Integrated Pest Management 523

for habitat purchase and protection, fueled in part by increased public increased. Other species have become pests as a consequence of the
awareness of the magnitude and importance of insect biodiversity. availability of abundant resources for their survival and reproduc-
tion; resource concentration in time and space is conducive to rapid
See Also the Following Articles buildup of insect populations. Still other species have become pests
in regions of their origin when they expanded their host range from
Conservation ■ Museums and Display Collections ■ Photography of comparatively unimportant native hosts to economically important
Insects ■ Rearing of Insects ■ Teaching Resources
introduced hosts. Finally, some species have become pests almost
instantly upon being transported by humans to new locales having
Further Reading favorable resources but devoid of effective natural enemies.
Chicago Zoological Society (1947). “Guide Book, Chicago Zoological Park.”
Chicago Zoological Society, Brookfield, IL.
Hoage, R., and Deiss, W. A. (eds.) (1996). “New Worlds, New Animals.” CLASSIFICATION OF INSECT PESTS
Johns Hopkins University Press, Baltimore, MD. For purposes of devising an appropriate IPM strategy, insect pests
Jones, M. (2001). Personal communication. San Diego Zoological Society. may be classified as key, secondary, or induced. Key pests are those
Kisling, V. N. (ed.) (2001). “Zoo and Aquarium History—Ancient Animal, whose populations, if unmanaged, repeatedly exceed tolerable lev-
Collections to Zoological Gardens.” CRC Press, Boca Raton, FL.
els; these are the principal focus of IPM endeavors. Secondary pests
Lange, J. (2001). Personal communication. Zoo-Aquarium Berlin.
Loisel, G. (1912). Epoque contemporaine. In “Histoire des ménageries de
are those whose populations occasionally reach intolerable levels;
l’antiquité à nos jours,” Vol. III, Henri Laurens/Octave Doin etfils, Paris. their potential threat is recognized by the very act of devising IPM
New York Zoological Society (1911). Zoological park notes. Zool. Soc. Bull. strategies. Induced pests are those whose populations rarely exceed
47, 788–789. tolerable levels under natural conditions, but if they become resist-
New York Zoological Society (1940). Notes from the park and aquarium. ant to pesticides or other single-tactic control measures that harm
Zool. Soc. Bull. 43(6), 198–203. their natural enemies, they can reach outbreak proportions. Usually
Parsons, M. (1992). Butterfly farming and conservation in the Indo-Australian
region. Trop. Lepid. 3, 1–28.
induced pests return to nonpest status under a true IPM approach.
I
Praschag, R. (1986). “Constructions of Aquaria and Terraria.” Thesis,
University of Graz, Austria, pp. 460–468. EVOLUTION OF CONCEPT OF IPM
Saul-Gershenz, L. S., Arnold, R. J., and Scriber, J. M. (1995). Design of cap-
tive environments for endangered invertebrates. In “Conservation of
Through trial and error across centuries, humans gradually came
Endangered Species in Captivity: An Interdisciplinary Approach.” State to use tactics such as cultural control, host resistance, and biologi-
University of New York Press, Albany, NY. cal control in efforts to protect themselves, livestock, crops, and for-
Yajima, M. (1996). The development of insectariums and their future. Int. ests against pests. By the latter half of the 19th century, some pest
Zoo News 43, 484–491. control strategies that blended these tactics could rightfully be con-
sidered to be the precursors of modern IPM strategies. During the
20th century, efforts to maintain pests at tolerable levels became
more formalized as they became more intensive; these efforts can be
considered as having progressed along the following four pathways.
Integrated Pest Management “Pest control” was the terminology used during the first half of
the 20th century to describe the set of actions taken to avoid, attenu-
ate, or delay the impact of pests. Early in the century, inorganic and
Ronald Prokopy†
botanical insecticides gained increasing prominence as a control tactic
University of Massachusetts against pest insects. By the mid-century, use of organosynthetic insec-
ticides supplanted virtually all other tactics in becoming the dominant
Marcos Kogan approach to insect pest control, especially in developed countries.
Oregon State University “Integrated control” surfaced about 1950 in California as a concept
of pest control aimed at combining and integrating biological and chemi-

A
cross millennia, humans have used a variety of approaches in cal control. The emergence and eventual popularity of this concept had
attempts to maintain pest insects at tolerable levels. The char- roots in problems associated with overuse of organosynthetic insecticides,
acter of these approaches has evolved over time. Since the late particularly a surge of key, secondary, and induced insecticide-resistant
1960s, an approach termed integrated pest management (IPM) has pests and environmental harm caused by insecticides. The publication
ascended to dominance internationally. In essence, IPM is a decision- of Silent Spring by Rachael Carson in 1962 was especially important in
based process involving coordinated use of multiple tactics for optimiz- spurring widespread interest in the principles of integrated control.
ing the control of all classes of pests (arthropods, microbial pathogens, “Pest management” represents a shortened version of “protective
vertebrates, weeds) in an ecologically and economically sound manner. population management,” a concept coined in 1964 by Australian
ecologists to emphasize direct human interference in maintaining
pests at tolerable levels, as opposed to reliance on unmanaged natu-
HOW INSECT PESTS ORIGINATE
ral abiotic and biotic factors acting on pest populations. The concept
The manner by which an insect has become a pest influences of pest management embraced a broader range of pest control tac-
the strategy used for managing it within an IPM framework. Some tics than did the concept of integrated control. Until the late 1960s,
species have reached the status of pest because human thresholds both these concepts flourished simultaneously in accenting the need
for tolerating them have decreased as economic well-being has to move beyond the use of insecticides as a sole pest control tactic.
“Integrated pest management” originated in 1968 as a contraction
† of “integrated pest population management,” an expression used first in
Deceased May 14, 2004.
 524 Integrated Pest Management

1967 by R. F. Smith and R. van den Bosch. Soon afterward, the abbre- or less distinctive levels along the continuum are described in the fol-
viation “IPM” came into use worldwide for signifying a desirable and lowing sections (Fig. 1). Degree of success in integration at each level
holistic approach to controlling pests. Numerous definitions have been is shaped not only by ecological processes but also by government
put forward for IPM, but one that captures the broad and essential ele- policy, regulatory legislation, social relations, economic forces, and
ments of many others is the following: IPM is a decision support system cultural background that may enhance or constrain progress.
for the selection and use of pest control tactics, singly or harmoniously
coordinated into a management strategy, based on cost–benefit analy- FIRST-LEVEL IPM
ses that take into account the interests of and impacts on producers,
society, and the environment. No single definition, however, is likely In the most basic and also the most widely practiced form of IPM,
to encompass all facets of IPM for all time. IPM has been and likely emphasis is on monitoring development and/or abundance of a sin-
will continue to be an evolving concept. For example, a compendium gle pest species at a single locale (e.g., a household, cow barn, green-
of IPM definitions, available on the World Wide Web (http://ipmnet. house, cropped field, or woodlot) and using thresholds for deciding
org/IPMdefinitions/home.html), listed 67 definitions in the mid-2002. whether to take action. Application of a pesticide is by far the most
common form of action taken under the first-level IPM. Integration
occurs when abundance of natural enemies of the pest in question
ECOLOGICAL FOUNDATION OF IPM also is considered in the decision-making process and when selection
Ecology is the study of relationships among organisms and their among candidate pesticides involves explicit attention to minimizing
environment. Consideration of these relationships usually begins harm to these and other beneficial organisms. This form of IPM has
with focus on individuals or populations of a single species and sub- been characterized by some as “integrated pesticide management.”
sequently broadens to include communities of organisms and, even-
tually, ecosystems. Monitoring Pest Development
Conceptually, the foundation of IPM is ecological. Ideal IPM Because the developmental rate of an arthropod is regulated
I programs are those that fully embrace ecosystem structure and proc-
esses in time and space. In reality, ecological complexity increases
largely by temperature, the monitoring of developmental rate for
pest management purposes usually takes the form of measuring
dramatically with each step from population to community to eco- accumulation of heat units above a threshold temperature at which
system. Such complexity challenges the realization of ideal IPM development begins. At temperatures above these fostering the max-
programs. imal developmental rate, development may decrease. Such decrease
One approach that has been taken toward recognition of the eco- has not been investigated for most pest arthropods and has not yet
logical foundation of IPM, especially in developing countries, accen- played a significant role in making pest management decisions.
tuates the pest-suppressing properties inherent in natural ecosystems The simplest and most prevalent approach to measuring accumula-
as primary building blocks for the construct of human-designed eco- tion of heat units above developmental threshold temperature involves
systems. After system construction based on ecological principles, the the use of degree-days (DD). For a specific date, the number of accu-
intent is to minimize human intervention to the greatest extent pos- mulated DD equals the average temperature of that date minus the
sible while still maintaining pest populations within tolerable levels. developmental threshold temperature of the arthropod. Several pro-
Another approach, common in developed countries, takes as its cedures have been devised to estimate average daily temperature. The
starting point an existing ecosystem constructed by humans and aims most common one, albeit somewhat crude, consists simply of averaging
at reducing negative impact in a succession of steps used in the man-
agement of pests. Such an approach usually commences with a focus
on the ecology of a single-species population and may expand to con-
sideration of structures and processes associated with communities
and ecosystems.

ADVANCING LEVELS OF INTEGRATION IN

IPM IMPLEMENTATION
A hierarchical structure results from the ecological foundation of
IPM that lends itself to viewing IPM as progressing in scope through
a series of ecologically rooted steps. These steps are characterized
by ascending levels of complexity and spatial scale: from focus on a
single-species population in a restricted locale to focus on a commu-
nity of pest and other organisms in a larger area to focus on a whole
ecosystem. Coincident with this ecocentric hierarchy is another step-
wise hierarchy conceived of as a vehicle for measuring progress in
achieving the goals of IPM. This hierarchy comprises a succession of
levels from single-tactic (almost invariably based on pesticide use) to
multitactic measures of pest and habitat management. The steps fur-
ther involve ascending from focus on a single pest species in a single
class of pests (e.g., insects) to multiple pest species across all classes
of pests (insects, microbial pathogens, vertebrates, and weeds). These
distinctive hierarchies can be blended in the form of a continuum of FIGURE 1 Levels of IPM integration: main targets, ecological
advancing levels of integration in IPM implementation. Three more scales, and levels of ecological complexity.
 Integrated Pest Management 525

the maximum and the minimum ambient temperature of the day. To The emerging technologies of global positioning systems (GPS) and
illustrate the DD approach, if the high and low temperature for a given geographical information systems (GIS) offer unsurpassed capability
day were 30°C and 20°C, respectively, with a developmental threshold of aiding in the mapping of site-specific variation in characteristics of
temperature of 10°C, then 15 DD would have accumulated on that day. areas under consideration for sampling. A GPS uses triangulation of
Pest development as monitored by DD accumulation may benefit signals from a constellation of satellites to identify the precise location
decision making under first-level IPM in several ways, particularly for (within a meter) of an area on the earth’s surface. A GIS is a com-
optimal timing of management activities. For example, ability to pre- puter program for the mapping and spatial analysis of georeferenced
dict when a majority of pest adults is about to emerge from pupae is information. GIS capabilities include assemblage, storage, manipula-
useful for optimal timing of deployment of traps for monitoring adults. tion, retrieval, and graphic display of information about attributes of
Knowledge about when oviposition is likely to begin and peak can precise locations identified through GPS. Such information can be
facilitate optimal timing of pesticide application against newly hatched exceptionally useful in forming associations between characteristics of
larvae, which often is the stage most vulnerable to pesticide treatment. a specific locale (e.g., terrain, soil, extent of vegetative growth, micro-
Sometimes this determination is made in conjunction with date of first climate) and density of a population (Fig. 2). For pests, sampling can
capture of adults by traps, known as a “biofix” point for initiation of be directed toward specific sites in which densities are suspected to
DD accumulation. The ability to forecast when a majority of larvae or be the highest.
nymphs is at a particular growth stage can aid in optimal timing of sam-
pling their abundance and the abundance of their natural enemies.
Deciding Whether to Take Action
Several approaches have been developed for deciding whether
Monitoring Pest Abundance an insect pest population has or has not reached a level requiring
Ideally, an IPM practitioner would have available a precise count intervention, such as an insecticide application. For agricultural pur-
of the number of individuals of an insect pest species present in an poses, the approach used most often centers on the concept of “eco-
area of concern; realistically, obtaining information on absolute den-
sities of pests is prohibitively costly. Therefore, most practitioners
nomic injury level” (EIL), formalized in 1959 by V. H. Stern, R. F.
Smith, R. van den Bosch, and K. S. Hagen and defined by them as
I
rely on imprecise estimates of pest population density obtained by the “lowest pest population density that will cause economic damage.”
using one or more population sampling techniques. The intent is to These entomologists also proposed a related concept, which they
capture a more or less consistent, if unknown, proportion of the pest termed the “economic threshold” (ET), defined as the “pest density
population. Choice of appropriate sampling technique varies con- at which control measures should be applied to prevent an increasing
siderably according to pest species, its developmental stage, and the pest population from reaching the economic injury level” (Fig. 3).
crop plant or other habitat where the pest occurs. The decision-making concepts of EIL and ET have been funda-
For sampling comparatively mobile individuals such as adults, mental to the development and implementation of first-level IPM,
traps using odor and/or visual stimuli are common tools. Odor stimuli particularly for insect management in agriculture (but less so for
usually consist of synthetic equivalents of either attractive sex odors
(sex or aggregating pheromones) or attractive food or host odors
(kairomones). Visual stimuli normally rely on synthetic mimics of vis- N
ually attractive sites where feeding, mating, or egg laying occurs. 0
1.0
For sampling less mobile individuals such as larvae, common
2.0
techniques include visual searching of the target area accompanied 3.2
by direct counts of detected pests, use of a sweep net (especially 4.5
effective for sampling individuals on foliage of nonwoody plants), 5.6
and use of a loose or framed cloth placed beneath vegetation that is 6.8
shaken or tapped to dislodge pests. Sampling immobile individuals 8.2
9.7
such as eggs or pupae usually is done by visual inspection.
10.5
To obtain an acceptably accurate and cost-effective estimate of the mean N. fallacis
size of a pest population by means of one of these techniques, care- density/10 leaves
ful attention must be given to the program under which sampling is Release sites
conducted. Effective sampling programs take into account the daily Sample points
activity pattern of the target species as well as its characteristic spatial 30 m
distribution (uniform, random, or clumped). Historically, most pro-
30 m
grams have incorporated sampling at several or numerous sites in a
target area to acquire sufficient representation of the size of a pest FIGURE 2 Dispersal of Neoseiulus fallacis for biological control
population; then researchers have counted the sampled individuals of spider mites in a strawberry field, 8–15 weeks following release of
of the target pest. New programs developed for some pests simplify 100 adult females at each of 15 sites: squares, release sites; crosses,
these procedures. Sequential sampling is an approach that optimizes sample points. This distribution is due to ambulatory foliar movement
the number of sampling sites needed for classifying a pest population and aerial dispersal (dominant winds from south and southwest).
as below or above a density requiring action. Binomial sampling is Data represented using GIS (GRASS v. 4.1). [From Coop, L. B.,
an approach that classifies an individual species as either present or and Croft, B. A. (1995). Neoseiulus fallacis: Dispersal and biologi-
absent at a sampling site, thereby precluding the need to count all cal control of Tetranychus urticae following minimal inoculation
members of that species taken in a sample. Both these simplifying into a strawberry field. Exp. Appl. Acarol. 19, 31–43. Reproduced
approaches require substantial species-specific background informa- by permission from the authors and Chapman & Hall (now Kluwer
tion for their development and use. Academic Publishers).]
 526 Integrated Pest Management

No remedial control action required permits ready identification and quantification of parasitized eggs in
Economic injury level addition to healthy eggs. If the level of egg parasitism is determined
Economic threshold
to be too low to prevent larval numbers from exceeding the EIL, the
lowest adequate rate of a “soft” pesticide (one having least impact
on parasitoids and other nontarget organisms) is recommended. This
Population density

approach is an example of application of the inaction level concept

and represents a high degree of first-level IPM implementation.
Area-wide IPM is an expansion of first-level IPM that may rep-
resent a significant transitional step toward second and third levels
of IPM. Under area-wide IPM, the key pest of a crop is targeted
for management by means of the most effective noninsecticidal
approach. For example, the codling moth, Cydia pomonella, is man-
aged in apple and pear orchards by tactics such as the pheromone
Time
mating disruption technique or the sterile insect release method
(A)
that impair normal reproduction. Such tactics are implemented over
Remedial control action required areas large enough to preclude recolonization by fertile females from
adjacent areas. By reducing the impact of broad-spectrum insecti-
cides, natural enemies are preserved and are usually capable of regu-
lating most secondary pests in the crop. As area-wide IPM programs
Economic injury level expand to incorporate multiple pest interactions, they become natu-
Population density

ral springboards to higher level integration in IPM systems.

Economic threshold

I SECOND-LEVEL IPM
Second-level IPM is intermediate between basic and advanced.
It is receiving increased research attention, but inherent complexi-
ties have greatly limited its effectiveness. Emphasis is on manage-
ment of key pests of all classes and their associated natural enemies
comprising a community (e.g., a village of dwellings, an entire farm,
(B) Time a wooded area surrounding a village). Emphasis also is on substi-
tuting a variety of comparatively environmentally benign manage-
FIGURE 3 Graphs depicting theoretical population fluctuations ment tactics (e.g., cultural management, host resistance, biological
of two insect pest species. control, behavioral control), to the greatest extent possible, for the
therapeutic practice of pesticide application. Decision makers must
disease, vertebrate, and weed management). They have been espe- determine how best to integrate these tactics to achieve long-term
cially useful when insect pest populations are expected to increase suppression of pests within a cost–benefit framework.
over time within a crop, can be sampled reliably, can be related in Cultural management is purposeful manipulation of the environ-
a predictable way to reduction in crop yield or quality, and can be ment to reduce pest abundance. It is most effective when directed
controlled readily by taking immediate action (e.g., application of at the most vulnerable life stage of a pest. Four forms of habitat or
insecticide) to prevent further damage. They are less valuable when environmental manipulation aimed at controlling pests have been
human comfort or aesthetics, rather than economic damage, is para- practiced for centuries in agriculture: crop rotation, timing of plant-
mount. Even for agriculture, the concepts of EIL and ET cannot be ing or harvest to minimize pest damage, sanitation or elimination of
applied rigidly because of inherent unpredictability of such factors noneconomic resources available for pest reproduction, and poly-
as future weather (which can markedly affect rate of pest popula- culture, or the interplanting of different crops to diffuse resource
tion growth and degree of crop susceptibility to a pest) and future concentration. More recent practices include the planting or encour-
value of the crop in the marketplace. Also, a type of action that may agement of selected types of noneconomic vegetation in the vicinity
require considerable time before reducing pest density, such as of crops or as cover crops to serve as harborage for natural enemies
application of a biocontrol technique, is likely to be less appropriate of pest insects. Analogues of these practices have been developed for
than an insecticide application within an EIL/ET framework. managing insect pests in nonagricultural situations.
A refinement of the concept of EIL, put forward by L. P. Pedigo Host resistance is any inherited characteristic of a host that less-
and L. G. Higley, introduces the element of environmental quality ens effects of an attacking pest. For centuries, humans may have
into the decision-making process. Negative effects of insecticides on unknowingly or intentionally selected for cultivars of plants or breeds
natural enemies of pests and on other organisms in the environment of animals that are best able to withstand pests. Modern breeding
are treated as costs in addition to monetary costs associated with programs, however, often have placed more emphasis on increasing
insecticide application. Quantifying environmental costs has proven yields than on protection against pests. Entomologically, resistant
to be challenging and subject to much debate, but progress under traits are preadaptive characteristics of a host that reduce its detecta-
this refined concept of EIL nonetheless has been made. bility, acceptance, or nutritional value, or enhance its toxicity to a
In 1984, W. L. Sterling advanced the concept of “inaction level,” pest insect. Molecular genetics techniques that facilitate introduc-
which is the density of natural enemies sufficient to maintain a pest tion of specific pest resistance genes into cultivars or breeds possess-
below the EIL. M. P. Hoffmann and collaborators developed a sam- ing desirable commercial or aesthetic traits are beginning to replace
pling program for eggs of tomato fruitworm, Helicoverpa zea, that traditional resistance breeding approaches.
 Integrated Pest Management 527

In biological control, parasitoids, predators, or pathogens are resulted in dramatic increases in awareness by entire communities of
deployed as natural enemies in the reduction of pest populations. an advanced form of IPM and often dramatic decreases in use of pes-
Of the myriad insect species that could become pests, most do not ticides on rice. It stands in contrast to modes of decision making and
because they are suppressed effectively by naturally occurring pop- levels of popular awareness characteristic of less advanced forms of
ulations of biological control agents. Natural levels of biocontrol, IPM implementation in many developed countries, where it is com-
however, often are insufficient for IPM purposes. Biological con- monplace for farmers to make IPM decisions either acting alone or
trol then takes the form of importing absent natural enemies from at most interacting with a private consultant, government extension
other locales (termed importation or classical biocontrol), augment- representative, or employee of a pesticide distributor.
ing existing natural enemies by rearing and then releasing substan-
tial numbers into the target community (termed augmentation), or
tailoring management tactics to reduce negative effects on existing
IPM AND SUSTAINABLE DEVELOPMENT
natural enemy populations (termed conservation). The latter is the In a broad sense, sustainable development is development that
most widely practiced form of biocontrol. meets the needs of the present without compromising the ability of
Behavioral control is manipulation of the behavior of pest indi- future generations to meet their own needs. Sustainable develop-
viduals to prevent them from causing harm or unpleasantness. ment is rooted in the concept of ecosystem integrity and permeates
Because of the expense and technological challenges associated all facets of human endeavor, whether economic, social, or cultural.
with its use, behavioral control usually is directed only at key pests. The scope of concerns and practices of third-level IPM as
Behavioral control may involve use of natural or synthetic chemical described here corresponds closely to that of sustainable development.
or physical stimuli to lure pests to sites where they are killed, or use Each emphasizes preservation of processes associated with natural
of such stimuli to disrupt the ability of pests to find or use a potential ecosystems, long-term well-being of humans as members of communi-
resource. An ideal form of behavioral control might involve joint use ties, economic viability, and deployment of exogenous resources only
of disruptive and attractive stimuli to achieve maximum effect, but after careful consideration. For agriculture, concepts underlying third-
level IPM can be equated with concepts underlying sustainable agri-
this form is not yet widespread in practice.
Vineyards in parts of Europe and North America represent one culture. For both, one can expect concepts to evolve further over time. I
of the few areas in which pest management is practiced effectively
under the second-level IPM concept. Besides using essential ele-
See Also the Following Articles
ments of first-level IPM for insect pests, certain practitioners of vine-
yard IPM in these locations blend host plant resistance with cultural, Agricultural Entomology ■ Biological Control ■ Extension Entomology
biological, and behavioral controls for suppression of key pest insects ■ Insecticides ■ Physical Control ■ Population Ecology ■ Sterile Insect

and also use a suite of cultural controls for managing key disease and Technique
weed pests. This approach has resulted in marked reduction in pesti-
cide use and greater stability of relationships among organisms com- Further Reading
prising vineyard communities.
Altieri, M. A., and Nicholls, C. I. (1999). Biodiversity, ecosystem function,
and insect pest management in agricultural systems. In “Biodiversity in
THIRD-LEVEL IPM Agroecosystems” (W. W. Collins, and C. O. Qualset, eds.), pp. 69–83.
CRC Press, Boca Raton, FL.
Although many IPM practitioners aspire to implement third- Benbrook, C. M. (1996). “Pest Management at the Crossroads.” Consumers
level IPM, the most advanced form remains largely in an embryonic Union, Yonkers, NY.
state of development. Emphasis is on using principles and practices Coop, L. B., and Croft, B. A. (1995). Neoseiulus fallacis: Dispersal and bio-
of second-level IPM in harmony with all other elements that affect logical control of Tetranychus urticae following minimal inoculations into
long-term productivity or well-being of an ecosystem. Such elements a strawberry field. Exp. Appl. Acarol. 19, 31–43.
include sound horticultural or husbandry practices (for agriculture), Dent, D. (1995). “Integrated Pest Management.” Chapman & Hall, New York.
sound forest management (for silviculture), and sound community Higley, L. G., and Pedigo, L. P. (1993). Economic injury level concepts and
health practices (for villages or subunits of cities). Third-level IPM their use in sustaining environmental quality. Agric. Ecosyst. Environ. 46,
233–243.
features attention to environmental and societal costs and benefits in
Kenmore, P. E. (1996). Integrated rice pest management. In “Biotechnology
the making of pest management decisions. The focal ecosystem may
and Integrated Pest Management” (G. J. Persley, ed.), pp. 76–97. CAB
be an entity no larger than a community, as considered under sec- International, Wallingford, Oxon, U.K.
ond-level IPM, or it could be an entity as extensive as an ecological Kennedy, G. G., and Sutton, T. B. (2000). “Emerging Technologies for
region. For crops, third-level IPM is roughly synonymous with the Integrated Pest Management.” APS Press, St Paul, MN.
concept of integrated crop management. It is not, however, synony- Kogan, M. (1998). Integrated pest management: Historical perspectives and
mous with organic agriculture, which disallows some materials and contemporary developments. Annu. Rev. Entomol. 43, 243–270.
practices acceptable under third-level IPM. Kogan, M., and Jepson, P. (2007). “Perspectives in Ecological Theory and
Spearheaded by P. E. Kenmore, an approach has been developed Integrated Pest Management.” Cambridge University Press, Cambridge, U.K.
for growing rice in developing parts of Asia that reflects many of the Lewis, W. J., van Lenteren, J. C., Phatak, S. C., and Tumlinson, J. H. (1997).
A total system approach to sustainable pest management. Proc. Natl Acad.
tenets of third-level IPM. This approach accentuates societal contri-
Sci. USA 94, 12243–12248.
bution to the IPM decision-making process. It involves weekly gather-
Metcalf, R. L., and Luckman, W. H. (1994). “Introduction to Insect Pest
ings of small groups of rice farmers, accompanied by experienced pest Management.” Wiley, New York.
management personnel, who jointly conduct agroecosystem obser- Pedigo, L. P. (1996). “Entomology and Pest Management.” Prentice-Hall,
vations, engage in data analysis, and consider local ecosystem struc- Upper Saddle River, NJ.
ture, environmental health, and a range of immediate and long-term Prokopy, R. J. (1993). Stepwise progress toward IPM and sustainable agricul-
tactics before making pest management decisions. This process has ture. IPM Pract. 15(3), 1–4.
 528 Integument

Sterling, W. (1984). Action and inaction levels in pest management. Texas The epidermal cells undergo mitotic divisions at the onset of molt-
Agricultural Experimental Station, Bulletin 1480. Texas A&M University, ing, resulting in an increase of cell number and total epidermal sur-
College Station. face. To allow the animal to increase in size at molting, the epicuticle
Tan, K. H. (ed.) (2000). “Area-Wide Control of Fruit Flies and Other Insect deposited above the apical cell surface has a larger area than the previ-
Pests.” Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia.
ous epicuticle, and the epidermis together with the epicuticle is folded
Zalom, F. G. (2000). Moving along the IPM continuum. Proc. Am. Soc. Enol.
Vitic. 50th Meeting, pp. 356–359. Seattle, WA.
to be accommodated in the space available inside the old cuticle.
Deposition of new cuticle occurs simultaneously with the degra-
dation of the old cuticle. An enzyme mixture, containing proteases,
peptidases, chitinases, and glucosidases, is secreted into the space
between the old cuticle and the new epicuticle, and the old cuticle
is gradually degraded to free amino acids and N-acetylglucosamine.
Integument The degradation products are resorbed by the insect and reused for
building proteins and chitin for the new procuticle. Chitin is synthe-
sized by an enzyme complex (chitin–synthetase) located at the top
Svend O. Andersen of microvilli on the apical surface of the epidermal cells, and chitin
The Royal Danish Academy of Sciences and Letters microfibrils grow from here into the subcuticular space, the deposi-
tion zone. The cuticular proteins are synthesized intracellularly and

T
he integument is the external layer of tissue that covers the transported via the Golgi complex to the apical plasma membrane,
outer surface of insects and the surfaces of the foregut and and are secreted into the subcuticular lumen by exocytosis. The chi-
hindgut. It is composed of the epidermis, which is a continu- tin and protein molecules are in some way organized into a macro-
ous single-layered epithelium, and an underlying thin basal lamina molecular complex in the deposition zone between cells and cuticle,
plus the extracellular cuticle that lies on top of the epidermis. possibly by a process of self-assembly.
I Soon after emerging from the old cuticle (exuvium), the insect
expands the new cuticle to a predetermined size, often dependent
BASAL LAMINA on the area of the epicuticle. Cuticular deposition of chitin and pro-
The basal lamina separates the epidermal cells from the hemo- teins is resumed and continues for several days after ecdysis, while
lymph in the body cavity; it varies in thickness from 0.15 to 0.5 μm smaller and largerregions of the new cuticle are hardened (sclero-
and is composed of structural proteins including collagens, glycopro- tized) by oxidative incorporation of phenolic compounds into the
teins, and glycosaminoglycans. It is negatively charged and can act as cuticular matrix. Both sclerotization and post-ecdysial deposition of
a filter between the hemolymph and the epidermal cells, regulating endocuticle are governed by the neurohormone bursicon.
which molecules gain access to the cells. Secretion of material from the epidermal cells occurs not only at
the apical surface. Some of the peptides and proteins synthesized by
the cells are exported to the hemocoel via the basolateral membrane
EPIDERMAL CELLS system, and others, such as arylphorins, are synthesized in the fat
The epidermal cells are attached to the basal lamina by body and secreted into the hemolymph to be taken up by the epi-
hemidesmosomes, which anchor the cell membrane to collagen fib- dermal cells and incorporated into the cuticle.
ers in the basal lamina. Near their base, the cells are attached to
each other by desmosomes; near their apical end, they are attached
to each other by a narrow, impermeable zone (the adhering zonule),
effectively separating the cuticular compartment from the lateral
PORE CANALS
space between cells. Below the zonule are bands of septate desmo- Most cuticles contain pore canals, minute ducts that traverse the
somes, which may be adhesive, and gap junctions through which the cuticle from the apical surface of the epidermal cells to or close to
cells can communicate chemically with each other by interchange of the cuticular surface. When viewed with an electron microscope
low-molecular-weight compounds. they may seem empty, but they often contain one or more cuticular
The cuticular materials (chitin and proteins) are secreted from filaments composed of wax and lipids. Cytoplasmic processes may
the apical surface of the epidermal cells into the subcuticular space, extend into the ends of the pore canals during cuticle deposition.
or deposition zone, where they are assembled into an intact cuticle. The pore canals are generally assumed to be a transport route for
The apical surface is folded into shorter or longer microvilli, depend- lipids and possibly also for sclerotizing agents and proteins to the
ing on the stage of the molting cycle and the secretory activity of epicuticle and outer exocuticle.
the cells.

THE MOLTING PROCESS SENSE ORGANS

The integument of insects contains a large number of sensory cell
The cuticle is a rather inextensible structure, and in order to types, involved in transferring information from the environment to
grow, insects need to shed their old cuticle at intervals after having the insect. The sensory cells in the epidermis are often connected to
produced a new one with a larger surface area. The whole process, specific cuticular structures, forming sense organs of various types,
from breaking the connections between the epidermal cells and the such as contact chemoreceptors (taste), olfactory chemoreceptors
cuticle (apolysis) to emerging from the remnants of the old cuticle (smell), and mechanoreceptors, which register any small distortion
(ecdysis), is called molting. The consecutive steps of the process are of the cuticle caused either by the movements of the animal or by
controlled by hormones. influences from the environment.