Otiditaenia macqueeni, Raillietina sp., Paronchocerca tonkinensis and Allodapa sp. were recovered from a group of rufous-crested bustards (Eupodotis ruficrista) which died after importation into the United Arab Emirates.  Associated findings at post-mortem examination included cardiac rupture, weight loss, trichomoniasis and enteritis.  Histologic examinations revealed Paronchocerca sp. microfilariae in sections of liver, kidney, lung and myocardium.  Haemoproteus telfordi and H. tenderoi were identified in blood smears from two of the birds.  These parasites may be a contributary factor in the high mortality of rufous-crested bustards in captivity

Bailey, T.A.

Gibbons, L.M.

Jones, A.

Nicholls, P.K.

Samour, J.H.

English

Research Repository

Journal of Zoo and Wildlife Medicine 26(4): 590-596, 1995 Copyright 1995 by American Association of Zoo Veterinarians PARASITIC INFECTION IN A FLOCK OF RUFOUS-CRESTED BUSTARDS (EUPODOTIS RUFICRISTA) IN THE UNITED ARAB EMIRATES Philip K. Nicholls, B.Sc., B.V.Sc., Thomas A. Bailey, B.Sc., B.V.Sc., Lynda M. Gibbons, B.Sc., Ph.D., Arlene Jones, B.Sc., Ph.D., and Jaime H. Samour, M.V.Z., Ph.D. Abstract: Otiditaenia macqueeni, Raillietina sp., Paronchocerca tonkinensis, and Allodapa sp. were recovered from a group of rufous-crested bustards {Eupoditis ruficrista) which died after importation into the United Arab Emirates. Associated findings at postmortem examination in cluded cardiac rupture, weight loss, trichomoniasis, and enteritis. Histologie examinations revealed Paronchocerca sp. microfilariae in sections of liver, kidney, lung, and myocardium. Haemoproteus telfordi and H. tenderoi were identified in blood smears from two birds. These parasites may be a contributing factor in the high mortality of rufous-crested bustards in captivity. Key words: Otiditaenia sp., Raillietina sp., Paronchocerca sp., Allodapa sp., Haemoproteus sp., rufous-crested bustard, Eupodotis ruficrista. INTRODUCTION The rufous-crested bustard {Eupodotis ruficrista) is a member of the Otitidae fam ily occurring in three separate regions in Af rica. In west Africa it occurs from Senegal and Mauritania to Sudan, in east Africa it occurs from South Ethiopia and Somalia southward to Tanzania, and in southern Af rica it is found south of a line from south Angola to south Mozambique.11 Rufous crested bustards inhabit semiarid lands with some cover.8 The southern and eastern races are common, but the west African race is rarer and little-known.811 Published cases of morbidity and mor tality in bustards are scarce,5 and, to our knowledge, the clinical and pathologic as pects of parasitic infestations in rufous crested bustards have not been described previously. The rufous-crested bustards de scribed in this article were examined by staff of the National Avian Research Centre, United Arab Emirates (UAE), a scientific and conservation organization primarily concerned with conservation of the houbara bustard {Chlamydotis undulata macqueeni) but also involved in a captive breeding pro gram for rufous-crested bustards at Al Ain Zoo, UAE. Investigations into the causes of disease in rufous-crested bustards should contribute to the success of captive breeding programs. CASE REPORTS In April 1993, 10 rufous-crested bustards were imported from Somalia by a private individual into the UAE. The birds were transported in two woven-reed shopping baskets, and, although no further history was available, it was suspected that the birds had been transported by air. Two birds (Nos. 1 and 2) were dead on arrival at the quaran tine facility at Al Ain Zoo, a third bird (No. 3) died in the afternoon of the same day, and a fourth bird (No. 4) died the following day. A fifth bird (No. 5) died 2 days after From the Animal Pathology Division, Department of Clinical Veterinary Medicine, University of Cam bridge, Cambridge, CB3 OES, England, United King dom (Nicholls); the Veterinary Science Department, National Avian Research Centre, Box 45553, Abu Dhabi, United Arab Emirates (Bailey, Samour); and the International Institute of Parasitology, 395A Hat field Road, St. Albans, Hertfordshire, AL4 OXU, En gland, United Kingdom (Gibbons, Jones). Send correspondence to P. K. Nicholls, BSc, BVSc, MRCVS, Dip. RCPath, Animal Pathology Division, Department of Clinical Veterinary Medicine, Univer sity of Cambridge, Madingley Road, Cambridge CB3 OES, United Kingdom. 590 NICHOLLS ET AL.-PARASITES OF RUFOUS-CRESTED BUSTARDS 591 arrival, and the remaining five birds were reported to be healthy 1 mo later. At the request of the importer, all dead birds were submitted to us for postmortem examina tion to investigate the possible causes of mortality. Clinical findings and treatments On arrival at Al Ain Zoo the seven sur viving birds were given full clinical exam inations. All birds were in poor or emaci ated condition as judged by palpation of pectoral muscles. The range in body weights was 413-517 g (mean = 504 ? 56 g). Four birds had yellow caseous necrotic plaques in the oral cavity; wet mounts examined microscopically revealed numerous flagel lated protozoa typical of Trichomonas sp. One bird was treated for a fractured lateral digit of the left foot and also had a broken toenail on the middle digit of the right foot. No other abnormalities were detected. As part of a routine preventive medicine program, all birds were treated with 200 p%l kg i.m. ivermectin (Ivomec, Merck, Sharp and Dohme, Hoddesdon, Hertfordshire, EN11 9BU, United Kingdom) 25 mg/kg p.o. mebendazole (Vermox, Janssen Pharma ceuticals, Grove, Wantage, Oxfordshire, OX 12 ODQ, United Kingdom), and 0.2 ml i.m. of a multivitamin preparation (Multi vet, C-Vet, Bury St. Edmunds, Suffolk, IP33 3SU, United Kingdom). All birds with trichomoniasis received 50 mg/kg p.o. met ronidazole benzoate (Flagyl-S, May and Ba ker, Dagenham, Essex, RM 10 7XS, United Kingdom). As a routine prophylactic mea sure, the drinking water for all birds was medicated with dimetridazole (Emtryl 40%, Rhone Merieux, Harlow, Essex, CM 19 5TS, United Kingdom) at a dose of 0.9 g/L of water for 5 days, followed by 0.7 g/L of water for 10 days. Postmortem examination findings The two female (Nos. 1,2) and three male (Nos. 3, 4, 5) birds which died were ex amined postmortem using standard tech niques.10 The weight range of the dead birds was 365-513 g (mean = 447 ? 60 g), and all were in poor or emaciated nutritional condition as judged by pectoral muscle ex amination. One bird (No. 1) had marked hemopericardium secondary to rupture of the right ventricular myocardium. In the right ventricle and pulmonary arteries of three birds (Nos. 1, 3, 4), there were large numbers of nematodes, 3-4 cm in length. Additional nematodes were present in the vena cava and testicular blood vessels of one bird (No. 3). Cestodes were present in the ileum and jejunum of two birds (Nos. 1, 3), and nematodes were recovered from the cecum of these birds. Focal raised, pale lesions typical of trichomoniasis were seen in the oropharynx of birds Nos. 3 and 4. Thickened jejunal mucosa, in the absence of helminths, was seen in one bird (No. 5) which had been given anthelmintic treat ment 2 days previously. Histologie examinations Microscopic examinations of tissue from the three birds in which Paronchocerca sp. were found revealed numerous microfilar iae in the arteries and small blood vessels of the lung. There was mild thickening of some of the smaller arterial walls and a prominent accumulation of eosinophils throughout the lung tissue, and occasional foci of mixed inflammation, including nu merous eosinophils and macrophages, were present in some sections of lung. There were no signs of thrombosis in the pulmonary vessels. Some macrophages filled with crys talline debris surrounded the larger airways, and this probably represented phagocytosed airborne debris such as small sand particles. Histologie examination of hearts revealed microfilariae in large numbers throughout the microvasculature of the myocardium (Fig. 1). Although there was no obvious tis sue reaction to the microfilariae in two of the birds, the bird with a cardiac rupture showed focal areas of prominent myocar 592 JOURNAL OF ZOO AND WILDLIFE MEDICINE ?y#Ff zmm&& '' ;-:.^3 Figure 1. Myocardium with several Paronchocerca tonkinensis microfilariae (arrow). No host tissue reaction is apparent in this field. H&E, x 400. dial degeneration and fibrosis in the right ventricular free wall. Microfilariae were seen in the microvasculature of the liver (Fig. 2) and kidney in these three birds, although no tissue reaction or other lesions were seen. The tissues from the two other birds showed no signs of microfilariae. Sections from dif ferent levels of the intestinal tract in all birds showed variable amounts of mononuclear mucosal inflammation, varying from in apparent to moderate in degree, with oc casional foci of lymphoid proliferation. Parasitologic identifications Whole parasites were preserved in 10% buffered formalin and submitted to the In ternational Institute of Parasitology, St. Al bans, Hertfordshire, England, United King dom, for identification. Specimens from il eum and jejunum were identified as very early to gravid Otiditaenia macqueeni (Bloch, 1782) and immature specimens of Raillietina sp., probably R. neyrai (Baer, 1955), both from the family Davaineidae. The parasites found in the heart and vas cular system were identified as Paroncho cerca tonkinensis (Filaroidea: Onchocerci dae) (Chow, 1939). There were minor dif ferences in measurements and in the ar rangement of one small pair of papillae on the male tail compared to the original de scription by Chow. The bustard is unlikely to be the natural host for this parasite, which may account for these minor differences. These differences are insufficient to estab lish a new species, and further studies are required to establish the full host and geo graphic range of the parasite. The specimens recovered from the cecum were identified as Allodapa sp. (Subuluroidea: Subuluri dae). Further identification was impossible since all the available specimens were from females. NICHOLLS ET AL.-PARASITES OF RUFOUS-CRESTED BUSTARDS 593 Figure 2. Liver with a microfilarial Paronchocerca tonkinensis (arrow) and no apparent host tissue reaction. H&E, x400. H?matologie findings Blood samples were collected as de scribed by Hawkey and Samour7 from bird Nos. 3 and 5 shortly before they died and from the five surviving birds 10 days after arrival. Differential white blood cell counts gave the following mean percentage com positions: neutrophils, 69 (?5.9); lympho cytes, 18 (?4.0); monocytes, 8 (?1.7); eo sinophils, 2.5 (?2.4); and basophils, 2.8 (?1.9). Total white blood cell counts were not evaluated, although the blood films sug gested a high value. The mean thrombocyte count was 68 (?54) thrombocytes per 100 white blood cells. The red cell picture was one of mild to moderate anisocytosis, mild polychromasia, and mild poikilocytosis. Haemoproteus spp. were seen in two birds (No. 5 and one of the surviving birds, No. 6) and identified as H. telfordi and H. ten der oi. Sections of lung, liver, heart, and kid ney from bird No. 5 were extensively ex amined under xlOO oil immersion, but no evidence of hemoproteid schizonts was found. This suggested that either the schiz onts for this species have a predilection for skeletal muscle or were simply not present in the samples of tissue available. Serology results Serum samples from four of the surviving birds were submitted to the Dubai Veteri nary Research Laboratory for Newcastle disease hemagglutination inhibition testing. One sample gave a titre of 1:4, and the other three were negative. DISCUSSION Rupture of the aorta or atrium is a well known condition in fast-growing domestic species such as the turkey.9 Its exact etiology is unknown, although systemic hyperten 594 JOURNAL OF ZOO AND WILDLIFE MEDICINE I'/.: 's:* ' M ' '""" J. *?m m Figure 3. Pulmonary artery with lumen occupied by an adult Paronchocerca tonkinensis. H&E, x 100. sion, dietary protein, fat, and copper im balances are possible causes.1213 Nonper forating rupture of the heart apex with he mopericardium has been recorded in three capercaillie {Terao urogallus) reared in cap tivity.3 Capercaillie show high levels of anx iety and excitability in response to stimuli such as handling. Tachycardia, violent myocardial contraction, local ischaemia, or capture myopathy may have been under lying factors in the cardiac rupture.3 The cause of myocardial rupture and hemoperi cardium in the rufous-crested bustard de scribed here is unknown, although it seems likely that the stress of capture, handling, and poor transportation conditions may have caused systemic hypertension. Addi tionally the presence of large numbers of adult Paronchocerca sp. in the pulmonary arteries (Fig. 3) may have caused a degree of right ventricular heart failure, and the numerous microfilariae seen in the ventric ular wall may have affected the perfusion of the myocardium. Whether the presence of microfilariae caused the focus of myocardial degeneration seen in the ruptured heart is not clear, although myocardial degeneration associated with microfilariae has been re ported in other species.4 The presence of microfilariae in the living bird can be dem onstrated by microscopic examination of a peripheral blood smear using routine stains, and this might be a useful technique for screening groups of birds for infection and subsequent treatment. Heartworm was recorded in the frozen carcass of a rufous-crested bustard exam ined postmortem at Al Ain Zoo in 1993 (Nicholls and Bailey, unpubl. obs.). In this bird the origin and clinical history were not available, but it may have been a member of the captive breeding population at Al Ain Zoo that had originated from the wild some years earlier. Furley5 examined large num NICHOLLS ET AL.-PARASITES OF RUFOUS-CRESTED BUSTARDS 595 bers of bustards imported into Al Ain Zoo in the early 1980s and reported finding 3-cm long nematodes in the ventricle of a newly imported white-bellied bustard {Eupodotis senegalensis), but no identification of the parasite was undertaken. The genus Paron chocerca has been reviewed by Bartlett and Anderson,1 and P. tonkinensis has been de scribed in Ardeola bacchus, ?rdea cin?rea, Botaurus stellaris, Egretta garzetta, Gorsa chius melanolophus thomasi, and Ardea herodias.6 The mode of transmission of Pa ronchocerca sp. is poorly understood, al though lice have been identified as inter mediate hosts of heartworms in swans.215 Although lice have been found on recently imported bustards, none were seen on the bustards described in this report. The pres ence of adult heartworms in the right ven tricle and pulmonary artery has been as sociated with thickening of the pulmonary arteries, pulmonary arterial thrombosis, and myocardial degeneration.4 The large num bers of heartworm found in some bustards suggest a pathogenic role in these individ uals, and Seegar14 found that parasitism of whistling swans {Cygnus columbianus col umbianus) by heartworm was associated with significant weight loss, indicating that preventive treatment with levamisole could have a useful management role in bustard husbandry. The mean body weight for captive rufous crested bustards is 600 g for females (range, 470-760 g) and 670 g for males (range, 600 770 g) (Bailey, unpubl. data). The body weights of all the bustards described in this study were below average (mean male weight, 461 g; mean female weight, 422 g), and one female (No. 1) was more than 30% below the average weight for captive birds. Transportation conditions of bustards im ported into the UAE are often inadequate, and little consideration is given to the ad equate provision of food or water during transit (Bailey, unpubl. obs.). The mortality of bustards imported into the UAE is high. A survey of mortality in houbara bustards (imported from Pakistan to Al Ain Zoo during an 11 -wk period from February 1993 to April 1993 (J. Naldo, un publ. data) revealed that 21 of 123 birds died, an overall mortality of 17%. These findings have important implications for the husbandry of bustards in captive breeding programs. Acknowledgments: We thank our colleagues in the National Avian Research Centre (NARC), in particular H. H. Sheik Khalifa bin Zayed Al Nahyan, H. H. Sheikh Mohammed bin Zayed Al Nahyan, and Mr. M. al Bowardi, the man aging director, for their personal interest and sup port of this work. We also thank Dr. Ullie Wer nery from Dubai Veterinary Research Labora tory for the s?rologie studies; Mike Hart from J. S. Pathology, United Kingdom, for reading the blood films; Dr. M. A. Pierce for identifying the blood parasites; and Dr. M. Nael and Mr. P. Divakiran from the Al Ain Zoo for their assis tance during this study. Emma Newstead pre pared the histologie sections, and Dr. R. Hornby reviewed the manuscript. LITERATURE CITED 1. Bartlett, C. M., and R. C. Anderson. 1986. Pa ronchocerca struthionus n. sp. (Nematoda: Filaroidea) from ostriches {Struthio camelus), with a redescription of Paronchocerca ciconarum Peters, 1936 and a review of the genus. Can. J. Zool. 64: 2480-2491. 2. Cohen, S., M. T. Greenwood, and J. A. Fowler. 1991. The louse Trinotron anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eu rycera (Filaroidea: Nematoda), a heartworm of swans. Med. Vet. Entomol. 5: 101-110. 3. Domingo, M., I. Marco-Sanchez, A. J. Marco Valle, and M. Pumarola. 1991. Heart rupture and haemopericardium in capercaille {Tetrao urogallus) reared in captivity. Avian Pathol. 20: 363-366. 4. Ensley, P. K. 1978. Levamisole hydrochloride for treatment of Paronchocerca ciconarum microfilar iae in a marabou stork. J. Am. Vet. Med. Assoc. 173: 1246-1248. 5. Furley, C. 1980. Veterinary Problems in Bus tards. National Avian Research Centre, Abu Dhabi, United Arab Emirates. 6. Gr?ve, J. H., and D. L. Graham. 1980. Heart worm {Chinesocerca tonkinensis) in a wild great blue heron {Ardea herodias) in Iowa. Proc. Helminthol. Soc. Washington 47: 269. 7. Hawkey, C, and J.H.Samour. 1988. The value of clinical hematology in exotic birds. In: Jacobson, E. R., and G. V. Kollias, (eds.). Contemporary Issues in 596 JOURNAL OF ZOO AND WILDLIFE MEDICINE Small Animal Practice, vol. 9. Churchill Livingstone, New York, New York. Pp. 110-111. 8. Johnsgard, P. A. (ed.). 1991. Bustards, Hemi pods and Sandgrouse?Birds of Dry Places. Oxford Univ. Press, Oxford, England, United Kingdom. P. 189. 9. Julian, R. J. 1990. Cardiovascular disease. In: Jordan, F. T. W. (ed.). Poultry Diseases. Bailliere Tin dall, London, England, United Kingdom. P. 338. 10. Nicholls, P. K., T. A. Bailey, J. H. Samour, J. Naldo, J. Howlett, and M. D'Aloia 1993. Guidelines for the Post-mortem Examination of Bustards. Na tional Avian Research Centre, Abu Dhabi, United Arab Emirates. 11. Osborne, P., N. Collar, and P. Goriup. 1984. Bustards. Dubai Wildlife Research Center, Dubai, United Arab Emirates. 12. Pritchard, W. R., W. Henderson, and C. W. Beall. 1958. Experimental production of dissecting aneu rysms in turkeys. Am. J. Vet. Res. 19: 696-705. 13. Riddell, C. 1991. Developmental metabolic and miscellaneous disorders. In: Calnek, B. W. (ed.). Poultry Diseases, 9th ed. Iowa State Univ. Press, Ames, Iowa. Pp. 827-862. 14. Seegar, W. S. 1979. Prevalence of parasitic heartworms in swans in England. Wildfowl 30: 147 150. 15. Seegar, W. S., E. L. Schiller, W. J. L. Slader, and M. Trapis. 1976. A mallophaga, Trinoton anserinum, as a cyclodevelopmental vector for a heartworm par asite of waterfowl. Science 194: 739-740. Received for publication 23 March 1995. 

A mallophaga, Trinoton anserinum, as a cyclodevelopmental vector for a heartworm par asite of waterfowl. Science 194: 739-740. Received for publication 23

Bustards, Hemi pods and Sandgrouse?Birds of Dry Places.

Cardiovascular disease.

Developmental metabolic and miscellaneous disorders.

Experimental production of dissecting aneu rysms in turkeys.

Guidelines for the Post-mortem Examination of Bustards. Na tional Avian Research Centre, Abu Dhabi, United Arab Emirates.

Heart rupture and haemopericardium in capercaille {Tetrao urogallus) reared in captivity.

Heart worm {Chinesocerca tonkinensis) in a wild great blue heron {Ardea herodias) in Iowa.

Levamisole hydrochloride for treatment of Paronchocerca ciconarum microfilar iae in a marabou stork.

Pa ronchocerca struthionus n. sp. (Nematoda: Filaroidea) from ostriches {Struthio camelus), with a redescription of Paronchocerca ciconarum Peters,

Prevalence of parasitic heartworms in swans in England.

The louse Trinotron anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eu rycera (Filaroidea: Nematoda), a heartworm of swans.

The value of clinical hematology in exotic birds.

Veterinary Problems in Bus tards. National Avian Research Centre, Abu Dhabi, United Arab Emirates.

Parasitic infection in a flock of Rufous-crested Bustards (Eupodotis ruficrista) in the United Arab Emirates

http://researchrepository.murdoch.edu.au/3369/

Parasitic infection in a flock of Rufous-crested Bustards (Eupodotis ruficrista) in the United Arab Emirates

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