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Parasitic infections of Indian yak Bos (poephagus) grunniens—an overview
veterinary parasitology ELSEVIER
Veterinary Parasitology 53 (1994) 75-82
Parasitic infections of Indian yak Bos (poephagus) grunniens an overview G.S.C. RangaRao, R.L. Sharma*, Hemaprasanth Indian VeterinaryResearch Institute, Campus, Mukteswar-263 138, Nainital, India (Accepted 25 August 1993)
Abstract
For centuries, the yak and its hybrids with domestic cows (dzomo/dzo) have been contributing to the socio-economic status of their owners in desolate regions of the Greater Himalayas. Studies on the prevalence of parasitic diseases in these animals were undertaken in Ladakh (Jammu and Kashmir), Sikkim and villages near the Indo-Nepal border of Uttar Pradesh. Visceral organs of necropsied animals were observed for the presence of adult metazoan parasites, fresh or preserved faecal samples were examined for the eggs of helminth parasites and protozoan cysts, and blood smears were examined for haemo-protozoa and microfilariae. In all, examination of 225 faecal samples, 180 blood smears and the visceral organs of thirteen yaks and dzomo/dzo was undertaken. On necropsy, visceral organs revealed various adult liver and stomach flukes, gastrointestinal nematodes, tapeworms, cysts of Coenurus spp. and hydatid cysts, as well as Setaria cervi worms and large a n d / o r small sized Sarcocystis cysts. On coprological examination, egg prevalences of 10% for Fasciola spp., 6.6% for various amphistomes, 10% for Moniezia spp., 76.4% for Strongylate spp., 24% for Neoascaris spp. and 13.7% for Nematodirus spp. were recorded. Identification of infective larvae from the faecal cultures showed that a majority of eggs (86.3%) in the host faeces were contributed by nematodes belonging to Trichostrongyle spp., Ostertagia spp. and Cooperia spp. This was followed by Chabertia spp. (6.5%). Haemonchus spp., Bunostomum spp. and Nematodirus spp. together contributed only 7.2% of the eggs found. Among protozoan infections, Eimeria brasiliensis and E. zurnii were common. None of the blood smears evidenced any haemoprotozoa or microfilariae. Likewise, none of the animals were positive for Trichuris spp. All animals were positive for one or more species of parasites. An immediate need to undertake systematic studies on the health problems of yak is stressed in order to save this species from extinction.
Key words:Yak parasites *Corresponding author. 0304-4017/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0304-401 7 ( 9 3 ) 0 0 5 9 0 - U
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G.S. C. RangaRao et al. / Veterinary Parasitology 53 (1994) 75-82
1. Introduction
Grunting Ox, the popular name for the yak Bos (poephagus) grunniens, is a native of the Tibetan plateau and surrounding central Asian countries. This bovine species thrives well on grasslands at high altitudes (4300-6100 m) in the Greater Himalayas, with cold to extreme cold climate, where other domestic animals either fail to survive or do not maintain their optimum productivity. In India, yaks are found in Ladalda valley (Jammu and Kashmir), Pangi, Sangla, Lalaoul and Spiti valley (Himachal Pradesh), Uttrakhand (Uttar Pradesh) and in small numbers in Sikkim and Arunachal Pradesh. They migrate to high altitudes during the summer and back to lower altitudes, along the snow-line, during winter. Although the yak has contributed significantly towards improving the socio-economic status of its owners in these desolate regions, its development and health status have been neglected. Practically no efforts have been made to study the various diseases threatening its survival and productivity. Except for sporadic reports on the occurrence of a few parasites (Fasciola spp., Amphistomes, Trichostrongyle spp., Cooperia spp., Thelazia spp., Moniezia spp., hydatid and cysts caused by Coenurus spp. as well as warble flies) from the USSR, Mongolia, China, Tibet, Bhutan and Nepal (Southwell, 1930; Ivashkin, 1953; Rezvikh, 1958; Mukhamadiev, 1968, 1971, 1975, 1981; Biryukov, 1970; Chaudhary, 1970; Joshi and Tiwari, 1975; Joshi and Pradhan, 1977; Roy et al., 1986; Katiyar and Sinha, 1987 ), no systematic studies on the prevalence and/or impact of the parasites of yak have been undertaken. Hence, the scope of this paper is to review the available information and to incorporate the authors' current observations on parasitic diseases of yak in India.
2. Materials and methods
The prevalence studies on the parasitic diseases of yak were undertaken in Ladakh (Jammu and Kashmir), Sikkim and villages in the Indo-Nepal border of Uttar Pradesh. Animals were screened for various parasites, by a detailed examination of preserved necropsy materials for adult parasites and fresh or preserved rectal faecal samples and blood smears for eggs of helminth parasites and protozoan cysts and haemoprotozoans, respectively. The experimental materials were either collected personally and/or by field veterinarians working in these far-flung areas, and were then forwarded to the laboratory. In all, 225 faecal samples, 180 blood smears and visceral organs from 13 yak and dzomo/dzo, female and male hybrid, respectively, of a male yak with a hill cow were received for the purpose. Standard parasitological techniques for faecal examinations for parasite eggs and oocysts (Whitlock, 1948 ), faecal culture for identification of nematode larvae (Anantaraman, 1942), recovery of parasites from necropsy materials, their preservation and counting (Dhar et al., 1982 ), staining and microscopic exami-
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nation of blood smears for haemoprotozoans and preparation of faecal cultures for development and identification of coccidial oocysts (Georgi, 1990 ) were used during the course of the investigation.
3. Results
3.1. Necropsy of visceral organs Detailed examination of necropsy materials from yak and dzomo/dzo, which were either slaughtered for meat or died due to accidents or natural causes, revealed the presence of liver and stomach flukes, gastro-intestinal nematodes, adult tapeworms, cysts of Coenurus spp. and hydatid cysts, and five adult female Setaria cervi from the peritoneum. Large and small size cysts of Sarcocystis were observed in the abdominal muscles. All the animals examined were positive for one or more species of parasites. The flukes recorded from the liver and gall bladder were identified as Fasciola hepatica, F. gigantica and Gigantocotyle explanatum, and amphistomes recovered from the stomach were identified as Cotylophoron cotylophorum, Gastrothylax crumenifer, Fischoederius cobboldi and Paramphistomum cervi. The majority of hydatid cysts recovered from livers were fertile, whereas those from the lungs were infertile. The adult gastro-intestinal nematode species observed were Trichostrongylus, Ostertagia, Cooperia, Nematodirus, Bunostomum, Chabertia, Haemonchus, Mecistocirrus and Neoascaris. The adult tape worms recovered from intestines were identified as Moniezia spp. An up-dated checklist of parasitic fauna of the yak is given in Table 1.
3.2. Coprologicalexamination Microscopic examination of 225 faecal samples, which were received/collected from various villages in the study area, showed the presence of amphistomes, Fasciola spp., Trichostrongylus spp., Ascaris spp., Nematodirus spp. and Moniezia spp. eggs as well as coccidial oocysts. The d z o m o / d z o and male yaks were more susceptible to these infections than female yaks. Interestingly, none of the animals screened were positive for Trichuris spp. eggs. No microfilariae could be detected in detailed microscopic examination of stained blood smears. The prevalence of Fasciola spp. and amphistome infections as revealed from egg counts was 10% and 6.6%, with average number of eggs per gram (EPG) of faeces of 13.3 (0-300) and 30 (0-400), respectively. The prevalence of Moniezia spp. infection was 10%, with an average EPG of 80 (0-1000) eggs. Coprological examination also revealed a high prevalence of Strongylate spp. (76.4%), including Nematodirus spp. (13.7%), followed by Ascaris spp. (24%), with an overall prevalence rate of 91.1% for gastro-intestinal nematode infections (Table 2). These eggs in fresh faeces were cultured to infective-stage larvae. Morphological examination of these larvae showed that the majority of eggs in the faeces
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Table 1 Updated checklist of the parasites of the yak Parasite
References
1. Protozoan parasites
1.1. Eimeria brasiliensis 1.2. Eimeria zurnii 1.3. Cysts of sarcocystis 2. Helminth parasites 2.1. Nematodes 2.1.1. Eye worms
Thelazia gulosa Thelazia lacrymalis 2.1.2. Gastro-intestinal worms
Cooperia hrenktahnsa Neoascaris vitulorum Haemonchus contortus Mecistocirrus digitatus spp. Trichostrongylus spp. Ostertagia spp. Chabertia spp. Nematodirus spp. Bunostornum spp. 2.1.3. Parasites of the peritoneum
RangaRao, 1974
Ivashkin, 1953 Jiang et al., 1987 Mukhamadiev, 1975 Wu, 1965; RangaRao, 1974; Mukhamadiev, 1981 Roy et al., 1986 Jiang et al., 1987
Mukhamadiev, 1968; RangaRao, 1974
Setaria cervi 2.2. Trematodes 2.2.1. Liver flukes
Fasciola hepatica Fasciola gigantica Gigantocotyle explanatum 2.2.2. Stomach flukes
RangaRao, 1974 Joshi and Tiwari, 1975; Mukhamadiev, 1981 RangaRao, 1974
Cotylophoron cotylophorurn Gastrothylax curmenifer Fischoederius cobboldi Paramphistornum cervi 2.3. Cestodes
Moniezia spp. Cysts of cysticercus Cysts of coenurus Hydatid cysts
3. Arthropod parasites Hypoderma lineatum (warble flies)
Southwell, 1930; RangaRao, 1974; Linyuguang et al., 1983; Mukhamadiev, 1981 Rezvikh, 1958 Biryukov, 1970 RangaRao, 1974; Katiyar and Sinha, 1987; Chen et al., 1982; Li et al., 1985 Breev and Baratov, 1970; Chaudhary, 1970
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G.S.C. RangaRao et aL / Veterinary Parasitology 53 (1994) 75-82 Table 2 Prevalence of nematode parasites in the yak (coprological examination) Location
Ladakh Sikkim Uttar Pradesh
No. of animals
Results of faecal examination, No. (%)
Ascaris spp.
Strongylate spp.
Nematodirus spp.
Overall prevalence, No. (%)
187 27 11
44 (23.5) 6 (22.2) 3 (27.4)
143 (76.5) 21 (77.8) 8 (72.7)
25 (13.4) 4 (14.8) 2 (18.0)
170 (91.0) 25 (92.9) 10 (90.9)
225
53 (24.0)
172 (76.4)
31 (13.7)
205 (91.1)
Table 3 Prevalence of infective larvae of gastro-intestinal parasites in faecal cultures Parasite
Trichostrongylus spp. Ostertagia spp. Cooperia spp. Chabertia spp. Haemonchus spp. Bunostomum spp. Nematodirus spp.
No. of cultures
10 10 10 10 10 10 10
Mean prevalence %
Range
62.7 14.7 8.9 6.5 3.9 2.4 0.9
55-71 9-20 7-11 4-9 2-6 1-3 0-2
of hosts were Trichostrongylus spp. (62.7%) and Ostertagia spp. (14.7%), followed by Cooperia spp. (8.9%) and Chabertia spp. (6.5%). The Haemonchus spp., Bunostomum spp. and Nematodirus spp. together accounted for 7.2% (Table 3 ). Extreme care was taken and all possible efforts were made to culture coccidial oocysts, which were preserved and despatched to this laboratory in two percent potassium dichromate solution. Even then, these oocysts failed to develop and sprulate. However, the oocysts were identified on the basis of size, shape and presence/absence of polar caps etc., and were assigned to Eimeria brasiliensis and E. zurnii. Detailed microscopic examination of stained blood smears did not reveal the presence of any haemoprotozoan infection in yaks.
4. Discussion The role of the yak in improving the socio-economic status of owners in desolate regions in the Greater Himalayas is well recognised and documented. The yak is a source of milk and meat and is also used as a pack animal. A mating of male yak with domestic cow is quite common. A dzomo (chaori) calf is fertile and is a higher milk yielder than female yaks. In contrast, a dzo (choru) calf is
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infertile and is used for cultivation, riding, as a pack animal and as meat for human consumption. Yak hair is used by itself or blended with other animal fibres: for making ropes or weaving bags and blankets. The white tail tuft of the yak is a valuable item and is sold at a high price for ceremonial purposes in temples. Above all, yak dung is used as fuel in the treeless plateaus and as fertilizer. In the snowbound mountainous areas, the army has been using yaks as a pack animal for transportation of rations, war equipment and ammunition, etc. Until 1923, the parasite fauna of the yak remained completely unexplored. Southwell (1930) published a pioneering report on the occurrence of Moniezia spp. in yak from Tibet. No systematic work on prevalence, incidence or epizootiology of parasitic diseases in the yak appears to have been undertaken until recently. The prevalence of hydatid cysts, mainly in lungs and/or liver and occasionally in other organs, was 42-96% in yak. This is a highly prevalent cestode infection in the yak populations of India, China and USSR (Chen et al., 1982; Li et al., 1985; Katiyar and Sinha, 1987 ). Infections with cysts of Coenurus spp. and adult Moniezia spp. were commonly encountered (Rezvikh, 1958; Mukhamadiev, 1981 ). Amongst trematodes, infection with Fasciola spp. and amphistomes predominates. The prevalence of these infections varied between 5 and 25%. Lymnaea luteola snails, the intermediate host of Fasciola spp., are also prevalent in yak breeding/rearing regions (Mukhamadiev, 1981 ). No blood flukes have been reported so far from yak. Infection with Trichostrongylus orientalis was the most prevalent (81.8%) amongst nematode parasites in yak (Jiang et al., 1987 ) from China. Eyeworms ( Thelazia spp. ) are also not uncommon. The yak has also been reported as an intermediate host for Linguatula serrata (Mukhamadiev, 1971 ). Interestingly, neither the yak nor its hybrids with cows has so far been found to be infected with Trichuris spp. and filarial nematodes. Likewise, no evidence of haemoprotozoan infections has been observed. The results of the limited investigations reported here indicated that amongst cestodes, hydatid cysts, adult Moniezia spp. and cysts of Coenurus spp. were the most commonly encountered tapeworm infections in Indian yak and its hybrids. Infection with Fasciola spp. and amphistomes had a comparatively lower prevalence of 10% and 6.6%, with mean faecal egg output of 30 and 13.3 per gram of faeces, respectively, than infections with other helminths. Eight species of gastrointestinal nematodes were observed. Of these, infection with Trichostrongylus spp, and Ostertagia spp. predominated and contributed maximally to faecal egg counts (77.4%), with mean EPG of 875. Interestingly, none of the animals studied suffered from infection with Trichuris spp. The occurrence of Eimeria brasiliensis and E. zurnii infections seems to be the first report on the prevalence of protozoan infections in yak from India. Amongst ectoparasitic infestations, warble fly seems to be the only documented arthropod pest of yak. The results of this study are in conformity with earlier reports from other countries on parasitic diseases of the yak. The difficult agro-climatic conditions that prevail on high altitude areas in the Greater Himalayas are in a way a blessing in disguise for this bovine species, as these conditions are not congenial for the propagation of various tropical para-
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sitic infections. They are responsible for the lower prevalence of haemonchosis, oesophogostomiosis, hookworm infections, schistosomiosis, etc., and account for the virtual absence of diseases caused by ectoparasites and haemoprotozoans, as well as filariosis and other arthropod-borne diseases. However, further systematically planned detailed epizootiological investigation on various diseases of this least studied species are essential before drawing any final inferences.
5. Conclusion In India, although various research schemes have been sanctioned since the late 1960s for the development of the yak, no tangible results have yet come forth. Consequently the yak, the only economically important and all-purpose animal that thrives well at high altitudes, is on the verge of extinction. Dedicated and sincere team efforts on the part of field veterinarians, researchers and planners, and awareness amongst yak owners about the factors responsible for lowered productivity and mortality are the need of the hour.
References Anantaraman, M., 1942. The life history of Oesophagostornum radiatum, the bovine nodular worm. Indian J. Vet. Sci. Anim. Husb., 12: 87-132. Biryukov, V.A., 1970. Cysticercus in Mongolian yak from slaughter-house data. Nauch. Trudy. Omsk. Vet. Inst., 27(2): 240-241. Breev, K.A. and Baratov, Sh.B., 1970. The warble-fly of yaks in the Pamirs. Parasitologiya, 4: 241244. Chaudhary, R.P., 1970. Occurrence ofwarble-fly--Hypoderma lineatum infection in yaks in Bhutan. J. Parasitol., 56: 377. Chen, D.M., Lei, H.K., Ze, R., Jing, M. and Jia, B., 1982. [Diagnosis of hydatidosis in domestic animals using the indirect haemagglutinationtests]. Chinese J. Vet. Med., 8:14-16. Dhar, D.N., Sharma, R.L. and Bansal, G.C., 1982. Gastrointestinal nematodes in sheep in Kashmir. Vet. Parasitol., 11: 271-277. Georgi, J.R., 1990. Parasitology for Veterinarians. Saunders, London, pp. 1-412. Ivashkin, V.M., 1953. Thelazia disease of the eye of yaks and cattle. Paper on helminthology presented to Academician K.I. Skrajabin on his 75th birthday, Moscow. Jiang, X.L., Zhou, W.L., Gowg, G.J. and Liu, S.M., 1987. [Finding of Trichostrongylus orientalis in yaks in Sichuan]. Chinese J. Vet. Med., 13: 19-20. Joshi, D.D. and Pradhan, P.N.S., 1977. Prevalence of parasitic infection of yaks, chauries and khirkho cattle of Khumbu valley. Bull. Vet. Sci. Anim. Husb., Nepal, 6: 7-12. Joshi, D.D. and Tiwari, H.C., 1975. Some observations on the incidence of fasciioliasis in yak and hill cattle. Bull. Vet. Sci. Anim. Husb., Nepal, 4: 1-3. Katiyar, R.D. and Sinha, A.K., 1987. Hydatid disease in livestock in Sikkim. Livestock Advisor, 6: 57-58. Li, Z.H., Zhu, X.Q. and Sun, J., 1985. [Indirect haemagglutinationtest in echinococcosis of domestic animals]. Chinese J. Vet. Sci. Tech., 6: 3-6. Linyuguang, J.X., Guan, J., Wang, P., Zhang, C. and Yang, W., 1983. [Studies on the anoplocephalata cestode and the oribatid mites, vectors of Moniezia in Ar-Baz Country, Sichuan Province]. Acta Zoologica Sin., 29: 323-332.
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Mukhamadiev, S.A., 1968. [The helminth fauna of yaks from Pamirs ]. Mater. Knof. Posvyashchennoi pamyati N.V. Badanina, Tashkent, pp. 235-236. Mukhamadiev, S.A., 1971. [Discovery ofLinguatula serrata (Frouhlich, 1789 ) in yaks. ] Biol. Abst., 55: 50622. Mukhamadiev, S.A., 1975. [Species composition of Thelazia in cattle and their distribution in the Central Asian Republics ]. In: Problemy parazitologii, Materialy VII Nauchnoi Konferentsii Parazitologov USSR Chast 2 Kiev, USSR; Naukova Dumha ( 1975 ) 53-54. Mukhamadiev, S.A., 1981. [Helminth of cattle and yak in the Tajik SSR]. Gelminty Krupnogo rogatoga skota i yakov Tadzhikistana, p. 183. RangaRao, G.S.C., 1974. Studies on certain aspects of some of the major helminthic and protozoan infections, including associated lesions in camels (Carnelus dromedarius) and yak (Bos grunniens) and other army animals. Ph.D. Thesis, Agra University, Agra, pp. 110-121. Rezvikh, A.I., 1958. Coenurus in the brain of yaks. Abstr. Vet., 35: 82. Roy, S., Mazumdar, B.K., Chakraborti, A. and Banerjee, A.K., 1986. Efficacy of three thioallophanates against strongyle infection in yaks (Bos rnutus). Indian J. Vet. Med., 6: 128-129. SouthweU, T., 1930. The Fauna of British India includingCeylon and Burma. Cestoda. Vol. II. Taylor & Francis, London, p. 262. Whitlock, H.V., 1948. Some modifications of McMaster helminth egg counting technique apparatus. J. Counc. Sci. Ind. Res., 21: 177-180. Wu, S.W., 1965. A new species of Cooperia. (Nematoda; Trichostrongylidae). Acta Vet. Zootech., Sin., 8: 293-296.
Veterinary Parasitology 53 (1994) 75-82
Parasitic infections of Indian yak Bos (poephagus) grunniens an overview G.S.C. RangaRao, R.L. Sharma*, Hemaprasanth Indian VeterinaryResearch Institute, Campus, Mukteswar-263 138, Nainital, India (Accepted 25 August 1993)
Abstract
For centuries, the yak and its hybrids with domestic cows (dzomo/dzo) have been contributing to the socio-economic status of their owners in desolate regions of the Greater Himalayas. Studies on the prevalence of parasitic diseases in these animals were undertaken in Ladakh (Jammu and Kashmir), Sikkim and villages near the Indo-Nepal border of Uttar Pradesh. Visceral organs of necropsied animals were observed for the presence of adult metazoan parasites, fresh or preserved faecal samples were examined for the eggs of helminth parasites and protozoan cysts, and blood smears were examined for haemo-protozoa and microfilariae. In all, examination of 225 faecal samples, 180 blood smears and the visceral organs of thirteen yaks and dzomo/dzo was undertaken. On necropsy, visceral organs revealed various adult liver and stomach flukes, gastrointestinal nematodes, tapeworms, cysts of Coenurus spp. and hydatid cysts, as well as Setaria cervi worms and large a n d / o r small sized Sarcocystis cysts. On coprological examination, egg prevalences of 10% for Fasciola spp., 6.6% for various amphistomes, 10% for Moniezia spp., 76.4% for Strongylate spp., 24% for Neoascaris spp. and 13.7% for Nematodirus spp. were recorded. Identification of infective larvae from the faecal cultures showed that a majority of eggs (86.3%) in the host faeces were contributed by nematodes belonging to Trichostrongyle spp., Ostertagia spp. and Cooperia spp. This was followed by Chabertia spp. (6.5%). Haemonchus spp., Bunostomum spp. and Nematodirus spp. together contributed only 7.2% of the eggs found. Among protozoan infections, Eimeria brasiliensis and E. zurnii were common. None of the blood smears evidenced any haemoprotozoa or microfilariae. Likewise, none of the animals were positive for Trichuris spp. All animals were positive for one or more species of parasites. An immediate need to undertake systematic studies on the health problems of yak is stressed in order to save this species from extinction.
Key words:Yak parasites *Corresponding author. 0304-4017/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0304-401 7 ( 9 3 ) 0 0 5 9 0 - U
76
G.S. C. RangaRao et al. / Veterinary Parasitology 53 (1994) 75-82
1. Introduction
Grunting Ox, the popular name for the yak Bos (poephagus) grunniens, is a native of the Tibetan plateau and surrounding central Asian countries. This bovine species thrives well on grasslands at high altitudes (4300-6100 m) in the Greater Himalayas, with cold to extreme cold climate, where other domestic animals either fail to survive or do not maintain their optimum productivity. In India, yaks are found in Ladalda valley (Jammu and Kashmir), Pangi, Sangla, Lalaoul and Spiti valley (Himachal Pradesh), Uttrakhand (Uttar Pradesh) and in small numbers in Sikkim and Arunachal Pradesh. They migrate to high altitudes during the summer and back to lower altitudes, along the snow-line, during winter. Although the yak has contributed significantly towards improving the socio-economic status of its owners in these desolate regions, its development and health status have been neglected. Practically no efforts have been made to study the various diseases threatening its survival and productivity. Except for sporadic reports on the occurrence of a few parasites (Fasciola spp., Amphistomes, Trichostrongyle spp., Cooperia spp., Thelazia spp., Moniezia spp., hydatid and cysts caused by Coenurus spp. as well as warble flies) from the USSR, Mongolia, China, Tibet, Bhutan and Nepal (Southwell, 1930; Ivashkin, 1953; Rezvikh, 1958; Mukhamadiev, 1968, 1971, 1975, 1981; Biryukov, 1970; Chaudhary, 1970; Joshi and Tiwari, 1975; Joshi and Pradhan, 1977; Roy et al., 1986; Katiyar and Sinha, 1987 ), no systematic studies on the prevalence and/or impact of the parasites of yak have been undertaken. Hence, the scope of this paper is to review the available information and to incorporate the authors' current observations on parasitic diseases of yak in India.
2. Materials and methods
The prevalence studies on the parasitic diseases of yak were undertaken in Ladakh (Jammu and Kashmir), Sikkim and villages in the Indo-Nepal border of Uttar Pradesh. Animals were screened for various parasites, by a detailed examination of preserved necropsy materials for adult parasites and fresh or preserved rectal faecal samples and blood smears for eggs of helminth parasites and protozoan cysts and haemoprotozoans, respectively. The experimental materials were either collected personally and/or by field veterinarians working in these far-flung areas, and were then forwarded to the laboratory. In all, 225 faecal samples, 180 blood smears and visceral organs from 13 yak and dzomo/dzo, female and male hybrid, respectively, of a male yak with a hill cow were received for the purpose. Standard parasitological techniques for faecal examinations for parasite eggs and oocysts (Whitlock, 1948 ), faecal culture for identification of nematode larvae (Anantaraman, 1942), recovery of parasites from necropsy materials, their preservation and counting (Dhar et al., 1982 ), staining and microscopic exami-
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nation of blood smears for haemoprotozoans and preparation of faecal cultures for development and identification of coccidial oocysts (Georgi, 1990 ) were used during the course of the investigation.
3. Results
3.1. Necropsy of visceral organs Detailed examination of necropsy materials from yak and dzomo/dzo, which were either slaughtered for meat or died due to accidents or natural causes, revealed the presence of liver and stomach flukes, gastro-intestinal nematodes, adult tapeworms, cysts of Coenurus spp. and hydatid cysts, and five adult female Setaria cervi from the peritoneum. Large and small size cysts of Sarcocystis were observed in the abdominal muscles. All the animals examined were positive for one or more species of parasites. The flukes recorded from the liver and gall bladder were identified as Fasciola hepatica, F. gigantica and Gigantocotyle explanatum, and amphistomes recovered from the stomach were identified as Cotylophoron cotylophorum, Gastrothylax crumenifer, Fischoederius cobboldi and Paramphistomum cervi. The majority of hydatid cysts recovered from livers were fertile, whereas those from the lungs were infertile. The adult gastro-intestinal nematode species observed were Trichostrongylus, Ostertagia, Cooperia, Nematodirus, Bunostomum, Chabertia, Haemonchus, Mecistocirrus and Neoascaris. The adult tape worms recovered from intestines were identified as Moniezia spp. An up-dated checklist of parasitic fauna of the yak is given in Table 1.
3.2. Coprologicalexamination Microscopic examination of 225 faecal samples, which were received/collected from various villages in the study area, showed the presence of amphistomes, Fasciola spp., Trichostrongylus spp., Ascaris spp., Nematodirus spp. and Moniezia spp. eggs as well as coccidial oocysts. The d z o m o / d z o and male yaks were more susceptible to these infections than female yaks. Interestingly, none of the animals screened were positive for Trichuris spp. eggs. No microfilariae could be detected in detailed microscopic examination of stained blood smears. The prevalence of Fasciola spp. and amphistome infections as revealed from egg counts was 10% and 6.6%, with average number of eggs per gram (EPG) of faeces of 13.3 (0-300) and 30 (0-400), respectively. The prevalence of Moniezia spp. infection was 10%, with an average EPG of 80 (0-1000) eggs. Coprological examination also revealed a high prevalence of Strongylate spp. (76.4%), including Nematodirus spp. (13.7%), followed by Ascaris spp. (24%), with an overall prevalence rate of 91.1% for gastro-intestinal nematode infections (Table 2). These eggs in fresh faeces were cultured to infective-stage larvae. Morphological examination of these larvae showed that the majority of eggs in the faeces
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Table 1 Updated checklist of the parasites of the yak Parasite
References
1. Protozoan parasites
1.1. Eimeria brasiliensis 1.2. Eimeria zurnii 1.3. Cysts of sarcocystis 2. Helminth parasites 2.1. Nematodes 2.1.1. Eye worms
Thelazia gulosa Thelazia lacrymalis 2.1.2. Gastro-intestinal worms
Cooperia hrenktahnsa Neoascaris vitulorum Haemonchus contortus Mecistocirrus digitatus spp. Trichostrongylus spp. Ostertagia spp. Chabertia spp. Nematodirus spp. Bunostornum spp. 2.1.3. Parasites of the peritoneum
RangaRao, 1974
Ivashkin, 1953 Jiang et al., 1987 Mukhamadiev, 1975 Wu, 1965; RangaRao, 1974; Mukhamadiev, 1981 Roy et al., 1986 Jiang et al., 1987
Mukhamadiev, 1968; RangaRao, 1974
Setaria cervi 2.2. Trematodes 2.2.1. Liver flukes
Fasciola hepatica Fasciola gigantica Gigantocotyle explanatum 2.2.2. Stomach flukes
RangaRao, 1974 Joshi and Tiwari, 1975; Mukhamadiev, 1981 RangaRao, 1974
Cotylophoron cotylophorurn Gastrothylax curmenifer Fischoederius cobboldi Paramphistornum cervi 2.3. Cestodes
Moniezia spp. Cysts of cysticercus Cysts of coenurus Hydatid cysts
3. Arthropod parasites Hypoderma lineatum (warble flies)
Southwell, 1930; RangaRao, 1974; Linyuguang et al., 1983; Mukhamadiev, 1981 Rezvikh, 1958 Biryukov, 1970 RangaRao, 1974; Katiyar and Sinha, 1987; Chen et al., 1982; Li et al., 1985 Breev and Baratov, 1970; Chaudhary, 1970
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G.S.C. RangaRao et aL / Veterinary Parasitology 53 (1994) 75-82 Table 2 Prevalence of nematode parasites in the yak (coprological examination) Location
Ladakh Sikkim Uttar Pradesh
No. of animals
Results of faecal examination, No. (%)
Ascaris spp.
Strongylate spp.
Nematodirus spp.
Overall prevalence, No. (%)
187 27 11
44 (23.5) 6 (22.2) 3 (27.4)
143 (76.5) 21 (77.8) 8 (72.7)
25 (13.4) 4 (14.8) 2 (18.0)
170 (91.0) 25 (92.9) 10 (90.9)
225
53 (24.0)
172 (76.4)
31 (13.7)
205 (91.1)
Table 3 Prevalence of infective larvae of gastro-intestinal parasites in faecal cultures Parasite
Trichostrongylus spp. Ostertagia spp. Cooperia spp. Chabertia spp. Haemonchus spp. Bunostomum spp. Nematodirus spp.
No. of cultures
10 10 10 10 10 10 10
Mean prevalence %
Range
62.7 14.7 8.9 6.5 3.9 2.4 0.9
55-71 9-20 7-11 4-9 2-6 1-3 0-2
of hosts were Trichostrongylus spp. (62.7%) and Ostertagia spp. (14.7%), followed by Cooperia spp. (8.9%) and Chabertia spp. (6.5%). The Haemonchus spp., Bunostomum spp. and Nematodirus spp. together accounted for 7.2% (Table 3 ). Extreme care was taken and all possible efforts were made to culture coccidial oocysts, which were preserved and despatched to this laboratory in two percent potassium dichromate solution. Even then, these oocysts failed to develop and sprulate. However, the oocysts were identified on the basis of size, shape and presence/absence of polar caps etc., and were assigned to Eimeria brasiliensis and E. zurnii. Detailed microscopic examination of stained blood smears did not reveal the presence of any haemoprotozoan infection in yaks.
4. Discussion The role of the yak in improving the socio-economic status of owners in desolate regions in the Greater Himalayas is well recognised and documented. The yak is a source of milk and meat and is also used as a pack animal. A mating of male yak with domestic cow is quite common. A dzomo (chaori) calf is fertile and is a higher milk yielder than female yaks. In contrast, a dzo (choru) calf is
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infertile and is used for cultivation, riding, as a pack animal and as meat for human consumption. Yak hair is used by itself or blended with other animal fibres: for making ropes or weaving bags and blankets. The white tail tuft of the yak is a valuable item and is sold at a high price for ceremonial purposes in temples. Above all, yak dung is used as fuel in the treeless plateaus and as fertilizer. In the snowbound mountainous areas, the army has been using yaks as a pack animal for transportation of rations, war equipment and ammunition, etc. Until 1923, the parasite fauna of the yak remained completely unexplored. Southwell (1930) published a pioneering report on the occurrence of Moniezia spp. in yak from Tibet. No systematic work on prevalence, incidence or epizootiology of parasitic diseases in the yak appears to have been undertaken until recently. The prevalence of hydatid cysts, mainly in lungs and/or liver and occasionally in other organs, was 42-96% in yak. This is a highly prevalent cestode infection in the yak populations of India, China and USSR (Chen et al., 1982; Li et al., 1985; Katiyar and Sinha, 1987 ). Infections with cysts of Coenurus spp. and adult Moniezia spp. were commonly encountered (Rezvikh, 1958; Mukhamadiev, 1981 ). Amongst trematodes, infection with Fasciola spp. and amphistomes predominates. The prevalence of these infections varied between 5 and 25%. Lymnaea luteola snails, the intermediate host of Fasciola spp., are also prevalent in yak breeding/rearing regions (Mukhamadiev, 1981 ). No blood flukes have been reported so far from yak. Infection with Trichostrongylus orientalis was the most prevalent (81.8%) amongst nematode parasites in yak (Jiang et al., 1987 ) from China. Eyeworms ( Thelazia spp. ) are also not uncommon. The yak has also been reported as an intermediate host for Linguatula serrata (Mukhamadiev, 1971 ). Interestingly, neither the yak nor its hybrids with cows has so far been found to be infected with Trichuris spp. and filarial nematodes. Likewise, no evidence of haemoprotozoan infections has been observed. The results of the limited investigations reported here indicated that amongst cestodes, hydatid cysts, adult Moniezia spp. and cysts of Coenurus spp. were the most commonly encountered tapeworm infections in Indian yak and its hybrids. Infection with Fasciola spp. and amphistomes had a comparatively lower prevalence of 10% and 6.6%, with mean faecal egg output of 30 and 13.3 per gram of faeces, respectively, than infections with other helminths. Eight species of gastrointestinal nematodes were observed. Of these, infection with Trichostrongylus spp, and Ostertagia spp. predominated and contributed maximally to faecal egg counts (77.4%), with mean EPG of 875. Interestingly, none of the animals studied suffered from infection with Trichuris spp. The occurrence of Eimeria brasiliensis and E. zurnii infections seems to be the first report on the prevalence of protozoan infections in yak from India. Amongst ectoparasitic infestations, warble fly seems to be the only documented arthropod pest of yak. The results of this study are in conformity with earlier reports from other countries on parasitic diseases of the yak. The difficult agro-climatic conditions that prevail on high altitude areas in the Greater Himalayas are in a way a blessing in disguise for this bovine species, as these conditions are not congenial for the propagation of various tropical para-
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81
sitic infections. They are responsible for the lower prevalence of haemonchosis, oesophogostomiosis, hookworm infections, schistosomiosis, etc., and account for the virtual absence of diseases caused by ectoparasites and haemoprotozoans, as well as filariosis and other arthropod-borne diseases. However, further systematically planned detailed epizootiological investigation on various diseases of this least studied species are essential before drawing any final inferences.
5. Conclusion In India, although various research schemes have been sanctioned since the late 1960s for the development of the yak, no tangible results have yet come forth. Consequently the yak, the only economically important and all-purpose animal that thrives well at high altitudes, is on the verge of extinction. Dedicated and sincere team efforts on the part of field veterinarians, researchers and planners, and awareness amongst yak owners about the factors responsible for lowered productivity and mortality are the need of the hour.
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