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Sharing schistosomes: the elephant schistosome Bivitellobilharzia nairi also infects the greater one-horned rhinoceros (Rhinoceros unicornis) in Chitwan National Park, Nepal

Published online by Cambridge University Press:  31 October 2012

R. Devkota*
Affiliation:
Center for Evolutionary and Theoretical Immunology (CETI), Department of Biology, University of New Mexico, New Mexico, USA
S.V. Brant
Affiliation:
Center for Evolutionary and Theoretical Immunology (CETI), Department of Biology, University of New Mexico, New Mexico, USA Museum of Southwestern Biology, University of New Mexico, USA
A. Thapa
Affiliation:
Biodiversity and Environmental Management, NOMA Program, Central Department of Botany, Tribhuvan University, Kirtipur, Kathmandu, Nepal
E.S. Loker
Affiliation:
Center for Evolutionary and Theoretical Immunology (CETI), Department of Biology, University of New Mexico, New Mexico, USA Museum of Southwestern Biology, University of New Mexico, USA
*

Abstract

Because the digenetic trematode fauna of Nepal is poorly known, we began to search for schistosomes in and around Chitwan National Park (CNP) of southern Nepal. Both domestic and wild Indian elephants (Elephus maximus) are present, and we found one of two dung samples from wild elephants and 1 of 22 (4.5%) dung samples from domestic elephants to be positive for schistosome eggs. The morphology of the eggs and both cox1 and 28S sequences derived from the eggs/miracidia were consistent with Bivitellobilharzia nairi, reported here for the first time from Nepal. Also, 7 of 14 faecal samples from the Asian or greater one-horned rhinoceros (Rhinoceros unicornis) contained viable eggs indistinguishable from those of B. nairi. This identification was confirmed by comparison with both cox1 and 28S sequences from B. nairi eggs/miracidia derived from Nepalese and Sri Lankan elephants. This represents the first sequence-verified identification of a schistosome from any species of rhinoceros, and the first verified occurrence of a representative of Bivitellobilharzia (a genus of ‘elephant schistosomes’) in mammals other than elephants. Our work suggests that elephants and rhinos share B. nairi in CNP, even though these two members of the ‘charismatic megafauna’ belong to unrelated mammalian families. Their shared life style of extensive contact with freshwater habitats likely plays a role, although the snail intermediate host and mode of definitive host infection for B. nairi have yet to be documented. This report also supports Bivitellobilharzia as a monophyletic group and its status as a distinct genus within Schistosomatidae.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2012 

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References

Agatsuma, T., Rajapakse, R.P.V.J., Kuruwita, V.Y., Iwagami, M. & Rajapakse, R.C. (2004) Molecular taxonomic position of the elephant schistosome, Bivitellobilharzia nairi, newly discovered in Sri Lanka. Parasitology International 53, 6975.Google Scholar
Anonymous (1984) Parasite killed elephant. 9 September 1984, Associated Press.Google Scholar
Brant, S.V., Morgan, J.A.T., Mkoji, G.M., Snyder, S.D., Rajapakse, R.P.V.J. & Loker, E.S. (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology 92, 7788.Google Scholar
Brant, S.V., Pomajbíková, K., Modry, D., Petrželková, K.J., Todd, A. & Loker, E.S. (2012) Molecular phylogenetics of the elephant schistosome, Bivitellobilharzia loxodontae (Trematoda: Schistosomatidae) from the Central African Republic. Journal of Helminthology 86, 16.Google Scholar
Chakraborty, A. & Gogoi, A.R. (1995) Parasites of rhinoceros (Rhinoceros unicornis). Indian Journal of Animal Sciences 65, 421422.Google Scholar
Chakraborty, A. & Islam, S. (1993) A survey of gastrointestinal parasitic infection in free-living rhinoceros of Kaziranga National Park. Indian Journal of Animal Sciences 63, 155156.Google Scholar
Devkota, R. (2008) Inventory of trematode cercariae infections in freshwater snails in Chitwan and Nawalparasi Districts and trematode infections in domestic elephants of Sauraha (minor study). A thesis submitted to Central Department of Zoology, Institute of Science and Technology, Tribhuvan University, Kirtipur, Kathmandu, Nepal.Google Scholar
Dutt, S.C. & Srivastava, H.D. (1961) On the morphology and life history of a new mammalian blood fluke, Ornithobilharzia dattai n. sp. (preliminary report). Indian Journal of Parasitology 13, 6173.Google Scholar
Dutta, G.C., Bordoloi, G.C., Pathak, M. & Choudhury, A. (1990) Incidence of intestinal helminthic infection in Rhinoceros unicornis in captivity. Zoos' Print 5, 14.Google Scholar
Fitzsimmons, W.M. (1962) Parabronema roundi n. sp. (Spiruridae: Nematoda) from Rhinoceros bicornis in Kenya. Journal of Helminthology XXXVI, 3944.Google Scholar
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic tress. Bioinformatics 17, 754755.CrossRefGoogle Scholar
Karki, K. & Manandhar, P. (2008) Incidence of gastrointestinal helminthes in captive elephants in wildlife reserves of Nepal. Articlesbase, Free Online Articles Directory. Available at websitehttp://www.articlesbase.com/health-articles/incidence-of-gastrointestinal-helminthes-in-captive-elephants-in-wildlife-reserves-of-nepal-335689.html (accessed accessed 4 February 2012).Google Scholar
Kinsella, J.M., Deem, S.L., Blake, S. & Freeman, A.S. (2004) Endoparasites of African forest elephants (Loxodonta africana cyclotis) from the Republic of Congo and Central African Republic. Comparative Parasitology 71, 104110.CrossRefGoogle Scholar
Laurie, A.L. (1978) The ecology and behavior of the great one horned rhinoceros. A dissertation submitted to the University of Cambridge for the degree of doctor of philosophy, Selwyn College, Cambridge.Google Scholar
Meredith, R.W., Janečka, J.E., Gatesy, J., Ryder, O.A., Fisher, C.A., Teeling, E.C., Goodbla, A., Eizirik, E., Simão, T.L.L., Stadler, T., Rabosky, D.L., Honeycutt, R.L., Flynn, J.J., Ingram, C.M., Steiner, C., Williams, T.L., Robinson, T.J., Burk-Herrick, A., Westerman, M., Ayoub, N.A., Springer, M.S. & Murphy, W.J. (2011) Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521524.CrossRefGoogle ScholarPubMed
Mudaliar, S.V. & Ramanujachary, G. (1945) Schistosoma nairi n. sp. from an elephant. Indian Veterinary Journal 12, 14.Google Scholar
Muryani, A., Tiuria, R., Andriansyah, & Agil, M. (2008) Helminthes parasite at feces of Sumatran Rhinoceros (Dicerorhinus sumtrensis) and Sumatran Elephant (Elephas maximus surnatranus) in Way Kambas National park Lampung (semi in situ). Proceedings of Asian Zoo/Wildlife Medicine and Conservation, 1922August, Bogor, Indonesia.Google Scholar
Palmieri, J.R., Purmono, & Ammann, H. (1980) Parasites of the lesser one-horned rhinoceros (Rhinoceros sondaicus Desmarest). Journal of Parasitology 66, 1031.CrossRefGoogle ScholarPubMed
Penzhorn, B.L., Krecek, R.C., Horak, I.G., Verster, A.J.M., Walker, J.B., Boomker, J.D.F., Knapp, S.E. & Quandt, S.K.F. (1994) Parasites of African rhinos: a documentation. Proceedings of a Symposium on ‘Rhinos as Game Ranch Animals’, 9–10 September, Onderstepoort, Pretoria, South Africa.Google Scholar
Posada, D. (2008) jModeltest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.Google Scholar
Rao, R. & Hiregauder, L.S. (1953) Schistosomiasis in elephants in Bombay State. Indian Veterinary Journal 30, 241242.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Silberman, M.S. & Fulton, R.B. (1979) Medical problems of captive and wild rhinoceros: a review of the literature and personal experiences. The Journal of Zoo Animal Medicine 10, 616.Google Scholar
Southwell, T. (1921) A new species of cestode (Anoplocephala vulgaris) from an African Rhinoceros. Annals of Tropical Medicine and Parasitology 14, 355364.Google Scholar
Stothard, J.R., Webster, B.L., Weber, T., Nyakaana, S., Webster, J.P., Kazibwe, F., Kabatereine, N.B. & Rollinson, D. (2009) Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136, 18131824.Google Scholar
Sundaram, R.K., Padmanabha Iyer, R., Peter, C.T. & Alwar, V.S. (1972) On Bivitellobilharzia nairi (Mudaliar and Ramanujachari, 1945) Dutt and Srivastava, 1955 (Trematoda: Schistosomatidae) parasitic in Indian elephants (Elaphas maximus) with a redescription of the species. Indian Veterinary Journal 49, 110.Google Scholar
Swofford, D.L. (2002) PAUP*: Ver 4.0. Phylogenetic Analysis Using Parsimony (*and other methods). Sunderland, Sinauer Associates.Google Scholar
Thapar, G.S. (1925) On some new members of the Genus Kiluluma from the African Rhinoceros. Journal of Helminthology III, 6380.Google Scholar
Tiuria, R., Primawidyawan, A., Pangihutan, J., Warsito, J., Hariyadi, A.R.S., Handayani, S.U. & Priosoeryarito, B.P. (2006) Identification of endoparasites from faeces of Javan rhino (Rhinoceros sondaicus) in Ujung Klon National Park, Indonesia. The Second Symposium on the Asian Zoo and Wildlife Medicine and the First Workshop on Zoo and Wildlife Pathology (AZWMP). Bangkok, Thailand, Faculty of Veterinary Science, Chulalongkorn University.Google Scholar
Vogel, H. & Minning, W. (1940) Bilharziose bei Elefanten. Archiv für Schiffs und Tropenhygiene 44, 562574.Google Scholar
Zhang, J., Daszak, P., Huang, H., Yang, G., Kilpatrick, A.M. & Zhang, S. (2008) Parasite threat to panda conservation. EcoHealth 5, 69.Google Scholar
Zumpt, F. (1964) Parasites of the white and black rhinoceroses. The Lammergeyer 3, 5970.Google Scholar