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Differences between chimpanzee and baboon gastrointestinal parasite communities

Published online by Cambridge University Press:  03 March 2015

M. A. EBBERT ,
W. C. McGREW  and
L. F. MARCHANT
M. A. EBBERT*
Affiliation:
Department of Biology, Orange County Community College, 115 South Street, Middletown, New York 10940, USA
W. C. McGREW
Affiliation:
Department of Archaeology and Anthropology, University of Cambridge, Fitzwilliam Street, Cambridge CB2 1QH, UK
L. F. MARCHANT
Affiliation:
Department of Anthropology, Miami University, 501 East High Street, Oxford, OH 45056, UK
*
*Corresponding author. Department of Biology, Orange County Community College, 115 South Street, Middletown, New York 10940, USA. E-mail: [email protected]
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Summary

Cross-species infection among humans, chimpanzees (Pan troglodytes) and baboons (Papio spp.) is potentially a significant public health issue in Africa, and of concern in the conservation of P. troglodytes. However, to date, no statistical comparisons have been made between the prevalence, richness and composition of parasite communities in sympatric populations of baboons and P. troglodytes. We compared parasite communities in sympatric P. troglodytes and Papio papio living in a wilderness site, in the Republic of Senegal, West Africa. We asked whether, in the absence of humans, there are significant differences between these hosts in their interactions with gastrointestinal parasites. We tested whether host, location, or time of collection accounted for variation in prevalence, richness and community composition, and compared prevalence across six studies. We concluded that, despite being closely related, there are significant differences between these two hosts with respect to their parasite communities. At our study site, prevalence of Balantidium, Trichuris and Watsonius was higher in P. papio. Papio papio harboured more parasites per host, and we found evidence of a positive association between Trichuris and Balantidium in P. troglodytes but not P. papio.

Keywords

Pan troglodytesPapio papiohelminthsprevalencerichnessbiodiversitymixed infectionscross infectioncommunity composition
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 958 - 967
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Baldwin, P. J., McGrew, W. C. and Tutin, C. E. G. (1982). Wide-ranging chimpanzees at Mt. Assirik, Senegal. International Journal of Primatology 3, 367–385.CrossRefGoogle Scholar
Bakuza, J. and Nkwengulila, G. (2009). Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. International Journal of Primatology 30, 43–53.CrossRefGoogle Scholar
Brearley, G., Rhodes, J., Bradley, A., Baxter, G., Seabrook, L., Lunney, D., Liu, Y. and McAlpine, C. (2013). Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88, 427–442.CrossRefGoogle ScholarPubMed
Cooper, N., Griffin, R., Franz, M., Omotayo, M. and Nunn, C. L. (2012). Phylogenetic host specificity and understanding parasite sharing in primates. Ecology Letters 15, 1370–1377.CrossRefGoogle ScholarPubMed
Crockett, E. and Dipeolu, O. (1984). A survey of helminth parasites of game animals in Kainji Lake National Park of Nigeria. International Journal of Zoonoses 11, 204–215.Google ScholarPubMed
Drakulovski, P., Bertout, S., Locatelli, S., Butel, C., Pion, S., Mpoudi-Ngole, E., Delaporte, E., Peeters, M. and Mallié, M. (2014). Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon. Parasitology Research 113, 2541–2550.CrossRefGoogle ScholarPubMed
Ebbert, M. A., McGrew, W. C. and Marchant, L. F. (2013). Community composition, correlations among taxa, prevalence and richness in gastrointestinal parasites of baboons in Senegal, West Africa. Primates 54, 183–189.CrossRefGoogle ScholarPubMed
Eswarappa, S., Estrela, S. and Brown, S. (2012). Within-host dynamics of multi-species infections: facilitation, competition and virulence. PLoS ONE 7, e38730.CrossRefGoogle ScholarPubMed
File, S. K., McGrew, W. C. and Tutin, C. E. G. (1976). The intestinal parasites of a community of feral chimpanzees, Pan troglodytes schweinfurthii . Journal of Parasitology 62, 259–261.CrossRefGoogle ScholarPubMed
Ghai, R. R., Chapman, C. A., Omeja, P. A., Davies, T. J. and Goldberg, T. L. (2014 a). Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission. PLoS Neglected Tropical Disease 8, e2641.CrossRefGoogle Scholar
Ghai, R. R., Simons, N. D., Chapman, C. A., Omeja, P. A., Davies, T. J., Ting, N. and Goldberg, T. L. (2014 b). Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Neglected Tropical Disease 8, e3256.CrossRefGoogle ScholarPubMed
Gillespie, T. R., Lonsdorf, E. V., Canfield, E. P., Meyer, D. J., Nadler, Y., Raphael, J., Pusey, A. E., Pond, J., Pauley, J., Mlengeya, T. and Travis, D. A. (2010). Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. American Journal of Physical Anthropology 143, 534–544.CrossRefGoogle ScholarPubMed
Goldsmid, J. M. (1974). The intestinal helminthzoonoses of primates in Rhodesia. Annales de la Société Belge de Médecine Tropicale 54, 87–101.Google Scholar
Goldsmid, J. M. and Rogers, S. (1978). A parasitological study on the chacma baboon (Papio ursinus) from the northern Transvaal. Journal of the South African Veterinary Association 49, 109–111.Google Scholar
Gómez, J. M., Nunn, C. L. and Verdú, M. (2013). Centrality in primate–parasite networks reveals the potential for the transmission of emerging infectious diseases to humans. Proceedings of the National Academy of Sciences 110, 7738–7741.CrossRefGoogle ScholarPubMed
Graham, A. L., Cattadori, I. M., Lloyd-Smith, J. O., Ferrari, M. J. and Bjørnstad, O. N. (2007). Transmission consequences of coinfection: cytokines writ large? Trends in Parasitology 23, 284–291.CrossRefGoogle ScholarPubMed
Hasegawa, H., Kano, T. and Mulavwa, M. (1983). A parasitological survey on the feces of pygmy chimpanzees Pan paniscus at Wamba Zaire. Primates 24, 419–423.CrossRefGoogle Scholar
Howells, M. E., Pruetz, J. and Gillespie, T. R. (2011). Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: the case of sympatric western chimpanzees (Pan troglodytes verus) and Guinea baboons (Papio hamadryas papio) at Fongoli, Senegal. American Journal of Primatology 73, 173–179.CrossRefGoogle ScholarPubMed
Huffman, M. A., Gotoh, L., Turner, A., Hamai, M. and Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 115–125.CrossRefGoogle Scholar
Kooriyama, T., Hasegawa, H., Shimozuru, M., Tsubota, T., Nishida, T. and Iwaki, T. (2012). Parasitology of five primates in Mahale Mountains National Park, Tanzania. Primates 53, 365–375.CrossRefGoogle ScholarPubMed
Leggett, H. C., Brown, S. P. and Reece, S. E. (2014). War and peace: social interactions in infections. Philosophical Transactions of the Royal Society B: Biological Sciences 369, 20130365.CrossRefGoogle ScholarPubMed
Mafuyai, H., Barshep, Y., Audu, B., Kumbak, D. and Ojobe, T. (2013). Baboons as potential reservoirs of zoonotic gastrointestinal parasite infections at Yankari National Park, Nigeria. African Health Sciences 13, 252–254.Google ScholarPubMed
McGrew, W. C., Baldwin, P. J. and Tutin, C. E. G. (1981). Chimpanzees in a hot, dry and open habitat: Mt. Assirik, Senegal, West Africa. Journal of Human Evolution 10, 227–244.CrossRefGoogle Scholar
McGrew, W. C., Tutin, C. E. G., Collins, D. A. and File, S. K. (1989). Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). American Journal of Primatology 17, 147–155.CrossRefGoogle ScholarPubMed
McGrew, W. C., Baldwin, P. J., Marchant, L. F., Pruetz, J. D. and Tutin, C. E. G. (2014). Chimpanzees (Pan troglodytes verus) and their mammalian sympatriates: Mt. Assirik, Niokolo-Koba National Park, Senegal. Primates 55, 525–532.CrossRefGoogle ScholarPubMed
Miller, J. H. (1960). Papio doguera (dog face baboon), a primate reservoir of Schistosoma mansoni in East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 44–46.CrossRefGoogle ScholarPubMed
Muehlenbein, M. P. and Wallis, J. (2014). Considering risks of pathogen transmission associated with primate-based tourism. In Primate Tourism: A Tool for Conservation? (ed. Russon, A. E. and Wallis, J.), pp. 278–291. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Muriuki, S. M. K., Murugu, R. K., Munene, E., Karere, G. M. and Chai, D. C. (1998). Some gastro-intestinal parasites of zoonotic (public health) importance commonly observed in old world non-human primates in Kenya. Acta Tropica 71, 73–82.CrossRefGoogle ScholarPubMed
Murray, S., Stem, C., Boudreau, B. and Goodall, J. (2000). Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. Journal of Zoological and Wildlife Medicine 31, 176–178.Google Scholar
Pedersen, A. B. and Davies, T. J. (2010). Cross-species pathogen transmission and disease emergence in primates. EcoHealth 6, 496–508.CrossRefGoogle Scholar
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Petrášová, J., Modrý, D., Huffman, M., Mapua, M., Bobáková, L., Mazoch, V., Singh, J., Kaur, T. and Petrželková, K. (2010). Gastrointestinal parasites of indigenous and introduced primate species of Rubondo Island National Park, Tanzania. International Journal of Primatology 31, 920–936.CrossRefGoogle Scholar
Petrželková, K. J., Hasegawa, H., Appleton, C. C., Huffman, M. A., Archer, C. E., Moscovice, L., Mapua, M., Singh, J. and Kaur, T. (2010). Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. American Journal of Primatology 72, 307–316.CrossRefGoogle ScholarPubMed
Pick, F. (1951). Sur un nouveau trematode du genre Watsonius chez Papio sphinx . Bulletin de la Societe de Pathologie Exotique 44, 59–61.Google ScholarPubMed
Pomajbíková, K., Oborník, M., Horák, A., Petrželková, K. J., Grim, J. N., Levecke, B., Todd, A., Mulama, M., Kiyang, J. and Modrý, D. (2013). Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS Neglected Tropical Disease 7, e2140.CrossRefGoogle ScholarPubMed
Price, D. L. (1994). Procedure Manual for the Diagnosis of Intestinal Parasites. CRC, Boca Raton, FL, USA.Google Scholar
Pullan, R. L. and Brooker, S. J. (2012). The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasites and Vectors 5, 81.CrossRefGoogle ScholarPubMed
Ravasi, D., O'Riain, J., Adams, V. and Appleton, C. (2012). A coprological survey of protozoan and nematode parasites of free-ranging chacma baboons (Papio ursinus) in the Southwestern Cape, South Africa. South African Journal of Wildlife Research 42, 35–44.Google Scholar
Roberts, L. S. and Janovy, J. (2005). Foundations of Parasitology, 7th Edn. McGraw Hill, Boston, MA, USA.Google Scholar
Sa, R. M., Petrasova, J., PomajbÍkova, K., Profousova, I., Petrzelkova, K. J., Sousa, C., Cable, J., Bruford, M. W. and Modry, D. (2013). Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. American Journal of Primatology 75, 1032–1041.CrossRefGoogle ScholarPubMed
Sharman, M. J. (1981) Feeding, ranging and social organization of the Guinea baboon. Ph.D. thesis. University of St. Andrews, Scotland.Google Scholar
Stiles, C. W. and Goldberger, J. (1910). A Study of the Anatomy of Watsonius (n.g.) Watsoni of Man, Vol. 60. Hygienic Laboratory Bulletin, Government Printing Office, Washington, DC, pp. 264.Google Scholar
Toft, J. D. II and Eberhard, M. (1998). Parasitic diseases. In Nonhuman Primates in Biomedical Research: Diseases (ed. Bennett, B. T., Abee, C. R. and Henrickson, R.). Academic Press, New York.Google Scholar
Wallis, J. and Lee, D. R. (1999). Primate conservation: the prevention of disease transmission. International Journal of Primatology 20, 803–826.CrossRefGoogle Scholar
Weyher, A. H., Ross, C. and Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology 27, 1519–1534.CrossRefGoogle Scholar
Wolfe, N., Escalante, A., Karesh, W., Kilbourn, A., Spielman, A. and Lal, A. (1998). Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4, 149–158.CrossRefGoogle ScholarPubMed
Zommers, Z., Macdonald, D. W., Johnson, P. J. and Gillespie, T. R. (2013). Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes). Conservation Letters 6, 264–273.CrossRefGoogle Scholar