicking) by Caterpillars Reference Brown SG, Boettner GH, Yack JE (2007) Clicking caterpillars: acoustic aposematism in Antheraea polyphemus and other Bombycoidea. J Exp Biol 210:993–1005 Cloaca The rectum, a common chamber into which the anus and gonopore open; the vagina.  Reproduction  Vagina Clone A population of identical cells often containing identical recombinant DNA molecules. Also a group of organisms produced from one individual cell through asexual processes. The offspring are identical. The word may be used either as a noun or a verb. Closed Cell A cell bounded on all sides by wing veins. Clothes Moths Members of the family Lepidoptera).  Fungus Moths  Butterflies and Moths Tineidae (order Climatic Release The release of a population from climatic constraints by a favorable change in weather, allowing it to attain a population increase or outbreak. Clothodidae A family of web-spinners (order Embiidina).  Web-Spinners Climax The end point of an ecological successional sequence; the community has reached a steady state. Cline A geographic gradient in the frequency of a gene. Clover Mite, Bryobia praetiosa Koch (Acari: Tetranychidae) These clover and grass-feeding mites damage vegetation and also enter homes, becoming a nuisance.  Mites 931 932 C Club Fleas Club Fleas Members of the family Rhopalopsyllidae (order Siphonaptera).  Fleas Clubtails A family of dragonflies in the order Odonata: Gomphidae.  Dragonflies and Damselflies Clumped Distribution A distribution of organisms in which there is some aggregation of individuals that exceeds the clumping that would occur randomly. This is the most common distribution displayed by insects. Clusiid Flies Members of the family Clusiidae (order Diptera).  Flies Clusiidae A family of flies (order Diptera). They commonly are known as clusiid flies.  Flies Cluster Analysis A method of hierarchically grouping taxa or sequences on the basis of similarity or minimum distance. UPGMA is an unweighted pair group method using the arithmetic average. WPGMA is the weighted pair group method using the arithmetic average. Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae) aLLen heath AgResearch Wallaceville, Upper Hutt, New Zealand The name cluster fly (or loft fly) is given to two species of Northern Hemisphere blowflies (Calliphoridae) Pollenia rudis and P. pseudorudis that preferentially breed in earthworms of the genera Allolobophora, Eisenia (= Helodrilus) and Lumbricus. Many other members of the genus breed in earthworms, but so far as is recorded, only P. rudis and P. pseudorudis invade buildings in large numbers in autumn, achieving pest status, leaving again in spring. The identities of these flies have been confused until recently. Only in 1985 was Pollenia pseudorudis recognized as distinct from both P. rudis and P. angustigena, and the previously named P. obscura was subsumed in P. pseudorudis. Apart from New Zealand records, there is no clear indication that P. pseudorudis invades houses elsewhere in the world, because in the Northern Hemisphere and Hawaii, only P. rudis is recorded as the nuisance species, although it may just be that no effort has been made to gauge whether P. pseudorudis is present as well. It is possible that both species (and perhaps others) occur together in houses in North America, and perhaps elsewhere, as they do in the wild, but possibly because of the P. obscura synonymy no distinction has been attempted. Lofts are a common sanctuary, hence one of the common names, and the flies cling together, often in ropy clusters. They have been described as “the most frustrating of … structural insect pests.” First reports of cluster flies as a household nuisance appeared in the mid nineteenth century, although the first published mention of a fly associated with earthworms was in 1881, when Charles Darwin, in his treatise on earthworms reported an earlier observation by Perrier. Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae) In the 1930s, a link between earthworms and swine influenza was postulated, with a view that “the virus of swine influenza is a surviving prototype of the agent responsible for the great human pandemic of 1918” and that hogs and earthworms may serve as the source of future epidemics. Because of its links with earthworms, the cluster fly was regarded as a possible vector of human influenza, an hypothesis that has not been supported by subsequent research. The tribe Polleniini to which the cluster flies belong occurs in four distinct geographical groups, the Palearctic (with at least 30 species), the Nearctic and Austro-Oriental regions, each with at least eight species in the genus Melanodexia and two in Pollenia. The Australasian and Oceanian regions have three genera, Anthracomyia (which is monotypic), Dexopollenia (five species) and Pollenia (43 species, the majority in New Zealand). However, there are still a further 17 species unnamed in New Zealand designated as species “a” to species “q” inclusive. It appears that only the two Northern Hemisphere (widely distributed throughout the Nearctic and Palearctic) species, P. rudis and P. pseudorudis, congregate in houses, although further work may alter this view. Both species have been intercepted in New Zealand, but only P. pseudorudis, which reached New Zealand in the early to mid-1980s, appears to have established and, over the next 20 years or so, subsequently dispersed throughout both main islands. In the Holarctic, a P. rudis species group is recognized, and contains six species of Pollenia: P. angustigena, P. rudis, P. pseudorudis, and three exclusively in the Palearctic: P. hungarica (Central Europe and southern parts of Scandinavia), P. longitheca (eastern Mediterranean) and P. luteovillosa (Algeria and Morocco). There is a seventh species of doubtful status. The adult flies (Fig. 68) are slow-flying, easilycaught insects; they are active in spring and summer in pasture and gardens, and then, as ground temperatures begin to drop in autumn (fall), the flies move towards shelter, usually houses or other C Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae), Figure 68 A recently emerged cluster fly. Normally the fly at rest has the wings folded back more than is shown here, and they obscure the abdomen (photo courtesy of Lynnette Schimming). buildings that act like large flytraps. In the afternoon they settle on the upper parts of walls and on roofs, facing towards the setting sun. As the sun sets, the flies crawl into any crevice and into roof spaces, and may enter rooms, using drapes, pictures, etc., as hiding places. For a few days, the flies will go back outside, and then return at night, but this behavior eventually ceases, except if there is a spell of mild weather during winter. Mild weather will break the fragile hibernation of the flies and they will become sluggishly active. Outside of human habitations, the overwintering locations of cluster flies are not well known, although they have been recorded from the tunnels made by beetles in timber and fungi and also in animal burrows. The flies return to the outside in spring, again causing a nuisance as they do so. The cluster fly P. rudis is frequently seen in very large numbers in spring moving over moist grass. The female deposits a batch of eggs on the soil surface and then moves some distance away and deposits another batch, about 100–130 eggs in all. Three days later the eggs hatch and the larvae descend into the soil by following natural pore spaces, such as gaps between plant stems and soil and worm burrows, although not if the latter are blocked by casts. It seems the larvae locate a host 933 934 C Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae) by a random locomotion through the soil pores rather than following any product of the host. Some species of earthworms emerge from their burrows at night and move freely about on the surface, and after rain many worms can be seen above ground. This surface movement could be a mechanism that would improve the potential for cluster fly larvae to encounter potential hosts. Adult flies are on the wing from early spring in the Northern Hemisphere (February, March) to late autumn (October, November). They are sometimes attracted to horse and human feces, but are more attracted to meat and fruit, with banana reported to be especially good bait. Larvae enter the earthworm through almost any point in the body wall, but mostly on the dorsal side and sometimes through spermiducal and other pores. Larvae must penetrate a worm within 3 days after hatching if they are to survive. Penetration is attempted under the influence of a substance present in both the slime and coelomic fluid, which has been named “penetration-inducing factor.” They have been reported to re-emerge after a short period to produce an opening through which they protrude the posterior spiracles. It has been reported that during the first two stadia the larva acts as an internal parasite, and during the last it feeds on the host from the outside. Larvae may also leave the host and commence feeding on healthier parts of the same worm or on a fresh worm. Up to seven larvae may occur in a single worm, although a single larva will feed on as many as three earthworms, resulting in larger pupae than usual. The larvae can eventually eat the entire body of the worm and pupate in the soil nearby. Development times vary with climatic conditions. In Canada, total development time is 25–30 days at 23°C, of which 11–14 days are spent in the pupal stage. There are three or four generations per year. In Europe, after wintering in a dormant state in the body cavities of earthworms, the larvae molt twice over about a 20 day period and then pupariate outside the host. The pupal stage typically lasts from 32 to 45 days, although it can be as short as 7 days at high temperatures (e.g., 27°C). A number of species of worms are variously reported as hosts. In Europe, cluster flies attack Allolobophora chlorotica, A. (latterly Eisenia formerly Helodrilus) rosea, and L. terrestris, whereas in North America both of the Allolobophora spp. as well as A. caliginosa are parasitized. But A. rosea and A. chlorotica seem to be the most common hosts in North America; both are surface-dwelling species occurring mainly in the top 10 cm of the soil. In general, attempts to experimentally infest worms with P. rudis larvae have met with mixed success and only A. rosea was infested in all attempts. It is possible to rear P. rudis in the laboratory using A. rosea as a host. Parasitism in the field in North America is said to occur only in A. chlorotica and A. rosea, although other species (A. caliginosa, L. terrestris, L. rubellus, Eiseniella tetraedra, Eisenia foetida, Octalasium lacteum) in a crushed form will support first instar larvae. Studies in Hungary showed that P. rudis, P. pseudorudis and P. hungarica could be bred out of A. rosea. The sexes of overwintering flies are approximately equal in numbers and the abdomen of flies at this time is full of fat globules, possibly the remnants of larval fat bodies. The following spring, the flies possess a shrunken or desiccated appearance because the fat has been used up during the winter. It has been reported that there are important differences in the life history of P. rudis in Europe compared with North America, with the first instar larva as the over-wintering stage in Europe, rather than the adult as in North America. In addition, there is only one generation a year reported from Europe. However, apparently there are three species in the “rudis” species complex in North America and the life cycle of each may differ. Discrepancies between North American and European reports with regard to cluster fly biology (and coincidentally larval morphology) may be because early work may not apply to any rudis group member and it is possible that the authors worked with different species. Enlargement of the distribution of P. rudis into the Oceanic and Australasian regions has occurred relatively recently, with Hawaii recording its first flies in 1955, with A. caliginosa serving Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae) as the host. Pollenia rudis was intercepted at the New Zealand border in 1981. This species does not appear to have broached the border, as no specimens have been subsequently found in the wild. However, in 1984 a species soon to be recognized as P. pseudorudis was found in a house in Auckland, New Zealand, and over the next 19 years spread throughout the country, but up to 2007 no worm hosts have yet been identified. During the first 12 years after its discovery in New Zealand, P. pseudorudis populations established themselves throughout the North Island, being more numerous in some years and districts that at other times. Simultaneously, in 1996 with the end of this initial expansion period, the first South Island populations were recorded. Further expansion in the South Island took place over the next 7 years to the southernmost districts. It appears that P. pseudorudis is not found in either Hawaii or Australia at present, although P. rudis occurs in the former. The clustering habit of adult flies would provide an opportunity for them to collect in shipping containers and facilitate their trans-hemispheric movement. It might be thought that the large numbers of cluster flies appearing each year would have a detrimental effect on local earthworm faunas. In Europe and North America, four species of earthworms are used as hosts: A. chlorotica, A. caliginosa, A. rosea and L. terrestris. However, there have been no reports of notable reductions in earthworm numbers or any horticultural consequences. Given the enormous numbers of earthworms in pasture, variously estimated from 70,000 to around 10 million per hectare, there would seem to be enough to spare for cluster fly population maintenance. Apart from this unresolved question of whether earthworm numbers suffer as a consequence of cluster fly activity, the insects evoke strong emotional responses in humans and present a major housekeeping nuisance. If swatted they leave greasy spots. There can also be economic effects if businesses decide to close because of fly activity, and such closures have been recorded. In addition, there is a potential public C health nuisance, and a town water supply contained in a large wooden reservoir tank in New Zealand had to be drained after cluster flies settled inside and an excess of fecal coliform bacteria was found in the water. Invasion of a hospital in Europe provoked concern and although no bacteriologically sterile flies could be found, an enrichment culture technique had to be used to provide sufficient bacteria for identification. This suggests that cluster flies may be a low health threat. Keeping cluster flies out of houses can be difficult, although finding possible entry points and blocking them with appropriate materials such as wire mesh can work. The flies are capable of squeezing through very small crevices, however, and even the most assiduous search may miss openings. The principal control method favored by pest control firms involves insecticide application on outside walls of buildings, fogging of interiors, such as roof spaces, and even treatment of vegetation and soil. Overuse of insecticides both inside and outside is not a particularly safe option for either humans or other animals. Simply vacuuming flies up as they enter houses is safe and effective, especially because flies killed by insecticides would have to be cleared up in some manner in any event. References Heath ACG, Marris JWM, Harris AC (2004) A cluster fly, Pollenia pseudorudis Rognes, 1985 (Diptera: Calliphoridae): its history and pest status in New Zealand. NZ J Zool 31:313–318 Oldroyd H (1964) The Natural history of flies. Weidenfeld & Nicolson, London Rognes K (1987) The taxonomy of the Pollenia rudis speciesgroup in the Holarctic region (Diptera: Calliphoridae). Syst Entomol 12:475–502 Thomson AJ (1973) The biology of Pollenia rudis, the cluster fly (Diptera: Calliphoridae). I. Host location of first-instar larvae. Can Entomol 105:335–341 Thomson AJ, Davies DM (1973) The biology of Pollenia rudis, the cluster fly (Diptera: Calliphoridae). II. Larval feeding behaviour and host specificity. Can Entomol 105:985–990 Yahnke W, George JA (1972) Rearing and immature stages of the cluster fly (Pollenia rudis) (Diptera: Calliphoridae) in Ontario. Can Entomol 104:567–576 935 936 C Clypeofrontal Suture Clypeofrontal Suture The suture marking the division between the clypeus and the epicranium. The clypeal suture. Clypeus A part of the head below the front (Fig. 69) to which the labrum is attached.  Head of Hexapods Coarctate Larva This term usually is applied to the third phase of hypermetamorphic development in Meloidae. At this point in development, which corresponds approximately to instar six, the larva typically is strongly sclerotized, immobile, and the legs are greatly reduced. Sometimes it is used to describe a larva that is similar to the puparium of a fly, in which the cuticle of the preceding instar is not completely shed but remains attached to the posterior end of the body. Coarctate Pupa A pupa that is enclosed in the hardened shell formed by the last larval cuticle. This is usually called a puparium. Coccidae A family of insects in the superfamily Coccoidae (order Hemiptera). They sometimes are called soft scales, wax scales, and tortoise scales.  Bugs  Scale Insects and Mealybugs Coccinellidae A family of beetles (order Coleoptera). They commonly are known as ladybird beetles.  Beetles Coccoidae A superfamily of insects in the order Hemiptera. They sometimes are called scale insects, though Clypeus, Figure 69 Front view of the head of an adult grasshopper, showing some major elements. Cockroaches (Blattodea) mealybugs also are found in this superfamily. This superfamily contains such families as Margarodidae, Ortheziidae, Kerridae, Coccidae, Aclerididae, Cryptococcidae, Kermesidae, Asterolecaniidae, Lecanodiaspididae, Cercoccidae, Dactylopiidae, Diaspididae, Conchaspididae, Phoenicococcidae, Pseudococcidae, and Eriococcidae.  Scale Insects and Mealybugs  Bugs Cochineal Insects Members of the family Dactylopiidae, superfamily Coccoidae (order Hemiptera).  Bugs  Scale Insects and Mealybugs  Lacquers and Dyes from Insects Cockerell, Theodor Dru Alison Theodor Cockerell was born in London on August 22, 1866, and became interested in natural history at an early age with parental encouragement. This interest extended to insects and slugs and snails and was further encouraged after the death of his father by a trip to Madeira. Upon finishing school, he was employed by a flour company, but developed tuberculosis. At the age of 20 he sailed to the United States and journeyed to Colorado to find a climate that would cure his illness. That climate was beneficial and his health recovered. In Colorado he worked on a catalogue of the flora and fauna there, but returned to London in 1890 to work in the British Museum (Natural History). He was invited by Alfred Russel Wallace to help in the preparation of a new edition of the latter’s book “Island Life.” In 1891 he was appointed Curator of the Public Museum (now Institute of Jamaica) in Kingston and became interested in scale insects. Unfortunately, his tuberculosis had returned by 1893. Fortunately for him, he was able to trade jobs with C.H.T. Townsend of the New Mexico College of Agriculture, and he moved to Las Cruces to become entomologist at the Experiment Station and C Professor of Entomology and Zoology. But there his wife died giving birth to a second son, who died at the age of eight, the first son having died in infancy in Jamaica. Later, he took an American wife, Willmatte. In New Mexico, he developed an interest in wild bees, studied their taxonomy and behavior, and eventually published description of 5,480 new names for species, subspecies and varieties, together with 146 new names for genera and subgenera. In 1903 he returned to Colorado and took a position as Curator of the Museum of Entomology at Colorado College. Here, he continued his work on bees but also developed an interest in paleoentomology and paleobotany and numerous other natural history subjects, and even art, poetry and politics. He traveled to Europe, Japan, Thailand, India, Siberia, Australia, Morocco and other parts of Africa, Canada, and Honduras. Upon retirement, he divided his time between Colorado and southern California. His published works amount to over 3,000 items, in which he described over 7,000 species of plants and animals, extant and fossil. He died on January 26, 1948, in California. Reference *Mallis A (1971) Theodore Dru Alison Cockerell. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 357–362 Cockroaches (Blattodea) John L. Capinera University of Florida, Gainesville, FL, USA The cockroaches (also called roaches) are members of an ancient order of insects. The order name is derived from the Latin word blatta, or cockroach. They are closely related to the praying mantids (Mantodea), and often are grouped with them (as suborders) to form the order Dictyoptera. Though the mantids evolved from the cockroaches, they are a specialized group of predatory insects that warrant individual recognition. Termites 937 938 C Cockroaches (Blattodea) (Isoptera) can also be placed in the order Dictyoptera, and are considered by some to be social cockroaches. The order name for cockroaches sometimes is given as Blattaria. Classification About 4,000 species are found throughout the world, though most are tropical. They usually are grouped into six families. Order: Blattodea Superfamily: Blattoidea Family: Blattidae Superfamily: Blaberoidea Family: Polyphagidae Family: Cryptocercidae Family: Nocticolidae Family: Blattellidae Family: Blaberidae Characteristics The cockroaches are small to large in size, measuring from about 2 mm to over 60 mm. The largest, Megaloblatta blaberoides, measures 100 mm when the tegmina are included in the measurement, and has a wing span of 185 mm. They are flattened, oval, and often dark or reddish brown, though some are black or green. Species that live under bark or rocks sometimes are extremely flattened, though this degree of compression also is useful for defending against attack by ants because the cockroaches cling so tightly and closely that the ants cannot get beneath them to their more vulnerable under-surface. The head is concealed (when viewed from above) by the pronotum. Compound eyes are usually present and well-developed, though absent in some cavedwelling species and myrmecophiles. The filiform antennae are long. They possess chewing mouthparts. Both males and females usually bear two pairs of wings, though the front wings are thickened. Both short-winged and wingless species are known. The cursorial legs are not greatly modified, and only moderately long, but some species run quite rapidly. There are five tarsal segments. Cerci are present, though varying in length, and consisting of one to five segments. Some species burrow, and these are among the heaviest of the cockroaches. Megoblatta rhinoceros, for example weighs over 30 g. Burrowers are often wingless, heavy-bodied, hard, and bear spines. On the other end of the scale, some cockroaches inhabiting the nests of social insects (mostly ants and termites) are only 2.7 mm long. Indeed, it is surprising to most people that small species predominate, but they are easily overlooked. The accessory glands of female cockroaches produce oothecae, or egg cases, which contain few to many eggs. The eggs are usually are arranged in two rows, and in many cases the ootheca is surrounded by a thick, protective covering. The ootheca may be inserted into a protected location or just dropped by the female in the general environment in which she lives, but others carry the ootheca until the eggs are ready to hatch. Cockroaches in the family Blaberidae retain their eggs internally and give birth to living young. Sexual dimorphism is sometimes quite pronounced. The sexes are so different in some species that they were originally described as separate species. These differences suggest that competition to win a mate is quite keen. The abdomen of the female, not surprisingly, is more elongate. As with other hemimetabolous insects (incomplete metamorphosis), the immatures resemble the adults in general appearance, differing primarily by the absence of the tegmina and wings in immatures (nymphs). Immatures also have poorly developed genitalia, and lack characters useful for identification. Some are colored quite differently from the adult stage. Although we tend to think of cockroaches as nocturnal, some are active during the day. Not surprisingly, their color is quite different. Day-active cockroaches often sport bright colors: some are brightly colored; others are aposematically colored because they are chemically defended; still others mimic other species (Batesian mimics). They commonly mimic beetles, including such brightly Cockroaches (Blattodea) colored species as ladybird beetles (Coccinellidae), carrion beetles (Silphidae), and metallic wood-boring beetles (Buprestidae). Cave-dwelling species are typically depigmented, and have a thin cuticle, elongated appendages and loss of vision. The cockroaches are basically terrestrial insects, though some semi-aquatic species are known. Flight is not well known for most species, but most seem to fly poorly, despite the presence of large wings. The presence of wings is the primitive condition, and wings have been reduced or lost in many taxa. Those living below-ground or in burrows, galleries or crevices are most prone to winglessness, as are those living in stable habitats. The absence of wings in the adult form of some species is associated with retention of juvenile characters (paedomorphosis). Habitats and Food Cockroaches are found in nearly all habitats, from the forest canopy to the soil, within burrows and caves, within logs and detritus, and in nests of social insects, rodents, reptiles and birds. They are most numerous in the hot, humid tropics, between 30°N and 30°S. They are also more common at sea level (where temperatures are warmer) rather than at high altitudes. In the tropics, there is considerable vertical stratification on trees at night, with most species returning to the ground litter during the day. The species that inhabit the most elevated portions at night are also the best fliers; not surprisingly, the flightless species are lowest on the trees. Favored habitats of cockroaches are dark, humid, poorly ventilated, and cramped or crowded. Thus, they are commonly found with loose substrate such as leaf litter and clods of soil. Some force themselves into small voids such as spaces under bark, within the bases of palm trees, or under rocks. Only a few excavate burrows in wood or compacted soil, but rotting logs are popular habitats. Caves may or may not be populated. The presence of vertebrate guano maintains large numbers of cockroaches in caves. Despite the C aforementioned preferences, some cockroaches have not only managed to exploit desert environments, but have become some of the most abundant mesofauna present. Many desert dwellers live beneath the sand, at least for a portion of the day. They also take advantage of natural burrows created by rodents and vertebrates. Only a few species actually inhabit the water, though many favor the water-vegetation interface. Cockroaches are usually thought of as scavengers or omnivores. However, this mostly reflects our knowledge of domiciliary pest species, plus the tendency of cockroaches to behave abnormally when constrained to the laboratory environment. Most display some degree of preference, though they are by no means highly selective (Table 14). For example, in a natural environment such as a tropical rain forest, there seem to be three dominant night-time feeding strategies: they forage on the forest floor, feeding on decaying vegetation but also ingesting nematodes, fungi, insects, and other invertebrates; they emerge from crevices and tree holes, ascend to a preferred height in the trees, and feed on material that has fallen onto the leaves or is growing on the leaves; they emerge from harborages and flit about the vegetation irrespective of height, scraping algae and other microvegetation from the tree foliage, bark, or elsewhere. Cockroaches search actively for food but also use olfaction to locate suitable food. They usually consume the food as they find it, though some species will transport food elsewhere. They can learn where food is located and return after an absence. Juvenile cockroaches require more nitrogen than do older cockroaches so they initially favor meals from animal or microbial sources. Females consume more than males. Generally cockroaches are not thought of as plant pests, but there are important exceptions. In a closed environment such as a greenhouse, any species can be damaging if they become sufficiently abundant. Others, such as Pycnoscelus surinamensis and Blatella asahinai, commonly are associated with plant injury, even under field conditions. Cockroaches are quite tolerant of starvation, living from five to over 40 days without 939 940 C Cockroaches (Blattodea) Cockroaches (Blattodea), Table 14 Diet of four species of Parcoblatta based on nocturnal observations (after Gorton REJ (1980) The University of Kansas Science Bulletin 52:21–30) Food source P. pennsylvanica P. uhleriana Mushrooms + + P. lata + Cambium + Flower petals + Moss + Sap + Cercopid spittle + Live insects + Bird feces Mammal feces P. virginica + + + Mammal cartilage water and food. Water is a more critical resource, and they can survive longer without food than without water, perhaps 60–90 days. Dead conspecifics and shed cuticles are a common food resource; not surprisingly, biting and cannibalism are reported. The digestive system of cockroaches is well equipped with a diversity of microbiota. The resident fauna and flora, plus the microbes ingested along with food, comprise a rich microbial “brew” that enhances fermentation. They also contribute cellulases, though endogenous cellulases also occur. It has been postulated that cellulose ingestion indirectly benefits cockroaches by fueling their microbial gut inhabitants, with the microbes and their products being the primary source of nutrition. The significance of microbes in the gut of cockroaches is seen in the regular coprophagous (feces-feeding) behavior of young cockroaches, which provides an important inoculum for the young insects. The wood-feeding cockroaches in the family Cryptoceridae are the link to termites. Not surprisingly, digestion is about the same in cryptocerids and termites, the principal difference between the two groups being the evolution of a higher level of sociality in termites. Fecal pellets are attractive to cockroaches. Fecal chemicals function as short-distance attractants and arrestants. Cockroaches may aggregate + in locations with these chemicals. The response is not species specific: they prefer the chemicals produced by their own species, but will aggregate at sites contaminated by other species, including distant relatives. Due to their lack of specificity, the chemicals are not usually considered to be aggregation pheromones, but they clearly are a form of behavior-eliciting chemicals. Other factors such as acoustic, tactile, visual and olfactory stimuli also influence aggregation, as do environmental stimuli such as light, humidity, temperature, and air movement. Parental Care Most cockroaches display some form of parental care, though the degree of care differs (Table 15). Care of eggs is most widespread; carrying and hiding oothecae, and defense of oothecae, are examples of care. Brooding behavior is a shortterm association of the mother and neonates. In some species, the young cluster around, under and on the mother, though this behavior may only persist for about a day. Though often not lasting long, this behavior allows the cuticle of neonates to harden. The transfer of gut microbiota also may occur at this time, probably via a fecal meal. Cockroaches (Blattodea) C Cockroaches (Blattodea), Table 15 Parental care in cockroaches where offspring are provided with bodily secretions by adults (adapted from Nalepa, Bell (1997) Social behavior in insects and arachnids) Offspring Species Location Food source Perisphaerus sp. Cling ventrally Hemolymph Trichoblatta sericea Cling ventrally Sternal exudate Pseudophoraspis nebulosa Cling ventrally ? Phlebonotus pallens Under tegmina ? Thorax porcellana Under tegmina Tergal exudate Gromphadorina portentosa Abdominal tip of female Secretion from brood sac Salganea taiwanensis Mouthparts of adult Stomodeal fluids Cryptocercus punctulatus Abdominal tip of adult Hindgut fluids Cryptocercus kyebangensis Abdominal tip of adult Hindgut fluids Blatella vaga Under tegmina Tergal exudate Sometimes the brooding behavior is extended for a longer period of time, perhaps 2 weeks. Females may accommodate offspring during this period by allowing young cockroaches to cling to her body, and some have evolved external brood chambers under their wing covers. An example of a higher level of brood care is found in Thorax porcellana, which maintains its young in a brood pouch for about 7 weeks. It seems that the young feed on a pinkish material secreted by the dorso-lateral regions of the tergites. Parental feeding of young is not unusual. Usually it is only the female that is involved in parental care. Ecological Importance Cockroaches contribute to ecosystem functioning by breaking down organic matter and aiding in release of nutrients. They are aided both by their endogenous cellulases and their microbial symbionts. Cockroaches can be considered to be soil fauna, though they rarely are acknowledged as such. The principal diet of cockroaches is organic material, and in living and feeding in the litter, soil and decaying trees, they contribute to the make-up of the soil. Their role is not in the direct mineralization of soil, because that is the role of microorganisms. Rather, it is to put the organic material in contact with the microbes. This is done by fragmenting litter, exposing litter to microbes, and by transporting microbes to new resources. Cockroaches are less dependent on water for functioning than are microbes, and microbes in the gut are afforded the correct conditions for activity. Also, the fecal pellets produced by cockroaches are an important substrate for microbes, and speed the return of above-ground productivity to the soil. Microfauna such as mites, springtails, nematodes and protozoa utilize the bacteria and fungi growing on the pellets as a principal food resource. The importance of litter decomposers for soil formation and enrichment is widely acknowledged. What is not known, however, is the relative importance of cockroaches. We can likely assume that it is quite significant in tropical forests, but in temperate forests they also are abundant, often comprising about half of the soil macrofauna. Domiciliary Cockroaches Some “domiciliary” species invade dwellings, and a few species are well-adapted to living in 941 942 C Cockroaches (Blattodea) buildings and on ships, where they can become numerous enough to be considered pests. Lack of hygiene is normally associated with cockroach infestation in temperate areas, though in tropical and subtropical regions cockroaches live out-ofdoors and invade dwellings irrespective of hygiene. Cockroaches often produce an odor that is unpleasant, and are implicated in a limited amount of disease transmission. They are a major source of allergens. Cockroaches are often the target of chemical suppression efforts, especially in food establishments. Thus, it is not surprising that insecticide resistance is widespread in some species. Cockroaches may be eaten by predatory vertebrates, and parasitized by nematodes and mites, but the most important natural enemies are egg parasitoids. About six families of wasps, but particularly Evaniidae and Eulophidae, parasitize cockroach eggs, sometimes quite effectively. Cockroaches as Pests Traditionally, efforts to suppress cockroach populations in the urban environment have relied almost exclusively on repeated applications of synthetic pesticides. However, the chemical approach to cockroach control has become increasingly less popular. This is primarily due to the development of multi-chemical resistance among German cockroach populations and increased public concern about pesticide exposure in their living environment. These two issues have led to development of less toxic approaches to cockroach management. The Principal Cockroach Pest Species The predominant pest cockroach species in the world is the German cockroach, Blattella germanica (Fig. 70). German cockroaches are small, with adults <1.5 cm in length. They are gold in color and have two dark longitudinal bands on their pronotum near the head. Immature German cockroaches are smaller than adults, wingless and dark brown in color. German cockroaches are primarily indoor pests. They have strict moisture requirements so they are usually found in kitchen and bathroom areas. Adults live about 6 months, and during this time the female produces from 4 to 8 oothecae. The female carries the egg case throughout embryonic development (3–4 weeks) often releasing it from her body only hours before the nymphs hatch. Each female produces about 28 nymphs in each egg case. German cockroaches are the most prolific cockroach pest species, most likely to be insecticide resistant, and therefore the most difficult to control. An increasingly important species is the brown-banded cockroach, Supella longipalpa. Although it is favored by warm climates, it can be quite abundant in more temperate environments, and has replaced German cockroach as the dominant pest species in some areas. It is more tolerant of low humidity than German cockroach, so it is found inhabiting areas without a ready source of water, such as bedrooms and closets. The common name is most descriptive of the nymphal stage, though even the adult has two dark bands on the wings. It lacks the two parallel dark stripes found on the prothorax of German cockroaches. The female carries an egg capsule with up to 18 eggs initially, but after a day or two she attaches it to an object. The incubation period of eggs is about 70 days, and time to complete development is about 160 days. Some other pest species include the American cockroach, Periplaneta americana, Australian cockroach, P. australasiae; brown cockroach, P. brunnea; smoky-brown cockroach, P. fuliginosa; Oriental cockroach, Blatta orientalis; and the Florida woods cockroach, Eurycotis floridana. These other species of cockroaches (Fig. 70) are much larger and heavier than German and brown-banded cockroaches. Adults range in size from 3 to 4 cm in length and are reddish brown to black in color. Some of these large cockroaches can live up to 2 years in the adult stage. Adult females can produce an egg case about every 1–2 weeks. A typical female will produce about 20–80 Cockroaches (Blattodea) C Cockroaches (Blattodea), Figure 70 Some common cockroaches: top left, German cockroach, Blatella germanica; top right, brown-banded cockroach, Supella longipalpa; second row left, American cockroach, Periplaneta americana; second row right, Australian cockroach, Periplaneta australasiae; third row left, smoky-brown cockroach, Periplaneta fulginosa; third row right, Florida woods cockroach, Eurycotis floridana; bottom left, Oriental cockroach, Blatta orientalis; bottom right, Cuban cockroach, Panchlora nivea (photos by J. L. Castner, University of Florida). 943 944 C Cockroaches (Blattodea) oothecae during her lifetime, each containing 15–20 nymphs. Peridomestic females release the egg case from their body soon after it has developed. They then glue the egg case to a surface, usually in a hidden, moist area. In contrast, German cockroach females continue to carry the egg case throughout embryonic development. Some cockroaches live both indoors and outof-doors, especially in warm climates, and are called “peridomestic” cockroaches. Peridomestic cockroaches normally breed outdoors in sewers, palm trees, tree holes, piles of firewood, water meters, well pumps, mulch, and flower beds. These cockroaches usually enter homes only occasionally, when foraging for food, water or warmth. In some situations, however, they will establish breeding populations in attics, crawl spaces, wall voids and other indoor areas. Management · · · and toilets to keep the drain trap filled and off limits to cockroaches. Covering vent pipes on the roof with fiberglass window screen will prevent cockroaches from migrating up from sewer connections and gaining ready access to the roof, and hence to attics and windows. Groceries, produce and other packaged food products may have been stored in infested locations before they were purchased. Make an effort to visibly scan all grocery items for evidence of cockroachs before putting them away. Children can transport cockroaches from school to home in book bags and lunch pails. Inspect these items on a regular basis. Sanitation is critically important. For example, German cockroaches can remain alive for approximately 2 weeks with no food or water and for 42 days if only water is available. Therefore, it is important to realize that cockroaches can survive on minute amounts of food such as crumbs, grease or food residue. Exclusion and Sanitation · Long-term prevention of cockroach infestation is the best means of ensuring a cockroach free environment. This is most easily accomplished by exclusion (preventing cockroach entry) and sanitation (elimination of cockroach resources). Not only will these measures prevent a future infestation, they will also help to reduce an existing cockroach problem. Methods of preventing cockroach entry include: · · · Cockroaches migrate easily through multi-unit dwellings via plumbing and electrical connections. Sealing gaps around plumbing, wall outlets and switch plates will prevent cockroaches from migrating from infested units to others. Keep doors and windows closed and screened. Also, caulk cracks and gaps that may allow peridomestic cockroaches to invade from outdoors. Peridomestic cockroaches frequently enter homes by coming up through dry drain traps. Periodically run the water in spare bathrooms, utility tubs · · · · · Indoor trash containers should be emptied frequently, and kept clean both inside and out. Plastic bags lining trash containers can be kept closed with twist ties. This will prevent cockroaches from being attracted to the garbage area. Filled indoor garbage containers should be removed from the dwelling immediately and placed in outdoor containers with tight fitting lids or dumpsters. Keeping the area around dumpsters or other outdoor garbage storage areas clean and free of debris will also prevent peridomestic cockroach infestations in the area. Frequent emptying of sink strainers and running of the garbage disposal and will prevent food build up in the sink drain. Washing dishes immediately after a meal will prevent cockroaches from consuming food residue on dishes. Unwashed dishes are a major source of food for German cockroaches. Kitchen appliances (toasters, toaster ovens, microwaves, ovens, stoves, and refrigerators) should be kept clean and free of food particles Cockroaches (Blattodea) · · · · and grease. Additionally, the areas underneath and behind these appliances should be kept grease and crumb free. If pets are present, dry food should be kept in resealable containers. Do not leave food and water out all the time. Feed your pet at particular times and clean up after every meal. All foods products should be resealed after opening, stored in plastic snap-lid containers, or kept in the refrigerator. Regular sweeping/vacuuming of floors and furniture helps to eliminate cockroach food sources. Regular cleaning of food storage areas and shelves not only eliminates spilled or scattered food, but disrupts cockroach populations that may be using the area as a harborage. The single most important factor in determining cockroach survival is availability of water. German cockroaches live <2 weeks without a supply of free water, even if food is abundant. During periods of drought, the incidence of peridomestic cockroaches indoors will often increase as these large cockroaches invade structures in search of moisture. Therefore, it is important to eliminate all sources of moisture that contribute to cockroach survival. Important steps in water management include: · · · · Tightening loose pipes, patch plumbing leaks and replace used washers in the kitchen sink and bathroom areas. Outdoor water spigots and sprinklers should also be checked for drips and leaks. Water left in the sink or bathtub after dish washing or bathing also provides moisture for cockroaches. These sources are eliminated by drying out sinks and bathtubs after use. A common source of moisture is condensation under the refrigerator. This area should be frequently wiped dry or, if possible, a pan should be placed under the appliance to collect water. The collection pan should be emptied frequently. Condensation on pipes (under the sink or in wall voids) is also a problem. Insulate these pipes, if possible. Pet drinking dishes and aquariums are also sources of moisture. Empty pet water dishes at night when · · · C cockroaches are foraging but the pet is indoors or asleep. Aquariums should have tight fitting lids or screens to prevent cockroach entry. Be careful not to over-water indoor plants, because excess water is available to cockroaches. Glasses, cups and soda cans containing water or liquid residue are common sources of moisture for cockroaches. Be sure not to leave these containers in bedrooms, sinks, on counter tops or other areas. Rinse and invert cups and glasses to dry immediately after use, and dispose of soda cans in trash containers. Steps should be taken to eliminate places where water collects outdoors (tires, cans, tree holes, etc.). This will not only eliminate cockroach moisture sources but also mosquito breeding habitat. The third critical element for cockroach survival is harborage. By nature, cockroaches avoid open, well-lighted areas with frequent air movement. They prefer dark, warm cracks and crevices. Excess clutter provides numerous locations suitable for cockroach habitation. The elimination of these harborages (clutter) is important in controlling infestations. Practices that reduce harborage include: · · · · · · Adult cockroaches can fit into cracks only 1.6 mm wide (about 1/16 of an inch). Any small gap or hole that leads to a void is a prime cockroach harboring area. Cracks and crevices of this kind should be sealed with a tube of caulking. Removing clutter (boxes, bags, clothing, toys, food, books, papers, etc.) eliminates cockroach harborages and breeding areas. It is essential to keep all areas of the home, especially the kitchen and bathroom, uncluttered and free of useless debris. Outside, remove debris and trash from around the house. Stack firewood far away from the house, as this is a prime harborage area for peridomestic cockroaches. Filling in tree holes with cement also eliminates peridomestic cockroach harborage. Keep shrubbery and ornamentals well trimmed. In particular, keep palm trees free of loose and dead palm branches and remove all palm debris. 945 946 C Cockroaches (Blattodea) Toxicants Usually it is desirable to eliminate the need for toxicants, but this is not always possible. Reduced chemical control methods currently are available for indoor and outdoor cockroach control. The traditional approach of cockroach control based on application of liquid insecticides to floor, wall, and fixture surfaces has been supplanted by more selective application techniques. The most recent technological advances in reduced toxic and nontoxic cockroach control have been in bait formulations, and in insect growth regulators. Other currently used non-toxic measures include desiccating dusts, traps and biological controls. Each of these treatment methods can contribute to an effective cockroach management program. On the other hand, although ultrasonic devices are frequently advertised as a non-toxic method of cockroach control, extensive research has shown that these devices neither kill nor repel cockroaches. areas where bait station placement is difficult. The homeowner will often want the large bait stations placed inside the structure in order to kill peridomestic cockroaches that are caught foraging inside. This, however, does nothing about the population of cockroaches that continues to breed outdoors. Outdoor baiting products are used primarily for the control of peridomestic cockroaches. Spreadable granular baits or bait stations are the most common formulations used for peridomestic cockroach control. Spreadable baits are usually applied as a perimeter band around a structure, and can effectively suppress populations and reduce invasion rates of households. However, it is difficult to determine the residual longevity of these products, particularly in areas where precipitation is frequent. Even “weatherized” baits have difficulty retaining their residual properties where there is heavy rainfall or irrigation. This is particularly true in the southeastern United States where precipitation can ruin bait effectiveness in a single day. Cockroach Baits Insect Growth Regulators Cockroach baits consist of a toxicant mixed with a food source. Some baits also contain attractants or feeding stimulants designed to make the bait more attractive to cockroaches than other food sources that may be available in the immediate area. Current indoor bait formulations are applied as dusts, pastes, gels or bait stations. The bait station is one of the more popular application methods for cockroach baits. This is because the stations are easy to put out, safe around children and pets and have residual activity. Gel and dust bait formulations are formulated for injection into cracks and crevices, which reduces the potential contact of people with toxicants, and places the toxicants in areas frequented by cockroaches. Bait stations for peridomestic cockroaches are simply larger versions of those used for German cockroach baiting. The problem with this baiting system is that peridomestic species live and breed outdoors in palm trees, woodpiles, tree holes and other Insect growth regulators (IGRs) are a group of compounds that disrupt the normal growth and development of insects. The IGRs are considered to be reduced-risk tools. They generally have very low toxicity to mammals because they act by disrupting the hormonal processes that are specific to insects. IGRs that mimic the juvenile hormones of insects are called juvenile hormone analogues (JHAs). JHAs are chemical compounds with structural chemistry that is very similar to the hormones that the immature cockroach produces naturally. JHAs interfere with the proper development of last instar cockroach nymphs. Instead of the nymphs molting into reproductive adults they molt into “adultoids,” which often have twisted wings and are sterile. Because the adultoids are unable to reproduce, over the course of time the cockroach population will decline. JHAs are an effective method of long term German cockroach control. However, because JHAs eliminate reproduction but do not Cockroaches (Blattodea) kill existing cockroaches, they are very slow acting (from 4 to 9 months to achieve control). JHAs are often combined with residual insecticides. In this manner most of the population can be eliminated quickly by the insecticide, and cockroaches that survive the insecticide treatment are then sterilized by the JHA. Insect growth regulators are available in spray formulations or point source dispensers, where the IGR is released on a filter paper contained in a permeable plastic station then transmigrates throughout the infested area. Chitin synthesis inhibitors (CSIs) are another type of insect growth regulator that is being developed for use in management programs targeting a variety of insect pests. Exposure to CSIs results in the abnormal molting of nymphs, causing them to die during the molting process. CSIs also cause adult cockroaches to form abnormal egg cases and interferes with the hatching process. Inorganic Dusts Inorganic dusts such as silica gel and boric acid have been used frequently for indoor cockroach control. The dusts are applied with a squeeze-bulb duster into cracks and crevices under sinks, stoves, behind refrigerators, along baseboards, in electrical outlets, cabinets and wall voids. Silica gel is simply a finely ground sand-like product that adheres to, and absorbs, the protective waxes on the cockroach cuticle, resulting in cockroach death from dehydration. Boric acid is a stomach poison that is picked up by cockroaches walking across dusted areas. The boric acid adheres to the cockroach cuticle so when the cockroach grooms itself it ingests the boric acid and soon dies. Traps One of the non-chemical tactics available for reducing a cockroach infestation involves the use of traps. Sticky traps can be purchased and placed indoors, near the garbage, under the sink, in the C cabinets, under and behind the refrigerator, and in the bathroom. Outdoors, sticky traps are not recommended because they tend to capture many non-target animals (snakes, lizards etc.), and are not resistant to weathering. A second trapping method is the use of baited jars. Any empty jar (pickle, mayonnaise, peanut butter, etc.) with a rounded inside lip will suffice. Coat the inner lip of the jar with a thin film of Vaseline (to keep trapped cockroaches from escaping). The jar should then be baited with a quarter slice of bread soaked in beer (a cockroach favorite). If beer and bread are unavailable try other foods like cookies, dog food, apples, etc. The outside of the jar should be wrapped in paper towel so cockroaches have a surface to grasp as they climb up the sides of the jar. To kill trapped cockroaches simply pour dishwashing detergent into the jar and add hot water. The cockroaches can then be dumped outside or in the garbage. Wash out the jar and repeat the process every 2–3 days. Indoor jar traps should be placed in the same locations as those listed for sticky traps. When trapping outdoors, jars should be placed in trees, tree holes, mulched areas, firewood, near trash cans, compost piles, air conditioning units and storage sheds. Covering the jars with a dome-shaped piece of aluminum foil taped to the sides will prevent rain from filling the traps. Jar traps are very suitable for outdoor use because they present little threat to non-target organisms, and are not easily damaged by weather. Biological Control Natural controls do play an important role in managing cockroach populations. Natural cockroach enemies include wasps, nematodes, spiders, toads and frogs, centipedes, birds, lizards, geckos, beetles, mantids, ants and small mammals (mice). It is very important that these populations of natural enemies be maintained to help keep cockroach populations in check. Often, the importance of natural enemies in keeping the cockroach problem in check is overlooked. 947 948 C Cockroaches and Disease Oothecal Parasitoids Parasitic wasps are an important natural enemy of cockroaches. The wasps are parasitoids of the cockroach egg case (ootheca) and can have a significant negative impact on outdoor cockroach populations. Most species of parasitoid wasps are associated with peridomestic cockroaches. The majority of these wasps are minute (1–5 mm) and do not sting humans. Peridomestic cockroaches like the American and smoky-brown live in outdoor harborages such as palm trees, tree holes, and woodpiles. The parasitoids live with the cockroaches in the harborage parasitizing their egg cases. When the adult male and female wasps emerge they mate immediately. The female then begins to sting other oothecae, laying her eggs inside them. The wasp offspring eat the cockroach embryos inside the ootheca before hatching. This natural system results in 60–70% of all cockroach egg cases being parasitized without any human interference. Oothecal wasp parasitoids have been tested for potential indoor use. Domestic populations of brown-banded cockroaches were successfully controlled in a California animal rearing facility by these wasps. However, it is doubtful that parasitoid wasps will ever be reared for commercial use. Very few individuals would welcome a population of 200,000 wasps in their home even if they promised to eliminate a severe cockroach infestation. Wasp parasitoids are extremely susceptible to pyrethroid insecticides. When attempting to eliminate an outdoor cockroach infestation, it is important to realize the insecticide applications in peridomestic cockroach harborages may not kill all of the cockroaches but it certainly will eliminate the parasitoids. This can result in future cockroach problems because surviving cockroaches can reproduce unchecked once the parasitoids are eliminated. The application of bait around an infested area is the best way to treat a population of peridomestic cockroaches and preserve the wasp parasitoids.  Boric Acid  Diatomaceous Earth  Baits for Insect Control  Insecticides  Insecticide Resistance  Urban Entomology References Arnett RH Jr (2000) American insects, 2nd edn. CRC Press, Boca Raton, FL, 1003 pp Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore, MD, 230 pp Cornwell PB (1968) The cockroach, vol 1. Hutchinson & Company, London, UK, 391 pp Fisk FW (1987) Order Blattodea. In: Stehr FW (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA, pp 120–131 Miller DM, Koehler PG (1999) Least toxic methods of cockroach control. Florida Cooperative Extension Service Publication ENY-258 Roth LM, Willis ER (1960) The biotic associations of cockroaches. Smithsonian Miscellaneous Collections, vol 141, pp 1–470 Cockroaches and Disease Gary w. Bennett Purdue University, West Lafayette, IN, USA The importance of domestic cockroaches (those invading our buildings) as public health pests, especially as vectors of disease, is somewhat uncertain. Although many pathogenic organisms have been isolated from cockroaches, there is only circumstantial evidence to link diseases in human beings to the causal agents of those disorders known to be present on and in cockroaches closely associated with humans (Table 16). Cockroaches rank with termites as the most important insects found in association with humans. Cockroaches can be found in most any place humans inhabit, especially where food is stored, processed, prepared, or served. They seek not only our food, but also putrefied and decaying matter, virulent discharges, and feces. Cockroaches Cockroaches and Disease Cockroaches and Disease, Table 16 Pathogens associated with cockroachesa Pathogen type Pathogen Potentially associated disease Cockroach species Bacteria Alcaligenes faecalis wound infection, gastroenteritis American, Oriental Bacillus spp. food poisoning, conjunctivitis American, Oriental Campylobacter jejuni enteritis American, Oriental Clostridium spp. gas gangrene, food poisoning Oriental Escherichia coli diarrhea, wound infection American, Oriental, German Klebsiella pneumoniae pneumonia, urinary infections Unspecified cockroaches Mycobacterium leprae leprosy German, American, Australian Nocardia spp. actinomycetoma American Proteus spp. wound infection American, Oriental Pseudomonas aeruginosa respiratory infections, gastroenteritis American, Oriental, German Salmonella spp. food poisoning, gastroenteritis American Salmonella typhi typhoid Oriental Streptococcus pyrogenes pneumonia Oriental Serratia marcescens food poisoning American, Oriental, German Shigella dysenteriae dysentery German Staphylococcus aureus wound, skin and internal German infections Oriental Streptococcus faecalis pneumonia American, Oriental, German Yersinia pestis plague Oriental Fungi Aspergillus spp. respiratory infections American, Oriental Helminths Ancylostoma duodenale hookworm American Ascaris lumbricoides giant human roundworm American Ascaris spp. roundworm Oriental Enterobius vermicularis pinworm Oriental, German Hymenolopsis spp. tapeworm American Necator americanus hookworm American Trichuris trichuria whipworm American, Oriental, German Aspergillus niger otomycosis Oriental Molds C 949 950 C Cockroaches and Disease Cockroaches and Disease, Table 16 Pathogens associated with cockroachesa (Continued) Pathogen type Pathogen Potentially associated disease Cockroach species Protozoans Entamoeba hystolytica amebiasis Oriental, Australian, German, American Giardia spp. giardiasis Unspecified cockroaches Poliomyelitis paralytic polio German, American, brown-banded Viruses a Extracted from Roth LM, Willis ER (1960) The biotic associations of cockroaches. Smithsonian Institute, Washington, DC, 439 pp readily move from garbage disposal areas, to sewers, to toilets, to food ready for consumption. This movement creates the opportunity for the contamination of food and food preparation surfaces with disease-causing organisms. Important Species Cockroaches are tropical or subtropical in origin. Species that have adapted to living indoors originated in tropical Africa. Cockroaches probably became domesticated in prehistoric times when humans were cave dwellers. As humans evolved to more sophisticated structures, the cockroach also moved, readily adapting to new surroundings. Homes, restaurants, hospitals – any place that has warmth, food and water available – form ideal environments for the proliferation of these pests. Only a small number of species have moved from the fields and forests to take up residence in our structures. And of these domestic species, the German, Oriental, and American cockroaches are the most important species because of their wide distribution and common occurrence in buildings. The German cockroach is most often found in close association with kitchens and other food areas. American and Oriental cockroaches may also be found in food areas, but more often are found in basements, sewers, crawl spaces, and outdoor areas. Each of these species is routinely found in areas of filth and decaying organic matter. Thus, filth organisms are found both on their bodies and within their digestive tracts. Public Health Importance of Cockroaches Numerous published papers recount the incidence of cockroaches, their association with disease and filth organisms, their production of odorous secretions that can contaminate and affect the flavor of foods, the socially unacceptable nature of cockroaches in homes, and in some cases, the fear and anxiety some individuals have of cockroaches. These problems are justification for the large sums of money spent each year to control these pests. Domestic Nuisance Cockroaches are among the most common insects found associated with humans. They breed in our buildings and share our food, water, warmth and shelter. They consume the same food that we eat, as well as dead plant or animal materials, leather, glue, hair, wallpaper, fabrics, book bindings, and feces. They contaminate food by crawling around and defecating on it, or by leaving cast skins, empty egg cases, or dead bodies in foodstuff. They regurgitate saliva and intestinal fluids from their mouths while feeding and deposit fecal droppings as they crawl around on food. The nasty habits of this pest cause fear and social embarrassment for homeowners. Cockroaches and Disease Cockroach Bites Cockroaches have been reported to bite humans, although such instances are rare and not serious. They have been noted to gnaw on the skin and nails of sailors aboard heavily infested ships. Cockroaches are most likely to nibble on the eyelashes, fingernails, and toenails of sleeping children and the infirm, and in cases of heavy infestations they can cause small wounds on softer skin. Accidental Invasion of the Body Numerous accounts of cockroaches entering the ear, nose, or other body orifices have been recorded. These invasions usually occur at night when the human “host” is sleeping and when cockroaches are most active. There have also been instances of intestinal invasion by cockroaches, usually in young children in severely infested living conditions. As cockroaches forage for food in heavily infested areas, it certainly is possible for them to enter orifices of the body, especially when the person is sleeping and quite still. Disease Carriers Published papers recount the incidence of cockroaches and their association with disease organisms. They document the evidence that cockroaches carry pathogens in and on their bodies and in their excreta, but are unable to establish any cause and effect relationship with disease in humans. So to date, cockroaches can only be viewed with suspicion. Incriminating evidence is difficult to find linking cockroaches as vectors of disease outbreaks. There are many anecdotal stories, such as the one about an epidemic of food poisoning caused by Salmonella among children in the nursery of a hospital in Brussels. The infection persisted for 2 months, despite isolation of the patients. Cockroaches were considered as carriers only after a night nurse drew attention to an infestation of Blattella germanica, the C German cockroach. The insects were observed running over the bed clothing and over the children at night. Among the cockroaches caught, one was found to be carrying numerous bacteria identified as Salmonella. When the cockroach infestation was eliminated, the food poisoning epidemic stopped immediately. Thus, the circumstances were very suspicious, but there was no conclusive evidence that the cockroaches were involved in the disease outbreak. It is important to note that over 30 species of bacteria, most of them potentially pathogenic, have been found on cockroaches collected from public buildings, along with numerous viruses, protozoans, mold fungi, intestinal helminths (pinworms, tapeworms, etc.), and secretions which “may have” mutagenic and carcinogenic effects. So there certainly is not a lack of pathogens found on and in cockroaches. Allergies Some people are allergic to cockroaches. Cockroach secretions, body parts, and excrement contain a number of allergens to which many people exhibit allergic responses, such as skin rashes, watery eyes, and sneezing. For some very allergic individuals, and particularly for those who also have a lung disease such as asthma, allergic reactions to cockroach allergens can be very serious and even life threatening. “Cockroach asthma” is caused by the inhalation of any one of a number of protein fractions found in cockroaches that can cause allergies. High- and low-molecular-weight proteins that have been isolated from cockroach extracts have been used to illicit bronchospastic allergy responses in humans, with allergies to cockroaches being the second most common allergy in asthmatics (with even more important sensitivity occurring in asthmatic children in severely infested homes). Dermatitis and conjunctival edema also occur in asthmatic and skin-sensitive populations. Exposure to cockroaches increases the incidence of reaction to cockroach allergens. Sensitivity is quite high among asthmatic children in severely 951 952 C Cocoon infested homes. Any conditions favorable to an increase in cockroach populations, as well as the lack of fresh airflow to remove airborne allergens, will lead to greater allergy problems. Thus, it is important to create living environments free of cockroaches, as well as those that have a good supply of fresh air. Cocos nucifera L., feeding in extremely dense aggregations that cause scarring and distortion of the fruits. This mite is the only eriophyid mite that is a serious pest of coconut palm, and it is considered one of the worst arthropod pests of this palm, whether grown as a crop tree or as an ornamental. It is distributed in many tropical countries. Focus on Sanitation Cockroach infestations do have the potential for serious health consequences. Acceptable hygiene standards (including cockroach elimination) must be implemented to avoid the social unacceptability of cockroaches, the potential contamination of foodstuffs, and the health problems that they can cause.  Cockroaches References Alcamo IE, Frishman AM (1980) The microbial flora of fieldcollected cockroaches and other arthropods. J Environ Health 42:263–266 *Cornwell PB (1968) Diseases. In: The cockroach, vol 1. Hutchinson, London, UK Ebeling W (1975) Pests on or near food. In: Urban entomology. University of California, Los Angeles, CA Kang B, Chang JC (1985) Allergenic impact of inhaled arthropod material. Clin Rev Allergy 3:363–375 Roth LM, Willis ER (1957) The medical and veterinary importance of cockroaches. Smithsonian miscellaneous collection, vol 134, pp 1–147 Cocoon A sheath, usually of silk, formed by an insect larva as a chamber for pupation. Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) forrest w. howard University of Florida, Ft. Lauderdale, FL, USA The coconut mite, Aceria guerreronis Keifer (Acari: Eriophyidae), attacks fruits of the coconut palm, Distribution The coconut mite was described in 1965 from specimens collected in Guerrero, Mexico. The same year it was found near Rio de Janeiro, Brazil. Within the next several years it was found in many countries of Tropical America and also in West Africa. The native home of the species, which is especially of interest in searching for biological control agents, has been enigmatic. However, it was recently reported that DNA sequence data from disparate populations of coconut mite in the tropics of the Eastern and Western Hemispheres revealed that populations from the Americas were the most diverse, while those from Africa and Southern Asia were virtually uniform. This suggests that the mite evolved and diversified in the Americas, and spread in the tropics of the Eastern Hemisphere from a single introduction (presumably in West Africa). The coconut mite has not been found in the South Pacific Region, the original home of the coconut. Although the coconut mite is apparently native to the Americas, coconut palms are native to the South Pacific. Earlier introductions were brought first to the Caribbean Region and then elsewhere in the American Tropics from West Africa by Europeans in the 1500s. During this same period, a small population of coconut palms was found on the Pacific coast of Panama, but these are thought to have been introduced naturally or by seafarers from the South Pacific shortly before the arrival of the Spanish. As a worldwide agricultural industry developed around the coconut in the 1800s, additional coconut varieties were introduced to many localities. Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) It is not known how long this mite has been associated with coconut, but based on anecdotal evidence provided by farmers and other observers in various localities of the Americas, local people had been familiar with the damage typical of this mite long before it was discovered and described taxonomically. The greatest diversity of cocosoid palms, i.e., genera related to the monotypic Cocos, is found in South America. It has thus been suggested that the original host of the coconut mite may have been a Cocos relative native to the Americas. The most dramatic extension of the range of coconut mite in recent years occurred in the late 1990s, when it was found for the first time on coconuts in Tanzania (East Africa), India, and Sri Lanka. Description The adult female of coconut mite, which is the largest stage, is 205–255 μm long and 36–52 μm wide. The mites are white and translucent. Like eriophyid mites in general, they are elongate and possess two pairs of legs, instead of four pairs as is typical of mites in general. Massive colonies of the mites, but not individual mites, can be detected with difficulty with a 10X hand lens. At this magnification, the colonies appear as vague silvery patches. Hosts In nearly all localities where coconut mite is present, its only reported host is coconut palm. Rare exceptions include a record of this mite on fruit of Lytocaryum weddellianum (H.A. Wendland), and on queen palm, Syagrus romanzoffiana Chamisso (Glassman), both of which are cocosoid palms native to Brazil. Coconut palm varieties differ in their susceptibility to coconut mite. Almost all varieties have some level of susceptibility. C Biology and Ecology The mites infest the abaxial (lower) surfaces of the tepals and that part of the fruit surface that is covered by the perianth. They are able to penetrate between the perianth and fruit surface a month after the fruit begins development. Prior to this, the tepals are too tightly appressed to allow entry of the mites. The coconut mite has inefficient host-finding capabilities that are compensated for by a high reproductive rate and rapid development. Presumably, a population on a fruit is initiated by one or more fertilized females usually from either infested fruits on the same palm, perhaps even the same raceme, or from a nearby infested palm. The mites feed by piercing the superficial plant tissue to elicit juices which they then imbibe. A coconut mite develops from egg to adult in 10 days; thus, populations can build up rapidly. Often, thousands of mites in each of several aggregations occupy the same fruit. Massive populations of coconut mites may be present among the tepals and on the fruit surface beneath the perianth until about the sixth month of the coconut’s development, after which populations decline. They are no longer present on mature (12-month old) fruits. Coconut mites are probably capable of dispersing from one palm to the other on air currents or by phoresy (e.g., riding on insects or birds that visit palm flowers). Where coconut palm plantings are dense, the mites may disperse to new hosts by being blown a short distance, and in some cases probably crawl from one palm to another on foliage that is in contact, ultimately arriving on a fruit. Thus, their potential to spread to new host palms is greater where the palms are in close proximity. In densely planted coconut plantations, up to 100% of the palms are often infested, while the percentage infested is typically lower in more widely spaced plantings of coconut palm. However, isolated coconut palms may sometimes be highly infested. Some researchers indicate that the coconut mite is most damaging to palms under dry conditions, i.e., growing in relatively dry regions or 953 954 C Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) during the dry season in tropical areas with pronounced wet and dry seasons. Potential explanations for this relationship include that under dry conditions the perianth may open slightly so as to allow mites to enter more easily, that the coconut may develop more slowly and thus remain longer in a susceptible stage, or that fungi that help regulate the mites may be suppressed. However, other researchers have reported that coconut mite attack increases in wet periods, or that there is no clear association between seasonal rainfall patterns and coconut mite populations. Damage and Economic Importance The feeding site of the coconut mite is on the surface of the meristematic zone of the coconut fruit. This is a circular whitish zone covered by the perianth. The fruit expands from this zone, so that the young fruits of about 2.5–3.0 cm in length and diameter develop to the mature coconut of up to 25 cm long during the period of about 1 year. An early-stage infestation of a young coconut by coconut mites (Fig. 71) is often detectable as a small pale area, often triangular but sometimes broader, extending on the fruit surface from beneath the perianth. With exposure to the air, the pale area turns brown within a few days. The location of damaged sites on individual coconuts is partly determined by the arrangement of tepals of the perianth. Damage tends to be greater under tepals that overlap adjacent tepals at both ends, because mites find more space there than under tepals whose ends are overlapped. As an infested coconut develops, the tissue extending from beneath the perianth continues to incur damage, thus the damaged area eventually covers a large portion of the surface. In older damage, the affected surface is suberized (cork-like), with deep longitudinal fissures which may be intersected by horizontal cracks. If intense mite feeding is concentrated on one side of the fruit meristem, the fruit may develop unevenly, Coconut Mite, Aceria guerreronis (Acari: Eriophyidae), Figure 71 (above) A coconut mite, Aceria guerreronis; (center) young coconut fruit with early damage (pale triangular area) due to feeding of the coconut mite, Aceria guerreronis; (below) coconuts with suberized surfaces due to feeding of the coconut mite, Aceria guerreronis. Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) forming a distorted coconut. Highly severe damage stunts the fruits. Some observers report that damage to young fruits causes excessive numbers of them to drop, but other researchers suggest that some fruit shedding is normal and in many cases the additional fruit shedding that may be caused by coconut mites may not significantly affect yield of copra and other coconut products. Copra, a main product of the coconut industry, is the white kernel, or coconut “meat” after it is dried. In one study, coconut mite damage was found to cause a loss of up to 30% of the copra. Other researchers have reported a less serious impact on copra production. In many tropical countries, millions of coconuts are sold fresh in roadside stands and farmers’ markets for coconut water, i.e., the clear liquid in the coconut that serves as a beverage and is sometimes erroneously called “coconut milk.” (In the coconut industry, the latter term applies to the paste made by grinding the kernel.) Data is not available on the possible impact of the coconut mite on the production of coconut water, but the unappealing appearance of mite-damaged coconuts has been shown to adversely affect sales of this product. Coconut palms are an essential feature in the landscape of tropical resort areas, and are treasured by many residents of the tropics. Damage by coconut mite does not affect the vigor of the palm and the scarred coconuts are not highly noticeable from a distance, but the aesthetic damage is important to homeowners or managers of areas where coconuts are seen up close, such as in the landscaping around hotel swimming pools. Coconut mite damage can be spotted at a distance, but must be confirmed by closer examination. At maturity, the surface tissues of a coconut dry and become a tan color. Prior to maturing, coconuts are green, yellow, bronze, apricot, or a blend of these colors, depending on variety. Thus, the dark brown color of coconut mite damage is most noticeable when the fruit is C young. Any kind of mechanical damage can result in browning of the surface of young coconuts, but coconut mite damage consistently extends from beneath the perianth, which is not true of other kinds of mechanical damage. Colomerus novahebridensis Keifer is an eriophyid mite present in southeast Asia and the Pacific that causes damage to coconuts that is similar but much lighter and less frequent than that of A. guerreronis. In Florida, Puerto Rico, and presumably elsewhere in the Caribbean Region, Tarsonemus sp. (Acari: Tarsonemidae), causes damage similar in appearance to early coconut mite damage. However, this mite is rare, and apparently does not remain long on coconut fruits, as the damage never advances beyond the early stage. Stenotarsonemus furcatus DeLeon, which has been found in association with damage on coconut fruits in Brazil, may be the same or a similar species. Management Chemical Control Some acaricides have been shown to kill coconut mites. However, most chemicals applied topically had to be repeated indefinitely to maintain control. Systemic acaricides might persist longer in the plant, but such chemicals could result in residues in the fruits, and coconuts are harvested throughout the year. Chemical control is perhaps the least viable option for control of coconut mite. Mechanical Control A simple mechanical form of control practiced by some plantation managers is to prune all of the coconuts in all stages of development. This is said to result in a plantation free of coconut mites for an extended period. However, this method would cause a disruption in the economic benefits of the plantation. 955 956 C Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) Cultural Control As mentioned above, results of studies of environmental factors influencing coconut mite populations, including wet or dry conditions and nutrient levels, have been thus far controversial. Future research may provide a basis for economically feasible cultural control of the coconut mite. Host Plant Resistance Common coconut varieties in the Americas, viz., ‘Jamaica Tall,’ ‘Panama Tall,’ ‘Malayan Red Dwarf,’ ‘Malayan Yellow Dwarf,’ and ‘Malayan Green Dwarf,’ are all highly susceptible to coconut mite. Some observers have reported that certain varieties of coconut in some countries appear to be resistant to coconut mite. A highly resistant Cambodian variety was reported on a research station in Africa. It was suggested that the spherical shape of the fruit of this variety perhaps resulted in a very tight perianth that excluded coconut mites. In a study in St. Lucia, West Indies, highly spherical coconuts had less coconut mite damage than elongated coconuts on the same palm. However, extensive damage of coconut mites on some spherical-fruited coconut varieties has been observed. Biological Control Predatory mites found beneath the coconut perianth and in some cases observed to prey on coconut mites have been reported in various localities. They include Bdella distincta Baker and Balock (Bdellidae); Amblyseius largoensis Muma, Neoseiulus mumai Denmark, N. paspalivorus DeLeon (Phytoseiidae); Lupotarsonemus sp. (Tarsonemidae); and Proctolaelaps bickleyi Bram. (Ascidae). Under natural conditions, predatory mites have a minor effect at best on populations of the coconut mite, but researchers continue to explore the possibilities of biological control of coconut mite. The fungus Hirsutella thompsonii (Fisher), which is widely distributed and known to attack various species of mites, has been isolated from coconut mites in various countries, as has H. nodulosa Petch in Cuba. Control of several species of mites with fungus has been attempted, but success has often depended greatly on environmental conditions. In general, these efforts have been most successful under humid conditions favoring the development of the fungi. However, some recent advances in myco-acaricide development have been encouraging. Because coconut mites are almost microscopic and pass almost all of their life cycle in a cryptic habitat, it appears possible that in some regions the mite may be present at undetected levels. If such regions were known (e.g., if surveys in the South Pacific Region should reveal the presence of the coconut mite at extremely low levels), they would be promising sources of effective natural enemies of the coconut mite. References Navia D, de Moraes GJ, Roderick G, Navajas M (2005) The invasive coconut mite Aceria guerreronis (Acari: Eriophyidae): origin and invasion sources inferred from mitochondrial (16S) and nuclear (ITS) sequences. Bull Entomol Res 95:505–516 Fernando LCP, Moraes GJ, Wickramananda IR (2002) Proceedings of the international workshop on coconut mite (Aceria guerreronis), Sri Lanka, 6–8 January, 2000. Coconut Research Institute, Sri Lanka, 117 pp Howard FW, Abreu-Rodriquez E, Denmark HA (1990) Geographical and seasonal distribution of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), in Puerto Rico and Florida, USA. J Agr 74:237–251 Howard FW, Moore D, Giblin-Davis R, Abad R (2001) Insects on palms. CABI Publications, Wallingford, UK, 400 pp Moore D (2000) Non-chemical control of Aceria guerreronis on coconuts. Biocontrol News Inform 21:83N–87N Moore D, Howard FW (1996) Coconuts. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyid mites – their biology, natural enemies, and control. Elsevier, Amsterdam, The Netherlands, pp 561–569 Coelomomyces Cocoon Breaker A structure found on Lepidoptera pupae, usually on the head, that enables the insect to escape from the cocoon. Coding Strand The strand of the DNA molecule that carries the biological information of a gene and which is transcribed by RNA polymerase into mRNA. Codling Moth, Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) This is one of the most important pests of apple fruit.  Apple Pests and Their Management Codon A triplet of nucleotides that code for a single amino acid. Coelomomyces The phylum Chytridiomycota, once considered a member of the Mastigomycotina, is now included with the Oomycota in the kingdom Protoctista. Within the Chytridiomycetes, Coelomomyces (order = Blastocladiales) is the most notable insect pathogen. This genus contains more than 70 species and has been found worldwide. Coelomomyces is unique among the entomopathogenic fungi in that it requires two different hosts to complete its life cycle. The insect hosts are usually mosquito larvae, although other dipterans such as black flies and midges, as well as some backswimmers (Hemiptera), also can become infected. The alternate hosts are other aquatic arthropods (microcrustaceans) such C as copepods and ostracods. Alternation between hosts is obligatory, i.e., zoospores produced in mosquitoes will not infect other mosquitoes, and zoospores from infected microcrustaceans will not infect other Microcrustaceae. This development of different parasitic stages within two unlike hosts is termed heteroecism and was observed in the phytopathogenic rust fungi before it was discovered in Coelomomyces. Heteroecism may be considered similar to the terms digenetic or heteroxenous, used to describe certain protozoa (Amblyospora) that require two or more hosts for survival. Coelomomyces has not yet been cultured in vitro through its entire, two-phase life cycle. The in vivo culture of several species of Coelomomyces has been successfully achieved by cycling the fungus through its respective host systems, which in some cases can be maintained in small containers. The occurrence of Coelomomyces epizootics is dependent on the presence of both hosts, the relative sizes of their populations, and the age of host mosquito larvae. Studies have shown that infection of anopheline larvae with C. punctatus correlates with the seasonal abundance of the alternate copepod hosts, and that early-instar larvae are more readily infected than those from later instars. In the field, it has been observed that the larvae become infected primarily at dusk. This is apparently due to the dual photoperiodicity of gamete release from the alternate hosts, which, under laboratory conditions, also occurs at this time. Environmental factors such as pH and temperature of the water appear to be much less important in infection rates of mosquito larvae and in the progress of epizootics of Coelomomyces than the relationship between the two host systems. Finally, with respect to host range, some species of the fungus may infect several genera of mosquitoes, while others are specific for a single species. It is significant that under natural conditions, mosquito larvae from later instars can become infected with Coelomomyces. Older larvae particularly are susceptible just after molting, when the cuticle is not yet completely hardened. Infection in older larvae and even in some younger instars exposed to a low level of inoculum may not necessarily kill the 957 958 C Coelomomyces insect. Heavily infected larvae do not pupate and starve to death due to the depletion of nutritional reserves from the fat body by the fungus. In contrast, larvae with light infections may pupate and develop into infected adults. The fungal hyphae migrate from the hemocoel and penetrate the ovaries. Conversion of the fungal hyphae into resting sporangia is apparently stimulated by hormones (e.g., 20-hydroxyecdysone) produced by the mosquitoes after a blood meal; in healthy mosquitoes, the same hormones influence egg maturation. It has been observed that adult Aedes aegyptii mosquitoes infected with C. stegomyiae display normal reproductive behavior with respect to copulation, sperm transfer and storage, and oviposition. However, no eggs are produced because oocytes of infected ovaries do not endocytose vitellogenin and, as a result, vitellin yolk granules cannot form. During oviposition, infected females therefore discharge piles of Coelomomyces resting sporangia, which fill the ovaries rather than eggs. Obviously, this provides an excellent means of dispersal of the pathogen to its alternate host. Meiosis occurs in the germinating, resting sporangia, and the wall-less zoospores generated during this reduction division often are referred to as meiospores. Meiospores are posteriorly uniflagellate and are released from sporangia in masses covered by thin vesicles consisting of the inner regions of mature sporangial walls. Meiospores serve as the infective propagules of the alternate microcrustacean hosts. In the case of C. dodgei, the copepod hosts release substances recognized by the meiospores, increasing the probability of their attachment to the host cuticle. Meiospore attachment can be consolidated by secretion of adhesive material from cytoplasmic vesicles. At the time of attachment, the meiospores encyst and invade the host via a penetration germ tube. In C. psorophorae, appressoria may be produced and may function as an additional mechanism for attachment of the fungus to host surfaces; attachment of this species to host Cyclops vernalis takes place primarily in intersegmental regions. Meiospores are of opposite mating types, and each meiospore develops a thallus that will form a male or female gametangium within the alternate host. In C. dodgei, the male gametangia are bright orange due to the presence of carotene, and the female gametangia are light amber. Both types can occur within an individual copepod, and gametes, i.e., the haploid zoospores released as products of gametangial cleavages, therefore can fuse during swarming within the host. Alternatively, gametes may escape from the microcrustacean cadaver to mate outside the host. The biflagellate zygotes that result from mating of the gametes are the infective propagules of mosquito larvae. Susceptibility of mosquito larvae to infection by Coelomomyces varies and appears to depend upon the ability of the zygotes to attach to host cuticle. Attachment of C. psorophorae zygotes to the cuticle of a susceptible host occurs preferentially at intersegmental membranes, on head capsules, at the bases of anal gills, and around the anus. Attachment is closely associated with encystment of the zygotes. Germination is initiated at one end of the cyst, where an appressorium forms and functions in further attaching the cyst to the host. As germination continues, a penetration tube grows from the appressorium and traverses the cuticle to the epidermal region, where the infecting fungal protoplasts are deposited into host cells. After penetration, the thalli appearing as irregularly shaped, protoplast-like thalli (hyphal bodies) invade other larval tissues, especially the fat body and the hemocoel. There is no apparent host hemocytic response to Coelomomyces hyphal bodies, at least in the case of C. punctatus infecting Anopheles quadrimaculatus. This could be due to masking of the fungal surface by host material or to production of fungal surface components which are interpreted as self by host defense cells. As a Coelomomyces infection progresses within host mosquito larvae, extensive growth and branching of hyphae occurs, and resting sporangia, which will eventually cleave into the meiospores infectious to the alternate host, form to complete the life cycle. References Federici B (1981) Mosquito control by the fungus Culicinomyces, Lagendium, and Coelomomyces. In: Burges HD (ed) Microbial control of pests and plant disease. Academic Press, London, UK, pp 555–572 Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) Lucarotti CJ (1992) Invasion of Aedes aegypti ovaries by Coelomomyces stegomyiae. J Invertebr Pathol 60:176–184 Travland LB (1979) Structures of the motile cells of Coelomomyces psorophorae and function of the zygote in encystment on a host. Can J Bot 57:1021–1035 Whisler HC, Zebold SL, Shemanchuk JA (1975) Life history of Coelomomyces psorophorae. Proc Natl Acad Sci 72:693–696 Coelopidae A family of flies (order Diptera). They commonly are known as seaweed flies.  Flies Coenagrionidae A family of damselflies (order Odonata). They commonly are known as narrow-winged damselflies.  Dragonflies and Damselflies Coevolution Reciprocal, adaptive changes in traits of two populations. Coffee Bean Rot Stink bugs introduce fungi into coffee berries while feeding.  Transmission of Plant Diseases by Insects Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) fernando e. veGa USDA, ARS, Sustainable Perennial Crops Laboratory, Beltsville, MD, USA The coffee berry borer, Hypothenemus hampei (Ferrari), known throughout Latin America as C “la broca del café,” is the most devastating insect pest of coffee throughout the world. This minute insect (0.5–0.8 mm length and 0.2 mm wide) is endemic to Central Africa, and has now spread to most coffee growing regions throughout the world. Infestation levels can be quite high (e.g., Uganda 80%, Colombia 60%, Jamaica 58–85%, Tanzania 90%, Malaysia 50–90%, and Mexico 60%). It is striking that out of more than 850 insects reported on coffee, the coffee berry borer is the only one that has adapted to use the seed of Coffea arabica and Coffea canephora (=robusta) as its food source. Damage begins when an adult female (Fig. 72) bores a hole into the coffee berry and deposits her eggs; larvae feed on the coffee seed, lowering its quality and possibly causing abscission of the berry. An interesting aspect of the insect’s biology is the highly skewed sex ratio favoring females (10:1), which contributes to a high reproductive capacity. Wolbachia, a maternally inherited bacterium known to induce parthenogenetic development and skewed sex ratios favoring females, has been detected in coffee berry borers from 11 different countries. When larvae molt into adults, they mate with their siblings inside the berry; therefore, once females emerge, they are inseminated and ready to deposit eggs into another coffee berry. In contrast to females, males remain in the berry, and are unable to fly. Thus, insect development inside the coffee berry makes this insect very difficult to control. The highly toxic chlorinated hydrocarbon endosulfan has been widely used against the coffee berry borer but some countries have banned its use. Also, the insect has developed resistance to this product. The lack of safe and effective chemical control strategies has led to strong efforts by coffee scientists in many countries to develop biological control methods relying on parasitoids and fungal entomopathogens. Four of the most common coffee berry borer parasitoids originate in Africa: two bethylids (Prorops nasuta Waterston and Cephalonomia stephanoderis Betrem), one eulophid (Phymastichus coffea La Salle), and one braconid (Heterospilus coffeicola Schmiedeknecht). Some of these have been introduced 959 960 C Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) berry borer is being aggressively studied. The insect has also been shown to be associated with 40 species of fungi in 22 genera. Two nematodes have been reported as parasites of the coffee berry borer: Panagrolaimus sp. in India and Metaparasitylenchus hypothenemi in Mexico. Cultural practices such as complete collection of berries on the tree and ground immediately after harvest could greatly reduce coffee berry borer population levels. However, this laborious strategy is not considered a feasible or cost-effective alternative.  Coffee Pests and their Management References Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae), Figure 72 Adult coffee berry borer, Hypothenemus hampei. Drawing by Ann Simpkins (USDA). in coffee producing countries (e.g., Colombia, Jamaica, Mexico) in an attempt to reduce coffee berry borer damage, but their mass production remains expensive due to the need for coffee seeds in which to rear the coffee berry borers used to rear the parasitoids. The most common fungal entomopathogen isolated from the coffee berry borer is Beauveria bassiana, although Isaria fumosorosea, Paecilomyces lilacinus, and Metarhizum anisopliae have also been reported to a lesser extent. The use of B. bassiana as a fungal endophyte to control the coffee Baker PS (1999) The coffee berry borer in Colombia. Final report of the DFID – Cenicafé – CABI Bioscience IPM for Coffee Project, DFID – Cenicafé, Chinchiná, Colombia, 154 pp Brun LO, Marcillaud C, Gaudichon V, Suckling DM (1989) Endosulfan resistance in Hypothenemus hampei (Coleoptera: Scolytidae) in New Caledonia. J Econ Entomol 82:1311–1316 Bustillo PAE, Cárdenas MR, Villalba GA, Benavides MP, Orozco HJ, Posada FFJ (1998) Manejo integrado de la broca del café Hypothenemus hampei (Ferrari) en Colombia. Centro Nacional de Investigaciones de Café (Cenicafé), Chinchiná, Colombia, 134 pp Le Pelley RH (1968) Pests of coffee. Longmans, Green and Co, London, UK, 590 pp Pérez J, Infante F, Vega FE, Holguín F, Macías J, Valle J, Nieto G, Peterson SW, Kurtzman CP, O’Donnell K (2003) Mycobiota associated with the coffee berry borer (Hypothenemus hampei) in Mexico. Mycol Res 107:879–887 Poinar G Jr, Vega FE, Castillo A, Chavez IE, Infante F (2004) Metaparasitylenchus hypothenemi n. sp. (Nematoda: Allantonematidae), a parasite of the coffee berry borer, Hypothenemus hampei (Ferrari) (Curculionidae: Scolytinae). J Parasitol 90:1106–1110 Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:749–758 Varaprasad KS, Balasubramanian S, Diwakar BJ, Ramarao CV (1994) First report of an entomogenous nematode, Panagrolaimus sp. from coffee berry borer, Hypothenemus hampei (Ferrari) from Karnataka, India. Plant Protect Bull 46:42 Vega F, Benavides P, Stuart J, O’Neill SL (2002)Wolbachiainfection in the coffee berry borer (Coleoptera: Scolytidae). Ann Entomol Soc Am 95:374–378 Coffee Pests and their Management Coffee Pests and their Management Juan f. Barrera El Colegio de la Frontera Sur, Tapachula, Chiapas, Mexico The perennial and evergreen nature of the coffee plant (Coffea spp.) favors attack by a number of insects and mites (Table 17, Figs. 73 and 74). All portions of the plants are susceptible to attack, and damage may appear at the seed bed, nursery, plantation, or in the warehouse. Certain pests affect the coffee plant only temporarily, while others live for several generations on the plant. In some instances, the attack may cause the death of the plant, but in most cases the pests only weaken the plant, reducing yield. When the bean is attacked, quality also may be affected. Insects constitute the most numerous group of coffee pests; of more than 850 species of insects that feed on coffee in the world, approximately 200 (23.5%) have been reported in the tropical and sub-tropical areas in America. Out of these, hardly thirty species, mostly indigenous, cause losses considered important. The pests and the seriousness of the problems they cause vary from one country to another, and from one area to another. The coffee pest that is considered the most important in tropical America is the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae), now cosmopolitan but originating in Africa. The coffee leaf miner, Leucoptera coffeella Guérin-Méneville (Lepidoptera: Lyonetiidae), and the root mealybugs (Pseudococcidae) are causing serious problems in several countries. Bugs of the genus Antestiopsis (Pentatomidae), which are very harmful in Africa, have not yet been reported in the American hemisphere. Most of the insects that are found in coffee plantations are beneficial because they contribute to plant pollination, degrade organic matter, or feed on phytophagous organisms. A study conducted in Mexico showed that parasitic and C predatory organisms, which regulate the populations of many pests, represented 42% of the total of species collected in a coffee plantation. For this reason, it is important to protect and maintain the natural enemies of pests, avoiding the indiscriminate use of chemical pesticides and some agronomic practices that are harmful to natural control. The goal of this section is to describe the biological and ecological characteristics of the main insects and mites of C. arabica L. and C. canephora Pierre ex Froehner, the damage caused by these pests, their natural enemies, and pest management in coffee growing countries of tropical America. The pests to be described are listed in Table 17, which also includes the parts of the plant that are damaged and the development stage of the coffee plant that they damage. The criterion applied to include these organisms in the category of “major pests,” was that they were reported in at least one of the manuals on coffee pests that have been published in Brazil, Colombia, Costa Rica, Cuba, El Salvador, Guatemala, Honduras, Jamaica, Mexico or Venezuela. Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) Distribution This is the most serious insect pest of coffee worldwide. It originated in Africa. In the Americas, it is found in coffee plantations from Mexico to Brazil, including some countries in the Caribbean region such as Cuba, Jamaica, the Dominican Republic and Puerto Rico. Damage and Economic Importance Coffee berry borer (Fig. 73) is a direct pest because it causes direct damage to the product to be harvested, the coffee bean. The attacked green, ripe and dry fruits or berries usually show a hole 961 962 C Coffee Pests and their Management Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Brazil Nymph, adult Leaves Brazil, Jamaica, Mexico Nymph, adult Leaves Olygonychus coffeae (Nietner) Guatemala, Mexico Nymph, adult Leaves Olygonychus ilicis (McGregor) Brazil, Guatemala Nymph, adult Leaves Olygonychus punicae (Hirst) El Salvador Nymph, adult Leaves Olygonychus yothersi (McGregor) Colombia, Costa Rica, Venezuela Nymph, adult Leaves All coffee growing countries in America Larva, adult Bean Plagiohammus maculosus (Bates) Costa Rica, El Salvador, Guatemala, Honduras, Mexico Larva Stem, root Plagiohammus mexicanus Breuning Mexico Larva Stem, root Plagiohammus spinipennis (Thomson) Mexico Larva Stem, root Brachyomus quadrinodosus (Lacordaire) Venezuela Adult Leaves Cleistolophus similis Sharp Costa Rica Adult Leaves Compsus sp. Colombia Adult Leaves Epicaerus capetillensis Sharp Guatemala, Honduras, Mexico Adult Leaves Hypothenemus hampei (Ferrari) Mexico to Brazil, including Cuba, Jamaica, Dominican Republic, and Puerto Rico Larva, adult Fruit, bean Lachnopus buchanani Marshall Cuba Adult Leaves Macrostylus boconoensis Bordón Colombia, Venezuela Adult Leaves Pantomorus femoratus Sharp Costa Rica Adult Leaves Acari: Tarsonemidae Polyphagotarsonemus latus (Banks) Acari: Tenuipalpidae Brevipalpus sp. Acari: Tetranychidae Coleoptera: Anthribidae Araecerus fasciculatus (DeGeer) Coleoptera: Cerambycidae Coleoptera: Curculionidae Coffee Pests and their Management C Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Pantomorus godmani Crotch Brazil Adult Leaves Steirarrhinus sp. Costa Rica Adult Leaves Xylosandrus morigerus (Blandford) Mexico to Brazil Larva, adult Young stems, branches Anomala sp. El Salvador Larva Root Dyscinetus picipes Burmeister Cuba Larva Root Phyllophaga spp. Widely distributed in coffee Larva plantations in America Root Phyllophaga latipes (Bates) El Salvador Larva Root Phyllophaga menetriesi (Blanchard) El Salvador Larva Root Phyllophaga obsoleta (Blanchard) El Salvador Larva Root Phyllophaga sanjosecola Saylor Costa Rica Larva Root Phyllophaga vicina Moser Costa Rica Larva Root Coleoptera: Scarabaeidae Hemiptera: Aphididae Toxoptera auranti (Boyer de Fonscolombe) Tropical and sub-tropical Nymph, adult areas of the Old World. Widely distributed in coffee plantations in America Leaves, buds and other tender parts of the plant Coccus spp. Mexico Nymph, adult female Aerial part of the plant Coccus hesperidum L. Guatemala, Mexico Nymph, adult female Aerial part of the plant Coccus viridis (Green) Brazil, Colombia, Costa Nymph, adult female Rica, Cuba, Ecuador, El Salvador, Guatemala, Honduras, Jamaica, Mexico, Puerto Rico, Surinam, Venezuela Aerial part of the plant Parasaissetia sp. Colombia Nymph, adult female Aerial part of the plant Parasaissetia nigra (Nietner) El Salvador, Guatemala, Puerto Rico, West Indies Nymph, adult female Aerial part of the plant Saisettia spp. El Salvador, Mexico Nymph, adult female Aerial part of the plant Hemiptera: Coccidae 963 964 C Coffee Pests and their Management Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Saisettia coffeae (Walker) Brazil, Costa Rica, Cuba, El Nymph, adult female Salvador, Guatemala, Honduras, Mexico, Dominican Republic, Venezuela Aerial part of the plant Saisettia olae (Oliver) Brazil, Cuba, Guatemala, Mexico Aerial part of the plant Nymph, adult female Plant parts affected Toumeyella sp. Venezuela Nymph, adult female Root Toumeyella liriodendri (Gmelin) Guatemala Nymph, adult female Root Brazil Nymph, adult female Aerial part of the plant Chrysomphalus sp. Guatemala Nymph, adult female Aerial part of the plant Chrysomphalus dictyospermi (Morgan) Guatemala Nymph, adult female Aerial part of the plant Ischnaspis longirostris (Signoret) Colombia, Cuba, Guatemala Nymph, adult female Aerial part of the plant Lepidoshaphes beckii (Newman) Venezuela Nymph, adult female Aerial part of the plant Selenaspidus articulatus (Morgan) Colombia, Ecuador, Mexico Nymph, adult female Aerial part of the plant Venezuela Nymph, adult female Aerial part of the plant Nymph, adult female Aerial part of the plant Brazil Nymph, adult female Aerial part of the plant Guatemala Nymph, adult female Root Hemiptera: Cerococcidae Cerococcus catenarius Fonseca Hemiptera: Diaspididae Hemiptera: Margarodidae Icerya purchasi Maskell Hemiptera: Ortheziidae Insignorthezia insignis Browne Brazil, Colombia Praelongorthezia praelonga (Douglas) Hemiptera: Pseudococcidae Brevicoccus sp. Ceroputo sp. Costa Rica Nymph, adult female Root Dysmicoccus sp. Colombia, Ecuador Nymph, adult female Root Dysmicoccus bispinosus (Beardsley) Brazil, Guatemala, Honduras, Mexico Nymph, adult female Root Dysmicoccus brevipes (Cockerell) Costa Rica, El Salvador, Guatemala, Honduras, Mexico Nymph, adult female Root Coffee Pests and their Management C Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Ferrisia virgata (Cockerell) Brazil, Mexico, West Indies Nymph, adult female Aerial part of the plant Geococcus sp. Mexico, Venezuela Nymph, adult female Root Geococcus coffeae Green El Salvador, Guatemala, Honduras, Surinam Nymph, adult female Root Geococcus radicum Green El Salvador Nymph, adult female Root Neochavesia caldasiae (Balachowsky) Colombia Nymph, adult female Root Rhizoecus sp. Mexico, Venezuela Nymph, adult female Root Rhizoecus andensis Hambleton Colombia Nymph, adult female Root Rhizoecus coffeae Laing Costa Rica Nymph, adult female Root Paraputo sp. Guatemala Nymph, adult female Root Planococcus citri (Risso) Brazil, Colombia, Costa Rica, Cuba, El Salvador, Guatemala, Honduras, Jamaica, Mexico, Puerto Rico Nymph, adult female Root, aerial part of the plant Planococcus halli Ezzat & McLonnell Guatemala Nymph, adult female Root Pseudococcus elisae (Borchsenius) Guatemala Nymph, adult female Root Pseudococcus longispinus (Targioni-Tozzeti) Guatemala Nymph, adult female Root Pseudococcus jongispinus Targioni-Tozzetti Mexico Nymph, adult female Aerial part of the plant Puto sp. Costa Rica Nymph, adult female Root Puto antioquensis (Murillo) Guatemala Nymph, adult female Root Rhizoeccus campestris (Hambleton) Guatemala Nymph, adult female Root Rhizoeccus caticans (Hambleton) Guatemala Nymph, adult female Root Rhizoeccus kondonis Kuwana Guatemala Nymph, adult female Root Rhizoeccus nemoralis Hambleton El Salvador, Honduras Nymph, adult female Root Acromyrmex spp. Venezuela Adult Leaves Acromyrmex coronatus (F.) Brazil Adult Leaves Acromyrmex octospinosus (Wheeler) Trinidad Adult Leaves Hymenoptera: Formicidae 965 966 C Coffee Pests and their Management Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Atta spp. Guatemala, Ecuador, Nicaragua, Venezuela Adult Leaves Atta cephalotes (L.) Colombia, Costa Rica, Mexico, Surinam, Trinidad Adult Leaves Atta fervens Say Mexico Adult Leaves Atta insularis GuérinMéneville Cuba Adult Leaves Atta laevigata Smith Brazil Adult Leaves Atta mexicana (Smith) Guatemala, Mexico Adult Leaves Atta sexdens (L.) Brazil Adult Leaves Atta sexdens rubropilosa Forel Brazil Adult Leaves Colombia Larva Leaves Colombia Larva Leaves Dalcera abrasa Herrich-Schaeffer Brazil Larva Leaves Zadalcera fumata Schaus Brazil Larva Leaves Colombia Larva Leaves Glena sp. Brazil Larva Leaves Oxydia spp. Colombia Larva Leaves Oxydia saturniata Guenée Brazil Larva Leaves Phobetron hipparchia (Cramer) Brazil, Colombia Larva Leaves Sibine spp. Colombia Larva Leaves Widespread wherever coffee is grown in the Neotropical area Larva Leaves Megalopyge lanata (Stoll) Brazil, Colombia Larva Leaves Podalia sp. Brazil Larva Leaves Lepidoptera: Apateloididae Olceclostera moresca (Schaus.) Lepidoptera Arctiidae Estigmene acrea (Drury) Lepidoptera: Dalceridae Lepidoptera: Elachistidae Stenoma cecropia Meyrick Lepidoptera: Geometridae Lepidoptera: Limacodidae Lepidoptera: Lyonetiidae Leucoptera coffeella (GuérinMéneville) Lepidoptera: Megalopygidae Coffee Pests and their Management C Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Agrotis spp. Colombia, Costa Rica, Ecuador, El Salvador Larva Stems of small plants in germinating seedbeds or recently transplanted plants Agrotis ipsilon (Hufnagel) Brazil Larva Stems of small plants in germinating seedbeds or recently transplanted plants Agrotis repleta Walker Venezuela Larva Stems of small plants in germinating seedbeds or recently transplanted plants Feltia spp. Costa Rica, El Salvador, Venezuela Larva Stems of small plants in germinating seedbeds or recently transplanted plants Pseudoplusia includens (Walker) Honduras Larva Leaves Spodoptera sp. Colombia, Costa Rica, Ecua- Larva dor, El Salvador Stems of small plants in germinating seedbeds or recently transplanted plants Spodoptera eridania (Stoll) Venezuela Larva Stems of small plants in germinating seedbeds or recently transplanted plants Spodoptera frugiperda (Smith) Costa Rica, Brazil Larva Stems of small plants in germinating seedbeds or recently transplanted plants; leaves Trichoplusia ni (Hübner) Colombia Larva Leaves Oiketicus geyeri (Berg) Brazil Larva Leaves Oiketicus kirbyi Lucas Brazil, Cuba Larva Leaves Automeris sp. Brazil, Colombia Larva Leaves Automeris complicata Walker Brazil Larva Leaves Lepidoptera: Noctuidae Lepidoptera: Psychidae Lepidoptera: Saturniidae 967 968 C Coffee Pests and their Management Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of coffee in tropical America (Continued) Taxon (scientific and common name) Country where the insect/ mite is reported as coffee pest Developmental stage feeding in/on the plant Plant parts affected Automeris coresus Boisduval Brazil Larva Leaves Automeris illustris Walker Brazil Larva Leaves Eacles imperialis magnifica (Walker) Brazil Larva Leaves Eacles masoni Schaus Ecuador Larva Leaves Lonomia circunstans (Walker) Brazil Larva Leaves Paroecanthus guatemalae Saussure Guatemala, Honduras Adult female Stem, branch Paroecanthus niger Saussure El Salvador, Guatemala Adult female Stem, branch Gongrocnemis sp. Guatemala Nymph, adult Leaves, buds, fruit pulp, beans Idiarthron atrispinum (Stål) Costa Rica, Guatemala Nymph, adult Leaves, buds, fruit pulp, beans Idiarthron subquadratum Saussure & Pictet Colombia, Guatemala, El Salvador, Honduras, Mexico Nymph, adult Leaves, buds, fruit pulp, beans Orthoptera: Gryllidae Orthoptera: Tettigoniidae on its apical portion. The hole is located at the center or ring of the berry’s ostiole and the emission of sawdust can be observed through this hole. Its attack reduces the yield and affects the bean quality. Characteristic damage includes the rotting of developing beans as a result of saprophytic microorganisms that enter through the hole, the drop of young berries due to attack, and the loss of bean weight due to insect feeding. The borer can cause bean yield losses of 30–35% with 100% of perforated berries at harvest time; nevertheless, damage can be greater if harvest is delayed. All the commercial coffee varieties and species are attacked by this insect. However, it shows preference for C. canephora, and its multiplication is also higher on beans of this coffee species. Recently it was suggested that H. hampei serves as a vector for Aspergillus ochraceus Wilh., which produces ochratoxin A, a potent toxin that sometimes contaminates green coffee beans, roasted coffee, and coffee brews, including instant coffee. Description The egg is elliptical, crystalline and yellowish toward maturity. Its length varies from 0.52 to 0.69 mm. The larva is white-yellowish, without legs, with a “C”-shaped body and a wide thoracic region. The head is light brown, with visible and forward-extending mandibles. Visible hairs spread over the head and body. Females molt twice and males once. The length of the last larval instar is from 1.88 to 2.30 mm. The pre-pupa is similar to the larva, but its color is milky-white, Coffee Pests and their Management C Coffee Pests and their Management, Figure 73 Some coffee pests: (a) Coffee berry borer, Hypothenemus hampei (Curculionidae) infesting a coffee berry; (b) Damage of coffee leaf by coffee leaf miner, Leucoptera coffeella (Lyonetiidae); (c) Root mealybugs (Pseudococcidae); (d) Scale insects on coffee leaf (Coccidae). its body is less curved, and it does not feed. The pupa is milky-white and yellowish towards maturity. Many of the adult’s characteristics can be seen in the pupal stage. The pupa varies from 1.84 to 2.00 mm long. The adult is elongated with a cylindrical body slightly arched towards the end of the abdomen. It is about 1.50–1.78 mm long and its body is bright black, although 969 970 C Coffee Pests and their Management Coffee Pests and their Management, Figure 74 Some additional coffee pests: (a) Coffee branch perforated by Xylosandrus morigerus (Curculionidae); (b) Coffee stem attacked by a stem borer, Plagiohammus maculosus (Cerambycidae); (c) Aphids on coffee leaf; (d) Adults of a katydid, Idiarthron subquadratum; (Tettigoiidae) (e) Oviposition by a bush cricket, Paroecanthus (Gryllidae) on the stem of a coffee bush. Coffee Pests and their Management yellowish when emerging from the pupa. The head is ventrally located and is protected by the pronotum. The antennae are elbowed and clubbed at the ends. Mouthparts are the typical chewing type and the elytra are convex and possess longitudinal grooves that alternate with longitudinal series of bristles. Females have well-developed wings that allow them to fly, while the males’ wings are atrophied. Females are easily differentiated from males because they are larger. Biology and Ecology Adult females initiate the infestation. In general, a berry is infested by a single female. If the coffee bean is watery or milky, the insect tends to abandon it and the bean usually rots. But if the bean consistency is hard enough, the founding female constructs a gallery where she lays the eggs. The eggs are oviposited one by one, forming small groups within the coffee bean. The female lays from 1 to 3 eggs per day during the first 15–20 days; afterwards, the egg laying diminishes gradually. Both the founding female and the larvae build tunnels in the bean, where they also feed. Pupation takes place within the coffee bean where the larva hatched. The duration of the biological cycle, from egg to adult, varies according to the temperature: 21 days at 27°C, 32 days at 22°C and 63 days at 19.2°C. As the first adult offspring appear, the population inside an infested bean typically consists of 25–30 individuals in all stages of development, of which there are approximately 10 females for each male. Mating is conducted between siblings inside the bean. The mated females leave the bean where they developed to look for another where they will oviposit. Several generations occur while berries are available. After coffee harvest, the borer continues to reproduce in the non-harvested berries located on the plant and on the ground. In locations with low rainfall, where there is a clearly defined period between harvests, the C adults find refuge in the black, dry berries. Adult females emerge massively from these old berries with first rainfall, initiating the infestation by attacking berries from the earliest flowerings of the new harvest. Natural Enemies Coffee berry borer is attacked by several natural enemies. Four parasitoid species from Africa are the best known: Prorops nasuta Waterston (from Cameroon, Ivory Coast, Zaire, Kenya, Tanzania, Togo, Uganda) and Cephalonomia stephanoderis Betrem (Ivory Coast, Togo) (both Hymenoptera: Bethylidae), and two solitary ectoparasitoids of the larva, pre-pupa and pupa, Heterospillus coffeicola Schimideknecht (Hymenoptera: Braconidae) (Cameroon, Zaire, Kenya, Tanzania, Uganda) (a free-living wasp that deposits a single egg near a borer’s egg cluster in a recently attacked berry) and Phymastichus coffea LaSalle (Hymenoptera: Eulophidae) (Togo, Kenya) (a gregarious endoparasitoid of H. hampei adults which parasitizes the borer during the berry perforation). Other parasitoids that have been reported attacking H. hampei include Aphanogmus dictyna (Waterston) (Hymenoptera: Ceraphronidae) (Uganda), Sclerodermus cadavericus Benoit (Hymenoptera: Benthylidae) (Uganda, Zaire, Kenya), Cephalonomia hyalinipennis Ashmead (Mexico) and Cryptoxilos sp. (Hymenoptera: Braconidae) (Colombia). In Brazil and Colombia, there are reports of an undescribed species of Cephalonomia parasitizing H. hampei. Some of the predators that have been recorded include Dindymus rubiginosus (F.) (Hemiptera: Pyrrhocoridae) (Indonesia), Calliodes, Scoloposcelis (Hemiptera: Anthocoridae) (Colombia), and Leptophloeus sp. near punctatus Lefkovich (Coleoptera: Laemophloeidae) (Togo, Ivory Coast). However, most of the predators of H. hampei reported from around the world (most of them anecdotal records) have been ants (Hymenoptera: Formicidae), including Azteca instabilis (F. Smith), 971 972 C Coffee Pests and their Management Crematogaster curvispinosa Mayr, C. torosa Mayr, Dolichoderus bituberculatus Mayr, Pheidole radoszkowskii Mayr, and Solenopsis geminata (F.). Unknown species of Azteca, Brachymyrmex, Paratrechina, Pheidole, Prenolepis and Wasmannia have been recorded as well. Several entomopathogenic fungi attack the coffee berry borer, but Beauveria bassiana (Balsamo) Vuillemin is the most common species infecting H. hampei adults under natural conditions. Other fungi recorded infecting H. hampei are Fusarium oxysporum Schlechtend, F. avenaceum (Fr.) Sacc., Hirsutella eleutheratorum (Nex ex Gray) Petch., Metarhizium anisopliae (Metschnikoff) Sorokin, Nomuraea rileyi (Farlow) Samson, Paecilomyces amoenoroseus (Hennings) Samson, P. farinosus (Holm. ex S.F. Gray), P. fumosoroseus (Wize) Brown & Smith, P. javanicus (Friederichs & Bally) Brown & Smith, P. lilacinus (Thom.) Samson, and Verticillium lecanii (Zimmerman). Some of these fungi, such as M. anisopliae and P. lilacinus, have been isolated from H. hampeiinfested berries collected from the soil. Metaparasitylenchus hypothenemi Poinar (Tylenchida: Allantonematidae), an entomopathogenic nematode attacking H. hampei adults, has been reported in Mexico and appears to have a wide distribution in coffee plantation in Mexico and Central America This nematode cause sterility in female borers. The natural parasitism by an undescribed species of Panagrolaimus (Rhabditida: Panagrolaimidae) has been reported in H. hampei in India and Mexico. M. hypothenemi and Panagrolaimus sp. were found infecting the same H. hampei adults in Mexico. Species from Heterorhabditidae and Steinernematidae (Rhabditida) are able to infect H. hampei in the laboratory, but this has not been observed in the field. In Colombia, infections in the coffee berry borer caused by bacteria such as Bacillus sp. and Serratia sp. were observed. Also, infections of proteobacterium Wolbachia in H. hampei adults have been reported from samples around the world. The microsporidian Mattesia sp. was observed in a population of laboratory-reared insects. Management An integrated pest management strategy is used against the coffee berry borer. The principal tactics are cultural control, biological control, use of traps baited with attractants, and chemical control with synthetic insecticides. Sampling infested berries is used for pest control decision-making. Sampling Infested Berries The proportion of infested berries is calculated based on the following sampling protocol: in an area of 1–5 ha, 20 uniformly distributed sites are selected; at each site five coffee plants in a row are selected; 20 berries of each coffee plant are examined (without tearing them off), and the number of perforated berries is recorded. Cultural Control There are a number of cultural practices that may be used to minimize damage by borers. The berries left on the plant before maturity and on the ground after harvest are collected and boiled for 5 min to eliminate the borers in them. This practice is also called “manual control” or “rere.” Weeds are controlled after the harvest in order to facilitate the collection of berries from the ground and to increase the mortality of H. hampei by dehydration of the berries. The coffee and shade plants are pruned to create less favorable environmental conditions for multiplication of the borer. Coffee plant density is decreased because high sowing densities favor infestation. The coffee plants are fertilized so that they have more uniform flowerings. Varieties with the same fruiting pattern are used because the early flowering varieties are an infestation source for late flowering varieties; however, coffee varieties or species which flower earlier or later than the main variety can be used as “trap crops,” if managed properly. The harvest is conducted as the fruits ripen. Coffee Pests and their Management Biological Control The natural enemies most often used against the borer in tropical America have been the parasitoids C. stephanoderis, P. nasuta and P. coffea, and the entomopathogenic fungus B. bassiana. These three parasitoids were introduced to tropical America from Africa. They are established in most of the countries where they have been released. Nevertheless, classical biological control with these African parasitoids has not been sufficient to reduce the borer population below the economic injury level. Yearly inoculative and inundative releases of parasitoids have been used with better results. However, inundative releases are expensive because mass rearing methods and facilities have not been developed for area-wide releases. Parasitoids are produced for inoculative releases in laboratories where the borer is reared mostly in parchment coffee (35% humidity) for use in rearing the parasitoids. A rearing system for H. hampei in an artificial diet has been developed; however, its application for mass production of parasitoids is not fully employed. An alternative and less intensive rearing system to produce parasitoids for inoculative releases is production of the parasitoids in rural areas, also known as “parasitoid rural rearing.” In this system, the coffee growers rear the parasitoids at their farms or communities. Such rearing is conducted using coffee berries infested by the borer in the field. Regardless of the rearing method used, annual releases of parasitoids are needed to manage the borer population. The use of B. bassiana for borer control is more developed than is the use of parasitoids. Its success has resulted from the relatively easy propagation, formulation and application of this fungus. Strains of B. bassiana are commonly collected for mass production from infected H. hampei females in the field. Rice grains are used as the propagation substrate for this entomopathogen. The fungus requires high relative humidity for germination of the spores and it is very susceptible C to sunlight. Early in the morning is the most effective time to apply it in the field, when the borer is starting to penetrate the coffee berry. Insect Traps Traps are used for monitoring and control of the coffee berry borer. They are made using 2 L plastic bottles into which one or more windows have been cut to allow the entry of flying females. Borers are attracted by a mixture of methanol and ethanol (1:1 or 3:1) and they are caught and drowned in the water placed at the bottom of the trap. Typically, 16–25 traps are deployed per hectare. Each trap is suspended from a branch of a coffee plant at 1.2–1.5 m above the ground. Borers captured are removed from the traps and counted weekly. The best time to use the traps for H. hampei control is after the harvest, during the massive emergence of females from old berries. Better results for suppression of insect infestation in the next harvest can be obtained by combining the use of traps with strict sanitation. Chemical Control There are several chemical insecticides used for borer control, among which endosulfan is outstanding for its ability to cause high mortality of H. hampei. However, this organochlorine insecticide is being seriously questioned for negative side effects (it is highly toxic to fish and bees, and it causes secondary pest outbreaks by eliminating the natural enemies); borer resistance (apparently this pest is not resistant to endosulfan in tropical America; nevertheless, there is concern about the development of resistance, as in the case of New Caledonia); and sanctions in the international market due to the possible presence of residues in the coffee bean. The insecticide should only be used if the borer population reaches the economic threshold. The best time for spraying is when the adult borer starts 973 974 C Coffee Pests and their Management penetrating the fruit, at the so-called semi-consistency stage of development (about 20% dry weight in the bean). This period varies, according to the temperature, from 90 to 140 days after the main flowering. Formerly, treatments were throughout the plantation, but now sprays are directed only at infested areas. Coffee Leaf Miner, Leucoptera coffeella (Guérin-Méneville) (Lepidoptera: Lyonetiidae) Distribution This species is found in the Neotropics: Mexico, Central America, South America and the Caribbean region. It is widespread wherever coffee is grown. Damage and Economic Importance In some areas of tropical America, the coffee leaf miner is considered to be the principal insect pest of coffee; certainly this is the case in some coffee-growing areas in Brazil. Leaves are the only plant organs damaged by this insect. The damage is caused by the larva. Four larvae per leaf may cause leaf drop. The affected leaves show irregular light-brown spots. If the damaged surface of the leaf is rubbed, the leaf separates into two layers and between them is found a small white worm, from 2 to 5 mm in size. The coffee leaf miner lesions may be confused with the symptoms of Anthracnose (Colletotrichum sp.), but in the latter case the leaf layers do not separate when rubbed. Four months after flowering, a reduction in the rate of growth of the coffee berries and an increase in leaf production take place; this allows the plant to compensate for the damage caused by the miner. But when the fruit growth starts again, if there is more than one leaf miner lesion per leaf it will result in economic damage. The damage increases if simultaneously the plant is under drought stress. Attack of coffee by leaf miner can cause severe defoliation. In Ecuador, defoliation between 70 and 90% has been reported on C. arabica and from 30 to 40% on C. canephora. The lack of leaves on the plant reduces the photosynthetic activity, and consequently the availability of nutrients for the fruits. In Brazil, when 94–95% of the leaves were mined, a reduction in yield between 68–80% has been observed. Description The egg is oval, translucent yellow and similar to a flattened volcano in profile. It is 0.28 mm long, 0.18 mm wide, and 0.08 mm tall. The larva has a dorsoventrally flattened body with a more pronounced flattening of the head and the first thoracic segment. The true legs are found on the 1st, 2nd and 3rd thoracic segments but four pairs of prolegs occur on the 6th, 7th, 8th and 13th abdominal segments. It has four larval instars. The larva attains a length of 4.5 mm. The pupa is white in the initial stage and ochre towards maturity, except for the dorsal portion, which remains white. The pupa is covered by a white cocoon which resembles an elongated “H” or “X.” The adult is a small moth between 2.0 and 3.0 mm long with its body covered by silvery scales. The antennae are long and thin. The front wings possess a gray oval point distally, surrounded by a black line and edged by a yellow stripe that extends along the margin. Males tend to be slightly smaller than females. Biology and Ecology The female usually lays its eggs irregularly on the upper surface of the darkest, most mature leaves, particularly on the middle and lower parts of the coffee plant. Eggs are laid individually or in small clusters of up to seven eggs, with a total fecundity that varies between 30 and 80 eggs. Upon hatching, the larva makes a semi-circular cut at its base Coffee Pests and their Management and penetrates rapidly into the leaf, where it moves about, mining the palisade parenchyma tissue. When ready to pupate, the fully developed larva leaves the gallery very early in the morning, making a semi-circular cut on the face of the leaf, through which it slips down by a silk thread which it secretes from the mouth. Cocoon formation and pupation take place on the lower face of the coffee leaf, often on a curvature of the leaf or close to a protruding vein. The duration of the life cycle, from egg to adult, lasts between 25 and 75 days, depending on the temperature. Several generations occur annually, particularly in coffee plantations with full sunlight or only lightly shaded. The abundance of L. coffeella is significantly affected by the onset of rainfall, and by natural enemies, which are very numerous after the end of the dry season. Natural Enemies The coffee leaf miner is attacked by a large number of parasitoids; predators and some insect pathogens have also been recorded. More than 20 morphospecies of parasitoids wasps (Hymenoptera) have been reported in tropical America. Eulophidae are the most common parasitoids of L. coffeella; this group is largely unknown because keys for neotropical species do not exist. In Mexico, Neochrysocharis was the genus with the greater number of morphospecies, and also the one that was collected most frequently. It was followed, in order of abundance, by Pnigalio, Closterocerus, and Zagrammosoma. Of two braconids collected in Mexico, Stiropius letifer (Mann) was the most abundant and most widely distributed. Wasps (Vespidae) are the most important predators of coffee leaf miner in Brazil, but in Mexico, the most important predators are ants (Formicidae). The bacteria Pseudomonas aeruginosa (Schroeter) Migula and Erwinia herbicola (Löhnis) Dye, and the fungus Cladosporium sp., have been reported infecting L. coffeella. C Management There are several useful approaches to management of coffee leaf miner. population. Sampling is recommended prior to initiating chemical control. Sampling Damaged Leaves The recommended sampling protocol follows: sampling is initiated when the coffee flowers, and is conducted monthly until the berries stop growing. The coffee plantation to be sampled is divided into areas not larger than one hectare. The sampling is conducted by selecting a zigzag path across the coffee plantation and by selecting 12 coffee plants at random. From each coffee plant, 25 leaves are selected at random, and the number of leaves with mines is recorded. The first two pairs of leaves at the tip of the branches are not sampled. Cultural Control The shade canopy of coffee plantation should not be trimmed immediately after harvest; it should be thinned only when the onset of the rainy season is imminent. Adequate soil fertilization is important. Thick mulch coverage of the soil should be maintained. High coffee plant densities should be avoided. The coffee plant should be pruned to stimulate vigorous growth. Damaged leaves should be collected and placed in containers that allow the escape of parasitoids but not of the coffee leaf miner. Biological Control The introduction of natural enemies into new areas has not been widely explored. The most important action conducted so far has been to protect the already existing natural enemies by 975 976 C Coffee Pests and their Management avoiding the use of broad-spectrum, residual contact insecticides. The natural control exerted by the coffee leaf miner’s natural enemies varies from 2 to 70%; however, in most cases it is unnecessary to resort to the use of chemical control. Regrettably, the use of chemical insecticides may eliminate a large portion of the beneficial organisms, causing pest resurgence and making it difficult to implement control. In certain countries like Honduras, high and recurring L. coffeella infestations have diminished significantly when the use of chemical control is not applied for several years and the beneficial fauna is restored. This supports the idea that coffee leaf miner control should not be based on use of insecticides in order to avoid disrupting the actions of parasitoids and predators. Chemical Control Numerous chemical insecticides can be used for suppression of L. coffeella and protection of foliage. These products include both organophosphate and pyrethroid insecticides. They are inexpensive and can be applied at the same time with other agrochemicals, but they are highly toxic and they are more likely to cause ecological disturbances. Organophosphorates are often applied twice at an interval of 30–45 days, with an additional application in cases of severe attack. In the case of pyrethroids, one or two applications at an interval of 45–60 days are recommended. The application of granular insecticides with systemic action to the soil is also recommended in cases where it is difficult to apply foliar sprays. Soil applications interfere much less with the natural enemies of the coffee leaf miner, and this approach can be used to control pests and soil diseases simultaneously. Granular insecticides should be shallowly buried at the drip line of the plant once a year during the rainy season. Where this type of product is used, it is recommended that harvest occur 90 days after application. Root Mealybugs (Hemiptera: Pseodococcidae) Distribution Root mealybugs are found in Neotropical countries where coffee is grown. The principal root mealybugs affecting coffee plants in tropical America are shown in Table 17. Damage and Economic Importance These insects attack the coffee plant roots and some species also affect the foliage. The foliage of attacked coffee plants appears withered, the color of the leaves fade, and they have copper, brown or necrotic edges. Additionally, total or partial leaf drop may occur. These symptoms are more evident during the dry season. In case of serious attacks by Dysmicoccus bispinosus (Beardly), a thick, cork-like, dark crust covers the main and secondary roots; the attacked roots lose their absorbent root hairs. Heavily attacked plants perish. Infestation appears to be associated with ants (Formicidae). The symptoms may be confused with the symptoms of fungal diseases and with physiological plant problems. In the case of Neorhizoeccus coffeae (Laing) and D. brevipes (Ckll.) infestations, the branches turn whitish and the affected root seems to be covered with flour, the crust separates easily, and considerable deteriorated tissue appears. The attacked plants have little anchorage and are easily dislodged. Root mealybugs have become important coffee pests in some areas of tropical America during the last 20 years. In Guatemala, the most harmful species is D. bispinosus; in Costa Rica, N. coffeae and D. brevipes; in El Salvador, D. brevipes, Rhizoeccus nemoralis Ham. and Geococcus coffeae Green; and in Colombia, Chavesia caldasiae (Balachowsky). At some coffee plantations in Colombia, Planococcus citri (Risso) has also appeared as a pest, causing up to 30% yield loss in the attacked trees. Other forms of damage caused by root mealybugs include excessive extraction of potassium, destruction of the absorbent root hairs, Coffee Pests and their Management development of small rotting areas which tend to atrophy, and enhanced entry of plant pathogens. This damage creates a general condition of weakness, slow growth and plant death in many cases. Dysmicoccus brevipes weakens the coffee plants but it rarely kills them. In Costa Rica, plants with more than 20 mealybugs per liter of soil are more susceptible to infection by the fungus Cercospora coffeicola Berk & Cooke. Damage is more apparent on nutrient-deficient soils, and where weeds are abundant. Plants in seed beds and tree nurseries are also attacked. The varieties of C. arabica grown in Central America (e.g., Caturra, Catuaí, Bourbon) are susceptible to the mealybug attack, while tolerance has been observed on C. canephora, C. dewevrei De Wild. & Durand, and C. excelsa Chev. Description Mealybug eggs are small (0.5 mm). The nymphs are oval, slightly swollen, usually white, yellow or pinkcolored, and covered by a white waxy-mealy dust with waxy filaments projecting laterally. The female nymphs molt three times, and the males, contrary to the females, form a waxy cocoon in the third instar, where they pupate. The adult females have no wings and they are similar to the nymphs but larger. Smaller species, such as Geococcus and Rhizoecus, are from 1.5 to 2.0 mm long and the larger ones, such as Dysmicoccus and Pseudococcus, are from 2.5 to 5.0 mm long. Males are white, fragile-looking, smaller than the females, and they possess a pair of wings and a pair of terminal filaments. Biology and Ecology Mealybugs generally live attached to the coffee root, forming numerous colonies. Their reproduction may be sexual or parthenogenetic (partial or total). Eggs are laid in groups and covered by a layer of cotton-like wax or by an egg sac of crystalline wax filaments. A single female may deposit 300–600 eggs. C Other species, such as Pseudococcus adonidum (L.) are oviparous. Females die shortly after the eggs hatch. Upon eclosion, the small nymphs start looking for an appropriate place to settle on the plant root; at the selected site, they insert their mouthparts, and feed by suctioning the sap from the root. Some of them settle down permanently on a site until they reach maturity, and others may change their feeding site by moving short distances. Depending on the type of soil, the humidity, aeration and age of the coffee plant, they usually place themselves between 10 and 60 cm under the soil surface, their population diminishing as the soil depth increases. Different species prefer different parts of the root. For example, D. brevipes and R. nemoralis prefer the main and the lateral roots, while G. coffeae attacks the absorbent roots; the smaller species attack the whole root system near the soil surface. As they feed and develop, the nymphs and adults excrete their characteristic waxy cover and form compact colonies. Mealybugs excrete sugary substances (honeydew), which supports the growth of fungi (i.e., Bornetina), which contribute to formation of the thick, cork-like, dark crust covering and sheltering the mealybug colony; a succession of crusts give a knotty appearance to the root. The sugary substances also attract certain ant species, which live in a symbiotic association (trophobiosis) with the mealybugs. In exchange for the sugary foodstuff, the ants give them protection and transportation from one root to another and from one plant to another. The ants that associate with mealybugs in South America and in some of the Caribbean Islands are in the genus Acropyga. In Colombia, the Hope ant (A. robae Donisthorpe) and the Amagá ant (A. fuhrmanni Forel) are associated with N. coffeae and C. caldasiae, respectively. In Guatemala, D. bispinosus seems to be associated with the presence of the ant Solenopsis geminata (F.). P. citri does not produce large quantities of sugary excretions when it lives on the plant roots, and is not attractive to ants. In certain cases, the mealybugs have lived for more than a year in the absence of ants. The life cycle, from egg to adult, requires from 30 to 120 days, according to the species and the 977 978 C Coffee Pests and their Management temperature. Five generations develop per year in the case of D. bispinosus. Root mealybugs develop better during the rainy season, particularly in low or medium altitude plantations in Central America. Other conditions that favor their development are sandy, acid pH, and medium moisture soils. In Colombia, the damage caused by Rhizoecus sp. seems to increase in old, poorly fertilized plantations, and in Guatemala D. bispinosus is found most frequently in 1–5 year-old plantations. Mealybugs are polyphagous, also attacking other plants such as shade trees (Inga spp.), cassava (Manihot esculenta Crantz), sugarcane (Saccharum), banana trees (Musa), lemon trees (Citrus) and some herbs that grow on the coffee plantation. In Costa Rica, Anredera ramosa (Moq.) Eliasson is an alternate host of D. brevipes; in El Salvador, D. bispinosus has been found associated with Lantana camara L. Natural Enemies In general, the literature on coffee mealybugs in tropical America does not make reference to their natural enemies. In Cuba, Coccidoxenoides peregrinus (Timberlake) (Hymenoptera: Encyrtidae) is cited as a solitary, primary endoparasite of the pseudococcid complex in coffee. Other natural enemies of mealybugs reported in Cuba are Diadiplosis cocci Felton (Diptera: Cecidomyiidae), Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae) and Signiphora sp. (Hymenoptera: Signiphoridae). Management There are management options for mealybugs, but insecticides are normally used once pest populations develop. ant nests should be examined critically; from 15 to 20 plants/ha should be checked, paying more attention to those that are close to the ant nests and/or possess yellow leaves. The surrounding shade trees and bushes should also be checked. The plants are checked by moving the stems in all directions in order to gain visibility of the base of the roots. Cultural Control Mealybugs should not be present in the seed bed and tree nursery. The limits of any infestation sites should be determined and marked. Adequate fertilization should be provided, including addition of organic matter to the soil. Physical conditions of the soil should be improved in order to avoid floods. Planting coffee trees on land previously supporting plants that are highly susceptible to mealybugs (e.g., cassava, sugarcane) should be avoided. Alternate host plants should be eliminated from the plantation. Severely damaged plants should be removed and burned. Biological Control This is practically unexplored in the coffee growing countries of tropical America. Plant Resistance to Insects In Guatemala, some research has been conducted which supports the use of plants grafted on resistant rootstocks of C. canephora (genotypes 3757, 3754, 3751, 3581, 3752 and 3756) and C. dewevrei. Chemical Control Sampling Sampling should preferably be conducted on young coffee plantations (up to 6 years old). Plants near Systemic organophosphorate and carbamate insecticides produce good results, although they are expensive. The presence of mealybugs in seed beds or on plants younger than 1 year old is sufficient Coffee Pests and their Management justification for insecticide application. On plantations older than 3 years, insecticide application is made if more than 1.6 colonies per plant, on average, are found. In no case should the damage be allowed to exceed 25% of the absorbent roots. Insecticides are applied on the drip line of the plant if the damage is on the small roots. If the damage is on the main root a funnel-shaped hole should be made around the tree trunk, the insecticide should be poured in and the hole should be covered again with soil, adding also a layer of dead leaves. Application of granular insecticides is made at the beginning of the rainy season or 3 months before starting the harvest. Scale Insects, Mealybugs and Related Foliage Pests (Hemiptera) Distribution Different scale insects, mealybugs and related foliage pests live on the coffee plant. The geographic distribution of some is restricted to a few countries of tropical America, whereas others are distributed more widely. Some are reported attacking the coffee plant only in South America, others only in Central America or the Caribbean (Table 17). Damage and Economic Importance Scale insects, mealybugs and related species attack the aerial part of the coffee plant and, in some species, also the root (e.g., Planococcus citri [Risso]). The leaves, fruit, branches and young tissues of the aerial part of the attacked coffee plant often support colonies or groups of circular, oval or elongated scales, which may be flattened or swollen, with a soft or hard consistency. In other cases, colonies of insects have a soft body covered with white, cotton-like filaments. These insects cause damage by removing large quantities of sap, which causes plant malnutrition. Also, sticky honeydew and blackish molds can be found covering the foliage. C When Capnodium (sooty mold) and Meliola (black mildew) fungi grow on the honeydew excreted by the scales, they interfere with photosynthesis. Ants are present where scale insects are feeding. In cases of severe attack, a dirty appearance on the plant, general weakening, growth delay, yellowing and drop of foliage and fruit are observed. With the articulated scale, Selenaspidus articulatus (Morgan), old attacks may be recognized because the site where the scales were located turns yellow or discolored, resembling infection by the coffee rust fungus (Hemileia vastatrix Berk. and Br.). Some species, such as the green scale, Coccus viridis (Green), are considered to be quite important to coffee production, though some attack a number of different cultivated plants. Severe infestations of C. viridis may kill young tree nursery plants. The incidence of these pests is highest on coffee plantations lacking adequate shading. Pest Description The following cases are presented as examples: C. viridis – adult females are motionless, oval, sometimes asymmetric, very flat and pale yellow. They have some black spots centrally, and they tend to be soft and elastic. They are about 2.2 mm wide and 4.0 mm long. The presence of males is very rare. Saisettia coffeae (Walker) – adult females are motionless, almost spherically shaped and dark brown. They are 2.0–3.5 mm in diameter. The males are winged. P. citri – adult females are mobile, oval, pale yellow or dark orange, with very clear segments on the body, and 4.0 mm in size. They are covered with a dusty white glandular secretion except for a longitudinal stripe dorsally. They have filaments laterally. Males are smaller (1.0 mm), violet to yellow in color, and they have well-developed wings. Biology and Ecology The biology of these insects varies among species and can be quite complex. The first instar 979 980 C Coffee Pests and their Management has legs and antennae and is very active. To feed, the insects attach and insert their mouthparts. After the first molt, they generally lose their legs and antennae and the insect becomes sessile. By then, it begins to secrete a waxy, scale-shaped layer that covers the body. In the case of scales of the family Diaspididae, this layer of scale is almost always separated from the insect’s body. Adult females remain under this cover and they produce their eggs or directly give birth to the nymphs therein. The location on the plant, and the age of the plant they prefer to attack, depends on the species of scale: C. viridis is commonly located along the leaf veins, on the back of the leaves, on young buds and on seed bed coffee fruits of nursery plants; S. articulatus is found mainly on the leaves and fruits of production plants; the round scale, Parasaissetia sp., mostly attacks the stems and branches of coffee plants younger than 1 year; the black scale, Ischnaspis longirostris (Signoret), infests the leaves, branches and fruits of old, poorly attended coffee plantations; Cerococcus catenarius Fonseca gathers in the form of a line or chain along the trunks and branches; P. citri attacks new branches, leaves, flower buds, fruit peduncles and fruits; Orthezia spp. attack branches, leaves and fruits, mostly of robusta coffee in Brazil. The males develop very much like the females except that in the last stage, before transforming into adults, they go through a pupal stage; the wings develop externally over the pupa. Most of the scales reproduce parthenogenetically. Some species are oviparous (S. coffeae, S. olae [Oliver]) and others are viviparous (Coccus hesperidum L.). The total number of eggs produced per female varies among the species; for example: C. viridis, between 50 and 600 eggs; Orthezia praelonga Douglas, more than 200 eggs; C. catenarius, about 900; S. coffeae can lay up to 1,600 eggs. The complete life cycle, from egg to adult, lasts between 40 and 60 days. The scale insects are more abundant during the dry season and at the onset of the rainy period. Hard rains and natural enemies are important factors in the mortality of these pests. Natural Enemies These insects are susceptible to a large number of parasites, predators and pathogens as natural enemies. Management Sampling During the dry season, inspections should be conducted to check for the presence of scales and related species in the coffee plantation, as well as on other plants cultivated nearby or at the same time. Cultural Control The nursery shading should be reinforced during the dry season. Affected plants should not be transplanted. Weeds should be suppressed. The pests should be kept under control on host plants existing in or near the coffee plantations. Sanitary pruning should be performed to eliminate (by burning) old and unproductive branches infested by the pests. Biological Control Natural enemies should be protected and preserved, using insecticide only if necessary. Chemical Control Chemical control is directed only at infested plants, after checking to determine that the scale colonies are alive. For better control, mineral oil is added to the insecticide solution, with applications made every 15 days until the problem is corrected. The oil should not be used during flowering or during sunny periods of the day. During the rainy season, granulated insecticides may be used. Coffee Pests and their Management Cutworms and Armyworms (Lepidoptera: Noctuidae) Distribution These insects are widely distributed in the coffee plantations of tropical America (Table 17). Damage and Economic Importance Cutworms and armyworms constitute an economically important pest for many crops. Damage is caused during the night by the larval stage. The larvae attack the stems of small coffee plants in germinating beds, seedbeds or plant nurseries, and recently transplanted plants. On seed beds and plant nurseries, plant damage typically takes the form of plants cut at the soil level or slightly above, or withered plants. In the case of recently transplanted coffee plants, defoliated and sometimes dead coffee plants can be observed. Spodoptera frugiperda (Smith) larvae feed on the stem, causing withering and finally death of the small plants during the first year of their lives. In other cases, the stem breaks at the site of the ring formed by the larval feeding. When the infestation is severe, many plants are killed and re-sowings are needed, which increases the coffee plantation set-up costs. Damage is more frequent in plantations that are close to fields where corn, beans, vegetables, cassava or pasture are grown. C Biology and Ecology Adults are moths that are active at night, laying their eggs individually (A. ipsilon) or in groups (S. frugiperda). During the first two larval stages, they feed on leaves that are at soil level, and in the last three they act as cutting worms. During the day, they remain hidden in the soil. In some species, such as A. ipsilon, the larvae coil up when disturbed. Larvae pupate in the soil. Natural Enemies There are many natural enemies (parasitoids, predators and pathogens) of these pests. In Ecuador, the larval parasitoids Bonetia sp. (Diptera: Tachinidae) and Chelonus sp. (Hymenoptera: Braconidae) and the predatory ground beetle Calosoma sp. (Coleoptera: Carabidae), are cited. Management Sampling Night-time inspection of seedbeds and the young plantations should be made to detect initial infestations. Cultural Control Pest Description The following species are presented as examples: S. frugiperda – the larvae have a well-contrasted, inverted “Y” on the head; neonate larvae are white with a black head, but as they grow they turn dark. Large worms are light brown to dark green in color and they are about 4.0 cm long. Agrotis ipsilon (Hufnagel) – small larvae are brown with paler back marks, and large ones, which may be as be as large as 4.0–5.0 cm, are shiny black-gray in color, with a pale gray line on the back and black tubercles on each of the segments. Seedbeds or plant nurseries should be kept clean of weeds and dead leaves, since the larvae seek shelter there. Mechanical Control Larvae should be eliminated by hand during the night-time inspections. Heavy watering should be applied to get the larvae out of their hiding places, followed by manual elimination. Light traps can be used to capture the adults. 981 982 C Coffee Pests and their Management Biological Control Biological insecticides such as Bacillus thuringiensis Berliner should be used, particularly at the beginning of infestations, when the larvae are small. Chemical Control Insecticides can be incorporated into the soil, before or after sowing, for cutworm control. Granular products are used in a preventive manner. The use of poisoned baits during the night and dry weather is also recommended. Brown Coffee Borer, Xylosandrus morigerus (Blandford) (Coleoptera: Curculionidae: Scolytinae) Distribution This pest comes from the Oriental region, having its distribution center in the Indomalayan area. It was detected in the western hemisphere in 1958– 1959, and it is now found from Veracruz, Mexico to Brazil. Damage and Economic Importance Various tree species can be attacked by X. morigerus (e.g., avocado, cacao, cedar, coffee). This insect displays a strong preference for attacking robusta coffee, C. canephora. Some reports indicate that it may also infest C. arabica; however, this has not been confirmed in Mexico. The attacked coffee plant branches and young stems typically display a few or many holes of about 1.0 mm diameter. Blackening of the tissues may be seen around the perforations. A longitudinal cut of an affected branch reveals a gallery in which the whitish larvae can be observed, along with reddish brown adults. The attacked young branches and stems dry up distally and then die. Apparently, the mortality of the branches and stems is caused by microorganisms that invade the plant tissues through the feeding sites formed by the brown coffee borer. Ants, termites or mites can be found in the abandoned galleries. Often the ants cause the death of branches or stems when enlarging the abandoned galleries of X. morigerus to construct their own nests. If death of branches or stems does not occur, the yield is reduced as a result of damage to the flowering and development of the fruit. The symptoms can be observed more frequently on weak coffee plants, but attacks may also be seen on the young stems of pruned plantations. This pest is particularly important in Ecuador. In Mexico, X. morigerus is also an important pest in the Soconusco region in Chiapas. Description The egg is oval, white and very small. The larva is milky white, with a yellowish head, and lacks legs. The pupa is white initially, turning cream to brown toward maturity. The adult is cylindrical and from 1.40 to 1.90 mm long. It is differentiated from other species of the same genus by the bright brown-reddish color, by the stouter body and because the declivity commencing only on-third of the elytral length from the base, and by the near absence of punctures on the sides of the elytra (variable). Females have well-developed wings and fly, but males are incapable of flight. Females are larger than males. Biology and Ecology Mated females take flight during the day, leaving the gallery where they developed in search of branches or stems, which they penetrate to construct the new galleries. The female lays from 20 to 60 eggs in 8–10 days. X. morigerus is an ambrosia beetle. The adults and larvae get more nutrition by feeding on fungi (e.g., Ambrosiaemyces zeylanicus Trotter is reported from Ecuador; Coffee Pests and their Management Raffaelea tritirachium Batra from Mexico) than from the coffee plant tissues. These fungi grow inside the gallery, which is inoculated by the founding female. The larvae have three instars. The life cycle, from egg to adult, is 20–40 days. A gallery may contain more than 80 individuals in all stages of development. The sex ratio in galleries is femaledominated; various studies have found only one male for each 7, 11 or 20 females. Mating occurs within, or very close to the gallery. Infestation is apparently less evident under drought conditions, because the ambrosia fungi require moisture. Nevertheless, reports from Ecuador indicate that the populations are larger during the dry season of the year. X. morigerus is a pest which frequently attacks healthy plants; however, very strong attacks may be observed when the coffee plants have been weakened by droughts, malnutrition, nematode attacks and competition with weeds. The attacks may be accompanied by attacks from other Scolytinae. C ethanol have been used for monitoring flying females in robusta coffee plantations. Cultural Control Infested vegetative material, particularly in young or pruned plantations, should be cut and burned periodically. Adequate fertilization should be applied. Shade of coffee should be regulated by pruning. Weeds should be suppressed by shading, mulching, use of ground cover, and by selective weeding by hand. Biological Control This approach has not yet been attempted for this species. Chemical Control Natural Enemies No native parasitoids of this pest have been reported in coffee growing countries in tropical America. However, it should be mentioned that in Indonesia, a Tetrastichus sp. (Eulophidae) has been reported, and also probably a bethylid parasitoid. In Ecuador, ants (Formicidae) have been recorded as predators of the brown coffee borer, including species of Crematogaster, Leptothorax, Pheidole, Pseudomyrmex and Solenopsis. The entomopathogenic fungus B. bassiana has been reported infecting this insect pest. This is recommended when the beetle population has undergone a marked increase and natural and cultural control cannot restrain it. Insecticides are useful only when adults are out of the galleries or are boring on the branches; once they have taken refuge within the galleries, insecticides have little or no effect on X. morigerus. Stem Borers Plagiohammus spp. (Coleoptera: Cerambycidae) Distribution Management Sampling No sampling methods have been developed in coffee plantations; however, some studies indicate that penetrated branches and stems have an aggregated distribution in the field. Traps baited with Three species of Plagiohammus have been reported attacking the stem of coffee plants in Mexico and Central America. P. maculosus (Bates) has the wider geographic distribution (Costa Rica, El Salvador, Guatemala, Honduras, Mexico), while P. mexicanus Breuning and P. spinipennis (Thomson) have been recorded attacking coffee only in Mexican plantations. 983 984 C Coffee Pests and their Management Damage and Economic Importance A pile of white-yellowish sawdust or powder present at the base of coffee plants, at the soil level, in a good indication of infestation by Plagiohammus. Infested plants may have a withered, yellow-like and decaying appearance. Careful observation at the stem base may help identify the hole or holes (ca. 5.0 mm in diameter), where the sawdust originates. A longitudinal cut of the stem and root may uncover a large, white or creamy-colored larva with long gallery containing powder; the gallery begins at the stem and may go as low as the tip of the central tap root. These borers are one of the most destructive coffee plant pests in certain areas of tropical America. The damage is caused by the larva when it bores into the stem and the root. The borer attack delays the plant growth and it may cause death directly by damaging its root, or indirectly, by facilitating stem breakage following wind action or other factors. ready to pupate, the larva moves close to the excretory opening, which has been made close to the ground, and it isolates itself within the stem in a chamber surrounded by sawdust. The larval period lasts from 2 to 3 years. Adults are more visible at the beginning of the rainy season (April through June), the period when egg laying occurs. The abundance of these cerambycids is higher in high-altitude coffee plantations (>1,000 m) and in places with long summers or with lack of rain. Abandoned coffee plantations are more severely attacked. Natural Enemies There is no information on the natural enemies of the Plagiohammus spp. Management Sampling Description The egg is unknown. The larva is creamy-white, with the thorax wider than the abdomen, and legless. Its head is light brown with strong and visible mandibles extended forward. A well-developed larva is about 4.5 cm long. The pupa is brown and similar in size to the adult. The adult has an elongated body, cylindrical, from 2.0 to 3.5 cm long by 0.8 cm wide. The body is light brown with two white lines on the prothorax and with irregular white spots on the elytra. The antennae are longer than the body (4.0 cm). Coffee plants having sawdust as the base of the trunk should be searched for. If damage is recent, the sawdust is white or pale yellow. Cultural Control Infested stems should be removed. Adequate fertilization should be applied. Weeds should be managed by shading, mulching, ground cover, and mechanical removal. Biology and Ecology Biological Control Not much is known about the bionomics of Plagiohammus spp. Adult females lay eggs on the bark of coffee plant stems, at a height below 30.0 cm. Upon eclosion, the larva penetrates the stem and bores longitudinally all the way to the root, while it feeds, grows and develops. The larvae may be found in the stem, from the base to a height of one meter. When This has not been attempted yet. Chemical Control In places where the pest appears yearly, a preventive insecticide application with a brush or a Coffee Pests and their Management manual pump is recommended, treating from the stem base up to 60.0 cm high. Application may be repeated once or twice every 20 days. In order to kill the larva within the stem, a cotton ball soaked in an insecticide can be inserted through the respiration and excretion opening made by the larva, or insecticide solution can be injected into the opening with a syringe. When treating in this manner, the orifice is enlarged, the product is applied and the orifice is sealed with mud, clay or any other material that solidifies. This step, though effective, can be expensive due to the labor it may require. White Grubs (Coleoptera: Scarabaeidae) Distribution Phyllophaga is a well-represented genus of white grubs in coffee plantations in tropical America (Table 17). In El Salvador, P. latipes (Bates), P. menetriesi (Blanch) and P. obsoleta (Blanch) are found, whereas in Costa Rica P. sanjosecola Saylor and P. vicina (Moser) are reported. Other white grubs recorded in coffee are Anomala sp. (El Salvador) and Dyscinetus picipes Burmeister (Cuba). Damage and Economic Importance White grubs attack the coffee plant root. The damage is caused by larvae that live in the soil and feed on the root system of the plant. In the seedbed and plant nursery, the plants wither and die rapidly; in the coffee plantation, irregular areas on one or several coffee plants, usually young, may be observed, which show symptoms of yellowishness, limited growth, scarce fruits and mummified fruits.When the affected plants are taken out of the soil, lesions, very few small roots and partial or total bark peeling on the main and secondary roots are observed. In some coffee growing areas, these pests can be economically C important, because they may cause death of the plants. The attacks are more severe in plant nurseries, on recently transplanted coffee bushes and on 1 year-old plants, although mature plantations may also suffer the attacks of these pests. In some plantations it is estimated that 2 or 3% of the transplanted coffee plants may be lost to white grub attack. Coffee plantations located in the vicinity of pastures are most affected. Pest Description The egg is white; when recently laid, they are elongated, and later on they adopt a round shape. The larva has a milky-white colored body with a “C” shape, with long thoracic legs covered with hair. The head is dark or light, with strong mandibles. There are three larval stages; the last stage grows up to 3.5–4.0 cm long. The pupa is brown-golden in color, with a size that varies between 1.8 and 2.0 cm. The adult is a strong, heavy bodied scarab. Depending on the species, they may be light or dark brown or reddish-brown in color, measuring from 0.5 to 2.5 cm in length; the antennae are enlarged distally, with the apical expansion consisting of several laminated segments. They are able to fly. Biology and Ecology Adult females, which have twilight habits, come out at the beginning of the rainy season and they lay their eggs within the first 10.0 cm of depth in the soil, close to pastures or fodders. The eggs are laid one by one or forming small groups. A female may lay up to 200 eggs. Small larvae feed themselves with organic matter and small roots, and when they reach the last development stage, they are voracious root eaters. They are found at different depths, according to the soil temperature and humidity. They are common in areas that have been gramineous pastures. The larval stage lasts about 6 months. Pupation takes place in a chamber or cell located in the soil at a depth between 10.0 and 20.0 cm. The duration of the life cycle, from egg to adult, varies from 9 to 10 985 986 C Coffee Pests and their Management months. Adults are strongly attracted by artificial light and they feed from the leaves of some plants, such as cassava, African oil palm and Erythrina trees (Fabaceae). Natural Enemies The larval parasitoids Campsomeris, Elis and Tiphia (Hymenoptera: Scoliidae) have been reported in coffee plantations. Parasitism of bacteria Micrococus sp. on larvae and parasitism of fungi Spicaria sp. and Metarhizium sp. on pupae has been observed. Nematodes as parasites of larvae have been observed as well. A robber fly Diogmites species (Diptera: Asilidae) has been recorded predating larvae in the soil. Several mammal, reptile and bird species predate on the adults. Management Sampling Root and soil samples at a depth of up to 20.0 cm should be taken, in order to determine the infestation sources. The samples are taken from three coffee plants, at 30.0 m intervals. On areas <7 ha, sampling should be taken diagonally and for larger areas sampling should be taken in parallel. manually. Light traps, preferably 40 watt blacklight traps, should be used to capture and eliminate adults. The use of a trap for every 10–15 ha is recommended, which should be turned on from 18:00 to 21:00 o’clock. This procedure has the disadvantage of attracting a number of other night habit insect species, which should not be eliminated. Biological Control Biological control has not been attempted in coffee plantations. Chemical Control In the case of plant nurseries and recently transplanted coffee plants (<1 year old), one larva per plant justifies the use of granular insecticides. The application can also be made at sowing time. With three large larvae or seven small larvae per square meter, insecticides are recommended for young plants. Three year old plants withstand up to eight larvae; for 4 year-old plants, 12–15 larvae; well-attended mature plantations withstand up to 20 larvae per coffee plant. Black Citrus Aphid, Toxoptera aurantii (Boyer De Fonscolombe) (Hemiptera: Aphididae) Cultural Control Distribution Weeds should be suppressed principally by shading, by mulching, by ground cover vegetation, by slashing back and by selective weeding by hand. Shade trees should be pruned. This aphid comes from the tropical and sub-tropical areas of the Old World. It is widely distributed in coffee plantations in tropical America. Physical-Mechanical Control Damage and Economic Importance During preparation of the seedbed or plant nursery, the soil to be used for bag filling should be sifted, and the larvae found therein killed T. aurantii attacks leaves, buds and other tender parts of the coffee plant. Coiled, deformed and curled leaves and tender buds are signs of infestation; Coffee Pests and their Management also, reduced growth, and leaf and flower drop occur. Damage may occur in seedbeds, plant nurseries, and on adult coffee plants. Yellow, green or black insect colonies, more or less round shaped, can be found on the lower surface of foliage. They are easily excited, producing a characteristic noise which may be audible if the colonies are very large. The infestation may be accompanied by a fungus, called sooty mold, on the foliage, and also by the presence of ants. In general, this aphid is not very important as a pest; however, a considerable yield reduction may appear when severe and prolonged attacks occur, particularly if the infestation appears during the flowering and fruiting season. The damage is often more severe in the plant nursery, on growing plants. T. aurantii is reported to be responsible for the transmission of pathogens to coffee plants in Costa Rica and Guadeloupe. Description The nymphs are similar to adults, but smaller and dark-brown in color. The adults have a globoid, dark green or black body, and they may or may not have wings; apterous females are larger (2.0–2.1 mm) than winged ones (1.7–1.8 mm). They bear a pair of cornicles on the back of the body. C Natural Enemies More than 70 species of natural enemies have been reported on T. aurantii around the world. In coffee plantations in tropical America, the following have been reported: the braconid parasitoids Diaretus sp. and Lysiphlebus testaceipes (Cresson); the entomopathogenic fungus Acrostalagmus albus Preuss; the coccinellid predators Hippodamia sp. and Cycloneda sp.; the syrphid predators Allograpta sp., Paragus borbonicus Macquart and Baccha clavata Fabricius; and the green lacewing predator Chrysopa sp. (Chrysopidae). Management Sampling Growers are advised to monitor young leaves throughout the dry season for aphids or damage. Cultural Control Reinforce shade of coffee plantation during the dry season. Affected plants should not be transplanted. Biology and Ecology Biological Control Adult females generally reproduce by parthenogenesis and are viviparous. Males are winged and rarely seen. An apterous female may produce 50 female nymphs in 7 days. The life cycle, from nymph to adult, is 6 days at 25°C. These aphids excrete honeydew on which the sooty mold fungus grows. The fungus gives a blackish appearance to the plant. The honeydew is highly appreciated by ants; hence the association of ants with aphids, providing them with protection and transport to other plants. T. aurantii finds conditions more favorable during the dry season. When conditions are adverse, winged females are produced in order to disperse and colonize new plants. Infestations appear in a cyclic manner. It is generally acknowledged that natural enemies contribute importantly to prevent T. aurantii from having greater economic impact. Natural enemies should be conserved. Chemical Control If chemical control becomes necessary, either insecticidal oil or an insecticide may be used. Chemical control should only be applied at the first signs of damage during periods of young leaves’ growth. Young leaves should be completely moistened after application of chemicals. 987 988 C Coffee Pests and their Management Leaf-Cutting Ants, Atta and Acromyrmex (Hymenoptera: Formicidae) Distribution Leaf-cutting ants of the Atta and Acromyrmex genera are found in Neotropical countries where coffee is grown. The principal leaf-cutting ant species affecting coffee plants in tropical America are shown in Table 17. Damage and Economic Importance Leaf-cutting ants attack leaves, tender buds and flowers of the coffee plant. The leaves of attacked coffee plants have semi-circular cuts or these plants are completely defoliated. Leaf fragments dispersed on the ground are seen around the defoliated plants. In recent attacks, the presence of ants carrying leaf and flower pieces may be observed. It is possible to detect earth mounds (nests) nearby or relatively far away. Situations in which ants are direct plant pests are rare; however, in the tropical and sub-tropical areas of America, ants of the Atta and Acromyrmex genera can constitute important pests of many cultivated and wild plants. In tropical America, cutting ants constitute the dominant group of herbivorous animals, because they consume much more vegetation than any other animal group. In the case of coffee, these ants are generally considered of minor importance. Nevertheless, in some areas like the Turrialba region of Costa Rica, A. cephalotes attacks on coffee plants can be severe in monocultures. The damage is caused by the worker caste when they cut the coffee foliage and flowers with their mandibles. In some Atta species, from 5 to 28 colonies/ha have been observed, with the possibility of having one or more millions of workers in each colony. The nests they construct may have dimensions that vary between 30 and 600 m2. From one day to the other, one or more coffee plants may be completely defoliated by these ants. Coffee plantations near woody or weedy areas are attacked more commonly. Pest Description Atta cephalotes (L.) is hereinafter described. Their colonies contain three castes: queens, males and workers. Queens are big (16 mm), with a strong brown-reddish color, and they have wings (although they lose them after the nuptial flight); also, they have a pair of horns on the occipital lobules and another pair on the lower part of the head, close to the mandibles. Males are winged but smaller (13 mm) than the queens, and they do not have the aforementioned horns. Workers are wingless. Soldier workers present abundant yellowish hair on the forehead sides, and they are about 13–15 mm long. Forager workers have less hair and they are about 9–10 mm long; fungus-cultivator workers are lighter colored and smaller (from 2 to 4 mm). Biology and Ecology Atta and Acromyrmex ants are social insects that use plant leaves to cultivate symbiotic fungus (Leucoagaricus gongylophorus (Möller) Singer; Attamyces spp.), which serves as their foodstuff. They form colonies constituted of three castes: queens, males and workers; the latter are sterile and present acute polymorphism and functions (soldiers, foragers, cultivators). The mating of queens with males takes place outside the nest during the nuptial flight, at the beginning of the first rains. Newly mated females dig their nests in the soil and begin to cultivate the fungi which will serve as their food and to lay their first eggs. The eggs give birth to the larvae and after 40–60 days, the first adult workers emerge. New colonies have a single tower-like mound of small size of <200 cm2 in area, and with a small entrance hole, whereas older colonies are flattened, with larger entrance holes and a colony surface area >200 cm2. The growth of the colony is very slow at the beginning, but during the second and third year it accelerates rapidly and then it diminishes as the colony starts production of males and winged queens. Towards the end of the Coffee Pests and their Management third year, the population is enormous, and it is possible to observe more than 1,000 entrance/exit holes on the nest. The Acromyrmex nests are simpler than those of Atta. In order to reach the plants which serve as their food, the forager workers move from the nest, which is often in noncultivated fields, through narrow paths which can go more than 100 m in distance. The workers’ activity is more intense during the night. Natural Enemies Apparently these ants have few natural enemies. Several predators, such as birds, toads, lizards and anteaters feed on the queens and males during the nuptial flight. In Colombia, other carnivorous ants have been observed to be predators of leaf-cutting ants. The importance of all these natural enemies in regulating leaf-cutting ant populations is unknown. Management The optimal time of the year to control leaf-cutting ants has not been determined. However, the nuptial flight period, a crucial event within the ant life cycle, should be taken into account. Considering the ecological importance of leaf cutting ants as plant population regulators in woody and grazing areas, and taking into account that in certain areas they are eaten by humans, it is recommended that population regulation, not elimination, be the primary goal. Sampling No sampling techniques have been developed for leaf-cutting ants in coffee plantations. The nests can be located by following the narrow paths used by the ants. Ant colony density can be estimated by sampling four 125-m2 plots at each edge of a farm (north, west, east and south), and a single 500-m2 area in the center of the farm (a total area of 1,000 m2). C Cultural Control Queens should be eliminated at the recently formed nests using a grub hoe. Repellent plants (e.g., sorghum) should be sown. Because coffee on farms with low vegetational diversity is at greater risk of attack by A. cephalotes, it is recommended that shade trees be planted in order to increase shade levels and therefore to decrease ant colonization. Also, it may be desirable to plant shade trees that are palatable to leaf-cutting ants, but that should be either not commercially valuable (e.g., Erythrina poeppigiana [Walp]. Cook, Cordia alliodora (Ruiz & Pav.) Oken, Swietenia macrophylla King, Cedrela odorata L.), or that are tolerant of ant attack, in order to divert ants from foraging coffee plants. Biological Control Some entomopathogenic (e.g., Paecilomyces sp. and M. anisopliae) and antagonist (Trichoderma viride Persoon ex Gray) fungal strains have proved to be successful against leaf-cutting ant colonies in experimental studies. However, the practicality of these fungi has not been assessed in commercial coffee plantations. Chemical Control Insecticides are applied directly through some of the entrance/exit holes of the nests, taking the precaution of plugging or closing most of them before. The “ant hill beating” procedure may also be used, which consists of digging in the nest with a shovel in order to uncover the ant brood, and spraying them with insecticide. Also, leafcutting ants can be successfully controlled using baits containing insecticides. Treatment results can be improved by basing the amount of insecticide applied on an estimate of the colony volume, instead of surface colony area. An experimental study shows that mounds of dump material can be used as a highly effective 989 990 C Coffee Pests and their Management small-scale deterrent to protect Hibiscus plants from defoliation by A. cephalotes, but this method has not been tested in coffee. fungi may be involved in the damage (e.g., Phoma costarricensis Echandi). Description Long-Horned Grasshoppers or Katydids (Orthoptera: Tettigoniidae) Distribution Two Idiarthron species, I. subquadratum Saussure & Pictet and I. atrispinum (Stål), and one unknown Gongrocnemis species have been reported attacking coffee in Mexico and Central America; apparently, I. subquadratum is present in Colombia too. Of these, I. subquadratum is the most important katydid pest in coffee because very high infestations have been reported in some coffee plantations in El Salvador and Mexico. Most of the information available on katydids comes from this species. The eggs of I. subquadratum are brown in color, elongated, with a hard chorion; they are oviposited in compact clusters. There are six nymphal instars. Newly emerged nymphs are fragile and gray in color. Nymphs resemble adults, but are smaller, lighter colored, and lack wings. Nymphs and adults have strong and large mandibles and the antennae are very thin and longer than the body. Adults have a heavy set, more or less cylindrical body, greenish, brown-gray or light gray in color, with females from 5.0 to 6.0 cm long. Males are smaller. With their thorny, strong and long back legs, they can jump. Their ability to fly is limited and in general their movements are clumsy. Females have an ovipositor, from 1.0 to 2.3 cm long, at the tip of the abdomen, which looks like a spur or a knife point. Damage and Economic Importance Biology and Ecology Attacked coffee leaves show irregular holes marginally and centrally; feeding can also be observed on the tender buds, shoots and branch tips. A characteristic symptom of katydid damage is the appearance of green and ripe fruits with damaged pulp, so that the coffee beans are exposed. The damage is caused by both the nymphs and adults. In coffee plantations where heavy attacks of I. subquadratum occur, complete destruction of leaves, buds and small branches, the fall of tender fruits and the destruction of fruits can be observed. In general, I. subquadratum is not an economically important problem in coffee, although it sometimes may create some concern in certain areas of Central America and Mexico. In southeastern Mexico (Siltepec, Chiapas), the most critical attack period is from June through November. Damage is more important in very shaded and abandoned coffee plantations. In addition to direct damage caused by I. subquadratum, plant pathogenic Idiarthron subquadratum is arboreal, polyphagous, and nocturnally active. Both nymphs and adults leave their daytime shelters at night and disperse by jumping between tree and bush canopies. They hide in shady places, such as dead leaves, rotten trunks and weeds; in particular, they take refuge in plants of wind-breaks, izote (Yucca guatemalensis Baker) barriers, banana plants (Musa spp.) and Sanseviera sp. This species feeds on leaves and fruits of several plants, including coffee (Coffea spp.), banana (Musa spp.), orange (Citrus spp.), chayote [Sechium edule (Jacq.) Swartz], and pacaya (Chamaedorea sp.). Mating occurs in plant canopies at night or in daytime shelters. Adult females place their eggs in the soil and, in some cases, under the bark. The eggs are placed in a mass (from 5 to 50), and one female may lay several hundred. In Siltepec, Chiapas, Mexico, mating usually occurs in October, and oviposition occurs Coffee Pests and their Management C in November and December. Adults are killed by low temperatures in January and February, and eggs undergo diapause. At the beginning of the rainy season, between May and June, nymphs emerge and start to feed on coffee plants. Generations are overlapping in warmer regions. The life cycle from egg to adult is about 80 days at 28°C. In El Salvador, this pest is especially common in high altitude coffee plantations. Some strains of B. bassiana kill nymphs in the laboratory. However, the use of this biocontrol agent has not been attempted in field. Natural Enemies Chemical Control Birds, spiders, parasitic nematodes and an unknown tachinid fly species (Diptera: Tachinidae) have been reported in Mexico. When infestations are heavy, the application of chemical insecticides at the places of refuge is recommended. Toxic baits placed inside the bamboo traps are also recommended. The most convenient period for chemical control is 1 month after the beginning of rainfall and before oviposition takes place. Because high infestations of the pest have been related to low populations of natural enemies, insecticide use should be avoided in order to conserve natural control. Management Sampling “Shelter traps” made with a 10-cm-diameter by 30-cm-long bamboo (Bambusa vulgaris Schrad.) internode closed at one end, can be used for sampling I. subquadratum. The bamboo traps are placed on coffee bushes upon the first rainfall events, and during daytime are checked every week for captured insects. Cultural Control Weed control should be applied. The shade should be regulated. Trash and rotten trunks in the coffee plantation should be prevented. Dry banana and plantain leaves should be eliminated. the insects are killed manually and/or used as food for domestic animals (e.g., chickens and dogs). Biological Control Bush Crickets, Paroecanthus spp. (Orthoptera: Gryllidae) Distribution Bush crickets appear sporadically, affecting coffee plants and shade trees in coffee plantations in some areas of Central America and Mexico. The reported species are Paroecanthus guatemalae Saussure (Guatemala, Honduras) and P. niger Saussure (El Salvador, Guatemala). The Paroecanthus species in Mexico remains unknown. Recently, high infestations of bush crickets have been reported in Honduras. Mechanical Control Bamboo traps as described earlier for sampling can be used for elimination of I. subquadratum. The traps are placed in dark spots of the plantation and in the vicinity of the plants that are normally used as refuge. The traps are checked weekly and Damage and Economic Importance Paroecanthus spp. attack lignified stems and branches of coffee bushes and shade trees. The affected plants show small marks or holes, 3.0 mm 991 992 C Coffee Pests and their Management in diameter by 1.0 mm in depth, distributed in line throughout the affected stems and branches. This mark along the stem gives it the appearance of a flute; hence this damage is known as “flute disease.” If the stem or branch bark is lifted right below each hole, an “X” shaped scar on the wood may be observed. The damage is caused when the adult female of the cricket lays its eggs. Heavy attacks of the bush cricket (when there are many holes), may cause physiological disorders in the coffee plant, which affects its development. The cricket can be a pathogen vector, or perhaps the lesions may favor the penetration of diseases. A severe infestation can kill the coffee plant. In Honduras, where high infestations have been reported, the affected plants develop a yellowish color and they lose leaves and fruits. Description The egg is white with elongated shape (1.0 by 5.0 mm). Nymphs are similar to adults, but their wings are not well developed and they are smaller than adults. The adult has a cylindrically shaped body and is 2.0–2.5 cm long. The legs are yellowish in color and the abdomen is dark brown. The antennae are filiform and their length is almost twice the size of the body. In the female, the wings do not cover all of the abdomen, which at its tip shows the cerci and a long pin-shaped ovipositor. coffee plant. Three or four generations appear per year. The attacks are more severe in unshaded coffee plantations. In Honduras, acute infestations have been reported in the dry season in plantations located between 900 and 1,250 m above sea level. Natural Enemies An egg parasitoid wasp, Acmopolynema sp. (Hymenoptera: Mymaridae), has been reported in Honduras and Mexico. Management Sampling Scouting should be conducted to determine the limits of the infestation during the dry season. Upon detection of damage, the trunk bark should be scratched in search of the insect’s eggs. If the damage is recent, the perforations are white and unhatched eggs shall be observed; if the damage is old, the perforations are dark and the eggs have hatched. Cultural Control Weeds should be controlled within and on the edges of the plantation. Severely damaged plants should be re-planted, or pruned of the affected stems, and burned thereafter to eliminate the eggs. Biology and Ecology The bush cricket is active at night, while during daytime it takes refuge in dark places in the weeds, dead leaves and some plants such as bananas (Musa spp.) and izotes (Y. guatemalensis). Only on cloudy days and when it is very abundant can it be seen during the day. The female lays about eight eggs in each oviposition hole, distributing two on each end of the scar it makes on the wood, in an “X” shape. The nymphs emerge in about 3 weeks, and they go through several molts for 3 months before becoming adults. Nymphs and adults can feed from the Biological Control This has not been attempted. Chemical Control In plantations that are close to the affected plantations, a preventive insecticide application with a brush or a manual pump is recommended, treating from the stem base up to 60.0 cm high. Application may be Coffee Pests and their Management repeated once or twice every 20 days. Also, an insecticidal dust can be directed to the main stem, to the soil, and to the plantation edges during the dry season. C There is a large and diverse group of leaf-eating caterpillar species in tropical American countries affecting coffee. The principal leaf-eating caterpillars are shown in Table 17. species, such as Phobetron hipparchia (Cramer), Sibine spp., Olceclostera moresca (Schaus), Megalopyge lanata (Stoll & Cramer) and Automeris sp., among others, have urticating hairs which cause painful lesions to anyone touching them. Measuringworms, which are active nocturnally, possess camouflage which allows them to go unnoticed during the day. In general, the pupation takes place in the soil. In Ecuador, Automeris sp. and Eacles masoni Schaus appear cyclically during the rainy season. The adults or moths have nocturnal habits. Insecticide abuse and climatological changes can affect the natural enemies of leaf-eating caterpillars, so their populations may increase and become damaging. Damage and Economic Importance Natural Enemies Coffee bushes affected by leaf-eating caterpillars show totally or partially consumed leaves. Sometimes the fruits are also affected. Eventually, voracious worms or caterpillar larvae, as well as, their feces, can be observed. Some of these are urticating caterpillars. These insects are frequently mentioned in the coffee pest manuals of South American countries, such as Brazil and Colombia. Some species even defoliate entire sections of the coffee plantation. There are many natural enemies of leaf-eating caterpillars.Among them,birds,parasitic Hymenoptera and Diptera, and fungal, bacterial and viral diseases are notable. Leaf-Eating Caterpillars (Lepidoptera) Distribution Management Sampling Regular inspection of the coffee plantation should be made to detect initial infestation sources. Description As example of leaf-eating caterpillars, Oxidia sp. (Geometridae), is described. When small, they are black, and when large, they are light gray. These caterpillars attain a length of 5.0–6.0 cm. The larvae are called inchworms or measuringworms. Mechanical Control The larvae of urticating worms should be eliminated manually using gloves. In the case of measuringworms, the same can be done, but at night. Adults should be eliminated with light traps. Biology and Ecology Biological Control Adults lay their eggs individually or in groups on the foliage of various plants. The larvae or worm feeds on the foliage. The caterpillar goes through several molts, and as it grows, feeds itself voraciously. Some Bacillus thuringiensis Berliner can be used, particularly at the beginning of infestations when the caterpillars are small. 993 994 C Coffee Pests and their Management Chemical Control Biology and Ecology Some organophosphates and pyrethroids are recommended. In general, the use of chemical insecticides is not necessary, because the natural enemies provide regulation of the populations of these leaf-eating caterpillars. Thus, it is important to preserve the natural enemies, and use insecticides only in extreme cases. Adults feed from the foliage of coffee and other plants. A distinctive characteristic of these weevils is that when they feel threatened they contract their legs and snout and let themselves fall to the ground where they seemingly disappear. Their eggs are laid in the soil and the larvae lead a subterranean life (between 10.0 and 20.0 cm deep), feeding from weed roots, including the coffee plant root. The weevil populations are higher from June through August in Honduras. In Brazil, Pantomorus leucoloma (Boheman) is more frequent in the summer and it attacks both C. arabica and C. canephora. In Honduras, the most frequent attacks appear in the highest altitude areas. Very weedy areas favor infestation. Leaf Weevils (Coleoptera: Curculionidae) Distribution Various leaf weevils are present in coffee plantations in tropical America (Table 17). Natural Enemies Damage and Economic Importance Leaf weevils attack the coffee bush leaves. The leaves show irregular holes, tearing and notches on their edges, often beginning at the tip and from the edge towards the vein. The most affected parts are new leaves and shoots. The damage is caused by the adults, which feed on the coffee foliage. The attack of these weevils can become important when they affect the buds of recently pruned plants and of trees <1 year old. The lesions caused by this pest on the leaves may favor the infection of P. costarricensis. Predation by assassin bugs (Hemiptera: Reduviidae) is reported in Costa Rica. Management Sampling Tender buds and new leaves of the coffee plants should be checked. When the damage only appears on old leaves and not new ones, no control measure should be initiated. Cultural Control Description Larvae are whitish and legless. The color of adults varies according to the species, being off-white (Compsus sp.), light brown with yellow spots (Macrostylus sp.), grayish, light brown or black (Epicaerus capetilensis Sharp.) or green. Their size varies from 9.0 to 13.0 mm. The snout is fairly well developed in these insects. Weeding should not be complete, so that adult and larvae weevils have a feeding source and abstain from attacking the coffee plants. Biological Control It has not been attempted. Coffee Pests and their Management Chemical Control When the populations are large, applications of insecticides to the foliage and then to the soil are recommended. Coffee Bean Weevil, Araecerus fasciculatus (De Geer) (Coleoptera: Anthribidae) Distribution Present in all coffee growing countries in America. Damage and Economic Importance Araecerus fasciculatus attacks stored coffee beans. Coffee beans stored in warehouses, coffee mills and other places used to gather the harvest will show perforations and irregular and relatively large galleries caused by this weevil. Accumulation of a fine yellowish powder is also observed. Highly infested warehouses will have a large number of little beetles, +the walls, roofs and windows. This weevil, which attacks a wide variety of grain in storage, is considered as one of the few economically important pests of stored coffee in the American countries, particularly in South America. It creates problems in warehouses that store poorly processed coffee containing more than 12% humidity. The damage is caused by the weevil larvae, which live in and feed on the grains. The attack is also favored when the warehouse temperature is higher than 27°C and relative humidity is above 60%. In 6 months of infestation, losses of 30% have been estimated. C. arabica apparently is more susceptible than C. canephora. The fruits that remain on the plant after harvest may also be attacked. C 5.0 to 7.0 mm. They have about five molts. Pupal size varies from 3.0 to 4.0 mm. The adult is oval, with an arched body, covered by hairs and with a length of 2.5–4.5 mm. The head has round prominent eyes, with a short, wide, curved-downwards “snout” and the mouthparts distally. Biology and Ecology Adult females lay eggs on the parchment coffee grooves, placing one per grain and approximately three per day. The average number of eggs laid is 52. Larvae create galleries in the seed, and they pupate there also. The life cycle, from egg to adult, is 35–40 days. Between 55 and 74% of the descendants are composed of females. Infestation is more acute on softened coffee beans. Up to ten generations are reported per year. Natural enemies In Colombia, the following natural enemies of A. fasciculatus have been reported: Aniseptoromalus calanadrae (Howard) (Hymenoptera: Pteromalidae), Cephalonomia gallicola (Ashmead) (Hymenoptera: Bethylidae), Cheyletus sp. (Acari: Cheyletidae) and Monieziella sp. (Acari: Tyroglyphidae). Management Sampling Fortnight visits should be made to the storehouses to check the presence of weevils, particularly in the wet season and in places with very humid weather. Description Cultural Control The larva is without legs, white, with a “C” shaped body and a relatively wide thorax. The head is small, light brown in color. They measure from Adequate fertilizing, harvesting and pulp extraction should be conducted. Coffee should be stored 995 996 C Coffee Pests and their Management with adequate humidity. Warehouses and storage places should be kept clean. Infested lots should be set aside and placed in the sunlight. Bilogical Control It is not conducted. Chemical Control In the case of preventive treatments and the treatment of infested lots, fumigation is recommended. After fumigation, spraying of a 3-month residual effect pyrethroid with motorized equipment is recommended. The preventive treatment should be conducted when there are 1–2 weevils/m2 of sacks. Treatment of the walls, floor and roof of the warehouse where the coffee is going to be stored is also recommended. Spider Mites (Acari) Distribution At least, six spider mite species have been recorded in coffee in tropical America (Table 17). Olygonychus (Acari: Tetranychidae) is the most representative genus. Damage and Economic Importance Spider mites attack coffee foliage in all their stages of development. Attacked plants present yellowish, brown or copper colored leaves, with more undulated edges. Sometimes the attacked leaves may dry up and fall. Also, the leaves lose their shine and present a dirty appearance. The symptoms take place in large patches in the coffee plantation, and more frequently in old, poorly attended coffee plantations, and near the roads. These symptoms are easily recognized at a distance. Upon examination of the upper face of the leave with a magnifying glass, little animals moving on the leave can be observed, and in general, silky threads which retain dust and other residues. The damage, which consists of the destruction of superficial cells of the leaf, is caused by immature and adult mites when they feed. Spider mites may be especially important in some areas of tropical American countries during abnormally dry weather. In severe attacks the leaf functions are interrupted and they may drop. Leaf defoliation and yield decreases may occur when more than 30 mites per leaf are present, particularly under dry weather conditions. The economic importance of some species of mites on coffee, for example, Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae) in Brazil, is unknown. Description The egg is elliptic or spherical, bright orange, reddish or red in color, depending on the species. Its length varies from 0.100 to 0.127 mm. The larva has three pairs of legs, an almost circular body, and according to the species, orange or yellow colored when hatching, turning green-yellowish as they feed. They are from 0.15 to 0.16 mm long. Nymphs (protonymph and deutonymph) have four pairs of legs, and they are ovoid and about 0.20 mm long. In the deutonymph, which is larger, females (0.20–0.26 mm) can be differentiated from males (0.18–0.23 mm). Adult females are larger (0.28–0.50 mm) and more oval than the males (0.25–0.35 mm). Color varies according to the species and the sex; however, colors such as red and orange are blended, and in some cases the mites have spots. The broad mite, P. latus, has a white-milky color and it is smaller than the other species (0.15–0.20 mm). Biology and Ecology Adult females reproduce sexually and parthenogenetically. The eggs are laid one by one, preferentially on the upper face of leaves, close to the veins, Coffee Pests and their Management although P. latus, unlike the others, prefers the lower side of the leaves. The eggs may be fixed to the leaf with the silk threads (cobweb) produced by the mites and which serves for protection and for moving from one leaf to another. Unlike the Tetranychidae, Tenuipalpidae (Brivipalpus sp.) do not produce silky threads. Egg laying, in the case of Olygonychus coffeae (Nietner), occurs at a rate of 4–6 eggs/day/female for 2 or 3 weeks. Upon eclosion, the larvae feed from cells that they puncture with their chelicerae, and in time they become protonymphs and the latter become deutonymphs. At the end of their development, both protonymphs and deutonymphs go through an inactive stage called “quiescence.” An accumulation of various residual materials such as dust and the old exuviae of spider mites can be observed in the cobweb producing species. The egg to adult life cycle varies from 8 to 28 days, according to the temperature. Females mate with one or more males, and a male may fertilize several females. Females, which are more abundant than males, disperse from one leaf to another and from one coffee plant to another, by the use of silk threads. However, the factors that contribute the most to dispersion are the wind, humans and other animals. Spider mites prefer to colonize the sunlit coffee plants and the older leaves, although in severe infestations they also attack the young leaves. Natural Enemies Predators such as ladybirds (Coleoptera: Coccinellidae) and rove beetles (Coleoptera: Staphylinidae) are reported. However, the literature on coffee pests is not clear about the predator species present. Management Sampling The plantation should be checked during the summer or dry periods, preferably on roadsides. The infestation of a coffee plantation plot is C determined by making parallel inspection routes 25 m apart from each other, and examining 24 leaves at random from four coffee plants every 25 m. Cultural Control Shade trees should be planted in very sunlit areas. Weed control should be conducted. Adequate fertilizing should be applied. Biological Control Not applied. Chemical Control Some pesticides have a selective action, affecting only mites, and others (non-selective) kill mites and insects. In case of a simultaneous attack by mites and leaf miners, non-selective products are recommended. However, the overuse of this practice can negatively affect the beneficial parasitoids and predators. Applications should be made only to infested areas. Various pesticides are recommended, making one application and sometimes a second one. A population of 30–40 spider mites per leaf in the dry season cause defoliation, so this density must be avoided. References Barrera JF (ed) (2002) Tres plagas del café en Chiapas. El Colegio de la Frontera Sur. México, 198 pp Cárdenas-M R, Posada-F FJ (2001) Los insectos y otros habitantes de cafetales y platanales. Comité Departamental de Cafeteros del Quindío. Armenia, Colombia, 250 pp Castillo-Ponce G, Contreras-J A, Zamarripa-C A, Méndez-L I, Vázquez-M M, HolguínM F, Fernández-R A (1996) Tecnología para la producción de café en México. Instituto Nacional de Investigaciones Forestales y Agropecuarias. México. 88 pp. Primera reimpresión. Folleto Técnico Núm 8 Coffee Industry Development Company Ltd (1986) Growing coffee in Jamaica. Jamaica, 103 pp 997 998 C Cold Tolerance in Insects García-G A, Campos-A O, Barrera-S CA, Meoño-R JE (1998) Manual de caficultura. Tercera edición. Asociación Nacional del Café, Guatemala, 218 pp Le Pelley RH (1973) Las plagas del café. Editorial Labor, SA, Barcelona, 693 pp Matiello JB (1991) O café. Do cultivo ao consumo. Publicações Globo Rural. Coleção do Agricultor. Grãos. Editora Globo, SA, Brasil, 320 pp Muñoz-H R (2001) Plagas insectiles del cafeto. In: Manual de caficultura. Instituto Hondureño del Café, Honduras, pp 115–142 Páliz-S V, Mendoza-M J (1993) Plagas del cafeto. In: Manual de caficultura. Estación Experimental Pichilingue. GTZ, FUNDAGRO, Quevedo, Ecuador, pp 144–166 Cold Tolerance in Insects david rivers Loyola College in Maryland, Baltimore, MD, USA Exposure to low temperatures is among the most important abiotic factors limiting the range of insects in temperate climates. The relationship between insects and cold is dynamic, particularly when considering the actual temperature at the surface of the integument versus internal and/or ambient conditions, the length of exposure to low temperature, and the degree of temperature fluctuation over a defined period of time (e.g., day, week or winter season). These issues make it challenging to categorize insect tolerance to a specific set of temperatures, particularly in terms of survival. As poikilotherms, although some are heterothermic under specific conditions, insects have adapted to cold environments resulting in extension of locomotor and/or reproductive activity during low temperature exposure, enhancement of metabolic rate, and maintenance of a positive energy balance. The implications to many of these insects are a lengthening of the life cycle and a requirement for individuals to overwinter one or more times. The actual mechanisms associated with these adaptations have received extensive study in recent years, including attempts to decipher the underlying genetic basis of individual and population responses to low temperatures and seasonal change. Classification of Cold Tolerance Insect cold tolerance classifications have traditionally been divided into freezing tolerance and freeze intolerant strategies. This division has been criticized in recent years by a number of investigators. The arguments for the classification scheme have depended on the definitions applied to the two terms, and it is how freezing tolerant and freeze intolerant species have been defined that evokes the controversy. For example, in freeze tolerance, these insects are said to be capable of withstanding ice formation in some or nearly all parts of the body and associated fluids. Most insects in this grouping usually freeze at temperatures between −5 and −10°C, though others require lower temperatures. Once frozen, these species can tolerate cooling to much lower temperatures, and upon thawing, the insects recover and apparently resume normal development and behaviors. Some experts, however, have contended that this example of freeze tolerance is at the extreme end of cold tolerance and only represents insects which are most suited to survive low temperatures. An examination of some 60–70 species of insects classified as freezing tolerant has led to the suggestion that there are distinct freeze tolerance strategies that allow insects to be grouped based on supercooling points (SCPs) and lower lethal temperature (LLT): (i) partially freeze tolerant species that survive a small portion of their body water converted to ice; (ii) moderately freeze tolerant species, if the exposure is sufficiently long, die at temperatures <10° below their SCP; (iii) strongly freezing tolerant insect species display LLT twenty degrees or more below their SCP; and (iv) freezing tolerant species possess very low SCPs and freeze at extremely low temperatures. Insects in this latter group are capable of surviving at temperatures a few degrees below their SCP. Insects that are not tolerant of any ice formation in their bodies are generally termed freeze intolerant species. The natural tendency has been to assume that these insects will die if tissues or body fluids freeze, and presumably if they avoid the frozen state, these insects will survive. Such Cold Tolerance in Insects classification appears to be an oversimplification of the freeze intolerant strategy, because most species of insects found in temperate regions are susceptible to injury and possibly death at non-freezing temperatures. For these insects, the more correct terminology for their low temperature survival strategy is freeze susceptible (avoidance). In this classification, a distinction is made between freezing and chilling, recognizing that injury and death may result from low-temperature processes occurring at non-freezing temperatures. Even in this system of classification, there is further division in which freeze avoiding species are distinguished from those insects susceptible to chilling. Freeze avoidance is defined as both a low temperature survival strategy and a description of a specific circumstance under which the insect will die, that is, when it freezes. Chill tolerant species possess extensive supercooling ability and a high level of cold tolerance, but is distinguished from the freeze avoiding insects by displaying some mortality above the SCP, which in most cases increases with decreasing temperatures and increasing length of exposure. Some insects are strongly influenced by the severity of the preceding winter conditions, indicating that the cold tolerance of these species is not as well developed as those that seem to be independent of yearly variations in winter temperatures. These insects are referred to as chill susceptible and are characterized by extensive supercooling that allows them to survive moderate low temperature exposure (0–5°C), but only brief exposure to temperatures below −5°C can induce death. SCPs are not indicators of cold temperature tolerance in these species. The final category of cold tolerance is termed opportunistic survival. It is used to describe insects that originate in tropical or semi-tropical regions, which implies that these species are deficient in cold hardiness adaptations or characteristics, and as such, are not likely to survive at temperatures below the threshold that permits “normal metabolism.” These insects may have extensive supercooling but can only survive low temperatures by opportunistic exploitation of a favorable habitat or location. Essentially such C insects are non-hardy since they possess no physiological adaptations to survive low temperatures. Mechanisms of Cold Tolerance Cold adapted insects have developed a complex of strategies that allow survival at their physiological temperature minimum. These strategies broadly include (i) morphological (e.g., melanism, hair/ pubescence, reduction in size, physical barriers); (ii) behavioral (migration, opportunistic exploitation, parasitism); (iii) physiological (depression of SCPs, removal or acquisition of ice nucleators); and (iv) biochemical (synthesis of antifreeze proteins and/or polyhydric alcohols) adaptations. The latter two adaptations have received considerable attention, resulting in a fairly clear picture of the mechanisms characteristically associated with freeze tolerant versus freeze susceptible strategies. In freeze-tolerant insects, potent ice-nucleating agents are produced or acquired in the extracellular fluids, promoting a protective extracellular freezing at a few degrees below zero. Polyhydroxy alcohols (polyols) and sugars accumulate in extracellular fluids to cryoprotect partially frozen tissues. In addition, fat body and localized tissues synthesize antifreeze proteins that function to inhibit secondary recrystallization of ice. Collectively, these adaptations sharply drop the lower lethal temperature to –40°C or below. Other adaptations used by freeze tolerant insects include changes in membrane composition to maintain the liquid crystalline state at low temperatures, a process referred to as homeoviscous adaptation. These changes can occur at low temperatures through an increase in points of unsaturation along phospholipids fatty acid chains. Membrane composition changes have also been shown to occur by increasing the cholesterol content or changes in the distribution of phospholipid classes composing plasma membranes. Changes in membrane composition are not restricted to freezing strategies and can occur with freeze susceptible species as well. In contrast, freeze susceptible species generally attempt to remove or inactivate ice nucleators, 999 1000 C Cole Crops most commonly through purging the contents of the digestive tract. Many of these insects have the ability to maintain a liquid state at temperatures well below the equilibrium freezing point (FP) of their body fluids through manipulation of the colligative properties of their body fluids. This can be achieved by increasing the solute concentration of extracellular fluids (directly or through a reduction of water mass), accumulation of cryoprotective polyols and sugars, and through supercooling. Production of thermal hysteresis factors function to stabilize the supercooled state. Some species also elicit a rapid cold-hardening (RCH) response that protects insects against non-freezing (cold shock) injury. Rapid cold-hardening is a swift physiological response elicited by exposure to mild chilling to turn on one or more of the above mechanisms to enhance the cold hardiness of insects, thereby affording protection from exposure to subsequent low temperature exposures. Together, these adaptations contribute to a depression of the SCP and lower the temperatures that promote freezing.  Diapause  Overwintering in Insects  Thermoregulation in Insects References Bale JS (1996) Insect cold hardiness: a matter of life and death. Eur J Entomol 93:369–382 Lee RE Jr, Denlinger DL (1991) Insects at low temperatures. Chapman & Hall, New York, 513 pp Lencioni V (2004) Survival strategies of freshwater insects in cold environments. J Limnol 63:45–55 Sinclair BJ (1999) Insect cold tolerance: how many kinds of frozen? Eur J Entomol 96:157–164 Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832 Cole Crops Crops of the family Cruciferae, such as cabbage, broccoli, and collard. Cole crops are also called crucifers. Collectors In an aquatic community, insects that collect fine particles of organic matter from the water. Coleophoridae A family of moths (order Lepidoptera). They commonly are known as casebearer moths.  Casebearer Moths  Butterflies and Moths Coleoptera An order of insects. They commonly are known as beetles.  Beetles Collecting and Preserving Insects pauL m. Choate, J. howard frank University of Florida, Gainesville, FL, USA Insects provide many opportunities for biological studies, ranging from detailed research to casual field observations. Frequently the need arises for collecting specimens to accurately identify the species of interest. Collecting techniques and methods of preservation of insects vary considerably. A few of these techniques are described here. Key elements to successful insect collecting Collectors frequently wish to find as many different insects as possible. In order to accomplish this, the greater the diversity of collection techniques employed and habitats explored, the greater the diversity of insects that will be collected. Collecting and Preserving Insects Most entomology textbooks present an overview of collecting and preserving insects for study. There are two major categories of information dealing with these subjects, collecting techniques and preservation techniques (how to deal with the insects once collected). Collecting Techniques Collecting techniques are limited only by the imagination of the student or researcher. Practically any technique will yield a few insects. Here are a few: Hand-collecting, turning over logs and rocks and other objects Unbaited pitfall traps Pitfall traps baited with carrion, dung, yeast, or fermented fruits Hand-collecting, or use of sweep nets, beating trays, aspirators Cutting sections of plants to place into containers within which the insects will later emerge, breaking logs apart with an ax or chisel, stripping bark of dead trees to find subcortical insects Hand-held nets Passive intercept traps: Malaise and window traps Attractant traps with mercury-vapor or ultraviolet light, or carbon dioxide, or specific insect pheromones as bait For Subterranean Insects Sifting soil or debris with a sieve Placing debris into a Berlese or Tullgren funnel to extract insects by heat, or light, or a chemical repellent Aquatic nets Living Insects If your objective is to collect insects alive for study alive, then your best option to prevent damage is to chill them as soon as they are collected. To do this, place them into suitable containers in an insulated chest with ice or other refrigerant, and C transport them as soon as you can. If your objective is to kill them to obtain preserved specimens, kill rapidly to prevent damage. Killing Methods Large specimens typically are killed in a jar with a closely fitting lid using a volatile toxicant such as ethyl acetate absorbed onto plaster or sawdust or cotton. Small specimens may be killed in vials using the same toxicant. Alternatively, if they will not be damaged by immersion in liquid, they may be killed in 70% alcohol or soapy water. Freezing (several hours) also is an option, though it may result in certain deformities. Recording Vials or other containers should be labeled in the field as the specimens are collected. Never use a ball-point pen for insect labels; if you do not have a pen with India ink available in the field, make a temporary label with pencil. Record at least all the information you may eventually need (see section below on Labeling specimens). Preserving Insects Small and soft-bodied insects should be stored in 70% alcohol (either ethanol or isopropanol) in tightly sealed glass vials. Isopropanol (rubbing alcohol) is inexpensive and readily obtained in most countries. Ethanol may be subject to excise laws because it may be used for human consumption, so typically is more expensive and more difficult to obtain, and there seems to be no point in going to that trouble if isopropanol can be obtained.A label should be placed in the vial, with information printed or written in insoluble ink. An additional label may be taped to the outside of the vial. Insect larvae may need brief insertion in boiling water before they are preserved in alcohol, without which they will blacken. 1001 1002 C Collecting and Preserving Insects Vials These are available in many shapes and sizes. Plastic vials are useful in the field because they are less subject to breakage than are glass vials, but glass vials are very much preferable for longterm storage. When specimens are stored in alcohol in vials, be aware that the type of vial and type of stopper is important. Straight-sided glass vials (“shell vials”) are thinner-walled and more fragile than other types. Vials stoppered with screw-caps or corks will sooner or later allow the liquid contents to evaporate. Thick-walled glass vials with necks (“homeopathic vials”), when fitted with natural rubber stoppers, seem to offer the greatest permanence, but the rubber will eventually crack and decompose. Stoppers of neoprene or other synthetic materials have not yet shown an advantage over natural rubber. If using homeopathic vials with rubber or neoprene stoppers, it is important to seat the stopper firmly; this may be done by inserting a straightened-out steel paper clip alongside the stopper as the latter is inserted, then withdrawing the paper clip to release trapped air. All vials should be checked periodically for leakage and loss of preservative. Collecting and Preserving Insects, Figure 75 Spreading board used to prepare moths and butterflies. Different insects require different mounting techniques. Large moths and butterflies and some other winged insects are mounted with wings neatly (Fig. 75) spread on a spreading board. increasing in thickness with increase in numerical value. Extremely narrow pins are of size 00, and extremely thick pins are of sizes 4–7 but are longer. Most insects large enough to be pinned may be pinned on sizes 2 or 3. Insects are pinned in specific locations depending on their classification. Large beetles are pinned in the middle of their right wing cover, close to the front margin. Other examples of pin positions are included in the diagrams provided in the accompanying figures. (In the United Kingdom, white brass pins once were used; their length varied with width). Minuten pins (from a German adjective meaning minute) are very small, fine pins used for pinning tiny insects into a small block of pinning material, which is in turn pinned by a standard pin. Pinning Storage in Transparent Envelopes Insects of average size usually are mounted on pins. In many countries, steel pins of 3.5 cm length are used; the best quality is stainless steel with nylon heads. Lacquered steel pins may rust, and brass pins may corrode (become covered with green verdigris) in humid climates. Pin widths are numerically designated, with standard sizes 0–3 Some Odonatologists (dragonfly collectors) stuff their specimens into semi-transparent (Glassine) envelopes. This is an alternative to pinning (Fig. 76) specimens, saving much museum space. However, this is not necessarily the most desirable method of storage because the specimens are prone to breakage. Mounting Techniques Collecting and Preserving Insects Collecting and Preserving Insects, Figure 76 Position of pins in various kinds of insects. Pointing Insects too small to be pinned safely may be mounted on cardboard points, glued to the point on their right side. Points should be bent down slightly to better attach to the side of each specimen. Such points may be purchased, or may be made by a hand-held device called a point press, which cuts points (Fig. 77) from a sheet of cardboard. Care should be taken not to cover the underside of the insect with glue, obscuring key characters. This is the standard mounting technique in the USA, and it is claimed to be better because underside characters are visible. However, there are two major problems: (i) insects thus mounted are very susceptible to physical damage, Collecting and Preserving Insects, Figure 77 Examples of how to position mounting point under right side of insect specimen. C 1003 1004 C Collecting and Preserving Insects and (ii) adhesives used to obtain secure adhesion to the small surface may be soluble only in harsh solvents (benzene, toluene, xylene, acetone, etc.). Subsequent attempts to dissect soft body tissues are thwarted because these are destroyed. (2) It is said that such a method of preparation is more time-consuming. This may be true, but it varies with the expertise of the preparator. More importantly, if the specimen is rare and from a distant locality, it makes far more sense to spend a few seconds more to prepare it this way (better-protected) Card Mounts Some groups of insects are better mounted on tiny (Figs. 78–80) rectangular cards. Cards of standard sizes are sold by some supply houses. This technique is popular with European entomologists. It is claimed to be better because the specimens are better-protected from physical damage and because they may be viewed in one plane against the white background of the card (as contrasted with specimens that may be drooped over card points), and because they may later be removed easily for dissection. Only water-soluble adhesives should be used. There are perhaps two problems: (1) The underside characters are not visible without removal from the card. However, preparators with a series of specimens available will mount some dorsal side up, and some ventral side up. Collecting and Preserving Insects, Figure 78 Minuten pin used to position small insect above piece of cork. This technique is frequently used for delicate flies and very small moths and butterflies. Collecting and Preserving Insects, Figure 79 Card-mounted specimen (European fashion). Collecting and Preserving Insects, Figure 80 Large long-legged flies such as crane flies may need to have their body supported with an extra large point. Alternatively, the specimen could be place on a card mount, which will offer much more protection from damage by protecting the legs, too. Collecting and Preserving Insects than to face the days or weeks and expense necessary to collect more specimen from the distant locality, even assuming that a replacement specimen can be found for a rare species. Adhesives Many kinds of adhesives are used to secure insects to card points. The objective is to secure the insect firmly to the point. It is recommended that only water-soluble or alcohol-soluble adhesives be used. When other kinds of adhesives are used, there will arise questions about the necessary solvents to remove the specimens (it is virtually impossible to guess what adhesive some collector may have used and what its solvent is). For specimens adhered to card mounts, only water-soluble adhesives should be used. When card-mounting, the strength of the adhesive is less important because much more surface area is used. Many water-soluble adhesives are available, although the two most commonly sold in stationery stores in the USA are unsuitable, one because it dries hard, cracks and turns brown, and the other because it is not truly transparent and dries from the outside inward, forming first a sticky “skin.” Card Mounts, Card Points, and Labels Use only a heavy weight, high quality, non-yellowing, 100% rag card stock for making these items. Some years ago, “Bristol board,” a laminated card, was recommended. We see no advantage to such laminated card stock. Genitalia It is often desirable to dissect specimens to make the genitalia evident for identification purposes. With card-mounted specimens, the genitalia (if large enough and well-sclerotized) may be mounted on the same card as the specimen, a great advantage. If, C however, they are feebly sclerotized or too small, they may be mounted (after dehydration through alcohols to xylene) in a drop of Canada balsam on a small celluloid rectangle pinned directly below the specimen (no cover slip is needed). When specimens are card-pointed, the usual method is to place them in “genitalia vials” pinned through the stopper below the specimen. Such genitalia vials are tiny, of glass or plastic, and contain a cork or stopper of some synthetic material; typically, they contain alcohol, glycerine, or a mixture of the two. When genitalia almost fill the vial, and when such vials are checked frequently for leakage, the method may have merit. Otherwise they can be disastrous: extremely small genitalia in a vial can be lost when the stopper is pulled, or the vial can leak and desiccate the parts. Such genitalia vials are to be avoided wherever possible. Slides Some insect specimens are best mounted on microscope slides. These include very small and soft-bodied insects as well as dissections of insect parts. The most permanent mountant available is Canada balsam. Some insects (scale insects, aphids and lice, minute parasitic Hymenoptera, and many insect larvae) typically are prepared by clearing and differential staining before being mounted on microscope slides. Soft-Bodied Specimens Because of their hard exoskeleton, very many insects will maintain their shape when dead and dry. Some, however, will not – they tend to shrivel. Techniques have been developed for maintaining the shape of dried specimens (one alternative was to preserve them in alcohol, another to mount them on microscope slides). For decades, the preferred method for preserving large Orthoptera (grasshoppers and crickets), Phasmida (stick-insects) and Mantodea (mantids) was to eviscerate them and stuff their 1005 1006 C Collecting and Preserving Insects abdomen with cotton before pinning and drying. For Odonata (dragonflies and damselflies), the method was to eviscerate them and stuff a toothpick-shaped object into the abdominal cavity. For larvae of butterflies and moths (caterpillars), the method was to roll the abdominal contents out through the anus, then inflate the abdomen (by blowing into it) while drying the inflated skin in a tiny oven. Mosquitoes and some other flies, and Trichoptera, having feeble exoskeletons, could not be dealt with by such rough physical methods because they are covered in scales, and the scales would be lost by such treatment; they were destined to shrivel as they dried. Many of these methods have now been abandoned because of the availability of critical-point drying. A critical-point drier is an expensive piece of equipment and may be unavailable in some institutions and to amateur collectors. The top label should contain (i) country, (ii) province or state, etc., (iii) township, etc., (iv) route information when known if the collection was a result of a route followed, (v) date of collection, and (vi) collector’s name(s). A second label should contain method of collection (bait, technique, trap) and habitat. Dates should be written in order day-month-year (the international standard) with month either in letters or in Roman numerals and the year with four digits. For example, a date of the 4th of July 2002 should thus be written as 4-JUL-2002 or 4-VII-2002, and not as 7/04/02 (as in commonly done in the USA) or as 4/7/02 (as is commonly done in most of the world) or as 2002/7/4 as is commonly done in the Far East. A third label may contain rearing information. A fourth label may contain determination information, species name, determiner, and date of determination. Labeling Specimens Pinning Blocks Specimens without accurate and complete collection data are of little value. A proper label contains locality data, date of collection, collector’s name, method of collection, and identification label with determiner’s name. Additional information may be included (host plant, behavior, etc.). Computergenerated laser-printed labels in general seem entirely adequate. Such labels with a font size of 3 or 4 are suitable for pinned specimens. Labels with larger font (10 or 12) can be used in vials with alcohol. Most laser-printer inks seem stable in alcohol (you may want to test labels made with the laser printer available to you before relying upon them), and printed labels are far easier to read than are most hand-written labels, Use them wherever you can for pinned and alcohol-preserved specimens (provided that the ink is not alcohol-soluble). Information on Labels Labels for pinned insects should be placed beneath specimens, aligned parallel with the insect’s body. Supply houses sell blocks on which specimens and labels may be pinned. These achieve a standard height for each specimen and label and make a resultant collection appear more uniform. Unfortunately, we have not seen a block from a supply house with more than three steps. If the steps are (i) specimen, (ii) dissections of genitalia from the specimen, (iii) locality information, (iv) habitat information, and (v) identification information, then five steps are needed. The only current option seems to be for collectors to manufacture their own pinning blocks (one of us has done so). Storing Collections Insect collections require protection from atmospheric conditions such as humidity and pests capable of destroying specimens. Such pests include cockroaches, silverfish, ants, dermestid and anobiid beetles, booklice, and mice. Tight Collecting and Preserving Insects containers, with a fumigant, will deter most pests. Be sure not to use chemicals toxic to humans or pets. The safest method is to store in or donate a collection to a recognized museum where it will be maintained safely. Museum curators often will provide space for your materials, hoping that at some time in the future you will donate your collection to them. C Supply Houses Several companies maintain an inventory of entomological supplies and sell by mail order. They sell nets, beating sheets, light traps, vials, pins, forceps, lenses, pinning blocks, storage boxes, cabinets, microscopes, microscope illuminators, microscope slides, preservatives, light traps, numerous other items, and assorted entomological literature. Storage Containers and Cabinets Insect specimens are typically housed in wooden storage boxes (in the USA called Schmit or Schmitt or Schmidt boxes) or in cabinets with drawers. The storage boxes have tightly-fitting lids, and the floor is lined with a material into which pins can easily be thrust. Traditionally, this material was cork, usually lined with paper, but now is normally some white synthetic foam. European cabinets were and are of numerous sizes, each drawer lined with a pinning material. The disadvantage of the European system is that dozens or hundreds of specimens may have to be moved one by one to make way for a few new specimens. Additionally, drawers of some cabinets are exceptionally shallow, allowing vertical space only for short pins. In the USA, another system arose in which drawers of standard size were designed to accept a standard number of cardboard unit trays, the unit trays (not the drawers themselves) are lined with a pinning material, and all drawers accept standard 3.5 cm pins. Unit trays are manufactured in a range of complementary sizes so that a combination of small and large trays, as need arises, will fit precisely into a drawer. The trays make it easy to move groups of specimens about a drawer or from drawer to drawer, and protect specimens from physical damage. The “US system” was a good idea, but, unfortunately, the “system” is at least three systems, not one, and developed at competing museums, which differ in dimensions of drawers and size of unit trays so that they are not interchangeable. Permits A very few species of insects have been declared to be endangered species. They may not be collected, even on your own property, without a very hard-to-obtain permit. In many countries, you may collect any other insect (apart from endangered species) on your own property, or (with permission from the landowner) on someone else’s property. If the landowner is a government agency and the property is a park or preserve, you may need a written permit from that agency. In a few countries you may not collect insects of any kind without a government permit; even if you use a pesticide to kill pests on your property, and along with the pests you kill harmless or beneficial insects, you may not collect any of these insects without a permit. So, be aware of the laws in your country. References Hatch M (1926) Concerning the insect collection. Entomol News 37:329–332 Lehker GE, Deay HO (1969) How to collect, preserve, and identify insects. Extension circular 509. Cooperative Extension Service, Purdue University, Lafayette, IA, 43 pp Ross HH (1962) How to collect and preserve insects. Illinois State Natural History Survey Circular 39, Urbana, IL, 71 pp Smart J (1954) Instructions for collectors. No 4A Insects. British Museum (Natural History), London, UK, 178 pp Steyskal GC, Murphy WL, Hoover EM (eds) (1986) Insects and mites: techniques for collection and preservation. US 1007 1008 C Collembola Department of Agriculture, Miscellaneous Publication No 1443, Washington, DC, 103 pp. Available Online at http:// www.sel.barc.usda.gov/Selhome/collpres/contents.htm Collembola An order of hexapods in the class Entognatha, and sometimes considered to be insects. They commonly are called springtails.  Springtails Colleterial Glands Female insects commonly secrete glue that attaches the egg to a substrate. Also secreted in some cases are jelly-like materials, oothecae, or pods containing the individual eggs. The glands that secrete these are known by various names, including accessory, mucous, cement, and colleterial glands. Colonization The introduction and establishment of a species, usually a beneficial insect, in a new geographic area or habitat. Colony A group of individuals, other than a mated pair, which rears offspring in a cooperative manner, and may construct a nest. (contrast with aggregation) Colony Fission Among social insects, the same as budding: multiplication of colonies by the departure from the parental nest of one or more reproductive forms accompanied by workers. Thus, the parental nest remains functional and new ones are founded. Colletidae A family of bees (order Hymenoptera, superfamily Apoidae). They commonly are known as plasterer bees and yellow-faced bees.  Wasps, Ants, Bees and Sawflies  Bees Collophore A tube-like structure located ventrally on the first abdominal segment of springtails (Collembola). Colobathristidae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs Coloburiscidae A family of mayflies (order Ephemeroptera).  Mayflies Colony Odor The odor specific to a particular colony. This odor allows social insects to identify their nestmates among others of the same species.  Social Insect Pheromones Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) donaLd C. weBer USDA Agricultural Research Service, Beltsville, MD, USA Colorado potato beetle is the most important insect pest of potatoes in the northern hemisphere. Larvae and adults feed on potato foliage, and under many agricultural conditions the pest will completely defoliate the crop if not controlled. It is also a major pest of eggplant (aubergine) and tomato in some regions, as well as feeding on Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) solanaceous weeds such as horsenettle, Solanum carolinense. Although it is occasionally found on other nightshade crops such as peppers (Capsicum), tobacco, and husk tomato (Physalis), it cannot complete its life-cycle on these hosts. The original range of Colorado potato beetle was probably restricted to southwestern USA and/ or northern Mexico, where the host plants were the spiny nightshade herbs Solanum rostratum (buffalobur) and Solanum elaeagnifolium (silverleaf nightshade). The species was described in 1824, but the first occurrence on potato was not reported until 1859 in Nebraska. From there it spread rapidly, especially eastward, reaching the Atlantic coast of North America in 1874. By then the potato crop was a staple food, and the spread of Colorado potato beetle infestation prompted early development of arsenical pesticides and application methods in the USA. In 1870, responding in part to the threat of Colorado potato beetle introduction, Germany established the first-ever quarantine law followed within several years by other European countries. Following the eradication of numerous isolated European introductions, its establishment into France in 1921 initiated another rapid geographic invasion which now includes all of Europe (except for the United Kingdom, Ireland, and Scandinavia), continues through central Asia eastward into China, and threatens to spread into east and south Asia, where one-third of the world’s potatoes are grown. The range is now about 8 million km2 in North America and a like area in Eurasia. Climatically favorable areas not yet infested include east Asia, parts of south Asia temperate South America and Africa, Australia and New Zealand. Colorado potato beetle adults are approximately 10 mm long, convex, with cream-yellow and black striped elytra, and variable black markings (Fig. 81) in the pronotum. Larvae are typically orange with two rows of black lateral spots, and as later instars are characteristically hump-backed in shape. Colorado potato beetle overwinters as the adult in the soil, and has from one to several generations per year, depending on temperature, C photoperiod, and availability and quality of host plants. In the spring, overwintered adults emerge from the soil and begin their search for host plants to feed upon. This commences with walking, but after a few days beetles may take to flight. The yellow-orange eggs, laid on leaf undersides in masses of 20–60 (several hundred to a few thousand total per female), soon hatch into leaf-feeding larvae which eat about 40 cm2 of foliage. The fourth instar larva drops to the ground and digs down a few cm to pupate in the soil, emerging 10–20 days later as a callow adult. Also a voracious leaf feeder, the imago consumes up to 10 cm2 per day. Depending on food, photoperiod, and temperature, this young adult may mate and reproduce, or after feeding, bury itself 10–50 cm deep in the soil to spend months in diapause before emerging the next spring. In areas where tomatoes abound, it has evolved an improved fitness on this plant, as in the southeastern USA and Uzbekistan. Even where it does not thrive on tomato, large numbers may damage this valuable crop. In contrast, potato plants can tolerate light to moderate defoliation at certain times of year, but without control, major to complete crop loss is common. A typical economic threshold is one adult equivalent per plant, where small larvae are counted as equivalent to 1/4 of one adult, and large larvae (3rd and 4th instars) equate to 2/3 of an adult. Yield impact is dependent on timing, variety, and other crop stresses. In early years, control relied on hand-picking, but this gave way to arsenical insecticides and in the 1940s the more powerful synthetic chemical controls. No other agricultural pest better exemplifies evolution of resistance to insecticides. Within the first decade of DDT use, it was failing against Colorado potato beetle in the intensive potatogrowing region of Long Island, New York, USA. Resistance followed to numerous other chlorinated hydrocarbons, organophosphates, carbamates, and pyrethroids. This sustained evolution of pesticide resistance has prompted development and use of additional novel chemical controls such as neonicotinoids and ecdysteroids, as well as transgenic crops incorporating high levels of beetle-specific 1009 1010 C Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), Figure 81 Colorado potato beetle (a) egg mass, (b) larvae, (c) pupa and (d) adult. (Egg mass photo by D. Weber; others by Doro Röthlisberger, Zoological Museum, University of Zurich.) Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) Cry3A BT toxins (derived from Bacillus thuringiensis). Transgenic potatoes were developed and introduced as the cultivar “Newleaf ” in the 1990s, later also incorporating resistance to important aphid-transmitted potato viruses. Yet this highly effective tactic met with a mixed and then negative reception, first because it was introduced contemporaneously with an effective and broaderspectrum systemic insecticide, imidacloprid, and later because large multinational processors decided that using transgenic potatoes would risk consumer opposition across their global markets. Two years after registration in the US, major buyers announced plans to discontinue Newleaf purchases, and commercial sales have been discontinued. Transgenic technology continues with limited field trials in eastern Europe, and may be commercialized in the future. One prerequisite for sustainable use, as with chemical controls, is the implementation of resistance management plans. Periodic failure of chemical controls has prompted research into a variety of alternatives ranging from pedestrian to peculiar. These include native and introduced biological controls, crop rotation, cover crop mulches, trap crops, trenches to disrupt crop colonization, early planting, late planting, and multi-row propane-fueled flamers and crop vacuums. Collectively and as complements to chemical control, these are essential tactics to manage the pest and help avert resistance. For an insect that is the focus of thousands of published scientific articles, there is still surprisingly much to learn. In just the past few years, plant-based attractants as well as a male-produced aggregation pheromone, (S)-3,7-dimethyl-2-oxo-6-octene-1,3diol, have been discovered. The exact role that these behaviorally active substances will play in Colorado potato beetle management remains to be seen, but perhaps in combination with selective toxins and/or antifeedants, a push-pull behavioral strategy can succeed in suppressing the Colorado potato beetle instead of whole-field treatments which have historically failed due to selection of resistance. Natural enemies of Colorado potato beetle may sometimes keep the pest below economic C threshold, but not reliably in most current cropping systems. Predatory stink bugs (Podisus and Perillus) as well as several species of generalist Coccinellidae and Carabidae, spiders and harvestmen are common predators. During the 1980s, the egg parasitoid wasp Edovum puttleri was introduced to the USA from Colombia (where it is native on L. undecemlineata (Stål)), and enjoyed success as an inundative biocontrol in the highvalue eggplant crop. This parasitoid is not winterhardy. Rearing efforts ceased with the advent of the systemic neonicotinoid imidacloprid. Two of the most promising natural enemies native to North America are quite poorly studied. Lebia grandis is a carabid ground beetle predator of Colorado potato beetle eggs and larvae as an adult, whose larvae are ectoparasitoids of Colorado potato beetle pupae. The newly hatched larvae locate the Colorado potato beetle host soon after it buries itself to pupate, then obtain their entire larval food requirement from a single host pupa, emerging weeks later as blue-metallic and orange, very mobile and hungry adult predator beetles. Two species of tachinid parasitoid flies of the genus Myiopharus attack larvae or in the fall even Colorado potato beetle adults, where they overwinter as an early-instar larva inside their host, then develop and emerge the next season as an adult fly. Beauveria bassiana has potential to suppress Colorado potato beetle populations under some conditions, and commercial formulations have been developed. If the agroecosystem can somehow better nurture natural enemies, especially early in the season before Colorado potato beetle damage the crop, then Colorado potato beetle management may not so frequently require costly and sometimes troublesome insecticidal inputs. Crop rotation is consistently an effective means to delay and reduce colonization of overwintered adults. But in many cases, land tenure and intensive culture may prevent farmers from rotating the several hundred meters which constitute an effective separation in successive years. Yet even unrotated crops are amenable to border treatments, trap crops or trenches to thwart beetle colonization, because 1011 1012 C Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) many adults overwinter in wooded or other noncrop areas adjacent to crop fields. Physical controls of flaming and vacuuming have enjoyed limited success against the pest. Rye straw or other killed cover crops suppress Colorado potato beetle populations, probably by a combination of abiotic and biotic effects. One novel cultural-physical control uses late-maturing trap crops to attract beetles to concentrated overwintering areas which are then stripped of their snow and mulch covering in midwinter to enhance diapause mortality. Colorado potato beetle is one of the most frequently used bioassay insects for toxicological and physiological research, and usually the first beetle to be tested with candidate insecticides. It is easily maintained on a potato diet, hosting few diseases in the lab, and is also amenable to semi-artificial diet, which aids in precisely controlling its nutrition. Colorado potato beetle has played a key role in development of concepts of host-plant location and selection, host shifts, molecular and population mechanisms of pesticide resistance, gene flow, and integrated pest management. There is also active research on conventional and engineered crop resistance, neurophysiology, dispersal behavior, biochemical and molecular reaction of host plants to Colorado potato beetle feeding, digestive, microbial and immunological defenses of Colorado potato beetle and, of course, novel natural and synthetic toxins and antifeedants. Providing sustainable control options requires not only laboratory and molecular insights into the mechanisms, but also ecological and behavioral insights, especially into the movement of beetles within and between fields which could lead to the spread or suppression of pesticide resistance genes in agricultural populations. The quantification of gene flow and frequencies, which in turn depends on selection, dispersal and reproduction, provides the basis for rational deployment of refugia in resistance management. Questions of movement are also critical to effective employment of crop rotation and pest colonization in a variety of regional cropping systems. In some areas, the beetle flies frequently. In others, it flies rarely. In Siberia, it buries deeply over winter, while in milder areas, it buries less deeply. Some beetles delay emergence from diapause for years at a time. Researchers express both reverence and frustration at the variability in its behavior. Just why is the Colorado potato beetle so flexible in responding to changing ecology and toxicology? The reason may lie in its evolutionary history of genetic and biochemical diversity in ecological and evolutionary pursuit of toxicologically complex and ephemeral groups of host plants. This beetle reinforces the need for flexible and integrative thinking in developing pest management strategies: one tactic alone will not quell it for long. Witness the latest entry, the chloronicotinyl imidacloprid, starting to fail after about 10 years of intensive use in the eastern USA. Integration of multiple effective tactics will continue to be essential for an intelligent and sustainable approach to management of the formidable Colorado potato beetle.  Potato Pests and Their Management  Vegetable Pests and Their Management References Boiteau G, Alyokhin A, Ferro DN (2003) The Colorado potato beetle in movement. Can Entomol 135:1–22 Casagrande RA (1987) The Colorado potato beetle: 125 years of mismanagement. Bull Entomol Soc Am 33:142–150 Chang GC, Snyder WE (2004) The relationship between predator density, community composition, and field predation of Colorado potato beetle eggs. Biol Control 31:453–461 Dickens JC, Oliver JE, Hollister B, Davis JC, Klun JA (2002) Breaking a paradigm: male-produced aggregation pheromone for the Colorado potato beetle. J Exp Biol 205:1925–1933 Ferro DN, Logan JA, Voss RH, Elkinton JS (1985) Colorado potato beetle (Coleoptera: Chrysomelidae) temperaturedependent growth and feeding rates. Environ Entomol 14:343–348 Grapputo A, Boman S, Lindström L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219 Jermy T (1994) Hypotheses on oligophagy: how far the case of the Colorado potato beetle supports them. In: Jolivet PH, Cox ML, Petitpierre E (eds) Novel aspects of the biology of Chrysomelidae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 129–139 Common Stoneflies Hough-Goldstein JA, Heimpel GE, Bechmann HE, Mason CE (1993) Arthropod natural enemies of the Colorado potato beetle. Crop Protect 12:324–334 Mota-Sanchez D, Hollingworth RM, Grafius EJ, Moyer DD (2006) Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manag Sci 62:30–37 Weber DC (2003) Colorado beetle: pest on the move. Pest Outlook 14:256–259 Colorado Tick Fever A viral disease transmitted by ticks in the USA.  Ticks C Common Fleas Members of the Siphonaptera).  Fleas family Pulicidae (order Common Name A vernacular name, reflecting the language of a particular country, as opposed to a scientific name, which is universal.  Common (Vernacular) Names of Insects Common Oviduct Columnar Cells The tall, and generally most numerous cells, of the midgut. They conduct most of the enzyme secretion and absorption of digested products. Colydiidae A family of beetles (order Coleoptera). They commonly are known as cylindrical bark beetles.  Beetles A median tube (median oviduct) of the female genital tract (Fig. 82) that leads from the lateral oviducts to the cloaca (vagina).  Reproduction Common Sawflies Members of the family Tenthredinidae (order Hymenoptera, suborder Symphyta).  Wasps, Ants, Bees and Sawflies Common Scorpionflies Comb A layer of brood cells or cocoons produced by social insects and clustered together in a regular arrangement. Members of the family Panorpidae (order Mecoptera).  Scorpionflies Common Skimmers Comb-Clawed Beetles Members of the family Alleculidae (order Coleoptera).  Beetles Commensalism An association between two organisms from distant taxa that harms neither and benefits at least one. A family of dragonflies in the order Odonata: Libellulidae.  Dragonflies and Damselflies Common Stoneflies Members of the stonefly family Perlidae (order Plecoptera).  Stoneflies 1013 1014 C Common Thrips Common Oviduct, Figure 82 Diagram of female reproductive system, as found in Rhagoletis (Diptera) (adapted from Chapman, The insects: structure and function). Common Thrips Members of the family Thripidae (order Thysanoptera).  Thrips Common (Vernacular) Names of Insects J. howard frank University of Florida, Gainesville, FL, USA There are two meanings of the word “common” as applied to names. One is that a name is abundant or widespread. Quite another is that a name is written in the vernacular language of the place where it is used, rather than in Latin. Take, for example, the species Danaus plexippus whose common name in the USA is monarch butterfly. That name is common on both counts. But take instead the scarab species Serica rhypha which has been assigned the invented English language name “crooked silky June beetle.” That “common” name is unlikely to be known to more than a handful of people anywhere; it is a vernacular name that is not commonly used. Very few vernacular names are common in the sense of abundantly used and widespread. A more appropriate term for this entry would be vernacular names, but this expression itself is not common (in the sense of being widely used and abundant), although it deserves to be so. The English language has a few true common names for insects. Ant, bee, beetle, butterfly, and cricket are some of them. They are old names, having come into use before entomologists began to classify the five or six million insect species that may exist. In medieval bestiaries, such names were Common (Vernacular) Names of Insects used as if they applied to individual species, so that we may read in bestiaries about the habits of “the ant” alongside habits of “the lion.” Entomologists soon realized that they were dealing with many species of ants, and by 1990 had described about 8,800 species of them, with the task of description still unfinished. Together, they are classified as the family Formicidae, they have 8,800 + scientific species names, and entomologists call them “the ants.” In contrast,“the lion” of medieval bestiarists remains the one species Panthera leo. The general public seems to have little grasp of this complexity. News writers, when interviewing an entomologist about ants, typically insist that the entomologist provide a “common name” for whatever ant species is being discussed. Then, the news writer typically uses this “common name” and writes about it being “a variety of ant[s].” By using the expression “variety” instead of species, the news writer seems to be drawing on a medieval classification (that “the ant” is the classificatory equivalent of “the lion”), refusing to acknowledge that there may be more than one species of ant. It is a sad reflection on public education that news writers may have only a medieval knowledge of insect classification and, that with such [lack of] knowledge, their task is to inform the public. Entomologists, when challenged with the question of “what is the common name of the insect you are talking about?,” invented some names in vernacular English. They invented such names as “the wood ant,” “the carpenter ant,” “the black imported fire ant,” “the red imported fire ant,” “the Argentine ant” and a few others. But those names do not go C very far in listing the 8,800+ species of ants known worldwide. Even those few names became cumbersome for news writers who preferred greater simplification. Thus, “the red imported fire ant” got simplified to “the fire ant” (by which “the black imported fire ant” became “downsized”). There is no hope for systematically providing “common” (vernacular) names for all the approximately one million insect species that have now been described (and have scientific names) much less the three to five million that have not yet been described. Nor is there any point in doing so in English or the world’s other over 900 current written languages. The emphasis should instead be on providing scientific (Latin) names for all species. Then we will have at least one name that may be used worldwide for each species, as was the intent of scientific names. For any group of people insisting on a name in its own language for some particular insect species where none exists, one may be invented on the spur of the moment. Conventionally, “common names” are not capitalized in English. If, however, a proper noun (such as a geographical name or the name of a person or a month) is incorporated in that “common name,” then that word (a proper noun) alone needs capitalization (for example, “a June beetle”). Vernacular Names Derived from Scientific Names For higher taxa of insects and any other animals, there are accepted methods of deriving English Common (Vernacular) Names of Insects, Table 18 Examples of common (vernacular) names Classification Name Common name Derived singular Derived plural 1 tribe Brachinini bombardier beetles brachinine brachinines 2 subfamily Cicindelinae tiger beetles cicindeline cicindelines 3 family Culicidae mosquitoes culicid culicids 4 order Plecoptera stoneflies plecopteran plecopterans 5 class Insecta – insect insects 6 phylum Arthropoda – arthropod arthropods 1015 1016 C Common (Vernacular) Names of Insects vernacular names (“common names”) from the scientific names. The table below gives the scientific name of a tribe, a subfamily, a family, an order, a class, and a phylum. English vernacular names have been derived as shown. It is unfortunate that the derived vernacular names in rows 1 and 2 are identical in ending. The same method may be used for deriving vernacular names from all names of higher taxa. These derived names are English (not Latin) and are typically written with all letters in the same case, which is to say that there is no more reason to capitalize the first letter than there is to capitalize the first letter of the English words bird or cat. Editorial guidelines of major entomological journals, with no exceptions, require that they not be capitalized, to avoid confusion with scientific names. The same method is used to derive vernacular names in other languages using the Latin alphabet, but with twists according to the language in question. In French, the singular and plural from Culicidae are culicide and culicides, but many French texts do capitalize the first letter. In Italian they are culicido and culicidi, and it seems permissible although not required in at least some Italian entomological journals to capitalize the first letter. In Spanish they are culícido and culícidos, and the tendency, as in English, is not to capitalize the first letter. In German the plural is Culiciden, and this word must be capitalized because all German nouns must have the first letter capitalized; the singular should be Culicid (capitalized), but such a word is avoided by circumlocution. “Official” Common Names The Entomological Society of America has taken an unusual step of publishing a list of “common names.” The names selected for this list and their form are due to opinions of a committee. By 1989 this list had a few more than 2,000 “common names,” and they applied to selected taxa at various levels from subspecies to class, including some non-insect invertebrates. The list was developed because “standardized common names are useful when communicating with the public and with other entomologists.” The list includes names of “species [that], in most cases, will inhabit the United States, Canada, or their possessions and territories.” To promote adoption of these approved names, the ESA requires that only they be used in manuscripts submitted to that society for publication. More than 100,000 species of insects inhabit the United States and/or Canada, and far fewer than 2% of species have been given approved “common names.” ESA’s printed list of common names was recently supplemented with an online capability by which common names or scientific names may be searched (http://www.entsoc.org/pubs/common_ names/index.htm). Long delay in implementing this online search ability, meanwhile requiring purchase of the printed edition, may have contributed to lack of adoption of the approved names by other organizations within the United States. For example, in the mid-1990s, this writer used the ESAapproved “common name” for Apis mellifera (honey bee) in a manuscript submitted as a book chapter for publication by a commercial publishing house. That name was changed to “honeybee” by the editorial staff on grounds that “honeybee” is the “house style” of that publishing house. Outside the United States, the ESA-approved “common names” have even less weight, because contrasting “common names” may be commonly used. For example, the ESA-approved “common name” for the butterfly Pieris rapae is “imported cabbageworm” (based upon the medieval concept that its larva is a “worm,” and the more recent concept that it was “imported” from Europe [in fact, it probably arrived as an immigrant, which is to say that it may have been a contaminant or hitchhiker on some cargo, never deliberately imported, but the possibility that it arrived by a combination of winds and flight from Europe or eastern Asia is hard to rule out]) but, in the United Kingdom where it is native, it has been called “small white” or “small white butterfly” perhaps since the eighteenth century. Australia’s CSIRO and the Entomological Society of Canada list “common” names of insects Compound Eyes on websites http://www.ento.csiro.au/aicn and http://esc-sec.org/menu.htp, respectively, with free public access. Reference ESA (1989) Common names of insects and related organisms. Entomological Society of America, Lanham, MD, 199 pp C Competitive Displacement Replacement of one species by another. Species that replace other species typically are ecological homologues, or nearly so. This also is known as competitive exclusion.  Gause’s Principle Complex Metamorphosis Common Walkingsticks A family of walkingsticks (Heteronemiidae) in the order Phasmatodea.  Walkingsticks and Leaf Insects Communal Behavior A level of sociality less than eusocial behavior. A type of presocial behavior. It involves members of the same generation sharing a nest, but without brood care.  Presocial  Solitary  Subsocial  Communal  Quasisocial  Semisocial  Eusocial Behavior Community A group of populations that interact within a certain geographic area. The biotic portion of an ecosystem. This is also called an ecological community. Companion Planting The interplanting of repellent and susceptible host plants, affording protection to the susceptible plants. A change in body form in which the insect displays a striking change in appearance over the course of its development. This is also referred to as holometabolous development. The developmental process consists of the egg, larval, pupal and adult stages. Complex metamorphosis is also known as complete metamorphosis.  Metamorphosis  Incomplete Metamorphosis Compliance Procedure (for a Consignment) From a regulatory perspective, this is an official procedure that is used to verify that a consignment (usually of plants or other regulated articles) complies with stated phytosanitary procedures.  Risk Analysis (Assessment)  Regulatory Entomology  Invasive Species Compound Eyes The principal organs of visual reception in most insects, consisting of individual functional units (ommatidia), each of which is marked externally by a facet. The number of ommatidia present in an eye varies greatly among taxa. Species with great visual acuity may have thousands of ommatidia per eye, whereas others with poor vision may have as few as a dozen ommatidia per eye. Compound 1017 1018 C Compsocidae eyes are very effective at detecting motion, but less suitable for discerning form. Color vision apparently in present in most insects, and polarization of light can be detected by some.  Head of Hexapods Compsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Compound Nest A nest containing more than one species of social insect. Although there may be intermingling by the adults, the broods are maintained separately. Comstock, John Henry Henry Comstock was born on a farm in Wisconsin on February 24, 1849. His father, in attempt to pay off the farm’s mortgage, decided to search for gold in California, but died of cholera on the journey, leaving his mother to support the family. She became ill after she moved with her son to New York in 1853, and John was first placed in an orphanage, then cared for by unsympathetic relatives, then taken in by a farming/sailing family. He became a cook on sailing ships on the Great Lakes to earn his living. In 1869 he entered Cornell University, and in summer 1870, after reading Thaddeus Harris’ book “Insects injurious to vegetation” he determined to become an entomologist. Unfortunately for him no course in entomology was being offered at Cornell University, so in summer 1872 he studied entomology at Harvard University with Hermann Hagen. After this brief introduction, he returned to Cornell University and there taught entomology while he was still a student. Until that time, he had supported himself by working as a laborer and at other part-time jobs. Now, he was paid as a lecturer. He continued his studies and graduated in 1874 with a B.S. degree, the only degree that he ever earned. He continued to lecture at Cornell University and in 1876 was appointed (Fig. 83) Assistant Professor of Entomology. In 1878 he married Anna Botsford, one of his students. But by then he had accepted and acted upon an invitation by Charles Riley to study Alabama argillacea, a pest of cotton, and the following year he became Chief Entomologist in the U.S. Department of Agriculture. In the winter of 1879–1880 he began studies of scale insects on citrus in Florida and continued them in California. He returned to Washington, was replaced as Chief Entomologist by Charles Riley, who reoccupied the position, then returned to academic life at Cornell University. His wife graduated from Cornell in 1885, and by then had taught herself wood-engraving, which she used with acclaim to illustrate her husband’s (1888) first part of his “An introduction to entomology” and other works. This was followed (1894) by “Manual for the study of insects,” a book which was so successful that the “Comstock Publishing Company” Comstock, John Henry, Figure 83 John Henry Comstock. Concealer Moths (Lepidoptera: Oecophoridae) was formed, and it continues to this day as a branch of Cornell University Press and outlet for major entomological works. Later works (1904) “How to know the butterflies” and (1912) “The spider book” followed. Anna Comstock’s “Handbook of nature study” was published in 1911 and her “Pet book” in 1914. His “Introduction to entomology” was published in full in 1920. He resigned from his university position in 1913 and died in 1931, surviving his wife by less than a year, having suffered a brain hemorrhage in 1926 and merely existing for the next 5 years. C Concealer Moths (Lepidoptera: Oecophoridae), Figure 84 Example of concealer moths (Oecophoridae), Alabonia geoffrella (Linneaus) from Italy. Reference *Mallis A (1971) John Henry Comstock and Anna Botsford Comstock. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 126–138 Concealer Moths (Lepidoptera: Oecophoridae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Concealer moths, family Oecophoridae, are a large family of about 7,550 described species from all faunal regions, with most species being from Australia; the actual fauna may well exceed 12,000 species worldwide. There are ten subfamilies recognized: Depressariinae, Ethmiinae, Peleopodinae, Autostichinae, Xyloryctinae, Stenomatinae, Oecophorinae, Hypertrophinae, Chimabachinae, and Deuterogoniinae. Many of the subfamilies have at various times been considered separate families (e.g., Ethmiinae, Stenomatinae, Xyloryctinae). Even some of the odd tribes of Oecophorinae have been considered separate families, such as the tribe Stathmopodini. The family is part of the superfamily Gelechioidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small to medium size (5–80 mm wingspan), with smooth head (rarely slightly roughened); haustellum scaled; maxillary palpi 3–4-segmented and folded over haustellum base (or reduced to one segment). Maculation varies from somber to very colorful and iridescent, and variously marked; venation (Fig. 84) usually complete (rarely reduced as in such narrow-winged groups as Stathmopodini). Adults mostly nocturnal but some are diurnal or crepuscular. Larvae include many leaf litter feeders, but also leaf tiers, leaf webbers, bark feeders, and a few leafminers, with a very diverse assemblage of biologies involved. Host plants include a large number of plant families, plus lichens, fungi, and detritus or leaf litter. Some groups are recorded more on some plants, such as Ethmiinae, which have many host records in Boraginaceae, and the Australian Hypertrophinae, which are mostly on Myrtaceae. References *Common IFB (1994–1997) Oecophorine genera of Australia. In: Monographs on Australian Lepidoptera 3:1–390 (1994); 5:1–407 (1997), CSIRO, Canberra *Gaede M (1938–1939) Oecophoridae. In: Lepidopterorum catalogus, 88, 92:1–476. W Junk, The Hague Gozmány L (2000) In: Microlepidoptera Palaearctica, Band 10: Holcopogonidae. Goecke & Evers, Keltern, 174 pp, 8 pl 1019 1020 C Conchaspididae Hodges RW (1974) Gelechioidea. Oecophoridae. In: Dominick RB (eds) The moths of America North of Mexico including Greenland, Fasc 6.2. EW Classey, London, 142 pp, 8 pl Powell JA (1973) A systematic monograph of New World ethmiid moths (Lepidoptera: Gelechioidea). Smithsonian Contrib Zool 120:1–302 Sattler K (1967) Ethmiidae. In: Amsel HG, Gregor F, Reisser H (eds) Microlepidoptera Palaearctica, vol 2. G Fromme, Vienna, 185 pp, 106 pl *Toll S (1964) Oecophoridae. In: Klucze do Oznaczania Owadów Polski. 27. Motyle – Lepidoptera, 35:1–174. Polskie Towardzystwo Entomologiczne [in Polish. Engl transl 1975. 176 pp. National Science Foundation, Washington] Conchaspididae A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs Conditional Lethal A mutation that may be lethal only under certain environmental conditions. Congeners Member of the same genus. Congo Floor Maggot, Auchmeromyia senegalensis (luteola) (Diptera: Calliphoridae) The larvae of this curious fly feed on the blood of humans and other mammals, though they do not infest the tissues. The normal hosts are warthogs, hyenas and other animals. Occasionally the females deposit eggs on the floor of huts and the larvae live within the earthen floor or in the bedding of primitive habitations in sub-Saharan Africa. The larvae become active at night, feeding on sleeping inhabitants. They repeatedly feed for periods of 15–20 min, and then retreat to their hiding places. Inhabitants can avoid this pest by sleeping above the floor, in beds or hammocks.  Myiasis Congener Conditioned Stimulus A stimulus that evokes a response that was previously elicited by an unconditioned stimulus. Condyle A process by means of which an appendage is articulated at the point of attachment, and particularly the point of articulation of the mandible and the head. Confused Flour Beetle, Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) This has several meanings, but generally means an organism belonging to the same genus as another organism. Congeners within the same geographical region tend to compete with one another so many adaptations can be observed that mitigate this pressure on populations. Congenic organisms are organisms with very similar genomes. Conidiophore A specialized hypha on which one or more conidia are produced. Conidium This important grain pest feeds on flour, but not on whole grain kernels.  Stored Grain and Flour Insects A sexual fungus spore formed at the end of a conidiophore. Conservation Biological Control Conifer Bark Beetles Members of the family Boridae (order Coleoptera).  Beetles Conifer Sawflies Some members of the family Diprionidae (order Hymenoptera, suborder Symphyta).  Wasps, Ants, Bees and Sawflies Coniopterygidae A family of insects in the order Neuroptera. They commonly are known as dustywings.  Lacewings, Antlions, Mantidflies Conjunctiva A membraneous infolded portion of the body wall (Fig. 85) that connects two segments. C Connexivum In Hemiptera, the junction of the dorsal and ventral abdominal plates, which is marked by a pronounced ridge. Conopidae A family of flies (order Diptera). They commonly are known as thick-headed flies.  Flies Conservation Biological Control kenneth w. mCCravy Western Illinois University, Macomb, IL, USA Conservation biological control is the implementation of practices that maintain and enhance the reproduction, survival, and efficacy of natural enemies (predators, parasitoids, and pathogens) of pests. Natural enemies are important in regulating populations of many agricultural and forest insect pests. Approaches to conservation of these natural Conjunctiva, Figure 85 Head and thorax of a grasshopper (Orthoptera). 1021 1022 C Conservation Biological Control enemies involve avoidance of practices harmful to them, as well as adoption of practices that benefit them. Like other animals, insect natural enemies require food, water, and shelter, and protection from adverse conditions. To achieve the goals of conservation biological control, fundamental knowledge of the biology and requirements of natural enemies is needed. Practices Detrimental to Natural Enemies Perhaps the most important rule of conservation biological control is the physician’s maxim, “first, do no harm.” Many insecticides can have both direct and indirect effects on natural enemies. Direct effects include acute or chronic mortality as a result of direct contact with pesticides. Direct sublethal effects, such as decreased adult fecundity, reduced viability of offspring, and changes in feeding habits or other behaviors can also occur. Indirect effects can result from mortality in populations of alternate prey or hosts of the natural enemies. Use of broad-spectrum insecticides that have detrimental effects on natural enemies can lead to rapid resurgence of targeted pest populations. In addition, secondary pest outbreaks (rapid increase to pest status of populations of non-target arthropods) can result if naturally occurring biological control of these secondary arthropods is disrupted. Use of more selective “biorational” insecticides, or insecticides with short residual activity, can be an effective strategy for conservation of biological control agents. Timing insecticide applications when natural enemies are absent or in life stages that are not susceptible to the insecticide can also aid in natural enemy conservation. Recent research involving development of pesticideresistant natural enemies holds promise as well. Conservation biological control also includes implementation of agricultural and silvicultural practices compatible with maintenance of natural enemy populations. Monoculture environments are highly advantageous to many herbivorous pests, but are usually very poor environments for natural enemies. Plowing, mowing, and harvesting operations, dust from these practices, burning of crop residues, and poorly timed irrigation practices can cause direct mortality of natural enemies. Of greater importance, however, is the habitat disruption associated with these practices. This disruption can create harsh conditions for natural enemies. Alternate hosts or prey, nectar and pollen sources, free water, and refugia are generally found in greater quantities in habitats with greater diversity of vegetation. Microclimatic conditions are generally more moderate as well. However, increasing reliance on intensive agriculture and forestry practices has tended to decrease habitat heterogeneity as well as genetic diversity of crops. Densities of parasitoids, as well as parasitism rates of pest species, have been found to be higher in mixed species habitats and in agricultural field edges near mixed species habitats. Avoidance or modification of cultural practices that disrupt natural enemy populations is an important strategy for maintaining natural enemy effectiveness. Practices that Enhance Natural Enemy Effectiveness Incorporating practices that are beneficial to natural enemies requires fundamental knowledge of natural enemy ecology and life history. These practices can be divided into two broad categories: (i) alternate foods or hosts of natural enemies, and (ii) shelter and refugia. Many predators and parasitoids require alternate food sources. For instance, certain ladybird beetles (Coccinellidae), which are important aphid predators, feed on plant pollen before switching to aphids. Many adult parasitoids require food in the form of pollen, nectar, or honeydew. Availability of such foods has been found to increase fecundity, longevity, survival, and effectiveness of many species. Availability of plant food sources may also increase the host searching efficiency of parasitoids, since degree of hunger can influence whether Conservation of Ground Beetles in Annual Crops the parasitoids spend more time searching for hosts or for food. Starved parasitoids have demonstrated greater attraction to flower odors over hostassociated odors. Maintenance of non-crop plants in or around agricultural fields or forest plantations can provide these foods, and also harbor alternate hosts or prey of natural enemies, helping to maintain natural enemy populations when pest populations are low. Provision of artificial supplementary food sources has also been shown to increase longevity of some agricultural and forest parasitoids in the laboratory and field. Natural enemies also require shelter from the elements. Artificial shelters have been found to increase winter survival of various peach orchard predators, allowing them to provide improved control of early season peach pests. Windbreaks and shelterbelts may increase searching efficiency and oviposition of parasitoids and predators adversely affected by high winds. Within-field and border refugia in the form of mixed species habitats can also increase the natural enemy: pest ratio by providing overwintering and aestivation sites. Conservation biological control is likely to increase in importance as agricultural and commercial forest systems become more intensively managed and restrictions on the use of conventional insecticides increase. It is an approach that requires integration of fundamental insect life history and natural enemy/pest interactions with knowledge of the ecology of the systems in which these interactions take place. This combination of factors makes conservation biological control research and implementation a challenging, but potentially rewarding, endeavor. References Barbosa P (ed) (1998) Conservation biological control. Academic Press, New York, NY, 396 pp Croft BA (1990) Arthropod biological control agents and pesticides. Wiley, New York, NY, 723 pp Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann Rev Entomol 45:175–201 C Pickett CH, Bugg RL (eds) (1998) Enhancing biological control: habitat management to promote natural enemies of agricultural pests. University of California Press, Berkeley, CA, 422 pp Conservation of Ground Beetles in Annual Crops faBián d. menaLLed, douGLas a. Landis USDA ARS National Soil Tilth Laboratory, Ames, IA, USA Michigan State University, East Lansing, MI, USA Ground beetles (Coleoptera: Carabidae) are an important and diverse group of ground-dwelling insects with over 2,500 species known from North America alone, and more than 40,000 known species worldwide. They occur in many habitats including forests, riparian areas, grasslands, orchards, and crop fields. As immatures, carabid beetle larvae usually live in litter or the upper soil layers and have ten well-defined body segments tapering towards their posterior end. Adult beetles are primarily nocturnal, with a body size ranging from a few millimeters up to 3–4 cm. Adult beetles have relatively long legs and are black or dark reddish, although several species are colored. Adult and larva beetles feed on insects, snails, slugs, and weed seeds. Because of their voracious feeding behavior and their abundance in agricultural settings, carabid beetles are considered important biological control agents with the potential of restricting the abundance of many pest species. Among the different pests carabid beetles are known to consume are: black cutworms, Agrotis ipsilon Rottemburg; gypsy moth, Lymantria dispar (Linné); cabbage maggot, Delia radicum (Linné); armyworm, Pseudaletia unipuncta (Haworth); European corn borer, Ostrinia nubilalis (Hübner); western corn rootworms, Diabrotica virgifera virgifera LeConte; and many aphid species. Several species of ground beetles are omnivorous, consuming not only insects, but also seeds of common agricultural weeds such as giant 1023 1024 C Conservation of Ground Beetles in Annual Crops foxtail (Setaria faberi Herm.), velvetleaf (Abutilon theophrasti Medicus), redroot pigweed (Amaranthus retroflexsus L.), and common lambsquarters (Chenopodium album L.). Due to the potential of ground beetles as biological control agents, their biology and ecology have been widely studied. However, ground beetles are not commercially available for augmentation and several studies have demonstrated that common agricultural practices such as tillage, pesticide applications, and harvest reduce ground beetle abundance and alter carabid beetle community characteristics. As a result, pest control by predatory ground beetles in conventionally managed annual crop fields is usually diminished. Moreover, the current tendency of increasing agricultural landscape simplification, where farmers manage large monocultures with high mechanical and chemical inputs, increases the impact of management practices on carabid beetle survivorship. In row crop systems, to fully exploit the potential of ground beetles as biological control agents, it is necessary to generate an environment that allows their survivorship and reproduction. Habitat management represents a viable approach to reduce the negative impact that several agricultural management practices have ground beetles. Habitat management is defined as a series of practices aimed to alter habitats to improve availability of resources required by natural enemies for optimal performance. Several habitat management practices have been shown to encourage carabid populations, including no-tillage or conservation tillage practices, cover crops, and maintenance of refuge habitats in close spatial association with crop fields. The goal of these practices is to provide ground beetles with the ecological infrastructure necessary for their survivorship and reproduction. Several studies have evaluated the impact of tillage on ground beetle abundance and diversity. In general, lower number of individuals are found in conventional tillage than in no-tillage or reduced tillage systems. This could be due to either a direct mortality inflicted by soil disturbance, or the indirect effect caused by removal of resources and food. The impact that tillage has on carabid beetles depends on the species, but it has been found that species diversity and evenness tends to increase in reduced tillage fields when compared to conventionally tilled ones. Cover crops have also been shown to be a suitable habitat management practice to enhance ground beetle abundance. Cover crops are crops not grown for harvest, but rather for other benefits they provide, including protection from soil erosion, improving soil structure, supplying soil nutrients, suppression of weed germination and weed growth, and contribution to management of insect pests and plant pathogens. From an insect’s point of view, cover crops can increase humidity, reduce temperature, and serve as a host for alternate prey species. In total, cover crops often provide a favorable habitat for generalist predators such as carabid beetles. However, it is important to note that the increase in surface plant material occurring in cover crop systems may be responsible for a decrease in carabid beetle mobility. Due to the ephemeral characteristics of annual crop systems, it is critical to assure the overwinter survivorship of ground beetles. Providing refuge habitats in close association with crop fields has been shown to be a promising approach to conserving ground beetles. Examples of refuge habitats include non-crop sites such as woodlands, hedgerows, riparian buffers, cross wind trap strips, perennial pastures, and grassy strips. Crop field edges not sprayed with pesticides can also act as refuge habitats for carabid beetles. Refuge habitats benefit carabid beetles through several mechanisms. First, refuge habitats provide suitable overwintering sites for carabid larvae and adults. Several studies have shown that the density and diversity of overwintering carabids is higher in refuge strips than in adjacent crop fields. Possible mechanisms for these differences include a differential mortality and/or a preferential selection of habitat. Second, refuge habitats act as a stable resource of food such as aphids and springtails. Conservation of Insects This is particularly important early in the growing season when prey have not colonized crop fields and has been observed to correlate with an increase in the weight and reproductive output of female carabid beetles. Third, refuge strips provide favorable microclimates during hostile weather conditions such as high temperature and low humidity. Finally, refuge habitats protect carabid beetles from disruptive management practices. If pesticide applications, cultivation, or harvest damage carabid populations, refuge habitats can serve as sources of natural enemies that colonize agricultural fields, inflict mortality on pests, and return to refuges. A common denominator among all habitat management practices aimed at conserving carabid beetles in row-crops is an increase in the planned biodiversity (organisms purposely included in the agroecosystem by the farmer) and the associated biodiversity (all soil flora and fauna, herbivores, carnivores, etc. that colonize the crop fields (Fig. 86) but are not intentionally established by farmers). However, it is not increasing diversity per se the final objective of habitat management. A key component is to identify the C elements of diversity that enhance ecological services necessary to secure the establishment, survivorship, and reproduction of this diverse group of beneficial organisms. This knowledge should be combined with an understanding of the spatial scale over which habitat management operates (within-field, farm-level, agricultural landscape), any potential negative aspect associated with the addition of new plants into the systems (i.e., increasing the risk of pest outbreak or weed invasion), and the associated economic costs and benefits. References Desnder K, Dufrene M, Loureau M, Luff ML, Maelfait JP (1994) Carabid beetles: ecology and evolution. Kluwer Academic Publishers, Dordrecht, The Netherlands Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pest in agriculture. Ann Rev Entomol 45:175–201 Lee JC, Menalled F, Landis D (2001) Refuge habitats modify impact of insecticide disturbance on carabid beetle communities. J Appl Ecol 28:472–483 Lovei GL, Sunderland KD (1996) The ecology and behavior of ground beetles. Ann Rev Entomol 41:231–256 Stork NE (1990) The role of ground beetles in ecological and environmental studies. Intercept, Andover, UK Conservation of Insects andrei sourakov, thomas C. emmeL University of Florida, Gainesville, FL, USA Conservation of Ground Beetles in Annual Crops, Figure 86 Anisodactylus sanctaecrusis (F.), a ground beetle commonly found in agricultural fields (Drawing by S. Kudrom). Insect conservation is a relatively new concept. Traditionally, invertebrates are the lowest priority for conservation organizations due to their relative inconspicuousness to the public eye and the lack of showy charismatic flagship species among the large invertebrate numbers. Even our most basic scientific knowledge of insects is relatively poor. Some taxonomists estimate that there are more than four million insect species alone, but other entomologists believe the number could be as high as 50 million. Of these insect 1025 1026 C Conservation of Insects species, only 5–10% have scientific names. Even for described and well known species, the information on their biology and population dynamics is scarce, which makes it harder to determine their conservation status. There is also a misconception among the general public that a good bug is a dead one, which makes it more difficult to obtain public money for insect conservation projects. At the same time, the roles that the insects play in our lives can hardly be overestimated. They are responsible for reproduction of most plants, and are essential food sources for many vertebrates from fish to birds and even mammals. Though most pest species indeed belong to the Insecta, there also are many insect species that keep pests under control through predation and parasitism. Though we consider conservation of the pollinators and of the natural enemies to be as essential as conservation of endangered insect species, here we discuss only conservation of endangered and threatened species, and focus on the diurnal Lepidoptera as an example of the problems and opportunities inherent in the overall field of insect conservation. Cites The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) was signed in 1973 and entered into force in 1975. The treaty now has 152 Parties. CITES species are listed in Appendices according to their conservation status. In addition, listed species must meet the test that trade is at least in part contributing to their decline. CITES regulates international trade in species of animals and plants according to their conservation status. Appendix I species are species in danger of extinction, for which all commercial trade is prohibited. Appendix II species are not necessarily threatened with extinction, but may become so unless trade is strictly regulated. These include species that are in international trade and are vulnerable to overexploitation. Regulated trade is allowed provided that the exporting country issue a permit that includes a finding that the trade will not be detrimental to the survival of the species or its role in the ecosystem. This regulation includes a requirement for documentation from the country of export, monitoring of imports and, in some cases, export quotas. Appendix III. A country may unilaterally (without a vote) list in Appendix III any species which is subject to regulation within its jurisdiction for which the cooperation of other Parties is needed. Importing countries must check for export permits for the species issued by the country of origin for Appendix III species. The Importance of Subspecies The U.S. Endangered Species Act is written to allow the preservation of any recognized unique taxonomic entity, subspecies included. Indeed, preserving a subspecies is as important as conservation of a species as a whole. Not only do subspecies frequently turn out to be separate species with thorough study, but most insect populations thrive on the gene flow that occurs between populations in the intergrade zones and through migration. Unique morphological characteristics of subspecies reflect the genetic diversity that allows species to survive. These morphological features are often linked with various ecological and physiological characteristics. Many local populations go extinct at one time or another, and such extinction events are becoming more and more frequent with shrinking of the average population size. Occasional repopulating from an extant neighboring population is therefore required for long-term survival of most populations. It is not enough to conserve a species in a single locality, but in as many localities as possible, connected by corridors of habitat. A distribution range containing as wide variability as possible should ideally be designated Conservation of Insects in a successful conservation effort. Subspecies, under current legislation, play an instrumental role in achieving these goals. Butterflies as an Index Group in Conservation Despite the large numbers of insects that have been placed on various lists of threatened or endangered species, and even larger numbers that have already become extinct or are on the verge of extinction, by far the most interest and funding have been attracted by the butterflies. The latter group accounts for only 20,000 species, or half a percent of the total insect diversity, but there are probably more books written on that group than on the rest of the insects combined. This popularity, the result of butterflies’ esthetic appeal, is also responsible for the amount of knowledge on them that has been accumulated since the time of Linnaeus, mostly by amateur naturalists. The last two decades have seen publication of books on the butterfly fauna of nearly every country of the world, and there also are numerous books that cover worldwide faunas of particular groups or different aspects of butterfly biology. These works, combined with the efforts of hundreds of regional butterfly-enthusiast organizations, provide a significant framework for conservation. We should note that this knowledge is far from complete, as life histories and survival requirements are still not understood for the majority of species. As with many conservation movements, the conservation of butterflies takes many, sometimes contradictory forms. For instance, some ill-informed people, driven by good intentions focus their efforts almost entirely on prohibition of collecting. Collecting, however, has been repeatedly demonstrated to play no important role in endangering butterfly populations. Indeed, quite the opposite is true: collecting is instrumental in acquiring scientific information, as well as in attracting new people into the movement for C butterfly conservation. By far outweighing all other factors that threaten butterflies (or any other species) are those of habitat degradation and pollution, in that order. The highest diversity of insects on the planet is found in the Amazonian rainforest, the equatorial area which has had no recent major cataclysms such as glaciation leading to mass extinction. Lesser, but nevertheless impressive, diversity of insects is found in the tropical forests of West Africa, Asia, and New Guinea. Despite the rapid disappearance of these forests, these are not the habitats that contain most of the species placed on the “endangered” lists. Instead, that dubious distinction falls to the temperate zones. Here, conservation efforts are much more extensive in the developed countries, such as United States, Japan, and the countries of Western Europe, where ecological awareness and general education level are higher. This creates a misleading impression, as most of the potentially threatened or truly endangered species actually occur in the developing tropical countries. Another peculiar phenomenon is that many species are given preference in being declared endangered because of the demand they attract from collectors. Normally, these are the larger and more attractive species. Even when these species are in decline, this decline is caused by loss of habitat, and has little to do with collecting. Habitat, at least in the developing countries, often is not provided protection from such legislation. The focus on collecting occurs mostly because people who create insect conservation legislation are general wildlife biologists, whose primary focus as well as education and training are in the area of large vertebrate animals. Wildlife biologists tend to extrapolate their experiences with large vertebrates to insect conservation. Thus, they don’ t take into account that even the smallest insect population consists of thousands of individuals, and that most insects reproduce with large numbers of eggs from a single female, and have very high biotic potentials. 1027 1028 C Conservation of Insects The population numbers can naturally vary tremendously from year to year, which is also rarely taken into account by those monitoring them. The threat from collectors seems obvious to vertebrate wildlife biologists because it is parallel to their experience with hunters and game animals. However, it is sometimes enough to just mow a meadow or burn the grass in it to destroy the whole insect population consisting of thousands of individuals: a task that could never be even deliberately accomplished by a dozen collectors. Nevertheless, over- collecting in rare populations that are already greatly diminished in size by habitat degradation could be a problem, and no commercial collecting should be allowed in such localities. Even in the tropics, some habitats are more threatened and contain more endangered species than others. Mountain chains and the islands create the conditions of isolation that are often responsible for new species formation. Mountains also support a wide variety of unique habitats associated with elevation change, with correspondingly unique or specialized and highly localized species of plants and animals inhabiting them. In the tropics, these habitats are often claimed for settlements and agriculture because they have much more favorable climatic and soil conditions than the lowlands. Reforestation in such areas, when it occurs, often is conducted with exotic fast-growing tree species, such as temperate pines and Australian eucalyptus, which only contributes to exotic replacement and extinction of the native insect species. The fauna of tropical islands, such as those of Oceania, the Antilles or Madagascar, are composed of mostly endemic species. Some of the most threatened insect species are found on these islands, where overpopulation of humans often leads to deforestation and erosion. Even in the areas where population densities are low, the demand for cheap timber that can be easily hauled away by sea, as well as weakness of environmental laws and governmental corruption, lead to deforestation and extinction. Case Studies of Four Endangered Swallowtail Butterflies (Papilionidae) from Different World Regions Ornithoptera alexandrae, New Guinea, and other birdwing butterflies The first specimen of the Queen Alexandra’s birdwing, Ornithoptera alexandrae (Fig. 87), the largest butterfly in the world, was discovered in New Guinea at the turn of the century. Recognizing it was something new, but always flying high and out of reach, the collector, A. S. Meek, had to fire a shotgun blast at the insect to bring it down in 1906. Today, the butterfly persists only in small patches of primary forest left around Popondetta. Population surveys of this species are difficult, as adults fly in the canopy. It is extremely local and its distribution even before recent habitat destruction was apparently restricted, perhaps by host specificity of the species, which feeds on three related Aristolochiaceae vine species: Aristolochia dielsiana, Paraaristolochia alexandriana and P. meridionaliana. Ornithoptera alexandrae has had the legal status of Endangered since 1967 in Papua New Guinea, and is listed as a CITES Appendix I species. As a result, ironically, it does not enjoy the protection of habitat that accrues to other Ornithoptera species from local people who could be ranching it for sale to collectors, if it were not so listed. (Papua New Guinea and Australia are now jointly planning a ranching project, which may require re-listing it to Appendix II status.) In addition, restoration of the rainforest habitat that was lost to oil-palm plantations and volcanic devastation (in 1951) is underway, and eventually O. alexandrae might see removal of present restrictions on its commercial propagation and marketing. Several other species of that colorful butterfly genus, as well as many other insects of New Guinea, are already raised for sale. This activity is under the centralized control of IFTA (Insect Farming Conservation of Insects C Convervation of Insects, Figure 87 Adult of Queen Victoria’s birdwing, Ornithoptera victoriae (photo by Andrei Sourakov). and Trading Agency) at the town of Bulolo. The individual ranching incomes from this activity, though low by the standards of the western countries, often exceed the national income average by ten-fold. This fact provides strong incentive for planting host plants and preserving habitat for the species being ranched. Ranching requires very little effort and no initial investment. Wild female butterflies from the surrounding forest lay eggs on their respective host plants. Most birdwing species, for example, feed on the widespread pipe vine, Aristolochia tagala, which readily grows in small farm plots. Caterpillars are allowed to feed and pupate freely, while pupae are collected and brought inside a hut. No cages are used to hold the emerged butterflies or to keep ants and parasitic wasps away because ranchers usually do not have money to buy these much-needed supplies. Instead, they wait for a pupa to turn dark, and then watch it closely until the butterfly emerges. Then it is killed and papered for sale to IFTA, and further commercial distribution abroad. Following the example of Papua New Guinea, other countries in the region have established similar programs with different degrees of success. For example, two birdwing species are found exclusively on the Solomon Islands. Smaller than O. alexandrae, they are nevertheless among the world’s largest and most beautiful butterflies. Males are valued by collectors for their dazzling coloration, females for their immense size. Queen Victoria’s birdwing, Ornithoptera victoriae, displays different shades of brilliant green, while the wings of d’ Urville’s birdwing, Ornithoptera priamus urvillianus (Fig. 88), are sky-blue. The females are colored inconspicuously brown and are slow fliers that mostly stay inside the forest. In the Solomons, butterfly specimens are sold to a middleman in Honiara, who accumulates a sufficient number of butterflies to fill an order from a Western dealer. Ranchers receive a fraction of what a butterfly will be actually sold for in the developed world. With more coordination brought into the program, perhaps by the Solomon Islands Development Trust organization, some middlemen could be bypassed, and the ranching would become more economically important to the farmers. Now that local people have been introduced to ranching, which is a much more efficient way of acquiring 1029 1030 C Conservation of Insects Conservation of Insects, Figure 88 Adult of d’ Urville’s birdwing, Ornithoptera priamus urvillianus (photo by Andrei Sourakov). high-quality specimens than collecting, the trade (and thus conservation effort) is being hampered by the fact that these birdwings are presently prevented from normal trade in the largest potential market in the U.S. by a desire of some CITES officials there to punish the Solomon Islands government “for not doing enough for conservation.” The environmental threat to birdwing survival comes from the destruction of their forest habitat through logging and slash-and-burn agriculture, activities which disregard the presence of endangered butterflies and for which there is no punishment because the local people own the land and can develop it as they wish. Without the economic impetus to preserve these forests for butterfly ranching and other sustainable activities, there is no local incentive to resist the lucrative logging concessions requested by foreign timber companies. Thus, outside political pressure in the form of a unilateral U.S. trade embargo, which is not endorsed by other CITES nations, is having an anti-conservation outcome and inhibiting insect conservation measures undertaken in the Solomon Islands. Homerus swallowtail, Papilio homerus, Jamaica This is the largest swallowtail in the Americas. Once it inhabited seven of the thirteen parishes of the island of Jamaica in the West Indies, but now it is found only in St. Thomas and Portland parishes at the junction of the Blue Mountains and the John Crow Range. In the late 1930s, P. homerus butterflies (Fig. 89) were relatively common. By 1945, the species was rapidly disappearing from its larger stronghold in the eastern Blue Mountains. It is now one of four endangered swallowtail species listed in the IUCN Red Data Book “Threatened Swallowtail Butterflies of the World.” The rugged Blue Mountains run approximately one-third the length of the island. The climate is uneven throughout the island. For instance, the northern parish of Portland receives heavy rainfall of 381 cm, while the south is much drier (89 cm). Papilio homerus larvae require humidity to be close to 100% to survive. Thus, the species only inhabits wet limestone forest at the western end of Jamaica, and lower montane rain forest at Conservation of Insects C Conservation of Insects, Figure 89 Adult of Homerus swallowtail, Papilio homerus (photo by Thomas C. Emmel). the eastern end. The first area is characterized by trees such as Jamaican cedar, prickly yellow and figs. Secondary succession areas frequently have bracken ferns and citrus trees. The second area supports mountain guava, Santa Maria, cobywood, roadwood and tree ferns. Papilio homerus normally occur below an elevation of 1,000 m. Hernandia catalpifolia, locally known as water mahoe or water wood, and H. jamaicensis (pumpkin wood, suck axe) are the larval host plants, in the family Hernandiaceae. Ocotea nr. leucoxylon (loblolly sweetwood in the Lauraceae) may also be used by larvae. Forest reserve areas were established in these mountains, including prohibition of cutting trees. However, FIDCO (Forest Industries Development Company), formed by the Jamaican government in 1979, began cutting 2,000 hectares of rainforest per year to plant Caribbean Pine to help the charcoal production industry. With the rapid disappearance of the wet streamside rain forests, this activity presented the major threat to P. homerus survival. In 1984 the film “Papilio homerus, the vanishing swallowtail,” was produced. This film and other similar publicity efforts over the potential national symbol represented by this rare flagship species, have created a positive movement of preservation, culminating in the establishment of Blue and John Crow Mountains National Park in 1991, with Papilio homerus as the official symbol of the Park Service. Subsequent educational efforts have continued annually in Jamaica’s elementary schools, with written materials on the butterfly’s life history and the manifold importance of the montane rain forest habitat to watershed protection, wildlife, recreation, and tourism-based economic benefits. After Hurricane Gilbert destroyed most of the planted Caribbean Pines at the end of the 1980s, the establishment of the montane rain forest park has allowed natural succession to begin reclaiming these areas. Fortuitously, Hernandia species are among the foremost recolonizing rain forest trees, rapidly increasing the potential habitat for the Homerus Swallowtail. 1031 1032 C Conservation of Insects Parnassius apollo, Europe This is the first butterfly species that was placed on the CITES list for prevention of trade. While numerous cases of local extinction are known for the species throughout Europe, none of them has been linked to collecting. Acid rains were blamed for its demise in the 1970s in Germany and the Alps, while around Moscow the mass spraying for gypsy moth might be a key factor for its disappearance. Everywhere, habitat loss is also a significant factor. In our view, one of the weaknesses of the current conservation legislation concerning P. apollo (Fig. 90) (as well as of all other endangered butterfly species) is that it targets the species rather than the habitat. Additionally, this legislation recognizes all subspecies of P. apollo as endangered, despite the fact that many of them, particularly in Central Asia mountain ranges, are very common. Some captive breeding and reintroduction programs for the endangered European subspecies are being developed locally. Schaus’ Swallowtail, Heraclides aristodemus ponceanus Schaus, Florida The Schaus’ swallowtail is the resident H. aristodemus subspecies that is found in South Florida and the Florida Keys. An assortment of other distinct subspecies is found on some of the Bahamian and Caribbean islands. Only a few of the Keys have suitable hardwood hammock habitat today, and even fewer support the Schaus butterflies. This is one of the cases where pollution by mosquito control practices has evidently contributed significantly to the demise of the species. Were it not for this impact since 1972, the population (though impaired by the loss of habitat) would be substantially above present precarious levels. The adult butterflies (Fig. 91) emerge from their pupae after the first rains in May, following a long dry season. The major population is that on Elliott Key, an isolated, seven-mile-long and quarter-mile-wide island, where there are no recent human developments or mosquito control practices. The annual number of adults flying there has usually hovered at several hundred to as many as a thousand, though it varies from summer to summer. Schaus’ swallowtail was once widespread throughout south Florida, but its population size and distribution have been reduced by the growth of Miami and urbanization of the Keys, and, later, by the spraying of Dibrom and Baytex pesticides. Prior to the development of the area, butterflies migrated freely around the northern Keys and mainland. Capture/recapture data shows individuals fly as much as 3.5 miles within a few hours. This movement supported the genetic diversity of each of the smaller populations, and ensured population of new sites and natural repopulation of those suffering a temporary extinction. Today, Elliott Key has the only large population of the butterfly, and the area is currently protected as a part of Biscayne National Park. When Schaus’ swallowtail was recognized as an endangered species by the U. S. Fish and Wildlife Service in 1984, a research group from the University of Florida began looking for ways to secure its future. Although now protected, the Schaus’ swallowtail, even on Elliott Key, remains at risk. The small size of this sanctuary, and the absence of secure populations outside it, make the Elliott population vulnerable. Should it be wiped out by an ecological disaster, there would be no natural source of Schaus’ swallowtails to repopulate the islands. Schaus’ swallowtail shares Elliott Key with two similar-looking swallowtails: the Bahama swallowtail, Heraclides andraemon bonhotei, apparently a very low-level resident population or an occasional visitor, and the Giant swallowtail, H. cresphontes, which forms a persistent but smaller resident population. The Giant swallowtail flies synchronously with Schaus’, but can easily be identified by its larger size and more powerful flight. Schaus’ swallowtails usually have slow fluttering flight to maneuver through the dense jungle of tropical hardwood hammock while avoiding lethal spider webs. It is Conservation of Insects C Conservation of Insects, Figure 90 Adult of Parnassius apollo (photo by Alexander Dantchenko). not uncommon to see a Schaus’ even “backing up,” a rarity among butterflies. While giant swallowtail larvae would feed on any citrus (Rutaceae) tree, Schaus’ larvae can complete development only on wild lime (Zanthoxylem fagara) and torchwood (Amyris elimifera). Females especially prize the latter for Therefore, Schaus’ require these host plants and the thick hardwood hammock, which provides a relatively cool, shady microclimate in the hot Keys. When Hurricane Andrew hit south Florida in August 1992, the hammock on Elliott Key was devastated: no canopy was left to protect the delicate undergrowth of torchwood and wild lime 1033 1034 C Conservation of Insects Conservation of Insects, Figure 91 Adult of Schaus’ swallowtail, Heraclides aristodemus ponceanus (photo by Andrei Sourakov). from the desiccating rays of the sun. Elliott Key’s wild Schaus’ population survived Hurricane Andrew in very low numbers (only 17 in 1993), and was later buttressed by releases of captively reared individuals. Fortuitously, 100 wild Schaus’ eggs had been removed to establish a captive colony at the University of Florida just 2 months before the hurricane. This colony was expanded to produce several thousands of Schaus’ swallowtails that were then released back in the wild at a series of sites on the south Florida mainland and the Florida Keys in 1995, 1996, and 1997. Capture-recapture data showed (Fig. 91) recovery to about 1,200 adults flying in 1996 and 1997. However, the possible genetic bottleneck that the population went through during the immediate post-hurricane years could cause serious problems for the population in the future. Additionally, a 5-year drought (1998–2002) in South Florida reduced the Schaus populations to, at most, 200 adults by mid 2002. In captivity a female can live up to 32 days and lay up to 430 eggs; in nature, she lays at most 80 eggs before dying at an average age of 3.6 days. Most of the eggs in nature are eaten by predators such as ants, or parasitized by wasps. Thus, captive propagation can work well with this species. The females can easily be hand-paired, and lay eggs on either torchwood or wild lime. The young larvae are raised in vials with fresh torchwood leaves, and later can be placed on potted trees. At maturity they are transferred back into individual plastic cups, in which the larvae pupate. Then, either pupae or emergent adults are released into the wild at suitable sites. Future studies will tell whether the 13 wild populations that were established after Hurricane Andrew through this captive propagation program are viable. In addition to monitoring the success of the introductions, there is a need for continuing the search for remnants of suitable, reintroduction-worthy habitat. The program’s survival greatly depends on funding, which has so far been provided by the U.S. Fish and Wildlife Service and private donations.  Endangered Species Construction Behavior of Insects References Collins M, Morris MG (1985) Threatened swallowtail butterflies of the world. The IUCN red data book. IUCN, Cambridge, UK, 401 pp New TR (ed) (1993) Conservation biology of Lycaenidae (Butterflies). IUCN, Gland, Switzerland, 173 pp New TR (1997) Butterfly conservation. Oxford University Press, Oxford, UK, 248 pp Samways MJ (1994) Insect conservation biology. Chapman & Hall, London, UK, 358 pp Conspecific Organisms belonging to the same species. Construction Behavior of Insects hoLLy downinG Black Hills State University, Spearfish, SD, USA One of the most complex and exciting areas of insect biology is that of nest architecture and construction behavior. There are four major groups of insects that are well-recognized builders, while there are individual species in other groups that also build structures. The four major groups of builders are the Isoptera (termites),the Hymenoptera (ants, bees and wasps), the Lepidoptera (butterflies and moths, though only moths build), and the Trichoptera (caddisflies). The moths and caddisflies build individual cases, cocoons, or group retreats, but the termites, ants, social bees and social wasps build the most elaborate structures. Some nests are enormous relative to the size of the builders (several miles high if the height is made proportional to human dimensions), able to maintain nearly constant temperature and humidity, and able to withstand years of harsh sun and driving tropical rains. Small insect groups that build, or with only a few building species, include the Diptera (flies), Embioptera (webspinners), Orthoptera (grasshoppers, crickets), Hemiptera (cicadas, hoppers), Neuroptera (lacewings, antlions, mantispids), and Coleoptera (beetles). C Types of Structure and Nest Architecture Of the many different types of structures built by insects, some of the simplest structures are the bubble nests of the froghoppers (Hemiptera). Bubble nests function in anti-predator defense and water conservation and are produced by frothing up secretions of the Malpighian tubules into a tight bubble mound around the builder. Another very simple form is the cocoon built by a moth caterpillar preparing for pupation. The larva finds a spot for this transitional stage to take place and begins the process of building the cocoon. The larva has large salivary or labial glands that produce a remarkable material called silk. This complex protein is drawn from the glands forming a durable and water resistant thread. The larva touches the substrate and attaches the end of the silk to one side and then draws out a length of silk in an arch and attaches the silk to the substrate on the other side of its body. Repeatedly attaching and looping over itself, the larva creates a covering that will protect and attach the denser cocoon pouch on the inside. Once the outer layer is in place, the larva will spin silk around and around itself to create the protective cocoon. In a cocoon of the silkworm moth, the length of the single thread is 500–1,300 m long. Silk material is made from the threads that are unwound from these cocoons. The cocoons are soaked in hot water and the loose outer thread is caught on a turning spool. The cocoon unwinds as one very long silk thread. Multiple strands are collected at the same time and combined to create a remarkably strong thread that can then be dyed and woven into a beautiful cloth. The larvae of other moth groups, such as the bagworms and the case making clothes moths, build individual silk cases with fragments of their food material or vegetation incorporated in the walls. The case is dragged around, serving to protect the larva as it feeds, and is spun closed during pupation. Other Lepidoptera species, including some tent caterpillars, lay their eggs in clusters. When 1035 1036 C Construction Behavior of Insects the larvae hatch, they work together to spin a common retreat. The silk in the walls of the retreat is so tightly layered that it takes on an almost leather-like appearance and texture. Some individuals are more active foragers and lay down silken trails to foraging locations, which the others follow. During the day, they return to the safety of the multi-layered retreat that protects them from predators and dampens temperature and humidity fluctuations. The Embioptera or webspinners are members of a small order of insects, but unique in that they use silk from tarsal glands in their front legs to spin silken passageways. Groups of individuals live together in what becomes a network of galleries. The caddisfly larva is the immature form of the Trichoptera. This insect group is closely related to the butterflies and moths, but it has little hairs instead of scales on its wings. Although the adult is a terrestrial insect, its immature larva is aquatic, living in streams among the rocks and vegetation at the bottom. As in the Lepidoptera, this group builds using silk produced by the salivary or labial glands. The caddisfly larvae build a variety of structures, depending on the species. Some build a silken web, which they use in straining food from the water flowing around them. Others build retreats by attaching small pebbles (Fig. 92) or plant material to silk in a case surrounding their body. As they grow, they add more building material on the front lip of the case, always keeping it just large enough to draw back into for safety, but small enough to drag around. The type of material and the form that the case takes is species-specific, so the characteristics of the case can help in identifying the animal that made it. Studies have shown that the larvae are very careful in their selection of building material, turning each item around repeatedly before rejecting or accepting it. If accepted, the item is then carefully oriented and glued with silk into position. Macronema transversum is a species of caddisfly that builds a more elaborate, curved case. This U-shaped case, which has an incurrent funnel facing upstream and a smaller excurrent funnel immediately downstream, not only provides a safe retreat, but also is used to support a web spun across the interior chamber and to filter food particles from the water. There are some insects that use the leaves of plants to create safe feeding locations for their developing brood. The females of a group of leafrolling weevils (Coleoptera) first use the mandibles at the end of a long proboscis to chew into the leaf petiole just at the base of the leaf. The female then moves out on the leaf and begins to break open the epidermal layer with tarsal claws and mouthparts until the leaf begins to curl with loss of turgor pressure. The female then aligns herself with the edge of the leaf and using the legs on one side, pulls the leaf edge over to begin the tight curl. The leaf is rolled to completion and glued tight with anal secretion. During the construction of the curl, the female enters the curl and lays an egg through a slit she makes in the inner layer. Thus, multiple leaf layers protect the egg, and when it hatches, the larva has a secure feeding spot. Construction Behavior of Insects, Figure 92 Caddisfly case built of small pebbles and silk by the larva. They are found in streams and other bodies of flowing water. Construction Behavior of Insects Many different types of animals, both vertebrate and invertebrate, build burrows, insects included. These burrows may be simple, consisting of a tube dug into the ground with a single chamber, or they may be quite complex in structure. Regardless of complexity, the burrows may serve a variety of functions including predator avoidance, brood rearing, feeding and vocalization enhancement. Immature cicadas, members of the order Hemiptera, live in burrows. The length of the nymphal stage varies with the species, but may extend as long as 17 years. During that time, they live underground and feed on roots accessed from their burrows. Some members of the order Orthoptera build burrows, but none more elaborate than that of the mole cricket, Gryllotalpa vineae. The male of this species builds a burrow with two adjacent, horn-shaped entrances. The double-barreled burrow curves downward where the two entrances join in a single, somewhat enlarged passage leading to the deeper blind retreat. The male calls from the enlarged passage while facing away from the entrance. He rubs his forewings producing a loud call, which is greatly amplified by the burrow design and can be heard by a person more than 400 m away. The call frequency with maximum energy is 3–4 kHz, while the call can reach over 100 dB at approximately a half meter above the burrow. The antlions of the order Neuroptera build prey-capturing traps in sandy soil, which at times can be spotted along hiking trails. The larva has large mandibulate mouthparts and builds its coneshaped pit by throwing sand up and out of the hole with its flat head and mandibles. It buries itself at the bottom of the pit and lies in wait for an unsuspecting ant or other small insect to slide down the side of the pit. By tossing sand up the edge of the pit, the antlion creates a mini-avalanche that causes the struggling prey to slide further down the side of the pit, whereupon it is bitten and sucked dry. There is a group of flies, the worm-lion, Vermileo comstocki, that also builds a similar trap to catch prey. C Those that build underground burrows to protect immature offspring are members of the Orthoptera, Coleoptera and Hymenoptera. Parental care may exist in the form of guarding the burrow, or provisioning the young. In the dung beetles, male and female pairs dig out a burrow and then pack the end of it with a ball of fresh dung (some collect the dung first, tap it into a ball and push it with the hind legs to a desirable location where they then cover it with dirt). An egg is laid on the ball of dung, or the ball may be subdivided a number of times and eggs laid on each of the balls. In some species, there is little parental care, while in others, the burrow is defended and the dung ball is kept from desiccating and molding. After hatching from the eggs, the young feed on the dung within the protective environment of the burrow. Burrow construction is most elaborate among the ants, bees and wasps. In some wasps and bees, multiple chambers are built either singly or in clusters off the main tube, or off branching tubes. Each chamber or cell houses one developing larva that feeds on food provisioned within the sealed cell. Some species, like Paralastor sp., build a mud tube elaboration on the burrow entrance that helps prevent parasitoids and predators from entering during the construction and provisioning of cells. In the stingless bees, the nest entrance has wax added to form a chamber for guard bees and a landing platform for returning foragers. The large nest chamber houses wax cells where the brood is reared and the reserves of honey and pollen are stored. In these insects, the honey and pollen are fed to the young and they are progressively provisioned. Tubes leading deeper into the ground provide space for water drainage and garbage disposal. One group of amazing underground builders is the leaf cutter ants, of the tribe Attini. The colonies of these extraordinary ants start with the founding queen who has been fertilized prior to sequestering herself in a newly formed blind burrow. She takes a small amount of fungus from her parental nest, plants it with a bit of her anal secretion, and carefully tends this small fungal 1037 1038 C Construction Behavior of Insects garden. She lays a few eggs, which are destined to become the first workers for the colony. From this obscure beginning, the colony grows until it has a fully formed caste system with sterile workers and soldiers numbering in the millions. Separate chambers are built to grow fungal gardens and rear brood. These ants forage for leaves, which they bring back to the colony along cleared paths. They attach the leaves to the fungal garden, sometimes using small amounts of anal fluid. Mycelia of the fungus are planted on the leaves where they grow and soon cover the entire leaf. The ants tend the fungal gardens, which in turn produce spherical swellings that are eaten by the ants. An Atta leafcutter queen is estimated to live ten or more years. By the time her colony is mature, the nest will have more than several million workers, will have thousands of chambers and over a thousand entrances. Nests have been described that reach as deep as 6 m below the surface and extend over 100 m2. Although termite nests typically start out underground, they are built up with loads of building material until they have some structures above ground. Even the termites with the simplest nests have covered passages made by gluing pieces of mud together with fecal material. Their building process includes creating an arch and then extending that arch to form the tunnel, which protects them from predators, the sun and desiccation. The mounds of some termites get to be enormous, with chimneys that extend 9–10 m above the ground. The mound of Macrotermes bellicosus is one of the most complex yet described. The mound has a central living area with chambers for the king and queen, the brood and the fungal gardens (like the leaf cutter ants). Surrounding this central living area is an open chamber that allows air to circulate around the inner core. The outer protective wall is filled with passages that act like capillaries and maintain a constant temperature within the mound, while decreasing potential water loss from evaporation. Warm air, produced by the termites and gardens within the core, rises and passes out to the air passages within the outer protective wall. The air cools in these outer passageways and sinks downward. The cooler air is then drawn into the core area as the warm air rises. Millions of workers and chambers filled with fungal gardens generate a great deal of heat, yet the architecture of the mound keeps the temperature constant, within one degree Celsius. The shape of the termite mounds may also contribute to colony thermoregulation. For example, the mounds of the compass termite stand about 4 m high and are long and thin. The broad surfaces face east and west, while the thin sides face north and south. Thus, during the cool mornings and evenings, there is a broad surface facing the sun to collect solar energy, while during the heat of the day, only a narrow surface is exposed to the sun, minimizing the heat uptake. The nests of other species have tall towers or buttresses, which also help to cool down the nest. There is a group of solitary wasps that are referred to as mud daubers. This group includes the potter wasps, which build single or clusters of small mud cells, each one built to house one developing offspring and the provisioned, paralyzed insects or spiders to feed it. In some cases, the pots truly look like a clay pot molded into a jug-shape with an outwardly curving lip at the entrance. After the jug has been stuffed full with paralyzed caterpillars and an egg laid, the jug is sealed with a mud plug. Because these wasps are small, their nests are often overlooked, and most homeowners are more likely to notice the long mud tubes of the organ-pipe wasp (Trypoxylon spp.) (Fig. 93) or the large cell clusters of the common mud dauber (Scelephrons spp.). The organ pipe nest is built by the female, as is typical in the Hymenoptera. She adds mud to form arching mud strips in a long half-tube attached along the edges to the substrate. The tube is long enough to house approximately six cells. She lines the inside, smoothing out the interior walls and adding to the tube along the substrate junction. She then begins the process of provisioning the cells with spiders, laying an egg on one of the spiders and sealing off the individual cells with mud in sequence down the length of the tube. This is one group in which Construction Behavior of Insects C Construction Behavior of Insects, Figure 94 Polistes wasp female building a petiole and the side of the first cell. Building material is a combination of plant fibers and glandular secretion. Construction Behavior of Insects, Figure 93 Organ-pipe mud dauber female constructing a mud tube. She will line the tube and then construct a series of cells down its length. Each cell will be provisioned with spiders, have an egg laid on one spider, and be sealed off with a mud wall. The fly in the photograph is a nest parasite of this wasp. the male contributes to the process of construction and brood provisioning by guarding the tube entrance from nest parasites that would otherwise sneak one or several of their own eggs into the cells. The male is then well placed to mate with the female when she is ready to lay her eggs. Social wasps usually use plant material of some sort to build aerial or underground nests, but some species use mud. Each nest is typically made of one or more combs of hexagonal cells in rows, and the nest may have one or many enclosing envelopes. The architecture of the nests made by wasps is typically cryptic in that the nests are thin and built on the underside of tree trunks, or leaves, or in cavities, have the color of the surrounding substrate and are easily overlooked. The nests of some social wasps have no enclosing envelope and are attached to the substrate by a narrow petiole (Fig. 94). The nests of a unique group of wasps, Microstigmus, are made using plant hairs from the underside of leaves. Microstigmus comes has been extensively studied; these small (4 mm long) tropical wasps begin by locating a nesting spot on the underside of a leaf of a species-specific host plant in the genus Chryosophila. A single female, or small group of cooperating females, then begins to chew up plant hairs in a wide circle. The hairs are pulled inward and a growing mound of hairs wrapped in silk forms around the edge of the circle. The wasp or wasps keep working until a ball of plant hairs and silk is located at the center of the area cleared of plant hairs. The base of the ball is worked into a long slender spiraling petiole, which suspends the ball that will form the actual 1039 1040 C Construction Behavior of Insects nest. The wasps create an entrance near the base of the petiole and excavate a space called the vestibule. This will be an area for adult wasps to gather that is located above the cells. The remaining ball is worked into 1–14 cells, which are lined with silk and provisioned with Collembola. Although some Microstigmus are progressive provisioners, M. comes is a mass provisioner. Prior to laying an egg, these wasps stuff each cell with enough Collembola to supply a developing larva through pupation. The entire nest is only approximately 1 cm3 in size. Building Materials The study of the building materials that insects use is still far from complete. There are two key ways the building material supports the weight of the structure, (i) compression, in which the nest bears the weight of the overlying structure like the bricks in the wall of a building, and (ii) tension, in which the weight of the structure is suspended and hangs. Insects use both methods. Silk, often used in suspension construction, is a polypeptide that is highly diverse in structure as well as in gland of origin when compared across species. However, in general, it is a remarkable type of material in that it is extremely light weight yet has a tensile strength 2–3 times that of steel. Its strength comes from its structure. Silk, in most arthropods, is a fibroin– a protein with long, unbranching polypeptides. Although the sequence and make up of the polypeptide chains vary between species, glycine, alanine and serine make up about 80% of most types of silk. Crystalline or highly organized regions are interspersed with amorphous or unorganized regions. The organized areas have tightly packed polypeptide chains that are in tightly linked pleats through hydrogen cross bonding. The amorphous areas give silk its flexibility. When building, bees use a second type of glandular secretion. Epidermal glands along the anterior edges of the abdominal sternites and/or tergites produce bees’ wax in thin scales. Wax is a component of the insect integument. During the course of evolution, it is likely that clusters of cells that produced wax for the integument became specialized for greater wax production. The bees scrape the wax off the wax producing surfaces of the abdomen and work it into a ball of material for adding to the comb. In some species, the wax is mixed with plant resins to make a mixture called cerumen. Although wax and cerumen are both water resistant and pliable, cerumen is more pliable than wax and is used for building the softer parts of the nest such as the storage pots and brood cells. In some species, wax is also mixed with other glandular secretions or even mud. Resins may even be used without the addition of wax to produce supporting pillars and protective layers. Thus, construction material for bees varies dramatically in the wax content and in the nature of the additives, depending on the species, the component of the nest under construction and the type of support the structure provides. Mud is often mixed with water and glandular secretions or fecal material and used in building. Insects building with mud usually use fine, moist soil. In some species such as the mud-daubing wasps, the builder vibrates as it collects and applies the mud. This has the effect of suspending the mud particles and liquefying the material, thus making it easier to manipulate and shape. The use of plant fibers and fragments requires the addition of glandular secretion, as well. Analysis of the building material of Polistes paper wasps shows that the glandular secretion adds a mix of more than 20 amino acids to the plant fibers, including glycine, serine, alanine, valine and proline. The combined material is pliable, strong, lightweight and water resistant. Not only is the glandular secretion added to the building material, but it also is added to the outer surface of the nest, especially around the petiole and comb back. The wasps apply the pure oral secretion by licking the nest and this often results in a shiny, dark outer layer. Construction Behavior of Insects C Function and Evolution of Insect Structures Protection is the primary function of all insectmade structures. The structure separates the insect from the exterior world and thus, may help to lessen fluctuations in temperature and humidity and may act as a protective barrier between developing brood and predators, parasitoids and parasites. The bubble nests of the spittle bug, the caddisfly case, the galleries of the Embioptera and the towering nests of termites all share the functional role of protection. However, the structures often have additional functions. For instance, the bubble nests of the spittle bug help the nymph avoid desiccation; the caddisfly case assists in feeding in some species, and helps move water over the gills. As previously described, the termite mound controls thermoregulation and humidity regulation, and shelters the colony from rain. It provides housing for the members of the colony and their sources of food. One feature of many social insect combs that has attracted attention is the hexagonal array of cells. This pattern of cells occurs in the combs of honey bees and many social wasps and appears to be the result of packing circular cells as closely as possible with a minimum use of building material. The builders actually build circular cells initially, which are possible to see along the edge of the comb, but as they add on additional cells, the adjoining walls straighten out. Once a cell is completely surrounded by other cells, it takes on the hexagonal shape. Occasionally cells are four- or five-sided, but this occurs when the cell arrangement is being adjusted for a confined space, or the rows of cells are out of alignment. The brood developing in the hexagonal cells of the comb is a rich food source for a number of predators, both vertebrate and invertebrate. The enclosing envelope that the nests of many species have helps to hide the comb, and the small entrance hole is easy to defend against ants (Fig. 95), which are an important invertebrate predator of social insect colonies. In addition, the envelope layers of Construction Behavior of Insects, Figure 95 Polybia occidentalis nest showing the enclosing envelope and small entrance hole that aids in nest defense against ants (photo R. L. Jeanne, Univ. Wisconsin). some wasp nests help to insulate the brood on the inside by creating a cushion of air around them. Nests with no enclosing envelope have a narrow attachment to the substrate as an anti-predatory defense. The comb appears to hang from this narrow petiole in a precarious manner, but the petiole is strengthened with many layers of glandular secretion or silk. The narrow petiole provides protection from marauding ants because it is difficult for them to find, and the wasps can defend it both physically and with applied chemical barriers. It is possible to compare nest structure among groups of related species and formulate hypotheses about the evolution of the different speciesspecific structures. For instance, in the social wasps, all of the variation in nest architecture was shown to be a derivation of the basic horizontal comb (cell openings facing down) hung from the substrate by a somewhat narrowed extension of 1041 1042 C Construction Behavior of Insects the comb top or back. In one derived set of nests, the comb top has become narrowed to form a petiole of variable length and combs take a variety of angles and forms. Another derived group developed envelopes that are the extension of the outer walls of the outer row of cells of the comb. Petioles may or may not be present and the envelope serves to protect the brood from predators. A third group of distinctive nests have narrowed petiole attachments, multiple combs and a separate envelope that is not an extension of the cell walls. It can only be hypothesized that predation, environmental pressures and evolving modifications in the building material combined to produce the larger, complex nests of the highly eusocial wasps. It has been suggested that the evolution of building material capable of holding together a large nest was a critical precursor to the development of highly eusocial behavior and large colony size. The building behavior has had to change as well, because as nests become larger, more construction material is needed for the nest attachment and supporting walls. As a result, mature nests are often structurally quite different from incipient nests. Regulation of Construction Behavior As shown in previous sections, the nests of most insects are species-specific in design and the nests can thus be used to enhance phylogenetic studies. There are several hypotheses attempting to explain how species-specific construction information is transmitted between generations. Insects could inherit a blueprint of the finished nest design and then build toward creating a structure that matches the blueprint. There is no support for this hypothesis, and intuitively one can consider a small termite building in the pitch-black galleries of the developing nest and see the difficulty. There is little possibility that such an insect could comprehend the entire structure and coordinate its construction with that of many other builders. A second possibility is that there are certain individuals that inherit the design blueprint, and these lead builders then direct the construction of others based upon information they have gathered while moving systematically about the nest. There is again no evidence supporting this hypothesis, and it would be difficult for an individual to compare what others are building to a blueprint design of the finished product. In all insects studied thus far, the only direction observed is by the queen or king (if present), and they simply act as pacemakers. A third hypothesis is that each individual inherits a construction program of sorts. This program consists of the steps of construction and a sensitivity to certain cues that regulate that construction process. When an insect builds, it has no sense of the finished product and is simply responding to the immediate cues, some of which come from previously completed construction. The process of building in response to previous construction is referred to as “stigmergy,” a word coined by P. Grassé. In solitary insects, the building program follows a linear series of steps with the completion of one step triggering the next. Cues associated with the completion of an act are tested with the addition of a load. A simple decision is made – is the previous step done? If no, add building material in the same way as before, if yes, go on to the next step of construction. By building through a specific set of construction steps and responding in a species-specific way to certain cues, the results are a species-specific nest. Because each individual (Fig. 96) is independently responding to the cues in its surroundings, no coordination among individuals is necessary. With social insects, nests develop over a longer period of time. Throughout the nesting season, cells are progressively lengthened as the brood grows, entrances, chambers and cells are added, and petioles and envelopes are enlarged. Although the building may start out with a linear series of construction steps, this soon can no longer describe the process where building can take place in any of many different sites simultaneously. Builders must evaluate competing locations and Construction Behavior of Insects Construction Behavior of Insects, Figure 96 Diagrammatic representation of a building program. choose one site for building. In large complex nests, like those built by termites, different areas of the nest have distinct structures added at certain times in the colony’s reproductive cycle (e.g., platforms are built for dispersing reproductive allates.) This array of different structural components challenges stigmergy because the builders cannot just keep building based on previous construction and must switch to different building programs at appropriate times. Thus, building in highly eusocial insects must have a more complex regulatory mechanism or additional components to their building program. Nonetheless, stigmergy has been shown to be an important means for explaining the regulation of construction in a wide array of species, insect and non-insect, social and C non-social. Studies of construction behavior in different organisms can help identify common construction mechanisms. Where species differ, these comparisons can lead to insights into the evolution and regulation of this behavior. The building process actually involves two types of decisions: (i) where to build next, and (ii) how to shape the building material in that location. For instance in the paper wasp, Polistes fuscatus, which builds a comb suspended by a petiole, brood size and cell mouth angle impact the decision about which cell to lengthen next, while the antennae are used to measure the width of the cell as pulp is added. By constantly rotating the antennae in adjacent cells, wasps maintain a speciesspecific cell diameter. Cut one of the antennae and the cell wall measurements are altered. Most behavioral studies of construction have investigated the first type of decision only. The second type of decision and its relationship with the first have been studied in only a few insect species and many questions still remain to be investigated. Individual building decisions are a part of the larger phenomenon of colony wide activity. The regulation of the pace of construction and how the tasks of foraging for water, collecting wood pulp for building and building itself are partitioned has been studied in the swarm founding wasps. Polybia occidentalis has been shown to have complex interactions among the builders, pulp foragers and water foragers, with smaller colonies having longer queuing delays that result in less efficient task partitioning. In another swarm founding species of wasp, Metapolybia spp., water or water saturation of the colony appears to be a critical regulator of task partitioning dynamics, with water availability affecting water foraging, pulp foraging, and consequently, the number of builders. As it has become clear that among insects, individuals build by rather simple rules and act independently of one another, it has become apparent that colony wide behavior can be understood as a culmination of all of these individual building events. Self-organization is an epi-phenomenon seen in some aspects of social insect behavior. The 1043 1044 C Construction Behavior of Insects Construction Behavior of Insects, Figure 97 Some diverse types of insect construction: top left, paper wasp nest showing detail of brood cells; top right, paper wasp nest early in construction showing early formation of cells; second row left, tubes constructed by subterranean termites to maintain high humidity as they seek food; second row right, mud dauber nest; third row left, pits for capture of ants constructed by ant lion larvae; third row right, mound constructed by imported red fire ants; bottom row left, tent constructed by eastern tent caterpillar larvae; bottom row center, paper wasp nest; bottom row right, nests constructed by fall webworm larvae. (All photos by J. L. Castner, University of Florida.) Contamination honey, pollen and brood storage pattern seen in honey bee combs can be explained through a selforganizing process. Likewise, positive feedback during construction can amplify small differences in worker behavior, and can lead to the distinct and repeated patterns of galleries observed in both ant and termite nests. Computer modeling studies have shown that, indeed, relatively simple rules and a programmed responsiveness to the location and activity of other colony units within the virtual nest can lead to clustered building and a chamber pattern of walls and spaces similar to those of real nests and other repeating patterns seen in nature. Modeling studies have also shown that relatively small changes in the building program can lead to pronounced differences in the appearance of nests. These results suggest a mechanism for the evolution of the diversity in nest structures observed in nature. Conclusions Much of behavior is transient, with little in the way of a permanent record left behind. Construction behavior (Fig. 97), however, does leave physical evidence behind that has even been fossilized. These trace fossils include burrow remains, nests and such things as the dung balls made by beetles some 30–35 million years ago. The amazing fact is that fossilized ant nests from 60 million years ago show little variation from those seen today, suggesting that at least some social insects have not changed their behavior over extremely long periods of time. Thus, the complex behaviors associated with insect construction have been around for millions of years. Some of the evolutionary process and the regulation of construction behavior is now understood, but this area of insect biology remains a vital and fertile area for ongoing and future research. References Hansell MH (1984) Animal architecture and building behaviour. Longman, New York, NY, 324 pp C Matthews RW, Matthews JR (1978) Insect behavior. Wiley, New York, NY, 507 pp Ross KG, Matthews RW (eds) (1991) The social biology of wasps. Cornell University Press, Ithaca, NY, 678 pp Turner JS (2000) The extended organism. Harvard University Press, Cambridge, MA, 235 pp Von Frisch K (1974) Animal architecture. Harcourt Brace Jovanovich, New York, NY, 306 pp Consumption Efficiency The proportion of energy available that is consumed at a trophic level. In the case of herbivorous insects, it is the proportion of net primary productivity that is ingested. Contact Poison A pesticide that acts after external contact of the insect with the toxicant, and does not require ingestion to be effective.  Insecticides Contagious Disease A disease which is naturally transmitted by hosts of the disease; synonymous with communicable disease. Containment From a regulatory perspective, containment consists of phytosanitary measures in and around an infested area to prevent spread of a pest.  Risk Analysis (Assessment)  Regulatory Entomology  Invasive Species Contamination Harboring of, or contact with, microorganisms (or other organisms such as insect parasites). 1045 1046 C Continental Drift Continental Drift temperatures, and the low temperatures have an effect on insect mortality, while at other times the controlled atmosphere directly affects the desired insect control. Reported effects of controlled atmosphere on insect physiology include the reduction of NADPH levels in hypercarbonic (>10% CO2) environments, a reduction in energy charge as a result of slower production of ATP, the production of glutathione is reduced, and the inhibition of the regeneration of choline to acetylcholine under hypercarbonic environments. There is also an observed reduction of high temperature tolerance in insects exposed to anoxic environments. Controlled atmosphere can also mean controlling the environment surrounding an insect, meaning the temperature, light, humidity, pressure, and atmospheric gases. Any postharvest situation allows for the manipulation of the environment for pest control. Traditionally, controlled atmospheres means the alteration of atmospheric gases, such as oxygen and carbon dioxide. This can be achieved through the use of flow-through systems in which oxygen is lowered by a nitrogen purge and carbon dioxide is increased by injection of this gas. The levels of oxygen and carbon dioxide The separation and movement of land masses in geologic time. Controlled Atmosphere Technologies for Insect Control Lisa neven, eLizaBeth mitCham USDA, ARS, Wapato, WA, USA University of California, Davis, CA, USA Controlled atmosphere treatments have been employed to control stored products pests for centuries. The first example is the storage of grains in ancient Egypt, where the cribs were sealed tightly to prevent the propagation and growth of insects through the use of lowered oxygen environment. Historically, controlled atmosphere treatments were designed to preserve commodity quality during long-term storage. The secondary effect of providing some level of insect control was serendipitous. Sometimes the controlled atmosphere provides extra time to store a commodity at low Controlled Atmosphere Technologies for Insect Control, Table 19 USDA-APHIS approved controlled atmosphere treatments for fresh fruits as of 2007 Percentage Temperature Heating rate Total Time Commodity Pest O2 CO2 °C °C/hr Apple Codling Moth & Oriental Fruit Moth 1 15 46 12 Cherry Codling Moth & Western Cherry Fruit Fly 1 15 47 >200 25 min Cherry Codling Moth & Western Cherry Fruit Fly 1 15 45 >200 45 min Nectarines & Peaches Codling Moth & Oriental Fruit Moth 1 15 46 24 2.5 h Nectarines & Peaches Codling Moth & Oriental Fruit Moth 1 15 46 12 3.0 h 3h Controlled Atmosphere Technologies for Insect Control C Controlled Atmosphere Technologies for Insect Control, Table 20 Some potential controlled atmosphere treatments to control arthropod pests in fresh fruits and vegetables Percentage O2 CO2 Temperature Time (°C) (Days) Commodity Pest Apple San Jose scale <1 >90 >12 2 Apple San Jose scale 0 96 22 1 Apple Codling moth 1.5–2 <1 0 91 Apple Mites 1.0 1.0 20.8 Apple 4 tortricid pests 0.4 5.0 40 Asparagus Aphid & thrips 8.4 60 0–1 4.5 Strawberry Thrips 1.9–2.3 88.7–90.6 2.5 2 Sweet potato Sweetpotato weevil 4 60 25 7 Sweet potato Sweetpotato weevil 2 40 25 7 Sweet potato Sweetpotato weevil 2 60 25 7 Table grapes Mites, thrips, omnivorous leafroller 11.5 45 2 13 Walnut Codling moth 8.4 60 25 Mango Fruit flies Broccoli Thrips 0.0025 Lettuce Thrips 0.0025 used in controlled atmosphere treatments vary in relation to commodity tolerance and insect intolerance. The levels of atmospheric gases necessary to kill a target pest will vary in relation to the pest/ commodity complex. Controlled atmosphere technologies have unique terminology associated with them. Some of the important terms/acronyms and their definitions are: Controlled atmosphere (CA): Alteration of the chemical content of the air environment from that normally experienced at STP. Chilling mortality: Death of an organism due to cumulative, non-freezing, low temperature damage. Anoxic: Low oxygen to no oxygen environment. Hypercarbonic: High carbon dioxide environment. 160 >0.6 7 MAP: Modified atmosphere packaging. Vacuum: Reduction of atmosphere through evacuation. Reduction of atmospheric pressures below STP. STP: Standard temperature and pressure. Internationally, the current STP defined by the IUPAC (International Union of Pure and Applied Chemistry) is an absolute pressure of 100 kPa (1 bar) and a temperature of 273.15°K (0°C). Hypobaric treatments: Reduction of atmospheric pressures below STP. Hyperbaric treatments: Increase of pressure above STP. Film wraps: Plastic impermeable or semi-permeable wraps of fresh fruits and vegetables to reduce respiration and dehydration. Coatings: Usually wax or shellac type mixtures that cover fruits and vegetables to reduce respiration and dehydration. 1047 1048 C Controlled Atmosphere Technologies for Insect Control Low Oxygen The most common types of controlled atmosphere treatments are those that employ low oxygen environments. In the case of apples, oxygen levels vary from 1 to 5%, and carbon dioxide levels can vary from 0.3 to 3%. Other treatments use ultra low levels of oxygen, such as the case with broccoli, which employs oxygen levels of 0.0025%. Both of these treatments are performed at temperatures well below 5°C. Low oxygen treatments can be effective in killing insects provided that the temperature is high enough to put a stress on the metabolic system of the insect. Reduced O2 consumption leads to a decreased rate of ATP production. As a result of energy insufficiency, the membrane ion pumps fail, leading to K+2 efflux, Na+ influx, and membrane depolarization. The voltage-dependent Ca+2 gates are then opened, causing Ca+2 influx. The high Ca+2 concentration in the cytosol activates phospholipases and leads to increased membrane phospholipid hydrolysis. The cell and mitrochondrial membranes become further permeable, causing cell damage or death. Omnivorous leafroller pupae use metabolic arrest as a major response to hypoxia. The pupae’s O2 consumption rate and metabolic heat rate decrease slightly with decreasing O2 concentration until a critical concentration is attained, below which the decrease become rapid. The critical concentration points are 10, 8 and 6 kPa at 30, 20 and 10°C, respectively. Although the pupae’s metabolism decreases quickly below the critical concentration points, the pupae do not initiate anaerobic metabolism until the O2 concentration is below 2 kPa at 20°C. Concentrations of O2 below the anaerobic compensation point appear to be in the insecticidal range. at temperatures within the normal growing range (10–40°C). High carbon dioxide treatments have been shown to be very effective in controlling mites and diapausing insects. However, when elevated carbon dioxide is used in combination with low oxygen levels, the results on insect mortality have been variable. Combination high temperature and controlled atmosphere treatments used effectively against lepidopteran pests do not work as effectively against fruit flies. This may be due to the differences in the respiratory systems and regulatory mechanisms of terrestrial (Lepidoptera) and semi-aquatic (fruit fly larvae) insects. At low temperatures, near 0°C, mortality of the moth Platynota stultana is greater with 45 kPa O2 + 11.5 kPa O2 (air) as compared with 45 kPa CO2 + 0.5 kPa O2. In some cases, when only a small amount of CO2 is present in an O2-deficient atmosphere, it can enhance mortality by up to ten-fold. Elevated CO2 (hypercapnia) can reduce the rate of insect respiration. High levels of CO2 can reduce oxidative phosphorylation by inhibiting respiratory enzymes such as succinate dehydrogenase and malic enzyme. Reduced oxidative phosphorylation leads to reduced ATP generation, which in turn leads to a failure of membrane ion pumps, membrane depolarization and eventual cell death, as described for hypoxia. Elevated CO2 levels can decrease pH through the formation of carbonic acid. Reduced pH can increase intercellular Ca2+ concentration, which causes the cell and mitochondrial membranes to become more permeable, suggesting that high CO2 can increase membrane permeability. High CO2 levels can alter the ratio of pyruvate to lactate by 25% of normal, changing the redox potential and a lesion in the electron transport chain, presumably by a modification in the permeability of mitochondrial membranes. High Carbon Dioxide Modified Atmosphere Packaging There are other treatments that use carbon dioxide levels of 60% or greater, with the oxygen level not being regulated. These treatments have been used Controlled atmosphere can also be achieved through the use of semi-permeable membranes, Controlled Atmosphere Technologies for Insect Control called modified atmosphere packaging, which reduces the movement of oxygen and carbon dioxide. Modified atmosphere packaging is generally performed at temperatures between 0–20°C, with 1–18% O2, and 0–10% CO2, and is of a long duration, generally weeks to months. Modified atmosphere packaging can also be generated using film wraps. Also, film coverings and coatings can form modified atmospheres in fresh horticultural commodities. These treatments are usually carried out at 20–27°C, for long durations, with variable levels of atmospheric gases, depending on commodity respiration rates and film permeability. The commodity will consume oxygen and increase carbon dioxide during normal respiration processes. Normally, the reduction of oxygen and elevation of carbon dioxide are not as severe because there is a point where either the level of oxygen will no longer support commodity respiration or the level of elevated carbon dioxide is inhibitory to commodity respiration. Therefore, modified atmosphere packaging often takes longer to kill the target pest. Temperature Combinations Temperature control has been a traditional means of controlling the environment to affect insect mortality. Typically, low temperature has been the means used to control postharvest pests. Low temperatures work because they are usually below the optimal growth and development temperatures of most insect species. Low temperature causes mortality through cumulative, systemic tissue and metabolic damage, and the inability to repair that damage. Unfortunately, low temperature controlled treatments require a significant time, measured in days, weeks, or even months, to affect insect mortality. The advantage of low temperature controlled atmosphere is that it could be applied during marine transit. A 13 day treatment with 45 kPa CO2 (11.5 kPa O2) at 2°C or lower has been developed for control of Pacific spider mite, western flower thrips and omnivorous leafroller on table grapes. Although table grapes C tolerate this treatment, exposure to insecticidal atmospheres for this length of time, even at low temperatures, would not be tolerated by many fresh commodities. There has been considerable research on controlled atmosphere at intermediate temperatures (10–28°C), but interest in this approach has been diminishing due to increasing research on high temperature CA treatments (40–55°C). The advantage of intermediate temperature controlled atmosphere treatments is that they range from hours to days, much faster than low temperature controlled atmosphere treatments. However, high temperature controlled atmosphere treatments have gained popularity because the treatments are relatively short and easy to apply. High temperature controlled atmosphere applies two simultaneous stresses, which greatly reduces total treatment time and minimizes commodity phytotoxicity due to elevated temperatures. In fact, high temperature controlled atmosphere treatments may be beneficial for climacteric fruits (fruits that continue to ripen after harvest) because the elevated temperatures knock out many of the enzymes involved in fruit ripening, and therefore extends shelf life. High temperature controlled atmosphere treatments appear to block thermal acclimation by blocking the synthesis of heat shock proteins due to lack of oxygen, wherein the elevated carbon dioxide inhibits respiration and alters internal pH, causing systematic breakdown of oxidative phosphorylation and electron transport. Hot water dips not only raise temperature, but alter the levels of atmospheric gases in the commodity. As temperature rises, oxygen level in the commodity is reduced and carbon dioxide is elevated. This is due to the interaction of cuticle permeability and ability of the gases to dissolve in water. Ozone, Other Chemicals and Processes Ozone has typically been used for control of postharvest diseases. However, the advances in ozone generation and application of vacuum has allowed 1049 1050 C Controlled Atmosphere Technologies for Insect Control for treatments to be developed for arthropod pests. The problem with ozone is that it is nonpenetrating and can only effectively control external pests. Also, ozone penetration is inhibited by water. So, wet commodities are poor candidates for ozone treatments. In addition, there may be some problems with ozone if the commodities have green stems and leaves. Ozone decomposes chlorophyll and may cause a “bleaching” effect of green commodities. Hypobaric treatments have been gaining popularity. These treatments work by reducing atmospheric pressures below STP (Standard Temperature and Pressure), and in turn reduce both the availability of oxygen and the ability of the spiracles to remain closed. This may cause anoxia and desiccation stress, resulting in mortality of the insect. Only recently, hyperbaric or hydrostatic pressures have been tested for controlling internal feeding insects. This technology uses very high pressures of 10,000–80,000 psi, pressures experienced in the deep ocean environments, to disinfest and decontaminate foods. It is not known how these very high pressures kill insects, but it is presumed that it causes protein denaturation and wide-scale tissue break-down. Machinery The most attractive feature of controlled atmosphere treatments is the wide range of locations and situations where it can be applied. Controlled atmosphere treatments can be applied in huge warehouses, individual pallets in cold rooms, specially designed heat/controlled atmosphere chambers, hot water dipping tanks, shipping containers in transit, in individual boxes (via modified atmosphere packaging), and in individual fruits (via wraps and coatings). With today’s technology, controlled atmosphere is becoming more affordable and portable. Nitrogen generators needed to form low oxygen environments are becoming more compact and affordable. Compressed tanks of carbon dioxide are still relatively inexpensive, and are needed only when the protocol calls for CO2 levels higher than the commodity can produce. Modified atmosphere packaging is found in every aspect of the fresh food market. Each modified atmosphere packaging system provides an affordable and portable controlled atmosphere system. Approved Treatments To date there are only a few controlled atmosphere treatments in the USDA, APHIS treatment manual (see “approved controlled atmosphere” table). These treatments were the first to be approved and were only entered into the Federal Register on April 16, 2007. These treatments employ a combination of controlled atmosphere (Fig. 98) and hot forced air (called CATTS for “Controlled Atmosphere Temperature Treatment System”). Other controlled atmosphere treatments have been developed (see “potential controlled atmosphere” table), but are not yet in the APHIS treatment manual. Adoption of controlled atmosphere quarantine treatments by industry has been slow because of the wide availability of chemical fumigants like methyl bromide. Although methyl bromide was identified as an ozone depleter under the Montreal Protocol, its use for commodity disinfestations is still allowed while other uses, such as soil and structural fumigations, are restricted. The cost of methyl bromide has rapidly increased from US$5 for a 100 lb. tank in 1995 to nearly US$1,000 in 2007. As fumigation costs rise, alternative, nonchemical quarantine treatments will gain industry support and become more common. References Edwards LJ (1968) Carbon dioxide anaesthesia and succinic dehydrogenase in the corn earworm, Heliothis zea. J Insect Physiol 14:1045–1048 Fanestil DD, Hastings AB, Mahowald TA (1963) Environmental carbon dioxide stimulation of mitochondrial adenosine triphosphate activity. J Biol Chem 238:836–842 Cooloola Monsters Controlled Atmosphere Technologies for Insect Control, Figure 98 A commercial CATTS (controlled atmosphere temperature treatment system) can accommodate various types of produce and packaging, and produce insect-free products. Fleurat-Lessard F (1990) Effect of modified atmospheres on insects and mites infesting stored products. In: Calderon M, Barkai-Golan R (eds) Food preservation by modified atmospheres. CRC Press, Boca Raton, FL, pp 21–38 Friedlander A (1983) Biochemical reflections on a non-chemical control method. The effect of controlled atmospheres on the biochemical processes in stored product insects. In: Proceedings of the third international working conference on stored product entomology. Kansas State University, Manhattan, Kansas, pp 471–486 C Herreid CF (1980) Hypoxia in invertebrates. Comp Biochem Physiol (A) 67:311–320 Hochachka PW (1986) Defense strategies against hypoxia and hypothermia. Science 231:234–241 Mitcham EJ, Zhou S, Bikoba V (1997) Controlled atmosphere for quarantine control of pests of table grape. J Econ Entomol 90:1360–1370 Neven LG, Mitcham EJ (1996) CATTS (controlled atmosphere/temperature treatment system): a novel tool for the development of quarantine treatments. Am Entomol 42:56–59 Neven LG (2005) Combined heat and controlled atmosphere quarantine treatments for control of codling moth, Cydia pomonella, in sweet cherries. J Econ Entomol 98:709–715 Neven LG, Rehfield-Ray LM (2006) Combined heat and controlled atmosphere quarantine treatment for control of western cherry fruit fly in sweet cherries. J Econ Entomol 99:658–663 Neven LG, Rehfield-Ray L, Obenland D (2006) Confirmation and efficacy tests against codling moth and oriental fruit moth in peaches and nectarines using combination heat and controlled atmosphere treatments. J Econ Entomol 99:1610–1619 Neven LG, Rehfield-Ray L (2006) Confirmation and efficacy tests against codling moth, Cydia pomonella, and oriental fruit moth, Grapholitha molesta, in apples using combination heat and controlled atmosphere treatments. J Econ Entomol 99:1620–1627 Zhou S, Criddle RS, Mitcham EJ (2000) Metabolic response of Platynota stultana pupae to controlled atmospheres and its relation to insect mortality response. J Insect Physiol 46:1375–1385 Zhou S, Criddle RS, Mitcham EJ (2001) Metabolic response of Platynota stultana pupae during and after extended exposure to elevated CO2 and reduced O2 atmospheres. J Insect Physiol 47:401–40 Convergent Evolution The evolution of unrelated species or lineages resulting in similar structures and behaviors. Cooloola Monsters A family of crickets (Cooloolidae) in the order Orthoptera.  Grasshoppers, Katydids and Crickets 1051 1052 C Cooloolidae Cooloolidae A family of crickets (order Orthoptera). They commonly are known as cooloola monsters.  Grasshoppers, Katydids and Crickets Cooties A popular term applied to human body lice.  Human Lice  Chewing and Sucking Lice (Phthiraptera) Coppers Some members of the family Lycaenidae (order Lepidoptera).  Gossamer-Winged Butterflies  Butterflies and Moths Copromorphidae A family of moths (order Lepidoptera). They commonly are known as tropical fruitworm moths.  Tropical Fruitworm Moths  Butterflies and Moths Copularium The initial chamber constructed by a pair of colony-founding termites. Coquillett, Daniel William Daniel Coquillett was born on a farm in Illinois on January 23, 1856. He collected insects while a youth, and published his first entomological paper “On the early stages of some moths” in the Canadian Entomologist in 1880. However, he developed an incipient tuberculosis, and his parents moved the family to Anaheim, California, in 1882. There, he began to specialize in flies. His entomological activities drew the attention of C.V. Riley who appointed him as a U.S. Department of Agriculture field agent in 1885. He worked on chemical control of pest insects (Fig. 99) and on part of the cottony cushion scale biological control program. At the same time, he continued his studies of Diptera, especially bee flies and robber flies. When C.V. Riley’s relationships with California growers become strained in 1893, Coquillet was called to Washington, DC, and was made an honorary Coprophagous Feeding on fecal material. Coprophagy Feeding on dung or excrement by animals. Such arthropods are said to be coprophagous or coprophages.  Food Habits of Insects Coptopsyllidae A family of fleas (order Siphonaptera).  Fleas Coquillett, Daniel William, Figure 99 Daniel W. Coquillett. Corazonin custodian of the Diptera collections in the U.S. National Museum. There, he published extensively on Tachinidae, Simuliidae, Culicidae, and other flies, eventually describing about 1,000 species. A major work was his (1910) “Type species of North American Diptera.” He died on July 7, 1911, and his Diptera collection became part of the US National Museum. Reference Mallis A (1971)Daniel William Coquillet. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 389–391 C moths, but no cardio-stimulating action is found in any of these other insects. In the sphinx moth, Manduca sexta, this molecule plays a role in controlling eclosion. [Thr4, His7]-corazonin occurs in the European commercial honey bee, Apis mellifera, but its function is yet to be elucidated. The last molecule is [His7]-corazonin that has been identified from a stick insect, a grasshopper, and locusts. Immunohistochemical observations indicate that corazonin is synthesized in the brain and sent via the axon to the corpus cardiacum where it is presumably secreted into the hemolymph in some insects. In locusts and grasshoppers, corazonin induces melanization and also has other physiological functions, as described below in association with phase polyphenism. Coral Treaders Members of the family Hermatobatidae (order Hemiptera).  Bugs Corazonin seiJi tanaka National Institute of Agrobiological Sciences (Ohwashi), Tsukuba, Ibaraki, Japan Corazonin is a neuropeptide that is found in many insects. It consists of 11 amino acid residues, and three molecule types are known (Fig. 100). [Arg7]-corazonin was the first molecule discovered, from the cockroach Periplaneta americana, and is a potent cardio-stimulating neuropeptide. It has been found in other species including other cockroaches, a cricket, and Role of Corazonin in the Control of Body-Color Polymorphism in Locusts In 1921, B.P. Uvarov proposed the phase theory to explain that locusts that had been regarded as two distinct species (Locusta danica and L. migratoria) belonged to the same species, which was designated as L. migratoria. According to his theory, locusts display body-color polyphenism in response to population density and some environmental factors. Locusts under low population density are called solitarious phase, whereas those under high population density are called gregarious phase. Solitarious nymphs are uniformly colored. Their body color is cryptic and assumes green, brown, yellow, reddish, grey, or black depending on the background color of their habitat. In contrast, gregarious pGlu-Thr-Phe-Gln-Tyr-Ser-Arg-Gly-Trp-Thr-Asn-amide [Arg7]-corazonin pGlu-Thr-Phe-Thr-Tyr-Ser-His-Gly-Trp-Thr-Asn-amide [Thr4, His7]-corazonin pGlu-Thr-Phe-Gln-Tyr-Ser-His-Gly-Trp-Thr-Asn-amide [His7]-corazonin Corazonin, Figure 100 Corazonin molecule types. Different amino acids are emphasized. 1053 1054 C Corazonin nymphs develop black patterns with an orange background color. Locusts growing under intermediate population densities are often called transient phase and display intermediate body coloration. Juvenile hormone (JH) is responsible for the induction of green color. Because the green body color is common among solitarious locusts, JH was once believed to control the phase-related body-color polyphenism. The administration of JH to gregarious nymphs causes them to lose the black patterns and induces green color, but destruction of the corpus allatum, the gland producing JH, does not induce black patterns. An albino mutant strain of L. migratoria was used to study the hormonal control of body color polyphenism. This strain was derived from a laboratory culture in Japan, and the albinism is a recessive trait controlled by a simple Mendelian unit. The possible involvement of a neuropeptide in the control of body-color polymorphism was noticed in L. migratoria in which albino nymphs turned darker after receiving an injection of methanol extracts of brains and corpora cardiaca taken from normal (pigmented) nymphs. The extracts are heat-stable, but lose the dark-color inducing activity after incubation with a proteinase. This dark-color inducing factor was later demonstrated to be identical to [His7]-corazonin. The albinism of the above strain is caused by deficiency of this neuropeptide. Albino nymphs injected with [His7]-corazonin (Fig. 101) develop not only black patterns but also various other colors depending on the dose and the timing of the injection. Nymphs with a completely black body color appear if they are injected with a high dose of the neuropeptide at the beginning of the previous stadium, whereas those injected with lower doses at the same stage turn brown, light brown or yellow in the following nymphal stadium. Uniformly reddish body coloration appears in nymphs injected with the hormone shortly before the previous ecdysis. These body colors are similar to those normally observed in solitarious nymphs of L. migratoria in the field. Green solitarious nymphs are brownish or reddish in the ventral side of the body as well as some portions of the legs. Such body coloration can be induced in albino nymphs when both JH and corazonin are injected. As previously mentioned, gregarious nymphs typically develop black patterns with an orange background color. This type of body coloration can also be induced by injection of [His7]-corazonin at a certain stage in albino nymphs. It is highly likely that changes in corazonin concentration control the expression of body coloration in the locust. For a certain type of body coloration to be maintained in successive nymphal stadia, the specific changes in corazonin and JH concentrations required for the expression would be repeated Corazonin, Figure 101 Albino Locusta migratoria nymphs. The individual on the right was injected with corazonin in the previous stadium. Corazonin in each stadium. The hormonal induction of solitarious and gregarious body coloration is independent of the rearing density. Other locusts and grasshoppers also show body-color polyphenism and corazonin appears to be present in their central nervous system and corpora cardiaca. Transplantation of their brain and corpora cardiaca into albino L. migratoria induces darkening in the latter. Injection of [His7]-corazonin causes darkening in all locusts and grasshoppers so far tested. In the desert locust, Schistocerca gregaria, and the American grasshopper, S. americana, [His7]corazonin has been isolated and is responsible for the induction of black patterns, but not the background color. An albino strain is known for S. gregaria that is inherited by a simple Mendelian unit, as in the case for L. migratoria. However, the albinism in the former is caused by some unknown mechanism other than deficiency of [His7]-corazonin, because this neuropeptide is present in this strain. Some katydids display body-color variation. The albino bioassay suggests that their brain also contains corazonin or a similar compound, but injection of [His7]-corazonin has no biological activity on the body color in the katydids. Effect of Corazonin on Body Shape The body dimensions of locusts are affected by crowding. Morphometric ratios (Fig. 102) of F/C and E/F (F = hind femur length; C = maximum head width; E = forewing length) are often used to evaluate the degree of “gregarization” or “solitarization.” Gregarious adults have a smaller F/C ratio and a larger E/F ratio than solitarious adults. In the laboratory, similar values can be obtained by rearing locusts in a group or in isolation. Neither JH nor molting hormone influences these ratios in a consistent manner, indicating that these hormones play no major role in the control of phase-related changes in body shape. On the other hand, C Corazonin, Figure 102 Effect of corazonin injection on morphometric ratios in Locusta migratoria. (Based on data of Tanaka et al., 2002. Reproduced with permission of Journal of Insect Physiology.) injection of [His7]-corazonin induces morphometric gregarization in isolated-reared adults of L. migratoria and S. gregaria. This gregarizing effect is greater as the injections are made earlier during nymphal development. Effect of Corazonin on the Formation of Antennal Sensilla Locusts have several types of sensilla on the antennae. In S. gregaria and L. migratoria, the total number of antennal sensilla is greater in solitarious adults than in gregarious ones, although the significance of this difference is unknown. Corazonin causes locusts reared in isolation to develop fewer antennal sensilla when injected during the nymphal stage as compared with oil-injected counterparts, and the total number of antennal sensilla in the former becomes similar to that for locusts reared in groups. Among the four major antennal sensilla (Figs. 103 and 104), basiconic sensilla do not show a phase-specific difference in abundance. Injection of corazonin does not influence the abundance of this sensillum. As in the case for 1055 1056 C Corazonin Corazonin, Figure 103 Four types of antennal sensilla in Schistocerca gregaria. A: basiconic sensillum type with high density of pores; B: basiconic sensillum type B with low density of pores; C: coeloconic sensillum; D: trichoid sensillum with a terminal pore in the inset. (After Maeno and Tanaka, 2004. Reproduced with permission of Journal of Insect Physiology.) morphometric gregarization, the earlier the injection of corazonin during nymphal development the greater the effect on the total abundance of antennal sensilla in the adult stage. Corazonins in Other Insects Corazonin, Figure 104 The number of sensilla. (After Maeno and Tanaka, 2004. Reproduced with permission of Journal of Insect Physiology.) Corazonins have been chemically identified in only a small number of species. It is highly likely that more than three molecular types of corazonin exist in insects. Immunohistochemical observations are a powerful tool to visualize the presence and localization of corazonin and similar compounds in many species, although this technique still requires laborious Corazonin C Corazonin, Figure 105 Dark-color inducing activity of various organs from a heelwalker, Hemilobophasma montaguensis when implanted into albino nymphs of Locusta migratoria. (After Tanaka, 2006. Reproduced with permission of Applied Entomology and Zoology.) procedures. Probably the easiest and fastest method to detect corazonin is use of the albino L. migratoria strain as a bioassay. As mentioned earlier, implantation of a brain or corpora cardiaca taken from normal locusts into albino nymphs causes the latter to turn darker. Using this method, more than 90 species of insects have been checked. The results indicate that insects belonging to a total of 19 insect orders have been shown to have a dark-color inducing activity (Table 21) when their brain or/and corpora cardiaca were implanted into albino locusts. This includes both pterygote and apterygote orders of insects, indicating that corazonin or a corazonin-like compound is old in origin. Interestingly, no coleopterans show a sign of corazonin activity, which is also supported by immunohistochemical evidence. Brains and corpora cardiaca taken from twistedwinged parasites, Strepsiptera, which are often placed in the order Coleoptera, display a darkcolor inducing activity when implanted into albino locusts. Heelwalkers, belonging to a recently discovered new insect order, Mantophasmatodea, also have a positive response (Fig. 105). These observations suggest that corazonin or a similar molecule is widespread in the Insect class including pterygote and apterygote insects except for the Coleoptera.  Polyphenism in Insects and Juvenile Hormone (JH)  Phase Polymorphism in Locusts  Grasshoppers and Locusts References Pener MP (1991) Insect phase polymorphism and its endocrine relations. Adv Insect Physiol 23:1–79 Pener MP, Yerushalmi Y (1998) The physiology of locust polyphenism, an update. J Insect Physiol 44:365–377 Tanaka S (2001) Endocrine mechanisms controlling bodycolor polymorphism in locusts. Arch Insect Biochem Physiol 47:139–149 Tanaka S (2006) Corazonin and locust phase polyphenism. Appl Entomol Zool 41:179–193 Uvarov B (1966) Grasshoppers and locusts, vol 1. Cambridge University Press, Cambridge, UK, 481 pp Uvarov B (1977) Grasshoppers and locusts, vol 2. Centre for Overseas Pest Research, London, UK, 475 pp Veenstra JA (1991) Presence of corazonin in three species and isolation and identification of [His7] corazonin from Schistocerca americana. Peptides 12:1285–1298 1057 1058 C Corbicula Corazonin, Table 21 A list of insects tested by the albino bioassay for dark-color inducing activity. Class Order No. species testeda Insecta Thysanura 1/1 Ephemenoptera 2/2 Odonata 3/3 Orthoptera 18/18 Phasmatidae 1/1 Mantophasmatodea 1/1 Dictyoptera 6/6 Dermaptera 1/1 Isoptera 2/2 Plecoptera 2/2 Hemiptera 9/9 Neuroptera 1/1 Mecoptera 1/1 Trichoptera 6/6 Lepidoptera 11/11 Diptera 7/7 Hymenoptera 7/7 Strepsiptera 2/2 Coleoptera 0/13 Corduliidae A family of dragonflies (order Odonata). They commonly are known as green-eyed skimmers.  Dragonflies and damselflies Coreidae A family of bugs (order Hemiptera). They sometimes are called leaf-footed bugs.  Bugs Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea) ánGeLes vázquez Universidad Complutense de Madrid, Madrid, Spain a No. of species with a positive response/No. of species tested. Corbicula A pollen basket. A specialized scopa, or pollen holding apparatus, found in bumble bees and honey bees. The corbicula consists of the broad, concave hind tibia surrounded by a fringe of long hairs. Cordulegastridae A family of dragonflies (order Odonata). They commonly are known as biddies.  Dragonflies and Damselflies The superfamily Coreoidea of the suborder Heteroptera includes principally phytophagous bugs, but also some coprophagous and carrion feeding species. Ocelli are present on the head and the antennae are four-segmented (Fig. 106). Usually their metapleural scent-gland peritremes (plates on the metapleural scent glands) are well developed, with showy orifices that emit a strong scent. Coreoidea consists of five families: Order Hemiptera Suborder Heteroptera Infraorder Pentamorpha Superfamily Coreoidea Family Stenocephalidae Family Coreidae Family Alydidae Family Rhopalidae Family Hyocephalidae Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea) Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea), Figure 106 Coreoid bugs: (a) adult red-shouldered bug, Jadera haematoloma (Rhopalidae) by golden rain tree seed, a favorite food; (b) nymph of J. haematoloma; (c) adult C 1059 1060 C Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea) Stenocephalidae The small family Stenocephalidae, with two genera and over 30 species, possesses intermediate characters between Lygeidae and the Coreidae. This family is restricted to the Eastern Hemisphere. The greatest species diversity occurs in the Afrotropical Region. Stenocephalids are phytophagous, and often polyphagous. Many species in the Palaearctic region live in association with Euphorbiaceae. Stenocephalidae are slender bugs, 8–16 mm long. The head is elongated, subtriangular, with mandibular plates longer than the clypeus. The bucculae are short and explanate (flat and spreading). The antennae four segmented. Metathoracic glands are present. The abdominal spiracles are located ventrally. Females oviposit on plant surfaces. Coreidae This family consists of over 1,800 species and 250 genera, and is worldwide in distribution. Various groups are commonly called leaf-footed bugs, squash bugs or pod bugs. The family Coreidae was established by Leach in 1815 and included the present families Alydidae and Rhopalidae. All of them plus the Stenocephalidae have numerous veins in the membrane of the hemelytra. Coreids vary in size from 5 mm to more than 4 cm and although most have a robust body, some are thin or display peculiar legs and antennae and even spiny or hairy bodies. In some species, males use the modified hind legs for territorial combat. They show varied coloration, though in temperate climates they are generally brown or gray, and more or less dark. In tropical and subtropical countries, they sometimes are colorful. In coreids, the head tends to be small in relation to the body and generally is shorter than the pronotum. The antennae are four segmented. Metapleural scent-gland peritremes are well developed. Currently, the family is considered to consist of four subfamilies: Agriopocorinae, Coreinae, Meropachydinae and Pseudophloeinae. Agriopocorinae contains Australian coreids that are flattened and generally wingless. They possess spiracles on abdominal segments 2 and 3 that are visible from above. The vast majority of coreid bugs are contained on the Coreinae. They display very different shapes and sizes. They have a median sulcus (groove) on the head in front of the eyes. The tibiae possess deep grooves on the outer surface. The abdominal spiracles are not visible from above. This subfamily includes many tribes throughout the world, but mainly in warmer regions. The Meropachydinae include over 12 genera with a small head, the hind femora large, and hind tibiae with the distal end produced into a spine or tooth. The abdominal spiracles are not visible from above. This subfamily is restricted to the Neotropical Region. The Pseudophloeinae are relatively small in size. Their head does not have a medial sulcus in front of the eyes, the tibiae are not grooved (sulcate) on the outer surface, and the abdominal spiracles are not visible from above. This subfamily consists of about 28 genera and 165 species, and is mainly old-world in distribution. Stenocoris sp. (Alydidae), sometimes known as broad-headed bugs or rice bugs; (d) adult of cactus bug, Chelinidea vittiger (Coreidae), a species commonly associated with prickly pear cactus (Optuntia spp.) in North America; (e) adult of squash bug, Anasa tristis (Coreidae), a serious pest of squash in North and Central America; (f) adult golden egg bug, Phyllomorpha laciniata (Coreidae) with eggs carried on its back; (g) adult Euthochtha galeator (Coreidae) is found widely in eastern North America where it occasionally can become a pest, feeding on such plants as oranges and roses; (h) adult Leptoglossus phyllopus (Coreidae), one of the most damaging of the leaffooted bugs in North America, where it feeds on fruits, vegetables, grains and other crops. (photo credits: a, b, d, g, Lyle Buss; f, Arja Kaitala; c, e, h, John Capinera). Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea) Most coreids are phytophagous, feeding on seed or fruit. A few species are considered to be of economic importance. Cucurbits, various nut and fruit trees, rice, legumes and greenhouse vegetables are crops damaged by coreids worldwide. They even can attack conifers, junipers and Eucalyptus. Among the economically important species is the squash bug, Anasa tristis, which occurs from Brazil to Canada, and is especially a pest in Mexico and the USA. The genus Leptoglossus has more than 40 species and variable feeding habits. Formerly this genus was restricted to the Western Hemisphere, but there have been introductions to Europe (Italy and Spain) and to northern Africa. Some species are serious pests, such as the polyphagous Leptoglossus occidentalis and L. phyllopus. Coreids are not generally thought of as plant virus vectors, but their feeding secretions can be toxic, causing phytotoxicity. Also, they are associated with the transmission of fungi and other pathogens. Few behavioral studies have been done on Coreidae, although it is known that some males with large femora fight for territory, and that some employ pheromones for sexual attraction or aggregation. Of special interest is the behavior associated with parental care displayed by some coreids. Golden egg bug (Phyllomorpha laciniata Villiers) shows a very peculiar oviposition behavior. Females can lay eggs on plants (Paronychia argentea), or on the bodies of conspecifics of both sexes, where they remain until hatching. Egg carrying on P. laciniata has been known for over a century. It is common to see both males and females carrying 1–15 eggs/individual glued to their backs. The eggs laid on plants experience high rates of predation and attacks by parasitoid wasps. However, when the eggs are carried by an adult, fewer eggs are attacked by parasitoid wasps. Female oviposition choice may be adaptive and minimizes offspring mortality. The golden egg bug is not unique among insects in the sense that males carry eggs (it is also known in belostomatid bugs) but rather it is unique because there are different explanations for this behavior. Some authors have interpreted this behavior as parental care. Others C have suggested alternative explanations, such as the notion that this behavior results from the egg-laying female behaving as an intraspecific parasite. Alydidae The Alydidae, which are called broad-headed bugs, are a cosmopolitan family known worldwide. It includes about 42 genera and over 250 species, with most living in the subtropical and tropical regions. Many alydid nymphs are dark red-brown, and some adults look like ants or wasps. Alydidae includes three subfamilies: Alydinae that feed mainly on Fabaceae, and Micrelytrinae and Leptocorisinae that feed predominantly on grasses. The body and appendages of alydids are elongated. The head is subtriangular. The head relatively broad, with the width greater than half the width of the posterior margin of the pronotum. The bucculae is shorter than the antennal insertion. Two ocelli are present, but they are not found on tubercles. The metathoracic glands have distinct external peritremes, and they often produce a foul odor. The wing membrane has numerous veins. Some species are economically important, including Leptocorisa acuta on Poeacea, and Riptortus linearis and R. serripes on Fabaceae. Rhopalidae The family Rhopalidae includes 20 genera and about 210 species in two subfamilies: Serinethinae and Rhopalinae. These subfamilies are represented in both the Eastern and Western Hemispheres. Rhopalinae are most diverse in the Palaearctic Region whereas Serinethinae are more tropical in distribution. In Rhopalidae, the clypeus extends beyond the mandibular plates. Two ocelli are present on tubercles. Rhopalidae have greatly reduced metapleural scent-gland peritremes; for this reason they are called scentless plant bugs.The hemelytral membrane contains numerous veins. The secondary dorsal 1061 1062 C Coremata abdominal scent gland opens close to that of the first gland. All of the rhopalids are phytophagous on herbs and woody plants, but are not known to be economic pests of any significance. However, in Florida, USA, the rhopalid bug Jadera haematoloma feeds on golden rain tree, Koelreuteria spp. (Sapindaceae) and other plants in this family, becoming so abundant as to become a significant nuisance around homes. Niesthrea lusitanica (Sailer) is beneficial, and is used to control the invasive weed velvetleaf, Abutilon theophrasti. Hyocephalidae The small family Hyocephalidae includes only two genera and three species from Australia: Hyocephalus aprugnus Bergroth and Moevius with two species. The adults are large, elongate, and mostly dark in color. The head is very extended. The bucculae are enlarged, extending posteriorly to the eyes. The gula has a labial groove. The pronotum is trapezoidal. The scutellum is small. Macropterous and brachypterous morphs are known. The wing membrane contains four veins forming three basal cells. All spiracles occur ventrally. Hyocephalids live under stones in sandy and gravelly areas and may be associated with Acacia and Eucalyptus.  Bugs (Hemiptera)  Paternal Behavior in Heteroptera  Squash Bug, Anasa tristis (Degeer) (Hemiptera: Coreidae) Lansbury I (1966) A revision of the Stenocephalidae Dallas 1852 (Hemiptera-Heteroptera). Entomologists’ Monthly Magazine 101:145–160 Mitchell PL (2000) Leaf-footed bugs (Coreidae). In: Schaefer CW, Panizzi AC (eds) Heteroptera of economic importance. CRC Press, Boca Raton, FL, pp 337–403 Moulet P (1995) Hémiptères Coreoidea (Coreidae, Rhopalidae, Alydidae), Pyrrhocoridae, Stenocephalidae, EuroMéditerranéens. Faune de France 81:1–336 Schaefer CW (1965) The morphology and higher classification of the Coreoidea (Hemiptera: Heteroptera). III. The families Rhopalidae, Alydidae, and Coreidae. Misc Publ Entomol Soc Am 5:1–76 Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera). Classification and natural history. Cornell University Press, Ithaca, NY, 336 pp Vázquez MÁ (1985) Los Coreoidea ibéricos. Tesis Doctoral. Publicaciones de la Universidad Complutense de Madrid, 322 pp Coremata Long eversible tubes found at the tip of the male’s abdomen is some Lepidoptera (Fig. 107). These structures are inflated pneumatically, and release pheromones. The pheromones released from the coremata are thought to be aphrodisiacs, and to function in courtship. References Brailovsky H (2002) A new species of Maevius Stål from Australia and some notes on the family Hyocephalidae (Hemiptera: Heteroptera). Proc Entomol Soc Washington 104:41–50 Dolling WR (1991) The Hemiptera. Oxford University Press, Oxford, UK, 274 pp Göllner-Scheiding U (1983) General-Katalog der Familie Rhopalidae (Heteroptera). Mitteilungen aus dem Zoologischen Museum in Berlin 59:37–189 Kaitala A (1996) Oviposition on the back of conspecifics: an unusual reproductive tactic in a coreid bug. Oikos 77:381–389 Coremata, Figure 107 Fully inflated coremata in a specimen of a tiger moth (Arctiidae) (photo by A. Sourakov). Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae) Corethrellidae A family of flies (order Diptera)  Flies Corioxenidae A family of insects in the order Strepsiptera  Stylopids Corium The thickened basal region (Fig. 108) of the front wing in Hemiptera.  Wings of Insects Corixidae A family of bugs (order Hemiptera). They sometimes are called water bugs  Bugs Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae) James h. tsai University of Florida, Ft. Lauderdale, FL, USA C The corn delphacid, Peregrinus maidis (Ashmead) (Fig. 109) is known to be a vector of at least two viral diseases of maize (Zea mays L.), and is of particular economic importance in the lowland humid tropics. It has even been suggested that its introduction into Central America resulted in the collapse of the Mayan civilization. P. maidis is pantropical, having been recorded from most tropical regions, including the West Indies, Central and South America, Africa, islands in the Indian and Pacific Oceans, India, Malaysia, Taiwan, Indonesia, China and Australia. In the United States, it has been recorded from Washington, DC, south to Florida, and west to Ohio and Texas. P. maidis is the only known vector of two major viral diseases of maize, maize mosaic virus and maize stripe virus. The former is a tropical and subtropical disease and is found in Hawaii and in southern Florida. Maize stripe virus, also a tropical and subtropical disease, has been known to occur in southern Florida. The corn delphacid feeding causes damage to corn and sorghum (Sorghum bicolor Moench) extracting a large quantity of sap and excretion of honeydew. Both nymph and adult are efficient vectors of maize stripe and maize mosaic viruses. In general, the nymph is a more efficient transmitter than the adult. The virus can be acquired in less than an hour. The average incubation period of virus in P. maidis is 10–14 days, Corium, Figure 108 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and membranous distally. 1063 1064 C Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae) depending on age of vector and virus titre in the infected plant. Once the viruses are acquired by P. maidis, they are retained for life. Both viruses multiply in the vector, and only maize stripe virus is transovarially transmitted by P. maidis. Corn plants and P. maidis can be doubly infected, bearing both viruses. The life cycle of corn delphacid varies with temperature and host plant. The average developmental periods at 10–32°C are 2–10 days for first instar nymph, 4–20 days for second instar, 4–24 days for third instar, 17–19 days for fourth instar and 4–13 days for fifth instar. Nymphs undergo five instars within the range of 16–27°C. The adult longevity averages 10–97 days for males, and 19–108 days for females, within the temperature range of 17–32°C. At 27°C, the average number of eggs laid per day per female range from 15 to 25 eggs and a mean of 605 eggs, ranging from 297 to 938 eggs per female. The preoviposition period ranges from 3 to 6 days, and the oviposition period ranges from 11 to 48 days. The developmental period of immature stages is also affected by the host plants on which they are reared. At 27°C, the respective average length of nymphal development on corn, itch grass (Rottboellia exaltata L.), sorghum (Sorghum bicolor (L.) Moench), goose grass (Eleusine indica (L.) Gaertn.), barnyard grass (Echinochloa crusgalli L.), and gamma grass (Tripsacum dactyloides L.) is 17, 18, 20, 25, 27 and 61 days. The adult longevity on these respective plants averages 20, 28, 8, 8, 7 and 43 days. The number of eggs laid daily per female on corn, itchgrass and gamma grass is 21, 6 and 4 eggs, respectively. The number of eggs per female per life on these three plants averages 612, 146 and 46 eggs. The eggs are deposited under the epidermal cells along the leaf sheath and midrib. The egg is lined in one or more rows numbering 4–7 eggs. The egg is elongate and curved with a round posterior end. The average size of egg measures 1.06 mm long and 0.28 mm wide. Freshly laid eggs are translucent white with red eye suffusion at posterior end. Young nymphs are mostly aggregated and feed on the inside of the leaf sheath. It is very common to find adults attending the nymphal Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae), Figure 109 Adult corn delphacid, Peregrinus maidis (photo J. Tsai). Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) aggregations in the field. The average size of the first instar measures 1.4 mm long and 0.4 mm wide. The average measurement of second instar is 1.7 mm long and 0.6 mm wide. The average size of third instar is 2.3 mm long and 0.8 mm wide. The fourth and fifth instars measure 2.8 and 4.0 mm long, and 1.2 and 1.7 mm wide, respectively. The morphological characters such as number of tarsomeres on metatarsi and the development of metatibial spur and wingpad are useful in distinguishing the instars. Both adult males and females typically are dimorphic, containing macropterous and brachypterous forms. In rare case, the adult can be completely wingless. P. maidis can be controlled by the use of pesticides that are routinely used for control of lepidopteran pests affecting corn. Most research emphasis is placed on breeding corn hybrids resistant to the viral pathogens instead of the insect vector.  Maize (Corn) Pests and their Management References Bradfute OE, Tsai JH (1983) Identification of maize mosaic virus in Florida. Plant Dis 67:1339–1342 Falk BW, Tsai JH (1998) Biology and molecular biology of viruses in the Genus Tenuivirus. Ann Rev Phytopathol 36:139–163 Tsai JH (1996) Development and oviposition of Peregrinus maidis (Homoptera: Delphacidae) on various host plants. Fla Entomol 79:19–26 Tsai JH, Wilson SW (1986) Biology of Peregrinus maidis with description of immature stages (Homoptera: Delphacidae). Ann Entomol Soc Am 79:395–401 Tsai JH, Zitter TA (1982) Characteristics of maize stripe virus transmission by the corn delphacid. J Econ Entomol 75:397–400 Tsai JH, Steinberg B, Falk BW (1990) Effectiveness and residual effects of seven insecticides on Dalbulus maidis (Homoptera: Cicadellidae) and Peregrinus maidis (Homoptera: Delphacidae). J Entomol Sci 25:106–111 C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) John L. Capinera University of Florida, Gainesville, FL, USA Corn earworm is found throughout North America except for northern Canada and Alaska. In the eastern United States, corn earworm does not normally overwinter successfully in the northern states. It is known to survive as far north as about 40 degrees north latitude, or about Kansas, Ohio, Virginia, and southern New Jersey, depending on the severity of winter weather. However, it is highly dispersive, and routinely spreads from southern states into northern states and Canada. Thus, areas have overwintering, both overwintering and immigrant, or immigrant populations, depending on location and weather. In the relatively mild Pacific Northwest, corn earworm can overwinter at least as far north as southern Washington. Life Cycle and Description This species is active throughout the year in tropical and subtropical climates, but becomes progressively more restricted to the summer months with increasing latitude. In northeastern states dispersing adults may arrive as early as May or as late as August due to the vagaries associated with weather; thus, their population biology is variable. The number of generations is usually reported to be one in northern areas such as most of Canada, Minnesota, and western New York; two in northeastern states; two to three in Maryland; three in the central Great Plains; and northern California; four to five in Louisiana and southern California; and perhaps seven in southern Florida and southern Texas. The life cycle can be completed in about 30 days. Egg Cornea The cuticular part of an eye. Eggs are deposited singly, usually on leaf hairs and corn silk. The egg is pale green when first 1065 1066 C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) deposited, becoming yellowish and then gray with time. The shape varies from slightly dome-shaped to a flattened sphere, and measures about 0.5–0.6 mm in diameter and 0.5 mm in height. Fecundity ranges from 500 to 3,000 eggs per female. The eggs hatch in about 3–4 days. microspines. Although it is easily confused with corn earworm, it rarely is a vegetable pest and never feeds on corn. Close examination reveals that in tobacco budworm larvae the spines on the tubercles of the first, second, and eighth abdominal segments are about half the height of the tubercles, but in corn earworm the spines are absent or up to one-fourth the height of the tubercle. Larva Upon hatching, larvae wander about the plant until they encounter a suitable feeding site, normally the reproductive structure of the plant. Young larvae are not cannibalistic, so several larvae may feed together initially. However, as larvae mature they become very aggressive, cannibalizing other larvae. Consequently, only a small number of larvae (often only one) are found in each ear of corn. Normally, corn earworm displays six instars, but five is not uncommon and seven to eight have been reported. Mean head capsule widths are 0.29, 0.47, 0.77, 1.30, 2.12, and 3.10 mm, respectively, for instars 1–6. Larval lengths are estimated at 1.5, 3.4, 7.0, 11.4, 17.9, and 24.8 mm, respectively. Development time averaged 3.7, 2.8, 2.2, 2.2, 2.4, and 2.9 days, respectively, for instars 1–6 when reared at 25°C. The larva (Fig. 111) is variable in color. Overall, the head tends to be orange or light brown with a white net-like pattern, the thoracic plates black, and the body brown, green, pink, or sometimes yellow or mostly black. The larva usually bears a broad dark band laterally above the spiracles, and a light yellow to white band (Fig. 111) below the spiracles. A pair of narrow dark stripes often occurs along the center of the back. Close examination reveals that the body bears numerous black thorn-like microspines. These spines give the body a rough feel when touched. The presence of spines and the light-colored head serve to distinguish corn earworm from fall armyworm, Spodoptera frugiperda (J.E. Smith), and European corn borer, Ostrinia nubilalis (Hubner). These other common American corn-infesting species lack the spines and have dark heads. Tobacco budworm, Heliothis virescens (Fabricius), is a closely related species in which the late instar larvae also bear Pupa Mature larvae leave the feeding site and drop to the ground, where they burrow into the soil and pupate. The larva prepares a pupal chamber 5–10 cm below the surface of the soil. The pupa is mahogany-brown in color, and measures 17–22 mm in length and 5.5 mm in width. Duration of the pupal stage is about 13 days (range 10–25) during the summer. Adult As with the larval stage, adults (Fig. 110) are quite variable in color. The forewings of the moths usually are yellowish brown in color, and often bear a small dark spot centrally. The small dark spot is especially distinct when viewed from below. The forewing also may bear a broad dark transverse band distally, but Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), Figure 110 Adult of corn earworm, Helicoverpa zea. Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), Figure 111 Corn earworm larva. the margin of the wing is not darkened. The hind wings are creamy white basally and blackish distally, and usually bear a small dark spot centrally. The moth measures 32–45 mm in wingspan. Adults are reported to live for 5–15 days, but may survive for over 30 days under optimal conditions. The moths are principally nocturnal, and remain active throughout the dark period. During the daylight hours they usually hide in vegetation, but sometimes can be seen feeding on nectar. Oviposition commences about 3 days after emergence, continuing until death. Freshsilking corn is highly attractive for oviposition but even ears with dry silk will receive eggs. Fecundity varies from about 500–3,000 eggs, although feeding is a prerequisite for high levels of egg production. Females may deposit up to 35 eggs per day. Host Plants Corn earworm has a wide host range; hence, it is also known as tomato fruitworm, sorghum headworm, vetchworm, and cotton bollworm. In addition to corn and tomato, perhaps its most favored vegetable hosts, corn earworm also attacks artichoke, asparagus, cabbage, cantaloupe, collard, cowpea, cucumber, eggplant, lettuce, lima bean, melon, okra, pea, pepper, potato, pumpkin, snap bean, spinach, squash, sweet potato, and watermelon. Not all are good hosts, For example, a study of relative suitability of crops and weeds in Texas found that although corn and lettuce were excellent larval hosts, tomato was merely a good host, and broccoli and cantaloupe were poor. Other crops injured by corn earworm include alfalfa, clover, cotton, flax, oat, millet, rice, sorghum, soybean, sugarcane, sunflower, tobacco, vetch, and wheat. Among field crops, sorghum is particularly favored. Cotton is frequently reported to be injured, but this generally occurs only after more preferred crops have matured. Fruit and ornamental plants may be attacked, including ripening avocado, grape, peaches, pear, plum, raspberry, strawberry, carnation, geranium, gladiolus, nasturtium, rose, snapdragon, and zinnia. In studies conducted in Florida, corn earworm larvae fed on all 17 vegetable and field crops studied, but corn and sorghum were most favored. In cage tests earworm moths preferred to oviposit on tomato over a selection of several other vegetables that did not include corn. Such weeds as common mallow, crown vetch, fall panicum, hemp, horsenettle, lambsquarters, lupine, morningglory, pigweed, prickly sida, purslane, ragweed, Spanish needles, sunflower, toadflax, and velvetleaf, have been reported to serve as larval. Crimson clover and winter vetch, which may be both crops and weeds, are important early season hosts in Mississippi. Cranesbill species were particularly important weed hosts in this area. In North Carolina, especially important wild hosts are toadflax and deergrass. Adults collect nectar or other plant exudates from a large number of plants. Trees and shrub species are especially frequented. Among the hosts are Citrus, Salix, Pithecellobium, Quercus, Betula, Prunus, Pyrus and other trees, but also alfalfa; red and white clover; milkweed, and Joe-Pye weed and other flowering plants. Damage Corn earworm is considered by some to be the most costly crop pest in North America. It is more 1067 1068 C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) damaging in areas where it successfully overwinters, however, because in northern areas it may arrive too late to inflict extensive damage. It often attacks valuable crops, and the harvested portion of the crop. Thus, larvae often are found associated with such plant structures as blossoms, buds, and fruits. When feeding on lettuce, larvae may burrow into the head. On corn, its most common host, young larvae tend to feed on silks initially, and interfere with pollination, but eventually they usually gain access to the kernels. They may feed only at the tip, or injury may extend half the length of the ear before larval development is completed. Such feeding also enhances development of plant pathogenic fungi. If the ears have not yet produced silk, larvae may burrow directly into the ear. They usually remain feeding within a single ear of corn, but occasionally abandon the feeding site and search for another. Larvae also can damage whorlstage corn by feeding on the young, developing leaf tissue. Survival is better on more advanced stages of development, however. On tomato, larvae may feed on foliage and burrow in the stem, but most feeding occurs on the tomato fruit. Larvae commonly begin to burrow into a fruit, feed only for a short time, and then move on to attack another fruit. Tomato is more susceptible to injury when corn is not silking; in the presence of corn, moths will preferentially oviposit on fresh corn silk. Other crops such as bean, cantaloupe, cucumber, squash, and pumpkin may be injured in a manner similar to tomato, and also are less likely to be injured if silking corn is nearby. Natural Enemies Although numerous natural enemies have been identified, they usually are not effective at causing high levels of earworm mortality or preventing crop injury. For example, in a study conducted in Texas, <1% of the larvae were parasitized or infected with disease. However, eggs may be heavily parasitized. Trichogramma spp. (Hymenoptera: Trichogrammatidae), and to a lesser degree Telenomus spp. (Hymenoptera: Scelionidae), are common egg parasitoids. Common larval parasitoids include Cotesia spp., and Microplitis croceipes (Cresson) (all Hymenoptera: Braconidae); Campoletis spp. (Hymenoptera: Ichneumonidae); Eucelatoria armigera (Coquillett) and Archytas marmoratus (Townsend) (Diptera: Tachinidae). General predators often feed on eggs and larvae of corn earworm; over 100 insect species have been observed to feed on H. zea. Within-season mortality during the pupal stage seems to be important, and although overwintering mortality is often very high, the mortality is due to adverse weather and collapse of emergence tunnels rather than to natural enemies. In Texas, Steinernema riobravis (Nematoda: Steinernematidae) has been found to be an important mortality factor of prepupae and pupae, but this parasitoid is not yet generally distributed. Epizootics caused by pathogens may erupt when larval densities are high. The fungal pathogen Nomuraea rileyi and the Helicoverpa zea nuclear polyhedrosis virus are commonly involved in outbreaks of disease, but the protozoan Nosema heliothidis and other fungi and viruses also have been observed. Management Sampling Eggs and larvae often are not sampled on corn because eggs are very difficult to detect, and larvae burrow down into the silks, out of the reach of insecticides, soon after hatching Moths can be monitored with blacklight and pheromone traps. Both sexes are captured in light traps whereas only males are attracted to the sex pheromone. Both trap types give an estimate of when moths invade or emerge, and relative densities, but pheromone traps are easier to use because they are selective. The pheromone is usually used in conjunction with an inverted cone-type trap. Generally, the presence of five to ten moths per night is sufficient to stimulate pest control practices. Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) Insecticides Corn fields with more than 5% of the plants bearing new silk are susceptible to injury if moths are active. Insecticides are usually applied to foliage in a liquid formulation, with particular attention to the ear zone, because it is important to apply insecticide to the silk. Insecticide applications are often made at 2–6 day intervals, sometimes as frequently as daily. Because it is treated frequently, and over a wide geographic area, corn earworm has become resistant to many insecticides. Susceptibility to Bacillus thuringiensis also varies, but the basis for this variation in susceptibility is uncertain. Mineral oil, applied to the corn silk soon after pollination, has insecticidal effects. Application of about 0.75–1.0 ml of oil 5–7 days after silking can provide good control in the home garden. Trap cropping is often suggested for this insect; the high degree of preference by ovipositing moths for corn in the green silk stage can be used to lure moths from less preferred crops. Lima beans also are relatively attractive to moths, at least as compared to tomato. However, it is difficult to maintain attractant crops in an attractive stage for protracted periods. In southern areas where populations develop first on weed hosts and then disperse to crops, treatment of the weeds through mowing, herbicides, or application of insecticides can greatly ameliorate damage on nearby crops. In northern areas, it is sometimes possible to plant or harvest early enough to escape injury. Throughout the range of this insect, population densities are highest, and most damaging, late in the growing season. Tillage, especially in the autumn, can significantly reduce overwintering success of pupae in southern locations. Biological Control The bacterium Bacillus thuringiensis, and steinernematid nematodes provide some suppression. Entomopathogenic nematodes, which are available commercially, provide good suppression of C developing larvae if they are applied to corn silk; this has application for home garden production of corn if not commercial production. Soil surface and subsurface applications of nematodes also can affect earworm populations because larvae drop to the soil to pupate. This approach may have application for commercial crop protection, but larvae must complete their development before they are killed, so some crop damage ensues. Trichogramma spp. (Hymenoptera: Trichogrammatidae) egg parasitoids have been reared and released for suppression of H. zea in several crops. Levels of parasitism averaging 40–80% have been attained by such releases in California and Florida, resulting in fruit damage levels of about 3%. Host Plant Resistance Numerous varieties of corn have been evaluated for resistance to earworm, and some resistance has been identified in commercially available corn. Resistance is derived from physical characteristics such as husk tightness and ear length, which impede access by larvae to the ear kernels, or chemical factors such as maysin, which inhibit larval growth. Host plant resistance thus far is not completely adequate to protect corn from earworm injury, but it may prove to be a valuable component of multifaceted pest management programs.  Vegetable Pests and Their Management  Maize (Corn) Pests and their Management References Archer TL, Bynum ED Jr (1994) Corn earworm (Lepidoptera: Noctuidae) biology on food corn on the high plains. Environ Entomol 23:343–348 Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp Harding JA (1976) Heliothis spp.: seasonal occurrence, hosts and host importance in the lower Rio Grande Valley. Environ Entomol 5:666–668 Hardwick DF (1965b) The corn earworm complex. Entomological Society of Canada Memoir 40, 246 pp 1069 1070 C Cornicles Neunzig HH (1964) The eggs and early-instar larvae of Heliothis zea and Heliothis virescens (Lepidoptera: Noctuidae). Ann Entomol Soc Am 57:98–102 Oatman ER, Platner GR (1971) Biological control of the tomato fruitworm, cabbage looper, and hornworms on processing tomatoes in southern California, using mass releases of Trichogramma pretiosum. J Econ Entomol 64:501–506 Cornicles Two tubular structures located on the posterior part (fifth or sixth abdominal segment) of an aphid’s abdomen. They vary greatly in structure, and are the source of aphid alarm pheromone. They are also called siphunculi.  Abdomen of Hexapods  Aphids Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) John L. Capinera University of Florida, Gainesville, FL, USA This species may be of Asiatic origin, but now has a world-wide distribution in temperate areas. However, corn leaf aphid does not persist in areas with severe winters, so it dies out from cold areas such as most of Canada, and northern Europe and Asia, and re-invades large areas of temperate regions annually. Life History This species overwinters as viviparous females (displaying parthenogenetic reproduction) in warm winter areas (such as the southern USA). During mild winters, there is evidence that such overwintering may occur in moderately cold winter regions, too (such as the mid-western USA). Overwintering does not occur in cold winter areas (such as most of Canada). Oviparous (egg producing) forms and males are rare, though in Pakistan, eggs overwinter on Prunus sp. The northern areas of North America and southern Canada are thought to be invaded annually, with the timing of invasion and the number of subsequent generations in an area a function of weather. The short life cycle of this aphid, normally 6–12 days, allows production of 20–40 generations per year in such southern locations as Texas and about nine generations in Illinois, but fewer further north. There are 4 instars. The young nymph initially is pea green in color, with red eyes and colorless antennae and legs, and measures about 0.5 mm long. Body length increases to about 0.9, 1.1, and 1.3 mm, the green body color becomes darker, and the appendages gain some dark pigmentation as the nymph progresses through instars 2–4. Mean development times are 4.5, 4.5, 4.5, and 4.7 days, respectively, for instars 1–4 among nymphs destined to grow into apterae, when cultured at 11°C. The corresponding development times for 19 and 29°C are 1.7, 1.8, 1.7, and 1.9 days; and 1.2, 1.2, 1.5, and 1.7 days, respectively. Development times for alatae are quite similar, except that instar 4 tends to require an additional day. The viviparous females generally are bluish green, although they become darker with time, some becoming almost black. Fine white powder covers the entire body. The winged form (alatae) has a black thorax and head, whereas in the wingless form (apterae) only the head is black (Figs. 112 and 113). The winged form also tends to bear three black spots laterally on the abdomen, and the base of the cornicles is enveloped in a small area of purple or black color. In both female forms the appendages are black. The alatae measure about 1.7 mm long, the apterae about 2.4 mm. The adult male aphid measures about 1.5 mm long. The head, thorax, and legs are black. The abdomen is dark bluish green, with a dark spot laterally on each segment. Corn leaf aphid feeds on numerous grasses in addition to corn, and is considered to be a serious pest of cereal grains due to its ability to transmit virus diseases. The crops fed upon, in addition to corn, include barley, chufa, oat, rye, millet, sorghum, Sudan grass, and sugarcane. Barley is the Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae), Figure 112 Winged female corn leaf aphid, Rhopalosiphum maidis (Fitch). C most important early season host. While the leaf blades are rolled, aphid colonies develop within the furled barley leaves. However, once the corn is about 30 days old it also becomes very suitable for aphids; the tassels forming within the furled leaves are particularly suitable for aphid population growth. As the tassel extends, aphids disperse over the entire plant to feed. Among weeds and prairie grasses known to serve as hosts are barnyardgrass, Echinochloa crusgalli; buffalo grass, Buchloe dactyloides; crabgrass, Digitaria sanguinalis; foxtail, Setaria spp.; grama grass, Bouteloua spp.; and Johnson grass, Sorghum halepense. These aphids feed on exposed areas of the plant and often are subject to significant levels of predation and parasitism. Numerous species of ladybird beetles attack corn leaf aphid. Despite their abundance, however, the ladybird beetles generally are numerous and effective predators only after the aphid populations attain high and damaging densities. Other common predators include various flower flies (Diptera: Syrphidae), predatory midges (Diptera: Cecidomyiidae), minute pirate bugs (Hemiptera: Anthocoridae), and lacewings (Neuroptera: Chrysopidae). Several wasps parasitize corn leaf aphid. Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae) is the most widespread and common parasitoid, but Aphelinus varipes (Foerster) (Hymenoptera: Aphelinidae) is an important parasitoid in Texas. Other parasitoids include Diaeretiella rapae (M’Intosh) and Ephedrus persicae (Froggatt) (both Homoptera: Aphidiidae) and Aphelinus asychis Walker (Hymenoptera: Encyrtidae). Damage Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae), Figure 113 Wingless female corn leaf aphid, Rhopalosiphum maidis (Fitch). Corn leaf aphid is commonly found feeding on the tassel and silk of the corn plant in addition to the leaves. It interferes with pollen production and fertilization, resulting in poor kernel fill of the ears. Infestation also can cause a delay in plant maturity, and reduced plant size. Honeydew secreted by the aphids supports growth of sooty mold fungus, 1071 1072 C Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae) causing an unsightly appearance of the ears and interfering with photosynthesis in small grains. In general, crop plants are very tolerant of aphids, and only extremely dense infestations cause injury. If soil moisture conditions are inadequate, however, then the damage by the aphids is increased, and yield reductions are more likely. The ability to transmit plant viruses greatly exacerbates the damage potential of this aphid. Several diseases, including barley yellow dwarf, beet yellows, cucumber mosaic, lettuce mosaic, maize streak, maize dwarf mosaic, and maize stripe are transmitted. Even in crops not successfully colonized by the aphids, corn leaf aphid is implicated in the transmission of numerous stylet-borne viruses. Management Sampling for corn leaf aphids on young leaf tissue is usually done by visual examination of the whorls. As the aphids disperse from the whorls, they are readily apparent on other plant structures. As populations increase and honeydew accumulates, remote detection of aphid populations is possible by examination of photographs taken by aircraft using infrared-sensitive film; sooty mold growing on honeydew impedes the reflectance of infrared radiation. It is advisable to monitor populations in barley early in the season, as incidence in this favored crop may reflect potential incidence in corn later in the season. Populations of alate aphids may be monitored with yellow water pan traps or sticky traps, though aphids collected on sticky traps are often damaged and difficult to identify. Systemic insecticides applied to the young plants or to the soil soon after plant emergence from the soil are particularly effective at controlling aphids. They may be killed by contact insecticides as well, though the increase in crop yield does not justify spraying on some low value grain crops. Early plantings can escape injury, especially in northern areas where aphids do not overwinter. In New York, for example, corn planted before June 10 escape injury by corn leaf aphid and maize dwarf virus, but incidence of aphids and disease increase thereafter. Little work on the management of corn leaf aphid as a virus vector has been reported, other than the assessment of corn varieties for resistance.  Maize (Corn) Pests and their Management References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp Kring TJ (1985) Key and diagnosis of the instars of the corn leaf aphid Rhopalosiphum maidis (Fitch). Southwest Entomol 10:289293. Straub RW (1984) Maize dwarf mosaic virus: symptomatology and yield reactions of susceptible and resistant sweet corns. Environ Entomol 13:318–323 Straub RW, Boothroyd CW (1980) Relationship of corn leaf aphid and maize dwarf mosaic disease to sweet corn yields in southeastern New York. J Econ Entomol 73:92–95 Wildermuth VL, Walter EV (1932) Biology and control of the corn leaf aphid with special reference to the southwestern states. USDA Technical Bulletin 306, 21 pp Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae) James h. tsai University of Florida, Ft. Lauderdale, FL, USA The corn leafhopper, Dalbulus maidis (Delong and Wolcott) is found only in subtropical and tropical areas of America. Its host range is limited to maize and its relatives. Maize (Zea mays L.) is one of the major cereal crops; it ranks third in production following wheat and rice with an average of 380 million tons produced annually on 120 million ha by 53 countries. It is the world’s most widely grown crop in almost all tropical areas of the world including tropical highlands over 3,000 m in altitude, to temperate areas as far north as the 65th latitude. In tropical and subtropical areas of America, maize is often infected with at least three serious phytoplasmal and viral agents. They are known as corn stunt spiroplasma (CSS), maize bushy stunt phytoplasma Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae) (MBP) and maize rayado fino virus (MRFV). These three pathogens are all transmitted by D. maidis in a persistent manner. However, the former two pathogens are known to multiply in the D. maidis. In Florida, corn plants often have been infected by any two of these pathogens. Occasionally, multiple pathogens can be found in the same corn plants in the field. CSS can be acquired by D. maidis in 15 min. All these pathogens require a protracted incubation period in the vector, ranging from 14 to 21 days, depending upon the isolate and titre of pathogen, and biotype and age of vector. The life cycle of D. maidis varies with temperature and host plant. In general, nymphs undergo five instars; an additional instar is often noted. The average developmental times for first through fifth instars range from 12 to 34 days at 10°C, 6 to 13 days at 16°C, 3 to 4 days at 27°C and 2 to 4 days at 32°C. The adult (Fig. 114) longevity averages 67 days for males and 38 days for females at 10°C, 107 days for males and 52 days for females at 16°C, 78 days for males and 30 days for females at 27°C, and 16 days for males and 10 days for females at 32°C. There is a minimum of one day preoviposition period, and it is affected by rearing temperature. The number of eggs oviposited C per day per female averages 4 eggs at 16°C, and 15 eggs at 27°C. The number of eggs laid per female per life averages 402 eggs at 16°C and 611 eggs at 27°C. Other plants such as Tripsacum dactyloides L., Tripsacum sp., Rottboellia exaltata L., Secale cerale L., and Avena sativa L. can be used as temporary feeding hosts, but not for rearing hosts. Besides corn, T. dactyloides var. meridonale is suitable for continuous rearing of D. maidis. Eggs are mainly deposited in the mesophyll tissue of the midrib. The egg is elongate, and curved with a round posterior end. The average size of egg measures 1.04 mm long and 0.25 mm wide. Young nymphs often are found aggregating more on leaves than stems. The average size of instar I through V measures 0.87 mm long and 0.27 wide, 1.14 mm long and 0.37 mm wide, 1.69 mm long and 0.49 mm wide, 2.14 mm long and 0.62 mm wide, 2.82 mm long and 0.81 mm wide, respectively. The average size of male and female measures 2.80 mm long and 0.81 mm wide, and 3.18 mm long and 0.88 mm wide, respectively. D. maidis can be controlled by the use of pesticides that are commonly used for control of lepidopteran pests of corn.  Maize (Corn) Pests and their Management Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae), Figure 114 Adult corn leafhopper, Dalbulus maidis (photo J. Tsai). 1073 1074 C Corn Stunt References Falk BW, Tsai JH (1998) Biology and molecular biology of viruses in the Genus Tenuivirus. Ann Rev Phytopathol 36:139–163 Nault LR, Bradfute OE (1979) Corn stunt: involvement of a complex of leafhopper-borne pathogens. In: Maramorosch K, Harris KF (eds) Leafhopper vectors and plant disease agents. Academic Press, New York, NY, pp 561–586 Tsai JH (1987a) Bionomics of Dalbulus maidis (DeLong and Wolcott). A vector of mollcutes and virus (Homoptera: Cicadellidae). In: Maramorosch K, Raychaudhuri SP (eds) Mycoplasma diseases of crops: basic and applied aspects. Springer-Verlag, New York, NY, pp 209–221 Tsai JH (1987b) Mycoplasma diseases of corn in Florida. In: Maramorosch K, Raychaudhuri SP (eds) Mycoplasma diseases of crops: basic and applied aspects. SpringerVerlag, New York, NY, pp 317–325 Tsai JH, Falk BW (1988) Tropical corn pathogens and their associated vectors. In: Harris KF (ed) Advances in disease vector research. Springer-Verlag, New York, NY, pp 177–201 Tsai JH, Steinberg B, Falk BW (1990) Effectiveness and residual effects of seven insecticides on Dalbulus maidis (Homoptera: Cicadellidae) and Peregrinus maidis (Homoptera: Delphacidae). J Entomol Sci 25:106–111 Corn Stunt A disease transmitted by leafhoppers to maize (corn).  Transmission of Plant Diseases by Insects  Corn Leafhopper, Dalbulus maidis  Juvenile Hormone  Reproduction  Corpus Cardiacum  Nervous System Corpus Cardiacum (pl., Corpus Cardiaca) Small organs between the corpus allata (Fig. 115) that releases PTTH to the hemolymph.  Endocrine Regulation of Insect Reproduction  Reproduction  Corpus Allatum  Nervous System Corpus Pendunculatum A portion of the protocerebral region of the brain, also called “mushroom bodies.” The size of the corpus pendunculatum is correlated with the occurrence of complex behaviors in insects, and seems best developed in social insects.  Nervous System  Learning in Insects  Learning in Insects: Neurochemistry and Localization of Brain Functions Corpora Pedunculata The mushroom bodies of the brain. These are large bilateral integrative centers located in the protocerebrum. They are thought to function in olfactory learning.  Nervous System Corydalidae A family of insects in the order Megaloptera. They commonly are known as dobsonflies and fishflies.  Alderflies and Dobsonflies Corpus Allatum (pl., Corpora Allata) Corylophidae Small endocrine glands behind the brain (Fig. 115), with nervous connections to the brain, and the source of juvenile hormone.  Endocrine Regulation of Insect Reproduction A family of beetles (order Coleoptera). They commonly are known as minute fungus beetles.  Beetles Cosmet Moths (Lepidoptera: Cosmopterigidae) C Corpus Allatum (pl., Corpora Allata), Figure 115 Cross section showing the relationships of the principal endocrine glands with the brain (adapted from Chapman, The insects: structure and function). Cosmetic Damage Superficial injury that affects the appearance, and hence the value of a crop, though leaving the quantity and nutritional value unaffected. Cosmet Moths (Lepidoptera: Cosmopterigidae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Cosmet moths, family Cosmopterigidae, total over 1,540 species worldwide, but the extant fauna may encompass 3,500 species. Three subfamilies are used: Antequerinae, Cosmopteriginae, and Chrysopeleiinae. The family is part of the superfamily Gelechioidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (6–32 mm wingspan), with head smoothscaled; haustellum scaled; labial palpi recurved; maxillary palpi 4-segmented. Wings very linear and with long fringes on hindwings. Maculation varies greatly (Fig. 116) but many have various spots or lines, often with metallic-iridescence. Adults mostly diurnal, but some are crepuscular. Larvae mostly leafminers or needleminers, but some are borers of various plant parts; a few are predaceous on Hemiptera. Hosts are varied but many records are for Leguminosae. Ovovivipary has been recorded in a few species. Some economic species are known. 1075 1076 C Cosmopolitan Costa The basal segment of the leg, articulating with the body. Also the thickened anterior-most vein that forms the anterior margin of the wing.  Legs of Hexapods Cosmet Moths (Lepidoptera: Cosmopterigidae), Figure 116 Example of cosmet moths (Cosmopterigidae), Ithome concolorella (Chambers) from Florida USA. Costal Break A section of the costal vein where the sclerotization is weak or absent, and the vein appears to be broken.  Wings of Insects References Clarke JFG (1965) Cosmopterigidae. In: Clarke JFG (ed) Catalogue of the type specimens of Microlepidoptera in the British Museum (Natural History) described by Edward Meyrick, 5:471–559. British Museum (Natural Hisory), London Hodges RW (1978) Gelechioidea. Cosmopterigidae. In: Dominick RB (eds) The moths of America north of Mexico including Greenland. Fasc. 6.1. E. W. Classey, London, 166 pp, 6 pl Mariani M (1935) Monografie sulle Cosmopteryx d’ Europa. Giornale del Sciencia Naturale Economica Palermo 38:1–54 (1934) Riedl T (1962–69) Matériaux pour la connaissance des Momphidae (Lepidoptera) paléarctiques. Polski Pismo Entomologica, 32:69–75 (1962); 33:101–106 (1963); 35:419–468 (1965); 36:75–84 (1966); (B) 1–2:115–118 (1966); 37:25–46 (1967); 39:635–923 (1969) [mostly Cosmopterigidae] Costal Cell The wing space between the costal and subcostal veins.  Wings of Insects Costal Margin The anterior margin (Fig. 117) of the wing.  Wings of Insects Costs and Benefits of Insects John L. Capinera University of Florida, Gainesville, FL, USA Cosmopolitan Distributed throughout the world, or nearly so. Cossidae A family of moths (order Lepidoptera). They commonly are known as carpenterworm moths, goat moths, and leopard moths.  Carpenterworm Moths  Butterflies and Moths Insects (arthropods) have a well-deserved reputation for significant economic and ecological effects, but there tends to be over-emphasis on negative effects and under-emphasis on beneficial effects. The emphasis on negative effects results from wellknown insect competition with humans for food and fiber resources, and the role of insects in transmitting diseases to humans, domesticated and wild animals, and to crop and forest plants. The negative effects of insects are due not only to their direct damage (usually by feeding) and indirect Costs and Benefits of Insects C Archetype tracheation of wing pad basal fold fulcrum (1C) − Sc + R ∗ costal margin + − (1R1) + − (M) − Μ1+2 + (M4 ) 3A 3A jugal fold jugal notch jugum 2A 1A R5 M2 M3 M4 (1A) P Cu2 anal notch anal margin apex R4 M1 (2M2) (Cu1) (P) (2A) (M1) (M3) (Cu) + 2A + 1J R3 (2R3) (R4) m + 1A + 2J s (R5) (1M2) m-cu (3A) (R2) (1R3 ) r-m Μ3+4 R2 (2R1) r − R2+3 R4+5 (R) + Cu − P axilla R1 (Sc) RS − Sc2 (Scr) R1 M Sc1 (2C) h Cu1 apical margin anal furrow vannus remigium Archetype wing venation Costal Margin, Figure 117 Hypothetical ancestral pattern of wing venation. effects (often by transmission of plant and animal diseases), but by the costs of preventing or reducing damage (Table 21). There is a rich literature purporting to provide documentation of losses attributable to pests, though some of it has been challenged. In contrast, the beneficial effects are less well documented. In part, there has not been much incentive to document the beneficial effects of insects. However, the under-appreciation of insects is also due to the difficulty in assigning monetary value to the benefits derived from insect pollination (next to items of commerce such as silk and honey, probably the best-documented benefit), the decomposition of plant materials and animal dung, the biological suppression of pest insects and weeds, and the role of insects in recreation, or as food for fish and other wildlife. The benefits of insects as food for humans, and in production of silk, shellac, and pigments is worth mentioning, but small in comparison to some other benefits. The Negative Effects of Insects on Crops and Livestock Yield Loss The reduction in crop yields and costs of preventing damage attributable to insects are notoriously difficult to obtain. Even in the USA, where considerable efforts to estimate loss have been made, there is considerable variation among loss estimates, and concern about their reliability. Studies of the major crops conducted in the USA indicate that without insecticides, 50% or more of the major crops could be lost to insects. Generally, crop losses in the USA due to insect and mite pests (with pest control practices) are estimated to be 13–15%, a value of perhaps $35 billion annually (1998 estimate). In developing countries, however, losses are greater, usually 20–30% of preharvest yield, and then additional losses during storage. The cost of pesticides for prevention of crop 1077 1078 C Costs and Benefits of Insects Costs and Benefits of Insects, Table 21 Losses associated with some nonindigenous pests in the USA (adapted from Pimentel et al. 2000). NA signifies information not available Type of organism Losses ($ millions) Control costs ($ millions) Total costs ($ millions) Plants Purple loosestrife NA 45 45 Aquatic weeds 10 100 110 Melaleuca tree NA 3–6 3–6 Crop weeds 23,400 3,000 26,400 Pasture weeds 1,000 5,000 6,000 NA 1,500 1,500 5 NA 5 Feral pigs 800 0.5 800.55 Mongooses 50 NA 50 Rats 19,000 NA 19,000 Cats 17,000 NA 17,000 Dogs 250 NA 250 Pigeons 1,100 NA 1,100 Starlings 800 NA 800 1 4.6 5.6 1,000 NA 1,000 Imported fire ant 600 400 1,000 Formosan termite Turfgrass weeds Mammals Wild horses and burros Birds Reptiles and amphibians Brown tree snake Fishes Arthropods 1,000 NA 1,000 Green crab 44 NA 44 Gypsy moth NA 11 11 13,900 500 14,400 NA 1,500 1,500 2,100 NA 2,100 NA NA 100 Asian clam 1,000 NA 1,000 Shipworm 205 NA 205 21,000 500 21,500 NA 2,000 2,000 2,100 NA 2,100 Crop pests Turfgrass pests Forest pests Molluscs Zebra mussel Microbes Crop plant pathogens Turfgrass pathogens Forest plant pathogens Costs and Benefits of Insects C Costs and Benefits of Insects, Table 21 Losses associated with some nonindigenous pests in the USA (adapted from Pimentel et al. 2000). NA signifies information not available (Continued) Type of organism Losses ($ millions) Control costs ($ millions) Total costs ($ millions) Dutch elm disease NA 100 100 Livestock disease 9,000 NA 9,000 NA 6,500 6,500 Human disease All organisms damage in the USA is estimated at $3 billion annually (2003 estimate). Because about 40% of pests are nonindigenous, their contribution to the loss is estimated at about $15 billion. However, nonindigenous pests are more likely to be serious pests than are indigenous species, so this is likely an underestimate of the effects of invaders. Also, considerable effort is directed to preventing movement of pests from country to country, and in eliminating (eradicating) or suppressing newly arrived pests, so these costs should be added to the losses associated with nonindigenous species. The losses to livestock are estimated to total an additional $9 billion annually. Nonindigenous (Invasive) Pests The monetary cost of only the nonindigenous insect pests affecting the USA was estimated in 2000 to total about 15% of the total cost of nonindigenous organisms. The effects of nonindigenous weeds, mammals, and plant pathogens were each estimated to be greater than the effects of insects, but insects reportedly accounted for more loss than birds, reptiles and amphibians, fishes, molluscs, livestock diseases, and human diseases. Monetary loss due to nonindigenous arthropods is considered to be about $16 billion in both the USA and in India, and is variously considered to represent 40–60% of the losses due to arthropods. Sometimes the damage attributable to nonindigenous species is partitioned according to proportions of indigenous and nonindigenous species in the pest species assemblage. This approach has 136,630 been used, but it likely underestimates the effects of nonindigenous species, which often account for disproportionately large amounts of damage. For example, of the total crop losses attributable to arthropods in three states of the USA, Hawaii, Florida and California, the proportions due to nonindigenous species are estimated to be 98, 95, and 67%, respectively, much higher than the proportions of species that are nonindigenous. The effects of nonindigenous insects are much greater than the simple monetary loss. For example, the woolly adelgid, Adelges piceae (Ratzeburg) (Hemiptera: Adelgidae), has killed about 90% of Fraser fir (Abies fraseri) trees in the southern Appalachian Mountains, disrupting local ecosystems and leading to local shifts in avifauna. In New England, the occurrence of gypsy moth defoliation in oak-dominated forests is apparently contributing to the decline in abundance of Saturniidae and other large summer moths, although it is debatable whether the decline is due to loss of favored food, enhanced abundance of generalist parasitoids, or nontarget effects of gypsy moth suppression. Although biodiversity is obviously affected, it is not possible to affix a monetary value to these changes. Pesticides An important negative effect of pests is the cost of preventing their damage. These costs include the economic, environmental, and health effects of pesticides. The world market for pesticides is estimated at about $31 billion (2005 estimate). The 1079 1080 C Costs and Benefits of Insects USA is the biggest market, both in terms of costs (33%) and amount of active ingredients applied (22%). After North America, the next biggest consumer of pesticides is Southeast Asia, followed by Europe, South America, and finally Africa and the Middle East. However, herbicides are used more extensively than insecticides. The use of insecticides, as measured by amount of active ingredient, is about 20% of all pesticide use. In North America, insecticide use in agriculture has been decreasing for some time due to both the shift to products that are effective at lower rates of application, and the recognition that overuse of insecticides has many detrimental effects. In many other areas of the world, however, insecticide use continues to increase. The cost of insecticides used worldwide is $7.7 billion (2005 estimate), about 25% of the cost of all pesticides. For comparison, the cost of other pesticides (in $ billions) is herbicides, 14.8; fungicides, 7.5; and other, 1.1. Nearly everywhere, the agricultural sector is the principal consumer of pesticides. In the USA, for example, agriculture uses about 77% of the pesticides applied, whereas the urban pest control industry (structural, building interiors, and landscape) and government use about 14%, and consumer use (self-applied home and garden) is only about 9%. The Negative Effects of Insects on Wildlife Biting and Stinging Insects can be detrimental to wildlife due to direct effects (biting, stinging, disease transmission) or indirect effects (nontarget effects of insecticides). Blood feeding by mosquitoes (Diptera: Culicidae), deer flies (Diptera: Tabanidae), ticks (Acarina: Ixodida) and other wildlife parasites undoubtedly causes considerable annoyance, and sometimes determines suitability of habitat or affects feeding behavior. For example, birds have been known to abandon their nests and fledglings due to the abundance of blood-feeding ticks or mites, and many ticks can cause paralysis of mammals. Predation of ground-nesting bird nestlings, sea turtle eggs, and other small wildlife by red imported fire ant, Solenopsis invicta Buren, is of considerable concern in the southeastern USA, as is predation by Argentine ant, Linepithema humile (Mayr) (formerly Iridomyrmex humilis Mayr), on the west coast of the USA. Disease Transmission Of particular importance to wildlife is the transmission of diseases by arthropods. Eastern equine encephalitis is an example of a common wildlife disease transmitted by mosquitoes. Found in eastern North America and south to Argentina and Peru, the disease is due to a virus that is harbored most commonly in passerine and other perching birds, which serve as the amplification hosts. Mosquitoes feeding on these birds when they are viremic obtain high concentrations of virus in the ingested blood, and in turn become infected. Upon feeding on other birds, the mosquitoes transmit the disease. Wildlife differ greatly in susceptibility. Nonindigenous species such as pheasants, chukar partridge, and pigeon are most susceptible, but an endangered native bird, whooping crane, readily succumbs to the disease. Symptoms of infection can include lethargy and lack of coordination; surely such animals are more susceptible to predation even if they survive infection. Other examples of diseases affecting wildlife include tularemia (rabbit fever) caused by Francisella tularensis, which is transmitted by tick and insect bites and infects over 100 species of mammals and 25 species of birds; bubonic plague caused by Yersinia pestis, which is transmitted by fleas to rodents, rabbits and other mammals; Lyme disease caused by Borrelia burgdorferi, which is transmitted by Ixodes ticks to deer, mice, bats, squirrels, weasels, and others, including reptiles and birds; and West Nile virus caused by a flavivirus, and which is transmitted by mosquitoes to 250 species of birds and 18 species of mammals. Costs and Benefits of Insects Pesticides Insects can be considered detrimental to wildlife by virtue of stimulating use of insecticides; exposure to pesticides can be deleterious to all wildlife, but particularly to birds. A simple example is the presence of seed-feeding flies, Delia spp. (Anthomyiidae), which damage crop seeds planted in the spring. To prevent damage by insects while the seed is germinating, coatings containing insecticides are commonly applied to seeds before they are planted. Seed treatment with insecticides (and often fungicides) not only protects the germinating seed, but if the insecticide acts systemically it may also impart protection to young plants, particularly from piercing-sucking insects such as aphids. Unfortunately, birds will often feed on seeds that have been recently planted, and thereby ingest a lethal dose of insecticide. Another problem results from broadcast application of granular insecticides to the soil surface. Probably because sand is sometimes consumed by birds to aid in grinding up seeds, birds sometimes feed on granular insecticide, again resulting in bird mortality. Lastly, application of liquid insecticides sometimes results in a lethal dose of insecticide being applied directly to wildlife. Though this seems unlikely, when aircraft are used to apply insecticides, extensive land area is treated quickly and wildlife may not have adequate time to escape. Not only are crop fields treated, but often adjacent border areas (hedge rows, fence rows, irrigation ditches, road margins) are treated deliberately or inadvertently. In the case of nestling birds, there is no opportunity to avoid exposure. There is also a problem with birds flying into fields that were recently treated, perhaps to feast on dying insecticide-containing insects, thereby ingesting a lethal dose of insecticide. Other vertebrates are not immune to such poisoning, but it is most pronounced in avifauna and fish. The United States Fish and Wildlife Service estimates that over 670 million birds are exposed to pesticide on farmlands in the USA, and that about 10% die immediately as a result. This does not include those that are sickened and die C later, or eggs left unhatched or nestlings left to starve. Organophosphate and carbamate insecticides are most commonly implicated. The use of persistent lipophilic insecticides, which tend to accumulate in animals that are higher on the food chain, has long been known to affect hatching success in predatory birds (raptors). The widespread use of DDT, in particular, was linked to production of abnormally thin egg shells and subsequent declines in successful raptor reproduction. DDT and related products interfere with calcium metabolism. Less well known, but not at all surprising, are the effects of DDT and dicofol on alligators. Male alligators living in Lake Apopka, Florida, have low testosterone levels. Lake Apopka was the site of a DDT and dicofol (which is closely related to DDT) spill, and the insecticides had estrogen-like effects, resulting in feminization of the males. The penises of male alligators were 25% smaller, bone density was affected in females, and egg hatching was reduced. Alligator numbers plummeted in the years after the pesticide spill. DDT was widely used before its adverse effects were fully appreciated, and though its use is prohibited in many areas of the world, it remains in use elsewhere due to its effectiveness, persistence, and low cost. Birds that migrate long distances may move into and out of countries where DDT is used, so it remains a continuing threat even where it is not currently used. The benefits of DDT to humans are not trivial, especially in countries plagued by malaria and other mosquito-vectored diseases, so there remains considerable interest in continuing its use. Consequently, there is extensive literature for and against DDT. Although the use of DDT has attracted considerable attention as a disruptor of wildlife populations, its direct toxicity is quite limited. Certain cyclodiene insecticides, particularly heptachlor, dieldrin and aldrin, are similarly persistent and more toxic. Indeed, it is the cyclodiene insecticides that accounted for most of the direct mortality to birds in the 1950s–1960s, not DDT. Generally, use of DDT, cyclodienes, and similar 1081 1082 C Costs and Benefits of Insects lipophilic products that accumulate in wildlife has declined greatly. Where use of these products has been reduced, wildlife populations have recovered. Pesticide use also affects wildlife indirectly, and these indirect effects may be more important than the direct exposure of wildlife to insecticides. One important indirect effect is the depletion of insect populations caused by insecticide use. Broad-spectrum insecticides cause treated fields to become almost sterile, and if the products are persistent the fields may remain depleted of insect life for weeks. Birds will attempt to compensate for loss of insect food by foraging elsewhere, but there are limits as to how far they can fly and then return regularly to a nest with food for nestlings. If the distance is too great, the nest will be abandoned. Due to the high cost of insecticide development and registration, agrochemical companies favor development of broad-spectrum products because, once registered, they can be used extensively and generate large profits before the patent expires. The nonselective nature of such products is particularly damaging to bird populations; if only the pests were affected, some insect fauna would remain to support bird life. Another indirect effect of pesticides on wildlife is the change in floral diversity (loss of edible weeds, weed seeds, or fungi, and also depletion of habitat or cover) caused by herbicide (and to a lesser degree by fungicide) application. Grass and weed seed can be an important food resource, and clean culture of crops – though beneficial in terms of plant growth efficiency, energy efficiency and water conservation – can greatly reduce food abundance for bird life. This problem is exacerbated by the ever-increasing scale (field size) in agriculture, which usually results from merging smaller fields, reducing crop heterogeneity, and in destroying hedge-row and other border area habitat. The results of the combined effects are often dramatic. In Britain, for example, two-thirds of farmland bird species have shown declines in abundance. The Negative Effects of Biting Pests and Vectors of Human Disease Many people are killed annually by diseases that are vectored by arthropods, and even more suffer chronic infections that impair their ability to work efficiently and live normal lives. Probably the top arthropod-transmitted diseases are malaria, leishmaniasis, sleeping sickness, lymphatic filariasis, and dengue. These also are among the most important diseases in tropical areas of the world. Some of the important arthropod-transmitted diseases, the vector, and human pathogen are: African relapsing fever (Ornithodorus spp. (Borrelia spp.) Amoebic dysentery (Musca domestica) (Entamoeba histolytica) Chagas’ disease (Triatoma spp.) (Trypanosoma cruzi) Cholera (flies) (Vibrio cholerae) Dengue (Aedes aegypti) (virus) Encephalitis (mosquitoes) (virus) Epidemic fever (Pediculus humanus) (Rickettsia prowazeki) Epidemic relapsing fever (Pediculus humanus) (Borrelia recurrentis) Filariasis (mosquitoes) (Wuchereria bancrofti) Sleeping sickness (Glossina spp.) (Trypanosoma spp.) Leishmaniasis (Phlebotomus spp.) (Leishmania spp.) Loasis (Chrysops spp.) (Loa loa) Lyme disease (ticks) (Borrelia burgdorferi) Malaria (Anopheles spp.) (Plasmodium spp.) Murine typhus (Xenopsylla cheopis) (Rickettsia typhi) Onchocerciasis (Simulium spp.) (Onchocerca volvulus) Plague (Xenopsylla cheopis) (Pasturella pestis) Rocky Mountain spotted fever (ticks) (Rickettsia rickettsii) Scrub typhus (Trombicula spp.) (Rickettsia tutsugamushi) Trench fever (Pediculus humanus) (Rickettsia quintana) Tularemia (Chrysops spp.) (Francisella tularensis) Typhoid fever (flies) (Salmonella typhi) Yaws (flies) (Treponema pertenue) Yellow fever (Aedes aegypti) (virus) Likely the most important arbovirus is dengue, which is found throughout the world in Costs and Benefits of Insects tropical areas. According to the USA’s Centers for Disease Control and Prevention (CDC), as of 2005 tens of millions of people were being infected, and tens of thousands of people were contracting dengue hemorrhagic fever. Though dengue usually is not lethal, the closely related but more severe dengue hemorrhagic fever can be very dangerous, often resulting in mortality of about 5% of its victims. Yellow fever remains an important arbovirus in the tropics, with perhaps 200,000 cases per year, and 30,000 deaths. Similarly, Japanese encephalitis causes about 40,000 cases per year, inflicting 10–15,000 deaths annually in Asia. West Nile virus recently gained access to North America, and though only a few thousand people have contracted this disease thus far, like other encephalitis diseases, survivors often suffer significant neurological impairment. Malaria remains the most important insect-vectored disease, infecting 300–500 million people per year, and resulting in about one million deaths per year. The economic and sociological consequences of this disease are devastating. Domestic animals are a very important source of food and companionship for humans, and they also can succumb to diseases transmitted by arthropods. Among the important diseases of domesticated animals, the vector, and the animal pathogen are: African horse sickness (Culicoides spp.) (virus) Anthrax (Musca domestica) (Bacillus anthracis) Blue tongue of sheep (Culicoides spp.) (virus) Cattle filariasis (blackflies) (Onchocerca gutturosa, etc.) Dirofilariasis (mosquitoes) (Dirofilaria spp.) Fowl spirochaetosis (Dermanyssus gallinae) (Borrelia anserina) Heartwater of cattle (Amblyomma hebraeum) (Rickettsia ruminantium) Mal de caderas (Stomoxys calcitrans) (Trypanosoma equinum) Nagana (Glossina spp.) (Trypanosoma spp.) Surra (Tabanidae) (Trypanosoma evansi) Texas cattle fever (Boophilus annulatus) (Babesia bigemina) C The Negative Effects of Urban (Structural, Household, and Landscape) Pests Urban pests are among the most important because they affect so many people, not only those in rural/agricultural environments. Also, the pesticide market for structural, household and landscape pests is large and unusually lucrative for pesticide companies. Thus, pesticide use is actively promoted at the same time that major efforts are under way to reduce pesticide use in crops. In some cases there is justification for pest control in the urban environment, particularly in the case of termite and red imported fire ant control. Other examples of important urban pests, and the basis of their importance, include cockroaches (mostly a sanitation issue), flies (sanitation), household ants (sanitation), stored grain insects (sanitation), carpet beetles and clothes moths (damage to wool products), lice and fleas (human and pet health), and turf and ornamental plant pests (aesthetics). Termites can be extremely destructive by attacking wood buildings, compromising their structural integrity. Even buildings constructed largely of concrete can be damaged because subterranean termites will tunnel over concrete to get to wood roof supports, and because drywood termites and some subterranean termites will alight on roofs and attack from above. In addition to structural materials, damage may be inflicted to cabinetry, furniture, and wood paneling and trim. Damage by termites is a severe problem in all but the northernmost climates, but is especially acute in warmer areas because termites are active for longer periods of time. The economic effect of termites is estimated at $5–6 billion per year (2006 estimate) in the USA, with most of the damage occurring in the warmweather, southern states from Florida to California, and also in Hawaii. Arthropods living indoors, such as house dust mites and cockroaches, can be an important source of allergens. Cockroach allergens are proteins shed 1083 1084 C Costs and Benefits of Insects by cockroaches, and also found in their feces. Exposure by children to cockroach allergens is believed to be a major risk factor for asthma. Currently, about 20% of American children are allergic to cockroach allergens, and asthma rates are particularly high in inner-city areas where cockroach problems frequently occur. Such children miss more school and have more hospitalizations for asthma. Cockroach allergy is not limited to children, however. In addition to allergy/asthma issues, about $200 million is expended annually in the USA for cockroach suppression in homes and businesses, particularly in the food/restaurant industries. Red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), is an interesting and complex case because not only is it a very important urban pest, but it also affects agricultural and natural environments, and even has beneficial aspects. A native of South America, it entered the USA without its natural enemies and has proliferated largely unchecked. Because it stings, it threatens the lives of people, pests, livestock and wildlife. The economic effect in the USA is estimated at $5.6 billion per year, with the principal impacts being to residential households ($3.6 billion), disruption of electric and communication systems ($637 million), crop destruction ($428 million), golf course damage and treatment ($318 million), and effects on schools and school yards ($130 million) (2004 estimates). Other ants can be a nuisance, and carpenter ants can cause structural damage, but none approach the impact of S. invicta. On the other hand, S. invicta is an effective predator of insects, and in some cropping systems such as sugarcane, this species contributes significantly to the biological suppression of other pest species. The Benefits of Pollination and Honey Production Pollination Pollination is accomplished by insects, vertebrates (birds and bats), and wind, but certain crops are mostly dependent on insects, and bees in particular, for successful pollination. Notable among crops requiring pollination are most fruits and nuts, many vegetables, and a few field crops. The grain crops, including corn (maize) are wind-pollinated. Wild pollinators can be quite important for plants requiring insect pollination, and may be completely effective for isolated plants or small fields. However, in modern crop production the high density of crops and the long distance of crops from uncultivated areas may limit the ability of wild pollinators to effectively provide pollination of crop plants. Therefore, hives of bees (usually Hymenoptera: Apidae and specifically Apis mellifera) are often moved adjacent to the crops requiring pollination. In the USA, about 2.5 million hives were rented for pollination services in 1999, clearly indicating the importance of pollination. Nearly 85% of the rentals occurred in only seven crops (in descending order of importance): almond, apple, melons, alfalfa seed, plum/prune, avocado, and blueberry. Estimates of the dependence of crops on pollination, and the proportion of pollination accomplished by wild pollinators versus domesticated honey bees, are shown in Table 22. Note that dependence varies considerably from crop to crop, and even within related crops (e.g., compare grapefruit to lemon, which are both citrus crops). The value of pollination is estimated at over $3 billion in the USA alone (2001 estimate), though there are earlier estimates of $5.7 billion in pollination benefits. Though this is a small value relative to the total value of crops, these insect-pollinated crops account for important diversity in our diet. Imagine subsisting on corn, wheat and barley, spiced up with an occasional potato; a bland diet, indeed! The benefits of fruit and vegetables are considerable, both for nutrition and appetite. However, some caution should be used in interpreting pollination data. Sometimes “insect pollinated crops” can be produced without pollination. Thus, with asparagus, carrots and alfalfa (for example) a crop can be obtained in Costs and Benefits of Insects Costs and Benefits of Insects, Table 22 The value of crop production in the USA resulting from pollination, 2001–2003, in relation to the source of pollinators (adapted from Losey and Vaughn, 2006) Crop Mean annual value ($ millions) Dependent on Domesticated pollination (%) nonindigenous bees (%) Indigenous bees (%) Mean value from indigenous bees ($ millions) Fruits and nuts Almond 1120.0 100 100 10 158.51 Apple 1585.1 100 90 20 4.2 Apricot 30.0 70 80 10 38.24 Avocado 382.4 100 90 10 2.31 23.1 100 90 10 19.29 192.9 100 90 10 0.31 3.9 80 90 10 0.31 290.6 90 90 10 26.15 56.3 90 90 10 5.07 Grapefruit 278.4 80 90 10 22.27 Lemon 286.1 20 10 90 51.50 2.0 30 90 10 0.06 Orange 1713.6 30 90 10 51.41 Tangelo 10.8 40 90 10 0.43 112.0 50 90 10 5.60 6.1 30 90 10 0.18 159.7 10 90 10 2774.8 10 10 90 249.73 16.7 90 90 10 1.50 158.0 50 80 20 15.80 Blueberry, wild Blueberry, cultivated Boysenberry Cherry, sweet Cherry, tart Citrus Lime Tangerine Temple Cranberry Grape Kiwifruit Loganberry Macadamia 15097 31.1 90 90 10 2.80 121.2 60 80 20 14.54 Olive 66.5 10 10 90 5.99 Peach 487.9 60 80 20 58.55 Pear 263.9 70 90 10 18.47 Plum & prune 197.8 70 90 10 13.85 95.8 80 90 10 7.19 1187.6 20 10 90 213.77 Asparagus 164.3 100 90 10 16.43 Broccoli 543.4 100 90 10 54.34 Carrot 575.5 100 90 10 57.55 Nectarine Raspberry Strawberry Vegetables C 1085 1086 C Costs and Benefits of Insects Costs and Benefits of Insects, Table 22 The value of crop production in the USA resulting from pollination, 2001–2003, in relation to the source of pollinators (adapted from Losey and Vaughn, 2006) (Continued) Crop Mean annual value ($ millions) Dependent on Domesticated pollination (%) nonindigenous bees (%) Indigenous bees (%) Mean value from indigenous bees ($ millions) Cauliflower 219.8 100 90 10 21.98 Celery 256.5 100 80 20 51.30 Cucumber 379.5 90 90 10 34.16 Cantaloupe 401.0 80 90 10 32.08 Honeydew 94.1 80 90 10 7.53 808.0 100 90 10 80.80 75.5 90 10 90 61.16 192.3 90 10 90 155.76 61.0 100 90 10 6.10 Onion Pumpkin Squash Vegetable seed Watermelon 315.9 0.7 0.9 0.1 22.11 Field crops Alfalfa hay 7212.8 100 95 5 360.64 Alfalfa seed 109.0 100 95 5 5.45 Cotton lint 3449.5 20 80 20 137.98 Cotton seed 689.3 20 80 20 27.57 Legume seed 34.1 100 90 10 3.41 793.1 10 20 80 63.45 0.3 100 90 10 0.03 15095.2 10 50 50 754.76 Peanut Rapeseed Soybean Sugar beet 1057.3 10 20 80 84.58 Sunflower 312.7 100 90 10 31.27 Total the absence of pollinators, but they require pollinators for propagation (seed production). A relatively small area of carrots, if properly pollinated, can produce enough seed for all the carrots grown as vegetables. In the case of alfalfa, the crop can be harvested several times per year, and for several years, before replanting. The extreme case is asparagus, which is normally harvested for a decade before replanting. Thus, although the existence of these crops (and many others) is dependent on insect pollination, the production of any particular field may not 3074.13 require the presence of pollinators. In contrast, for other crops (e.g., apple, avocado, and blueberry) every fruit harvested requires visitation by an insect pollinator. We take for granted that pastures and prairies will be populated by wildflowers. A spring walk through woodlands is a wonderful way to see small herbaceous plants in their full glory. And what would a tropical landscape be without a profusion of flowers? Without insects to perform pollination services, these and many other environments would seem sterile, lacking Costs and Benefits of Insects in the bright colors we normally expect in our landscapes. Most plants that produce colorful flowers do so to attract insects, and without these pollinators the plants would decline or disappear. Biodiversity would decline tremendously, and highly coevolved systems, such as some orchids, would certainly disappear. It is difficult to assign economic or even aesthetic values to the loss of insect pollination, but it certainly would represent a very different world than we now enjoy. Honey Honey is an important by-product of pollination. At one time, honey production was more important; farmsteads routinely produced their own supply of sweetener from their own hives. Later, an industry grew up to supply honey, often manned by migratory beekeepers who kept hundreds or thousands of hives and followed the availability of nectar for their bees. While this still occurs to some extent, in many instances the importance of honey has been supplanted by other sweeteners (from sugar cane, sugar beet, or corn). Nevertheless, honey production is an important supplement to pollination services for many beekeepers, and the only product for some. The value of honey produced in the USA was $157 million in 2005, coming from 2.4 million colonies. But about 60%of the honey consumed in the USA was imported from other countries, so this value underestimates its importance. World honey production in 2005 was estimated by the Food and Agriculture Organization of the United Nations to be slightly over 1.4 billion kg. Production has increased steadily over the last decade or so, with most of the increases coming from Asia and South America, while honey production in the USA continues to decline, along with the number of beekeepers and colonies of bees. It is difficult to estimate the value of honey throughout the world due to differing currencies, but it likely was about $3 billion in 2005. C The Benefits of Animal Dung Decomposition Although it is difficult to estimate the benefits of insect decomposition of plant products, in a qualitative sense it is certain that insects speed up plant matter decomposition, allowing more light to reach the forest floor and increasing the rate of nutrient recycling. By hastening the demise of senescent vegetation, especially trees, insect decomposers allow the forests to boost productivity. Averaged across ecosystems, insects consume about 5% of available (not including woody tissues) biomass. Thus, herbivores can affect ecosystem productivity by regulating the rate of energy input. Saprophytic species (feeding on feces and honeydew) cannot directly affect primary productivity, but can regulate it indirectly by affecting the rate of nutrient recycling. Feces and honeydew allow premature release of nutrients, boosting nitrogen flow to the plants. One aspect of decomposition that has been studied is consumption of dung by insects, particularly by dung beetles (Scarabaeidae: Scarabaeinae). Cattle produce large quantities of dung, about 9,000 kg (about 21 cubic meters) per animal per year. Scarab beetles are quite efficient at decomposing this waste, which otherwise smothers vegetation, fouls vegetation leading to avoidance by grazing animals, and ties up nitrogen in an unusable form. Decomposition also reduces the breeding of parasites and nuisance and biting flies that would otherwise breed in the dung. The accelerated decomposition of dung by dung beetles in the USA is estimated to provide at least $380 million in benefits annually (2006 estimate). The economic benefits attributable to specific actions include reduction in fouling of forage, $122 million; reduced volatilization of nitrogen, $58 million; reduced parasitism, $70 million; and reduced numbers of pest flies, $130 million. Dung beetle activity is not as great in the USA as it is in many other countries due to the animal husbandry practices of the USA. Specifically, large numbers of cattle are pastured in feedlots (beef cattle) or on concrete (dairy 1087 1088 C Costs and Benefits of Insects cattle) rather than on rangeland, and dung beetles do not inhabit these areas. Also, over half of the cattle in the USA are treated with avermectin pesticides to control parasites, and the avermectin residues in the dung inhibits development of dung beetles. Thus, the benefits due to dung beetles are likely considerably greater in countries that maintain their livestock in pastures or do not treat with avermectins. The benefit of dung beetles is perhaps best seen in Australia, a continent that lacked mammals (and mammal dung) until cattle were introduced during settlement by Europeans in 1788. The abundance of cattle in Australia (about 20 million currently) produces an abundance of dung that is slow to decompose, which allows bush fly, Musca vetustissima Walker (Diptera: Muscidae), to breed in huge numbers in the dung. Marsupial dung, the natural food source of bush fly, is much smaller and tends to dry out quickly and become unsuitable for fly larvae. To deal with the reduction in pasture by the slowly decomposing dung, and to reduce fly breeding, many species of dung beetles from Africa and Europe were introduced. The result has been an 80% reduction of bush flies. This approach has only recently been extended to target dog dung, a problem in urban areas. Losses attributed to forage fouling are derived from the concept that cattle will not, or cannot, consume forage covered with dung. Studies conducted in California, USA, determined that the presence of dung beetles would increase the decomposition rate of dung by about 20%. Projected over cattle on pasture and rangeland throughout the country, it is possible to estimate a $122 million saving due to dung beetles. This assumes that stocking rates are optimized to use all food. However, this is not always a realistic assumption. The California data may not be applicable universally. In Australia, for example, the benefits are much greater because dung retention time was reduced from as long as four years to as little as 48 h. Drying of dung causes marked reduction of its inorganic nitrogen content, with the nitrogen being released into the atmosphere. In contrast, if the dung is incorporated into the soil, the nitrogen is available to plants and thus functions as a fertilizer. The difference is considerable, about an 80% difference in nitrogen content. The enhanced plant growth associated with incorporation of dung into the soil by dung beetles is estimated to increase available forage by about $58 million per year in the USA. As in the previous example, this is only true if the stocking rate is adjusted appropriately to take advantage of the additional forage. The availability of dung allows survival of parasites and pests, and reducing the longevity of the dung should reduce survival of the parasites and pests as well. The economic benefits have been calculated to be $70 million and $380 million per year, respectively, in the USA. As noted earlier, however, avermectins are widely used in the USA, so the benefit of beetles might be better in regions not using these pesticides. Also, these calculations are based only on beef cattle, but benefits also accrue to other livestock such as dairy cattle, horse, goats, and sheep, so these certainly are low estimates of the economic benefit of dung beetles. The Benefits of Insects for Recreation Insects are quite important as food for wildlife populations that, in turn, support recreational activities such as hunting, fishing, and wildlife viewing. The importance of insects relative to wildlife populations is often overlooked, except for freshwater fish, where there is considerable appreciation for the role of insects in supporting fish populations. The importance of wildlife in technologically advanced countries is often limited mostly to recreation, and the analyses reported below (2005 estimates) relate only to such values, and are limited to calculations made only for the USA. However, in some parts of the world wildlife is an important part of the human diet, so the effects of insects would be proportionally greater in such locations. Small game, but not large game, is often critically dependent on insects for food. Chicks of such popular game birds as pheasant, quail and grouse Costs and Benefits of Insects cannot survive without insects as a nutritional resource. Therefore, the economic effects of insects, based on the proportion of expenditures related to hunting these birds, is about $1.48 billion annually in the USA (Table 23). Waterfowl also eat insects, but to a lesser degree than the terrestrial species. Thus, the economic effect of insects as food for waterfowl is estimated at only $0.58 billion. Other vertebrates that are popular with hunters, such as squirrels and raccoons, also consume insects as part of their diet, but their contribution to the hunting economy has not been calculated. The majority of freshwater fish are insectivorous, so the entire value of the freshwater fishing (recreational fishing) economy can be attributed to insects (Table 24). This value is $27.9 billion. Although saltwater fish are not normally thought of as insectivorous, about 25 species spend part of their life in freshwater habitats where they feed on insects. If the proportion of the marine fisheries (commercial fishing) due to these species is calculated, it represents about $0.22 billion. Wildlife watching is an important form of recreation, and birdwatching is central to wildlife observation. Wildlife viewers often also appreciate opportunities to view small mammals, reptiles and amphibians, which often use insects as well, and many make efforts to view insects. Nevertheless, the benefits of wildlife watching are calculated only on the basis of birdwatching, and only on the basis of species of North American birds that are primarily insectivorous. Thus, this is a very conservative estimate, but still accounts for an economic impact of $19.8 billion. The Benefits of Biological Control by Insects As noted previously, insecticides are often used to suppress pests and their damage, and this is a costly undertaking. However, pest control would be vastly more expensive were it not for control of insects by their natural enemies, principally other insects. As with other estimates of insect effects, it is difficult to C assess the benefits of natural biological control. However, it has been estimated that 65% of insects are being maintained in a non-damaging status relative to their host plants by the action of natural enemies, and only about 7% attain damaging levels (the others do not feed on plants). In the USA, the benefit (in 2005) of beneficial insects (predators and parasitoids) to cropping systems has been calculated to be about $4.5 billion annually, whereas the benefits due to the actions of other factors (insect diseases, weather, etc.) working in conjunction with beneficial insects totals about $13.6 billion. Other Benefits of Insects Silk production (sericulture) Silk is produced by special glands (generally modified salivary glands) in the larvae of some Lepidoptera, and by other structures in some immatures and adults of mites and spiders. Only moth larvae, however, have been exploited by humans for their ability to produce silk commercially. The silk naturally serves various functions, such as larval dispersal in the wind, leaf rolling, anchoring of pupae, and construction of cocoons. It is this latter function, which consists of production of a single long strand of silk, which allows the silk to be unwound from the pupal case and harvested. In different parts of the world, various species have been used to produce silk, but generally it involves insects of the superfamily Bombycoidea, and particularly Bombyx mori L. Silk has been harvested by humans from Bombyx mori at least since 2600 B.C. It was one of the first, and most valuable, trade commodities between China and Europe. Though originating in China, once the insect was smuggled out of China it was quickly spread around the world, where its cultivation was limited only by the ability to produce mulberry trees, its natural host. Besides China, Japan and India are the most important production centers. Now it can be produced on artificial diet as well. Silk is a valuable commodity, valued at over $1 billion annually. 1089 1090 C Costs and Benefits of Insects Costs and Benefits of Insects, Table 23 Insectivory in North American bird species (adapted from Losey and Vaughan, 2006) Order Common name Gavliiformes Loons No. species No. primarily insectivorous No. partially insectivorous No. not insectivorous 5 0 5 0 Podicipediformes Grebes 7 5 2 0 Procellariiformes Tubenoses 6 1 4 1 Pelicaniformes Pelicans & allies 11 0 5 6 Ciconiiformes Herons & allies 20 5 12 3 Phoenicopteriformes Flamingos 1 1 0 0 Anseriformes Waterfowl 44 19 24 1 Falconiformes Vultures, hawks, & falcons 31 3 18 10 Galliformes Quail, grouse & allies 22 2 20 0 Gruiformes Cranes & allies 13 8 5 0 Charadriiformes Shorebirds & gulls 108 51 22 35 Columbiformes Pigeons & doves 11 0 3 8 Cuculiformes Cuckoos & roadrunners 6 6 0 0 Strigiformes Owls 19 6 11 2 Caprimulgiformes Goatsuckers 8 8 0 0 Apodiformes Swifts & hummingbirds 20 6 14 0 Trogoniformes Trogons 1 1 0 0 Coraciiformes Kingfishers 3 0 1 2 Piciformes Woodpeckers 22 22 0 0 Passeriformes Perching birds 285 251 34 0 643 395 180 68 61 28 11 Total % Shellac Several scale insects (Hemiptera: Kerriidae) can be grown on trees in Southeast Asia and used as a source of lac, a resin that is the principal ingredient of shellac. Laccifer lacca Kerr is the species most commonly cultured for this purpose. India produces the largest proportion of the shellac on the world market, though production has fallen greatly due to the availability of synthetic resins. Costs and Benefits of Insects C Costs and Benefits of Insects, Table 24 Value of commercially landed fish that rely on insects as a critical nutritional resource (adapted from Losey and Vaughan, 2006) Species Fish weight (kg landed) Fish value ($) 1,675,935 384,968 15,473,230 9,504,673 Mullet, white 509,887 241,064 Mullets 444,000 310,680 Mummichog 4,590 13,221 Perch, white 2,482,006 1,082,354 Alewife Mullet, striped Perch, yellow 1,714,342 2,914,078 Salmon, chinook 27,345,066 32,633,445 Salmon, chum 92,031,758 16,900,456 Salmon, coho 32,256,133 15,261,440 176 538 Salmon, pink 334,080,474 24,758,990 Salmon, sockeye 184,505,904 109,897,597 Shad, American 2,074,686 1,190,072 Shad, gizzard 5,306,259 700,916 Shad, hickory 88,339 23,199 1,081,152 160,842 Smelt, rainbow 489,467 730,685 Smelts 480,212 150,728 Suckers 157,164 45,384 Tilapias 5,482,778 1,223,061 Trout, lake 558,129 228,773 Trout, rainbow 308,306 189,625 25,810 42,396 8,604,823 6,048,110 Salmon, Pacific Smelt, eulachon Walleye Whitefish, lake Total – Dyes Commercially important dyes have been extracted from insects. Probably best known is cochineal dye, obtained from the bodies of cochineal scales, Dactylopius coccus (Hemiptera: Dactylopiidae). Cultivated on Opuntia cactus, it can be used to 224,637,295 produce a bright red dye that once was very popular, declined in importance as synthetic materials became available, and now is becoming more popular again as a “natural” dye. It also is useful in cosmetics and food. Lac dye is a byproduct of shellac production. It has been used as a skin cosmetic, in medicine, and for dyeing wool, silk and leather. 1091 1092 C Costs and Benefits of Insects Human and Animal Food Insects are not ordinarily a major source of nutrition for humans in western societies. In some societies, however, insects are consumed if they are especially available or provide needed nutrition during times of famine (e.g., locusts in Africa), or as part of cultural tradition (e.g., as a condiment – canned grasshoppers in Southeast Asia or Maguey worms in Mexico). In Africa, Asia, Oceania, and Latin America it is not unusual to find a great diversity of insects in local marketplaces, and in some countries children are especially likely to eat insects opportunistically. Insects are good sources of proteins, lipids, and vitamins, but it is difficult to raise them economically. Thus, they tend to be eaten opportunistically rather than cultured. The economic value of insects as food has not been assessed, but likely is relatively low. In a few societies, insects have been prized as food. For example, the emperor Montezuma and the Aztec kings who preceded him prized the eggs of aquatic Hemiptera (called “ahuahutle”), where it was the equivalent of caviar, and transported at great effort and expense to Tenochtitlan for ceremonies. Surely if more of the world’s leaders would set an example of consuming insects, others would be induced to follow, setting the stage for a new insect-based food industry! Insects often are useful for maintenance of pets, as they are readily accepted and nutritious. Easily cultured insects are most generally used, including house cricket, Acheta domesticus; mealworm, Tenebrio molitar; waxworms, Galleria mellonella; and various flies (Muscidae and Calliphoridae). They are most often used as food or a food supplement for amphibians, reptiles and birds, but rodents and some small mammals also accept them. They are sold in various forms at pet shops, including alive, dried, and frozen. In recent time, dehydrated insects have been included in some types of wild bird food, although this is still relatively unusual. Also, zoos often seek live insects for their exhibit animals, both due to their nutritional value and also because higher animals often suffer from boredom in a zoo environment, and it is healthy to provide variety and diversion, which can be provided in the form of live insects. Thus, large mobile insects such as grasshoppers provide diversion as well as nutrition for some zoo animals, including monkeys. Lastly, but importantly, insects are used as a lure (bait) for fishing, as some fish take live insects preferentially. The same insects used for pet food tend to be used as fish bait. Medical Treatment Though more widely used for medical treatment in ancient societies, insects retain some uses in contemporary treatment of human ailments, most notably for apitherapy (bee venom therapy) and for maggot therapy. Apitherapy is sometimes recommended for rheumatic diseases, including arthritis and multiple sclerosis. Traditionally, bees were stimulated to sting the affected area, but injected venom is now also used as a form of treatment. Bee venom is also applied topically in creams, liniments and ointments. Maggot therapy is more well-founded scientifically, and takes advantage of the propensity of some fly larvae (usually Lucilia maggots) to feed on dead and decaying flesh, but to avoid feeding on living tissue. Thus, live maggots are introduced to wounds of humans or pets to clean out necrotic tissue. Also, maggots excrete products that inhibit growth of microbes that lead to infection of living tissue and stimulate regrowth of healthy tissue. More commonly used prior to the advent of modern antibiotics (the 1940s and 1950s), maggot therapy continues to be used for wounds that display difficulty in healing, and with the emergence of antibiotic-resistant bacteria, there is potential of renewed interest by the medical community.  Apiculture  Pollination and Flower Visitation  Bees  Ants Cotton Leafworm, Spodoptera littoralis (Boisduval)  Invasive Insects  Natural Enemies Important in Biological Control  Insecticides  History and Insects  Lyme Borreliosis  Eastern Equine Encephalitis  West Nile Fever  Plague: Biology and Epidemiology  Silkworms  Eri Silkworm  Sericulture  Shellac  Lacquers and Dyes from Insects  Entomophagy: Human Consumption of Insects  Maggot Therapy  Midges as Human Food  Native American Culture and Insects  Nutrient Content of Insects References Cox C (1991) Pesticides and birds: from DDT to today’s poisons. J Pestic Ref 11:(4)2–6 DeFoliart GR (1989) The human use of insects as food and as animal feed. Bull Entomol Soc Am 35:(1)22–35 DeFoliart GR (1999) Insects as food: why the western attitude is important. Annu Rev Entomol 44:21–50 Hill DS (1997) The economic importance of insects. Chapman and Hall, London, UK Hodkinson ID, Hughes MK (1982) Insect herbivory. Chapman and Hall, London, UK Lind PM, Milnes MR, Lundberg R, Bermudez D, Orberg J, Guillette LJ Jr (2004) Abnormal bone composition in female juvenile American alligators from a pesticidepolluted lake (Lake Apopka, Florida). Environ Health Perspect 112:359–362 Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323 Pimentel D, Lach L, Zunia R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65 Rosenstreich DL, Eggleston P, Kattan M, Baker D, Slavin RG, Gergen P, Mitchell H, McNiff-Mortimer K, Lynn H, Ownby D, Malveaux F (1997) The role of cockroach allergy and exposure to cockroach allergen in causing C morbidity among inner-city children with asthma. N Engl J Med 336:1356–1363 Southwick EE, Southwick L Jr (1992) Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. J Econ Entomol 85:621–633 Ware GW, Whitacre DM (2004) The pesticide book. MeisterPro Information Resources, Willoughby, OH Cost-Benefit Analysis An assessment of the total costs of an activity in comparison to its total benefits. Although environmental and societal aspects may be considered, all costs and benefits are usually expressed in monetary terms. Cotton or Melon Aphid, Aphis gossypii Glover (Hemiptera: Aphididae) This species is an important pest of crops and has a wide host range.  Aphids  Melon Aphid, Aphis gossypii Cotton Leafworm, Spodoptera littoralis (Boisduval) John L. Capinera University of Florida, Gainesville, FL, USA This insect occurs in Africa, Madagascar, Europe and the Middle East. A very similar but allopatric insect, Spodoptera litura (Fabricius) (taro caterpillar or tobacco cutworm), is found in Asia, Australia, and the Pacific region. For many years these two species were thought to be the same, and although they have been considered to be separate species by most authorities since 1962, confusion lingers. Other common names applied to S. littoralis include Egyptian cotton leafworm or Egyptian cotton worm, tomato caterpillar, tobacco caterpillar, and Mediterranean climbing cutworm, just to name a few. 1093 1094 C Cotton Leafworm, Spodoptera littoralis (Boisduval) Life History The number of generations displayed by this species depends on temperature. In southern Europe, for example, three generations are commonly observed, whereas in Egypt seven generations are not unusual. Warm, but not excessively hot, weather favors this species. Development ceases when temperature are less than about 10.5°C. This species lacks the ability to diapause and is intolerant of cold winters, so in Europe, for example, it occurs regularly only in the southernmost regions. Eggs are spherical, somewhat flattened, and measure about 0.4–1.0 mm in diameter. They are deposited in clusters of 100–300 eggs, in fairly regular rows comprising three layers, and covered with whitish scales from the abdomen of the female moth. The eggs are yellowish or green initially, but turn black before hatching. Eggs persist for 2–3 days in the summer, but considerably longer under cooler condition, up to 25 days. Females have been shown to produce 1500–2000 eggs. Larvae initially are pale green with black heads. The older larvae are more variable, often appearing gray, brown or almost black and with dark markings. The latter instars bear triangular spots laterally on each body segment, and dorsal stripes. They attain a length of 40–50 mm. Young larvae feed in groups, but after the third instar they disperse and become solitary. Normally there are six instars. Larvae are inactive during the day, with the older instars seeking shelter in the soil but the younger larvae remaining motionless on the foliage. Larval development may require only 12–18 days under hot conditions, but requires up to 85 days under cool conditions. Larvae burrow into the soil to a depth of 3–5 cm in preparation for pupation. Pupae are dark red to reddish brown, and are found in cells buried in the soil. The pupae are 15–20 mm in length, and the last segment bears two hooks. Pupal development time is only 5–10 days under warm conditions, but requires up to 30 days under cool conditions. The appearance of adults are typical of Spodoptera moths, with the forewings bearing brown, yellow and white markings, and the hind wings white with a narrow brown margin. The wing span is about 30–44 mm. It is nearly identical to the yellowstriped armyworm, S. ornithogalli (Guenée), of North America. Adults are active at dusk and during the evening. They mate immediately upon emergence and can begin to deposit eggs within two days of mating, though sometimes several days elapse before egg deposition. The adults are short-lived, rarely surviving seven days under warm conditions, though persisting for three weeks under cool conditions. Sex pheromones are produced and have been identified for use in traps. Many naturally occurring biological control agents have been identified, especially parasitoids (Braconidae, Encyrtidae, Tachinidae, and Ichneumonidae) and general predators. Several disease agents, including a baculovirus, microsporidia, fungi, and nematodes have been observed. Damage Cotton leafworm, like most Spodoptera species, is highly polyphagous. It attacks nearly 90 species of importance in 40 plant families, including virtually all vegetables; many flowers; avocado, citrus, and mulberry trees; coffee; grapes; field crops such as alfalfa, clover, cotton, grain amaranth, peanut, rice, soybean, sugarcane, and tobacco; and many other plants. Larvae feed on the foliage and the fruits or pods of plants. It is considered to be an extremely damaging agricultural pest where it occurs. Management Insecticides are commonly applied for control of this insect, particularly in cotton. However, it can be managed by using Bacillus thuringiensis, insect growth regulators and slow-release pheromones, thereby preserving natural enemies. Cover, Border and Trap Crops for Pest and Disease Management When management procedures are used in an integrated manner, the number of chemical insecticide applications can be greatly reduced. Insecticide resistance is a frequent problem when insecticides are used excessively. Not all strains of Bacillus thuringiensis are effective.  Taro Caterpillar or Tobacco Cutworm, Spodoptera litura (fabricius) (Lepidoptera: Noctuidae)  Yellowstriped Armyworm, Spodoptera ornithogalli (Guenée) (Lepidoptera: Noctuidae)  Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)  Beet Armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae)  Vegetable Pests and their Management References Baker CRB, Miller GW (1974) Some effects of temperature and larval food on the development of Spodoptera littoralis. (Boisd.) (Lep., Noctuidae)Bull Entomol Res 63:495–511 *CABI and EPPO (1997) Spodoptera littoralis and Spodoptera litura. In: Quarantine pests for Europe, 2nd edn. CABI International, Wallingford, UK, pp 518–525 Kehat M, Gordon D (1975) Mating, longevity, fertility and fecundity of the cotton leaf-worm, Spodoptera littoralis. (Boisd.) (Lepidoptera: Noctuidae) Phytoparasitica 3:87–102 Cotton Stainers Members of the family Pyrrhocoridae (order Hemiptera).  Bugs Cotton Whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) This species is also known as sweetpotato whitefly and silverleaf whitefly, and is a serious pest worldwide.  Whiteflies (Hemiptera: Aleyrodidae) C Cottony Cushion Scale, Iceryi purchasi Maskell (Hemiptera: Margarodidae) This is an important citrus pest if predators are absent.  Citrus Pests and their Management  Scale Insects and Mealybugs (Coccoidae)  Hemiptera  Area-Wide Pest Management Cover, Border and Trap Crops for Pest and Disease Management o. e. LiBurd, t. w. nyoike, C. a. sCott University of Florida, Gainesville, FL, USA Natural pest control provides a safer and more sustainable approach for managing pest populations. This type of control relies heavily on complex communities, natural enemies and the integration of cultural tactics including the use of mulches, trap crops, cover crops and other mechanisms that modify insect behavior to reduce the effect of insect herbivores on crop plants. This is also called “ecological management.” Two hypotheses have been proposed to explain the reduction in herbivore damage in complex crop communities. The “natural enemies” hypothesis proposes that more diverse food sources (nectar, pollen, prey host species) allow for the establishment of higher densities of predators and parasites, which regulate pest populations in diverse habitats. Secondly, the “resource concentration” hypothesis predicts that herbivores will not want to remain in sparsely populated plant stands because fewer resources are available. Conventional pest control programs rely heavily on monoculture environments with high usage of broad-spectrum pesticides. However, total reliance on chemical tactics to control pests can lead to resistance of arthropod pests, reduction in natural enemies, and resurgence of pest populations. In addition, this strategy is harmful 1095 1096 C Cover, Border and Trap Crops for Pest and Disease Management to the environment and it increases the cost of production. These effects have led to the search for other management alternatives, which are sustainable and cost effective. Such practices include use of mulches, cover crops, trap crops and border crops. The Role of Mulches for Suppression of Pest Populations Mulching is the art of using soil barriers to improve plant growth. This helps to reduce arthropod pest populations, disease symptoms and regulate soil temperatures. Generally, there are two types of mulches, which can be used to suppress pests: organic and synthetic (Figs. 118 and 119). Organic mulches These types of mulches are composed of lawn clippings, leaves, straw, sawdust, bark nuggets, wood chips, brown paper and living mulches. They are used extensively in the production of ornamental landscape plants but high usage also occurs within the fruit and vegetable industry. One common example of an organic mulch is living mulch. A living mulch is a minor crop that grows within a major crop. Living mulches are low-cost alternatives to synthetic mulches and are safe for the environment. Common living mulches include buckwheat, Fagopyrum esculentum Moench, white clover, Trifolium repens L., and wheat, Triticum aestivum L. Living mulches (Fig. 119) reduce the number of insect herbivores that alight onto crop plants. This is accomplished by modification of insect behavior. For instance, alate aphids locate their hosts by contrasting the soil background with the green color of the foliage. The establishment of living mulches will alter the appearance of the soil surface, subsequently reducing the image that is recognized by aphids. In addition, living mulches provide supplemental resources that support higher numbers of natural enemies (Fig. 118) contributing to pests’ regulation. Living mulches have also been shown to reduce the number of whiteflies, delay the onset of insectborne viruses and increase yields in vegetable plants. It is, however, important to select the appropriate living mulch suited for the crop to be planted and the pest to be controlled. In some instances competition between the crop and the living mulch can result in reduced yields. Cover, Border and Trap Crops for Pest and Disease Management, Figure 118 Occurrence of natural enemies in plots containing the living mulch buckwheat, Fagopyrum esculentum, compared with plots treated with synthetic mulch; note greater abundance in the presence of living mulch. Cover, Border and Trap Crops for Pest and Disease Management Cover, Border and Trap Crops for Pest and Disease Management, Figure 119 Types of mulch: (above) living mulch: buckwheat intercropped with zucchini squash; (center) zucchini squash growing on reflective plastic mulch; (below) Sunn hemp cover crop in an organic field in Citra, Florida. C 1097 1098 C Cover, Border and Trap Crops for Pest and Disease Management Synthetic Mulches Various colors of synthetic mulches including clear, white, black, yellow and silver-colored plastic (Fig. 119) are used commercially to grow vegetable crops. In semi-tropical regions, conventional growers use white in the summer, white on black (white top surface with black bottom) in the fall, and black in the winter and early spring. Black mulches increase soil temperatures during the cool season and white mulches reduce soil temperatures during the warm season. Ultraviolet light (UV)-reflective mulches, used by some growers, have the added benefit of reducing pests and the occurrence of viral diseases. They can reduce abundance of whitefly and aphid vectors that transmit viruses such as tomato spotted wilt virus and mosaic virus among various vegetable crops. UV-reflective mulches work by reflecting short-wave light, which repels incoming insect herbivores, thus reducing their potential for alighting on crop plants. However, these mulches lose their effect on insects once the reflecting surfaces are covered by the crop canopy. UVreflective mulches have an added advantage of increasing plant vigor and growth, which eventually results in increased yields. However, they do not decompose easily in the environment, which may limit their use in some farming systems. The Role of Cover Crops in Suppressing Pest Populations Cover crops can be annual, biennial or perennial herbaceous plants grown singly or within mixed stands throughout the year to cover the bare soil. Cover crops become green manures when they are plowed back into the soil specifically to improve soil nutrient quality. In addition to suppressing weeds and nematode populations, cover crops can influence insect population dynamics by diverting generalist pests, confusing specialist pests, reducing the success of the pest by changing the quality of the host plant, and by increasing natural enemy abundance by providing supplemental resources (food, water, and overwintering sites). In temperate climates, cover crops are usually winter annuals that are planted in late summer to give soil cover during the winter. Barley, Hordeum vulgare, and rye, Secale ceceale, are excellent examples of winter grass-like cover crops whereas hairy vetch, Vicia villosa, is a very common winter legume cover crop. Summer grass-like cover crops include sorghum, Sorghum bicolor, and sudan grass, Sorghum sudanense, whereas leguminous summer cover crops include cowpeas, Vigna unguiculata, sunn hemp, Crotalaria juncea, and velvet bean, Mucana deeringana. In the United States, summer cover crops are planted in June, July and August and are termed warm-season crops. In well-managed orchards, the combination of leguminous and graminaceous cover crops can provide improved cover crop benefits as opposed to using only one pure stand cover crop. Cover crops are an important part of sustainable organic agriculture and provide good potential for managing economically important pests. Crops that produce high glucosinolate levels have been effective in reducing nematode populations when they are incorporated into the soil and allowed to decompose. For instance, residues of nematode-resistant radish proved to be effective in suppressing the sugarbeet nematode, Heterodera schachtii. A significant decline in the nematode population as well as the rate of nematode infection has been observed in sugarbeet crops when fodder radish, Raphanus sativus L., and white mustard, Sinapsis alba L., were used as cover crops. The Role of Barrier or Border Crops in Suppressing Pest Populations Barrier or border crops have been used as a cultural strategy for reducing pest populations for more than half a century. It involves establishing another minor crop on the perimeter of the main crop for pests and disease suppression. Several Cover, Border and Trap Crops for Pest and Disease Management theories have been suggested to describe the mechanisms by which barrier crops reduce pest populations. Barrier crops reduce pest and related problems (incidence of pepper veinal mottle virus disease) by acting as a physical barrier for vectors. However, factors including plant height can affect the effectiveness of the barrier crop. Barrier crops also may act as a “sink” for virus invading new environments. For instance, aphids landing on the barrier crop will lose their virus charge while probing, consequently preventing them from transmitting diseases. The Role of Trap Crops in Suppressing Pest Populations Trap crops are plants grown before or with the main crop to attract pests from the main crop into a smaller area (the trap crop). Trap crops are the more-preferred host when grown with the main crop. The ecological behavior of the target pests should be considered when selecting the trap crop. In addition, the agronomic compatibility between the main crop and trap crop should be known to prevent competition for natural resources (nutrients and water). Trap crops can increase the efficiency of control by concentrating the pests in one location and by applying a chemical treatment without spraying the main crop, or by destroying the trap crop and associated pests through tillage or burning. It is also possible to release biological control agents into the trap crop, using it as a nursery for beneficial organisms that will then spread into the main crop. The overall cost of management can be significantly reduced because pesticide treatments or other management tactics are only applied to areas on the trap crop, where the pest congregates. Monitoring the pest population density on the trap crop is necessary in order to prevent the pest from migrating to the main crop. Planting a few rows of squash ahead of the main planting can be used to protect from pickleworm, Diaphania nitidalis, infestation because C the invading moths are attracted to the blossoms of the older plants. Squash can also be planted in conjunction with tomato to protect against silverleaf whitefly, Bemisia argentifolii, because squash is more preferred. In both cases, however, the squash must be sprayed with insecticide or destroyed before the insects disperse to the main crop. Economics of Sustainable Agriculture Ecological management of arthropod and nematode pests is a practical sustainable approach to achieving effective pest control while protecting the environment. The primary economic focus of sustainable agriculture is the input cost savings from reduced pesticide usage and fertilizer applications. In some instances, it can be less expensive since many of the tactics employed (mulching, cover crops, trap crops, etc.) are not imported and are tied directly into daily farming activities. Also, incorporating leguminous cover crops into different cropping systems may decrease the amount of N applications, and the energy needed for crop production. However, this may not necessarily result in increased profits for farmers because of two important factors affecting the profitability of cover crops: (i) the ability to improve crop yield, and (ii) the establishment cost of the cover crop. Overall, more research is needed to determine the long-term profitability of these sustainable practices. References Alegbejo MD, Uvah I (1986) Effect of intercropping pepper with tall crops on the incidence of pepper veinal mottle virus disease on pepper. Niger J Entomol 7:82–87 Cradock RK, da Graca JV, Laing MD (2002) Studies on the control of virus diseases in zucchini crops. S Afr J Sci 98:225–227 Csizinszky AA, Schuster DJ, Kring JB (1995) Color mulches influence yield and insect populations in tomatoes. J Am Soc Hortic Sci 120:778–784 1099 1100 C Cover Crops Frank DL, Liburd OE (2005) Effects of living and synthetic mulch on the population dynamics of whiteflies and aphids, their associated natural enemies, and insecttransmitted plant diseases in zucchini. Environ Entomol 34:857–865 Hilje L, Costa HS, Stansly PA (2001) Cultural practices for managing Bemisia tabaci and associated viral diseases. Crop Prot 20:801–812 Liburd OE, Frank DL (2007) Synthetic and living mulches for control of homopteran pests and diseases in vegetables. In: Saxena G, Mukerji KG (eds) Management of nematode and insect-borne plant diseases. The Haworth Press Inc., New York, NY pp 67–86 Lu Y, Watkins B, Teasdale JR, Abdul-Baki AA (2000) Cover crops in sustainable food production. Food Rev Int 16:121–157 Smith HA, Koenig RL, McAuslane HJ, McSorley R (2000) Effect of silver reflective mulch and a summer squash trap crop on densities of immature Bemisia argentifolii (Homoptera: Aleyrodidae) on organic bean. J Econ Entomol 93:726–731 Zitters AT, Simons JN (1980) Management of viruses by alteration of vector efficiency and by cultural practices. Annu Rev Phytopathol 18:289–310 winter season to improve soil condition), to suppress weeds, or to harbor beneficial insects. Cover, Border and Trap Crops for Pest and Disease Management Coxa The basal-most segment of the insect leg (Fig. 120), attaching to the thorax.  Legs of Hexapods Crab Lice, Phthirus pubis (Linnaeus) (Phthiraptera: Pthiridae) These lice infest the genital regions of humans.  Human Lice Cover Crops Crabronidae Cultivation of a second type of crop, principally to improve the production system for a primary crop (e.g., legumes or rye maintained during the A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies Coxa, Figure 120 Leg of a beetle (Coleoptera: Scarabaeidae) leg showing its component parts, and a close-up of one type of beetle tarsus (foot). Crane Flies (Diptera: Tipulidae and Others) Cranberry Fruitworm, Acrobasis vaccinii Riley (Lepidoptera: Pyralidae) This is a pest of blueberries in eastern North America.  Small Fruit Pests and their Management Cranberry Girdler, Chrysoteuchia topiaria (Zeller) (Lepidoptera: Pyralidae) This species affects both cranberries and turfgrass.  Small Fruit Pests and their Management Cranberry Tipworm, Dasineura oxycoccana (Johnson) (Diptera: Cecidomyiidae) Cranberry tipworm affects both cranberries and blueberries.  Small Fruit Pests and their Management C transverse suture between mesonotal prescutum and scutum, or roughly at the level of the wing bases. Three other, relatively small families share this characteristic. The Tanyderidae, or primitive crane flies, have five branches of the radial vein reaching the wing margin. Tipulidae have four or fewer. Trichoceridae, or winter crane flies, possess ocelli, while tipulids have none. Ptychopteridae, or phantom crane flies, have a single anal vein in each wing, compared to two in Tipulidae. Most adult crane flies are slender-bodied, with elongate, membranous wings and conspicuously long, slender legs (Fig. 121). People not familiar with insects often mistake crane flies for large mosquitoes. In fact, the colloquial term “gallinipper” has been applied to both crane flies and mosquitoes. However, no crane flies are able to bite. In size, crane flies range from two species of Holorusia (originally Ctenacroscelis) of southeastern Asia, with a wing span of over 100 mm, or Holorusia hespera in western United States, with approximately a 70 mm wing span, to the tiny Tasiocera ursina, with wingspread of only 4.5–5.0 mm, smaller than that of mosquitoes. Wings of many crane flies are unmarked except for the somewhat darkened stigma, while many other species have the wings spotted, transversely Crane Flies (Diptera: Tipulidae and Others) GeorGe w. Byers University of Kansas, Lawrence, KS, USA Largest of the families of true flies (Order Diptera) in number of known species, the crane flies (Family Tipulidae, of suborder Nematocera) are abundantly represented on all continents except Antarctica. Some 15,000 species have been named and described, more than 10,000 of these through the work of one man, Prof. Charles P. Alexander, of the University of Massachusetts. Over 1,600 species are known from North America. Crane flies can be differentiated from most other nematocerous flies by the presence on the dorsum of the thorax of a broadly V-shaped, Crane Flies (Diptera: Tipulidae and Others), Figure 121 Adult male of Tipula sp., dorsal aspect. Body length 18 mm, wing length 21 mm. Legs are arranged unnaturally to show relative lengths of segments. 1101 1102 C Crane Flies (Diptera: Tipulidae and Others) banded, or with a mottled or clouded pattern of brown, gray or black. The slender legs of some species are banded with dark brown, while those of others may be partially white (for example,Brachypremna or some Hexatoma). While most kinds of flies, indeed most insects, have the trochanter firmly attached to the adjacent femur, the legs of crane flies are readily broken off between trochanter and femur, possibly so that a leg seized by a predator can quickly be shed, to spare the fly. The adult life of most crane flies is brief. The adults emerge from the pupal skin, often at night in order to have the body hardened, the wings fully extended and the insect capable of flight by sunrise when birds and other predators become active. Males usually appear a night or two before females. Males of many species form swarms to which females are attracted. Following mating, females disperse and oviposit. Oviposition is often completed in two or three nights. Thus, an adult life of a few days is ordinarily adequate. Adults of Chionea, rendered inactive by night time chill, and forced to seek shelter from severe cold, may survive a few weeks. The adults of most crane flies do not feed but subsist on energy acquired and stored by the larva. Those of a few, such as species of subgenus Geranomyia of the large genus Limonia, possess elongate mouthparts or a proboscis and are known to obtain nectar from certain flowers. Ecology Adult Tipulidae are most often found in low, leafy vegetation in shaded, somewhat damp areas, such as along small woodland streams. However, there are a few species living in grasslands or even in semidesert habitats. At temperate latitudes, they are usually the most common in spring and late summer and may have two annual generations. Adults of Chionea, virtually wingless and almost spider-like in appearance, may be found on the surface of snow, in winter, in Eurasia and North America. The larvae of crane flies are subcylindrical and somewhat tapered toward the ends (Fig. 122). The Crane Flies (Diptera: Tipulidae and Others), Figure 122 Larva of Tipula sp., left lateral aspect. Body length 29 mm. head, variously sclerotized according to the species, can be withdrawn into the thoracic segments. The larvae occur in a great variety of moist to wholly aquatic, even marine intertidal microhabitats. Those of aquatic species may be found in decomposing plant material near the shore or in shallow water near sandbars. Larvae in aquatic situations may respire by means of a pair of large spiracles on the ninth abdominal segment that are raised to the surface from time to time. Others have such spiracles but appear to obtain sufficient oxygen through the skin. A few (e.g., larvae of Antocha and Hesperoconopa) have a closed tracheal system and lack spiracles. Most aquatic tipulid larvae leave the water to pupate. While some aquatic and semiaquatic larvae are detritivores, many others are carnivorous. The larvae of Pedicia, Limnophila and Hexatoma, for example, feed on midge larvae, other insect larvae and other small, aquatic invertebrates. Terrestrial crane fly larvae may occur in and feed upon rotting wood, fungi, or decomposing plant debris, in mosses and liverworts, among rootlets of grasses and other plants, and a few (e.g., Cylindrotoma) feed on leaves of herbaceous plants. The only larval Tipulidae that are of direct economic importance are those that eat rootlets of range-land grasses or seedling crops (particularly some species of Tipula and Nephrotoma). Geological Record The oldest fossil remains described as Tipulidae are of upper Triassic age, perhaps 180 million years old. In North America, the earliest remains, similar to modern Tipulidae, are in the fine-grained shale of the Green River formation, of the Eocene age, approximately 50 million years old. The Baltic Crapemyrtle Aphid Sarucallis Kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae) amber of northern Europe, which is upper Eocene to Oligocene in age (about 45 million years old), contains numerous species of crane flies, preserved in fine detail. Taxonomic Divisions The family Tipulidae has been divided into three subfamilies, Tipulinae, Cylindrotominae and Limoniinae. Most large crane flies belong to the Tipulinae, but there are a few large Limoniinae. For identification keys (North America), see Alexander 1942 (somewhat revised and reprinted in 1966) or Alexander 1967. In fairly recent years, European authors have elevated these three subfamilies and tribe Pediciini of Limoniinae to full family status. References *Alexander CP (1942) Family Tipulidae. In: The Diptera or true flies of Connecticut. Connecticut State Geological and Natural History Survey, Bulletin 64, pp 196–509 Alexander CP (1967) The crane flies of California. Bull Calif Insect Survey 8:1–269 Cranium C feeding exclusively on species of Lagerstroemia. Interestingly, other aphid species are not known to attack or infest crape myrtles. Crape myrtles are popular ornamental plants throughout tropical and subtropical areas of the world. Because aphids can be extremely difficult to detect on plants during shipping, S. kahawaluokalani has been transported throughout the world on shipments of crape myrtle. When aphid numbers are high, S. kahawaluokalani damages crops via a fungus that grows on its excrement. Several insect predators attack crapemyrtle aphids, but most are unable to provide permanent control of aphid populations. Crapemyrtle aphids (Fig. 123) reproduce at an astonishing rate, giving the impression that an infestation suddenly occurred overnight. Each adult S. kahawaluokalani gives birth parthenogenetically to several offspring per day, and the growth of crapemyrtle aphid populations is further accelerated by the process of telescoping generations. Parthenogenesis is a form of asexual reproduction where offspring are produced without mating. Furthermore, crapemyrtle aphids are viviparous, meaning they give live birth to their offspring. Telescoping generations refers to the process in which nymphs or immature aphids begin to develop offspring inside of them before they become adults. In many aphid species, a nymph that is developing inside of its mother has already begun to develop offspring The head capsule of an insect.  Head of Hexapods Crapemyrtle Aphid, Sarucallis kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae) John J. herBert, russeLL f. mizeLLiii University of Florida, Quincy, FL, USA The crapemyrtle aphid, Sarucallis kahawaluokalani (Kirkaldy), is native to Southeast Asia but may be found anywhere that crape myrtles, Lagerstroemia spp,. are grown. With the exception of henna and pomegranate, S. kahawaluokalani is host specific, Crapemyrtle Aphid Sarucallis Kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae), Figure 123 Winged adults and nymph of crape myrtle aphids, Sarucallis kahawaluokalani. 1103 1104 C Crapemyrtle Aphid Sarucallis Kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae) inside of itself. Telescoping generations allows aphids to reproduce immediately upon becoming an adult, and S. kahawaluokalani give birth within a few hours of reaching the adult stage. Crapemyrtle aphids exhibit a life cycle that is more complex than simple parthenogenesis, and under some environmental conditions, crapemyrtle aphids practice sexual reproduction. The life cycle of S. kahawaluokalani begins when overwintering eggs hatch in the spring. Aphids hatching from overwintering eggs are all female, and such mature wingless stem mother aphids that hatch from overwintering eggs are called fundatrices (singlular, fundatrix). Fundatrices reproduce through parthenogenesis, giving rise to a second generation known as virginoparae. Virginoparae reproduce through parthenogenesis and subsequent generations of aphids throughout the summer are also called virginoparae. In late summer and early fall, virginoparae produce a special generation of aphids known as sexuparae. Sexuparae give birth to both male and female aphids. The female aphids of this generation are known as oviparae, and after mating with males, oviparae deposit their eggs on the branches of crape myrtle. Eggs are deposited in loose clusters within the crevices of bark and remain on the plant until the following spring when the eggs hatch and the cycle restarts. Nymphs of S. kahawaluokalani are yellow in color with black hair-like projections protruding from their abdomen. Adult S. kahawaluokalani are yellow, mottled with black spots, and have two large black tubercles that project from their dorsum. Many aphids produce winged adults for dispersal, but usually do so in response to overcrowding of the host plant or a sudden drop in host plant quality. Sarucallis kahawaluokalani is unusual among aphids in that all adults, except for oviparae, are winged and capable of dispersing. Fecundity and development of S. kahawaluokalani are dependent on ambient temperature, and under optimal conditions, S. kahawaluokalani adults can produce over six offspring per day, and nymphs can mature in as little as five days. Adults can live up to 21 days, producing more than 150 offspring within their lifetime. Successful reproduction and development are dependent on the assimilation of nutrients. Crapemyrtle aphids acquire their nutrition by feeding on the phloem sap of their host plant. Phloem is rich in sucrose and other sugars, but contains low concentrations of amino acids. In addition to having small amounts of amino acids, phloem does not contain all of the amino acids required for successful growth, development, and reproduction. Crapemyrtle aphids have evolved several mechanisms to circumvent the disadvantages of feeding on phloem. To obtain the necessary quantity of nutrients, aphids feed on large volumes of phloem and use a special filter chamber in the gut to remove necessary nutrients. Furthermore, aphids harbor endosymbionts within the gut that manufacture amino acids that are required by the aphid but not present in the phloem. The most common endosymbiont of aphids are members of the genus Buchnera. Phloem contains large quantities of sucrose, which causes it to be a hypertonic solution. Thus, even though aphids feed on a liquid diet, they are confronted with the problem of becoming dehydrated from their source of food. Aphids can overcome this is by changing simple sugars into more complex sugars, which in turn lowers the osmotic pressure by creating fewer sugar molecules per molecule of water. Feeding on large quantities of phloem, followed by filtering and changing of sugar composition, creates a large amount of unused sugar and water. Crapemyrtle aphids excrete unused or transformed sugars, along with water, from the anus in a droplet known as honeydew. To avoid becoming coated and entangled in sticky honeydew, crapemyrtle aphids forcefully eject honeydew away from their feeding site. Honeydew can be easily spotted in the field as a shiny sticky substance on the leaves of crape myrtles. Honeydew is rich in sugars and promotes the growth of fungi and other microorganisms. The honeydew of S. kahawaluokalani promotes the growth of an undescribed black sooty mold in the genus Capnodium. Capnodium sp. can turn the entire plant an unsightly black color, detracting from the visual aesthetics. Furthermore, thick Crawler carpets of Capnodium sp. interfere with photosynthesis, causing the abscission of leaves and in some cases complete defoliation of the plant. Established plantings of crape myrtle do not show signs of long term damage and bloom beautifully the following year. Damage to crape myrtles is influenced by crape myrtle cultivar and interactions with aphid natural enemies. Crapemyrtle aphids are attacked by a variety of insect predators, but are not known to harbor any parasitoids. Lacewings (Chrysopidae), flower flies (Syrphidae), lady beetles (Coccinellidae), and other generalist predators feed on crapemyrtle aphids, especially when other prey are scarce. Predatory and parasitic hymenoptera of other insect pests feed on honeydew, allowing them to search for prey over greater distances. Because crapemyrtle aphids do not cause permanent damage to crape myrtles, and provide food for insect natural enemies, the use of chemical pesticides is strongly discouraged. If aphids reach high populations and control is necessary, the use of soapy water or power washing is usually sufficient for removing aphids from a particular plant. These methods are less harmful to insect natural enemies and help contribute to biological and natural control of crapemyrtle aphid and other insect pests. C Craw, Alexander Alexander Craw was born on Ayr, Scotland, on August 3, 1850. He emigrated to California, USA, when he was 23, and by 1875 was placed in charge of a very large orange grove near Los Angeles. He helped D.W. Coquillett in investigations of chemical control of the new pest cottony cushion scale. He was the first to suggest use of natural enemies for control of this pest when chemicals failed. In 1890, he was appointed quarantine inspector at the port of San Francisco by the California Board of Agriculture, and it was he who developed and put into practice the principles of horticultural quarantine. In 1904 he accepted a position as Superintendent and Inspector of the Hawaiian Board of Agriculture and Forestry in Honolulu, where he remained until his death in 1908. Most of his publications were about control of pests and about exclusion of new pests by quarantine, but he did describe a few new species of insects. Reference *Essig EO (1931) Craw, Alexander. In: A history of entomology. The Macmillan Company, New York, NY, pp 593–595 Crawler References Alverson DR, Allen RK (1991) Life history of the crapemyrtle aphid. Proc SNA Res Conf 36:164–167 Alverson DR, Allen RK (1992) Bionomics of the crapemyrtle aphid (Homoptera: Aphididae). J Entomol Sci 27:445–457 Dixon AFG (1998) Aphid ecology. Chapman and Hall, London, UK, 300 pp Mizell RFI, Schiffhauer DE (1987) Seasonal abundance of the crapemyrtle aphid, Sarucallis kahawaluokalani, in relation to the pecan aphids, Monellia caryella and Monelliopsis pecanis and their common predators. Entomophaga 32:511–520 Mizell RF, Knox GW (1993) Susceptibility of crapemyrtle, Lagerstroemia indica L., to the crapemyrtle aphid (Homoptera: Aphididae) in North Florida. J Entomol Sci 28:1–7 whitney Cranshaw Colorado State University, Ft. Collins, CO, USA Crawler is the active stage of an insect immediately after egg hatch (first instar) found among certain insects in the order Hemiptera. The term crawler is most commonly used to describe first instar scale insects, but may also describe similar stages found among mealybugs and whiteflies. The crawler stage is noted for mobility allowing distribution within and among host plants. Many species that have a crawler period (e.g., Diaspididae and Aleyrodidae) subsequently produce (Fig. 124) immature stages that move little, if at all, following the crawler period. 1105 1106 C Crawling Water Beetles Crawler, Figure 124 Cottony cushion scale adults and crawlers. The adults (large with a white, fluted, waxy secretion on the stem) are easily observed, whereas the small crawlers (small insects along the mid-vein on the leaf) are harder to detect. (Photo by Lyle Buss, University of Florida.) In management of insects, the crawler stage is often one that is targeted for control because crawlers are small and have a relatively thin wax coating that makes them easier to kill with pesticides. close association of humans with livestock, particularly horses and mules. Creeping Water Bugs Crawling Water Beetles Members of the family Haliplidae (order Coleoptera).  Beetles Members of the family Naucoridae (order Hemiptera).  Bugs Cremaster Creeping Myiasis Infestation of humans by bot fly larvae that ultimately cannot complete their development and perish in the abnormal human host. The larvae typically die in the first instar after burrowing beneath the skin, causing little serious injury but causing itching and creeping eruptions. Species of Gasterophilus are usually implicated, and follow In Lepidoptera, a process at the tip of the abdomen, usually bearing spines or hooks, by which pupae are suspended from silk attached to a substrate surface. Crenulate A tem used to indicate a wavy or scalloped appearance. Cresson, Ezra Townsend Crenulate Moths (Lepidoptera: Epiplemidae) John B. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Crenulate moths, family Epiplemidae, total about 632 species worldwide, with most being Neotropical (230 sp.) and Indo-Australian (301 sp.). The common name for the family refers to the often scalloped, or crenulate, margins of the wings. Two subfamilies are known: Auzeinae, with about 25 sp. (mostly Indo-Australian), and Epipleminae for all others. The family is in the superfamily Uranioidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults small to medium size (9–47 mm wingspan), with head scaling normal; labial palpi upcurved; haustellum naked; maxillary palpi minute, 1-segmented. Wings (Fig. 125) triangular, typically with distinct marginal emarginations and marginal points, and forewing tip often somewhat falcate; hindwing generally rounded to triangular and also usually with emarginations and marginal points or tail-like projections. Maculation mostly shades of brown with few markings and hindwings usually matching the forewing coloration; rarely more colorful; some are leaf-like. Adults nocturnal. Larvae leaf feeders or webbers. Crenulate Moths (Lepidoptera: Epiplemidae), Figure 125 Example of crenulate moths (Epiplemidae), Epiplema castanea Warren from Taiwan. C Host plants in several plant families, including Bignoniaceae, Caprifoliaceae, Olacaceae, Oleaceae, Rosaceae, Rubiaceae, and others. References *Boudinot J (1982) Insectes Lépidoptères Epiplemidae. In: Faune de Madagascar. 60:1–55. Paris: Off. Rech. Sci. Tech. Outre-Mer, France * von Dalla Torre KW (1924) Epiplemidae. In: Lepidopterorum catalogus. 30:1–57. W. Junk, Berlin. *Holloway JD (1998) Subfamily Epipleminae. In: The moths of Borneo, 8:78–82, 92–132, pl.1, 6–8. Malayan Nature Society, Kuala Lumpur (Malayan Nature Journal, 52). Seitz A (ed) (1912–33) Familie: Epiplemidae. Die GrossSchmetterlinge der Erde, 2:277–280, pl. 48 (1912); 2(suppl.):171–172 (1933); 6:1141–1170, pl. 169–172 (1930); 10:577–600 (1929), 601–604, pl. 58–59 (1930); 14:390–394, pl. 67 (1928). A. Kernen, Stuttgart *Stehr FW (1987) Epiplemidae (Geometroidea). In: Immature insects [1], 507. Kendall/Hunt, Dubuque Crepuscular Organisms in which the period of activity is twilight, either pre-dawn or dusk. Cresson, Ezra Townsend Ezra Cresson was born on June 18, 1838, in Pennsylvania, USA. He attended public schools in Philadelphia through the eighth grade, but then had to drop out to help support the family. Little of his paid employment was in entomology, and one of his positions was as clerk in the treasurer’ s office of the Pennsylvania Railroad Company, another was as secretary to a wealthy patron of the Philadelphia Academy of Sciences, and a third was with a fire insurance company. His interest in insects was kindled by his future father-in-law, James Ridings. He, Ridings, and George Newman, in 1859, were the founding members of an entomological society which, in 1867, changed its name to the American Entomological Society, and is now the oldest existing entomological society 1107 1108 C Cretaceous Period in the United States. The society, under its original name, began in 1863 to publish Proceedings of the Entomological Society of Philadelphia. Cresson was one of the society members who set the type for the printing: this was truly an in-house publication. In that first issue of the Proceedings appeared Cresson’ s “Catalogue of the Cicindelidae of North America,” after which he confined his own publications to works on Hymenoptera. Between 1861 and 1882 he published 66 papers on Hymenoptera including catalogs and descriptions. In 1901 his collection, including 2,367 type specimens representing 3,511 species, was presented to the American Entomological Society. He died on April 19, 1926. Two of his five children displayed a strong interest in entomology. These were Ezra T. Cresson, Jr., who specialized in Diptera, and George Binghurst Cresson, who specialized in ants. Reference *Mallis A (1971) Ezra Townsend Cresson. In: American entomologists.Rutgers University Press, New Brunswick, NJ, pp 343–348 Cretaceous Period A geological period at the end of the Mesozoic era, extending from about 170 to 65 million years ago.  Geological Periods Cribellum In spiders, a sieve-like structure found just in front of the spinnerets. Cribrate This describes a structure or surface that is pierced by narrowly spaced small holes, resembling a sieve or strainer, or that functions as a sieve. Crickets Certain members (suborder Ensifera, superfamily Grylloidae) of an order or insects (Orthoptera).  Grasshoppers, Katydids and Crickets Criddle, Norman Norman Criddle was born in Addlestone, Surrey, England, on May 14, 1875 and moved to Canada in 1882 with his parents. The Criddle family established a homestead in Aweme, Manitoba. From his early childhood, Criddle had a strong interest in flora and fauna. This was expressed, in part, by drawing and painting, which he developed to great proficiency. His artistic skills were “discovered” only after he developed a poison bait, a mixture that came into wide use for grasshopper control during periodic outbreaks on the Canadian prairie. The bait brought the attention of Dominion Entomologist James Fletcher, who came to admire Criddle’s artistic and entomological abilities. They coauthored a publication on weeds in Canada in 1905. This pioneer entomologist received a government appointment in 1913, and investigated the cause of grasshopper plagues, attributing them to cycles of weather correlated with changes in the numbers of sunspots. Over the years, he also came to mentor several of Manitoba’s foremost entomologists. His entomological interests extended well beyond grasshoppers, of course, and he was a major proponent of understanding the biology of insects as a basis for their control. Norman Criddle received an honorary degree in Agriculture from the Manitoba Agricultural College shortly before his death on May 4, 1933 in Brandon, Manitoba. Crimean-Congo Hemorrhagic Fever This virus affects humans, and is transmitted by several species of ticks.  Ticks Crop Diversity and Pest Management Cristate A term used to indicate the presence of a high ridge or crest. Critical Period The notion that the brain is needed for a period of time (the critical period) if the insect is to develop properly. The brain synthesizes PTTH that activates the prothoracic gland to secrete ecdysone. Removal of the brain after PTTH produced (after the critical period) does not disrupt development. Crochets The minute hooks found on the prolegs, mostly of caterpillars. They usually are arranged in rows or circles. Crop Diversity and Pest Management huGh smith Hawaii Agriculture Research Center, Aiea, HI, USA Contemporary theories concerning the relationship between crop diversity and arthropod damage originated from observations made during the early decades of the twentieth century in temperate tree plantations and mixed farming systems in the tropics. Seminal studies of insect damage on collards by Pimentel and Root provided a broad ecological framework for examining arthropod damage under mixed and simple cropping systems. The classic experiments of Risch and Bach in Costa Rica demonstrated that the relationship between mixed cropping systems and pest damage is ultimately determined by the specifics of arthropod behavior. C Crop diversity can take many forms. Traditional farming systems in the tropics are often characterized by intercropping, in which different crops are arranged in alternating rows, or mixed together without regard to row. Mixed cropping systems in both temperate and tropical regions can resemble a mosaic-like patchwork of distinct crops. Trees, hedgerows, cover crops and even weeds can increase the plant diversity on a farm. Modern examples of crop diversity include the intentional mixing of resistant and non-resistant wheat hybrids for Hessian fly management in the midwest of the USA. Several hypotheses have been put forward to explain why pest damage is sometimes less in polycultures, as mixed cropping systems are called. The “enemies” hypothesis, defined by Root, suggests that polycultures offer greater resources than monocultures to parasitoids and predators in the form of nectar and pollen, alternate hosts and prey, and habitat. Populations of natural enemies are hypothesized therefore to be more stable in mixed cropping systems than in simple ones, and so better able to keep herbivore populations below economically damaging levels. A complementary idea put forward by Root is the “resource concentration” hypothesis. This proposes that resources provided by a crop are more easily exploited by herbivores when “concentrated” in a uniform stand. It may become more difficult for the herbivore to find and exploit the crop when it is mixed with other crops. This is because the volatiles, appearance, and leaf characteristics of nonhost plants may interfere with the host-finding mechanisms of certain arthropods. According to the “resource concentration” hypothesis, once an herbivore has found a suitable host within a polyculture, within-stand effects such as shading, increased humidity, and the presence of non-host crops may influence the arthropod to feed and oviposit less than it would in a monoculture, and to emigrate from the crop patch sooner than it would from a large uniform stand. Trap cropping is another form of polyculture that has been used to reduce pest damage. The pest is drawn away from the crop being protected by 1109 1110 C Crop Diversity and Pest Management the presence of a more attractive crop – the trap crop. Trap crops are often sprayed with pesticides to keep pest populations from building up and moving on to the main crop. Neither the enemies hypothesis, resource concentration hypothesis or trap cropping has been shown consistently to predict how an arthropod will behave in a mixed cropping system. In the 1970s, mathematical theories were proposed to suggest that diverse systems should be more stable than simple ones, and therefore that polycultures should experience less pest damage than monocultures. The misconception that crop diversity in itself reduces pest damage has persisted in spite of the fact that it is inconsistent with empirical observation. Stability is not a characteristic of most annual cropping systems, which tend to begin and end with the complete destruction of all vegetation in the field. Whether one or several crops are grown in the field in the interim may have little bearing on the long-term stability of the cropping system. Reviews of the literature indicate that in over fifty percent of the cases studied, intercropping reduced arthropod damage compared to monoculture. Fifteen to eighteen percent of the time, damage was worse in intercropped systems, and in twenty percent of the cases the results were variable. A significant trend revealed by reviews of the intercropping literature is that damage by monophagous insects tends to be reduced in polyculture, while damage by polyphagous insects is more likely to be increased or unaltered in mixed cropping systems. Under traditional mixed cropping conditions in Costa Rica, densities of a monophagous species of leaf beetle are reduced under polyculture, while densities of a polyphagous leaf beetle species are not reduced. Studies such as this indicate that the damage caused by an arthropod species in polyculture will be determined by the quantity and quality of host plants in the mix rather than by crop diversity in the taxonomic sense. In addition to host range, the host-finding mechanisms and the mobility of an arthropod will determine how its behavior is influenced by a given polyculture. In Costa Rica, populations of a monophagous chrysomelid were reduced in polyculture because they tended to emigrate more quickly from the mixed stands. Arthropods with sensitive host-finding mechanisms may be more easily deterred by the presence of non-host plants than arthropods that do not rely on specific visual or olfactory host-finding cues. Highly mobile insects such as certain grasshoppers or beetles may abandon a patch in which suitable hosts are hard to find more quickly than weak fliers such as whiteflies or thrips. Host-finding, mobility, and host range also influence how natural enemies will behave in a complex cropping system. Generalist predators and parasitoids are probably better adapted than specialized natural enemies to search the varied visual and olfactory landscape presented by a polyculture. Like monophagous herbivores, natural enemies with a narrow host range may be more efficient when searching in a uniform environment. By influencing probing behavior, mixed cropping systems may also affect the transmission rates of insect-vectored diseases. For example, crop combinations that encourage vectors of nonpersistent viruses such as aphids to probe more frequently and for a shorter duration may increase the likelihood of non-persistent virus transmission. By contrast, the transmission of persistent viruses tends to require longer probing periods, and so might be reduced by a cropping environment that stimulates vectors such as whiteflies to probe for shorter periods. Recent efforts in biological control have emphasized the introduction of perennial refugia or nursery crops for natural enemies in and around cropped areas. This is a form of polyculture. Refugia crops are planted to maintain stable populations of natural enemies in a cropping system by providing habitat, pollen, nectar, and alternate victims, so that predators and parasitoids will be available near the crop to suppress incipient pest populations. Region-wide approaches to managing major pests such as whiteflies and certain Lepidoptera have included the establishment of refugia for natural enemies. Standard methods of field research that have been established for studying and managing pest Cross-Resistance populations in large monocultures may require modification for use in complex polycultures. Conventional field plot research designs require replication under uniform conditions that are often difficult to achieve in a heterogeneous environment. The reduction of field plot variability required for standard statistical analysis is also difficult to accomplish in polycultures, which are by definition highly variable environments. Elucidation of the relationship between polyculture and pest management may require the adaptation of multiple regression methods and spatial diversity analysis. Similarly, methods for establishing scouting protocols and calculating economic injury levels have been designed to address pest behavior in homogeneous environments, and may require adaptation for mixed cropping systems. The population dynamics and feeding behavior of both herbivores and natural enemies may be different on a crop when that crop is grown in polyculture as opposed to monoculture. The resources that can be allocated to scouting and managing the pest complex of a crop that represents only one component of a diverse farm may differ from the resources available to manage the pest complex of a large monoculture. C Root R (1973) Organization of a plant-arthropod association in simple and diverse habitats. The fauna of collards. Ecol Monogr 43:95–124 Crop A portion of the foregut in the alimentary canal of insects. The crop receives the insect’s meal, and in insects that feed only infrequently it may be greatly expanded to accommodate the occasional meal. Although lined with a thick lining that inhibits digestion, in some insects the digestive enzymes secreted from the mouth or regurgitated from the midgut pass into the crop and perform partial digestion.  Alimentary Canal and Digestion Crop Loss Assessment This refers to the procedure for assessing arthropod impact on crop yield and quality.  Methods of Measuring Crop Losses Crop Residue References Andow D (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–86 Bach CE (1980) Effects of plant density and diversity in the population dynamics of a specialist herbivore, the striped cucumber beetle, Acalymma vittata. Ecology 61:1515–1530 Bach CE (1980) Effects of plant diversity and time of colonization on an herbivore-plant interaction. Oecologia 44:319–326 Pimentel D (1961) Species diversity and insect population outbreaks. Ann Entomol Soc Am 54:76–86 Risch SJ (1980) The population dynamics of several herbivorous beetles in a tropical agroecosystem: the effect of intercropping corn, beans and squash in Costa Rica. J Appl Ecol 17:593–612 Risch SJ (1981) Insect herbivore abundance in tropical monocultures and polycultures: an experimental test of two hypotheses. Ecology 62:1325–1340 Risch SJ, Andow D, Altieri MA (1983) Agroecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environ Entomol 12:625–629 A portion of the crop that is not harvested, and usually is returned to the land by tillage or as mulch. Crossing Over The reciprocal exchange of polynucleotides between homologous chromosomes during meiosis. Cross-Resistance In pest management, the resistance of a pest population to a pesticide to which it has not been exposed that accompanies the development of resistance to a pesticide to which it has been exposed. 1111 1112 C Cross-Striped Cabbageworm, Evergestris rimosalis (Guenée) (Lepidoptera: Pyralidae) Cross-Striped Cabbageworm, Evergestris rimosalis (Guenée) (Lepidoptera: Pyralidae) This is an important crucifer pest in the southern USA.  Crucifer Pests and their Management 1873! One can only wonder at what he might have accomplished had he not died so young. The insects that he collected in the Azores are in the Natural History Museum (London), whereas his Coccinellidae and Erotylidae are in the Museum of Comparative Zoology, Harvard University. Reference Cross Vein Short crosswise veins between the lengthwise wing veins and their branches. Most insects have only a few cross veins, but the netwinged species have numerous cross veins.  Wings of Insects Crotch, George Robert George Crotch was born in Cambridge in 1842 and obtained his undergraduate education at Cambridge University. While still a student he was deeply involved in collecting insects. By the time he received an M.A. degree (1863) he had concentrated on Coleoptera, and he published a Catalogue of British Coleoptera. The next year he collected insects in the Canary Islands and, on return to England, obtained a job in the university library at Cambridge. In 1865 and 1870 he made collecting trips to Spain, and meanwhile had published several entomological papers including works on Coccinellidae and Erotylidae and had become sub-editor of Zoological Record. In the autumn of 1872 he sailed to the USA and traveled overland to California in the spring of 1873. A collecting expedition to British Columbia, Oregon and parts of California followed. In the autumn of 1873 he returned to Philadelphia (his point of arrival in the USA), having accepted an appointment from Louis Agassiz to curate insects in the Museum of Comparative Zoology at Harvard University. However, he had been infected with “consumption” (tuberculosis), of which he died on June 16, 1874. Despite his travel and illness, he published eight papers on North American Coleoptera in *Essig EO (1931) Crotch, George Robert. In: History of entomology. The Macmillan Company, New York, pp 598–600 Crowson, Roy Albert Roy Crowson was born in the county of Kent, England, on November 22, 1914. He graduated from University College, London, in 1936, and then began anatomical research on Coleoptera. He worked as assistant curator of the Tunbridge Wells Museum until World War II, when he served in the Royal Air Force. In 1948, he joined the Department of Zoology of Glasgow University. Numerous publications on structure of beetle adults and larvae followed, with more on classification, until his death. Major works were a series called “The natural classification of the families of Coleoptera” which (1955) were republished as a book, a (1971) book “Classification and biology,” and a (1981) book “The biology of the Coleoptera.” He died on May 13, 1999, survived by his wife, Betty. Reference Wheeler Q (2000) Professor Roy Albert Crowson 1914–1999. Coleopterists Bull 54:120–121 Crucifer A plant in the family Cruciferae, such as cabbage, broccoli, or collard. Crucifers also are called cole crops. Crucifer Pests and their Management Crucifer Flea Beetle, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae) This species is a pest of several crucifer crops.  Flea Beetles (Coleoptera: Chrysomelidae) Crucifer Pests and their Management Loke t. kok Virginia Polytechnic Institute and State University, Blacksburg, VA, USA Crucifer crops are members of the family Cruciferae and include cabbage, cauliflower, Brussels sprouts, broccoli, rape and mustard. Grown commercially or as garden vegetables, they attract a large number of insects. Since the common crucifer crops are introduced vegetables, most of the insect feeders originated in Europe or are species native to the United States that feed on a wide range of plants. The importance and abundance of a given insect species changes with location. Insects attacking crucifers can be divided into three groups: (i) leaf or foliage feeders, (ii) sap feeders, and (iii) root feeders. Leaf or Foliage Feeders: Caterpillars and Flea Beetles Caterpillars of moths, skippers, and butterflies in the order Lepidoptera are important leaf feeders. The adults have four large wings usually covered with brightly colored scales. The most common are the cabbage looper, the imported cabbageworm, and the diamondback moth. Two others with potential of becoming major pests are the cross-striped cabbageworm and the cabbage webworm. The rank of species importance generally varies with latitude. In the more southern areas of the United States, the cabbage looper is the most abundant, followed by the imported cabbageworm and the diamondback moth. C In the more northern latitudes, the cabbage looper populations become more variable and the imported cabbageworm becomes the dominant species. Both the cross-striped cabbageworm and the cabbage webworm are generally localized, occasional pests. The Imported Cabbageworm, Pieris rapae (L.) (Pieridae) The imported cabbageworm was first discovered in North America in 1860 when a single specimen was captured in Quebec. Nearly 30 years later, it had spread north to Hudson Bay, south to the Gulf of Mexico, and west to the Rocky Mountains. It now occurs throughout most of North America. It spends the winter as a cocoon in or near crucifer crops. In spring, the white adult (Fig. 126) butterfly emerges. The male butterfly has one black spot and the female has two black spots on each front wing. After mating, the female lays eggs within 24 h of emergence. Eggs are laid singly on the underside of the outer leaves of the plant. They hatch into caterpillars in four to eight days. The caterpillars molt four times and pass through five stages in 12–33 days. The dark velvety green caterpillars (Fig. 127) have a faint yellow stripe down the back and along the sides. They feed voraciously on leaves and reach 25 mm in length. When full grown, the caterpillar changes into a cocoon. Each cocoon changes to an adult butterfly in 8–20 days. The butterfly lives for approximately three weeks. Females generally lay 200–300 eggs. They generally have two to four generations a year, but as many as six generations have been observed in the southern portions of its range. A tiny wasp parasite, Cotesia glomerata (L.) (Hymenoptera: Braconidae), attacks the first three caterpillar stages. It lays 20–50 eggs into a caterpillar. The eggs hatch into parasite grubs that feed within the caterpillar. When the parasite grubs complete feeding on the caterpillar, they emerge as a group from the late fifth stage of the caterpillar, and spin yellow cocoons. The caterpillar dies. Cotesia rubecula (Marshall) is an exotic solitary wasp that is a close relative of C. glomerata. It generally attacks the first three caterpillar stages, 1113 1114 C Crucifer Pests and their Management Crucifer Pests and their Management, Figure 126 Imported cabbageworm adult. but it kills the imported cabbageworm caterpillar soon after it molts to the fourth caterpillar stage. The single C. rubecula grub inside it exits, and spins a white cocoon. Another parasitic wasp, Pteromalus puparum (L.) (Hymenoptera: Pteromalidae) attacks the cocoon stage of the imported cabbageworm. P. puparum is a gregarious internal parasite of the imported cabbageworm, attacking the newly formed cocoon. The parasitic grubs develop within the host and emerge as adult wasps through a small hole cut in the cocoon case. The Cabbage Looper, Trichoplusia ni (Hübner) (Noctuidae) The medium sized adult moth (Fig. 128) is grayish brown, about 25 mm long, with wing span of 38 mm. There is a silver figure 8 design near the center of each front wing. The back wings are light brown with a dark margin. In spring, about 300 eggs laid by a female singly on the upper and lower surfaces of leaves, hatch in three days into caterpillars. The caterpillar eats holes in leaves and reaches (Fig. 128) full size in two to four weeks. The green caterpillar forms a characteristic loop as it moves. It reaches 40 mm long when full grown and has a thin white line along each side of the body and two near the middle line of the back. It spins a cocoon and passes the winter in this stage. It emerges as an adult in spring. There are three to six generations a year. A parasitic fly, Voria ruralis (Fallén) (Diptera: Tachinidae), attacks the caterpillar. There are three parasitic wasps that attack the cocoon stage: Gambrus ultimus (Cresson), Stenichneumon culpator cincticornis (Cresson), and Vulgichneumon brevicinctor (Say) (Hymenoptera: Ichneumonidae). Diamondback Moth, Plutella xylostella (L.) (Plutellidae) The diamondback moth is a cosmopolitan insect. It is slender and grayish brown, 8.5 mm long, with Crucifer Pests and their Management C Crucifer Pests and their Management, Figure 127 Imported cabbageworm caterpillars. wing expanse of about 14 mm. When folded, the wings display three diamond-shaped yellow spots along the line where the wings meet. The colors of the female are lighter, and the markings less distinct than the males. The back or hind wings have a fringe of long hairs. The moth passes the winter under leaves. In spring, the moth lays an average of 160 small yellowish-white eggs that hatch in three to five days. The greenish caterpillars feed on the leaves and complete development in 10–30 days. The full-grown caterpillar (Fig. 129) is yellowish green with erect long black hairs. It forms a fine white mesh cocoon and the adult emerges in about a week. There are four to six generations a year in North America depending on temperature. In the tropics, there can be as many as 15–18 generations a year. The most common parasite of the caterpillar is a wasp, Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae), that is capable of killing up to 70% of the caterpillars. 1115 1116 C Crucifer Pests and their Management Cross-striped Cabbageworm, Evergestis rimosalis (Guenée) (Pyralidae) The adult is a small yellowish brown moth(Fig. 130) with a dark patch towards the end of the front margin of the front wing. The female lays about 80 eggs in small overlapping masses on the host plant leaf. The eggs are yellow, flattened, and hatch in three to seven days. There are four caterpillar stages that complete (Fig. 131) development in 6–17 days and change into a cocoon. The caterpillar is gray on the back and yellow on the lower side, with a broad distinctive black band on each side separating the gray from the yellow. The cocoon stage lasts for 9–10 days, before changing into the adult. There are three to four generations a year. This insect has the potential to be a very serious and destructive pest of crucifer crops in the eastern United States. The young caterpillars feed on leaves but the mature caterpillars migrate to the heart or head of the plant and can riddle the head with feeding holes making the plant unmarketable. It is naturally kept in check by a parasitic wasp, Cotesia orobenae Forbes (Hymenoptera: Braconidae), that feeds on the caterpillar. Indiscriminate use of insecticides that kill off the parasite will result in outbreaks of the cross-striped cabbageworm. Cabbage Webworm, Hellula rogatalis (Hulst) (Lepidoptera: Pyralidae) Crucifer Pests and their Management, Figure 128 Cabbage looper adult. The cabbage webworm is a sporadic but destructive pest of crucifer crops in the southeastern United States. It is potentially the most serious pest of broccoli. The front wing of the moth is light brown and gray. The newly emerged adults start laying eggs in three to four days and can deposit up to 161 eggs per female. Newly laid eggs are yellowish green, and turn pink as they mature. Crucifer Pests and their Management, Figure 129 Diamondback moth caterpillar. Crucifer Pests and their Management C Crucifer Pests and their Management, Figure 130 Cross-striped cabbageworm adult. Crucifer Pests and their Management, Figure 131 Cross-striped cabbageworm caterpillars. Most of the eggs are laid on the upper surface of the leaf, and hatch in three to eight days. There are five caterpillar stages and they complete development in 15–35 days. The first two caterpillar stages mine the leaf between the upper and lower leaf surface (Fig. 132). The larger caterpillars feed on the underside of the leaf causing them to curl and roll up. They also spin webs among the rolled leaves. The webs protect them from insecticide sprays. The last two caterpillar stages feed on the leaf and midrib, breaking it into two. The caterpillar moves to the heads after eating the leaves. The cocoon stage lasts for 7–17 days before changing to adult. The adult lives for 11–25 days. There are 1117 1118 C Crucifer Pests and their Management Crucifer Pests and their Management, Figure 132 Cabbage webworm damage. one to two generations per year. It is difficult to control cabbage webworms because the caterpillars are protected and there are no effective parasites that attack them. Occasional Caterpillar Pests Caterpillars that are occasional or minor pests include the corn earworm Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae); fall armyworm, Spodoptera frugiperda (J. E.Smith) (Lepidoptera: Noctuidae); green cloverworm, Plathypena scabra (Fabricius) (Lepidoptera: Noctuidae); yellowstriped armyworm (Lepidoptera: Noctuidae), and southern cabbageworm, Pontia protodice (Boisduval & LeConte) (Lepidoptera: Pieridae). Severe feeding on the leaves by these caterpillars results in loss of crop yield. All plant stages, from seedling to heading, are susceptible to attack. Before a management program is initiated, it is important to have an understanding of the occurrence of the individual species and their life stages during the growing season. Flea Beetles (Coleoptera: Chrysomelidae) Flea beetles are small elongate, oval, black beetles of 1.6–3.2 mm with back legs enlarged for jumping. When disturbed, they jump up resembling fleas bouncing up and down, hence their common name, flea beetles. The adult beetle is a general feeder of leaves, leaving tiny pits or small holes. When they are present in large numbers, their feeding can cause pitted areas and numerous holes on leaves. There are two common species among crucifers, the potato flea beetle Epitrix cucumeris (Harris) and the tobacco flea beetle Epitrix hirtipennis (Melsheimer). Eggs of flea beetles are very tiny and difficult to see. The potato flea beetle scatters its eggs in the soil close to roots of host plants. The tobacco flea beetle eggs are laid in batches or clusters. They hatch in about 10 days into whitish, slender, cylindrical worms that feed on the roots of weeds and crucifer plants. The worms or grubs usually do not cause as much damage as the adults. When full grown in about four weeks, the worms are 3.2–8 mm long, Crucifer Pests and their Management and have tiny legs and brownish heads. They change into the cocoon stage that lasts for 7–10 days before emerging as adults. There are usually one to two generations a year. Flea beetles are very common on new plantings and can cause severe damage to young seedlings or plants. They often infest weeds near crucifer crops and move onto young plants. Heavy infestations cause young plants to dry up. Sap Feeders: Harlequin Bugs, Aphids Harlequin bugs and aphids are the most serious sap feeders of crucifers. They can be especially damaging to young plants that cannot withstand as much damage as the larger plants. Thus, they are often serious pests during the early plantings or transplantings of crucifers. Both the adults and young nymphs suck sap from the plants. Harlequin Bug, Murgantia histrionica (Hahn) (Heteroptera: Pentatomidae) The harlequin bug (Figs. 133 and 134) is an exotic pest originating in Central America. It was first recorded in the United States in 1864. It passes the winter south of the 40°N latitude. Individuals found north of the 40°N latitude most likely are carried by wind currents or are due to seasonal migration. It was considered the most destructive insect pest of crucifers in the United States before the use of synthetic insecticides because it is capable of destroying entire crops. After the advent of synthetic insecticides, the importance of the harlequin bug declined. However, the harlequin bug has often caused substantial damage in crucifers during the past decade when insecticides were not used. The harlequin bug has a wide host range and has been reported to feed on over 50 species of plants, including crucifers. Cabbage, collards, broccoli, Brussels sprouts, kale, mustard, turnip, C and cauliflower are a few of the economically important crops attacked by this pest. It also has been found on many wild plants, allowing the bugs to survive when crucifers are not present. The number of harlequin bug generations per year varies by location. There are two generations in the north and up to five generations in the South. In the North, the adult finds shelter in cabbage stalks, grass or other debris. In the South, the insects feed and breed during the entire year. The adults become active in spring when they start feeding on weeds, and are ready to lay an average of 150 eggs when garden plants or crucifers are available. The tiny white eggs that look like kegs are laid mostly on the underside of leaves in two rows. There are normally 12 eggs per batch, and each egg has two broad black loops. They hatch in 4–29 days, depending on temperature into young (nymph) bugs. The young bugs molt after five days. Each developing bug molts four times and passes through five nymphal stages in about 45 days to reach the adult stage. Feeding damage results in death of young plants. The younger plants succumb to feeding injury sooner than the older plants. Time to death is shorter when larger numbers of harlequin bugs feed together on the same plant. Cabbage Aphids, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) Cabbage aphids are green, soft-bodied insects often referred to as plant lice because of the large numbers and their rapid rate of reproduction. They are 1.6– 3.2 mm in length. They feed by inserting their sharp needle-like stylets in their beaks into plant tissues and suck sap from the plant.Affected leaves (Fig. 135) curl and crinkle or become deformed. During severe infestations, they cover the whole plant, causing the plant to wilt and die. Infested plants that survive are shorter and grow more slowly, and cabbage heads that are formed are light in weight and are not suitable for marketing. The aphid can reproduce by normal sexual reproduction and asexually without 1119 1120 C Crucifer Pests and their Management Crucifer Pests and their Management, Figure 133 Harlequin bug adults on rape. mating. Sexual reproduction occurs in the fall when winged males and females are formed. These are the fall migrants that leave the summer host. The winged females produce wingless females that mate with the males of the previous generation. After mating, the true female lays small black fertilized eggs in a sheltered place to pass the winter. From these eggs rise the stem mother the next year. The eggs hatch into small nymphs (young aphids) and grow to full size as stem mothers with warmer weather. These stem mothers are wingless. Each can reproduce without mating and gives rise to 50–100 eggs that hatch while they are still inside the stem mother and emerge as active nymphs in 7–14 days. These young nymphs can reproduce just like their stem mothers within a week. Each generation takes about a month. The number of generations depends on temperature, and in the far south, they continue to breed year round. Several natural enemies feed on aphids. The most common predators are grubs and adults of ladybird beetles and green lacewings, and the maggots of the flower (syrphid) fly. These usually keep the aphid population down. During heavy infestations, chemical sprays or insecticidal soaps may have to be used. For chemical sprays to be effective, they have to reach the underside of the leaves where the aphids usually lodge. Root Feeder: Cabbage Maggot Cabbage Maggot, Delia radicum (L.) (Diptera: Anthomyiidae) This is a serious pest in the northern states above 40°N latitude, and in Canada. The adult fly resembles a housefly and is dark ash gray in color, but is smaller, 6.4 mm long. It lays its eggs in cracks and crevices in the soil near the roots. The eggs hatch in three to seven days into small maggots. The maggots feed on the roots of crucifers below ground level and thus are not easily seen. Small Crucifer Pests and their Management Crucifer Pests and their Management, Figure 134 Harlequin bug nymph. Crucifer Pests and their Management, Figure 135 Cabbage aphids. C 1121 1122 C Crypsis roots are entirely eaten and larger roots show feeding tunnels caused by the maggots. Heavy feeding causes the plant to wilt and become stunted. Such plants have a sickly color. The maggots are white, 6.4–8.5 mm and without legs, and feed for three to four weeks to reach full size. They move away from the root to the soil and form a brown casing called the puparium within the top few inches of the soil. The puparium stage lasts for two to three weeks. The adult fly that emerges begins laying eggs. There are two to four generations a year. The winter is passed in the quiescent pupa stage inside the puparium casing. To control this fly, it is best to cover the seedbeds of crucifers with thin cloth or fine mesh gauze. Insecticidal drenches also can be used at the time of planting or transplanting. References Chamberlin JR, Kok LT (1986) Cabbage lepidopterous pests and their parasites in southwestern Virginia. J Econ Entomol 79:629–632 Kok LT, Acosta-Martinez JA (2001) Development of Cotesia orobenae Forbes (Hymenoptera: Braconidae) in its host, Evergestis rimosalis (Gueneé) (Lepidoptera: Pyralidae). J Entomol Sci 36:9–16 Kok LT, McAvoy TJ (1989) Fall broccoli pests and their parasites in Virginia. J Entomol Sci 24:258–265 Lasota JA, Kok LT (1989) Seasonal abundance of imported cabbageworm (Lepidoptera: Pieridae), cabbage looper (Lepidoptera: Noctuidae), and diamondback moth (Lepidoptera: Plutellidae) on cabbage in southwestern Virginia. J Econ Entomol 82:811–818 Ludwig SW, Kok LT (2001) Harlequin bug, Murgantia histrionica (Hahn) (Heteroptera: Pentatomidae) development on three crucifers and feeding damage on broccoli. Crop Prot 20:247–251 Mays WT, Kok LT (1997) Oviposition, development, and host preference of the cross-striped cabbageworm (Lepidoptera: Pyralidae). Environ Entomol 26:1354–1360 Crypsis maLCoLm edmunds University of Central Lancashire, Preston, UK Crypsis is a Greek word meaning camouflage. An animal that is cryptic is one that is camouflaged so that it is difficult to discern from its background. The advantage of crypsis in most animals is that it gives protection against predators that detect prey by eyesight. For example, many green caterpillars are camouflaged on leaves, giving them protection against insectivorous birds. Some predators are also cryptic which enables them to get close to prey that detect predators visually. For example, a lion or a leopard crouching in yellow-brown grass is well camouflaged so its prey may inadvertently wander close to it. Among arthropods, the flower mantids Pseudocreobotra and Hymenopus, and the crab spider Misumena (Thomisidae), are all cryptic when resting on flowers while waiting to grab insects that visit the flower for nectar or pollen. Crypsis here could be both a defense against predators (Figs. 136 and 137) and also an aid for capturing insects that visit the flowers but do not see them. However, it has not been demonstrated that fewer insects visit flowers with conspicuous rather than with cryptic predators on them, so this suggestion remains unproven. The simplest form of camouflage involves the animal’s color matching that of its background, e.g., green lacewings, Chrysopa (Neuroptera), on green leaves or transparent mosquito larvae in the plankton of ponds. However, birds and some other vertebrate predators have excellent eyesight and can recognize a simply camouflaged insect either by the shadow on its lower surface or by its characteristic outline. Two evolutionary responses of cryptic insects to such predators are “countershading” and “disruptive coloration.” Green grasshoppers are cylindrical so, when sunlight comes from above, the ventral surface will be in shadow and hence appear to be darker green than the dorsal surface. Countershaded grasshoppers are paler green ventrally so that this shadow is reduced and the crypsis is improved because the animal appears uniformly green in side view. Green hawkmoth caterpillars usually rest upside down under leaves and stems and have reversed countershading with the upper ventral surface dark green and the lower dorsal surface pale green. Crypsis C Crypsis, Figure 136 The eyed hawkmoth (Smerinthus ocellata) larva showing reverse countershading. When the larva rests in its normal orientation (left), the body appears flat due to the lighter coloration of the dorsal surface of the insect. When the twig bearing the larva is inverted (right), the larva becomes very conspicuous as the sun shining on the light dorsum increases the contrast between the insect’s dorsal and ventral surfaces (photos by M. Edmunds). Crypsis, Figure 137 Shorthorn grasshoppers mating, with disruptive black markings that break-up the body outline and conceal the eye (photo by M. Edmunds). Many green grasshoppers have black streaks and stripes on their bodies which draw the eyes of predators to these marks rather than to the contour of the insect. These are disruptive colors. Similar disruptive markings occur in caterpillars, shield bugs and many other cryptic insects. Large compound eyes are possibly a feature by which vertebrate predators can recognize an otherwise well camouflaged insect. One way of concealing the eye is for disruptive lines to pass through it so that attention is drawn away from the eye to the line which does not look like insect prey. Disruptive eyestripes occur in many 1123 1124 C Crypsis grasshoppers. It is probable that disruptive colors increase the probability that a prey insect will not be found by a predator, but this has not been demonstrated experimentally. Crypsis can also be perfected by morphological adaptations, e.g., by flattening of the body so there is no ventral shadow, or by resembling a specific part of the environment, such as a stick or a leaf. Some (Figs. 138 and 139) green lycaenid caterpillars, the green Australian mantid Neomantis (both on green leaves) and the brown mantis Theopompa and bug Dysodius (both on bark) are all flattened so there is no ventral shadow. Other insects have excrescences that break up the body outline, e.g., the grass-living mantis Pyrgomantis and the grasshopper Cannula are both long and slender with a pointed vertex on the head so they resemble a blade of grass, while the mantids Phyllocrania and Hemiempusa both have foliose excrescences (leaf-like outgrowths) on the legs and head (Fig. 140). Looper caterpillars of geometrid and noctuid moths are usually brown with minute legs which are barely visible close to the head, and a slender, cylindrical body that may be rugose like the bark of a twig. They rest with the posterior claspers gripping a branch and the body extended in a straight line like a broken twig. Stick insects (Phasmida) and some praying mantids (e.g., Danuria, Heterochaeta, Angela) also have slender bodies and appropriate resting postures such that they closely resemble sticks, while leaf insects (Phasmida) and some mantids (Choerododis, Phyllocrania), butterflies (Kallima), and grasshoppers (Zabilius) closely resemble individual leaves. Some caterpillars rest conspicuously on the upper surfaces of leaves and closely resemble black and white bird droppings. Since insectivorous birds normally ignore droppings this probably gives good protection. However, as the caterpiller grows it becomes too large to mimic a bird dropping. The final instar of the alder moth (Apatele almi) is black and yellow (either aposematic or mimicking a wasp), that of Trilocha kolga changes to resemble the brown and black feces of a large lizard or bird. In Oxytenis naemia the final instar resembles brown leaf detritus fallen from the canopy, while in species of Papilio it is disruptively colored green and black and no longer rests on top of leaves. There is also a cicada, Ityraea, where a cluster of insects resembles a spike of flowers. These highly specific resemblances have been called stick mimicry, leaf mimicry, bird dropping mimicry, etc. However, since they have presumably evolved from simple camouflage by Crypsis, Figure 138 The brown chrysalis of the hawkmoth, Atemnora westermanni, resembles a dead leaf lying amongst brown leaves on the forest floor of Ghana (photo by M. Edmunds). Crypsis C Crypsis, Figure 139 The mantid, Neomantis australis, from Queensland, Australia, shows cryptic green coloration and a flattened body that reduces shadow (photo by M. Edmunds). predator selection progressively eliminating the more easily found insects, they are probably better considered as extreme forms of crypsis, and Cott called them examples of “special resemblance.” A cryptic insect is only well camouflaged when on the correct background, but if it moves somewhere else or if the background changes it is immediately vulnerable to predation. Many cryptic insects move until they find a suitable background on which to rest, typically one on which they are cryptic. Thus, when the polymorphic grasshopper Acrida turrita was given a choice of backgrounds, significantly more green than yellow insects rested on a green background and significantly more yellow than green insects rested on a yellow background (p<0.001 in both cases). Similar background choice occurs in other polymorphic grasshoppers and in praying mantids, resulting in green insects tending to rest on green substrates and brown ones to rest on brown substrates. Bark-resting moths with disruptive markings adopt resting postures which align their markings with similar marks on the tree. The geometrid moth Melanolophia canadaria normally rests sideways with its markings running vertically parallel to striations in the bark. Given a choice of resting on a white surface with vertical or horizontal black tape strips, Sargent found that significantly more insects rested with the markings parallel to the strips (p<0.001) giving excellent camouflage, but equal numbers rested sideways and vertically (with head up or down), so the moth adjusts its resting position to coincide with the strips. When the experiment was repeated with the strips covered with acetate so that there was no difference in texture, the resting positions of the moths were random with respect to the strips, with equal numbers facing sideways and vertically, so Sargent concluded that the resting position of this moth is determined by tactile rather than visual stimuli. The noctuid moth Catocala ultronia normally rests with the head down and the markings parallel with vertical ridges on the bark. In a similar experiment, significantly more insects rested with their markings aligned to the strips giving good camouflage (p<0.05), and almost all moths rested head vertically down rather than horizontally (p<0.001). The resting positions were unchanged if the strips were covered with acetate, so in this species, resting posture is innate and not modified by substrate pattern or texture. 1125 1126 C Crypsis Crypsis, Figure 140 The brown leaf mimicking preying mantid, Phyllocrania paradoxa, rests on brown dead vegetation in Ghana. Note the frills on head, body, and legs which break up the outline of the insect (photo by M. Edmunds). Some cryptic insects can change color (Fig. 141) so that they match their background, but this change usually takes several days or occurs only when the insect moults. Some swallowtail and other butterfly pupae can be either green or brown, usually matching their substrate. Details vary in different species, but in Papilio polyxenes short daylength induces most caterpillars to turn into brown pupae which are well camouflaged during the winter on deciduous shrubs. However, with a long photoperiod (i.e., in summer), pupae were usually brown on thick branches but green on thin twigs, giving good camouflage both on brown branches and on green twigs close to green leaves. Final instar poplar hawkmoth caterpillars (Laothoe populi) can be green or white depending on whether they are resting on green or whiteleaved food plants. When reared on two different Crypsis C Crypsis, Figure 141 This satyrid butterfly, Paralaza nepalica, from Nepal blends into a sandy background (photo by A. Sourakov). plants significantly more sibling poplar hawk caterpillars on green leaved Salix fragilis became green rather than white while significantly more reared on white-leaved Populus alba became white. Similarly, various grasshoppers and praying mantids can be green or brown depending on whether their substrate is green or brown. In all examples that have been studied, the specific cue that determines which color the insect becomes is not substrate color but some other factor such as humidity (in the mantid Miomantis paykullii and the grasshopper Syrbula admirabilis), light intensity (in the mantid Sphodromantis lineola), or substrate reflectance (in the hawkmoth Laothoe populi). Finally, there is abundant experimental evidence that crypsis does indeed reduce predation on insects. Most experiments involve placing some insects on a background where they are camouflaged and others on one where they are conspicuous and then exposing them to predators either in the laboratory or in the field. Polymorphic insects are especially good experimental subjects because the two morphs can be placed on two backgrounds, one of which matches the color of each morph. Experiments of this type have shown the selective advantage of resting on a background where the insect is cryptic in the peppared moth (Biston betularia), caterpillars of the pine looper (Bupalus piniarus) and poplar hawkmoth (Laothoe populi), grasshoppers (Acrida turrita), and praying mantids (Mantis religiosa). Experiments have also shown that countershaded green pastry prey were found significantly less often by wild birds than were uniformly green prey, so demonstrating the selective advantage of countershading. It is tempting to ask why, if crypsis is of such great advantage to an animal, many more animals are not cryptic. The main reason is because cryptic animals must remain motionless, and adaptations that perfect crypsis may conflict with other essential activities such as feeding, escape by running or flying, or finding a mate. However, predators can become more proficient at finding cryptic prey by developing a “searching image” for specific insects. One evolutionary response to this aspect of predator behavior is for the prey to evolve several different color forms (polymorphism) such that the density of each morph remains low and the predator must acquire several different searching images if it is to fully exploit the prey population. Cryptic polymorphic insects occur among grasshoppers (Acrida), mantids (Mantis, Sphodromantis), 1127 1128 C Cryptobiosis hemipterans (Philaenus spumarius), caterpillars (Bupalus piniarus, Herse convolvuli), and moths (Biston betularia). References Cott HB (1940) Adaptive coloration in animals. Methuen, London, UK, 508 pp Edmunds M (1974) Defence in animals: a survey of antipredator defences. Longman, Harlow, UK, 357 pp Edmunds M, Evans DL, Schmidt JO (eds) (1990) Insect defences. State University of New York, Longman, Harlow, UK, pp 3–21 Edmunds M, Dewhirst RA (1994) The survival value of countershading with wild birds as predators. Biol J Linn Soc 51:447–452 Edmunds M, Grayson J (1991) Camouflage and selective predation in caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata). Biol J Linn Soc 42:467–480 Wickler W (1968) Mimicry in plants and animals. Wiedenfeld & Nicholson, London, UK, 255 pp Cryptobiosis takashi okuda National Institute of Agrobiological Sciences, Ohwashi, Tsukuba, Japan Cryptobiosis is defined as the state of organism when it shows no visible signs of life and when its metabolic activity becomes hardly measurable, or comes reversibly to a standstill. Cryptobiosis is a generic term for ametabolism, and can be further divided into five categories based on factors inducing them: cryobiosis (induced by freezing), thermobiosis (low and high temperatures), osmobiosis (high osmolarity), anhydrobiosis (lack of water) and anoxybiosis (lack of oxygen). So far, the African chironomid Polypedilum vanderplanki is the only insect species exhibiting cryptobiosis (anhydrobiosis, in this case). The larvae of this chironomid live in small and shallow rock pools. When the pool dries up during the dry season, the larvae become completely desiccated. When the rainy season comes and the pool fills with water, they may revive after rehydration. The desiccated larvae also become resistant to extreme temperature conditions. So far, 17 years is the longest record of dormancy for this insect. When given water, the larvae quickly become active, usually within one hour, with no ill effects. Slow dehydration is more beneficial for the insect than rapid dehydration. Larvae make tubes by incorporating detritus and soil with their sticky saliva. The tube serves not only as a physical barrier against enemies and aids in feeding, but also reduces the dehydration rate. In the absence of tubes, larvae do not survive rehydration. During the dehydration process, larvae accumulate large amounts of trehalose (up to 20%), which provides effective protection against desiccation because of its high capacity for water replacement and vitrification. Although membranes are impermeable to trehalose, a trehalose transporter is expressed in the fat body, allowing trehalose production and transport into the hemolymph. Trehalose also serves to protect proteins and cell membranes. Late embryogenesis abundant (LEA) proteins occur in the dehydrating larvae, preventing protein aggregation when concentrated upon desiccation. The anhydrobiotic larvae attain tolerance to several extreme conditions to such an extent that they can revive after expose to -270 to + 103°C, irradiation up to 9 k Gy, and submersion in pure ethanol. References Clegg JS (2001) Cryptobiosis – a peculiar state of biological organization. Comp Biochem Physiol B 128:613–624 Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599 Kikawada T, Minakawa N, Watanabe M, Okuda T (2005) Factors inducing successful anhydrobiosis in the African Chironomid Polypedilum vanderplanki: Significance of the larval tubular nest. Integr Comp Biol 45:710–714 Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata K, Tanaka D, Watanabe M, Okuda T (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci USA 104:11585–11590 Csiki, Ernõ; (Ernst Dietl) Watanabe M, Kikawada T, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205: 2799–2802 Watanabe M, Nakahara Y, Sakashita T, Kikawada T, Fujita A, Hamada N, Horikawa D, Wada S, Kobayashi Y, Okuda T (2007) Physiological changes leading to anhydrobiosis improve radiation tolerance in Polypedilum vanderplanki larvae. J Insect Physiol 53:573–579 Cryptoceridae A family of cockroaches (order Blattodea).  Cockroaches Cryptochetid Flies Members of the family Cryptochetidae (order Diptera).  Flies Cryptochetidae A family of flies (order Diptera). They commonly are known as cryptochetid flies.  Flies Cryptophagidae A family of beetles (order Coleoptera). They commonly are known as silken fungus beetles.  Beetles Cryptorhamphidae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs Crystalliferous Producing or bearing crystals. This term is applied to a number of Bacillus and Paenibacillus species C which, in addition to the endospore, produce a discrete, characteristic crystal or crystal-like inclusion in the sporulating cell. Csiki, Ernõ; (Ernst Dietl) GeorGe hanGay1, otto merkL2, Győző széL 1 Narrabeen, New South Wales, Australia 2 Hungarian Natural History Museum, Budapest, Hungary Ernst Dietl was born on the October 22, 1875 at Zsilvajdejvulka, Hunyad Shire, Transylvania, Hungary, today Vulcan, Romania. In 1897 he graduated at the College of Veterinary in Budapest and shortly afterwards gained employment in the Hungarian National Museum’s Zoological Collections as assistant curator. He was mainly responsible for the library and the beetle collection. In 1898 he changed his original German name to the Hungarian “Csiki.” He remained in the service of the museum until his retirement in 1933, eventually ascending to the position of Departmental Head or Director. After his retirement he withdrew from active work for a few years but as World War II ended, he returned to the museum as an outside consultant to continue with his entomological activities. In 1953, at the age of 78 he received the Doctor of Biological Sciences degree. He has passed away in Budapest, on the 7th of July 1954. Ernő Csiki was probably the first Hungarian museum entomologist who could devote his entire active life to his chosen group of insects, the Coleoptera. During his years the museum’s beetle collection grew from 120,000 to well over one million specimens. This unprecedental growth was partially due to the personal collecting activities of Csiki which yielded more than 60,000 beetles and partially to the fact that in those years the museum had sufficient funds for purchasing valuable collections. One of the most notable acquisitions was Reitter’s European and Asian collection, containing over 200,000 specimens and more than 5,000 types. Ernő Csiki was 1129 1130 C Ctenidium (pl . ctenidia) one of the most prolific Hungarian coleopterists, describing more than 400 species, publishing 451 works containing over 9,000 pages. He had a wide interest, although the Carabidae was his favorite group. His major work, Die Käferfauna des Karpaten-Beckens, 1946 is still considered a fundamental monograph of the Central-European Carabidae. He was a major contributor to the Junk- Schenkling Coleoptorum Catalogus. He wrote 4,748 pages for the volumes published between 1910 and 1940. During his life he received numerous awards and prizes, and earned the respect of all his colleagues. In the Second District of Budapest, where he lived, a street was named Beetle Street, (Bogár utca) in honor of Ernő Csiki. References Sachtleben H (1955) Gestorben Dr. Ernő Csiki. Beiträge zur Entomologie 5:454 Székessy Vilmos (1954) Dr. Ernő Csiki (1875–1954). Folia enomologica hungarica (S. N.) 7:1–20 Székessy Vilmos (1955) Csiki Ernő emlékezete. állattani Közlemények 45:7–10 Ctenidium (pl. ctenidia) A comb-like structure found on any part of an insect, but particularly the comb of flat spines found in fleas and certain beetles. Cubitus The fifth longitudinal wing vein. It extends from the wing base and usually is two-branched before reaching the wing margin. Cuckoo Bees Members of the family Anthrophoridae (order Hymenoptera, superfamily Apoidae).  Bees  Wasps, Ants, Bees, and Sawflies Cuckoo Wasps Members of the family Chrysididae (order Hymenoptera).  Wasps, Ants, Bees, and Sawflies Cucujidae A family of beetles (order Coleoptera). They commonly are known as flat bark beetles.  Beetles Cucurbit A plant in the family Cucurbitaceae, such as cucumber, squash, and watermelon. Cucurbit Yellow Vine Disease Ctenoplectidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees, and Sawflies This disease occurs in North America, and squash bug is thought to be the vector.  Transmission of Plant Diseases by Insects Culicidae Ctenostylidae A family of flies (order Diptera).  Flies A family of flies (order Diptera). They commonly are known as mosquitoes.  Mosquitoes  Flies Cultivation Culicifuge A mosquito repellent. This term is derived from the family name for mosquitoes (Culicidae) and the Latin verb “fugere” (to flee). Culicinomyces clavisporus One species of the genus Culicinomyces, C. clavisporus, includes Australian, American and Canadian strains isolated from the mosquitoes Anopheles hilli, A. quadrimaculatus, and Culiseta inornata, respectively. The fungus is able to infect mosquito genera that transmit diseases in higher animals (e.g., Anopheles, Culex, and Aedes). Culicinomyces clavisporus also is pathogenic to some other aquatic dipteran larvae in the families Chironomidae, Ceratopogonidae, Simuliidae, Syrphidae, and Ephydridae. The three strains vary with respect to colony morphology, conidial development, and growth rates in different media; all three exhibit conidial dimorphism, with the smaller type of conidia more abundantly produced in the Australian and American strains. In addition, conidia can be generated on polyphialides, phialides with more than one neck, in all of the isolates. The gray-white colonies can appear more darkly pigmented in all of the strains depending upon culture conditions. Culicinomyces has been targeted as a potential biocontrol agent because it is easily cultured under surface or submerged conditions, and because it can recycle within mosquito populations. Recycling is due to the formation of external spores on dead, infected larvae which infect later generations of larvae either from the same genus or a different one. Culicinomyces clavisporus is unusual because its submerged conidia are produced both in vitro and in vivo, and it invades host larvae through the digestive tract (foregut) rather than the outer integument. Ingested conidia adhere to the cuticle of the digestive tract via their sticky outer coating. This bonding between the conidia and host epicuticle is strong enough to resist mechanical disruption by movements of the gut wall. Growth of C C. clavisporus germ tubes through host cuticle takes 6–18 hours. Melanized areas can form in the cuticle around the advancing hyphae, and the fungus is then forced to grow around this resistant material. As in the cuticle, zones of melanization also can develop in the hypodermis. Cylindrical blastospores form by budding from the hyphae and circulate in the hemolymph. Mycelial formation follows, and conidiophores eventually grow out through the thorax, abdomen, mouthparts, and bases of antennae. A dense layer of conidia is produced on the cadaver; however, the degree of sporulation depends upon the time of larval death. If the larvae die before they are completely filled with mycelia, external conidia may not form. It is speculated that toxins released by the high concentration of penetrating hyphae contribute to such rapid larval death because normally, up to one week is required for larvae to succumb to a Culicinomyces infection. References Cooper RD, Sweeney AW (1986) Laboratory studies on the recycling potential of the mosquito pathogenic fungus Culicinomyces clavisporus. J Invertebr Pathol 48:152–158 Goettel MS, Sigler L, Carmichael JW (1984) Studies on the mosquito pathogenic hyphomycete Culicinomyces clavisporis. Mycologia 76:614–625 Sweeney AW, Inmann AO, Bland CE, Wright RG (1983) The fine structure of Culicinomyces clavisporus invading mosquito larvae. J Invertebr Pathol 42:224–243 Cultivar An agricultural plant variety or strain developed for specific horticultural properties. Cultivation A tillage operation used to prepare land for cultivation. Cultivation also disrupts pest populations, including weeds and soil insects.  Cultural Control of Insect Pests 1131 1132 C Cultural Control of Insect Pests Cultural Control of Insect Pests John aLL University of Georgia, Athens, GA, USA Cultural control is using the production or utilization methods of a commodity with a concern for insect management. Cultural control practices are usually multipurpose technical procedures that create environments that either avoid high-risk situations for infestations or develop unfavorable conditions for pests. The operations are often the foundation of preventive control strategies in integrated pest management (IPM) programs. Cultural controls are not usually intended to suppress insect outbreaks, but are designed to prevent infestations from developing. These control methods are usually inexpensive because they are generally necessary for producing or using a commodity often with pest management as a secondary priority. Designing and implementing cultural control in IPM programs may call for greater professional competence, because greater knowledge of insect biology and behavior is usually required as compared to other insect management methods (e.g., control with insecticides). Patience and perseverance are important because the preventive nature of cultural control tactics often does not show tangible results other than a lack of pest problems on a commodity. Several cultural control methods are frequently combined with other pest management techniques in IPM programs for a commodity. Examples of cultural control methods used independently or in concert with other insect management tactics in IPM programs are: Sanitation is destroying the habitat associated with a commodity so that insect pests are deprived of shelter, protection from natural enemies, overwintering sites, etc. Sanitation also refers to methods that destroy or remove insects directly from the commodity environment. Examples include destruction of infested weeds and crop debris in and around crop fields, use of vacuums and/or high pressure water or air to clean machinery in food processing areas and warehouses, removal of potential termite-infested wood around homes, and composting garden debris to eliminate pests. Pest endurance practices are methods designed to aid commodity tolerance of pests without economic damage. Examples of agricultural methods that stimulate optimum health and vigor in crops for tolerance of insect injury include using vigorous seed, good seedbed preparation, optimal fertilization, irrigation and weed control, thinning, pruning, etc. Pest preventive maintenance practices are procedures that keep commodity environments clean and free of materials where pests can build up and methods that ensure rapid movement of commodities through production, storage, and shipment in order not to allow time for pests to increase. Crop and cultivar selection is choosing crops and cultivars with consideration of their susceptibility or resistance to the insect pests, along with high yield, produce quality, and other desirable agronomic characteristics. It is using adapted crops and cultivars that have the greatest profit potential with the least hazard for insect problems. Crop and cultivar selection includes the use of insect resistant varieties (including insecticidal transgenic plants), but it also includes decisions to avoid high-risk crops or cultivars that could produce insect outbreaks. Examples include use of cotton and corn varieties that express insecticidal Cry proteins derived from the bacterium Bacillus thuringiensis Berliner or the use of wheat containing native resistant genes to the Hessian fly, Mayetiola hibiscella (Swazey). Crop rotation is switching plant species within an environment in order that a resident insect population which is adapted to one of the crops cannot survive when the other is planted into the field. An example would be using corn and soybean as field crops in alternate years so that larvae of western corn rootworm, Diabrotica virgifera virgifera LeConte, cannot survive the shift from host corn to non-host soybean. Crop rotation is applicable to other situations such as in greenhouses, plant nurseries, etc. and can be used during the same year in Culture of Natural Enemies on Factitious Foods and Artificial Diets fields where multicropping is used. Crop rotation is also applicable for stored products as when soybean and corn are alternated in grain bins to discourage the build up of granary weevils, Sitophilus spp., and meal moths, Pyralis farinalis L. Disruption of phenological synchrony is interfering with a pest population’s natural association with susceptible growth stages of a crop. Alternating planting and harvest dates and using cultivars of desirable maturity are ways that crop growth can be manipulated to avoid peak levels of pests during the season, for example, early planting of sweet corn to avoid high populations of corn earworm, Helicoverpa zea Boddie, and fall armyworm, Spodoptera frugiperda (J.E. Smith). Deception and concealment practices is using lures, trap crops, or polyculturing crops to either decoy or hide a commodity from infestations. Examples include placing Japanese beetle, Popillia japonica Newman, traps in the backyard to help lure adults away from landscape plants; using an early maturing soybean cultivar around the periphery of a soybean field as a trap crop for stinkbugs, Nezara spp.; and companion planting various herbs and aromatic plants to hide garden plants from pests.  Cover, Border and Trap Crops for Pest and Disease Management References All JN (1999) Ruberson JR (ed) Handbook of pest management. Marcel Dekker Inc., New York, pp 395–415 Rabb RL, (1984) Defoliart GK, Kennedy GG, Huffaker CB, Rabb RL (eds) (1984) Ecological entomology. Wiley, New York, pp 697–728 Rajendran B, Pimentel D (ed) (2002) Encyclopedia of pest management. Marcel Dekker, Inc., New York, 929 pp C insect pests and useful insects which falls into the realm of economic or applied entomology. The second is the study of the biology of insects for the sake of knowing without practical application, which is generally referred to as basic entomology. However, recently a distinct field of entomology has been recognized called cultural entomology. Cultural entomology is the study of the influence of insects and other terrestrial arthropods in literature, languages, music, the arts, interpretive history, religion, and recreation. Because the term “cultural” is narrowly defined, some aspects normally included in studies of human societies are excluded. Thus, ethnoentomology, which is concerned with all forms of insect-human interactions in so-called primitive societies, is not completely synonymous with cultural entomology. For example, practical uses of insects such as entomophagy as part of the diet, in pharmacology, or in other wholly practical uses of insects, are not the subject matter of cultural entomology. Where primitive societies have employed insects in cultural activities such as art and religion, ethnoentomology and cultural entomology overlap. Reference Hogue CL (1987) Cultural entomology. Annu Rev Entomol 32:181–99 Culture of Natural Enemies on Factitious Foods and Artificial Diets patriCk de CLerCq Ghent University, Ghent, Belgium Cultural Entomology ron Cherry University of Florida, Belle Glade, FL, USA Entomology has long been concerned with two general areas of study. The first is the study of The use of arthropod predators and parasitoids in augmentative biological control programs necessitates the availability of cost-effective mass rearing systems, allowing the production of large numbers of beneficials at the lowest possible price. 1133 1134 C Culture of Natural Enemies on Factitious Foods and Artificial Diets In many cases, suppliers of beneficial arthropods must resort to employing so-called natural rearing systems. Here, the beneficial is cultured on its natural host or prey, which itself is maintained on one of its food plants. Natural rearing systems can be economically viable, like the production of the parasitoid, Encarsia formosa, on tobacco plants infested with the greenhouse whitefly, Trialeurodes vaporariorum. In many cases, however, the necessity to maintain three trophic levels (natural enemy, host and host’s food plant) leads to problems of discontinuity and the high costs of rearing facilities and labor result in a high price of the natural enemies, making them more expensive than chemical controls. Costs may be lowered when the herbivorous host used for natural enemy production can be reared on an artificial diet in lieu of plants, which is the case for many lepidopteran larvae. Costs may be further reduced when natural enemies can be produced on unnatural or factitious hosts that are easier and less expensive to rear than the natural host. Factitious hosts are organisms that are not normally attacked by the beneficial, mostly because they do not occur in its natural habitat, but do sustain its development. Eggs of the lepidopterans Ephestia kuehniella and Sitotroga cerealella, are routinely used in the commercial production of various natural enemies including coccinellid beetles, lacewings, predaceous heteropterans, and egg parasitoids of the genus Trichogramma. Hatching of the eggs is prevented by gamma- or UV-irradiation or by freezing. Although these moths are easily produced on inexpensive foods (wheat flour or grains), there are substantial monetary investments for the mechanization of rearing procedures and for the health care of workers (repeated inhalation exposure to scales is known to cause allergies). Because of a continuously high demand, this has led to high market prices especially for Ephestia kuehniella eggs, amounting to $800 to $1,200 (U.S.) per kilogram by the end of the 1990s. Other insects that are frequently used as factitious food in commercial insectaries and research labs include larvae of the greater wax moth, Galleria mellonella (for several ichneumonid, braconid and tachinid parasitoids and for predatory stink bugs), and of the yellow mealworm, Tenebrio molitor (e.g., for reduviids and predatory stink bugs). Trichogramma wasps can also be successfully mass produced on eggs of the rice moth, Corcyra cephalonica and a number of silkworms, such as the Chinese oak silkworm, Antheraea pernyi. Commercial suppliers routinely use astigmatid mites such as Tyrophagus putrescentiae and Carpoglyphus lactis as prey for culturing a number of phytoseiid mites. Some non-insect materials also may hold promise for use as foods in insect mass culturing. It has been shown that the anthocorid Orius laevigatus and the mirid Macrolophus caliginosus can be reared on cysts of the brine shrimp, Artemia franciscana, with similar developmental and reproductive success as on Ephestia kuehniella eggs. Given that Artemia cysts are at least an order of magnitude cheaper than flour moth eggs, they may be an economically viable alternative food for the mass propagation of these heteropteran predators and possibly other predaceous insects. The availability of an artificial diet that supports the growth and reproduction of a natural enemy offers a further alternative for the rationalization and automation of mass rearing procedures. Ideally, biochemical analyses of the natural food along with studies of the digestive and absorptive physiology of the insect should be used as guidelines for diet definition, but in fact, many successes with artificial diets were based on a mere trial-and-error approach. A nutritionally adequate artificial diet should contain the basic nutrients (proteins or amino acids, lipids, carbohydrates) in appropriate proportions. In addition, some specific minor components may be needed as growth factors, like sterols, vitamins, minerals and nucleic acids. Further, the diet has to be formulated and presented in a manner that makes it acceptable for feeding or oviposition. Therefore, physical properties such as shape, hardness, texture, homogeneity and water content are important considerations. Inert filling or gelling agents, Culture of Natural Enemies on Factitious Foods and Artificial Diets like agar, cellulose and gelatin, have been used to obtain adequate consistency mainly in diets for insects with chewing mouthparts. Several materials have been used to wrap or encapsulate liquid and semi-liquid media, like paraffin, Parafilm and certain polymeric coatings. Measures can be taken to prevent spoilage of the food by micro-organisms. This can be done by adding anti-microbial or anti-fungal agents (provided they are non-toxic to the insect), by adjusting pH or by sterilizing the diet. Artificial diets have been classified in three general types: (i) holidic diets, in which all ingredients are known in chemical structure, (ii) meridic diets, which have a holidic base supplemented with one or more unrefined or chemically unknown substances (e.g., liver extracts, yeast products), and (iii) oligidic diets, which are mainly made up of crude organic materials (like meat diets). It is, however, not always easy to discriminate between these three diet types and, in fact, only a complete description of its composition is able to fully characterize an artificial diet. A more relevant criterion to categorize a diet is the presence or absence of insect components. Many artificial diets still contain host materials to fulfill the need for certain growth factors, or to supply feeding or oviposition stimuli. Insect additions can vary from small quantities of host hemolymph to whole host bodies. Supplementing artificial diets with insect materials again implies the dependence on parallel host cultures, which may lead to an increase in production costs. In some cases, however, insect components are inexpensive and easy to obtain, like the hemolymph from silkworms in the silk-producing areas of Asia and Latin America. As an alternative to hemolymph or host extracts, insect cell cultures have been used to serve as a source for essential host factors in the artificial rearing of certain parasitoids. A number of arthropod natural enemies have been reared with variable success on artificial media. Several predatory heteropterans, chrysopids and coccinellids have been reared for consecutive generations on diets devoid of insect materials. C Promising results have also been obtained with artificial diets for hymenopterous egg and pupal parasitoids and for tachinid larval parasitoids. Endoparasitoids (i.e., parasitoids which develop inside their hosts) are generally more difficult to rear on artificial media than ectoparasitoids or predators; for the larvae of endoparasitoids, the diet is not only their food, but also their living environment. In diets for endoparasitoids, oxygen supply, osmotic pressure and pH are major concerns. The situation is even more complex for koinobiontic endoparasitoids. These parasitoids do not immediately paralyze or kill their hosts, allowing them to continue to develop for some time after oviposition. As a consequence, the developing parasitoid larva has strong physiological interactions with the still living host, that often supplies it with specific growth factors. Finally, understanding interactions with microbial symbionts may be the key to success in developing an adequate artificial food for a number of entomophagous insects. The main concern for natural enemies produced on artificial (or factitious) food is their quality as biological control agents. Artificially fed natural enemies may diverge biologically from their naturally fed counterparts and may have impaired abilities to find or kill their natural host. Biological, biochemical, physiological and behavioral parameters can be used to assess the fitness of an artificially reared beneficial in the laboratory, but excellent field performance against the target pest remains the ultimate quality criterion. In the early 1990s, Trichogramma egg parasitoids were already being produced on artificial eggs at an industrial scale in China; the parasitoids were being released on thousands of hectares resulting in excellent control of different lepidopterous crop pests. In the United States and Europe, biocontrol companies have also started to integrate artificial diets in their production process and some beneficials are at least partially being reared on artificial foods.  Augmentative Biological Control  Rearing of Insects 1135 1136 C Cuneus References Arijs Y, De Clercq P (2001) Rearing Orius laevigatus on cysts of the brine shrimp Artemia franciscana. Biol Control 21:79–83 Cohen AC (2004) Insect diets. Science and technology. CRC Press, Boca Raton, FL, 324 pp Etzel LK, Legner EF, Bellows TS, Fisher TW (eds) (1999) Handbook of biological control. Academic Press, San Diego, CA, pp 125–197 Grenier S, De Clercq P, van Lenteren JC (eds) (2003) Quality control and production of biological control agents. Theory and testing procedures, CABI Publishing, Wallingford, UK, pp 115–131 Thompson SN (1999) Nutrition and culture of entomophagous insects. Annu Rev Entomol 44:561–592 Waage JK, Carl KP, Mills NJ, Greathead DJ, Singh P, Moore RF (eds)(1985) Handbook of insect rearing, vol I. Elsevier, Amsterdam, The Netherlands, pp 45–66 Curculionidae A family of beetles (order Coleoptera). They commonly are known as snout beetles or weevils.  Beetles  Weevils, Billbugs, Bark Beetles and Others (Coleoptera: Curculionidae) Curculionoid Larva A larval body form that is robust, C-shaped, with a well-developed head. It is found in the weevils (Curculionidae) and the first instar of Bruchidae (both Coleoptera). Curran, Charles Howard Cuneus In Hemiptera, the small triangular area at the end of the corium on the hemelytra. In Odonata, the small triangular structure (Fig. 142) between the compound eyes. Cupedidae A family of beetles (order Coleoptera). They commonly are known as reticulated beetles.  Beetles Howard Curran was born in the province of Ontario, Canada, on March 20, 1894. He became interested in insects by the age of seven and built a collection, but left school at the age of 12. He worked in the newspaper-publishing business, at first in his father’s office and later in the province of Saskatchewan. In 1915 he was employed as an assistant in the Dominion Entomology Branch at Vi0neland Station, Ontario. He went to Europe with Canadian troops in 1917, served in France in Word War I, was wounded and invalided out. He returned to Vineland Station in 1919–1921, and in 1921 received a B.S.A. degree from Ontario Agricultural College (now the University of Guelph). At the college, he met C.J.S. Cuneus, Figure 142 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and membranous distally. Curtonotid Flies Bethune, who encouraged his interest in Syrphidae. At the annual meeting of the Entomological Society of America in Toronto in 1921, he was encouraged to apply for a fellowship at the University of Kansas for graduate studies. This he did, was successful, and obtained his M.Sc. degree in 1923 with a thesis on North America Syrphidae in partial fulfillment of the requirements. Meanwhile, in 1922, his father’s firm began printing The Canadian Entomologist. In 1923–1928, Howard was entomologist in charge of Diptera and stored products insects, and published many papers in the pages of The Canadian Entomologist. In 1928 he joined the staff of the American Museum of Natural History, rose in its ranks, retired in 1960, and then became Curator Emeritus. He received a D.Sc. degree from the University of Montreal in 1933 after a thesis “The families and genera of North American Diptera.” His primary entomological contribution was the description of 2,648 taxa in 62 families of Diptera. From the 1940s, he undertook much consulting work and his output of publications lessened. After retirement, he moved to Florida and was appointed entomologist with the University of Florida Agricultural Experiment Station at Leesburg. He died in Leesburg on January 23, 1972, survived by his second wife, Ethel, and three children. Reference Arnaud PH, Owen TC (1981) Charles Howard Curran (1894– 1972). Myxia 2:1–20 C Curtis, John, Figure 143 John Curtis. years he developed a talent for drawing, and began to collect butterflies. In 1807, he began to work for a solicitor. However, through contact with insect collectors, he found employment as curator and illustrator of insects. After some 12 years he began work on his series of books on “British entomology,” whose first part was published in 1824, with the last, part 16, in 1839. These works were illustrated by his 769 magnificent color plates. He also (1829) published “A guide to an arrangement of British insects.” In 1841 he became editor of the insect part of “Gardener’s Chronicle” and wrote over 100 articles for it, under the pseudonym “Ruricola.” He died on October 6, 1862, in London. Reference Cursorial Adapted for running. This term is used to describe legs adapted for running. Herman LH (2001) Curtis (Ruricola), John. Bull Am Mus Nat Hist 265:56–58 Curtonotid Flies Curtis, John John Curtis (Fig. 143) was born in Norwich, England, on September 3, 1791. During his school Members of the family Curtonotidae (order Diptera).  Flies 1137 1138 C Curtonotidae Curtonotidae A family of flies (order Diptera). They commonly are known as curtonotid flies.  Flies the epicuticle and epidermis are always present. During molting, the inner layers of the new cuticle (the future exocuticle and endocuticle) are not sclerotized into distinct layers, and is called the procuticle, but this is a temporary condition.  Juvenile Hormone Cushman, Robert Asa Robert Cushman was born in Massachusetts on November 6, 1880. He studied at the University of New Hampshire and at Cornell University. In 1906 he was employed by the U.S. Department of Agriculture and worked in part on applied entomology (boll weevil, pests of fruits, pests of grapes) and on taxonomy (ichneumonid and chalcidid wasps). He was active in the Entomological Society of Washington, and its president in 1925. He died in California on March 25, 1957. Reference *Mallis A (1971)American entomologists. Rutgers University Press, New Brunswick, NJ, pp 372–373 Cuticulin The very thin outer layer of the epicuticle. Cuticulin is a tough, insoluble and inelastic layer of crosslinked protein and lipid molecules. Cutworm Any of a number of caterpillars in the family Noctuidae that hide in the soil, feeding there or emerging at night to feed on foliage or seedlings.  Potato Pests and their Management  Vegetable Pests and their Management  Maize (Corn) Pests and their Management Cutworm Moths Cuticular Lipids Lipids comprise an important component of the cuticle of insects.  Metabolism of Cuticular Lipids Cuticle The noncellular outer layer of the integument, which is the outer covering of an insect. The cuticle serves as the exoskeleton, the site for muscle attachment and a barrier against predation, parasitism, and infection by pathogens. The cuticle consists of several layers, including the epicuticle, exocuticle, and endocuticle (Fig. 144). The exocuticle or endocuticle may be reduced or even absent on some parts of the insect, but Members of the family Noctuidae (order Lepidoptera).  Owlet Moths  Butterflies and Moths Cuvier, (Baron) Georges Léopold Chretien Frédéric Dagobert Georges Cuvier was born in Montbéliard, at that time in Württemberg (later absorbed into France, and now in Germany) on August 23, 1769. He was therefore born a Württemberger and became French. Actually, he was christened Jean Léopold Nicolas Frédéric Cuvier, but after the early death of his elder brother, Georges, he was renamed Georges. He studied theology and anatomy in Cycloalexy C Epicuticle Exocuticle Pore canal Endocuticle Schmidt’s layer Epidermis Basement membrane Cuticle, Figure 144 Cross section of the insect cuticle and epidermis (adapted from Chapman, The insects: structure and function). Stuttgart. In 1795 he moved to Paris and was employed as assistant in comparative anatomy at the Jardin des Plantes (later known as Muséum National d’ Histoire Naturelle). Much later he became professor at the Collège de France and chancellor of the Université de Paris. His contributions to entomology consisted of his first small publications, and the entomological part of his (1799–1805) work “Leçons d’ anatomie compare.” The entomological part of his (1816) book “Règne animal” was written not by him, but by Latreille. He had great influence on zoological anatomy, but little directly on entomology. Much of his influence, however, was by his stance that animal species are immutable – they do not evolve. Thus, his ideas contrast with those of Lamarck, who believed that evolution does take place, but by heredity of acquired characters. They contrast just as much with the later ideas of Charles Darwin about evolution. Cuvier’s ideas were adopted by Louis Agassiz (see above). He was made grand officer of France’s Legion d’ Honneur in 1826. He was made a peer of France (Baron) in 1831 by the king Louis Philippe. He died in France on May 13, 1832. Reference Tuxen, SL (1973) Smith RT, Mittler TE, Smith CN (eds) History of Entomology. Annual Reviews Inc., Palo Alto, CA, pp 95–117 Cyclical Polymorphism A complex life cycle characterized by the occurrence of several to many morphs. Many morphs are seasonally related, and are most clearly manifested in aphids, which produce various forms of winged and wingless, a nd asexual and sexually reproducing forms, over the course of a season.  Aphids  Polyphenism  Polyphenism and Juvenile Hormone (JH)  Phenotypic Plasticity Cyclidiidae A family of moths (order Lepidoptera) also known as giant hooktip moths.  Giant Hooktip Moths  Butterflies and Moths Cycloalexy pierre JoLivet Paris, France Cycloalexy is a form of gregarism, and involves group reactions. The name is derived from the Greek “kuklos” = circle and “alexo” = I defend, I protect. It is the attitude adopted at rest by some insect larvae, both diurnal and nocturnal, in a tight circle when 1139 1140 C Cyclo-Developmental Transmission either the heads or ends of the abdomen are juxtaposed at the periphery, with the remaining larvae at the center of the circle. It can also be named the ring defense behavior. Coordinated movements such as the adoption of threatening attitudes, regurgitation, reflex bleeding and biting are used to repel predators or parasitoids. If for any reason, the circle is broken, ants or pentatomids can easily catch some larvae. The system is more efficient against predators than against parasitoids that have all found a way to turn the defense. Cycloalexy has analogy in vertebrates, penguins and muskoxen, for instance, living in familial groups and sometimes adopting a circular formation of males protecting the young and females from potential predators. Cycloalexy is mainly known among Coleoptera: Chrysomelidae, (Cassidinae, Chrysomelinae, Criocerinae), Coleoptera: Curculionidae, sawflies, and several other insect orders (Diptera, Ceratopogonidae, Neuroptera, Lepidoptera, etc.). Generally, the individuals in a colony disperse to feed upon foliage by night (or by day when they rest during the night), one behind the other, to reaggregate before dawn. In Pergidae, to reaggregate the larvae communicate by means of low frequency vibrations created by tapping the uropod upon the substrate. Paropsine (Coleoptera: Chrysomelidae) larvae in Australia also tap the substrate with the abdomen to reunite the dispersed colony. All the insects demonstrating cycloalexy are subsocial in the larval stage and also often exhibit maternal care of eggs and larvae. Some cycloalexic leaf beetles like Platyphora in Brazil are viviparous. When dropped one by one by the mother, the larvae congregate immediately. Cycloalexy, like maternal care, can only be the result of a long evolutionary history. The behavior efficiently protects the larvae during their most vulnerable periods (at rest, during molting). However, the defense is not always perfect. Trigonalyid parasitoids have succeeded in having their eggs swallowed by the sawfly larvae, thus obviating the need to confront the defensive ring. Younger larvae sometimes seem to be protected inside the circle, and this could be interpreted as altruism on the part of the larvae at the periphery (Fig. 145). Also, reciprocal altruism may take place when the inner and outer larvae exchange positions. However, this interpretation has been challenged. In Australian sawflies in the genus Perga (Perga dorsalis Leach), some 20% of the larvae preferentially occupy the outer positions in the resting colony and appear to lead the foraging expeditions. Leaders are quick to regain outer positions if removed and placed in the center of the colony. So there seem to be differences in the dispersal behavior of larvae in time and space. Small colonies of larvae sometimes show non-viability (e.g., pergids). However, when larvae of Coelomera spp. (Coleoptera: Chrysomelidae) on a leaf of a Cecropia tree are divided into two or three subgroups, those groups seem as efficient as big ones in repelling predators.  Gregarious Behavior in Insects References Jolivet P, Vasconcellos-Neto J, Weinstein P (1990) Cycloalexy: a new concept in the larval defense of insects. Insecta Mundi 4:133–141 Vasconcellos-Neto J, Jolivet P (1988) Une nouvelle stratégie de défense: la stratégie de défense annulaire (cycloalexie) chez quelques larves de Chrysomélides brésiliens. Bulletin Societé Entomologique France 92:291–299 Vasconcellos-Neto J, Jolivet P (1989) Ring defense strategy (cycloalexy) among Brazilian chrysomelid larvae (Col.). Entomography 67:347–354 Verma KK (1996) Cycloalexy in leaf-beetles (Col. Chrys.). Insect Environ 2:82–84 Weinstein P (1989) Cycloalexy in an Australian pergid sawfly (Hym. Pergidae). Bull R Belg Entomol Soc 125:53–60 Weinstein P, Maelzer DA (1997) Leadership behaviour in sawfly larvae, Perga dorsalis. Oikos 79:450–455 Cyclo-Developmental Transmission Transmission of an arthropod transmitted disease wherein the causal organism undergoes cyclical changes but does not multiply in the body of the arthropod vector.  Mechanical Transmission  Cyclo-Propagative Transmission, and Propagative Transmission Cyclo-Developmental Transmission C Cycloalexy, Figure 145 Cycloalexy:(a) Third instar of Platyphora conviva Stål, 1858 (Coleoptera: Chrysomelinae). Rupture of the cycloalexic ring and predation by a bug of one larva. (photo J. Vasconcellos-Neto, 1986.) Itatiaia National Park, RJ, Brazil. (b) Eggs of Coelomera lanio Dalman Coleoptera: Galerucinae), laid on the underside of the folioles of Cecropia adenopus (Cecropiaceae). The newly hatched larvae will aggregate. (photo Jolivet, 1990.) Viçosa, MG, Brazil. (c) First instar larvae of Coelomera lanio Dalman (Coleoptera: Galerucina). Cycloalexic ring. (photo Jolivet, 1990.) Viçosa, MG, Brazil. (d) Second instar larvae of Coelomera lanio Dalman (Coleoptera: Galerucinae), on a leaf of Cecropia adenopus. The ring has been doubled. (photo Jolivet, 1990.) Viçosa, MG, Brazil. (e) Third instar of Coelomera lanio Dalman (Coleoptera: Galerucinae), on a leaf of Cecropia adenopus. The cycloalexic ring is near to be broken and the larvae to go feeding (Coleoptera: Galerucinae). (photo Jolivet, 1990.) Viçosa, MG, Brazil. (f) Cycloalexic ring of Platyphora conviva Stål (Coleoptera: Chrysomelinae). First instar. The larvae have covered themselves with the hair of the underside of the leaves for extra protection. (photo J. Vasconcellos-Neto, 1986.) Itatiaia National Park, RJ, Brazil. 1141 1142 C Cyclo-Propagative Transmission Cyclo-Propagative Transmission Transmission of an arthropod transmitted disease wherein the causal organism undergoes cyclical changes and multiplies in the body of the arthropod vector.  Mechanical Transmission  Cyclo-Developmental Transmission, and Propagative Transmission Cyclorrhapha A term sometimes applied to the higher flies (Diptera), usually treated as an infraorder, and also known as Muscamorpha. The cyclorrhaphous Diptera differ from the other (lower) flies in that pupation and the formation of the adult form occur within the old, hardened third instar cuticle.  Flies (Diptera) Cyclotornidae A family of moths (order Lepidoptera) also known as Australian parasite moths.  Australian Parasite Moths  Butterflies and Moths Cyphoderidae A family of springtails in the order Collembola.  Springtails Cypselosomatid Flies Members of the family Cypselosomatidae (order Diptera).  Flies Cypselosomatidae A family of flies (order Diptera). They commonly are known as cypselosomatid flies.  Flies Cyrtocoridae A small family of bugs in the order Hemiptera, suborder Heteroptera. It is treated by some as a subfamily of Pentatomidae.  Bugs Cydnidae A family of moths (order Hemiptera). They sometimes are called burrower bugs.  Bugs Cylindrical Bark Beetles Cystocyte A type of hemocyte, also known as coagulocytes, that participates in the coagulation process of hemolymph.  Hemocytes of Insects: their Morphology and Function Members of the family Colydiidae (order Coleoptera).  Beetles Cytochrome Cymidae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs The complex protein respiratory enzymes occurring within plant and animal cells in the mitochondria, where they function as electron carriers in biological oxidation. Cytosol Cytoplasm The fluid components of the cell, outside the nucleus. C Cytoplasmic Polyhedrosis Virus An RNA virus associated with inclusion bodies found in cytoplasm of cells. Cytoplasmic Incompatibility Cytosol Reproductive incompatibility between two populations caused by factors that are present in the cytoplasm. Often associated with microorganisms. The fluid portion of the cytoplasm, excluding the organelles in a cell. 1143