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251 Veterinary Practitioner Vol. 17 No. 2 December 2016 1 Professor and corresponding author e-mail: [email protected]; 2 Veterinary Surgeon/Project Lead Centre for Bear Rehabilitation and Conservation, WTI, Pakke Tiger Reserve, Seijusa, East Kameng, Arunachal Pradesh, e-mail: [email protected]; 3 Master of Veterinary Science scholar, Department of Parasitology, CVSc, AAU, Khanapara, Guwahati - 781 022, e-mail: [email protected]; 4 Deputy Director, Wildlife Trust of India (WTI), e-mail: [email protected]; 5 Divisional Forest Officer, Pakke Wildlife Sanctuary and Tiger Reserve, Seijosa, East Kameng District, Arunachal Pradesh, e-mail: [email protected] FILARIAL PARASITE FROM A FREE-LIVING GREAT PIED HORNBILL (BUCEROS BICORNIS) FROM PAKKE WILD LIFE SANCTUARY AND TIGER RESERVE, ARUNACHAL PRADESH, INDIA Saidul Islam 1 , Jahan Ahmed 2 , Nidarsana Rabha 3 , Sunil Kyarong 4 and Tana Tapi 5 Department of Parasitology, College of Veterinary Science Assam Agricultural University (AAU), Khanapara, Guwahati - 781 022, Assam, India ABSTRACT Parasitic infection in free living great pied hornbill (Buceros bicornis) is scanty. Present communication deals with the occurrence of a filarial parasite from a male B. bicornis from the Pakke Wildlife Sanctuary and Tiger Reserve, Arunachal Pradesh, India. A male bird was rescued from the wilderness of the Pakke Wildlife Sanctuary which was found to have severe traumatic injury. Even after providing intensive veterinary-medical care the bird succumbed on 9 th day after rescue. Post-mortem examination of the carcass revealed presence of filarial parasites located in the subcutaneous tissues and pleural sac of the bird. Parasitological evaluation of the samples confirmed filarial parasites that belonged to the family Onchocercidae and sub-family Lemdaninae. Key words: Great pied hornbill, Buceros bicornis, Ameeria spp., Pakke Wildlife Sanctuary and Tiger Reserve, Arunachal Pradesh Introduction Hornbills are medium to large sized free ranged birds of the family Bucerotidae. They possess massive bills with a variable sized casque. They are arboreal in habit and mainly feed on wild Ficus figs and various berries. Occasionally, the feed consist insects and small animals. In wilderness, they are found in pairs, often in small groups. They nest in holes of tall, wood trees (Fig. 1). Eggs are incubated by the female. As the female sits for incubating the eggs, the male paints the nest entrance with mud leaving a narrow vertical slit to feed the female from outside (Fig. 2). The male makes repeated visits to the nest to feed the female. There are various species of hornbills found in the country i.e. Mulbar gray hornbill (Ocyceros griseus), Indian grey hornbill (O. birostris), Malabar pied hornbill ( Anthracoceros coronatus ), Oriental pied hornbill ( A. albirostris), brown hornbill (Anorrhinus tickelli ), great pied hornbill (Buceros bicornis) and rufous-necked hornbill (Aceros nipalensis). Amongst these, the great pied hornbill is the most spectacular one (Fig.1) with size varying from 95 to 105 cm (Grimmett et al., 2015). Where the later species is endemic, the males are captured or poached for collection of feathers, casques and beaks as trophies. They also bear local traditional ethnic values. If the male fall victim of poaching or dies accidentally, the life of the female in incubation becomes at stake. Clandestine logging has become a contributory threat factor for the nesting habitats. The existing world population is roughly estimated as 13,000 - 27,000 mature birds; IUCN has enlisted B. bicornis as Near Threatened (NT) species (Bird Life International, 2016). In India, the species is fairly common, however, the number is declining. The Pakke Wildlife Sanctuary (PWLS) and Tiger Reserve is the abode of a good number of B. bicornis in addition to 268 species of resident birds (Varma et al., 2008). PWLS is an IUCN category II habitat of wildlife. It is located in East Kameng district of Arunachal Pradesh, established in 1966. The area coverage of the Sanctuary is 861.95 km 2 (332.80 sq mt) and located between the latitudes 26 0 542 -27 0 162 N and longitudes 92 0 362 - 92 0 092 E at an elevation of 2040 m (6,690 ft). The sanctuary has a good precipitation (2,506 millimeters or 98.7 inch) with an annual average summer temperature of 36 0 C (97 0 F) and 12 0 C (54 0 F) winter temperature. The forest type of the sanctuary is Assam valley tropical semi-evergreen forest. It has six types of vegetations, i.e., Sub-Himalayan light alluvial semi evergreen forests (2B/C/151), Eastern Hollock forests (3/152(b)), Upper Assam valley tropical evergreen forest (1B/C.2B), Tropical riverine forests (4E/RSI) and secondary moist bamboo tract (E1/2/SI) (Champion and Seth, 1959). B. bicornis is declared as the state bird of Arunachal Pradesh and legally it is protected under Schedule I, Part III of the Wildlife (Protection) Act (1972) of India. There is trade ban on B. bicornis according to CITES Appendix I. The species can be bred in captivity in zoos (Jensen, 2008). There is least information on the veterinary parasitic diseases of this NT species (Reddy and Rao, 1983; Ali, 1961, Galama, 1996; Galama et al., 2002 and Hossain, 2012) probably due to rarity of availing materials from the wilderness. We record here a chance case of natural filarial infection in a free ranged B. bicornis from PWLS. Materials and Methods Source of materials An adult male great pied hornbill (Buceros bicornis) weighing 3.28 kg was rescued at Lanka in the Pakke Wildlife Sanctuary and Tiger Reserve, East Kameng District of Received: 03.12.2016 Accepted: 17.12.2016

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Veterinary Practitioner Vol. 17 No. 2 December 2016

1Professor and corresponding author e-mail: [email protected]; 2Veterinary Surgeon/Project Lead Centre for Bear Rehabilitation and Conservation,WTI, Pakke Tiger Reserve, Seijusa, East Kameng, Arunachal Pradesh, e-mail: [email protected]; 3Master of Veterinary Science scholar,Department of Parasitology, CVSc, AAU, Khanapara, Guwahati - 781 022, e-mail: [email protected]; 4Deputy Director, Wildlife Trust ofIndia (WTI), e-mail: [email protected]; 5Divisional Forest Officer, Pakke Wildlife Sanctuary and Tiger Reserve, Seijosa, East Kameng District,Arunachal Pradesh, e-mail: [email protected]

FILARIAL PARASITE FROM A FREE-LIVING GREAT PIED HORNBILL(BUCEROS BICORNIS) FROM PAKKE WILD LIFE SANCTUARY AND TIGER

RESERVE, ARUNACHAL PRADESH, INDIA

Saidul Islam1, Jahan Ahmed2, Nidarsana Rabha3, Sunil Kyarong4 and Tana Tapi5Department of Parasitology, College of Veterinary Science

Assam Agricultural University (AAU), Khanapara, Guwahati - 781 022, Assam, India

ABSTRACT

Parasitic infection in free living great pied hornbill (Buceros bicornis) is scanty. Present communication deals with the occurrence ofa filarial parasite from a male B. bicornis from the Pakke Wildlife Sanctuary and Tiger Reserve, Arunachal Pradesh, India. A male birdwas rescued from the wilderness of the Pakke Wildlife Sanctuary which was found to have severe traumatic injury. Even afterproviding intensive veterinary-medical care the bird succumbed on 9th day after rescue. Post-mortem examination of the carcassrevealed presence of filarial parasites located in the subcutaneous tissues and pleural sac of the bird. Parasitological evaluation of thesamples confirmed filarial parasites that belonged to the family Onchocercidae and sub-family Lemdaninae.

Key words: Great pied hornbill, Buceros bicornis, Ameeria spp., Pakke Wildlife Sanctuary and Tiger Reserve, Arunachal Pradesh

IntroductionHornbills are medium to large sized free ranged birds of

the family Bucerotidae. They possess massive bills with avariable sized casque. They are arboreal in habit and mainlyfeed on wild Ficus figs and various berries. Occasionally, thefeed consist insects and small animals. In wilderness, theyare found in pairs, often in small groups. They nest in holes oftall, wood trees (Fig. 1). Eggs are incubated by the female. Asthe female sits for incubating the eggs, the male paints thenest entrance with mud leaving a narrow vertical slit to feed thefemale from outside (Fig. 2). The male makes repeated visitsto the nest to feed the female. There are various species ofhornbills found in the country i.e. Mulbar gray hornbill (Ocycerosgriseus), Indian grey hornbill (O. birostris), Malabar pied hornbill(Anthracoceros coronatus), Oriental pied hornbill (A.albirostris), brown hornbill (Anorrhinus tickelli), great piedhornbill (Buceros bicornis) and rufous-necked hornbill (Acerosnipalensis). Amongst these, the great pied hornbill is the mostspectacular one (Fig.1) with size varying from 95 to 105 cm(Grimmett et al., 2015). Where the later species is endemic,the males are captured or poached for collection of feathers,casques and beaks as trophies. They also bear local traditionalethnic values. If the male fall victim of poaching or diesaccidentally, the life of the female in incubation becomes atstake. Clandestine logging has become a contributory threatfactor for the nesting habitats. The existing world population isroughly estimated as 13,000 - 27,000 mature birds; IUCN hasenlisted B. bicornis as Near Threatened (NT) species (BirdLife International, 2016). In India, the species is fairly common,however, the number is declining.

The Pakke Wildlife Sanctuary (PWLS) and Tiger Reserveis the abode of a good number of B. bicornis in addition to 268

species of resident birds (Varma et al., 2008). PWLS is anIUCN category II habitat of wildlife. It is located in East Kamengdistrict of Arunachal Pradesh, established in 1966. The areacoverage of the Sanctuary is 861.95 km2 (332.80 sq mt) andlocated between the latitudes 260542 -270162 N andlongitudes 920362 - 920092 E at an elevation of 2040 m (6,690ft). The sanctuary has a good precipitation (2,506 millimetersor 98.7 inch) with an annual average summer temperature of360C (970F) and 120C (540F) winter temperature. The foresttype of the sanctuary is Assam valley tropical semi-evergreenforest. It has six types of vegetations, i.e., Sub-Himalayan lightalluvial semi evergreen forests (2B/C/151), Eastern Hollockforests (3/152(b)), Upper Assam valley tropical evergreen forest(1B/C.2B), Tropical riverine forests (4E/RSI) and secondarymoist bamboo tract (E1/2/SI) (Champion and Seth, 1959). B.bicornis is declared as the state bird of Arunachal Pradeshand legally it is protected under Schedule I, Part III of the Wildlife(Protection) Act (1972) of India. There is trade ban on B. bicornisaccording to CITES Appendix I. The species can be bred incaptivity in zoos (Jensen, 2008). There is least information onthe veterinary parasitic diseases of this NT species (Reddyand Rao, 1983; Ali, 1961, Galama, 1996; Galama et al., 2002and Hossain, 2012) probably due to rarity of availing materialsfrom the wilderness. We record here a chance case of naturalfilarial infection in a free ranged B. bicornis from PWLS.

Materials and Methods

Source of materialsAn adult male great pied hornbill (Buceros bicornis)

weighing 3.28 kg was rescued at Lanka in the Pakke WildlifeSanctuary and Tiger Reserve, East Kameng District of

Received: 03.12.2016Accepted: 17.12.2016

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Veterinary Practitioner Vol. 17 No. 2 December 2016

Fig.1: A male great pied hornbill (Buceros bicornis) near its nest

Fig. 2: A male B. bicornis feeding the female

Fig. 3: Post-mortem examination of a B. bicornis

Fig. 4: Filarial parasite located in the subcutaneous tissues (inset ) ofa B. bicornis

Fig. 5: Anterior end of a male Ameeria spp. showing cephalicpapillae

Fig. 6: Cuticular striations and rugae in the middle part of the body of amale Ameeria spp.

Fig. 7: Spirally coiled caudal end of a male Ameeria spp. showingcaudal papillae and the unequal spicules (left lateral view)

Arunachal Pradesh by the staffs of the sanctuary. The bird wasbrought for veterinary-medical care to the Centre for BearRehabilitation and Conservation (CBRC) jointly operated bythe Department of Environment and Forest, Government ofArunachal Pradesh and Wildlife Trust of India (WTI) located atSeijosa during the month of August, 2015. On clinicalexamination by the resident veterinary surgeon the bird wasfound to have severe injury caused due to hit by catapult. Thetraumatic injury was detected in the rump associated withconsistent loss of feather around the injured area. The birdalso became unable to fly. Though the patient was providedwith adequate veterinary-medical care, yet, it succumbed on

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of wild life (Islam, 2012) which might endanger the life ofprecious wildlife. The north-eastern region of India beingbiodiversity hotspot region needs attention in respect ofgenerating baseline information on the parasitic fauna andtheir pathology in wildlife. Present investigation could gatherdata on the occurrence of a filarial nematode Ameeria Ali, 1961for the first time from a free ranged B. bicornis from its in situhabitat.

AcknowledgementsAuthors acknowledge the Department of Forests and

Environment, Govt. of Arunachal Pradesh and Wildlife Trust ofIndia (WTI), Noida, for the materials and the Dean, Faculty ofVeterinary Science, Assam Agricultural University, Khanapara,Guwahati - 781 022 for the facilities to carry out this study.

ReferencesAli, S.M. (1961) J. Parasitol. 47: 715-716.Bird Life International (2016) Buceros bicornis. The IUCN Red List of

Threatened Species 2016: e.T22682453A92947174.http://dx.doi.org/10.2305/IUCN.UK.2016 3.RLTS.T. 22682453A92947174.en. (visited on 1.2.2017).

Champion, H.G. and Seth, S.K. (1968) A Revised Survey of the ForestTypes of India. Manager of Publications, Govt. of India, Delhi-6. pp. 404.

Galama, W. et al. (2002) EAZA Hornbill Management and HusbandryGuidelines. The EAZA Hornbill TAG, The Netherlands.pp.14-15.

Galama, W.T. (1996) Lords of the Asian forest canopy Buceros bicornis.Unpublishsed Masters’ Thesis. Free University atAmsterdam, Amsterdam. pp. 58.

Grimmett, R. et al. (2015) Birds of the Indian Subcontinent. OxfordUniversity Press. London. pp. 244-246.

Hossain, N. (2012) Investigation on gastrointestinal parasitesin captive wild animals and birds in BangabandhuSheikh Mujib Safari Park, Dulahazra, Cox’s Bazar .M.Sc. Thesis submitted to the Bangladesh AgriculturalUniversity, Mymensingh.

Is lam, S. (2012) Wildlife parasites in Indian context . In :Integrated Research Approaches in Veter inaryParasitology. Shanker, D., Tiwari, J., Jaiswal , A.K.Sudan, V. (Eds). 2012. Department of Parasitology,College of Veterinary Science and Animal Husbandry ,U.P. Pandit Deen Dayal Upadhyaya Pashu ChikitsaVigyan Vishwavidyalaya Evam Go-AnusandhanSansthan (DUVASU), Mathura (U.P.) India. pp.128-152.

Jensen, S.B. (2008) Gefiederte Welt. 132(6): 32. (cf. BirdLifeInternational (2016) Buceros bicornis. The IUCN RedList of Threatened Species 2016).

Reddy, R.K. and Rao, B.V. (1983) Current Sci. 52(7):316.Sood, M.L. (2006) Nematode Parasites of Birds ( inc luding

poultry) from South Asia. 1st ed. International BookDis tr ibution Company, Lucknow- 226 004, UttarPradesh, pp. 535-591.

Soulsby, E.J.L. (2012) Helminths, Arthropods and Protozoa ofDomesticated Animals. 7th ed. East-W est Press. NewDelhi-1.

The Wildlife (Protection) Act 1972 Amended up to 1991. NatrajPublishers(1994), Dehra Dun. pp. 115.

Varma, S . et al. (2008) Pakke Pachyderms-Ecology andConservation of Asian Elephants in Kameng ElephantReserve, Arunachal Pradesh. Wildlife Trust of India,New Delhi. pp. 27.

9th day after rescue at the CBRC facilities. A post-mortemexamination was conducted by the second author to ascertainthe cause of death. It revealed that, the bird died due to majororgan failure. In addition to the lesions in the organs and body,presence of a few helminth parasites could also be noticed inthe subcutaneous tissues and the pleural sac (Fig. 3 and Fig.4). The parasites were collected, fixed and preserved in 2%formalin. The samples were sent for parasitological evaluationto the Department of Parasitology, College of Veterinary Science,Assam Agricultural University, Khanapara, Guwahati-22. Theunknown parasitic species is the material for the presentcommunication.

Parasitological evaluationThe parasitic samples were cleaned in distilled water

and put in lactophenol for 48 hours for clearing. Thereafter,temporary mount was prepared and examined under acompound microscope for evaluation of morphologicalcharacteristics of the parasites following standard publishedkeys (Sood, 2006).

Results and DiscussionIn the present investigation, four nematode parasites

could be isolated, of which two were males and two females.The latter two were significantly damaged during collection.Based on the morphological features of the exhibits understudy, they could be assigned to the family Onchocercidae(Leiper, 1911) and sub-family Lemdaninae (Lopez-Neyra,1956). Further morphological features were similar to thegenera Ameeria (Ali, 1961; Sood, 2006) (Fig. 5, Fig. 6 andFig.7), pending species affiliation. Prevalence of helminthparasites in hornbills are scantily reported by a few authors.Previously, Ali (1961) described the morphology of filarialparasites recovered from the orbital cavity and under neathskin along trachea of a captive common grey hornbill (Tockusbirostris) from Hyderabad. Based on measurements of 2 malesand 6 females the author assigned the parasites to belong toa new genera Ameeria Ali, 1961 and a new species as A.sultanae (Ali, 1961). Reddy and Rao (1983) reported thepresence of Ascaridia galli in the intestine of a captive greathornbill (B. birostris) from the Nehru Zoological Park atHyderabad. Galama (1996) reported the occurrence of Ascaris,Trichostorngylus and Strongyloides in B. bicornis. Galama etal. (2002) in a compilation on hornbill management andhusbandry guidelines opined that a nematode parasiteSyngamus trachea, commonly known as gape worm infectionmay be one of the causes of mortality of young birds in nest.The parasite is transmitted from adult birds to the young.Hossain (2012) could recover Heterakis sp. and stomachworm during post-mortem examination of a great pied hornbill(Buceros birostris) from Bangabandhu Sheikh Mujib Safari Park,Dulahazra, Cox’s Bazar of Bangladesh. It could be observedthat, the life cycle of the parasites mentioned above or theirpathology in B. bicornis has not been worked out. Henceinference has to be drawn from the known species that occursin domesticated birds (Soulsby, 2012). Veterinary health careand management of captive wildlife especially endangeredspecies in exhibits, breeding, rescue or rehabilitation center isa challenge for the wildlife veterinarians due to lack of baselineinformation on pathogens. Parasites are common pathogens