A. A. Al-Moussawi

Bull. Iraq nat. Hist. Mus.
(2010) 11 (1):27-38

FIRST RECORD IN IRAQ OF TANQUA ANOMALA (LINSTOW, 1904)
FROM THE DICE SNAKE, NATRIX TESSELLATA TESSELLATA

(LAURENTI, 1768)

Azhar A. Al-Moussawi
Iraq Natural History Museum, Baghdad University, Baghdad, Iraq

Bab Al-Muadham, P.O. Box 59038

ABSTRACT
Tanqua anomala (von Linstow,1904) specimens were recovered, from the lining
wall of the gastro-intestinal tract of the dice snake Natrix tessellate tessellate
(Laurenti, 1768) collected in Baghdad city, central Iraq. Measurements of the males,
females and a comparison of the nematode with other studies tabulated. Reporting of
Tanqua anomala from this snake represents the first record for Iraq as well as a new
host record.

INTRODUCTION
Reptiles are commonly infected by a wide range of parasites, serving either as their
definitive or intermediate hosts.
Reptiles of Iraq encountered a hundred species, including forty one species of
snakes (Reed and Marx, 1959; Mahdi and George, 1969; Afrasiab,
1987;Afrasiaband Ali, 1988; 1989 a, b and Leviton et al., 1992). Surprisingly, little
attention had been paid to their parasites, the papers on parasitic fauna of Iraqi
reptiles are rather few and fragmentary.
Marinkelle and Al-Mahdawi (1980) described the Protozoan Trypanosoma turcici
from the gecko Hemidactylus turcicus. Al-Barwari and Nassir (1983) recorded the
nematode Thelandros sp. From Hemidactylus flaviviridis and H. Persicus. Kugi and
Mohammad (1988) described the cestodes: Oochoristica nupta from the lizard
Agama nupta and isolated Oochoristica agama from Uromastix microlepis. Hassan
and Abdullah (1989) isolated the cestodes: Oochoristica truncata from Agama
ruderata and Ophisops elegans; the cestode Oochoristica tuberculata and the two
nematodes Thelandros micipsae and Thelandros sp. were isolated from
Ceratopodium scaberium (=Gymnodactylus scaber). Salih and Rahemo (1989)
recovered Cysticercoid of Joyeuxiella sp. from the wall lizards: C. scaberium and
Phyllodactylus elisae. Rahemo and Ami (1993) isolated the cestode Ophiotaenia
europea from Natrix tessellata. Fattohy and Al-Zubaidy (1994) reported the
protozoa Balantidium duodeni from Hemidactylus flaviviridis and the Cysticercoid
of the genus Joyeuxiella from Trapelus (= Agama) ruderata; H. flaviviridis;
Ophisops elegans and Phyllodactylus elisae and Thelandros micipsae from T.
ruderata; C. scaberium; H. flaviviridis and O. elegans; and Thelandros sp. From T.
ruderata; C. scaberium and O. elegans and the nematode Salobrella sp. from C.
scaberium; H. flaviviridis and O. elegans. Al-Hadithi and Abdl-Majeed(1989)

First Record in Iraq of Tanqua nomala

recovered the nematodes, Pharyngodon laevicauda from H. turcicus, Thelanderos
micipsae from C. scaberium; H. flaviviridis and Physalopteroid sp. from H. turcicus.
Al-Zako (1999), reported four nematodes from three reptilian hosts: Camallanus sp.
from the tortoise Testudo graeca; Neopharyngodon sp. from the geckos C.
scaberium and Thelandros vittata and Trispiculascaris sp. from the lizard Mabuya
vittata. Al-Saadi (2002) isolated the nematodes: Thelandros micipsae from C.
scaberium; H. flaviviridis and H.turcicu;Thelandros sp. from H. turcicus and C.
scaberium and the nematode Neopharyngodon sp. from H. flaviviridis and C.
scaberium. Among four reptilian hosts Al–Hashimi (2006) reported six parasites,
two trematodes: Telorchis cyclemmids from Mauremys (=Clemmys) caspica and
Bilorichis indicum from Rafetus euphraticus; two cestodes Oochoristica sp. and
Crepidobothrium sp. from Natrix tessellata and two nematodes Camallanus sp.
And Trispiculascaris sp. from Mabuya aurata. From seven species of Iraqi reptiles,
nine species of helminthic parasites were encountered by Al-Barwari and Saeed
(2007), the digenetic trematode Telorchis stunkardi from the turtle Mauremys c.
caspica; the cysticercoid of Diplopylidium nolleri from the geckos: Asaccus elisae,
Hemidactylus flaviviridis, H. persicus and from thes nake Spalerosophis d. cliffordi;
and 7 nematode species, Angusticaecum holopterum and Atractis dactyluris from the
tortoise Testudo g. Iberia (= terrestris) ;Camallanus microcephalus from Mauremys
c. caspica; Falcaustra japonensis from the turtle Rafetus(= Trionyx) euphraticus;
Tachygonetriani colleri from Testudo g. terrestris; Thelandros sp. From
Acanthodactylus elisae, H. flaviviridis, H. persicus and Microtetrameres sp. from
H. flaviviridis.,
The nominate dice snake, Natrix tessellate tessellata (Laurenti, 1768), distributed
from Middle and Southern Europe through Western Asia to western China including
India, Persia, Iraq, Syria and Egypt (Boulenger, 1920 ; Arnold and Burton, 1978
and Baran and Atatu¨r, 1998). It is present throughout Iraq with remarkably wide
distribution in rivers, lakes, channels and marshes (khalaf, 1959 and Mahdi and
George,1969). The studies of parasite communities of this snakein Iraq are rare and
scanty. This paper deals with recording the nematode Tanqua anomala from the
gastro-intestinal tract of this snake for the first time in Iraq and it also constitutes a
new host record as well.

MATERIALS AND METHODS
A total of 28 adult specimens of the Dice snake Natrix tessellate tessellate were
collected at Diyala Bridge, Baghdad City, Central Iraq during the period January to
November 2008. The snakes were transferred to the laboratory a live, sacrificed and
dissected as soon as possible. All viscera were removed and each placed in Petri
dish with normal physiological saline. The recovered nematodes fixed and stored in
70% alcohol and cleared by lactophenol. Helminth identification was based on
(Yamaguti, 1961;York and Maplestone, 1962).

All measurements of the nematodes are with millimeters (mm) unless otherwise
stated. Images were taken with digital camera; drawings were made with aid of a
camera Lucida. Helminth specimens were deposited in the collection of Iraq Natural
History Research Center and Museum \University of Baghdad \ Baghdad \ Iraq.

A. A. Al-Moussawi

RESULTS AND DISCUSSION

Gnathostomidae
Genus:Tanqua Blanchard, 1904
Tanqua, R. Blanchard, 1904 (= Ctenocephalus, v. Linst., 1904) (Baylis, 1916).
Tanqua anomala (v.Linst.) Baylis,1916
Tanqua anomala (Linstow 1904)
Synonyms: Heterakis anomala vonLinstow,1904(Baylis, 1939)

Blanchard (1904) erected the genus Tanqua to accommodate the nematode
Ctenophorus tiara (originally named Ascaris tiara). Baylis(1916) reviewed and
amended von Linstow’s description of T. tiara, described T. anomala and confirmed
that T. diadema Linstow,1904 was a valid species, and gave a key to sep arate
bet ween T. tiara and T. diadema.
The species belong to the genus Tanqua were identified in several monitors
(Jacobson, 2007). Worldwide, nine species of this genus have been described from
reptilian and amphibian hosts: Tanqua bainae; T. geoclemydis; T. gigantica; T.
herpestis; T. occlusa; T. ophidis; T. tiara; T. sindensis and Tanqua sp.
Twenty males and eighteen females of Tanquaanomala were collected from the
gastrointestinal tract of 28 snakes. The worm is of medium sizefound embedded its
head in the inner mucous lining wall of the gastro-intestinal tract of the snake.Head
with two relatively large lips, dorsal and ventral, each bearing on its inner side three
rounded tooth – like projections, head –bulb is relatively small, divided externally
into two swellings separated by lateral longitudinal grooves, the head bulb is
provided with rows of thorn-like spines which help this nematode to attach with the
host tissue, that makes its removal rather difficult. There is a cuticular collar behind
the head – bulb, there are four elongated cervical sacs extend from anterior margin
of cervical collar they appears to open separately upon the surface of the swellings at
the base of the lips, the esophagus long, simple slender increasing gradually in
diameter posteriorly (Fig.1 A&B) Posterior end of the body provided with series of
muscle-bands on each side of the ventral surface, ending at front of the anus.
Measurements of 20 male and 18 female worms were done with an ocular
micrometer and means were tabulated.
Male Fig.(2):Twenty males were isolated from the gastrointestinal tract of the snake,
the body is attenuated towards the posterior ends. On the tail there are eight pairs of
ventro-laterally sessile caudal papillae, they are different in sizes: three preanals, one
adanal and four Postanals, the last pair is very small; the largest pair is the seventh
from posterior end. The two curved ventrally spicules are with blunt ends, they are
similar, equal in length and spiny, tail tapering to point with caudal alae.
Female: Fig. (3): Eighteen females were isolated from the snake. They are larger
than males. Posterior end of the body has a short tail, which bears a pair of papillae,
the vulva is nearer for the posterior end, it situated at about the posterior third of the
body, oviparous, eggs oval, with thin shells and fine granulations, tail is short,
tapering and pointed.

First Record in Iraq of Tanqua nomala

Table 2 shows a slight differences in present nematode measurements from that of
Baylis (1939) and Dewi et al.,(2008), it could be due to the difference of host
species and their habitat ecosystems since the nematodes of Baylis (1939) were
isolated from the water snake Tropidonotu spiscator in India and Ceylon and
specimens of Dewi et al., (2008) were isolated from the intestine of the semi-
aquatic snake Acrochordus javanicus in south Sumatra/Indonesia.
The description of T. anomala by Baylis (1916) was brief for the nematode which
isolated from the stomach of Tropidonotu spiscator in ceylon, and confirmed that T.
diadema Linstow, 1904 is a valid species for T. anomala, and gave a key to separate
between T. tiara and T. diadema. In 1939 from the same host in India and Ceylon
Baylis described T. anomala and gave detailed descriptions and dimensions for
males and females.

Table.1: Measurements of T. anomala (von Linstow, 1904)Baylis1939; Dewi

et al.,2008 and the present study.

Measurements T. anomala
(Baylis, 1939)

T. anomala
(Dewi et al.,

2008)

T. anomala
(present
study)

Body length ♂

♀

26.5 – 50.0

30.1 – 56.0

25.0 – 39.5

33.6 – 43.9

30 (12-42)

38 (27-50)
Body maximum
width ♂

0.8-2

0.95-2

0.49– 0.89

0.67–0.94

0.79 – 1.09

0.89 -1.22

Oesophagus ♂

♀

3.0 – 5.3

(not separated between

♂ and ♀)

3.224 – 5.798

3.454 –4.238

2.882- 3.118

3.575- 4.195

Spicules

1.3 – 1.7

0.745 – 1.326

0.520-1.65

Vulva (from
posterior
end)

1/3

1/3.72

1/3.44

Eggs (µm)

65 x 50

50 x 38

70 x 50

This worm was reported from the water snake Natrix piscator (=Tropinodonotus
piscator) (Baylis,1939;Sinha and Sahay, 1972; Soota and Chaturvedi, 1974; Rao et

A. A. Al-Moussawi

al., 1977; Naidu, 1978; Kalyankar and Kankal,1980; Lakshmi, et al., 1985 and
Kankal, 1989) from the snake Natrix stolatus (Soota and Chaturvedi, 1973;
Saharan and Sinha, 1974), Nama (1974) reported a single immature female Tanqua
anomala from the body-cavity of amphibian host Rana tigrina. From the snake
Cerberus rhyncopus it was isolated in Pakistan (Bilqees and Rehana, 1975), from
the stomach of Natrix sp. by Gupta and Duggal (1981) and in India from the
colubrid snake Atretium schistosum by Lakshmi et al. (1985).
Table 2 shows that females generally larger than males.
Recently Dewi et al.(2008) isolated and redescribed T. anomala from the intestine of
the semi-aquatic snake Acrochordus javanicus in south Indonesia and to resolve the
confusion of the status of T. anomala and to clarify the taxonomic position of the
two species(T.anomala and T.ophidis) they used the scanning electron microscopy
(SEM), and as a result of comparison between these two species according to the
morphological features they confirmed that T. anomala as a valid species and
Tanqua ophidis Johnston & Mawson, 1948 falls in synonymy with it. This agree
with Gupta and Duggal, (1981) who regarded that T. ophidis is as junior synonym
for T. anomala.

Table.2: Means of measurements for males and females of T.anomala (von
Linstow, 1904).

Measurements Males Females

Body (L x w)
30 x 7.0 38 x 1.0

Head (L x w) 0.23 x 0.25 0.25 x 0.30
Oesophagus(L x w)
3.0 x 0.40 3.7 x 0.44

Cervical sac (L) 0.50 0.54
Excretory pore from anterior
end 0.72 0.83

Nerve ring (L x w) 0.09 x 0.18 0.09 x 0.19

nerve ring from anterior end 0.40 0.44

Spicule 1.08 -

Eggs (L x w)
(µm) - 70 x 50

Vulva (from posterior end) -

Tail(L) 0.60

0.80

First Record in Iraq of Tanqua nomala

ACKNOWLEDGEMENTS
The author would like to thank Kartika Dewi and Amir Hamidy from the Museum
Zoologicum Bogoriense, Bogor/ Indonesia, to Dr. Isam Saeed from the University of
Copenhagen / Denmark, and to Prof. Farhan T. Mhaisen for sending papers.
From Iraq Natural History Research Center and Museum / University of Baghdad,
the author is very grateful to Prof. Mohammad K. Mohammad, the director, for
supporting the diagnosis of nematodes, Khalida Ibrahim for her kind assistance in
laboratory work and to Mohammad I. Ghazwan, for collecting the snakes.

LITERATURE CITED
Afrasiab, S.R. 1987 First record of Stenodactylus affinis (Murray) marsh geckos

(Reptilia: Gekkonidae) in Iraq.j. Biol. Sci. Res. 18 (1):231-233.

Afrasiab, S.R. and Ali, H.A. 1988.A new record of toad Bufo surdus Boulenger

(Amphibia, Bufonidae) from Iraq, with a preliminary key for Iraqi amphibian.
Bull. Iraq Nat. Hist. Mus. 8: 115-123.

Afrasiab, S.R. and Ali, H. A. 1989. A report on a collection of reptiles from

Rumaila Desert, south of Iraq. Bull. Iraq Nat. Hist. Mus. 8(2): 65 – 73.

Afrasiab, S.R. and Ali, H.A. 1989b. A new record of the snake Lytorbychu

skennedyi Schmidt (Reptilia: Colubridae) from Iraq. Bull. Iraq Nat. Hist. Mus.
8(2): 157-159.

Al-Barwari, S.E. and Nassir, J.K. 1983First record of ten species of helminthic

parasites from vertebrates in Iraq. Iraqi J Science, 24: 101-108.

Al-Barwari S.E. and Saeed, I. 2007.On the helminthfauna of some Iraqi

reptiles.Türkiye Parazitoloji Dergisi, 31(4): 330-336.

Al-Hadithi, I.A.W. and Abdl-Majeed, M. I. 1989 Some helminth parasites from

jeckos in Basrah, Iraq. Al-Mustansiriya J. Sci. Vol. 9(1): 19-22.

Al –Hashimi, S.F.A. 2006. Parasitic worms of alimentary canal of some reptile

species in Al-Ramadi city. Msc. thesis. Edu. Univ. Al-Anbar: 77pp. (in Arabic)

Al-Saadi, A.A.J. 2002. Incidence of three nematode species from the digestive tract

of three lizard species in Baghdad city. Diyala Journal, 13: 385-391.

Al-Zako, S.S.H. 1999. A survey on intestinal nematodes of some amphibians and

reptiles in Ninevah province with special reference to the histology of
Ascaridiagalli(Schrank, 1788)Freeborn, 1923.Ph.D. thesis, Edu. Univ. Mosul:
193 pp. (in Arabic)

A. A. Al-Moussawi

Arnold, E.N. and Burton, J.A. 1978. A field guide to the reptiles and amphibians of

Britain and Europe, Collins, London: 272 pp.

Baran, I., and Atatu¨r,M. K. 1998, Turkish Herpetofauna (Amphibians and Reptiles).

Publication Board of the Ministry of Environment, Ankara, Turkey: 214 pp.

Baylis, H. A. 1916The nematode genus Tanqua R. Blanchard. Annals and Magazine

of Natural History, series 8, vol.17: 223–232.

Baylis, H.A. 1939 The Fauna of British India. Nematoda’, vol.2 (Filarioidea,

Dioctophymoidea and Trichinelloidea). Taylor and Francis, London,:198–202.

Bilqees, F. M. and Rehana, R. 1975A record of helminth parasites from snakes of

Sind, Pakistan. Acta Parasitologica Polonica Vol.23 No. 41/51: 485-492.

Blanchard, R. 1904Tanqua, n. g., remplaçant Ctenocephalus vonLinstow. Archives

de Parasitologie, 8: 478.

Boulenger, G.A. 1920. A list of snakes from Mesopotamia collected by members of

the Mesopotamian expeditionary force, 1959 to 1919.Journal of Mombay
Natural History Society. Vol.27 No.2: 25-28.

Dewi,Kartika, Jones, Hugh, and Hamidy, Amir 2008. The Status of Tanqua

anomala (Von Linstow, 1904 (Nematoda: Gnathostomatoidea) Transactions of
the Royal Society of South Australia, Volume 132, Number 1, May , pp. 7-
13(7)

Fattohy, Z.I. and Al-Zubaidy, A.B. 1994.Parasites of some lacertidae in Baghdad

province,Iraq.J.Educ.sci.Vol. 18: 12-25 (in Arabic).

Gupta, N. K. and Duggal, C. L. 1981. On the redescripton of Tanqua anomala (V.

Linstow, 1904) Baylis, 1916 (Nematoda: Gnathostomatidae) and discussion on
the synonymy of T. ophidian Johnston and Mawson, 1948. Research Bulletin
of the Panjab University, Vol. 30 (1-4): 61-64.

Hassan, I.S. and Abdullah, I.A. 1989.Helminth parasites of the digestive tract of

lizards in Ninevah district, ira. J. Educ. and sci.Vol.9:88-99.

Jacobson, E.(Ed.) 2007. Infectious diseases and pathology of reptiles: color atlas

and text. University of Florida College of Veterinary Medicine Gainesville,
Florida.CRC Press, Taylor & Francis Group, LLC,716 pp.

First Record in Iraq of Tanqua nomala

Kalyankar, S. D. and Kankal, N. C. 1980 Preliminary study on the effect of diet
deficiency of certain biochemical compounds on the host infected by the
nematode parasite. Rivista di Parassitologia Vol. 41 No. 2 pp. 165-169.

Kankal, N. C. 1989Histochemistry of Tanqua anomala a nematode parasite of

water snake Tropidonatu spiscator. Rivista di Parassitologia, 4 (48), 2, pp 175-
184

Khalaf, K. T. 1959. Reptiles of Iraq with some notes on the amphibians, Ar –Rabitta

Press, Baghdad,: 96 pp.

Kugi G. and Mohammad, K. 1988Cestodes of the genus Oochoristica from Iraqi

lizards. Jps. J. Parasito., 37(6): 405-409.

Lakshmi, B.B., Hanumantha,Rao, K. and Shyamasundari 1985.'The nematode fauna

from reptiles of Andhra Pradesh.' Indian Journal of Helminthology (New
Series), Meerut 2(1&2): 115-125.

Leviton, A.E.; Anderson, S.C., Adler, K. and Minton, S.A. 1992. Handbook to

middle east amphibians and reptiles. Society for the study of amphibians and
reptiles: 252 pp.

Mahdi, N. and George, P.V. 1969A systematic list of vertebrates of Iraq. Iraq

Natural History Museum, Publication, No. 26.University of Baghdad, Al-
Awqat Press: 104 pp.

Marinkelle, C.J. and Al-Mahdawi, S.K. 1980.Trypanosoma turcici sp. n.

(Trypanosomatida) from the Meditettanean gecko, Hemidactylus turcicus from
Iraq. Bull Nat. Hist. Res. Centre, 7: 73-79.

Naidu, T. S. V. 1978. Observations on tissue changes caused at the sites of

attachment of the nematodes, Tanqua anomala and Dispharynx nausta. Current
Science pp. 788-789.

Nama, H. S. 1974. On the occurrence of Tanqua anomala (Nematoda:
Gnathostomatidae) from Rana tigrina. Journal of the Zoological Society of
India, Vol. 25 (1/2): 157-158.

Rahemo, Z.I.F. and Ami, S.N. 1993Ophiotaenia europea(Cestoidea:Protocephalidae)
from water snake Natrix tessellata in Iraq. Mutah Journal for Research and
studies. Vol. 8(3): 101 – 110.

Rao, K. H.,Shyamasundari, K. and Kumari, B. V. 1977.On nematode cleavage

pattern with special reference to Tanqua anomala (V.Linstow, 1904)

A. A. Al-Moussawi

(Gnathostomatidae) from the water snake Natrix piscator Schneider. Current
Science. 46 (16) 565-566.

Reed C. A. and Marx, H. 1959 A Herpetological Collection from Northeastern
Iraq. Transactions of the Kansas Academy of Science, Vol. 62 (1): 91-122.

Saharan, R. K. and Sinha, R. M. P. 1974 On the occurrence and heavy infection of
a spirurid nematode Tanqua anomala (Von Linst) in a new host. Indian Journal
of Helminthology, 24 (2): 2165-67.

Salih, N.E. and Rahemo, Z.I.F. 1989.Cysticercoid of Joyeuxiella sp. from the wall
lizards in Iraq with special reference to its cyst wall. Rivista Parasitologia, 6:
239-244.

Sinha, A. and Sahay, U. 1972. On the redescription of Atrophocaecum indicum
Simha, 1958 (Acanthostomidae Poche, 1926; Emend. Nicoll, 1935). Indian
Journal of Animal Research , 6 (1): 39-41.

Soota, T. D.andChaturvedi, Y. 1973. Systematic studies on some more nematodes
from the unnamed collections of the Zoological Survey of India.Records of the
Zoological Survey of India. 67(1/4): 121-137.

Soota, T. D.andChaturvedi, Y. 1974.The nematode fauna of Goa. Pt. II. Indian
Journal of Helminthology. Vol. 24 No. 1: 22-35.

Yamaguti, S. 1961 Systema Helminthum Vol.3 The nematodes of vertebrates.

Intersci. Pub. Inc., New York,779 pp.

York,W. and Maplestone P.A. 1962.The nematode parasites of vertebrates. Haf.

Pub.Com., New York: 536 pp.

First Record

Fig.1:
A- Anterior end of Tanqua anomala.
B- Head –bulb.

First Record in Iraq of Tanqua nomala

-A-

-B-

anomala.

Fig. 2: Posterior end of male Tanqua

Fig. 3: Posterior end of female Tanqua anomala

A. A. Al-Moussawi

Tanqua anomala.

Tanqua anomala

First Record in Iraq of Tanqua nomala

Bull. Iraq nat. Hist. Mus.
(2010) 11 (1): 27-38

ش ن ن تسجیل ألول مرة في العراق Tanqua anomala (Linstow, 1904) م
المدورة

Natrix tessellata tessellata (Laurenti, 1768) الماء

الموسويأزھار أحمد

مركز بحوث و متحف التأریخ الطبیعي
العراق –بغداد -جامعة بغداد

ahmeda_09@yahoo.com: البرید االلكتروني

الخالصة
حنش الماء حیة من الغشاء المبطن للقناة الھضمیة ل تم عزل الدودة المدورة

Tanqua anomala تم وصف ھذه المدورة .وسط العراق بغدادمدینة من
ومقارنة القیاسات بین الجنسین كما تمت مقارنتھا مع القیاسات المذكورة لھا في

ھذه المدورة ھو األول في العراق كما لیعتبر تسجی .الدراسات العالمیة السابقة
.سجلت في ھذه الدراسة الحیة كمضیف جدید لھا

mailto:ahmeda_09@yahoo.com