Skip to main content

Advertisement

Log in

Gastrointestinal Parasites in Crop Raiding and Wild Foraging Papio anubis in Nigeria

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

We compared parasitic infection in a crop-raiding and a wild-foraging troop of olive baboons, Papio anubis, in Gashaka Gumti National Park, Nigeria, to quantify how crop raiding may have influenced primate-parasite interactions. We recovered gastrointestinal parasites from fecal samples from all adult individuals in both troops and processed them via formal-ether sedimentation. We compared parasitic species richness, prevalence, output, and load across troops. We recovered 9 parasite taxa. The wild-foraging troop had a significantly higher mean output than the crop-raiding troop for Physaloptera sp., Trichuris sp., and also a significantly higher total helminth load. The crop-raiding troop had a significantly higher mean output for the protozoan Balantidium coli and also showed a higher parasitic species richness, with 9 species recovered compared to the 7 recorded for the wild-foraging individuals. The changes in nutritional intake, behavior, and human proximity caused by crop raiding may have important epidemiological impacts on wild primate populations, and the nature of such impacts may vary across different taxa of parasites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

REFERENCES

  • Aickin, M. (1999) Other method for adjustment of multiple testing exists. Br. Med. J. 318: 127.

    CAS  Google Scholar 

  • Allen, A. V. H., and Ridley, D. S. (1970). Further observations in the formal-ether concentration technique for fecal parasites. J. Clin. Pathol. 23: 545–547.

    PubMed  CAS  Google Scholar 

  • Altmann, J., Schoeller, D., Altmann, S. A., Muruthi, P., and Sapolsky, R. M. (1993). Body size and fatness of free-living baboons reflect food availability and activity levels. Am. J. Primatol. 30: 149–161.

    Article  Google Scholar 

  • Anderson, R. M., and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite- induced host mortalities. Parasitology 85: 373–398.

    PubMed  Google Scholar 

  • Anderson, R. M., and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. J. Anim. Ecol. 47: 219–247.

    Article  Google Scholar 

  • Appleton, C. C., and Brain, C. (1995). Gastro-intestinal parasites of Papio cynocephalus ursinus in the central Namib desert, Namibia. Afr. J. Ecol. 33: 257–265.

    Google Scholar 

  • Appleton, C. C., and Henzi, S. P. (1993). Environmental correlates of gastrointestinal parasitism in montane and lowland baboons in Natal, South Africa. Int. J. Primatol. 14: 623–635.

    Article  Google Scholar 

  • Appleton, C. C., Henzi, S. P., Whiten, A., and Byrne, R. (1986). The gastrointestinal parasites of Papio ursinus from the Drakensberg mountains, Republic of South Africa. Int. J. Primatol. 7: 449–456.

    Google Scholar 

  • Appleton, C. C., Henzi, S. P., and Whitehead, S. I. (1991). Gastro-intestinal helminth parasites of the chacma baboon, Papio cynocephalus ursinus, from the coastal lowlands of Zululand, South Africa. Afr. J. Ecol. 29: 149–156.

    Google Scholar 

  • Ash, L. R., and Orthiel, T. C. (1997). Atlas of Human Parasitology, 4th edn. American Society of Clinical Parasitologists, Chicago.

    Google Scholar 

  • Box, H. O., ed. (1991). Primate Responses to Environmental Change. Chapman and Hall, London.

    Google Scholar 

  • Bundy, D. A. P., and Golden, M. H. N. (1987). The impact of host nutrition on gastrointestinal helminth populations. Parasitology 95: 623–635.

    PubMed  Google Scholar 

  • Chapman, C. A., Gillespie, T. R., and Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evol. Anthropol. 14: 134–144.

    Google Scholar 

  • Coop, R. L., and Holmes, P. H. (1996). Nutrition and parasite interaction. Int. J. Parasitol. 26: 951–962.

    Article  PubMed  CAS  Google Scholar 

  • Coop, R. L., and Kyriazakis, I. (1999). Nutrition-parasite interaction. Vet. Parasitol. 84: 187-204.

    PubMed  Google Scholar 

  • Cowlishaw, G. and Dunbar, R. I. M. (2000). Primate Conservation Biology. University of Chicago Press, Chicago.

    Google Scholar 

  • Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitol 62: 179–193.

    Google Scholar 

  • Crompton, D. W. T. (1987). Host diet as a determinant of parasite growth, reproduction and survival. Mamm. Rev. 17: 117–126.

    Google Scholar 

  • Daszak, P., Cunningham, A. A., and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287: 443–449.

    Article  PubMed  CAS  Google Scholar 

  • Dittus, W. P. J. (1974). The sociological basis for conservation of the toque monkey (Macaca sinica) of Sri Lanka (Ceylon). In Prince Rainer III HSH of Monaco, and Bourne GH (eds.), Primate Conservation. Academic Press, New York, pp. 238–267.

  • Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitol. 91: 317–347.

    Google Scholar 

  • Dunn, A. (1999). Gashaka Gumti National Park: A Guide Book. National Park Service of Nigeria, Lagos.

  • Eley, R. M., Strum, S. C., Muchemi, G., and Reid, G. D. F. (1989). Nutrition, body condition, activity patterns, and parasitism of free-ranging troops of olive baboons (Papio anubis) in Kenya. Am. J. Primatol. 18: 209–219.

    Article  Google Scholar 

  • Else, J. G., and Lee, P. C., eds. (1986). Primate Ecology and Conservation, Vol. 2. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Ezenwa, V. O. (2004). Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. Int. J. Parasitol. 34: 535– 542.

    Article  PubMed  Google Scholar 

  • Fa, J. E., and Southwick, C. H., eds. (1988). Ecology and Behavior of Food Enhanced Primate Groups. Alan R. Liss, New York.

    Google Scholar 

  • Foreyt, W. J. (2001). Veterinary Parasitology: Reference Manual, 5th edn. Iowa State University Press, Iowa.

    Google Scholar 

  • Formenty, P., Hatz, C., Le Guenno, B., Stoll, A., Rogonmoser, P., and WidmerHuman, A. (1999). Infection due to Ebola virus subtype Côte d’Ivoire. Clinical and biologic presentation. J. Infect. Dis. 179(Suppl 1): S48–53.

    PubMed  Google Scholar 

  • Fortham-Quick, D. L. (1984). Effects of the consumption of human foods on the activity budgets of two troops of baboons, Papio anubis at Gilgil, Kenya. Int. J. Primatol. 5: 339.

    Google Scholar 

  • Fortham-Quick, D. L., and Demment, M. W. (1988). Dynamics of exploitation: Differential energetic adaptation of two troops of baboons to recent human contact. In. Fa, J. E., and Southwick, C. H. (eds.), Ecology and Behavior of Food Enhanced Primate Groups. Alan R. Liss, New York.

    Google Scholar 

  • Freeland, W. J. (1979). Primate social groups as biological islands. Ecology 60: 719– 728.

    Article  Google Scholar 

  • Gao, F., Balles, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., Cummins, L., Artur, L. O., Peeters, M., Shaw, G. M., Sharp, P. M., and Hahn, B. H. (1999). Origin of HIV in the chimpanzee Pan troglodytes troglodytes. Nature 397: 436–444.

    Article  PubMed  CAS  Google Scholar 

  • Georges-Courbot, M., Sanchez, A., Lu, C., Baize, S., Leroy, E., Lansout-Soukate, J., Tevi-Benissan, C., Georges, A., Trappiers, S., Zaki, S., Swanepoel, R., Leman, P., Rollin, P., Peters, C., Nichols, S., and Ksiazek, T. (1997). Isolation and phylogenetic characterization of Ebola viruses causing different outbreaks in Gabon. Emerg. Infect. Dis. 3: 59–62.

    PubMed  CAS  Google Scholar 

  • Ghandour, A. M., Zahid, N. Z., Banaja, A. A., and Ghanem, A. (1999). Histopathological and parasitological changes in baboons (Papio hamadryas) experimentally infected with baboon and human isolates of Schistosoma mansoni from Saudi Arabia: A comparative study. Ann. Trop. Med. Parasitol. 93: 197–201.

    Article  PubMed  CAS  Google Scholar 

  • Ghandour, A. M., Zahid, N. Z., Banaja, A. A., Kamal, K. B., and Boug, A. I. (1995). Zoonotic intestinal parasites of hamdryas baboons Papio hamadryas in the western and northern regions of Saudi Arabia. J. Trop. Med. Hyg. 98: 431–439.

    PubMed  CAS  Google Scholar 

  • Goldsmid, J. M., and Rogers, S. (1978). A parasitological study on the chacma baboon (Papio ursinus) from the northern Transvaal. J. S. Afr. Vet. Assoc. 49: 109– 110.

    PubMed  CAS  Google Scholar 

  • Grenfell, B. T., and Gulland, F. M. D. (1995). Introduction: Ecological impact of parasitism on wildlife host populations. Parasitol 111: S3–S14.

    PubMed  Google Scholar 

  • Gregory, R. D., and Blackburn, T. M. (1991). Parasite prevalence and host sample size. Parasitol. Today 7: 316–318.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, R. D., and Hudson, P. J. (2000). Parasites take control. Nature 406: 33–34.

    Article  PubMed  CAS  Google Scholar 

  • Guyatt, H. L., and Bundy, D. A. P. (1990). Are wormy people parasite prone or just unlucky? Parasitol. Today 6: 282–283.

    Article  PubMed  CAS  Google Scholar 

  • Hahn, B. H., Shaw, G. M., DeCock, K. M., and Sharp, P. M. (2000). AIDS as a zoonosis: Scientific and public health implications. Science 287: 607–614.

    Article  PubMed  CAS  Google Scholar 

  • Hahn, N. E., Proulx, D., Muruthi, P. M., Alberts, S., and Altmann, J. (2003). Gastrointestinal parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis). Int. J. Primatol. 24: 271–279.

    Article  Google Scholar 

  • Hall, A. (1982). Intestinal helminths of man: The interpretation of egg counts. Parasitol 85: 605–613.

    PubMed  Google Scholar 

  • Hausfater, G., and Sutherland, R. (1984). Little things that tick off baboons. Nat. Hist. 2: 54–61.

    Google Scholar 

  • Hausfater, G., and Watson, D. F. (1976). Social and reproductive correlates of parasite ova emissions by baboons. Nature 262: 688–689.

    Article  PubMed  CAS  Google Scholar 

  • Higham, J., Ross, C., Warren, Y., MacLarnon, A., Sommer, V., and Adanu, J. (2005). 4 years of rainforest baboons at Gashaka. Primate Rep. 72: 46–47.

    Google Scholar 

  • Hill, C. M. (1997). Crop-raiding by wild vertebrates: The farmer's perspective in an agricultural community in western Uganda. Int. J. Pest. Manage. 43: 77–84.

    Article  Google Scholar 

  • Hirsch, V. M., Dapolito, G., McGann, C., Olmsted, R. A., Purcell, R. H., and Johnson, P. R. (1989). Molecular cloning of SIV from sooty mangabey monkeys. J. Med. Primatol. 18: 279–285.

    PubMed  CAS  Google Scholar 

  • Ivens, V. R., Mark, D. L., and Levine, N. D. (1978). Principal Parasites of Domestic Animals in the United States, Special Publication 52. College of Agriculture and Veterinary Medicine, University of Illinois, Urbana-Champaign.

  • Leventhall, R. and Cheadle, R. F. (1996). Medical Parasitology: A Self Instructional Text, 5th edn. F.A. Davis, Philadelphia.

    Google Scholar 

  • Lozano, G. A. (1991). Optimal foraging theory: A possible role for parasites. Oikos 60: 391–395.

    Article  Google Scholar 

  • Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F., and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365: 797–805.

    Article  PubMed  CAS  Google Scholar 

  • Maples, W. R., Maples, M. K., Greenwood, W. F., and Walek, M. L. (1976). Adaptations of crop raiding baboons in Kenya. Am. J. Phys. Anthropol. 45: 309–316.

    Article  Google Scholar 

  • Marsh, C. W., and Mittermeier, R. A. (1987). Primate Conservation in the Tropical Rain Forest. Alan R. Liss, New York.

    Google 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). Am. J. Primatol. 17: 147–155.

    Article  Google Scholar 

  • Moran, M. D. (2003). Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100: 403–405.

    Article  Google Scholar 

  • Muller-Graf, C. D. M. (1994). Ecological Parasitism of Baboons and Lions. PhD Thesis, University of Oxford.

  • Muller-Graf, C. D. M, Collins, D. A., Packer, C., and Woolhouse, M. E. J. (1997). Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 115: 621–627.

    Article  PubMed  Google Scholar 

  • Muller-Graf, C. D. M., Collins, D. A., and Woolhouse, M. E. J. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112: 489–497.

    PubMed  Google 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.

    Article  PubMed  CAS  Google Scholar 

  • 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. J. Zoo Wildlife Med. 31: 176–178.

    CAS  Google Scholar 

  • Naughton-Treves, L., Treves, A., Chapman, A. C., and Wrangham, R. (1998). Temporal patterns of crop raiding by primates: Linking food availability in croplands and adjacent forest. J. Appl. Ecol. 35: 596–606.

    Article  Google Scholar 

  • Nesheim, M. C. (1993). Human nutrition needs and parasitic infections. Parasitol. 107: S7–S18.

    Article  Google Scholar 

  • Noble, E. R., Noble, G. A., Schad, G. A., and MacInnes, A. J., eds. (1989). Parasitology: The Biology of Animal Parasites, 6th edn., Lea and Febiger, Philadelphia.

    Google Scholar 

  • Patz, J. A., Graczyk, T. K., Geller, N., and Vittor, A. Y. (2000). Effects of environmental change on emerging parasitic diseases. Int. J. Parasitol. 30: 1395–1405.

    Article  Google Scholar 

  • Perneger, T. V. (1998). What's wrong with Bonferroni adjustments. Br. Med. J. 316: 1236–1238.

    Google Scholar 

  • Rice, W. R. (1989) Analyzing tables of statistical tests. Evolution 43: 223–225.

    Article  Google Scholar 

  • Scott. M. E. (1988). The impact of infection and disease on animal populations: implications for conservation biology. Cons. Biol. 2: 40–56.

    Article  Google Scholar 

  • Stephenson, L. S. (1987). Impact of Helminth Infections on Human Nutrition. Taylor and Francis, London.

    Google Scholar 

  • Stuart, M. D., Greenspan, L. L., Glander, K. E., and Clarke, M. R. (1990). A corporlogical survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. J. Wildlife Dis. 26: 347–349.

    Google Scholar 

  • Stuart, M., Pendergast, V., Rumfelt, S., Pierberg, S., Greenspan, L., Glander, K., and Clarke, M. (1998). Parasites of wild howlers (Alouatta spp.). Int. J. Primatol. 19: 493–512.

    Article  Google Scholar 

  • Stuart, M. D., and Strier, K. B. (1995). Primates and parasites: A case study for a multidisciplinary approach. Int. J. Primatol. 16: 577–593.

    Google Scholar 

  • Wakelin, D. (1987). Parasite survival and variability in host immune responsiveness. Mamm. Rev. 17: 135–141.

    Google Scholar 

  • Wakelin, D. (1996) Immunity to Parasites: How Parasitic Infections Are Controlled 2nd edn. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Wallis, J., and Rick Lee, D. (1999) Primate conservation: The prevention of disease transmission. Int. J. Primatol. 20: 803–826.

    Article  Google Scholar 

  • Warren, Y. (2003). Olive Baboons (Papio cynocephalus anubis): Behaviour, Ecology, and Human Conflict in Gashaka Gumti National Park, Nigeria. Unpublished PhD Thesis, University of Surrey Roehampton.

  • Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A., and Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: The missing link? Emerg. Infect. Dis. 4: 149–158.

    Article  PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

We thank the Nigerian authorities; the National Parks Service of Nigeria, through the Conservator General Alhaji Lawan B. Marguba; and the staff and management of Gashaka Gumti National Park and NCF/WWF-UK for their support. Many people, including our field assistants, Bobbo Buba and Nuhu, assisted with the field work. We thank Volker Sommer (UCL) for help and support through the Gashaka Primate Project and James Higham for invaluable assistance in the field. We thank John Williams and Claire Rogers of the London School of Hygiene and Tropical Medicine for training in parasitological analysis. Without the support and expertise of all of these people, the project would not have been possible. We also thank Dr. Colin Chapman and 2 anonymous reviewers for their constructive criticism of the article. Grants from The Leakey Trust, the North of England Zoological Society, and Roehampton University partially funded the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna H. Weyher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weyher, A.H., Ross, C. & Semple, S. Gastrointestinal Parasites in Crop Raiding and Wild Foraging Papio anubis in Nigeria. Int J Primatol 27, 1519–1534 (2006). https://doi.org/10.1007/s10764-006-9089-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-006-9089-1

KEY WORDS

Navigation