Bull


 

 

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Mohammad K. Mohammad and Azhar A. Al-Moussawi 
 

Bull. Iraq nat. Hist. Mus. 

(2017) 14 (3): 205-213 

 

THE SPOTTED SANDGROUSE, PTEROCLES SENEGALLUS 

(LINNAEUS, 1771) AS A NEW HOST FOR THE SPIRURID 

NEMATODE HARTERTIA GALLINARUM (THEILER, 1919) IN IRAQ 

 

Mohammad K. Mohammad and Azhar A. Al-Moussawi* 

Iraq Natural History Research Centre and Museum, University of Baghdad, 

Baghdad, Iraq 

*Corresponding Author:  azhar.nhm@gmail.com 

 
Received Date: 16.March.2017                                              Accepted Date: : 24.April.2017 

ABSTRACT 
    In this work, the spirurid nematode Hartertia gallinarum was reported in the intestine of 

the spotted sandgrouse, Pterocles senegallus, collected in three different locations: Ga'ara 

Depression, Iraqi Western Desert, Zurbatiyah and Al-Attariyah, Middle of Iraq. Description 

and measurements of the nematode were given. The role of termites in the infection of P. 

senegallus with H. gallinarum was discussed. Occurrence of H. gallinarum in P. senegallus 

represents a new host record. 

 

Key words: Hartertia, Iraq, Pterocles, Spotted sandgrouse, Termite. 

 

INTRODUCTION 
    The spotted Sandgrouse Pterocles senegallus is a common and widely distributed bird 

(Bolster, 1922) found in North Africa and Middle East, and it is a native bird in Iraq (BirdLife 

International, 2016). It inhabits mainly sand deserts and semi deserts with scattered plants and 

breeds nesting on ground in suitable areas of the middle and southern Iraq (Salim et al., 2006). 

This species is considered as one of the most popular game birds in its distribution range in 

Iraq.  

 

    The nematode Hartertia gallinarum (Theiler, 1919) is distributed in South and West Africa 

and Asia. It causes host diarrhea, weight loss, weakness and decreased egg production and 

losses of the bird host (Kaufmann, 1996).  

 

    In Iraq, Al-Hubaity (1976) found H. gallinarum in fowl Gallus gallus domesticus in Mousl, 

north of Iraq. Then it has been isolated from the caecum of Rock partridge, Alectoris graeca 

and from the gizzard, proventriculus, intestine and liver of Seesee partridge, Ammoperdix 

griseogularis in the Gara-area, Rutba, western desert district respectively (Mohammad, 1996; 

Mahmoud et al., 2000). Later, Khoshnaw and Abdullah (2013) recorded it in the caecum of 

chukar partridge Alectoris chukar in Shaqlawa district, Kurdistan region, North of Iraq.  

 

    The present paper deals with recording the nematode H. gallinarum from the intestine of P. 

senegallus for the first time in Iraq. 

 

  

 

 

DOI: http://dx.doi.org/10.26842/binhm.7.2017.14.3.0205\ 

 

http://dx.doi.org/10.26842/binhm.7.2017.14.3.0205/


 

 

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The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host 

MATERIALS AND METHODS 
    A total of 16 spotted Sandgrouse, Pterocles senegallus (10 males and 6 females) were 

collected in three different locations; Ga'ara Depression, Iraqi Western Desert (7 males and 4 

females), Zurbatiyah (1 male and 1 female) and Al-Attariyah (2  males and 1 female), Middle 

of Iraq (Map 1). Collection of birds was done during January-December 2016 in Zurbatiyah 

and Al-Attariyah while those of Ga'ara were previously collected during the years 2003-2004. 

Gastrointestinal tracts of the collected animals were excised, opened longitudinally and 

nematodes were removed, washed with physiological saline, fixed in 70% alcohol, cleared in 

lactopheno and identified morphologically based on the available keys and descriptions 

(Cram, 1927; Yamaguti, 1961). All measurements are in millimeters given as means followed 

by ranges in parentheses. Photomicrographs were taken with a digital camera Infinity lite-

K100 attached to compound microscope Micros MCX100. 

 

 
Map (1): Showing the collection sites of host birds from different regions of Iraq. 

 

 

RESULTS AND DISCUSSION 
Order Spirurata 

Family Spiruridae 

Genus Hartertia Seurat, 1915. 

Hartertia gallinarum (Theiler, 1919) Cram, 1927. 

Synonym: Filaria  gallinarum Theiler, 1919. (Cram, 1927). 

 

    Only specimens of the spotted sandgrouse, P. senegallus from Ga'ara Depression were 

infected with 29 specimens of H. gallinarum, 3 males and 26 females with an infection rate of 

100% while the rest of the host samples yielded no parasites. The total infection rate was 



 

 

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Mohammad K. Mohammad and Azhar A. Al-Moussawi 
 

68.75% with intensity of 2.64. According to Encyclopedia of Life (2017), GBIF (2017) and 

Fauna Europaea (2017), this nematode belongs to the order Spirurata and the family 

Hartertiidae. It has one synonym which is Filaria gallinarum Theiler, 1919. The worm is 

filiform attenuating at each extremity. Cuticle thick is finely striated transversely. Head small 

with a slight constriction. Two lips are trilobed and each lip toothed, with a lateral papilla and 

lined by a thick cuticle. Two cervical papillae just behind the lips. The pyriform vestibule is 

short. Esophagus is divided into two parts; the anterior one is short and muscular. The 

posterior is longer and glandular.  

 

Male (Pl. 1, 2 and 3): Three males were isolated, each with symmetrical caudal alae. Six 

pedunculated papillae, four pairs are preanal. Measurements of three specimens were: Body is 

16.003 (15.351-16.642) long x 0.79 (0.63-0.90) maximum wide. Cephalic papillae is situated 

at a distance of 0.052 (0.052-0.052) far from the anterior extremity of the body. Pyriform 

vestibule is 0.128 (0.120-0.135) long x 0.161 (0.145-0.182) wide. Oesophagus reaches 2.625 

long in one specimen in which body length was 15.351. Oesophagus length as a proportion of 

body length is 0.171. Nerve ring 0.038 (0.031-0.047) long x 0.184 (0.166-0.197) wide, at a 

distance of 0.3032 (0.208-0.400) far from anterior extremity. Six pairs of pedunculated 

papillae, of which four precloacal and two postcloacal and group of very small sessile papillae 

present at tip of the tail. Spicules unequal, right spicule is 0.4108 (0.3224-0.468), the left 

spicule is (measurements for two specimens only) 1.522 (1.510-1.534) long. Tail length is 

0.529 (0.5096-0.546). Tail length as a proportion of body length is 0.033 (0.0306-0.0356). 

 

Female (Pl. 4, 5): Twenty-six females were isolated. They are larger than males. Body is 

18.385 (9.807-28.455) long x 0.758 (0.260-1.523) maximum wide. Head is 0.089 (0.057-

0.119) long x 0.187 (0.130-0.244) wide. Tooth at a distance of 0.094 (0.050-0.124) from 

anterior extremity of the body. Cervical papillae are situated at a distance of 0.0349 (0.026-

0.0468) from anterior extremity. The vestibule is 0.143 (0.022-0.218) long x 0.161 (0.114-

0.234) wide. Excretory pore is situated at 0.451 (0.338-0.546) from anterior extremity. 

Oesophagus is 3.077 (2.654-3.675). Oesophagus as a proportion of body length is 0.179 

(0.147-0.209). Nerve ring is 0.055 (0.026-0.13) long x 0.204 (0.145-0.296) wide, at distance 

of 0.316 (0.208-0.520) from anterior extremity. Vulva distance from anterior extremity is 

11.485 (5.612-16.720). The embryonated eggs have thick double shell. Tail is conical, 

rounded at its end and 0.408 (0.025-1.575) long.  

 

    The morphology of H. gallinarum in the present study did not show differences from H. 

gallinarum found in Cram (1927) but there are some differences in measurements between 

the present specimens and those of Cram (1927) as well as with those of the other local 

studies by (Al-Hubaity, 1976; Mohammad, 1996; Mahmoud et al., 2000; Khoshnaw and 

Abdullah, 2013) which had been isolated from different bird species belonging to another 

order. Presence of the same species of parasites in different host species may induce some 

morphological variations (Hildebrand et al., 2015) and / or physiological variations 

(Mehlhorn, 2016). 

 

    It is worth to mention that Mohammad (1996) had reported this nematode from Alectoris 

graeca. This host was proved later to be A. chukar according to Salim et al. (2006). So, the 

hosts examined by Mohammad (1996) and Khoshnaw and Abdullah (2013) were actually the 

same bird species (A. chukar). Occurrence of H. gallinarum in P. senegallus of the present 

investigation represents a new host record in Iraq and to the best of our knowledge it is the 

first time that this parasite has ever been recorded from members of the family Pteroclididae 

(Order, Pterocliformes). Regarding transmitting of H. gallinarum to its present host which 

depends only on small seeds (Bolster, 1922), we have now only indirect evidence that the 



 

 

208 

The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host 

spotted sandgrouse P. senegallus eats ants and termites during its breeding season (Campbell 

and Lack, 1985) probably because protein is required for egg laying, incubation activities and 

chick growing. It is necessary to reveal this subject through crop analyses of a good number 

of male and female individuals of this bird collected from different parts of its distribution 

range in Iraq. It seems necessary also to investigate about another species of parasites 

infecting this game bird from the human health viewpoint since large numbers of the bird are 

eaten every year by humans.  

 

    The nematode H. gallinarum infects chicken and other birds (Baker, 1973). To complete its 

life cycle, it requires termites (Kaufmann, 1996). Babaeian and Zangiband (2014) found that 

this nematode needs the termite Anacanthotermes ubachi for its development. A. ubachi 

(found in Ga'ara Depression) and two other Anacanthotermes species: A. vagans and A. 

sawensis were previously recorded in Iraq by Al-Alawy (1987).  

 

 

 

 

 

 

 
 

Plate (1): Anterior end of male of Hartertia gallinarum. 

 

 



 

 

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Mohammad K. Mohammad and Azhar A. Al-Moussawi 
 

 
 

Plate (2): Head of male of H. gallinarum (lateral view) 

 

 

 

 
 

Plate (3): Tail of male of H. gallinarum 

 

 

 



 

 

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The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host 

 
 

Plate (4): Anterior end of female of H. gallinarum 

 

 

 
 

Plate (5): Posterior end of female of H. gallinarum 

 
 



 

 

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Mohammad K. Mohammad and Azhar A. Al-Moussawi 
 

LITERATURE CITED 
Al-Alawy, S.A. 1987. Taxonomical and ecological studies on termites “Insecta, Isoptera” in 

Iraq. Ph. D. Thesis, Department of Plant Protection, College of Agriculture, 

University of Baghdad, 223pp. 

 

Al-Hubaity, I.A. 1976. Studies on the parasites of fowl Gallus gallus domesticus in Mousl 

district, Iraq. Mesopotamia Journal of Agriculture, 14(1): 197-204.  

 

Babaeian, A. and Zangiband, P. 2014. A study of gastrointestinal helminth parasites of wild 

red-legged partridges (Alectoris rufa) from Kurdistan province, Iran. 8
th
 

International congress of Clinical Microbiology, Tabriz-Iran 30 Sep - 2 Oct 2014. 

 

Baker, D.G. 1973. Flynn’s Parasites of Laboratory Animals. Blackwell Publishing 

Publications, Oxford, 813pp. 

 

Bird Life International, 2016. Pterocles senegallus. The IUCN Red List of Threatened 

Species 2016:e.T22692994A93377532.  

                   http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22692994A93377532.en. 

(Accessed 12 March 2017). 

 

Bolster, R.C. 1922. The occurrence, habits and breeding of the spotted sandgrouse 

(Pteroclurus senegallus) in the Bahawalpur State, Punjab. The journal of the 

Bombay Natural History Society, 28: 807-809. 

 

Campbell, B. and Lack, E. (Eds.) 1985. A Dictionary of Birds. Buteo Books. Published for 

the British Ornithologists's Union. 1
st
 ed., T. and A. D. Poyser, Ltd., Carlton, 

UK,700pp. ISBN 0-931130-12-3. 

 

Cram, E.B. 1927. Bird parasites of the nematode suborders Strongylata, Ascaridata and 

Spirurata. Bulletin of the United States National Museum, 140: 464pp. 

 

EOL. 2017. Encyclopedia of Life on-line database, http//www.eol.org. (Accessed 18 April 

2017). 

 

Fauna Europaea 2017. Accessed via http://www.gbif.org/species/123246499 on 2017-04-18. 

DOI: 10.15468/ymk1bx. 

 

GBIF. 2017. Accessed via http://www.gbif.org/species/4557376 on 2017-04-18. DOI: 

10.15468/39omei. 

 

Hildebrand, J., Adamczyk, M., Laskowski, Z. and Zaleśny, G. 2015. Host-dependent 

morphology of Isthmiophora melis (Schrank, 1788) Lühe, 1909 (Digenea, 

Echinostomatinae): Morphological variation vs. molecular stability. Parasite and 

Vectors, 8: 481.  

 

Kaufmann, J. 1996. Parasitic Infections of Domestic Animals: A Diagnostic Manual. Springer 

Basel, xvi + 423pp.  

 



 

 

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The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host 

Khoshnaw, Z.O.I. and Abdullah, S.M.A. 2013. Study on the parasites of chukar partridge 

Alectoris chukar from Shaqlawa district, Kurdistan region, Iraq. Tikrit Journal of 

Pure Science, 18(3): 26-30.          

 

Mahmoud, S.S., Mohammad, M.K. and Ali, S.Y. 2000. Intensity and histopathological effects 

of the nematode Hartertia gallinarum (Theiler, 1919) on seesee partridge, 

Ammoperdix griseogularis (Brandt, 1843) collected from Qaara area, west of Iraq. 

Bulletin of the Iraq Natural History Museum, 9(2): 45-55.   

 

Mehlhorn, H. 2016. Animal Parasites: Diagnosis, Treatment, Prevention. Springer 

International Publishing, XVII, 719pp. 

 

Mohammad, M.K. 1996. Intestinal helminth parasites of the rock partridge Alectoris graeca 

in G'ara area, west of Iraq. Bulletin of the Iraq Natural History Museum, 8(4): 89-

101.                      

 

Salim, M.A., Porter, R.F., Christensen, S., Schiermacker-Hansen, P. and Al-Jbour, S. 2006. 

Field Guide to the Birds of Iraq. Nature Iraq and Bird Life International, Amman, 

284 pp.  (In Arabic). 

 

Yamaguti, S. 1961. Systema Helminthum. Vol. 3. The Nematodes of Vertebrates, Part I + II. 

Interscience Publisher, Inc., New York, 1261pp. 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 



 

 

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Bull. Iraq nat. Hist. Mus. 

(2017) 14 (3): 205-213 

 

كمّضيف جديد للدودة    Pterocles senegallus (Linnaeus, 1771) القطا المرقط

 Hartertia gallinarum (Theiler, 1919)الخيطية    

 في وسط العراق

 

 هللا محمد كاظم محمد و ازهار احمد سعد

 جامعة بغداد، بغداد، العراقي، ركز بحوث و متحف التأريخ الطبيعم

 
 610312162: تأريخ القبول                                                                   610317102: تأريخ االستالم

 

 الخالصة

من أمعاء القطا  Hartertia gallinarum هذا البحث معني بظهور الدودة الخيطية     

الذي جمع من منخفض القعرة في غرب العراق ومن  Pterocles senegallusالمرقط 

كما ألقي  أعطي وصف وقياسات تلك الدودة الخيطية،. زرباطية والعطارية في وسط العراق

في إصابة القطا المرقط  Anacanthotermes ubachiالضوء على دور النمل األبيض 

بموجب الدراسة الحالية يعتبر القطا المرقط مضيّفا جديدا لهذه الدودة . الدودة الخيطيةتلك ب

 .الخيطية في العراق