, Volume 38, Issue 2, pp 111–125 | Cite as

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

  • Michael A. Huffman
  • Shunji Gotoh
  • Linda A. Turner
  • Miya Hamai
  • Kozo Yoshida


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.

Key Words

Pan troglodytes schweinfurthii Seasonal variation Oesophagostomum stephanostomum Antiparasite behavior Sampling bias 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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
  2. Anderson, R. C. 1992.Nematode Parasites of Vertebrates: Their Development and Transmission. C.A.B. International, Walingford.Google Scholar
  3. Anderson, R. M.;May, R. M. 1982.Population Biology of Infectious Diseases. Springer-Verlag, Berlin.Google Scholar
  4. Ash, L. R.;Orihel, T. C. 1987.Parasites: A Guide to Laboratory Procedures and Identification. Amer. Society of Clinical Pathologists Press, Chicago.Google Scholar
  5. Beaver, P. C.;Jung, R. C.;Cupp, E. W. 1984.Clinical Parasitology (9th ed.). Lea & Febiger, Philadelphia.Google Scholar
  6. Behnke, J. M. 1987. Evasion of immunity by nematode parasites causing chronic infections.Adv. Parasitol., 26: 1–71.PubMedGoogle Scholar
  7. Bernard, C. J.;Behnke, J. M. 1990.Parasitism and Host Behaviour. Taylor & Francis, London.Google Scholar
  8. Brack, M. 1987.Agents Transmissible from Simians to Man. Springer-Verlag, Berlin.Google Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.PubMedGoogle Scholar
  11. Freeland, W. J. 1980. Mangabey (Cercocebus albigena) movement patterns in relation to food availability and fecal contamination.Ecology, 61(6): 1297–1303.Google Scholar
  12. Futuyma, D. J.;Slatkin, M. 1983.Coevolution. Sinauer Associates, Sunderland.Google Scholar
  13. Georgi, J. R. 1985.Parasitology for Veterinarians. Saunders, Philadelphia.Google Scholar
  14. 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
  15. Hamilton, W. D. 1964a. The genetical evolution of social behavior, I.J. Theoret. Biol., 7: 1–16.Google Scholar
  16. Hamilton, W. D. 1964b. The genetical evolution of social behavior, II.J. Theoret. Biol., 7: 17–52.Google Scholar
  17. Hamilton, W. D.;Zuk, M. 1982. Heritable true fitness and bright birds: a rule for parasites?Science, 218: 384–387.PubMedGoogle Scholar
  18. Hart, B. 1990. Behavioral adaptations to pathogens and parasites: five strategies.Neurosi. Behav. Rev., 14: 273–294.Google Scholar
  19. 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
  20. Hill, A. 1985. Nutritional aspects of parasite infection.Prog. Food Nut. Sci., 9: 227–256.Google Scholar
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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.Google Scholar
  29. Kawabata, M.;Nishida, T. 1991. A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania.Primates, 32: 275–278.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Myers, B. J.;Kuntz, R. E. 1972. A checklist of parasites and commensals reported for the chimpanzee (Pan).Primates, 13: 433–471.CrossRefGoogle Scholar
  32. Nelson, G. S. 1960. Schistosome infections as zoonoses in Africa.Transcrip. Royal Soc. Trop. Med. Hyg., 54: 301–314.Google Scholar
  33. 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
  34. Nishida, T.;Nakamaura, M. 1993. Chimpanzee tool use to clear a blocked nasal passage.Folia Primatol., 61: 218–220.PubMedGoogle Scholar
  35. 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
  36. 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
  37. 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.CrossRefGoogle Scholar
  38. 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
  39. 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.CrossRefGoogle Scholar
  40. 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
  41. 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.Google Scholar
  42. Price, P. W. 1980.Evolutionary Biology of Parasitism. Princeton Univ. Press, Princeton.Google Scholar
  43. 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
  44. Sharman, M. J. 1981. Feeding, ranging and social organization of the Guinea baboon. Ph.D. thesis, Univ. of St. Andrews.Google Scholar
  45. 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
  46. Toft, C. A.;Aeschlimann, A.;Bolis, L. 1991.Parasite-Host Associations: Coexistence or Conflict? Oxford Science Publ., Oxford.Google Scholar
  47. 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.PubMedGoogle Scholar
  48. 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
  49. Wrangham, R. M. 1995. Leaf-swallowing by chimpanzees, and its relation to a tapeworm infection.Amer. J. Primatol., 37: 297–303.CrossRefGoogle Scholar
  50. 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
  51. Wrangham, R. W.;Nishida, T. 1983.Aspilia spp. leaves: a puzzle in the feeding behavior of wild chimpanzees.Primates, 24: 276–282.Google Scholar

Copyright information

© Japan Monkey Centre 1997

Authors and Affiliations

  • Michael A. Huffman
    • 1
  • Shunji Gotoh
    • 1
  • Linda A. Turner
    • 2
  • Miya Hamai
    • 1
    • 2
  • Kozo Yoshida
    • 3
  1. 1.Primate Research InstituteKyoto UniversityAichiJapan
  2. 2.Faculty of ScienceKyoto UniversityKyotoJapan
  3. 3.Nihon UniversityMatsudoJapan

Personalised recommendations