Roving females and patient males: A new perspective on the mating strategies of chimpanzees

Biological Reviews

Volumn 89, Issue 2, 2014, Pages 356-374

  Newton Fisher, Nicholas E ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

Author keywords

Alpha male; Alternate strategies; Female choice; Mate choice; Pan troglodytes; Primate; Reproductive strategy; Roving male; Sequestration; Sexual conflict

Indexed keywords

ANIMALIA; PAN; PAN TROGLODYTES; PRIMATES;

ANIMAL; FEMALE; MALE; PAN TROGLODYTES; PHYSIOLOGY; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

ANIMALS; FEMALE; MALE; PAN TROGLODYTES; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 84898463255     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12058     Document Type: Article

References (206)

1. Altizer, S., Nunn, C., Thrall, P., Gittleman, J., Ezenwa, V., Pulliam, J., Pedersen, A., Dobson, A., Poss, M., Cunningham, A., Antonovics, J. & Jones, K. (2003). Social organization and disease risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34, 517-547.
2. Anderson, M. J., Chapman, S. J., Videan, E. N., Evans, E., Fritz, J., Stoinski, T. S., Dixson, A. F. & Gagneux, P. (2007). Functional evidence for differences in sperm competition in humans and chimpanzees. American Journal of Physical Anthropology 134, 274-280.
3. Anderson, M. J. & Dixson, A. F. (2002). Sperm competition: motility and the midpiece in primates. Nature 416, 496.
4. Arcadi, A. C. & Wrangham, R. W. (1999). Infanticide in chimpanzees: review of cases and a new within-group observation from the Kanyawara study group in Kibale National Park. Primates 40, 337-351.
5. Arnold, K. & Whiten, A. (2001). Post-conflict behaviour of wild chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Behaviour 138, 649-690.
6. Arnold, K. & Whiten, A. (2003). Grooming interactions among the chimpanzees of the Budongo Forest, Uganda: tests of five explanatory models. Behaviour 140, 519-552.
7. Arnqvist, G. & Rowe, L. (2005). Sexual Conflict. Princeton University Press, Princeton.
8. Aureli, F., Preston, S. D. & de Waal, F. B. M. (1999). Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. Journal of Comparative Psychology 113, 59-65.
9. Aureli, F. & Schino, G. (2004). The role of emotions in social relationships. In Macaque Societies: A Model for the Study of Social Organization, pp. 38-55. Cambridge University Press, New York.
10. Barrett, L. & Henzi, S. P. (2001). The utility of grooming in baboon troops. In Economics in Nature (eds R. Noë, J. A. R. A. M. van Hooff and P. Hammerstein ), pp. 119-145. Cambridge University Press, Cambridge.
11. Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. (1999). Market forces predict grooming reciprocity in female baboons. Proceedings of the Royal Society of London, Series B: Biological Sciences 266, 665-670.
12. Bates, L. A. & Byrne, R. W. (2009). Sex differences in the movement patterns of free-ranging chimpanzees (Pan troglodytes schweinfurthii): foraging and border checking. Behavioral Ecology and Sociobiology 64, 247-255.
13. Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour 117, 221-242.
14. Boesch, C. (1996). Social grouping in Taï chimpanzees. In Great Ape Societies (eds W. C. McGrew, L. F. Marchant and T. Nishida ), pp. 101-113. Cambridge University Press, Cambridge.
15. Boesch, C. & Boesch, H. (1989). Hunting behavior of wild chimpanzees in the Taï National Park. American Journal of Physical Anthropology 78, 547-573.
16. Boesch, C. & Boesch-Achermann, H. (2000). The Chimpanzees of the Tai Forest. Oxford University Press, Oxford.
17. Boesch, C., Kohou, G., Nene, H. & Vigilant, L. (2006). Male competition and paternity in wild chimpanzees of the Tai forest. American Journal of Physical Anthropology 130, 103-115.
18. Boone, J. L. (1991). Comments on Manson, J. H. & Wrangham, R. W. 'Intergroup aggression in chimpanzees and humans'. Current Anthropology 32, 377.
19. Boyko, R. H. & Marshall, A. J. (2009). The willing cuckold: optimal paternity allocation, infanticide and male reproductive strategies in mammals. Animal Behaviour 77, 1397-1407.
20. Bygott, J. D. (1979). Agonistic behaviour, dominance, and social structure in wild chimpanzees of the Gombe National Park. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 405-428. Benjamin/Cummings Publishing Company, Menlo Park.
21. Cameron, E. Z., Setsaas, T. H. & Linklater, W. L. (2009). Social bonds between unrelated females increase reproductive success in feral horses. Proceedings of the National Academy of Sciences of the United States of America 106, 13850-13853.
22. Carpenter, C. R. (1945). Concepts and problems of primate sociometry. Sociometry 8, 56-61.
23. Chapman, C. A. & Wrangham, R. W. (1993). Range use of the forest chimpanzees of Kibale: implications for the understanding of chimpanzee social organization. American Journal of Primatology 31, 263-273.
24. Clutton-Brock, T. H. & Parker, G. A. (1995). Sexual coercion in animal societies. Animal Behaviour 49, 1345-1365.
25. Coe, C. L. (1993). Psychosocial factors and immunity in non-human primates: a review. Psychosomatic Medicine 55, 298-308.
26. Constable, J. L., Ashley, M. V., Goodall, J. & Pusey, A. E. (2001). Noninvasive paternity assignment in Gombe chimpanzees. Molecular Ecology 10, 1279-1300.
27. Crockford, C., Wittig, R. M., Whitten, P. L., Seyfarth, R. A. & Cheney, D. L. (2008). Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Hormones and Behavior 53, 254-265.
28. Derocher, A. E., Andersen, M., Wiig, O. & Aars, J. (2010). Sexual dimorphism and the mating ecology of polar bears (Ursus maritimus) at Svalbard. Behavioral Ecology and Sociobiology 64, 939-946.
29. Deschner, T., Heistermann, M., Hodges, K. & Boesch, C. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour 66, 551-560.
30. Deschner, T., Heistermann, M., Hodges, K. & Boesch, C. (2004). Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Hormones and Behavior 46, 204-215.
31. Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford University Press, Oxford.
32. Duffy, K. G., Wrangham, R. W. & Silk, J. B. (2007). Male chimpanzees exchange political support for mating opportunities. Current Biology 17, R586-R587.
33. Dunbar, R. (1996). Grooming, Gossip and the Evolution of Language. Faber & Faber, London.
34. Dunbar, R. I. M. (1988). Primate Social Systems. First Edition (). Croom Helm, London.
35. Dunbar, R. I. M. (1991). Functional significance of social grooming in primates. Folia Primatologica 57, 121-131.
36. Dunbar, R. I. M. (2000). Male mating strategies: a modeling approach. In Primate Males: Causes and Consequences of Variation in Group Composition (ed. P. M. Kappeler ), pp. 259-268. Cambridge University Press, Cambridge.
37. Dunbar, R. I. M. & Sharman, M. (1984). Is social grooming altruistic? Zeitschrift fur Tierpsychologie-Journal of Comparative Ethology 64, 163-173.
38. Emery, M. A. & Whitten, P. L. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioral Ecology and Sociobiology 54, 340-351.
39. Emery Thompson, M. (2005). Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. American Journal of Primatology 67, 137-158.
40. Emery Thompson, M., Jones, J. H., Pusey, A. E., Brewer-Marsden, S., Goodall, J., Marsden, D., Matsuzawa, T., Nishida, T., Reynolds, V., Sugiyama, Y. & Wrangham, R. W. (2007). Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Current Biology 17, 2150-2156.
41. Emery Thompson, M. & Wrangham, R. W. (2006). Comparison of sex differences in gregariousness in fission-fusion species: reducing bias by standardizing for party size. In Primates of Western Uganda (eds J. D. Paterson, V. Reynolds, N. E. Newton-Fisher and H. Notman ), pp. 209-226. Cambridge University Press, Cambridge.
42. Emery Thompson, M. & Wrangham, R. W. (2008a). Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda. American Journal of Physical Anthropology 135, 171-181.
43. Emery Thompson, M. & Wrangham, R. W. (2008b). Male mating interest varies with female fecundity in Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park. International Journal of Primatology 29, 885-905.
44. Emlen, S. T. & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of social systems. Science 197, 215-223.
45. Engh, A. L., Beehner, J. C., Bergman, T. J., Whitten, P. L., Hoffmeier, R. R., Seyfarth, R. M. & Cheney, D. L. (2006). Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society B: Biological Sciences 273, 707-712.
46. Feh, C. & Demazieres, J. (1993). Grooming at a preferred site reduces heart-rate in horses. Animal Behaviour 46, 1191-1194.
47. Fraser, O. N., Stahl, D. & Aureli, F. (2008). Stress reduction through consolation in chimpanzees. Proceedings of the National Academy of Sciences of the United States of America 105, 8557-8562.
48. Fraser, O. N., Stahl, D. & Aureli, F. (2010). The function and determinants of reconciliation in Pan troglodytes. International Journal of Primatology 31, 39-57.
49. Gilby, I. C., Eberly, L. E., Pintea, L. & Pusey, A. E. (2006). Ecological and social influences on the hunting behaviour of wild chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour 72, 169-180.
50. Godbout, J. P. & Glaser, R. (2006). Stress-induced immune dysregulation: implications for wound healing, infectious disease and cancer. Journal of Neuroimmune Pharmacology 1, 421-427.
51. Gomes, C. M., Mundry, R. & Boesch, C. (2009). Long-term reciprocation of grooming in wild West African chimpanzees. Proceedings of the Royal Society B: Biological Sciences 276, 699-706.
52. Goodall, J. (1973). Cultural elements in a chimpanzee community. In Precultural Primate Behaviour, Fourth IPC Symposia Proceedings (Volume 1, (ed. E. W. Menzel ), pp. 144-184. Karger Press, Basel.
53. Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of behaviour. First Edition. Belknap Press, Cambridge.
54. Goodall, J. (1990). Through a Window: My Thirty Years with the Chimpanzees of Gombe. Goerge Weidenfeld & Nicolson Ltd., London.
55. Goodall, J., Bandora, A., Bergmann, E., Busse, C., Matama, H., Mpongo, E., Pierce, A. & Riss, D. (1979). Intercommunity interactions in the chimpanzee population of the Gombe National Park. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 13-53. Benjamin/Cummings, Menlo Park.
56. Graham, C. E. (1970). Reproductive physiology of the chimpanzee. In The Chimpanzee, Volume 3, Immunology, Infections, Hormones, Anatomy, and Behavior of Chimpanzees, pp. 183-220. University Park Press, Baltimore.
57. Hamai, M., Nishida, T., Takasaki, H. & Turner, L. A. (1992). New records of within-group infanticide and cannibalism in wild chimpanzees. Primates 33, 151-162.
58. Hansen, J. F., Alford, P. L. & Keeling, M. E. (1984). Diffuse myocardial fibrosis and congestive heart-failure in an adult male chimpanzee. Veterinary Pathology 21, 529-531.
59. Harcourt, A. H. (1997). Sperm competition in primates. American Naturalist 149, 189-194.
60. Harcourt, A. H. & Greenberg, J. (2001). Do gorilla females join males to avoid infanticide? A quantitative model. Animal Behaviour 62, 905-915.
61. Harvey, P. H. & Harcourt, A. H. (1984). Sperm competition, testes size, and breeding systems in primates. In Sperm Competition and the Evolution of Animal Mating Systems, pp. 589-600. Academic Press, Orlando.
62. Hasegawa, T. & Hiraiwa-Hasegawa, M. (1983). Opportunistic and restrictive mating among wild chimpanzees in the Mahale Mountains, Tanzania. Journal of Ethology 1, 75-85.
63. Hasegawa, T. & Hiraiwa-Hasegawa, M. (1990). Sperm competition and mating behavior. In The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies (ed. T. Nishida ), pp. 115-132. University of Tokyo Press, Tokyo.
64. Hayaki, H., Huffman, M. A. & Nishida, T. (1989). Dominance among male chimpanzees in the Mahale Mountains National Park, Tanzania: a preliminary study. Primates 30, 187-197.
65. Henzi, S. P., Clarke, P. M. R., van Schaik, C. P., Pradhan, G. R. & Barrett, L. (2010). Infanticide and reproductive restraint in a polygynous social mammal. Proceedings of the National Academy of Sciences of the United States of America 107, 2130-2135.
66. Herbinger, I., Boesch, C. & Rothe, H. (2001). Territory characteristics among three neighboring chimpanzee communities in the Tai National Park, Cote d'Ivoire. International Journal of Primatology 22, 143-167.
67. Hill, K., Boesch, C., Goodall, J., Pusey, A., Williams, J. & Wrangham, R. (2001). Mortality rates among wild chimpanzees. Journal of Human Evolution 40, 437-450.
68. Hinde, R. A. (1976). Interactions, relationships and social structure. Man 11, 1-17.
69. Hrdy, S. B. (1979). Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology 1, 13-40.
70. Janson, C. H. (2000). Primate socio-ecology: the end of a golden age. Evolutionary Anthropology 9, 73-86.
71. Johnson, D. D. P., Stopka, P. & Macdonald, D. W. (2004). Ideal flea constraints on group living: unwanted public goods and the emergence of cooperation. Behavioral Ecology 15, 181-186.
72. Kaburu, S. S. K., Inoue, S. & Newton-Fisher, N. E. (2013). Death of the alpha: within-community lethal violence among chimpanzees of the Mahale Mountains National Park. American Journal of Primatology 75, 789-797.
73. Kahlenberg, S. M., Emery Thompson, M., Muller, M. N. & Wrangham, R. W. (2008a). Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Animal Behaviour 76, 1497-1509.
74. Kahlenberg, S. M., Emery Thompson, M. & Wrangham, R. W. (2008b). Female competition over core areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda. International Journal of Primatology 29, 931-947.
75. Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., Li, Y., Learn, G. H., Beasley, T. M., Schumacher-Stankey, J., Wroblewski, E., Mosser, A., Raphael, J., Kamenya, S., Lonsdorf, E. V., Travis, D. A., Mlengeya, T., Kinsel, M. J., Else, J. G., Silvestri, G., Goodall, J., Sharp, P. M., Shaw, G. M., Pusey, A. E. & Hahn, B. H. (2009). Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460, 515-519.
76. Keverne, E. B., Martensz, N. D. & Tuite, B. (1989). Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14, 155-161.
77. Krebs, J. R. & Davies, N. B. (1987). An Introduction to Behavioural Ecology. Second Edition. Blackwell Scientific Publications, Oxford.
78. Kutsukake, N. & Castles, D. L. (2004). Reconciliation and post-conflict third-party affiliation among wild chimpanzees in the Mahale Mountains, Tanzania. Primates 45, 157-165.
79. Lehmann, J. & Boesch, C. (2004). To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behavioral Ecology and Sociobiology 56, 207-216.
80. Lehmann, J. & Boesch, C. (2005). Bisexually bonded ranging in chimpanzees (Pan troglodytes verus). Behavioral Ecology and Sociobiology 57, 525-535.
81. Lehmann, J. & Boesch, C. (2008). Sexual differences in chimpanzee sociality. International Journal of Primatology 29, 65-81.
82. Lehmann, J. & Boesch, C. (2009). Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Animal Behaviour 77, 377-387.
83. Lehmann, J., Korstjens, A. H. & Dunbar, R. I. M. (2007). Group size, grooming and social cohesion in primates. Animal Behaviour 74, 1617-1629.
84. Leigh, S. R. & Shea, B. T. (1995). Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology 36, 37-60.
85. Leinfelder, I., De Vries, H., Deleu, R. & Nelissen, M. (2001). Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons. American Journal of Primatology 55, 25-42.
86. Manson, J. H. & Wrangham, R. W. (1991). Intergroup aggression in chimpanzees and humans. Current Anthropology 32, 369-390.
87. Matsumoto-Oda, A., Oda, R., Hayashi, Y., Murakami, H., Maeda, N., Kumazaki, K., Shimizu, K. & Matsuzawa, T. (2003). Vaginal fatty acids produced by chimpanzees during menstrual cycles. Folia Primatologica 74, 75-79.
88. McGinnis, P. R. (1973). Patterns of sexual behaviour in a community of free-living chimpanzees. PhD Thesis: University of Cambridge.
89. McGinnis, P. R. (1979). Sexual behavior in free-living chimpanzees: consort relationships. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 429-439. Benjamin/Cummings Publishing Company, Menlo Park.
90. Mitani, J. (1994). Ethological studies of chimpanzee vocal behavior. In Chimpanzee Cultures (eds R. W. Wrangham, W. C. McGrew, F. B. M. de Waal and P. G. Heltne ), pp. 195-210. Harvard University Press, Cambridge.
91. Mitani, J. C. (2006). Reciprocal exchange in chimpanzees and other primates. In Cooperation in Primates and Humans: Mechanisms and Evolutions, pp. 107-119. Springer, New York.
92. Mitani, J. C. (2008). Chimpanzee behavior: there's no place like home. Current Biology 18, R166-R167.
93. Mitani, J. C. (2009). Male chimpanzees form enduring and equitable social bonds. Animal Behaviour 77, 633-640.
94. Mitani, J. C., Watts, D. P. & Amsler, S. J. (2010). Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Current Biology 20, R507-R508.
95. Moller, A. P. (1988). Ejaculate quality, testes size and sperm competition in primates. Journal of Human Evolution 17, 479-488.
96. Muller, M. N. (2002). Agonistic relations among Kanyawara chimpanzees. In Behavioural Diversity in Chimpanzees and Bonobos (eds C. Boesch, G. Hohmann and L. F. Marchant ), pp. 112-124. Cambridge University Press, Cambridge.
97. Muller, M. N., Emery Thompson, M., Kahlenberg, S. M. & Wrangham, R. W. (2011). Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behavioral Ecology and Sociobiology 65, 921-933.
98. Muller, M. N., Kahlenberg, S. M., Emery Thompson, M. & Wrangham, R. W. (2007). Male coercion and the costs of promiscuous mating for female chimpanzees. Proceedings of the Royal Society B: Biological Sciences 274, 1009-1014.
99. Muller, M. N., Kahlenberg, S. M. & Wrangham, R. W. (2009). Male aggression against females and sexual coercion in chimpanzees. In Sexual Coercion in Primates and Humans (eds M. N. Muller and R. W. Wrangham ), pp. 184-217. Harvard University Press, Cambridge.
100. Muller, M. N. & Mitani, J. C. (2005). Conflict and cooperation in wild chimpanzees. Advances in the Study of Behavior 35, 275-331.
101. Murray, C. M., Gilby, I. C., Mane, S. V. & Pusey, A. E. (2008). Adult male chimpanzees inherit maternal ranging patterns. Current Biology 18, 20-24.
102. Nadler, R. D. & Bartlett, E. S. (1997). Penile erection: a reflection of sexual arousal and arousability in male chimpanzees. Physiology & Behavior 61, 425-432.
103. Newton, P. N. & Nishida, T. (1990). Possible buccal administration of herbal drugs by wild chimpanzees, Pan troglodytes. Animal Behaviour 39, 798-801.
104. Newton-Fisher, N. E. (1997). Tactical behaviour and decision making in wild chimpanzees. PhD Thesis: University of Cambridge.
105. Newton-Fisher, N. E. (1999a). Association by male chimpanzees: a social tactic? Behaviour 136, 705-730.
106. Newton-Fisher, N. E. (1999b). Infant killers of Budongo. Folia Primatologica 70, 167-169.
107. Newton-Fisher, N. E. (2000). Male core areas: ranging by Budongo forest chimpanzees. Pan Africa News 7, 10-12.
108. Newton-Fisher, N. E. (2002a). Ranging patterns of male chimpanzees in the Budongo Forest, Uganda: range structure and individual differences. In New Perspectives in Primate Evolution and Behaviour (eds C. S. Harcourt and B. R. Sherwood ), pp. 287-308. Westbury, Otley.
109. Newton-Fisher, N. E. (2002b). Relationships of male chimpanzees in the Budongo forest, Uganda. In Behavioural Diversity in Chimpanzees and Bonobos (eds C. Boesch, G. Hohmann and L. F. Marchant ), pp. 125-137. Cambridge University Press, Cambridge.
110. Newton-Fisher, N. E. (2003). The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. African Journal of Ecology 41, 150-156.
111. Newton-Fisher, N. E. (2004). Hierarchy and social status in Budongo chimpanzees. Primates 45, 81-87.
112. Newton-Fisher, N. E. (2006). Female coalitions against male aggression in wild chimpanzees of the Budongo Forest. International Journal of Primatology 27(6), 1589-1599.
113. Newton-Fisher, N. E. & Emery Thompson, M. (2012). Comparative evolutionary perspectives on violence. In Oxford Handbook of Evolutionary Perspectives on Violence, Homicide, and War (eds T. Shackleford and V. Weekes-Shackleford ), pp. 41-60. Oxford University Press, New York.
114. Newton-Fisher, N. E., Emery Thompson, M., Reynolds, V., Boesch, C. & Vigilant, L. (2010). Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. American Journal of Physical Anthropology 142, 417-428.
115. Newton-Fisher, N. E. & Lee, P. C. (2011). Grooming reciprocity in wild male chimpanzees. Animal Behaviour 81, 439-446.
116. Nishida, T. (1968). The social group of wild chimpanzees in the Mahale Mountains. Primates 9, 167-224.
117. Nishida, T. (1979). The social structure of chimpanzees of the Mahale Mountains. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 73-122. Benjamin/Cummings Publishing Company, Menlo Park.
118. Nishida, T. (1983). Alpha status and agonistic alliance in wild chimpanzees (Pan troglodytes schweinfurthii). Primates 24, 318-336.
119. Nishida, T. (1991). Comments on Manson, J. H. & Wrangham, R. W. 'Intergroup aggression in chimpanzees and humans'. Current Anthropology 32, 381-382.
120. Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., Hosaka, K., Hunt, K. D., Itoh, N., Kawanaka, K., Matsumoto-Oda, A., Mitani, J. C., Nakamura, M., Norikoshi, K., Sakamaki, T., Turner, L., Uehara, S. & Zamma, K. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology 59, 99-121.
121. Nishida, T. & Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: cooperative relationships among males. In Primate Societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham and T. Struhsaker ), pp. 165-177. University of Chicago Press, Chicago.
122. Nishida, T., Hiraiwa-Hasegawa, M., Hasegawa, T. & Takahata, Y. (1985). Group extinction and female transfer in wild chimpanzees in the Mahale National Park, Tanzania. Zeitschrift für Tierpsychologie 67, 284-301.
123. Nishida, T. & Hosaka, K. (1996). Coalition strategies among adult male chimpanzees of the Mahale Mountains, Tanzania. In Great Ape Societies (eds W. C. McGrew, L. F. Marchant and T. Nishida ), pp. 114-134. Cambridge University Press, Cambridge.
124. Noë, R. (2001). Biological markets: partner choice as the driving force behind the evolution of mutualisms. In Economics in Nature (eds R. Noë, J. A. R. A. M. van Hooff and P. Hammerstein ), pp. 93-118. Cambridge University Press, Cambridge.
125. Noë, R. & Hammerstein, P. (1994). Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology 35, 1-11.
126. Noë, R. & Hammerstein, P. (1995). Biological markets. Trends in Ecology & Evolution 10, 336-340.
127. van Noordwijk, M. A. & van Schaik, C. P. (2000). Reproductive patterns in eutherian mammals: adaptations against infanticide?. In Infanticide by Males and its Implications, pp. 322-360. Cambridge University Press, Cambridge.
128. Notman, H. & Rendall, D. (2005). Contextual variation in chimpanzee pant hoots and its implications for referential communication. Animal Behaviour 70, 177-190.
129. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour 58, 229-246.
130. O'Hara, S. (2005). Female sexuality and male violence in wild chimpanzees. PhD Thesis: University of Cambridge.
131. Packer, C., Collins, D. A., Sindimwo, A. & Goodall, J. (1995). Reproductive constraints on aggressive competition in female baboons. Nature 373, 60-63.
132. Parker, G. A. (1970). Sperm competition and its evolutionary consequences in insects. Biological Reviews of the Cambridge Philosophical Society 45, 525-567.
133. Parker, G. A. (1979). Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects (eds M. S. Blum and N. A. Blum ), pp. 123-166. Academic Press, New York.
134. Parker, G. A. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of the two sexes. Journal of Theoretical Biology 96, 281-294.
135. Pepper, J. W., Mitani, J. C. & Watts, D. P. (1999). General gregariousness and specific social preferences among wild chimpanzees. International Journal of Primatology 20, 613-632.
136. Pusey, A. E. (1979). Intercommunity transfer of chimpanzees in the Gombe National Park. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 465-480. Benjamin/Cummings, Menlo Park.
137. Pusey, A. E. (2001). Of genes and apes: chimpanzee social organisation and reproduction. In Tree of Origin (ed. F. B. M. de Waal ), pp. 11-37. Harvard University Press, Cambridge.
138. Pusey, A., Williams, J. & Goodall, J. (1997). The influence of dominance rank on the reproductive success of female chimpanzees. Science 277, 828-831.
139. Reichard, U. (1995). Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology 100, 99-112.
140. Reynolds, V. (2005). The Chimpanzees of the Budongo Forest: Ecology, Behaviour and, Conservation. Oxford University Press, New York.
141. Reynolds, V. & Reynolds, F. (1965). Chimpanzees of the Budongo Forest. In Primate Behaviour (ed. I. DeVore ), pp. 368-424. Holt, Rinehart and Winston, Inc., New York.
142. Riedel, J., Franz, M. & Boesch, C. (2010). How feeding competition determines female chimpanzee gregariousness and ranging in the Tai National Park, Cote d'Ivoire. American Journal of Primatology 73, 305-313.
143. Sapolsky, R. M. (1993). The physiology of dominance in stable versus unstable social hierarchies. In Primate Social Conflict (eds W. A. Mason and S. P. Mendola ), pp. 171-204. State University of New York Press, Albany.
144. Sapolsky, R. M. (1996). Stress, stress-related disease and personality: studies of wild baboons. In XVIth Congress of the International Primatological Society. Madison.
145. Sapolsky, R. M. (2004). Social status and health in humans and other animals. Annual Review of Anthropology 33, 393-418.
146. Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science 308, 648-652.
147. Sapolsky, R. M., Krey, L. C. & McEwen, B. S. (2002). The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Science of Aging Knowledge Environment 2002, cp21.
148. Sapolsky, R. M., Uno, H., Rebert, C. S. & Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience 10, 2897-2902.
149. Saunders, C. D. & Hausfater, G. (1988). The functional significance of baboon grooming behavior. Annals of the New York Academy of Sciences 525, 430-432.
150. van Schaik, C. P. (2000). Social counterstrategies against infanticide by males in primates and other mammals. In Primate Males: Causes and Consequences of Variation in Group Composition (ed. P. M. Kappeler ), pp. 34-54. Cambridge University Press, Cambridge.
151. van Schaik, C. P. & Janson, C. H. (2000). Infanticide by Males and its Implications. Cambridge University Press, Cambridge.
152. van Schaik, C. P. & Kappeler, P. M. (1997). Infanticide risk and the evolution of male-female association in primates. Proceedings of the Royal Society of London B264, 1687-1694.
153. Schapiro, S. J., Nehete, P. N., Perlman, J. E., Bloomsmith, M. A. & Sastry, K. J. (1998). Effects of dominance status and environmental enrichment on cell-mediated immunity in rhesus macaques. Applied Animal Behaviour Science 56, 319-332.
154. Shutt, K., MacLarnon, A., Heistermann, M. & Semple, S. (2007). Grooming in Barbary macaques: better to give than to receive? Biology Letters 3, 231-233.
155. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M. & Cheney, D. L. (2010). Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20, 1359-1361.
156. Simpson, M. J. A. (1973). The social grooming of male chimpanzees. In Comparative Ecology and Behaviour of Primates (eds R. P. Michael and J. H. Crook ), pp. 411-506. Academic Press, London.
157. Smuts, B. B. & Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behaviour 22, 1-63.
158. Snook, R. R. (2005). Sperm in competition: not playing by the numbers. Trends in Ecology & Evolution 20, 46-53.
159. Sommer, V. & Reichard, U. (2000). Rethinking monogamy: the gibbon case. In Primate Males (ed. P. M. Kappeler ), pp. 159-168. Cambridge University Press, Cambridge.
160. Stanford, C. B. (1998). Chimpanzee and Red Colobus. Harvard University Press, Cambridge.
161. Stockley, P. (2004). Sperm competition in mammals. Human Fertility 7, 91-97.
162. Stumpf, R. M. & Boesch, C. (2005). Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Tai National Park, Cote d'Ivoire. Behavioral Ecology and Sociobiology 57, 511-524.
163. Stumpf, R. M., Emery Thompson, M. & Knott, C. D. (2008). A comparison of female mating strategies in Pan troglodytes and Pongo spp. International Journal of Primatology 29, 865-884.
164. Sugiyama, Y. (1968). Social organisation of chimpanzees in the Budongo Forest, Uganda. Primates 92, 225-258.
165. Sugiyama, Y. (2004). Demographic parameters and life history of chimpanzees at Bossou, Guinea. American Journal of Physical Anthropology 124, 154-165.
166. Takahata, Y., Ihobe, H. & Idani, G. (1996). Comparing copulations of chimpanzees and bonobos: do females exhibit proceptivity or receptivity?. In Great Ape Societies (eds W. C. McGrew, L. F. Marchant and T. Nishida ), pp. 146-155. Cambridge University Press, Cambridge.
167. Tanaka, I. & Takefushi, H. (1993). Elimination of external parasites (lice) is the primary function of grooming in free-ranging Japanese macaques. Anthropological Science 101, 187-193.
168. Terry, R. L. (1970). Primate grooming as a tension reduction mechanism. Journal of Psychology 76, 129-136.
169. Trivers, R. L. (1972). Parental investment and sexual selection. In Sexual Selection and the Descent of Man 1871-1971 (ed. B. Campbell ), pp. 136-179. Aldine Atherton, Chicago.
170. Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology 6, 29-38.
171. Tutin, C. E. G. & McGinnis, P. R. (1981). Chimpanzee reproduction in the wild. In Reproductive Biology of the Great Apes (ed. C. E. Graham ), pp. 239-264. Academic Press, New York.
172. Uehara, S., Hiraiwa-Hasegawa, M., Hosaka, K. & Hamai, M. (1994). The fate of defeated alpha male chimpanzees in relation to their social networks. Primates 35, 49-55.
173. Vigilant, L., Hofreiter, M., Siedel, H. & Boesch, C. (2001). Paternity and relatedness in wild chimpanzee communities. Proceedings of the National Academy of Sciences of the United States of America 98, 12890-12895.
174. de Waal, F. B. M. (1996). Macaque social culture: development and perpetuation of affiliative networks. Journal of Comparative Psychology 110, 147-154.
175. de Waal, F. B. M. & Aureli, F. (1997). Conflict resolution and distress alleviation in monkeys and apes. Annals of the New York Academy of Sciences 807, 317-328.
176. de Waal, F. B. M. & van Roosmalen, A. (1979). Reconciliation and consolation among chimpanzees. Behavioral Ecology and Sociobiology 5, 55-66.
177. Wallis, J. (1992). Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. American Journal of Primatology 28, 101-113.
178. Wallis, J. (1997). A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. Journal of Reproduction and Fertility 109, 297-307.
179. Wallis, J. & Lemmon, W. B. (1986). Social behavior and genital swelling in pregnant chimpanzees (Pan troglodytes). American Journal of Primatology 10, 171-183.
180. Watts, D. P. (1998). Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behavioral Ecology and Sociobiology 44, 43-55.
181. Watts, D. P. (2000a). Grooming between male chimpanzees at Ngogo, Kibale National Park. I. Partner number and diversity and grooming reciprocity. International Journal of Primatology 21, 189-210.
182. Watts, D. P. (2000b). Grooming between male chimpanzees at Ngogo, Kibale National Park. II. Influence of male rank and possible competition for partners. International Journal of Primatology 21, 211-238.
183. Watts, D. P. (2002). Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139, 343-370.
184. Watts, D. P. (2007). Effects of male group size, parity, and cycle stage on female chimpanzee copulation rates at Ngogo, Kibale National Park, Uganda. Primates 48, 222-231.
185. Watts, D. P. & Mitani, J. C. (2000). Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda. Primates 41, 357-365.
186. Watts, D. P. & Mitani, J. C. (2001). Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138, 299-327.
187. Watts, D. P., Muller, M., Amsler, S. J., Mbabazi, G. & Mitani, J. C. (2006). Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda. American Journal of Primatology 68, 161-180.
188. Westneat, D. F., Sherman, P. W. & Morton, M. L. (1990). The ecology and evolution of extra-pair copulations in birds. Current Ornithology 7, 331-369.
189. Williams, J. M., Oehlert, G. W., Carlis, J. V. & Pusey, A. E. (2004). Why do male chimpanzees defend a group range? Animal Behaviour 68, 523-532.
190. Williams, J. M., Pusey, A. E., Carlis, J. V., Farm, B. P. & Goodall, J. (2002). Female competition and male territorial behaviour influence female chimpanzees' ranging patterns. Animal Behaviour 63, 347-360.
191. Wittig, R. M. & Boesch, C. (2005). How to repair relationships: reconciliation in wild chimpanzees (Pan troglodytes). Ethology 111, 736-763.
192. Wittig, R. M., Crockford, C., Lehmann, J., Whitten, P. L., Seyfarth, R. M. & Cheney, D. L. (2008). Focused grooming networks and stress alleviation in wild female baboons. Hormones and Behavior 54, 170-177.
193. Wolff, J. O. & Macdonald, D. W. (2004). Promiscuous females protect their offspring. Trends in Ecology & Evolution 19, 127-134.
194. Wrangham, R. W. (1975). The Behavioural Ecology of Chimpanzees in the Gombe National Park. PhD Thesis: Cambridge University.
195. Wrangham, R. W. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In Primate Ecology (ed. T. H. Clutton-Brock ), pp. 504-538. Academic Press, London.
196. Wrangham, R. W. (1979). Sex differences in chimpanzee dispersion. In The Great Apes (eds D. A. Hamburg and E. R. McCown ), pp. 481-490. Benjamin/Cummings Publishing Company, Menlo Park.
197. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour 75, 262-300.
198. Wrangham, R. W. (1986). Ecology and social relationships in two species of chimpanzee. In Ecology and Social Evolution: Birds and Mammals (eds D. I. Rubenstein and R. W. Wrangham ), pp. 352-378. Princeton University Press, Princeton.
199. Wrangham, R. W. (1993). The evolution of sexuality in chimpanzees and bonobos. Human Nature 4, 47-79.
200. Wrangham, R. W. (1999). Evolution of coalitionary killing. Yearbook of Physical Anthropology 42, 1-30.
201. Wrangham, R. W. (2000). Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In Primate Males: Causes and Consequences of Variation in Group Composition (ed. P. M. Kappeler ), pp. 248-258. Cambridge University Press, Cambridge.
202. Wrangham, R. (2002). The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion?. In Behavioural Diversity in Chimpanzees and Bonobos (eds C. Boesch, G. Hohmann and L. F. Marchant ), pp. 204-215. Cambridge University Press, Cambridge.
203. Wrangham, R. W. & Smuts, B. B. (1980). Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. Journal of Reproduction and Fertility. Supplement 28, 13-31.
204. Wrangham, R. W., Wilson, M. L. & Muller, M. N. (2006). Comparative rates of violence in chimpanzees and humans. Primates 47, 14-26.
205. Wroblewski, E. E., Murray, C. M., Keele, B. F., Schumacher-Stankey, J. C., Hahn, B. H. & Pusey, A. E. (2009). Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour 77, 873-885.
206. Zamma, K. (2002). Grooming site preferences determined by lice infection among Japanese Macaques in Arashiyama. Primates 43, 41-49.