J. Crop Prot.

2014, 3 (1): 59-67________________________________________________________

New Record of two species belonging to superfamily Sphaerularioidea

(Nematoda: Tylenchida) from Iran

Farahnaz Jahanshahi Afshar1, Ebrahim Pourjam2* and Ahmad Kheiri3

1. Department of Nematology, Iranian Research Institute of Plant Protection, P.O. Box: 1454-Tehran, 19395, Iran.
2. Department of Plant Pathology, College of Agriculture, Tarbiat Modares University, Tehran, Iran.
3. Department of Plant Pathology, University of Agricultural and Natural Resources, Tehran University, Tehran, Iran.

Abstract: Morphological and morphometric characters of two species of

superfamily Sphaerularioidea, recovered in southwestern Iran namely
Deladenus durus and Prothallonema obtusum are given. The recovered
specimens of D. durus is characterized by having a valvular chamber in
metacorpus and excretory pore posterior to the hemizonid. The Iranian
population of P. obtusum is characterized by having four lines in the lateral
field, excretory pore anterior to the end of pharyrix, not bulgy vulva region
and short subcylindrical tail.

Keywords: Deladenus durus, Prothallonema obtusum, Pistacia atlantica, Iran.

12
Introduction The superfamily Sphaerularioidea with its
232 species from three families
More than thirty nematode families have been Neotylenchidae, Sphaerularidae and
known to be insect associated or parasites Allantonematidae belongs to the suborder
(Nickle, 1972, Poinar, 1975, 1983, 1990, Hexatylina Siddiqi, 1980 (with 298 species).
Maggenti, 1981 and Kaya and Stock, 1997). Members of this superfamily usually possess
Some groups of nematodes are obligate insect two types of generation i.e. entomoparasitic
parasites or entomopathogens which can (insect or mite haemocoel parasitic) and
infect and kill a broad range of insect hosts. free-living (fungus-feeder or plant-parasitic)
However, due to biocontrol potential of these forms (Andrássy, 2007). However, some
nematodes, several studies have focused on may have only one type of generation
seven families namely Mermithidae Braun, (Siddiqi, 2000).
1883, Allantonematidae Pereira, 1931, The main characters of the family
Neotylenchidae Thorne, 1941, Sphaerularidae Neotylenchidae are having long pharyngeal
Lubbock, 1861, Rhabditidae Oerley, 1880, overlapping and a well developed bursa. The
Steinernematidae Filipjev, 1934 and seven genera of this family contain 46 species
Heterorhabditidae Poinar, 1975 (Grewal et (Andrássy, 2007). Currently, three of these
al., 2005). Members of Steinernematidae and species namely Fergusobia indica (Jairajpuri,
Heterorhabditidae have attracted more 1962) Siddiqi, 1986, Gymnotylenchus zeae
attention as biocontrol agents of insect pests, Siddiqi, 1961 and Hexatylus mulveyi Das,
compared to the members of the rest families 1964 have been recorded from Iran (Barooti
(Lacey et al., 2001). et al., 2002, Barooti and Golzar, 1993 and
Kheiri, 1972a, respectively).
Handling Editor: Dr. Majied Pedram The main characters of the family
________________________________ Sphaerularidae are presence of a very long
*
Corresponding author, e-mail: pourjame@modares.ac.ir uterus in fertilized females and bulb-like
Received: 21 April 2013, Accepted: 30 September 2013

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pharyngeal glands, forming a short lobe over Deladenus durus (Cobb, 1922) Thorne, 1941
intestine; often with a stem-like extension. (Table 1; Fig. 1)
This family has ten genera and 47 species Description
(Andrássy, 2007).
There are reports on occurrence of three Mycetophagous female: Body slender, tapering
species of this family namely Prothallonema gradually toward both ends, straight or slightly
asymmetricum (Thorne, 1941) Siddiqi, 1986, P. curved ventrally after fixation. Cuticle with fine
intermedium (Christie, 1938) Siddiqi, 1986 and annuli, about 1 μm wide at mid-body. Lateral
P. mucronatum (Thorne and Malek, 1968) field with seven incisures. Lip region smooth,
Siddiqi, 1986 in Iran (Mirzaee-qomi et al., low and continuous with body contour. Head
2010, Motamedi et al., 2004 and Gharakhani et framework weakly sclerotized. Stylet delicate,
al., 2010, respectively). 8-10 µm long with distinct basal knobs. Dorsal
This study aims to discuss on morphological pharyngeal gland orifice near to the base of
characters and morphometric features of two stylet. Procorpus cylindrical, metacorpus
species belonging to the superfamily slightly swollen, with oval median chamber, 5
Sphaerularioidea, recovered from Jiroft region, µm long and 2.5 µm wide, isthmus narrow,
Kerman province of Iran. cylindrical, dorsal pharyngeal gland elongate,
overlapping intestine dorsally with distinct
Materials and Methods nucleus, the subventral glands obscure.
Excretory pore 128 μm from the anterior end,
A total number of 100 soil and root samples its duct heavily sclerotized. Deirids located near
were collected from several orchards during excretory pore. Hemizonid 4 μm long, 5 μm
2007-2008. The nematodes were extracted anterior to the excretory pore. Nerve ring at the
using sieving and centrifugal-flotation posterior portion of isthmus, about 88 µm from
techniques (Jenkins, 1964). The permanent the anterior end. Intestine joins pharyrix at the
slides of nematodes were prepared after level of the nerve ring. Ovary outstretched,
fixation and transferring to anhydrous vulva situated posterior at about 90% of the
glycerin (De Grisse, 1969). Identification of body length with protuberant lips, post-vulval
the recovered nematodes was carried out uterine sac absent, vagina anteriorly directed,
using morphological and morphometric spermatheca axial, elongate and filled with
characters. The measurements and drawings rounded sperm. Tail conoid, slightly longer
were performed using a drawing tube than vulva-anus distance, with a small mucro.
attached to an Olympus BH-2 light Male: Similar to mycetophagus female with
microscope. exception in reproductive system. Body more
slender. Spicules and gubernaculum tylenchoid,
Results and discussion bursa terminal, not enveloping the mucronate
Among several genera belonging to different tip of the tail.
orders, two species belonging to the suborder
Hexatylina (superfamily Sphaerularioidea) were Habitat and locality
recovered and identified. One of the recovered Deladenus durus was originally described as
species, Deladenus durus (Cobb, 1922) Thorne, Tylenchus durus by Cobb (1922), recovered
1941 belongs to the family Neotylenchidae and from galls of swamp chestnut-oak (Quercus
the other species, Prothallonema obtusum prinus L.) and decomposing fungi (Pleurotus
(Thorne, 1941) Siddiqi, 1986 belongs to the sp.) beneath dead bark of Fremont poplar
family Sphaerulariidae. The morphological and (Populus frenonti S. Wats) from Virginia in
morphometric characters of the two above USA. It was later recovered by Thorne (1941)
mentioned species are presented herein for the from the rhizosphere of Lucerne in Utah and
first time. Oregon (USA). It has also been found in sandy

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Jahanshahi Afshar et al. ____________________________________________ J. Crop Prot. (2014) Vol. 3 (1)

soil infested with wild grass rosettes from this species was recovered from the rhizosphere
Canada (Das, 1964), Italy (Vinciguerra, 1972), of wild pistachio or Baneh (Pistacia atlantica)
and India (Bajaj et al., 1981). In present study, in Jiroft region of Iran.

Table 1 Morphometric data of the Iranian population of Deladenus durus and data of other populations reported
by different authors (All measurements are given in micrometer and in the form mean ± SD (range)).
D.
Species (the Tylenchus D. durus D. andrassyi
D. durus (Cobb, 1992) Thorne, D. durus D. durus (Massey, paraduruD. durus Chitamber
original names durus Cobb Thorne Vinciguerra
1941 Das (1964) 1974) Chitamber, 1991 s Bajaj (1991)
are used) (1922) (1941) (1972
(1981)
Galls of Sandy soil
Soil
swamp Tthe infested Dendroctonus
The rhizosphere around Population cultured
Habitat chestnut-oak rhizosphere with wild Moss on rock adjunctus in
of Pestacia atlantica the roots on Coleophoma sp.
(Quercus of Lucerne grass ponderosa pine
of wheat
prinus L.) rosettes
Utah and
Virginia Las Cruces, New
locality Kermen,Iran Oregon Canada Villarosa, Italy Ruidoso, New Mexico India
(USA) Mexico
(USA)
Femal Femal
Characters Female Male Male Male Female Female Female Female Female
e e
n 5 2 1 1 - - 8 3 4 7 45

L 880 ± 25 (840-910) 525-605 820 1000 1000 1000 980-1360 1080-1120 874 ± 100.6 (796-944) 620-910 915 ± 35 (724-1232)

L' 842 ± 25 (800-867) 500-575 - - - - - - - - -

a 45.4 ± 2.0 (42.0-46.8) 50.4-52.3 37 37 30-50 50 29-39 27-32 38 ± 6.6 (34-44) 35-47 35 ± 2.2 (21-50)

b 9.6 ± 0.4 (9.1-10.2) 7.7-7.9 7.7 7.7 8-10 8-10 7.8-9.3 ? 9.8 ± 1.3 (8.6-10.4) 3.7-5 10.7 ± 0.4 (8.7-16)

b' 4 ± 0.5 (3.4-4.7) 3.7-3.7 - - - - - - 4.4 ± 0.8 (3.7-4.8) - 5.9 ± 0.5 (1.6-12.1)

c 23 ± 1.3 (21.5-25) 20.2-20.9 20.8 62.5 25 24 19.5-23.6 22-24 24.6 ± 2.4 (22.4-25.9) 21-28 27.8 ± 1.3 (20.9-39.3)

c' 3.4 ± 0.2 (3.2-3.6) 2.3-2.7 2.5 0.8 - - - - 2.9 ± 0.5 (2.6-3.3) - 2.2 ± 0.1 (1.6-2.8)

V or T 93.4 ± 0.2 (93.2-93.7) 36.2-42.8 93 - 93 65 92-93 90 93 ± 1.2 (91-93) 90-93 93 ± 0.3 (90-95)

V' 97.7 ± 0.3 (97.4-98.1) - - - - - - - - - -

Stylet lenght 8-9 8 6 10 8 - 8.4-10.8 10-11 8.5± 0.2 (8.4-8.6) 7-8 9.6± 0.2 (8-11)
Pharyngeal
91.6 ± 3.2 (86-94) 68-77 - - - - - - - - -
lenght
Overlapping* 131 ± 20.9 (100-155) 75-85 - - - - - - - - -
Max. body
19.4 ± 0.5 (19-20) 10-12 22 - - - - - 23 ± 3.6 (22-26) - 26 ± 2.3 (16-52)
diam
Head-vulva 822 ± 2 (785-845) - - - - - - - - - -
Vulva-anus
19.8 ± 2.9 (15-22) - - - - - - 40 31 ± 3.5 (28-33) - 28 ± 1.3 (18-41)
distance
Tail 38.4 ± 2.1 (35-40) 25-30 33 16 - 41.7 - 33 36 ± 2.9 (34-38) - 34 ± 1.5 (21-43)
Tail/ vulva-anus
2 ± 0.4 (1.7-2.6) - - - - - - - - - -
(%)
body diam. at
11.4 ± 0.5 (11-12) 11 14 20 - - - - 12 ± 1.4 (12-13) - 16 ± 0.7 (11-22)
anus
Spicule length - 15-19 - 24 - - - - - - -

Gubernaculum - 6 - - - - - - - - -

* Anterior end to pharngeal intestinal junction.

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Two species of Sphaerularioidea ______________________________________________________ J. Crop Prot.

Figure 1 Deladenus durus: Male (A-D), Female (E-K). A & K: Entire body; B & I: Oesphageal
region; C & F: Anterior end and D: Tail; E: Reproductive system; G: Lateral field; H: Posterior end.

Discussion synonymised D. paradurus Massey, 1974 and

D. andrassy Vinciguerra, 1972 with D. durus.
The morphological and morphometric Iranian population of D. durus resembles D.
characters of this species is similar to those ipini Massey, 1974, D. ulani Sultanalieva,
given in the original description (Cobb, 1922) 1983, D. obesus Thorne, 1941, D. aridus
and those given in the revision of the species Andrássy, 1957 and D. indicus Singh,1976 but
(Thorne 1941) except for shorter body length of it differs from D. ipini and D. ulani by absence
male (525-605 vs. 1000 µm). Chitamber (1991) of post-vulval uterine sac. It also differs from

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Jahanshahi Afshar et al. ____________________________________________ J. Crop Prot. (2014) Vol. 3 (1)

D. obesus, D. aridus and D. indicus by having Male: Not found.

an oval chamber in the median bulb. In Table 2 Measurements of the Iranian population of
addition, this species is closely related to D. Hadrodenus saccatus and its comparison with type
nevexii Bedding,1974 and D. apopkaetus population (All measurements are given in
Chitamber, 1991 but differs from those species micrometer).
P. obtusum (Thorne, Stictylus obtusus,
by anterior location of excretory pore to the Species
1941) Siddiqi, 1986 Thorne (1941)
hemizonid vs posterior (Chitamber, 1991, Habitat
the rhizosphere of peach the rhizosphere of
and apple sugar beets
Sumenkova, 1989).
locality Kermen,Iran Utah (USA)
Prothallonema obtusum (Thorne, 1941) Characters Female Female
Siddiqi, 1986
n 5 -
(Table 2; Fig. 2)
Table 2 Measurements of female of the Iranian L 807 ± 85.2 (680-900) 1000
population of Prothallonema obtusum and its
comparison with type population (All measurements L' 767.4 ± 86.9 (636-860) -
are given in micrometer and in the form mean ± SD a 26.2 ± 1.8 (24.3-29) 25
(range)).
b 6.3 ± 0.5 (5.7-7.1) 6.4
Description b' 5.6 ± 0.5 (4.8-6.1) -

Mycetophagous female: Body relatively long, c 19.6 ± 1.7 (17-20.9) 18

slightly ventrally arcuate after fixation, obese c' 2.3 ± 0.3 (2.0-2.8) -
(the widest part of body is anterior to the
V 88.8 ± 0.9 (87.5-89.7) 90
vulva), gradually tapering toward both ends.
Cuticle with fine transverse striae (1.5 µm V' 93.5 ± 0.2 (93.3-93.8) -
wide). Lip region rounded, smooth, continuous,
Stylet lenght 11.9 ± 0.7 (11-13) -
9-11 µm wide and 2-3 µm high. Lateral field
with four incisures. Stylet slightly longer than Pharyngeal lenght 129 ± 13.5 (110-143) -
lip region width with asymmetrical knobs Overlapping 14.6 ± 6.5 (5-21) -
(ventro-submedian knobs larger than the dorsal
knob). The dorsal pharyngeal gland orifice S-E-pore 123 ± 10.4 (107-133) -
located at the base of the stylet. Procorpus Mid body width 30.8 ± 2.4 (28-34) -
cylindrical, metacorpus slightly swollen without
Head-vulva 718 ± 81.7 (595-807) -
a valve, basal bulb of pharyrix oval with conical
extension. Excretory pore anterior to the Vulva-anus 50 ± 5.5 (41-55) -
junction of pharyrix with the intestine, almost at
Tail 41.2 ± 1.6 (39-43) -
the level of base of pharyrix, its duct
Tail/ Vulva-anus
sclerotized. Hemizonid 5 µm long and 9 µm (%)
0.8 ± 0.1 (0.8-1) -
anterior to excretory pore. Deirids between Anal body width 17.4 ± 0.9 (16-18) -
hemizonid and excretory pore. Vulva as a
depressed transverse silt, vagina extending
about one-third the body width into the body, Habitat and locality
uterus broad, thin-walled, spermatheca This species was originally described by
elongate, axial and filled with large (2.5-3.5 Thorne (1941), recovered from the rhizosphere
µm) sperm, ovary anteriorly directed with of sugar beets in Utah (USA). In the present
reflexed tip, post-vulval uterine sac absent. Tail study, this species was collected from the
subcylindrical with rounded terminus, about rhizosphere of peach and apple trees in Jiroft
twice as long as the anal body diameter. region of Iran.

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Figure 2 Prothallonema obtusum: Female (A-H). A: Entire body; B: Pharyngeal region; C: Anterior
end; D: Lateral field; E and F: Tail; G: part of reproductive system and the posterior end.

Discussion of some species of Stictylus (S. hastatus Khan,

1957) have everted uterus similar to that in
Thorne (1941), originally described the species Prothallonema. Fortuner and Raski (1987) did
Stictylus obtusus. Siddiqi (1986) synonymized not accept this synonymization and proposed the
the genus Stictylus with Prothallonema Christie, genus Stictylus Thorne, 1941 as genus incertae
1938, because infective female and adult female sedis in Tylenchida. Again, Siddiqi (2000)

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Jahanshahi Afshar et al. ____________________________________________ J. Crop Prot. (2014) Vol. 3 (1)

considered Stictylus as a synonym of Proceedings of the 11th Iranian plant protection

Prothallonema, that was accepted by Andrássy congress, Rasht, Iran, 97.
(2007). Barooti, S., Maafi, Z. T., Kheiri, A. and
Iranian population of P. obtusum (Thorne, Golmohamah Zadeh Khiabani, N. 2002.
1941) Siddiqi, 1986 closely resembles the Plant parasitic nematodes fauna from South
originally described population (Thorne, 1941). of Baloochestan area in Iran. Proceeding of
This species comes close to P. intermedium the 15th Iranian plant protection congress,
(Christie, 1938) Siddiqi, 1986 and P. Kermanshah, Iran, vol. 2: Plant diseases and
asymetricum (Thorne, 1941) Siddiqi, 1986. It weeds, 184-185.
can be separated from P. intermedium by Chitamber, J. J. 1991. On the genuse Deladenus
having four lines in the lateral field (vs. six in P. Thorne, 1941 (Nematoda: Allantonematidae).
intermedium), location of excretory pore (at the Review of the mycetophagous stage. Revue de
base of terminal bulb vs. anterior part of Nematologie, 14: 427-444.
terminal bulb) and the shorter tail. Moreover, in Cobb, N. A. 1922. Two tree- infesting nemas of
P. intermedium (female) intestine continues the genus Tylenchus. Annales de Zoologia
posterior to the rectum forming a blind sac that Aplicada, 9: 27-35.
occupies one third to one half of the tail which Das, V. M. 1964. Hexatylus mulveyi n. sp. and
was not seen in P. obtusum (Geraert, et al., Deladenus durus (Cobb, 1922) Thorne, 1941
1984). Iranian population of P. obtusum differs (Nematoda: Neotylenchidae) from the
from P. asymetricum by having lower c value Canadian Arctic. Canadian Journal of
(20.7 vs. 27). Zoology, 42: 649-653.
De Grisse, A. T. 1969. Redescription ou
Acknowledgements modification de quelques techniques dans
L’etude des nematodes phytoparasitaires.
The authors are grateful to Late Prof. István Mede. Rijks. fak. Landbou Weten Gent, 34:
Andrássy, Dr. Akbar Karegar and Dr. Zahra 351-369.
Tanha Maafi for their valuable comments. The Fortuner, R., and Raski, D. 1987. A review of
financial support of Tarbiat Modares University Neotylenchoidea Thorne, 1942 (Nemeta:
is also appreciated. Tylenchida). Revue de Nematologie, 10:
257-267.
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‫ﮔﺰارش ﺟﺪﻳﺪ از دو ﮔﻮﻧﻪ ﻧﻤﺎﺗﺪ ﻣﺘﻌﻠﻖ ﺑﻪ ﺑﺎﻻ ﺧﺎﻧﻮاده )‪Sphaerularioidea (Nematoda:Tylenchida‬‬

‫‪3‬‬
‫ﻓﺮﺣﻨﺎز ﺟﻬﺎﻧﺸﺎﻫﻲ اﻓﺸﺎر‪ ،1‬اﺑﺮاﻫﻴﻢ ﭘﻮرﺟﻢ‪ *2‬و اﺣﻤﺪ ﺧﻴﺮي‬

‫‪ -1‬ﺑﺨﺶ ﺗﺤﻘﻴﻘﺎت ﻧﻤﺎﺗﺪﺷﻨﺎﺳﻲ‪ ،‬ﻣﺆﺳﺴﻪ ﺗﺤﻘﻴﻘﺎت ﮔﻴﺎﻫﭙﺰﺷﻜﻲ ﻛﺸﻮر‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‪.‬‬

‫‪ -2‬ﮔﺮوه ﺑﻴﻤﺎريﺷﻨﺎﺳﻲ ﮔﻴﺎﻫﻲ‪ ،‬داﻧﺸﻜﺪه ﻛﺸﺎورزي‪ ،‬داﻧﺸﮕﺎه ﺗﺮﺑﻴﺖ ﻣﺪرس‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‪.‬‬
‫‪ -3‬ﮔﺮوه ﺑﻴﻤﺎريﺷﻨﺎﺳﻲ ﮔﻴﺎﻫﻲ‪ ،‬داﻧﺸﻜﺪه ﻛﺸﺎورزي‪ ،‬داﻧﺸﮕﺎه ﺗﻬﺮان‪ ،‬ﺗﻬﺮان‪ ،‬اﻳﺮان‪.‬‬
‫* ﭘﺴﺖ اﻟﻜﺘﺮوﻧﻴﻜﻲ ﻧﻮﻳﺴﻨﺪه ﻣﺴﺌﻮل ﻣﻜﺎﺗﺒﻪ‪pourjame@modares.ac.ir :‬‬
‫درﻳﺎﻓﺖ‪ 1 :‬اردﻳﺒﻬﺸﺖ ‪1392‬؛ ﭘﺬﻳﺮش‪ 8 :‬ﻣﻬﺮ ‪1392‬‬

‫‪Prothallonema obtusum‬‬ ‫ﭼﻜﻴﺪه‪ :‬ﺧﺼﻮﺻﻴﺎت ﻣﺮﻓﻮﻟﻮژﻳﻜﻲ و ﻣﺮﻓﻮﻣﺘﺮي دو ﮔﻮﻧﻪ ‪ Deladenus durus‬و‬

‫‪D.‬‬ ‫ﻣﺘﻌﻠﻖ ﺑﻪ ﺑﺎﻻ ﺧﺎﻧﻮاده ‪ Sphaerularioidea‬از ﺟﻨﻮب ﺷﺮق اﻳﺮان اراﺋﻪ ﻣﻲﺷﻮد‪ .‬ﺟﻤﻌﻴﺖ ﺑﻪدﺳﺖ آﻣﺪه از‬
‫‪ durus‬ﺑﻪواﺳﻄﻪ وﺟﻮد ﻣﺤﻔﻈﻪ درﻳﭽﻪ ﻣﺎﻧﻨﺪ در ﺣﺒﺎب ﻣﻴﺎﻧﻲ و ﻗﺮار ﮔﺮﻓﺘﻦ ﻣﻨﻔﺬ ﺗﺮﺷﺤﻲ ﺑﻌﺪ از ﻫﻤﻴﺰوﻧﻴﺪ‬
‫ﻗﺎﺑﻞ ﺗﺸﺨﻴﺺ اﺳﺖ‪ .‬ﺟﻤﻌﻴﺖ ‪ P. obtusum‬ﺑﻪواﺳﻄﻪ داﺷﺘﻦ ﭼﻬﺎر ﺷﻴﺎر ﻃﻮﻟﻲ در ﺳﻄﺢ ﺟﺎﻧﺒﻲ‪ ،‬ﻗﺮار‬
‫ﮔﺮﻓﺘﻦ ﻣﻨﻔﺬ ﺗﺮﺷﺤﻲ در ﺟﻠﻮي ﺑﺨﺶ اﻧﺘﻬﺎﻳﻲ ﻣﺮي‪ ،‬ﻣﺘﻮرم ﻧﺒﻮدن ﻧﺎﺣﻴﻪ وﻟﻮا و ﻛﻮﺗﺎه ﺑﻮدن دم ﻧﻴﻤﻪ‬
‫اﺳﺘﻮاﻧﻪاي ﺷﻜﻞ ﻣﺸﺨﺺ ﻣﻲﺷﻮد‪.‬‬

‫واژﮔﺎن ﻛﻠﻴﺪي‪ ، Pistacia atlantica ،Prothallonema obtusum،Deladenus durus :‬اﻳﺮان‬

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