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Noninvasive Monitoring of the Health of Pan troglodytes schweinfurthii in the Kibale National Park, Uganda

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Abstract

We assessed the health status of chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara group in the Kibale National Park in Western Uganda via noninvasive methods. We conducted visual veterinary inspection, parasitological and urine analysis in association with behavioral observations, causing minimal disturbance or stress to individually recognized chimpanzees. We applied multiple parasitological techniques to 252 stool samples to compare their efficacy in detecting parasitic infection and to increase the power of detecting a wide range of parasites at a more sensitive level. We examined 76 urine samples via a quick detection method to evaluate multiple parameters of urine that indicate organ dysfunction. Results of the different analyses are mutually supportive and provided useful information for monitoring bodily condition and diseases. The multifaceted health evaluation system is a beneficial tool for monitoring long-term and short-term changes in health status due to environmental stress, seasonal dietary change, and disease in wild chimpanzee populations. Use of this method to detect changes in health, when employed together with behavioral observations, may also provide important insights into the potential effects of self-medicative behaviors.

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References

  • Alados, C. L., and Huffman, M. A. (2000). Fractal long-range correlations in behavioural sequences of wild chimpanzees: a non-invasive analytical tool for the evaluation of health. Ethology 106: 105–116.

    Google Scholar 

  • Altmann, J. (1974). Observational study of behavior; sampling methods. Behaviour 48: 1–41.

    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. Parasitol. 94: 173–179.

    PubMed  CAS  Google Scholar 

  • Bailanger, J. (1973). Coprologie parasitaire et fonctionnelle. Imprimerie E. Drouillard, Bordeaux, France.

    Google Scholar 

  • Bailes, E., Gao, F., Bibolet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P. A., Hahn, B. H., and Sharp, P. M. (2003). Hybrid Origin of SIV in chimpanzees. Science 300(13): 1713

    PubMed  CAS  Google Scholar 

  • Balagizi Karhagomba, I., and Ntumba Kayembe, F. (1998). Plantes utilisées dans le traitement des helminthoses gastro-intestinales des petits ruminants dans le groupement d’Irhambi-Katana (Région du Bushi, Province du Sud-Kivu, RDC). Rech. Afr. 1: 90–99.

    Google Scholar 

  • Bouquet, A. (1969). Féticheurs et médecines traditionnelles du Congo (Brazzaville). Mémoire O.R.S.T.O.M.

    Google Scholar 

  • Collet, J.-Y., Bourreau, E., Cooper, R. W., Tutin, C. E. G., and Fernandez, M. (1984). Experimental demonstration of cellulose digestion by Troglodytella gorillae, an intestinal ciliate of lowland gorillas (Gorilla g. gorilla). Int. J. Primatol. 5: 328.

    Google Scholar 

  • Cotard, J.-P. (1993). Néphrologie et urologie du chien et du chat. CNVSPA, Paris.

    Google Scholar 

  • Cousins, D., and Huffman, M. A. (2002). Medicinal properties in the diet of gorillas- an ethnopharmacological evaluation. Afr. Stud. Monogr. 3: 65–89.

    Google Scholar 

  • Daszak, P., Cunningham, A. A., and Hyatt, A. D. (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78: 103–116

    PubMed  CAS  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  CAS  PubMed  Google Scholar 

  • Defour, G. (1994). Plantes médicinales traditionnelles au Kivu (République du Zaïre). Documentation du sous-réseau Prélude.

  • De Groot, N. G., Otting, N., Doxiadis, G. G. M., Balla-Jhagjhoorsingh, S. S., Heeney, J. L., Rood, J. J., Gagneux, P., and Bontrop, R. E. (2002) Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proce. Nat. Acad. Sci. 99(18): 11748–11753.

    CAS  Google Scholar 

  • Dupain, J., Van Elsacker, L., Nell, C., Garcia, P., Ponce, F., and Huffman, M. A. (2002). New evidence for leaf swallowing and Oesophagostomum infection in Bonobos (Pan paniscus). Int. J. Primatol. 23(5): 1053–1062.

    Google Scholar 

  • File, S. K., Mc Grew, W. C., and Tutin, C. E. G. (1976). The intestinal parasites of a community of feral chimpanzees, Pan troglodytes schweinfurthii. J. Parasitol. 62: 259–261.

    PubMed  CAS  Google Scholar 

  • Froment, A. (2001). Santé et nutrition des régions forestières. In Bahuchet, S., De Maret, P., Grenand, F., and Grenand, P. (eds.), Des forêts et des hommes, un regard sur les peuples des forêts tropicales, APFT-ULB, Bruxelles, pp. 177–186.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Healy, G. R., and Myers, B. J. (1973). Intestinal helminths. In Bourne, G. M. (ed.), The Chimpanzee, vol. 6, Bassel: Karger, pp. 265–296.

    Google Scholar 

  • Hercberg, S., Chauliac, M., Galan, P., Devanlay, M., Zohoun, I., Agboton, Y., Soustre, Y., Bories, C., Christides, J.-P., Potier de Courcy, G., Masse-Raimbault, A. M., and Dupin, H. (1986). Relationship between anaemia, iron and folacin deficiency, haemoglobinopathies and parasitic infection. Human Nutrition: Clini Nut. 40 C: 371–379.

    Google Scholar 

  • Heine, B., and König, C. (1988). Plant concepts and plant use. An ethnobotanical survey of the semi-arid and arid lands of East Africa. Part 2: plants of the So (Uganda). Cologne development Studies Verlag Breitenbach Publishers, Saarbrücken, Fort Lauderdale.

    Google Scholar 

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

    Google Scholar 

  • Huffman, M. A., and Seifu, M. (1989). Observations of illness and consumption of a possibly medicinal plant Vernonia amygdalina (Del.), by a wild chimpanzee in the Mahale Mountains National Park, Tanzania. Primates 30(1): 51–63.

    Google Scholar 

  • Huffman, M. A., Gotoh, S., Isutzu, D., Koshimizu, K., and Kalunde, M. S. (1993). Further observations on the use of medicinal plant, Vernonia amygdalina (Del.) by a wild chimpanzee, its possible effect on parasite load and its phytochemistry. Afr. Stud. Monogr. 14: 227–240.

    Google Scholar 

  • Huffman, M. A., Page, J. E., Sukhdeo, M. V. K., Gotoh, S., Kalunde, M. S., Chandrasiri, T., and Towers, G. H. N. (1996). Leaf swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections. Int. J. Primatol. 72: 475–503.

    Google Scholar 

  • Huffman, M. A., Gotoh, S., Turner, L., and Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38(2): 111–125.

    Google Scholar 

  • Huffman, M. A., Ohigashi H., Kawanaka, M., Page, J. E., Kirby G. C., Gasquet, M., Murakami, A., and Koshimizu, K. (1998). African great ape self-medication: A new paradigm for treating parasite disease with natural medicines. In Ebizuka, Y. (ed.), Towards Natural Medicine Research in the 21st Century, Elsevier Science B. V., Amsterdam, pp. 113–123.

    Google Scholar 

  • Huffman, M. A., and Hirata, S. (2004). An experimental study of leaf swallowing in captive chimpanzees: insights into the origin of a self-medicative behavior and the role of social learning. Primates 45: 113–118.

    PubMed  Google Scholar 

  • Huffman, M. A., and Caton, J. M. (2001). Self-induced increase of gut mobility and the control of parasitic infections in wild chimpanzees. Int. J. Primatol. 22: 329–346.

    Google Scholar 

  • Jessee, M. T., Shilling, P. W., and Stunkard, J. A. (1970). Identification of intestinal eggs in old world Primates. Lab. Anim. Care 20: 83–87.

    PubMed  CAS  Google Scholar 

  • Jisaka, M., Ohigashi, H., Takagaki, T., Nozaki, H., Tada, T., Hirota, M., Irie, R., Huffman, M. A., Nishida, T., Kaji, M., and Koshimizu, K. (1992). Bitter steroid glucosides, Vernoniosides A1, A2 and A3 and related B1 from a possible medicinal plant Vernonia amygdalina, used by wild chimpanzees. Tetrahedron 48: 625–632.

    CAS  Google Scholar 

  • Kaur, T., and Huffman, M. A. (2004). Descriptive urological record of chimpanzees (Pan troglodytes) in the wild and limitations associated with using multi-reagent dipstick test strips. J. Med. Primatol. 33(4): 187–196.

    PubMed  Google Scholar 

  • Kawabata, M., and Nishida, T. (1991). A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania. Primates 32: 275–278.

    Google Scholar 

  • Kelly, T. R., Sleeman, J. M., and Wrangham, R. W. (2004). Urinalysis in free-living chimpanzees (Pan troglodytes schweinfurthii) in Uganda. Veterinary Record 154(23): 729–730.

    PubMed  CAS  Google Scholar 

  • Knezevich, M. (1998). Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rheus macaques (Macaca mulatta). Am. J. Primatol. 44: 71–82.

    PubMed  CAS  Google Scholar 

  • Krief, S. (2003). Métabolites secondaires des plantes et comportement animal: surveillance sanitaire et observations de l’alimentation de chimpanzés (Pan troglodytes schweinfurthii) en Ouganda. Activités biologiques et étude chimique de plantes consommées. Thèse de Doctorat du Museum National d’Histoire Naturelle, Paris. 375 p.

    Google Scholar 

  • Krief, S., Jamart, A., and Hladik, C. M. (2004a). On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45(2): 141–145.

    Google Scholar 

  • Krief, S., Martin, M.-T., Grellier, P., Kasenene, J., and Sévenet, T. (2004b). Novel antimalarial compounds isolated in a survey of self-medicative behavior of wild chimpanzees in Uganda. Antimicrob. Age. Chemother. 48(8): 3196–3199.

    CAS  Google Scholar 

  • Krief, S., Huffman, M. A., Sévenet, T., Hladik, C.-M., Grellier, P., Loiseau, P., and Wrangham, R. W. (submitted). Bioactive properties of plants ingested by chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, Uganda.

  • Landsoud-Soukate, J., Tutin, C. E. G., and Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Réserve, Gabon, Ann. Trop. Med. Parasitol. 89: 73–79.

    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.

    Google Scholar 

  • Lozano, G. A. (1998). Parasitic stress and self-medication in wild animals. In Møller, P. A., Milinski, M., and Slater, P. J. B. (eds.), Adv. Study Behav. Acad. Lond. 27: 291–317.

    Article  Google Scholar 

  • Magliocca, F., Quérouil, S., and Gautier-Hion, A. (2003). Seed eating in elephant dung by two large mammals in the Congo Republic. Rev. Ecol. 58: 143–149.

    Google Scholar 

  • Mahaney, W. C., Watts, D. P., and Hancock, R. G. V. (1990). Geophagia by Mountain Gorillas (Gorilla gorilla beringei) in the Virunga Mountains, Rwanda. Primates 31: 113–120.

    Google Scholar 

  • Mahaney, W. C., Aufreiter, S., and Hancock, R. G. V. (1995a). Mountain Gorilla Geophagy: a possible seasonal behavior for dealing with the effects of dietary changes. Int. J. Primatol. 16: 475–488.

    Article  Google Scholar 

  • Mahaney, W. C., Stambolic, A., Knezevich, M., Hancock, R. G. V., Aufreiter, S., Sanmugadas, K., Kessler, M., and Grynpas, M. (1995b). Geophagy amongst rhesus macaques on Cayo Santiago, Puerto Rico. Primates 36: 323–334.

    Google Scholar 

  • Mahaney, W. C., Milner, M. C., Hancock, R. G. V., Aufreiter, S., Wrangham, R. W., and Pier, H. W. (1997). Analysis of geophagy soils in Kibale Forest, Uganda. Primates 38(2): 159–176.

    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.

    Google Scholar 

  • Meffe, G. (1999). Conservation Medicine. Con Bio 13: 953–954

    Google Scholar 

  • Messner, E. J., and Wrangham, R. W. (1996). In vitro testing of the biological activity of Rubia cordifolia leaves on primate Strongyloides species. Primates 37(1): 105–108.

    Google Scholar 

  • Myers, B. J., and Kuntz, R. E. (1972). A checklist of Parasites and commensals reported for chimpanzee (Pan). Primates 13: 433–471.

    Google Scholar 

  • O’Donoghue, P. J., Gasser, R. B., and Tribe, A. (1993). New host record for the entodiniomorph ciliate, Troglodytella abrassarti, from Siamangs (Hylobates syndactylus). Int. J. Parasitol. 23(3): 415–418.

    PubMed  Google Scholar 

  • Ohigashi, H., Huffman, M. A., Izutsu, D., Koshimizu, K., Kawanaka, M., Sugiyama, H., Kirby, G. C., Warhurst, D. C., Allen, D., Wright, C. W., Phillipson, J. D., Timmon-David, P., Delmas, F., Elias, R., Balansard, G. (1994). Toward the chemical ecology of medicinal plant-use in chimpanzees: The case of Vernonia amygdalina (Del.). A plant used by wild chimpanzees possibly for parasite-related diseases. J. Chem. Ecol. 20(3): 541–553.

    CAS  Google Scholar 

  • Santiago, M. L., Rodenburg, C. M., Kamenya, S., Bibollet–ruche, F., Gao, F., Bailes, E., Meleth, S., Soong, S.-J., Kilby, J. M., Modoveanu, Z., Fahey, B., Muller, M. N., Ayouba, A., Nerrienet, E., McClure H. M., Heeney, J., Pusey, A. E., Collins, D. A., Boesch, C., Wrangham, R. W., Goodall, J., Sharp, P. M., Shaw, G. M., and Hahn, B. H. (2002). SIVcpz in wild chimpanzees. Science 295: 465.

    PubMed  CAS  Google Scholar 

  • Van Riper, D. C., Day, P. W., Fineg, J., and Prine, J. R. (1966). Intestinal parasites of recently imported chimpanzees. Lab. Anim. Care 16: 360–363.

    PubMed  CAS  Google Scholar 

  • Walsh C. F., et al. (2003). Catastrophic Ape decline in western equatorial Africa. Nature 422: 611–614.

    PubMed  CAS  Google Scholar 

  • Wrangham, R. W., and Nishida, T. (1983). Aspilia spp. leaves: a puzzle in the feeding behavior of wild chimpanzees. Primates 24(2): 276–282.

    Google Scholar 

  • Wrangham, R. W. (1995). Leaf-swallowing by chimpanzees and its relationship to tapeworm infection. Am. J. Primatol. 37: 297–304.

    Google Scholar 

  • Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., and Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great ape groups. In McGrew, W. C., Marchant, L. F., and Nishida, T. (eds.), Great Ape Societies, Cambridge University Press, Cambridge, pp. 45–57.

    Google Scholar 

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Krief, S., Huffman, M.A., Sévenet, T. et al. Noninvasive Monitoring of the Health of Pan troglodytes schweinfurthii in the Kibale National Park, Uganda. Int J Primatol 26, 467–490 (2005). https://doi.org/10.1007/s10764-005-2934-9

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  • DOI: https://doi.org/10.1007/s10764-005-2934-9

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