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Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates

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Recent evidence of emerging human diseases with origins or likely transmission to humans, or both, that involve primates and a greater recognition of the risk of human pathogen transmission to free-ranging primates have raised awareness of the potential impact of zoonotic pathogen transmission on primate conservation and nonhuman primate and human health. As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitats, greater human-primate contact is inevitable and even higher rates of pathogen transmission are likely. Thus interest has grown in collecting baseline data on patterns of parasitic infections in wild primate populations to provide an index of population health and to begin to assess and, to manage disease risks. Primatologists traditionally have been involved with such surveys through noninvasive assessment of gastrointestinal parasites. Unfortunately, previous studies have tended toward divergent methodologies, compromising the potential for longitudinal and comparative work. Here, I provide practical guidelines and standardized methodologies for the noninvasive assessment of gastrointestinal parasites of primates.

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Notes

  1. For samples from primates consuming large amounts of insect or vertebrate material or both, an ethyl acetate concentration step added at this point may improve results (OIE, 2004).

REFERENCES

  • Anderson, R. M., and May, R. M. (1979). Population biology of infectious-diseases, vol. 1. Nature 280: 361–367.

  • Anderson, R. M., and Schad, G. A. (1985). Hookworm burdens and faecal egg counts: An analysis of the biological basis of variation. Trans. Roy. Soc. Trop. Med. Hyg. 79: 812–825.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ashford, R. W., Reid, G. D. F., and Butynski, T. M. (1990). The intestinal faunas of man and mountain gorillas in a shared habitat. Ann. Trop. Med. Parasitol. 84: 337–340.

    PubMed  CAS  Google Scholar 

  • Ashford, R. W., Reid, G. D. F., and Wrangham, R. W. (2000). Intestinal parasites of the chimpanzee Pan troglodytes, in Kibale Forest, Uganda. Ann. Trop. Med. Parasit. 94: 173–179.

    Article  PubMed  CAS  Google Scholar 

  • Boyce, M. S. (1990). The red queen visits sage grouse leks. Am. Zool. 30: 263–270.

    Google Scholar 

  • Bush, A. O., Lafferty, K. D., Lotz, J. M., and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasit. 83(4): 575–583.

    Article  PubMed  CAS  Google Scholar 

  • Chandra, R. K., and Newberne, P. M. (1977). Nutrition, Immunity, and Infection, Plenum Press, New York.

  • Christensen, C. M., Barnes, E. H., Nansen, P., Roepstorff, A., and Slotved, H. C. (1995). Experimental Oesophagostomum dentatum infection in the pig: Worm populations resulting from single infections with three doses of larvae. Int. J Parasit. 25: 1491–1498.

    Article  CAS  Google Scholar 

  • Coadwell, W. J., and Ward, P. F. (1982). The use of faecal egg counts for estimating worm burdens in sheep infected with Haemonchus contortus. Parasitology 85: 251–256.

    PubMed  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 

  • Côté, I. M., and Poulin, R. (1995). Parasitism and group size in social animals: A meta-analysis. Behav. Ecol. 6: 159–165.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Despommier, D. D., Gwazda, R. W., and Hotez, P. J. (1995). Parasitic Diseases, Springer-Verlag, New York.

  • Dineen, J. K., Donald, A. D., Wagland, B. M., and Offner, J. (1965). The dynamics of the host-parasite relationship: The response of sheep to primary infection with Haemonchus contortus. Parasitology 55: 515–525.

    Article  Google Scholar 

  • Dobson, A. P., and Hudson, P. J. (1992). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse: 2 population models. J. Anim. Ecol. 61: 487–498.

    Article  Google Scholar 

  • Eberhard, M. L., Kovacs-Nace, E., Blotkamp, J., Verwij, J. J., Asigri, V. A., Polderman, A. M. (2001). Experimental Oesophagostomum bifurcum in monkeys. J. Helminthol. 75(1): 51–56.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Esch, G., and Fernandez, J. C. (1993). A Functional Biology of Parasitism: Ecological and Evolutionary Implications. Chapman and Hall, London.

  • Freeland, W. J. (1977). Dynamics of Primate Parasites. Ph.D. Dissertation. University of Michigan, Ann Arbor.

  • Freeland, W. J. (1779). Primate social groups as biological islands. Ecology 60: 719–728.

    Article  Google Scholar 

  • Freeland, W. J. (1980). Mangabey (Cercocebus albigena) movement patterns in relation to food availability and fecal contamination. Ecology 61: 1297–1303.

    Article  Google Scholar 

  • Freeland, W. J. (1981). Parasitism and behavioral dominance among male mice. Science 213: 461–462.

    Article  PubMed  CAS  Google Scholar 

  • Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., Cummins, L. B., Arthur, L. O., Peeters, M., Shaw, G. M., Sharp, P. M., and Hahn, B. H. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397: 436–441.

    Article  PubMed  CAS  Google Scholar 

  • Garber, P. A., and Kitron, U. (1997). Seed swallowing in tamarins: Evidence of a curative function or enhanced foraging efficiency? Int. J. Primatol. 18: 523–538.

    Article  Google Scholar 

  • Gilbert, K. A. (1997). Red howling monkey use of specific defecation sites as a parasite avoidance strategy. Anim. Behav. 54: 451–455.

    Article  PubMed  Google Scholar 

  • Gillespie, T. R. (2004). Effects of Human Disturbance on Primate-Parasite Dynamics. Ph.D. Dissertation. University of Florida, Gainesville.

  • Gillespie, T. R., and Chapman, C. A. (2006). Forest fragment attributes predict parasite infection dynamics in primate metapopulations. Cons. Biol. 20:441–448.

    Google Scholar 

  • Gillespie, T. R., Greiner, E. C., and Chapman, C. A. (2004). Gastrointestinal parasites of the guenons of western Uganda. J. Parasitol. 90: 1356–1360.

    Article  PubMed  Google Scholar 

  • Gillespie, T. R., Greiner, E. C., and Chapman, C. A. (2005a). Gastrointestinal parasites of the colobus monkeys of Uganda. J. Parasitol. 91: 569–573.

    Article  PubMed  Google Scholar 

  • Gillespie, T. R., Chapman, C. A., and Greiner, E. C. (2005). Effects of logging on gastrointestinal parasite infections and infection risk in African primate populations. J. Appl. Ecol. 42:699–707.

    Google Scholar 

  • Glander, K. E. (1994). Nonhuman primate self-medication with wild plant foods. In Etkin, N. L. (ed.), Eating on the Wild Side: The Pharmacological, Ecologic, and Social Implications of Using Noncultigens. University of Arizona Press, Tuscon, pp. 227–239.

  • 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 

  • Hausfater, G., and Meade, B. J. (1982). Alteration in sleeping groves by yellow baboons Papio cynocephalus) as a strategy for parasite avoidance. Primates 23: 287–297.

    Article  Google Scholar 

  • Hill, K., Boesch, C., Goodall, J., Pusey, A., Williams, J. and Wrangham, R. (2001). Mortality rates among wild chimpanzees. J. Hum. Evol. 40: 437–450.

    Article  PubMed  CAS  Google Scholar 

  • Hochachka, V. W., and Dhondt, A. A. (2000). Density-dependent decline of host abundance resulting from a new infectious disease. Proc. Natl. Acad. Sci. USA 97: 5303–5306.

    Article  PubMed  CAS  Google Scholar 

  • Hudson, P. J., Dobson, A. P., and Newborn, D. (1992). Do parasites make prey vulnerable to predation: Red grouse and parasites. J. Anim. Ecol. 61: 681–692.

    Article  Google Scholar 

  • Hudson, P. J., Dobson, A. P., and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282: 2256–2258.

    Article  PubMed  CAS  Google Scholar 

  • Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H., and Dobson, A. P. (2002). The Ecology of Wildlife Diseases, Oxford University Press, Oxford, UK.

  • Huffman, M. A. (1997). Current evidence for self-medication in primates: A multidisciplinary perspective. Yrbk. Phys. Anthropol. 40: 171–200.

    Article  Google Scholar 

  • Huffman, M. A., and Wrangham, R. W. (1994). Diversity of medicinal plant use by chimpanzees in the wild. In Wrangham, R. W., McGrew, W. C., deWaal, F. B. M., and Heltne, P. G. (eds.), Chimpanzee Cultures. Harvard University Press, Cambridge, pp. 129– 148.

  • Janzen, D. H. (1978). Complications in interpreting the chemical defenses of trees against tropical arboreal plant-eating vertebrates. In Montgomery, G. G. (ed), The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC, pp. 73–84.

  • Kalema-Zikusoka, G., Kock, R. A., and Macfie, E. J. (2002). Scabies in free-ranging mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Vet. Rec. 150: 12–15.

    PubMed  CAS  Google Scholar 

  • Leech, F. B., and Sellers, K. C. (1979). Statistical Epidemiology in Veterinary Science. Charles Griffen, London.

  • Leroy, E. M., Rouquet, P., Formenty, P., Souquiere, S., Kilbourne, A., Froment, J. M., Bermejo, M., Smit, S., Karesh, W., Swanepoel, R., Zaki, S. R., and Rollin, P. E. (2004). Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303: 387–390.

    Article  PubMed  CAS  Google Scholar 

  • Lilly, A. A., Mehlman, P. T., and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 23: 555–573.

    Article  Google Scholar 

  • Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M., and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists. J. Parasitol. 68(1): 131–133.

    Article  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 

  • MAFF (Ministry of Agriculture, Fisheries, and Food). (1979). Manual of Veterinary Parasitology Laboratory Techniques. Her Majesty’s Stationary Office, London, U.K.

  • Morand, S., and Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evol. Ecol. 12: 717–727.

    Article  Google Scholar 

  • Muller, R., and Baker, J. R. (1990). Medical Parasitology. Gower, London.

  • Müller-Graf, C. D., Collins, D. A., Packer, C., and Woolhouse, M. E. (1997). Schistosoma mansion infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 15: 621–627.

    Article  Google Scholar 

  • OIE (Office International des Epizooties). (2004). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Office International des Epizooties, Paris, France.

  • Ott-Joslin, J. E. (1993). Zoonotic diseases of nonhuman primates. In Fowler, M. E. (ed.), Zoo and Wild Animal Medicine. W. B. Saunders, Philadelphia, pp. 358–373.

  • Packer, C., Altizer, S., Appel, M., Brown, E., Martenson, J., O’Brien, S. J., Roelk-Parker, M., Hofmann-Lehmann, R., and Lutz, H. (1999). Viruses of the Serengeti: Patterns of infection and mortality in African lions. J. Anim. Ecol. 68: 1161–1178.

    Article  Google Scholar 

  • Packer, C., Holt, R. D., Hudson, P. J., Lafferty, K. D., and Dobson, A. P. (2003). Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol. Lett. 6: 1–6.

    Article  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  PubMed  CAS  Google Scholar 

  • Phillips-Conroy, J. E. (1986). Baboons, diet, and disease: Food plant selection and schistosomiasis. In Taub, D. M., and King, F. A. (eds.), Current Perspectives in Primate Social Dynamics. Van Nostrand Reinhold, New York, pp. 287–304.

  • Poulin, R. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities, Chapman and Hall, London.

  • Putt, S. N. H., Shaw, A. P. M., Woods, A. J., Tyler, L., and James, A. D. (1988). Veterinary Epidemiology and Economics in Africa—A Manual for Use in the Design and Appraisal of Livestock Health Policy, FAO, Rome.

  • Roepstorff, A., Bjørn, H., Nansen, P., Barnes, E. H., and Christensen, C. M. (1996). Experimental Oesophagostomum dentatum infections in the pig: Worm populations resulting from trickle infections with three dose levels of larvae. Int. J. Parasitol. 26: 399–408.

    Article  PubMed  CAS  Google Scholar 

  • Stear, M. J., Bishop, S. C., Doligalska, M., Duncan, J. L., Holmes, P. H., Irvine, J., McCririe, L., McKellar, Q. A., Sinski, E., and Murria, M. (1995). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasit. Immunol. 17(12): 643–652.

    CAS  Google Scholar 

  • Stoner, K. E. (1996). Prevalence and intensity of intestinal parasites in mantled howling monkeys (Alouatta palliata) in northeastern Costa Rica: Implications for conservation biology. Cons. Biol. 10: 539–546.

    Article  Google Scholar 

  • Stuart, M. D., Greenspan, L. L., Glander, K. E., and Clarke, M. R. (1990). A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. J. Wildlife Dis. 26: 547–549.

    CAS  Google Scholar 

  • Stuart, M. D., Pendergast, V., Rumfelt, S., Greenspan, L., Glander, K., and Clarke, M. (1998). Patterns of parasitism in wild howler monkeys, Alouatta spp., with observations from a long-term study of Alouatta palliata in Costa Rica. Int. J. Primatol. 19: 493–512.

    Article  Google Scholar 

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

    Google Scholar 

  • Stuart, M. D., Strier, K. B., and Pierberg, S. M. (1993). A coprological survey of parasites of wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. J. Helminthol. Soc. Wash. 60: 111–115.

    Google Scholar 

  • Tarazona, J. M. (1986). A method for the interpretation of parasite egg counts in faeces of sheep. Vet. Parasitol. 22(1–2): 113–119.

    Article  PubMed  CAS  Google Scholar 

  • 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 

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ACKNOWLEDGMENTS

I thank Ellis Greiner of the Department of Pathobiology, College of Veterinary Medicine, University of Florida; Tony Goldberg of the Department of Pathobiology, College of Veterinary Medicine, University of Illinois; Patricia Reed of the Wildlife Conservation Society Field Veterinary Program; and 2 anonymous reviewers for valuable comments on the manuscript.

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  1. Program in Ecology and Evolutionary Biology and Departments of Anthropology and Veterinary Pathobiology, University of Illinois, Urbana, IL, 61802, USA

    Thomas R. Gillespie

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Gillespie, T.R. Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates. Int J Primatol 27, 1129–1143 (2006). https://doi.org/10.1007/s10764-006-9064-x

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