Skip to main content

Advertisement

Log in

Impact of Snare Injuries on Parasite Prevalence in Wild Chimpanzees (Pan troglodytes)

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

Abstract

Many primate populations are severely threatened by human activity. Illegal hunting with snares frequently causes fatal injuries and permanent mutilations in wild primates. Traumatic injuries and stressful experiences can reduce the efficacy of the immune system to fight parasitic infections. Snare-related changes in primate behavior may also influence the probability of exposure to parasites. We hypothesized that primates with permanent snare-related injuries would have a higher prevalence of intestinal parasites than control individuals. We tested the relationship between snare injuries and the prevalence of intestinal parasites in wild chimpanzees (Pan troglodytes) of Budongo forest, Uganda. We collected 487 fecal samples from known individuals (70 control and 20 snare-injured chimpanzees) and used flotation and sedimentation to isolate helminth eggs and an immunochromatographic assay to identify protozoan cysts. We found that the prevalence of Strongylida nematodes was significantly higher in snare-injured chimpanzees than in control individuals. In contrast, we found no association between snare injuries and three other parasite taxa: Ascaris, cestode, and Cryptosporidium parvum. Our study suggests that snare-injured primates may have higher exposure and/or be more susceptible to developing infections with helminth parasites than control individuals. Future studies should investigate whether snare injuries influence parasite prevalence in other species of wild primates.

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

  • Barrows, M. (1996). A survey of the intestinal parasites of the primates in Budongo Forest. Project for Glasgow University. Uganda: Glasgow University.

  • Byrne, R. W., & Stokes, E. J. (2002). Effects of manual disability on feeding skills in gorillas and chimpanzees. International Journal of Primatology, 23, 539–554.

    Article  Google Scholar 

  • Coe, C. L. (2012). Immunity in primates within a psychobiological perspective. In G. Demas & R. J. Nelson (Eds.), Ecoimmunology (pp. 144–164). Oxford: Oxford University Press.

    Google Scholar 

  • Davis, P. J. (2008). The immunology of wound healing: the body as a battlefield. Wounds UK, 4, 54–69.

    Google Scholar 

  • Fa, J. E., Ryan, S. F., & Bell, D. J. (2005). Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in Afrotropical forests. Biological Conservation, 121, 167–176.

    Article  Google Scholar 

  • Ghai, R.R., Fugère, V., Chapman, C.A., Goldberg, T.L., & Davies, T. J. (2015). Sickness behaviour associated with non-lethal infections in wild primates. Proceedings of the Royal Society of London B: Biological Sciences, 282. doi:10.1098/rspb.2015.1436.

  • Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology, 27, 1129–1143.

    Article  Google Scholar 

  • Hermans, V. (2011). Ranging behaviour of snare-injured female chimpanzees (Pan troglodytes schweinfurthii) of the Sonso community in the Budongo Forest, Uganda. MRes Primatology, University of Roehampton.

  • Hobaiter, C., & Byrne, R. W. (2010). Able-bodied wild chimpanzees imitate a motor procedure used by a disabled individual to overcome handicap. PLoS ONE, 5, e11959.

    Article  PubMed  PubMed Central  Google Scholar 

  • Janeway, J.A., Travers, P., Walport, M., & Shlomchik, M. (2001). The front line of host defense. In immunobiology: The immune system in health and disease (pp. 52–59). New York: New Garland Science.

  • Krief, S., Hladik, C. M., & Haxaire, C. (2005). Ethnomedicinal and bioactive properties of plants ingested by wild chimpanzees in Uganda. Journal of Ethnopharmacology, 101, 1–15.

    Article  PubMed  Google Scholar 

  • Matsubayashi, H., Yokogawa, M., Morishida, T., Ohosuru, M., Asami, K., et al. (1965). Handbook of parasitology. Tokyo: Asakura.

    Google Scholar 

  • Mugisha, L. (2004). A survey of gastrointestinal parasites of habituated wild chimpanzees (Pan troglodytes), humans and rodents in Budongo Forest Reserve. M.Sc. thesis, Makerere University.

  • Munn, J. (2006). Effects of injury on the locomotion of free-living chimpanzees in the Budongo Forest Reserve, Uganda. In N.E. Newton-Fisher, H. Notman, J.D. Paterson, & V. Reynolds (Eds.), Primates of western Uganda (pp. 259–280). Developments in Primatology: Progress and Prospects. New York: Springer Science + Business Media.

  • Mwavu, E. N., & Witkowski, E. T. F. (2008). Land-use and cover changes (1988–2002) around Budongo Forest Reserve, NW Uganda: implications for forest and woodland sustainability. Land Degradation & Development, 19, 606–622.

    Article  Google Scholar 

  • National Environment Management Authority. (2010). State of the environment report for Uganda 2010. Kampala: National Environment Management Authority.

    Google Scholar 

  • Noss, A. J. (1998). The impacts of cable snare hunting on wildlife populations in the forest of the Central African Republic. Conservation Biology, 12, 390–398.

    Article  Google Scholar 

  • Plumptre, A. J., & Reynolds, V. (1997). Nesting behavior of chimpanzees: implications for censuses. International Journal of Primatology, 18, 475–485.

    Article  Google Scholar 

  • R Core Team (2014). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/.

  • Reynolds, V. (2005). The chimpanzees of the Budongo forest: Ecology, behaviour, and conservation. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Sadd, B. M., & Schmid-Hempel, P. (2009). Principles of ecological immunology. Evolutionary Applications, 2, 113–121.

    Article  PubMed  Google Scholar 

  • Skrjabin, K.I., Shikhobalova, R.S., Schulz, T.I., Boev, S.N., & Dellyamure, S.L. (1952). Strongylata. In Key to parasitic nematodes III (pp. 883). Moscow: Akad.

  • Smith, R. (1995). Some effects of limb injuries on the chimpanzees of the Budongo Forest Budongo Forest Project Reports.

  • Stokes, E. J., & Byrne, R. W. (2001). Cognitive capacities for behavioural flexibility in wild chimpanzees (Pan troglodytes): The effect of snare injury on complex manual food processing. Animal Cognition, 4, 11–28.

    Article  Google Scholar 

  • Strait, K., Else, J. G., & Eberhard, M. L. (2012). Parasitic disease of nonhuman primates. In C. R. Abee, K. Mansfield, S. D. Tardif, & T. Morris (Eds.), Nonhuman primates in biomedical research: Diseases (2nd ed., pp. 197–297). San Diego: Academic.

    Chapter  Google Scholar 

  • Taylor, M.A., Coop, R.L., & Wall, R. (2007). Parasite taxonomy and morphology. In Veterinary parasitology (pp. 8–12). Oxford: Blackwell.

  • Tumusiime, D. M., Eilu, G., Tweheyo, M., & Babweteera, F. (2010). Wildlife snaring in Budongo Forest Reserve, Uganda. Human Dimensions of Wildlife, 15, 129–144.

    Article  Google Scholar 

  • Waller, J. (1995). The aetiologies of major limb injuries amongst chimpanzees in the Sonso area of the Budongo Forest, Uganda. M.Sc. thesis. University of Oxford.

  • Zommers, Z. (2010). Impact of human disturbance in Budongo Forest, Uganda, on four communities of chimpanzees. PhD thesis, Oxford University.

  • Zommers, Z., Macdonald, D. W., Johnson, P. J., & Gillespie, T. R. (2013). Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes). Conservation Letters, 6, 264–273.

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful for the support of the field assistants, staff, and researchers of the Budongo Conservation Field Station (BCFS). We thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this project. We thank the Royal Zoological Society of Scotland for providing core funding to the BCFS. We thank the ARCUS Foundation for funding the Chimpanzee Monitoring Programme. Funding for fieldwork was provided by the Institute of Biology and the Fonds des Donations of the University of Neuchâtel, as well as the M. Wüthrich and A. Mathey-Dupraz Foundation and an ERC grant (PRILANG 283871) to K. Zuberbühler. We thank the reviewers and the editor for their helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Harmony Yersin.

Ethics declarations

Conflict of Interest

The authors have no conflict of interest or any competing financial interest.

Ethical note

This research complied with ethical requierements for research involving animals as established by “Uganda Wildlife Authority” and “the Ugandan National Council for Science and Technology”.

Additional information

Handling Editor: Joanna M. Setchell

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 53 kb)

ESM 2

(DOCX 23 kb)

ESM 3

(DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yersin, H., Asiimwe, C., Voordouw, M.J. et al. Impact of Snare Injuries on Parasite Prevalence in Wild Chimpanzees (Pan troglodytes). Int J Primatol 38, 21–30 (2017). https://doi.org/10.1007/s10764-016-9941-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-016-9941-x

Keywords

Navigation