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Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania

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Abstract

A longitudinal study of nematode infection in chimpanzees was conducted between 1989 and 1994 on the M group chimpanzees of the Mahale Mountains National Park, Tanzania during two annual dry and rainy season periods and a third rainy season. Chemical and physical antiparasite properties of medicinal plant use against the strongyle nematodeOesophagostomum stephanostomum have recently been reported at Mahale. Here, the incidence of nematode infections were analyzed for seasonal trends to elucidate the possible influence of parasite infection on previously reported seasonality of medicinal plant use and to test the hypothesis that the use of these plants is stimulated byO. stephanostomum. The number of chimpanzees infected byO. stephanostomum was significantly higher in the rainy season than in the dry season of both 1989–1990 and 1991–1992. However, the incidence ofTrichuris trichura andStrongyloides fuelleborni showed no seasonality. Reinfection of individuals byO. stephanostomum occurred in synchrony with annual variation in rainfall: there was a sharp rise in the occurrence of new infections per individual within one to two months after the beginning of the first heavy rains of the season. This pattern coincides with the reproductive cycle of this nematode species.O. stephanostomum (95%) infections were associated significantly more frequently with medicinal plant use than eitherT. trichiura (50%) orS. fuelleborni (40%) infections. These observations are consistent with previous reports for the increased use of these plants during the rainy season and are consistent the hypothesis that medicinal plant use is stimulated byO. stephanostomum infection.

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References

  • Allison, A. C. 1982. Co-evolution between hosts and infectious disease agents and its effect on virulence. In:Population Biology of Infectious Diseases,Anderson,R. M.;May,R. M. (eds.), Springer-Verlag, Berlin, pp. 245–267.

    Google Scholar 

  • Anderson, R. C. 1992.Nematode Parasites of Vertebrates: Their Development and Transmission. C.A.B. International, Walingford.

    Google Scholar 

  • Anderson, R. M.;May, R. M. 1982.Population Biology of Infectious Diseases. Springer-Verlag, Berlin.

    Google Scholar 

  • Ash, L. R.;Orihel, T. C. 1987.Parasites: A Guide to Laboratory Procedures and Identification. Amer. Society of Clinical Pathologists Press, Chicago.

    Google Scholar 

  • Beaver, P. C.;Jung, R. C.;Cupp, E. W. 1984.Clinical Parasitology (9th ed.). Lea & Febiger, Philadelphia.

    Google Scholar 

  • Behnke, J. M. 1987. Evasion of immunity by nematode parasites causing chronic infections.Adv. Parasitol., 26: 1–71.

    CAS  PubMed  Google Scholar 

  • Bernard, C. J.;Behnke, J. M. 1990.Parasitism and Host Behaviour. Taylor & Francis, London.

    Google Scholar 

  • Brack, M. 1987.Agents Transmissible from Simians to Man. Springer-Verlag, Berlin.

    Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Freeland, W. J. 1980. Mangabey (Cercocebus albigena) movement patterns in relation to food availability and fecal contamination.Ecology, 61(6): 1297–1303.

    Google Scholar 

  • Futuyma, D. J.;Slatkin, M. 1983.Coevolution. Sinauer Associates, Sunderland.

    Google Scholar 

  • Georgi, J. R. 1985.Parasitology for Veterinarians. Saunders, Philadelphia.

    Google Scholar 

  • Goodall, J. 1983. Population dynamics during a 15 year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania.Z. Tierpsychol., 61: 1–60.

    Google Scholar 

  • Hamilton, W. D. 1964a. The genetical evolution of social behavior, I.J. Theoret. Biol., 7: 1–16.

    CAS  Google Scholar 

  • Hamilton, W. D. 1964b. The genetical evolution of social behavior, II.J. Theoret. Biol., 7: 17–52.

    CAS  Google Scholar 

  • Hamilton, W. D.;Zuk, M. 1982. Heritable true fitness and bright birds: a rule for parasites?Science, 218: 384–387.

    CAS  PubMed  Google Scholar 

  • Hart, B. 1990. Behavioral adaptations to pathogens and parasites: five strategies.Neurosi. Behav. Rev., 14: 273–294.

    CAS  Google Scholar 

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

    Google Scholar 

  • Hill, A. 1985. Nutritional aspects of parasite infection.Prog. Food Nut. Sci., 9: 227–256.

    Google Scholar 

  • Hiraiwa-Hasegawa, M.;Hasegawa, T.;Nishida, T. 1984. Demographic study of a large-sized unitgroup of chimpanzees in the Mahale Mountains, Tanzania: a preliminary report.Primates, 25: 401–413.

    Google Scholar 

  • Huffman, M. A. 1993. An investigation of the use of medicinal plants by wild chimpanzees: current status and future prospects.Prim. Res., 9: 179–187.

    Google Scholar 

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

    Google Scholar 

  • Huffman, M. A.;Nishida, T.;Uehara, S. 1990. Intestinal parasites and medicinal plant use in wild chimpanzees: possible behavioral adaptation for the control of parasites. In:Mahale Mountains Chimpanzee Research Project, Ecological Rept. (No. 72), Kyoto Univ., Kyoto.

    Google Scholar 

  • Huffman, M. A.;Page, J. E.;Sukhdeo, M. V. K.;Gotoh, S.;Kalunde, M. S.;Chandrasiri, T.;Towers, G. H. N. 1996. Leaf-swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections.Int. J. Primatol., 17: 475–503.

    Google Scholar 

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

    Google Scholar 

  • Huffman, M. A.;Wrangham, R. W. 1994. The diversity of medicinal plant use by chimpanzees in the wild. In:Chimpanzee Cultures,Wrangham,R. W.;McGrew,W. C.;DeWaal,F. B.;Heltne,P. G. (eds.), Harvard Univ. Press, Cambridge, Massachusetts, pp. 129–148.

    Google Scholar 

  • Jisaka, M.;Kawanaka, M.;Sugiyama, H.;Takegawa, K.;Huffman, M. A.;Ohigashi, H.;Koshimizu, K. 1992. Antischistosomal activities of sesquiterpene lactones and steroid glucosides fromVernonia amygdalina, possibly used by wild chimpanzees against parasiterelated diseases.Biosci. Biotech. Biochem., 56: 845–846.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • McGrew, W. C.;Tutin, C. E. G.;Collins, D. A.;File, S. K. 1989. Intestinal parasites of sympatricPan troglodytes andPapio spp. at two sites: Gombe (Tanzania) and Mt. Assirik.Amer. J. Primatol., 17: 147–155.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nelson, G. S. 1960. Schistosome infections as zoonoses in Africa.Transcrip. Royal Soc. Trop. Med. Hyg., 54: 301–314.

    CAS  Google Scholar 

  • Nishida, T. 1990. A quarter century of research in the Mahale Mountains: an overview. In:The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies,Nishida,T. (ed.), Univ. of Tokyo Press, Tokyo, pp. 3–35.

    Google Scholar 

  • Nishida, T.;Nakamaura, M. 1993. Chimpanzee tool use to clear a blocked nasal passage.Folia Primatol., 61: 218–220.

    CAS  PubMed  Google Scholar 

  • Nishida, T.;Takasaki, H.;Takahata, Y. 1990. Demography and reproductive profiles. In:The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies,Nishida,T. (ed.), Univ. of Tokyo Press, Tokyo, pp. 63–97.

    Google Scholar 

  • Nishida, T.;Uehara, S. 1983. Natural diet of chimpanzees (Pan troglodytes): long-term record from the Mahale Mountains, Tanzania.Afr. Stud. Monogr., 3: 109–130.

    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.;Delnas, F.;Elias, R.;Balansard, G. 1994. Toward the chemical ecology of medicinal plantuse in chimpanzees: the case ofVernonia amygdalina (Del.), a plant used by wild chimpanzees possibly for parasite-related diseases.J. Chem. Ecol., 20: 541–553.

    Article  CAS  Google Scholar 

  • Ohigashi, H.;Takagaki, T.;Koshimizu, K.;Watanabe, K.;Kaji, M.;Hoshino, J.;Nishida, T.;Huffman, M. A.;Takasaki, H.;Jato, J.;Muanza, D. M. 1991. Biological activities of plant extracts from tropical Africa.Afr. Stud. Monogr., 12(4): 201–210.

    Google Scholar 

  • Page, J. E.;Balza, F.;Nishida, T.;Towers, G. H. N. 1992. Biologically active diterpenes fromAspilia mossambicensis, a chimpanzee medicinal plant.Phytochem., 31: 3437–3439.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Phillips-Conroy, J. E.;Knopf, P. M. 1986. The effects of ingesting plant hormones on schistosomiasis in mice: an experimental study.Biochem. System. Ecol., 14: 637–645.

    CAS  Google Scholar 

  • Price, P. W. 1980.Evolutionary Biology of Parasitism. Princeton Univ. Press, Princeton.

    Google Scholar 

  • Rodriguez, E.;Wrangham, R. W. 1993. Zoopharmacognosy: the use of medicinal plants by animals. In:Phytochemical Potentials of Tropical Plants,Downum,K. R.;Romeo,J. T.;Stafford,H. A. (eds.), Plenum Press, New York, pp. 89–105.

    Google Scholar 

  • Sharman, M. J. 1981. Feeding, ranging and social organization of the Guinea baboon. Ph.D. thesis, Univ. of St. Andrews.

  • Takasaki, H.;Nishida, T.;Uehara, S.;Norikoshi, K.;Kawanaka, K.;Takahata, Y.;Hiraiwa-Hasegawa, M.;Hasegawa, T.;Hayaki, H.;Masui, K.;Huffman, M. A. 1990. Appendix: summary of meteorological data at Mahale Research Camps, 1973–1988. In:The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies, Nishida, T. (ed.), Univ. of Tokyo Press, Tokyo, pp. 291–300.

    Google Scholar 

  • Toft, C. A.;Aeschlimann, A.;Bolis, L. 1991.Parasite-Host Associations: Coexistence or Conflict? Oxford Science Publ., Oxford.

    Google Scholar 

  • Towers, G. H. N.;Abramowski, Z.;Finlayson, A. J.;Zucconi, A. 1985. Antibiotic properties of thiarubrine-A, a naturally occurring dithiacyclohexadiene polyine.Planta Medica, 3: 225–229.

    PubMed  Google Scholar 

  • Uehara, S.;Nyundo, R. 1983. One observed case of temporary adoption of an infant by unrelated nulliparous females among wild chimpanzees in the Mahale Mountains, Tanzania.Primates, 24: 456–466.

    Google Scholar 

  • Wrangham, R. M. 1995. Leaf-swallowing by chimpanzees, and its relation to a tapeworm infection.Amer. J. Primatol., 37: 297–303.

    Article  Google Scholar 

  • Wrangham, R. W.;Goodall, J. 1989. Chimpanzee use of medicinal leaves. In:Understanding Chimpanzees,Heltne,P. G.;Marquardt,L. A. (eds.), Harvard Univ. Press, Cambridge, Massachusetts, pp. 22–37.

    Google Scholar 

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

    Google Scholar 

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Author notes

  1. Michael A. Huffman & Shunji Gotoh

    Present address: Primate Research Institute, Kyoto University, Kanrin, Inuyama, 484, Aichi, Japan

  2. Linda A. Turner

    Present address: Faculty of Science, Kyoto University, Sakyo-ku, 606-01, Kyoto, Japan

  3. Miya Hamai

    Present address: Japan Monkey Centre, Kanrin, Inuyama, 484, Aichi, Japan

  4. Kozo Yoshida

    Present address: Nihon University, Sakae-machi, 271, Matsudo, Japan

Authors and Affiliations

  1. Primate Research Institute, Kyoto University, Kanrin, Inuyama, 484, Aichi, Japan

    Miya Hamai

  2. Faculty of Science, Kyoto University, Sakyo-ku, 606-01, Kyoto, Japan

    Miya Hamai

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  1. Michael A. Huffman
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Huffman, M.A., Gotoh, S., Turner, L.A. et al. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111–125 (1997). https://doi.org/10.1007/BF02382002

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