Current Evidence for Self-Medication in Primates: A Multidisciplinary Perspective

Yearbook of Physical Anthropology

Volumn 40, Issue , 1997, Pages 171-200

  Huffman, Michael A ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Parasites; Phytochemistry; Plant selection; Primates; Species comparison; Zoopharmacognosy

Indexed keywords

EID: 0037909474     PISSN: 0096848X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-8644(1997)25+<171::aid-ajpa7>3.0.co;2-7     Document Type: Article

References (169)

1. Abbiw DK (1990) Useful Plants of Ghana. Kew: Intermediate Technology Publications and Royal Botanic Gardens.
2. Allison AC (1982) Co-evolution between hosts and infectious disease agents and its effect on virulence. In RM Anderson and RM May (eds.): Population Biology of Infectious Diseases. Berlin: Springer-Verlag, pp. 245-267.
3. Anderson RC (1992) Nematode Parasites of Vertebrates. Their Development and Transmission. Walingford: C.A.B. International.
4. Anderson RM, and May RM (1982) Population Biology of Infectious Diseases. Berlin: Springer-Verlag.
5. Asaka Y, Kubota T, and Kulkarni AB (1977) Studies on a bitter principle from Vernonia anthelmintica. Phytochemistry 16:1838-1839.
6. Baker M (1996) Fur rubbing: Use of medicinal plants by capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38:263-270.
7. Barnard CJ, and Behnke JM (1990) Parasitism and Host Behaviour. London: Taylor and Francis.
8. Barrows M (1996) A survey of the intestinal parasites of the primate in Budongo Forest, Uganda. Report to the Dept. of Veterinary Medicine, University of Glasgow.
9. Beaver PC, Jung RC, and Cupp EW (1984) Clinical Parasitology. 9th ed. Philadelphia: Lea and Febiger.
10. Behnke JM (1987) Evasion of immunity by nematode parasites causing chronic infections. Adv. Parasitol. 26:1-71.
11. Berger PJ, Sanders EH, Gardner PD, and Negus NC (1977) Phenolic plant compounds functioning as reproductive inhibitors in Microtus montanus. Science 195: 575-577.
12. Berlin EA, and Berlin B (1996) Medical Ethnobotany of the Highland Maya of Chiapas. Mexico: The Gastrointestinal Diseases. Princeton. NJ: Princeton University Press.
13. Berry JP, McFarren MA, and Rodriguez E (1995) Zoopharmacognosy: A "Biorational" strategy for phytochemical prospecting. In DL Gustine and HE Flores (eds.) Phytochemicals and Health. Rockville: American Society of Plant Physiologist, pp. 165-178.
14. Boesch C (1995) Innovation in wild chimpanzees (Pan troglodytes). Int. J. Primatol. 16:1-16.
15. Bøgh HO, Andreassen J, and Lemmich J (1996) Anthelmintic usage of extracts of Embelia schimperi from Tanzania. J. Ethnopharmacol. 50:35-42.
16. Brack M (1987) Agents Transmissible from Simians to Man. Berlin: Springer-Verlag.
17. Brett JA (1994) Medicinal Plant Selection Criteria among the Tzeltal Maya of Highland Chiapas, Mexico. Doctoral dissertation. University of California, San Francisco.
18. Brooks DR, and McLennan DA (1993) Paraseript: Parasites and the Language of Evolution. Washington, DC: Smithsonian Institution Press.
19. Buckley JS (1983) The feeding behavior, social behavior, and ecology of the white-faced monkey Cebus capucinus at Trujillo, northern Honduras, Central America. PhD thesis, University of Illinois, Urbana. Ann Arbor: University Microfilms.
20. Burkill HM (1985) The Useful Plants of West Tropical Africa. 2nd ed., Vol 1. Kew: Royal Botanical Gardens.
21. Choquette LPE, Gibson GG, and Pearson AM (1969) Helminths of the grizzly bear Ursus arctos in northern Canada. Can. J. Zool. 47:167-170.
22. Chapman RF, and Blaney WM (1979) How animals perceive secondary compounds. In GA Rosenthal and DH Janzen (eds.): Herbivores, their interactions with secondary plant metabolites. New York: Academic, pp. 161-198.
23. Clayton DH, and Wolfe ND (1993) The adaptive significance of self-medication. TREE 8:60-63.
24. Cowen R (1990) Medicine on the wild side. Science News 138:280-282.
25. Crellin JK, and Philpot J (1990) Herbal Medicine Past and Present Vol. 2. A Reference Guide to Medicinal Plants. Durham: Duke University Press.
26. Dalziel JM (1937) The Useful Plants of West Tropical Africa. In J Hutchinson and JM Dalziel (eds.): Appendix to Flora of West Tropical Africa. London: Whitefriars Press.
27. Davies ND, and Baillie IC (1988) Soil-eating inred leaf monkeys (Presbytis rubicunda) in Saba, northern Borneo. Biotropica 20:252-258.
28. Ehrlich P, and Raven PH (1964) Butterflies and plants: A study in coevolution. Evolution 18:586-608.
29. Ewald PW (1994) Evolution of Infectious Disease. Oxford: Oxford University Press.
30. Fedigan LM (1991) History of the Arashiyama West Japanese Macaques in Texas. In LM Fedigan and PJ Asquith (eds.): The Monkeys of Arashiyama. Thirtyfive Years of Research in Japan and the West. Albany: State University of New York Press, pp. 54-73.
31. Feeny P (1976) Plant apparency and chemical defense. Recent advances in phytochemistry 10:1-40.
32. File SK, McGrew WC, and Tutin CEG (1976) The intestinal parasites of a community of feral chimpanzees, Pan troglodytes schweinfurthii. J. Parasitol. 62:259-261.
33. Fragazy DM, and Visalberghi E (1996) Social learning in monkeys: Primate "primacy" reconsidered. In CM Heyes and BG Galef (eds.): Social Learning in Animals: The Roots of Culture. San Diego: Academic, pp. 65-84.
34. Freeland WF, and Janzen DH (1974) Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Naturalist 108:269-289.
35. Futuyma DJ, and Slatkin M (1983) Coevolution. Sunderland: Sinauer.
36. Galef BG (1977) Mechanisms for the social transmission of acquired food preferences from adult to weanling rats. In LM Barker, MR Best, and M Domjan (eds.): Learning Mechanisms in Food Selection. Baylor, TX: Baylor University Press, pp. 123-148.
37. Gallegos AJ (1985) The zoapatle. VI. Revisited. Contraception 37:487-497.
38. Garey J, Markiewicz L, and Gurpide E (1992) Estrogenic flowers, a stimulus for mating activity in female vervet monkeys. In XIVth Congress of the International Primatological Society Abstracts, Strassbourg, p. 210.
39. Gasquet M, Bamba D, Babadjamian A, Balansard G, Timon-David P, and Metzger J (1985) Action amoebicide et anthelminthique du vernolide et de l'hydroxyvernolide isoles des feuilles de Vernonia colorata (Willd.) Drake. Europ. J. Med. Chem. Theory, 2:111-115.
40. Githens TS (1949) Drug Plants of Africa. Philadelphia: University of Pennsylvania Press.
41. Glander KE (1975) Habitat description and resource utilization: A preliminary report on mantled howler monkey ecology. In R.H. Tuttle (ed.): Socioecology and Psychology of Primates. The Hague: Mouton, pp. 37-57.
42. Glander KE (1980) Reproduction and population growth in free-ranging mantled howling monkeys. Am. J. Phys. Anthropol. 53:25-36.
43. Glander KE (1982) The impact of plant secondary compounds on primate feeding behavior. Yrbk. Phys. Anthropol. 25:1-18.
44. Glander KE (1994) Nonhuman primate self-medication with wild plant foods. In NL Etkin (ed.): Eating on the Wild Side: The Pharmacologic, Ecologic, and Social Implications of Using Noncultigens. Tuscon: University of Arizona Press, pp. 239-256.
45. Glander KE, Wright PC, Seigler DS, Randrianasolo V, and Randrianasolo B (1989) Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. Am. J. Primatol. 19:119-124.
46. Gompper ME, and Holyman AM (1993) Grooming with Trattinnickia resin: Possible pharmaceutical plant use by coatis in Panama. J. Trop. Ecol. 9:533-540.
47. Halstead JA (1968) Geophagia in Man: Its Nature and Nutritional Effects. Am. J. Clin. Nutr. 21:1384-1393.
48. Hamilton WD (1964a) The genetical evolution of social behavior. I. J. Theoret. Biol. 7:1-16.
49. Hamilton WD (1964b) The genetical evolution of social behavior. II. J. Theoret. Biol. 7:17-52.
50. Hamilton WD, and Zuk M (1982) Heritable true fitness and bright birds: A rule for parasites? Science 278:384-387.
51. Hart BL (1990) Behavioral adaptations to pathogens and parasites: Five strategies. Neurosci. Biobehav. Rev. 14:273-294.
52. Haseeb MA, and Fried B (1988) Chemical communication in helminths. Adv. Parasitol. 27:169-207.
53. Hikami K, Hasegawa Y, and Matsuzawa T (1990) Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. J. Comp. Psychol. 104:233-237.
54. Hladik CM (1977a) Chimpanzees of Gabon and chimpanzees of Gombe: Some comparative data on the diet. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic, pp. 481-502.
55. Hladik CM (1977b) A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic, pp. 324-353.
56. Hladik CM, and Simmen B (1996) Tast perception and feeding behavior in nonhuman primates and human populations. Evol. Anthropol. 5:58-71.
57. Holmes JC, and Zohar S (1990) Pathology and host behavior. In CJ Barnard and JM Behnke (eds.): Parasitism and Host Behavior. London: Taylor and Frances, pp. 34-63.
58. Howe HF, and Westley LC (1988) Ecological relationships of plants and animals. New York: Oxford University Press.
59. Huffman MA (1993) An investigation of the use of medicinal plants by wild chimpanzees. Current status and future prospects. Primate Res. 9:179-187.
60. Huffman MA (1994) The C.H.I.M.P.P. Group: A multidisciplinary investigation into the use of medicinal plants by chimpanzes. Pan Africa News 1:3-5.
61. Huffman MA (1996) Acquisition of innovative cultural behaviors in nonhuman primates: A case study of stone handling, a socially transmitted behavior in Japanese macaques. In CM Heyes and BG Galef Jr (eds.): Social Learning in Animals: The Roots of Culture. San Diego: Academic, pp. 267-289.
62. Huffman MA, and Seifu M (1989) Observations on the illness and consumption of a possibly medicinal plant Vernonia amygdalina (Del.), by a wild chimpanzee in the Mahale Mountains National Park, Tanzania. Primates 30:51-63.
63. Huffman MA, and Wrangham RW (1994) The diversity of medicinal plant use by chimpanzees in the wild. In RW Wrangham, WC McGrew, FB deWaal and PG Heltne (eds.): Chimpanzee Cultures. Cambridge, MA: Harvard University Press, pp. 129-148.
64. Huffman MA, Nishida T, and Uehara S (1990) Intestinal parasites and medicinal plant use in wild chimpanzees: Possible behavioral adaptation for the control of parasites. Mahale Mountains Chimpanzees Research Project. Ecological Report no. 72. Kyoto: Kyoto University.
65. Huffman MA, Gotoh S, Izutsu D, Koshimizu K, and Kalunde MS (1993) Further observations on the use of Vernonia amygdalina by a wild chimpanzee, its possible effect on parasite load, and its phytochemistry. African Study Monographs 14:227-240.
66. Huffman MA, Koshimizu K, and Ohigashi H (1996a) Ethnobotany and zoopharmacognosy of Vernonia amygdalina, a medicinal plant used by humans and chimpanzees. In PDS Caligari and DJN Hind (eds.): Compositae: Biology and Utilization. Vol 2. Kew: The Royal Botanical Gardens, pp. 351-360.
67. Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, and Towers GHN (1996b) Leaf-swallowing by chimpaazees, a behavioral adaptation for the control of strongyle nematode infections. Int. J. Primatol. 72:475-503.
68. Huffman MA, Gotoh S, Turner LA, Hamai M, and Yoshida K (1997) Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111-125.
69. Idani G, Kuroda S, Kano T, and Asato R (1994) Flora and vegetation of Wamba Forest, Central Zaire with reference to Bonobo (Pan paniscus) foods. TROPICS 3:309-332.
70. Inoue-Nakamura N, and Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J. Comp. Psychol. 111:159-173.
71. Jackson F (1993) Anthelmintic resistance. The state of play. Br. Vet. J. 149:1233-1235.
72. Jacobsen L, and Hamel R (1996) International Directory of Primatology. Madison: Wisconsin Regional Primate Research Center.
73. Janzen DH (1978) Complications in interpreting the chemical defenses of trees against tropical arboreal plant-eating vertebrates. In GG Montgomery (ed.): The Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institute Press, pp. 73-84.
74. Jisaka M, Kawanaka M, Sugiyama H, Takegawa K, Huffman MA, Ohigashi H, and Koshimizu K (1992a) Antischistosomal activities of sesquiterpene lactones and steroid glucosides from Vernonia amygdalina, possibly used by wild chimpanzees against parasite-related diseases. Biosci. Biotech. Biochem. 56-845-846.
75. Jisaka M, Ohigashi H, Takagaki T, Nozaki H, Tada T, Hirota M, Irie R, Huffman MA, Nishida T, Kaji M, and Koshimizu K (1992b) 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.
76. Jisaka M, Ohigashi H, Takegawa K, Hirota M, Irie R, Huffman MA, and Koshimizu K (1993a) Steroid glucosides from Vernonia amygdalina, a possible chimpanzee medicinal plant. Phytochemistry 34:409-413.
77. Jisaka M, Ohigashi H, Takegawa K, Huffman MA, and Koshimizu K (1993b) Antitumor and antimicrobial activities of bitter sesquiterpene lactones of Vernonia amygdalina, a possible medicinal plant used by wild chimpanzees. Biosci. Biotech. Biochem. 57:833-834.
78. Johns T (1990) With Bitter Herbs They Shall Eat It. Tucson: The University of Arizona Press.
79. Kasonia K, and Ansay M (1994) Métissages en santé animale de Madagascar a Haiti. Namur: Presses Universitaires de Namur.
80. Kawabata M, and Nishida T (1991) A preliminary note on the intestinal parasites of wild chimpanzees of the Mahale Mountains, Tanzania. Primates 32:275-278.
81. Kloos H, and McCullough FS (1987) Plants with recognized molluscicidal activity. In KE Mott (ed.): Plant Molluscicides, New York: John Wiley and Sons, pp. 45-108.
82. Koshimizu K, Ohigashi H, Huffman MA, Nisihda T, and Takasaki H (1993) Physiological activities and the active constituents of potentially medicinal plants used by wild chimpanzees of the Mahale Mountains, Tanzania. Int. J. Primatol. 14:345-356.
83. Krepel HP, Baeta S, Kootstra CJ, and Polderman AM (1995) Reinfection patterns of Oesophagostomum bifurcum and hookworm after anthelmintic treatment. Trop. Geogr. Med. 47:160-163.
84. Kreulen DA (1985) Lick use by large herbivores: A review of benefits and banes of soil consumption. Mammal Rev. 15:107-123.
85. Kreulen DA, and Jager T (1984) The significance of soil ingestion in the utilization of arid rangelands by large herbivores with special reference to natural licks on the Kalahari pan. In FMC Gilchrist and RI Mackie (eds.): Herbivore Nutrition in the Subtropics and Tropics. Johannesburg: The Science Press pp 204-221.
86. Kupchan SM, Hemingway RJ, Karim A, and Werner D (1969) Tumor Inhibitors XLVII. vernodalin and vernomygdin, two new cytotoxic sesquiterpene lactones from Vernonia amygdalina Del. J. Organic Chem 34:3908-3911.
87. Lewis WH, and Elvin-Lewis MPF (1977) Medical Botany. New York: John Wiley and Sons.
88. Ludes E, and Anderson JR (1995) 'Peat-bathing' by captive white-faces capuchin monkeys (Cebus capucinus). Folia Primatol. 65:38-42.
89. Luque MH, and Stokes AW (1976) Fishing behaviour of Alaskan brown bears. Bear Res. Management 3:71-78.
90. MacKinnon BM (1987) Sex attractants in nematodes Parsitol. Today, 3:156-158.
91. Mahaney WC, Watts DP, and Hancock RGV (1990) Geophagia by mountain gorillas (Gorilla gorilla beringei) in the Virunga Mountains, Rwanda. Primates 37:113-120.
92. Mahaney WC, Hancock RGV, and Aufreiter S (1995a) Mountain gorilla geophagy: A possible strategy for dealing with intestinal problems. Int. J. Primatol. 16:475-487.
93. Mahaney WC, Stambolic A, Knezevich M, Hancock RGV, Aufreiter S, Sanmugadas K, Kessler M, and Grynpas M (1995b) Geophagy amongst Rhesus macaques on Cayo Santiago, Puerto Rico. Primates 36:323-333.
94. Mahaney WC, Hancock RGV, Aufreiter S, and Huffman MA (1996) Geochemistry and clay mineralogy of termite mound soil and the role of geophagy in chimpanzees of the Mahale Mountains, Tanzania. Primates 37:121-134.
95. Mahaney WC, Milner MW, Sanmugadas K, Hancock RGV, Aufreiter S, Wrangham RW, and Pier HW (1997) Analysis of geophagv soils in Kibale forest. Uganda Primates 38:159-176.
96. Mathias E, McCorkle CM, and Schillhorn van Veen TW (1996) Introduction: Ethnoveterinary research and development. In CM McCorkle, E Mathias, and Schillhorn van Veen TW (eds.): Ethnoveterinary Research and Development. London: Intermediate Technology Publications, pp. 1-24.
97. Matsuzawa T, and Yamakoshi G (1996) Comparison of chimpanzee material culture between Bossou and Nimba. West Africa. In AE Russon, KA Bard, and S Taylor Parker (eds.): Reaching Into Thought. The Minds of the Great Apes. Cambridge: University of Cambridge Press, pp. 211-232.
98. McCorkle CM, Mathias E, and Schillhorn van Veen TW (1996) Ethnoveterinary Research and Development. London: Intermediate Technology Publications.
99. McGrew WC, Marchant L, and Nishida T (1996) Appendix: Great ape study sites. In Great Ape Societies. Cambridge: Cambridge University Press.
100. McKey D (1978) Soil, vegetation and seed-eating by black colobus monkeys. In GG Montgomery (ed.): The Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institute Press, pp. 423-437.
101. Messer EJ, and Wrangham RW (1995) In vitro testing of the biological activity of Rubia cordifolia leaves on primate Strongyloide species. Primates 37:105-108.
102. Milton K (1979) Factors influencing leaf choice by howler monkeys: A test for some hypotheses of food selection by generalist herbivores. Am. Nat. 114:362-378.
103. Moore M (1979) Medicinal Plants of the Mountain West. Santa Fe: The Museum of New Mexico Press.
104. Moutsamboté J, Yumoto T, Mitani M, Nishihara T, Suzuki S, and Kuroda S (1994) Vegetation and list of plant species identified in the Nouabalé-Ndoki Forest. Congo. TROPICS 3:277-293.
105. Müller K-H, Ahl C, and Hartman G (1997) Geophagy in masked titi monkeys (Callicebus personatus melanochir). Primates 35:69-77.
106. Murakami A, Ohigashi H, and Koshimizu K (1994) Possible anti-tumour promoting properties of traditional Thai foods and some of their active constituents. Asia Pacific J. Clin. Nutr. 3:185-191.
107. Murakami A, Ohigashi H, and Koshimizu K (1996) Anti-tumor promotion with food phytochemicals: A strategy for cancer chemoprevention. Biosci. Biotech. Biochem. 60:1-8.
108. Neuwinger HD (1996) African Ethnobotany: Chemistry, Pharmacology, Toxicology. London: Chapman and Hill.
109. Newton PN, and Nishida T (1990) Possible buccal administration of herbal drugs by wild chimpanzees, Pan troglodytes, Anim. Behav. 39:798-801.
110. Nishida T (1987) Learning and cultural transmission in non-human primates. In BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, and TT Struhsaker (eds.): Primate Societies. Chicago: The University of Chicago Press, pp 462-474.
111. Nishida T, and Uehara S (1983) Natural diet of chimpanzees (Pan troglodytes schweinfurthii): Long term record from the Mahale Mountains, Tanzania. African Studies Monographs 3:109-130.
112. Gates JF (1977) The guereza and its food. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic, pp. 276-321.
113. Oates JF (1978) Water-plant and soil consumption by guereza monkeys (Colobus guereza): A relationship between minerals and toxins in the diet? Biotropica 10:241-253.
114. Oates JF, Swain T, and Zantovska J (1977) Secondary compounds and food selection by colobus monkeys. Biochem. Systems Ecol. 5:317-321.
115. Oates JF, Waterman PG, and Choo GM (1980) Food selection by the south Indian leaf-monkey Presbytis johnii, in relation to leaf chemistry. Oecologia 45:45-56.
116. Ohigashi H (1995) Plants used medicinally by primates in the wild and their physiologically active costituents. Report to the Minestry of Science, Education and Culture for 1994 Grant-in-Aid for Scientific Research (no. 06303012).
117. Ohigashi H, Jisaka M, Takagaki T, Nozaki H, Tada T, Huffman MA, Nishida T, Kaji M, and Koshimizu K (1991) Bitter principle and a related steroid glucoside from Vernonia amygdalina, a possible medicinal plant for wild chimpanzees. Agricultural Biol. Chem. 55: 1201-1203.
118. Ohigashi H, Sakai Y, Yamaguchi K, Umezaki I, and Koshimizu K (1992) Possible anti-tumor promoting properties of marine algae and in vitro activity of wakame seaweed extract. Biosci. Biotech. Biochem. 56:994-995.
119. Ohigashi H, Huffman MA, Izutsu D, Koshimizu K, Kawanaka M, Sugiyama H, Kirby GC, Warhurst DC, Allen D, Wright CW, Phillipson JD, Timmon-David P, Delnas F, Elias R, and 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. 20:541-553.
120. Okunji CO, and Iwu MM (1988) Control of schistomsomiasis using Nigerian medicinal molluscicides. Int. J. Crude Drug Res. 26:246-252.
121. Oppenheimer JR (1968) Behavior and ecology of the white-faced monkey Cebus capucinus, on Barro Colorado Island, CZ, PhD thesis, University of Illinois, Urbana, Ann Arbor: University Microfiflms.
122. Page JE, Balza FF, Nishida T, and Towers GHN (1992) Biologically active diterpenes from Aspilia mossambicensis, a chimpanzee medicinal plant. Phytochemistry 31(10):3437-3439.
123. Page JE, Huffman MA, Smith V, and Towers GHN (1997) Chemical basis for medicinal consumption of Aspilia leaves by chimpanzees: Are-analysis. J. Chem. Ecol. 23:2211-2225.
124. Polderman AM, Krepel S, Baeta S, Blotkamp J, and Gigase P(1991) Oesophagtostomiasis, a common infection of man in northern Togo and Ghana. Am. J. Trop. Med. Hygiene 44:336-344.
125. Ponce-Monter H, Giron H, Lozoya X, Enriquez RG, Bejar E, Estrada AV, and Gallegos AJ (1983) The zoapatle III-biological anduterotonic properties of aqueous plant extract. Contraception 27:239-253.
126. Price PW (1980) Evolutionary Biology of Parasitism. Princeton, NJ: Princeton University Press.
127. Rausch R (1954) Studies on the heminth fauna of Alaska. XXI. Taxonomy, morphological variation, and ecology of Diphyllobothrium ursi n. sp. provis. on Kodiak Island. J. Parasitol. 40:540-563.
128. Rausch R (1961) Notes on the black bear, Ursus americanus Pallas, in Alaska, with particular reference to dentition and growth. Z. Saugetierk 26:77-107.
129. Revusky S (1984) Associative predispositions. In P Marler and HS Terrace (eds.): The Biology Learning. Berlin: Springer-Verlag, pp. 447-460.
130. Richard A (1970) A comparative study of the activity patterns and behavior of Aloutta villosa and Ateles geoffroyi. Folia Primatol. 12:241-263.
131. Rodriguez E, Aregullin M, Nishida T, Uehara S, Wrangham RW, Abramowski Z, Finlayson A, and Towers GHN (1985) Thiarubrin A, a bioactive constituent of Aspilia (Asteraceae) consumed by wild chimpanzees. Experientia 47:419-420.
132. Rodriguez E, and Wrangham RW (1993) Zoopharmacognosy: The use of medicinal plants by animals. In KR Downum, JT Romeo, and H Stafford (eds.): Recent Advances in Phytochemistry, vol. 27: Phytochemical Potential of Tropic Plants. New York: Plenum, pp. 89-105.
133. Roepstorff A, Bjørn H, and Nansen P (1987) Resistence of Oesophagostomum spp. in pigs to pyrantel citrate. Vet. Parasitol. 24:229-239.
134. Sadlier RM (1969) The Ecology of Reproduction in Wild and Domestic Mammals. London: Methuer.
135. Salafsky B, Wang Y-S, Kevin MB, Hill H, and Fusco AC (1984) The role of prostaglandins in cercarial (Schistosoma mansoni) response to free fatty acids. J. Parasitol. 70:584-591.
136. Sarmiento EE, Butynski TM, and Kalina J (1996) Gorillas of Bwindi-Impenetrable Forest and the Virunga Volcanoes: Taxonomic implications of morphological and ecological differences. Am. J. Primatol. 40:1-21.
137. Sayer JA, Harcourt CS, and Collins NM (1992) The Conservation Atlas of Tropical Forests, Africa. New York, IUCN.
138. Shiba T (1976) Chemistry of bitter and hot taste. Kagaku Sosetsu 14:129-156.
139. Smolenski SJ, Silinis H, and Farnsworth NR (1974) Alkaloid screening. V. Lloydia 37:506-536.
140. Starker LA (1976) Phytooestrogens: Adverse effects on reproduction in California quail. Science 191:98-100.
141. Struhsaker TT (1997) Ecology of an African Rain Forest. Gainesville: University Press of Florida.
142. SugiyamaY, and Koman J (1992) The flora of Bossou: Its utilization by chimpanzees and humans. African Studies Monographs 13:127-169.
143. Sukhdeo MVM, and Sukhdeo SC (1994) Optimal habitat selection behaviour by helminths within the host. Parasitology 109:41-55.
144. Synott TJ (1985) A checklist of the flora of Budongo Forest Reserve, Uganda, with notes on ecology and phenology. CFI Occasional Papers No. 27, Department of Forestry Commonwealth Forestry Institute, Oxford, University of Oxford.
145. Takasaki H, and Hunt K (1987) Further medicinal plant consumption in wild chimpanzees? African Studies Monographs 8:125-128.
146. Toft CA, Aeschlimann A, and Bolis L (1991) Parasite-Host Associations; Coexistence or Conflict? Oxford: Oxford Science Publications.
147. Toubiana R, and Gaudemer A (1967) Structure du vernolide, nouvel ester sesquiterpique isole de Vernonia colorata. Tetrahedron Lett. 14:1333-1336.
148. Towers GHN, Abramowski Z, Finlayson AJ, and Zucconi A (1985) Antibiotic properties of thiarubrine-A, a naturally occurring dithiacvclohedadiene polvine. Planta Medica 3:225-229.
149. Tutin CEG, White LJT, Williamson EA, Fernandez M, and McPherson G (1994) List of plant species identified in the northern part of the Lopé Reserve, Gabon. TROPICS 3:249-276.
150. Vermeer J (1995) A garden of enrichment. Animal Keepers' Forum 5:165-167.
151. Wallis J (1992) Socioenvironmental effects on timing of first postpartum cycles in chimpanzees. In T Nishida, WC McGrew, P Marier, M Pickford, and F de Waal (eds.): Topics in Primatology, Vol. 1: Human Origins. Tokyo: University of Tokyo Press, pp. 119-130.
152. Wallis J (1994) Socioenvironmental effects on full anogenital swellings in adolescent female chimpanzees. In JJ Roeder, B Thierry, JR Anderson, and N Herrenschmidt (eds.): Current Primatology, Vol. 2: Social Development, Learning and Behavior. Strasbourg: University of Louis Pasteur, pp. 25-32.
153. Wallis J (1995) Seasonal influence on reproduction in chimpanzees of Gombe National Park. Int. J. Primatol. 16:435-451.
154. Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J. Reprod. Fertil. 109:297-307.
155. Waterman PG (1984) Food acquisition and processing as a function of plant chemistry. In DJ Chivers, BA Wood, and A Bilsborough (eds.): Food Acquisition and Processing in Primates. New York: Plenum, pp. 177-211.
156. Watt JM, and Breyer-Brandwijk MG (1962) The Medicinal and Poisonous Plants of Southern and East Africa. Edinburgh: E. and S. Livingstone.
157. Westley J (1980) Rhodanese and the sulfane pool. In WB Jakoby (ed.): Enzymatic basis of detoxification. vol. 2. New York: Academic, pp. 245-262.
158. Whitten PL (1983) Flowers, fertility and females. Abstract. Am. J. Phys. Anthropol. 60:269-270.
159. Wink M, Hofer A, Bilfinger M, Englert E, Martin M, and Schneider D (1993) Geese and dietary allelochemicals-food palatability and geophagy. Chemoecology 4:93-107.
160. Wrangham RW (1977) Feeding behavior of chimpanzees in Gombe National Park, Tanzania. In TH Clutton-Brock (ed.): Primate Ecology. London: Academic, pp. 504-538.
161. Wrangham RW (1995) Relationship of chimpanzee leaf-swallowing to a tapeworm infection. Am. J. Phys. Primatol. 37:297-303.
162. Wrangham RW, and Goodall J (1989) Chimpanzee use of medicinal leaves. In PG Heltne and LA Marquardt (eds): Understanding Chimpanzees. Cambridge, MA: Harvard University Press, pp. 22-37.
163. Wrangham RW, and Nishida T (1983) Aspilia spp. leaves: A puzzle in the feeding behavior of wild chimpanzees. Primates 24:276-282.
164. Wrangham RW, and Waterman PG (1981) Condensed tannins in fruits eaten by chimpanzees. Biotropica 15:217-222.
165. Wrangham RW, Rogers ME, and Isabirye-Basuta G (1993) Ape food density in the ground layer in Kibale Forest, Uganda. African J. Ecol. 31:49-57.
166. Wright C, Phillipson GC, Kirby DV, Huffman MA, and Ohigashi H (1993) Do chimpanzees know how to treat protozoal diseases? Paper presentation at the Fifth British Society for Parasitology Malaria Meeting, September, 1993: Oxford.
167. Yumoto T, Yamagiwa J, Mwanza N, and Maruhashi T (1994) List of plant species identified in Kahuzi-Biega National Park, Zaire. TROPICS 3:295-308.
168. Zahorik DM (1977) Associative and non-associative factors in learned food preferences. In LM Barker, MR Best, and M Domjan (eds.): Learning Mechanisms in Food Selection. Baylor, TX: Baylor University Press, pp. 181-199.
169. Zahorik DM, and Albro Houpt K (1977) The concept of nutritional wisdom: Applicability of laboratory learning models to large herbivores. In LM Barker, MR Best, and M Domjan (eds.): Learning Mechanisms in Food Selection. Baylor, TX: Baylor University Press, pp. 45-67.