Reproductive Ecology of Female Chimpanzees

American Journal of Primatology

Volumn 75, Issue 3, 2013, Pages 222-237

  Thompson, Melissa Emery ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Energetics; Hormones; Life history; Reproduction; Seasonality; Sexual behavior

Indexed keywords

AGGRESSION; BIOENERGETICS; BODY SIZE; BREEDING SEASON; CAPTIVE POPULATION; ENERGY FLOW; EUSOCIALITY; FEMALE; FORAGING EFFICIENCY; HOMINID; HORMONE; LIFE HISTORY; REPRODUCTIVE BIOLOGY; REPRODUCTIVE COST; REPRODUCTIVE EFFORT; REPRODUCTIVE STRATEGY; RESOURCE AVAILABILITY; SEASONALITY; SEXUAL BEHAVIOR; SEXUAL CONFLICT; WILD POPULATION;

ANIMAL; FEMALE; MATE CHOICE; PAN TROGLODYTES; PHYSIOLOGY; REPRODUCTION; REVIEW;

ANIMALS; FEMALE; MATING PREFERENCE, ANIMAL; PAN TROGLODYTES; REPRODUCTION;

MAMMALIA; PAN; PAN TROGLODYTES; PRIMATES;

EID: 84872617004     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22084     Document Type: Review

References (178)

1. Altmann J, Alberts SC. 2003a. Intraspecific variability in fertility and offspring survival in a non-human primate: behavioral control of ecological and social sources. In: Wachter K, editor. Offspring: human fertility behavior in a biodemographic perspective. Washington, DC: National Academy Press. p 140-169.
2. Altmann J, Alberts SC. 2003b. Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401-409.
3. Anderson DP, Nordheim EV, Boesch C. 2006. Environmental factors influencing the seasonality of estrus in chimpanzees. Primates 47:43-50.
4. Basabose AK. 2004. Fruit availability and chimpanzee party size at Kahuzi montane forest, Democratic Republic of Congo. Primates 45:211-219.
5. Bentley GR. 1985. Hunter-gatherer energetics and fertility: a reassessment of the !Kung San. Hum Ecol 13:79-109.
6. Bentley GR. 1999. Aping our ancestors: comparative aspects of reproductive ecology. Evol Anthropol 7:175-185.
7. Bercovitch FB. 1987. Female weight and reproductive condition in a population of olive baboons (Papio anubis). Am J Primatol 12:189-195.
8. Bercovitch FB, Strum SC. 1993. Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313-318.
9. Boesch C, Boesch-Achermann H. 2000. The chimpanzees of the Tai Forest: behavioural ecology and evolution. Oxford: Oxford University Press. 316 p.
10. Boesch C, Bole C, Eckhardt N, Boesch H. 2009. Altruism in forest chimpanzees: the case of adoption. PLoS ONE 5:e8901.
11. Boyd IL. 2000. State-dependent fertility in pinnipeds: contrasting capital and income breeders. Funct Ecol 14:623-630.
12. Brewer-Marsden S, Marsden D, Emery Thompson M. 2006. Demographic and female life history parameters of free-ranging chimpanzees at the Chimpanzee Rehabilitation Project, River Gambia National Park. Int J Primatol 27:391-410.
13. Brockman DK, van Schaik CP. 2005. Seasonality and reproductive function. In: Brockman DK, Van Schaik CP, editors. Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge: Cambridge University Press. p 269-305.
14. Bronikowski AM, Altmann J, Brockman DK, Cords M, Fedigan L, Pusey A, Stoinski T, Morris WF, Strier KB, Alberts SC. 2011. Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331:1325-1328.
15. Bygott JD. 1979. Agonistic behavior, dominance, and social structure in wild chimpanzees of the Gombe National Park. In: Hamburg DA, McCown ER, editors. Perspectives on human evolution, Vol. V: The great apes. Menlo Park: Benjamin/Cummings Publishing Co. p 405-427.
16. Chapman CA, Wrangham RW, Chapman LJ. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. In: McGrew WC, Marchant LF, Nishida T, editors. Great ape societies. Cambridge: Cambridge University Press. p 45-57.
17. Charnov EL, Berrigan D. 1993. Why do female primates have such long lifespans and so few babies? or Life in the slow lane. Evol Anthropol 1:191-194.
18. Chimfunshi. 2007. Chimfunshi wildlife orphanage. Available online at: http://www.chimfunshi.org.za/pages/innnews. html [accessed August 28, 2012].
19. Clark C. 1977. A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In: Chevalier-Skolnikoff S, Poirier F, editors. Primate bio-social development: biological, social and ecological determinants. New York: Garland Press. p 235-260.
20. Clutton-Brock T, Albon S, Guinness F. 1989. Fitness costs of gestation and lactation in wild mammals. Nature 337:260-262.
21. Coe CL, Connolly AC, Kraemer HC, Levine S. 1979. Reproductive development and behavior of captive female chimpanzees. Primates 20:571-582.
22. Constable JL, Ashley MV, Goodall J, Pusey AE. 2001. Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279-1300.
23. Courtenay J. 1987. Post-partum amenorrhoea, birth intervals and reproductive potential in captive chimpanzees. Primates 28:543-546.
24. Czekala NM, Shideler SE, Lasley BL. 1988. Comparisons of female reproductive hormone patterns in the hominoids. In: Schwartz JH, editor. Orang-utan biology. New York: Oxford University Press. p 117-122.
25. de Magalhaes JP, Costa J. 2009. A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol 22:1770-1774.
26. Deschner T, Boesch C. 2007. Can the patterns of sexual swelling cycles in female Tai chimpanzees by explained by the cost-of-sexual-attractiveness hypothesis? Int J Primatol 28:389-406.
27. 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. Anim Behav 66:551-560.
28. Deschner T, Heistermann M, Hodges K, Boesch C. 2004. Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 46:204-215.
29. Deschner T, Kratzsch J, Hohmann G. 2008. Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Horm Behav 54:620-626.
30. Di Bitetti MS, Janson CH. 2000. When will the stork arrive? Patterns of seasonality in neotropical primates. Am J Primatol 50:109-130.
31. Doran DM. 1997. Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Taï chimpanzees. Int J Primatol 18:183-206.
32. Dufour DL, Sauther ML. 2002. Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am J Hum Biol 14:584-602.
33. Dyke B, Gage T, Alford P, Swenson B, Williams-Blangero S. 1995. Model life table for captive chimpanzees. Am J Primatol 37:25-37.
34. Eissa MK, Obhrai MS, Docker MF, Lynch SS, Sawers RS, Newton RR. 1986. Follicular growth and endocrine profiles in spontaneous and induced conception cycles. Fertil Steril 53:81-87.
35. Ellison PT. 1995. Understanding natural variation in human ovarian function. In: Dunbar RIM, editor. Human reproductive decisions: biological and social perspectives. Proceedings of the Thirtieth Annual Symposium of the Galton Instititute, London, 1993. London: St. Martin's Press/The Galton Institute. p 22-51.
36. Ellison PT. 2003. Energetics and reproductive effort. Am J Hum Biol 15:342-351.
37. Ellison PT, Lipson SF, O'Rourke MT, Bentley GR, Harrigan AM, Panter-Brick C, Vitzthum V. 1993a. Population variation in ovarian function. Lancet 342:433-434.
38. Ellison PT, Panter-Brick C, Lipson SF, O'Rourke MT. 1993b. The ecological context of human ovarian function. Hum Reprod 8:2248-2258.
39. Ellison PT, Peacock NR, Lager C. 1989. Ecology and ovarian function among Lese women of the Ituri Forest, Zaire. Am J Phys Anthropol 78:519-526.
40. Ellison PT, Valeggia CR. 2003. C-peptide levels and the duration of lactational amenorrhea. Fertil Steril 80:1279-1280.
41. Emery MA, Whitten PL. 2003. Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 54:340-351.
42. Emery Thompson M. 2005a. Endocrinology and ecology of wild female chimpanzee reproduction. [Ph.D. Dissertation]. Cambridge: Harvard University.
43. Emery Thompson M. 2005b. Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am J Primatol 67:137-158.
44. Emery Thompson M, Alvarado L. 2012. Human sexual conflict and sexual coercion in comparative evolutionary perspective. In: Goetz A, Shackelford T, editors. Oxford handbook of sexual conflict in humans. New York: Oxford University Press. p 100-121.
45. Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW. 2007a. Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17:2150-2156.
46. Emery Thompson M, Kahlenberg SM, Gilby IC, Wrangham RW. 2007b. Core area quality is associated with variance in reproductive success among female chimpanzees at Kanyawara, Kibale National Park. An Behav 73:501-512.
47. Emery Thompson M, Knott CD. 2008. Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm Behav 53:526-535.
48. Emery Thompson M, Muller MN, Kahlenberg SM, Wrangham RW. 2010. Dynamics of social and energetic stress in wild female chimpanzees. Horm Behav 58:440-449.
49. Emery Thompson M, Muller MN, Wrangham RW. 2012. The energetics of lactation and the return to fecundity in wild Chimpanzees. Behav Ecol 23:1234-1241.
50. Emery Thompson M, Muller MN, Wrangham RW, Lwanga JS, Potts KB. 2009. Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55:299-305.
51. Emery Thompson M, Wrangham RW. 2006. Comparison of sex differences in gregariousness in fission-fusion species: reducing bias by standardizing for party size. In: Newton-Fisher NE, Notman H, Reynolds V, Paterson J, editors. Primates of Western Uganda. New York: Springer. p 209-226.
52. Emery Thompson M, Wrangham RW. 2008a. Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda. Am J Phys Anthropol 135:171-181.
53. Emery Thompson M, Wrangham RW. 2008b. Male mating interest varies with female fecundity in Pan troglodytes of Kanyawara, Kibale National Park. Int J Primatol 29:885-905.
54. Emery Thompson M, Wrangham RW, Reynolds V. 2006. Urinary estrone conjugates and reproductive parameters in Kibale (Kanyawara) and Budongo (Sonso) chimpanzees. In: Newton-Fisher NE, Notman H, Reynolds V, Paterson J, editors. Primates of Western Uganda. New York: Springer. p 227-246.
55. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
56. Flint DJ, Sinnett-Smith PA, Clegg RA, Vernon RG. 1979. Role of insulin receptors in the changing metabolism of adipose tissue during pregnancy and lactation in the rat. Biochem J 182:421-427.
57. Gadgil M, Bossert WH. 1970. Life historical consequences of natural selection. Am Nat 104:1-24.
58. Ganzhorn JU, Klaus S, Ortmann S, Schmid J. 2003. Adaptations to seasonality: some primate and nonprimate examples. In: Kappeler PM, Pereira ME, editors. Primate life histories and socioecology. Chicago: University of Chicago Press. p 132-144.
59. Georgiev A, Emery Thompson M, Lokasola A, Wrangham RW. 2011. Seed-predation by bonobos (Pan paniscus) at Kokolopori, Democratic Republic of Congo. Primates 52:309-314.
60. Girard-Buttoz C, Higham JP, Heistermann M, Wedegartner S, Maestripieri D, Engelhardt A. 2011. Urinary C-peptide measurement as a marker of nutritional status in macaques. PLoS ONE 6:e18042.
61. Gittleman JL, Thompson SD. 1988. Energy allocation in mammalian reproduction. Am Zool 28:863-875.
62. Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior. Cambridge: Belknap Press. 673 p.
63. Graham CE. 1979. Reproductive function in aged female chimpanzees. Am J Phys Anthropol 50:291-300.
64. Graham CE. 1981. Menstrual cycle of the great apes. In: Graham CE, editor. Reproductive biology of the great apes. New York: Academic Press. p 1-43.
65. Graham CE, Collins DC, Robinson H, Preedy JRK. 1972. Urinary levels of estrogens and pregnanediol and plasma levels of progesterone during the menstrual cycle of the chimpanzee: relationship to the sexual swellings. Endocrinology 91:13-24.
66. Graham CE, Gould KG, Wright K, Collins DC. 1978. Luteal estrogen secretion and decidualisation in the chimpanzee. In: Chivers DJ, Ford EHR, editors. Recent advances in primatology, Vol IV: Medicine. New York: Academic Press. p 209-211.
67. Hamada Y, Udono T. 2002. Longitudinal analysis of length growth in the chimpanzee (Pan troglodytes). Am J Phys Anthropol 118:268-284.
68. Hamada Y, Udono T, Teramoto M, Sugawara T. 1996. The growth pattern of chimpanzees: somatic growth and reproductive maturation in Pan troglodytes. Primates 37:279-295.
69. Hanwell A, Peaker M. 1977. Physiological effects of lactation on the mother. Symp Zool Soc London 41:297-311.
70. Harris TR, Chapman CA, Monfort SL. 2010. Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21:46-56.
71. Hashimoto C, Furuichi T, Tashiro Y. 2001. What factors affect the size of chimpanzee parties in the Kalinzu Forest, Uganda? Examination of fruit abundance and number of estrous females. Int J Primatol 22:947-959.
72. Hendrickx AG, Nelson G. 1971. Reproductive failure. In: Hafez ESE, editor. Comparative reproduction of non-human primates. Springfield: Charles C. Thomas. p 403-425.
73. Hermes R, Hildebrandt TB, Goritz F. 2004. Reproductive problems directly attributable to long-term captivity-asymmetric reproductive aging. Anim Reprod Sci 82-83:49-60.
74. Hermes R, Hildebrandt TB, Walzer C, Goritz F, Patton ML, Silinski S, Anderson MJ, Reid CE, Wibbelt G, Tomasova K et al. 2006. The effect of long non-reproductive periods on the genital health in captive female white rhinoceroses (Ceratotherium simum simum, C.s. cottoni). Theriogenology 65:1492-1515.
75. Herndon JG, Lacreuse A. 2009. Commentary: "Reproductiveaging in captive and wild common chimpanzees: Factors influencing the rate of follicular depletion," by S. Atsalis and E. Videan, American Journal of Primatology 71, 271-282 (2009). Am J Primatol 71:891-892.
76. Higham JP, Heistermann M, Maestripieri D. 2011. The energetics of male-male endurance rivalry in free-ranging rhesus macaques (Macaca mulatta). Anim Behav 81:1001-1007.
77. Hill K, Boesch C, Goodall J, Pusey AE, Williams J, Wrangham RW. 2001. Mortality rates among wild chimpanzees. J Hum Evol 40:437-450.
78. Itoh N, Nishida T. 2007. Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates 48:87-96.
79. Janson CH, Goldsmith M. 1995. Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326-336.
80. Janson CH, Verdolin J. 2005. Seasonality of primate births in relation to climate. In: Brockman DK, Van Schaik CP, editors. Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge: Cambridge University Press. p 307-350.
81. Jasienska G, Ellison PT. 1998. Physical work causes suppression of ovarian function in women. Proc R Soc Lond B 265:1847-1851.
82. Jones JH, Wilson ML, Murray CM, Pusey A. 2010. Phenotypic quality influences fertility in Gombe chimpanzees. J Anim Ecol 79:1262-1269.
83. Jones KP, Walker LC, Anderson D, Lacreuse A, Robson SL, Hawkes K. 2007. Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biol Reprod 77:247-251.
84. Jones RG, Ilic V, Williamson DH. 1984. Physiological significance of altered insulin metabolism in the conscious rat during lactation. Biochem J 220:455-460.
85. Kahlenberg SM, Emery Thompson M, Muller MN. 2008a. Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Anim Behav 76:1497-1509.
86. Kahlenberg SM, Emery Thompson M, Wrangham RW. 2008b. Female competition over core areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda. Int J Primatol 29:931-947.
87. Knott CD. 2001. Ape models of female reproductive ecology. In: Ellison PT, editor. Reproductive ecology and human evolution. Chicago: Aldine. p 429-463.
88. Lehmann J, Boesch C. 2008. Sexual differences in chimpanzee sociality. Int J Primatol 29:65-81.
89. Leigh S, Shea BT. 1996. Ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43-65.
90. Leonard WR, Robertson ML. 1997. Comparative primate energetics and hominid evolution. Am J Phys Anthropol 102:265-281.
91. Li H, Nakajima ST, Chen J, Todd HE, Jw O, Bl L. 2001. Differences in hormonal characteristics of conceptive versus nonconceptive cycles. Fertil Steril 75:549-553.
92. Lindburg DG. 1987. Seasonality of reproduction in primates. In: Mitchell G, Erwin JM, editors. Comparative primate biology, Volume 2B: behavior, cognition, and motivation. New York: Alan R. Liss, Inc. p 167-218.
93. Lipson SF, Ellison PT. 1996. Comparison of salivary steroid profiles in naturally occurring conception and non-conception cycles. Hum Reprod 11:2090-2096.
94. Martin RD. 1984. Scaling effects and adaptive strategies in mammalian lactation. Symp Zool Soc London 51:87-117.
95. Marzke M, Young D, Hawkey D, Su S, Fritz J, Alford P. 1996. Comparative analysis of weight gain, hand/wrist maturation and dental emergence rates in chimpanzees aged 0-24. Am J Phys Anthropol 99:175-190.
96. Masters AM, Markham RJ. 1991. Assessing reproductive status in orang-utans by using urinary estrone. Zoo Biol 10:197-207.
97. Matsumoto-Oda A, Hosaka K, Huffman MA, Kawanaka K. 1998. Factors affecting party size in chimpanzees of the Mahale mountains. Int J Primatol 19:999-1011.
98. McFarland R. 1997. Female primates: fat or fit? In: Morbeck ME, Galloway A, Zihlman AL, editors. The evolving female: a life-history perspective. Princeton, NJ: Princeton University Press. p 163-176.
99. Mitani JC, Gros-Louis J, Richard AF. 1996. Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primaes. Am Nat 147:966-980.
100. Mitani JC, Watts DP, Lwanga JS. 2002. Ecological and social correlates of chimpanzee party size and composition. In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 102-111.
101. Muller MN. 2002. Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 112-124.
102. Muller MN, Emery Thompson M, Kahlenberg SM, Wrangham RW. 2011. Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behav Ecol Sociobiol 65:921-933.
103. Muller MN, Emery Thompson M, Wrangham RW. 2006. Male chimpanzees prefer mating with old females. Curr Biol 16:2234-2238.
104. Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham RW. 2007. Male coercion and the costs of promiscuous mating for female chimpanzees. Proc R Soc Lond B 274:1009-1014.
105. Muller MN, Kahlenberg SM, Wrangham RW. 2009. Male aggression against females and sexual coercion in chimpanzees. In: Muller MN, Wrangham RW, editors. Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Cambridge, MA: Harvard University Press. p 184-217.
106. Murray C, Eberly L, Pusey A. 2006. Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behav Ecol 17:1020-1028.
107. Murray C, Mane S, Pusey A. 2007. Dominance rank influences female space use in wild chimpanzees, Pan troglodytes: towards an ideal despotic distribution. Anim Behav 74:1795-1804.
108. Nadler RD, Graham CE, Gosselin RE, Collins DC. 1985. Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycles of the chimpanzee (Pan troglodytes). Am J Primatol 9:273-284.
109. Nash LT. 1984. Diet and breeding seasonality among prosimians. Am J Phys Anthropol 63:198.
110. Nishida T. 1989. Social interactions between resident and immigrant female chimpanzees. In: Heltne PG, Marquardt LA, editors. Understanding chimpanzees. Cambridge: Harvard University Press. p 68-89.
111. Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, 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. Am J Primatol 59:99-121.
112. Norman AW, Litwack G. 1997. Hormones. San Diego, CA: Academic Press.
113. Oftedal OT. 1984. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp Zool Soc London 51:33-85.
114. Ozasa H, Gould KG. 1982. Demonstration and characterization of estrogen receptor in chimpanzee sex skin: correlation between nuclear receptor levels and degree of swelling. Endocrinology 111:125-131.
115. Pagel M, Harvey PH. 1988. How mammals produce large-brained offspring. Evolution 42:948-957.
116. Panter-Brick C, Lotstein DS, Ellison PT. 1993. Seasonality of reproductive function and weight loss in rural Nepali women. Hum Reprod 8:684-690.
117. Parga JA, Lessnau RG. 2005. Female age-specific reproductive rates, birth seasonality, and infant mortality of ring-tailed Lemurs on St. Catherines Island: 17-year reproductive history of a free-ranging colony. Zoo Biol 24:295-309.
118. Pepper JW, Mitani JC, Watts DP. 1999. General gregariousness and specific social preferences among wild chimpanzees. Int J Primatol 20:613-632.
119. Potts KB, Watts DP, Wrangham RW. 2011. Comparative feeding ecology of two communities of chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. Int J Primatol 32:669-690.
120. Pusey A, Murray C, Wallauer W, Wilson M, Wroblewski E, Goodall J. 2008. Severe aggression among female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania. Int J Primatol 29:949-973.
121. Pusey AE. 1980. Inbreeding avoidance in chimpanzees. Anim Behav 28:543-552.
122. Pusey AE. 1990. Behavioural changes at adolescence in chimpanzees. Behaviour 115:203-245.
123. Pusey AE, Packer C. 1987. Dispersal and philopatry. In: Smuts B, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 250-266.
124. Pusey AE, Williams J, Goodall J. 1997. The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828-831.
125. Reichert KE, Heistermann M, Hodges JK, Boesch C, Hohmann G. 2002. What females tell males about their reproductive status: are morphological and behavioural cues reliable signals of ovulation in bonobos (Pan paniscus)? Ethology 108:583-600.
126. Richard AF, Dewar RE, Schwartz M, Ratsirarson J. 2000. Mass change, environmental variability and female fertility in wild Propithecus verreauxi. J Hum Evol 39:381-391.
127. Richard AF, Dewar RE, Schwartz M, Ratsirarson J. 2002. Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). J Zool 256:421-436.
128. Rijt-Plooij HHC, Plooij FX. 1987. Growing independence, conflict and learning in mother-infant relations in free-ranging chimpanzees. Behaviour 101:1-86.
129. Rubenstein A, Clark J, Melani F, Steiner D. 1969. Secretion of proinsulin C-peptide by pancreatic bold beta cells and its circulation in blood. Nature 224:697-699.
130. Schneider JE, Wade GN. 2000. Inhibition of reproduction in service of energy balance. In: Wallen K, Schneider JE, editors. Reproduction in context: social and environmental influences on reproduction. Cambridge: The MIT Press. p 35-82.
131. Schwartz M, Figlewicz D, Baskin D, Woods S, Porte DJ. 1992. Insulin in the brain: a hormonal regulator of energy balance. Endocr Rev 13:387-414.
132. Shimizu K, Udono T, Tanaka C, Narushima E, Yoshihara M, Takeda M, Tanahashi A, van Elsacker L, Hayashi M, Takenaka O. 2003. Comparative study of urinary reproductive hormones in great apes. Primates 44:183-190.
133. Skorupa JP. 1988. The effects of selective timber harvesting on rain-forest primates in Kibale Forest, Uganda [Ph.D. Dissertation]. Davis: University of California. 519 p.
134. Smith AH, Butler TM, Pace N. 1975. Weight growth of colony-reared chimpanzees. Folia Primatol 24:29-59.
135. Stearns S. 1992. Evolution of life histories. Oxford: Oxford University Press.
136. Stearns SC. 1989. Trade-offs in life history evolution. Funct Ecol 3:259-268.
137. Strack A, Sebastian R, Schwartz M, Dallman M. 1995. Glucocorticoids and insulin: reciprocal signals for energy balance. Am J Physiol Regul Integr Comp Physiol 268:R142-R149.
138. Strier KB, Mendes SL, Santos RR. 2001. Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and Northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 55:87-100.
139. Stumpf RM, Boesch C. 2006. The efficacy of female choice in chimpanzees of the Taï Forest, Côte d'Ivoire. Behav Ecol Sociobiol 60:749-765.
140. Stumpf RM, Emery Thompson M, Muller M, Wrangham R. 2009. The context of female dispersal in Kanyawara chimpanzees. Behaviour 146:629-656.
141. Sugiyama Y. 1994. Age-specific birth rate and lifetime reproductive success of chimpanzees at Bossou, Guinea. Am J Primatol 32:311-318.
142. Sugiyama Y. 2004. Demographic parameters and life history of chimpanzees at Bossou, Guinea. Am J Phys Anthropol 124:154-165.
143. Suzuki S, Noma N, Izawa K. 1998. Inter-annual variation of reproductive parameters and fruit availability in two populations of Japanese macaques. Primates 39:313-324.
144. Tigas S, Sunehag A, Haymond HW. 2002. Metabolic adaptation to feeding and fasting during lactation in humans. J Clin Endocrinol Metab 87:302-307.
145. Townsend SW, Slocombe KE, Emery Thompson M, Zuberbuhler K. 2007. Female-led infanticide in wild chimpanzees. Curr Biol 17:R355-356.
146. Turke PW. 1984. Effects of ovulatory concealment and synchrony on protohominid mating systems and parental roles. Ethol Sociobiol 5:33-44.
147. Tutin CEG. 1979. Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29-38.
148. Tutin CEG. 1994. Reproductive success story: variability among chimpanzees and comparisons with gorillas. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG, editors. Chimpanzee cultures. Cambridge: Harvard University Press. p 181-194.
149. Tutin CEG, McGinnis PR. 1981. Chimpanzee reproduction in the wild. In: Graham CE, editor. Reproductive biology of the great apes: comparative and biomedical perspectives. New York: Academic Press. p 239-264.
150. Ulijaszek SJ. 2002. Comparative energetics of primate fetal growth. Am J Hum Biol 14:603-608.
151. Valeggia C, Ellison PT. 2009. Interactions between metabolic and reproductive functions in the resumption of postpartum fecundity. Am J Hum Biol 21:559-566.
152. Valeggia CR, Ellison PT. 2004. Lactational amenorrhoea in well-nourished Toba women of Formosa, Argentina. J Biosoc Sci 36:573-595.
153. van Schaik CP, Brockman DK. 2005. Seasonality in primate ecology, reproduction, and life history. In: Brockman DK, van Schaik CP, editors. Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge: Cambridge University Press. p 3-20.
154. van Schaik CP, van Noordwijk MA. 1985. Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques (Macaca fascicularis). J Zool Lond 206:533-549.
155. Vernon RG. 1989. Endocrine control of metabolic adaptation during lactation. Proc Nutr Soc 48:23-32.
156. Videan EN, Fritz J, Heward CB, Murphy J. 2006. The effects of aging on hormone and reproductive cycles in female chimpanzees (Pan troglodytes). Comp Med 56:291-299.
157. Wallis J. 1992. Socioenvironmental effects on timing of first postpartum cycles in chimpanzees. In: Nishida T, McGrew WC, Marler P, Pickford M, de Waal FBM, editors. Topics in primatology: human origins. Tokyo: University of Tokyo Press. p 119-130.
158. Wallis J. 1994. Socioenvironmental effects on first full anogenital swellings in adolescent female chimpanzees. In: Roeder JJ, Thierry B, Anderson JR, Herrenschmidt N, editors. Current primatology, Vol II: social development, learning, and behaviour. Strasbourg: University of Louis Pasteur. p 25-32.
159. Wallis J. 1995. Seasonal influence on reproduction in chimpanzees of Gombe National Park. Int J Primatol 16:435-451.
160. Wallis J. 1997. A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fertil 109:297-307.
161. Wallis J. 2002. Seasonal aspects of reproduction and sexual behavior in two chimpanzee populations: a comparison of Gombe (Tanzania) and Budongo (Uganda). In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 181-191.
162. Wasser SK. 1996. Reproductive control in wild baboons measured by fecal steroids. Biol Reprod 55:393-399.
163. Wasser SK, Barash DP. 1983. Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol 58:513-538.
164. Watts DP. 1998. Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43-55.
165. Watts DP. 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.
166. Watts DP, Mitani JC. 2001. Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138:299-327.
167. Watts DP, Muller MN, Amsler SJ, Mbabazi G, Mitani JC. 2006. Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda. Am J Primatol 68:161-180.
168. Williams J, Oehlert GW, Carlis JV, Pusey AE. 2004. Why do male chimpanzees defend a group range? Anim Behav 68:523-532.
169. Williams JM, Pusey AE, Carlis JV, Farm BP, Goodall J. 2002. Female competition and male territorial behaviour influence female chimpanzees' ranging patterns. Anim Behav 63:347-360.
170. Wilson ML, Kahlenberg SM, Wells M, Wrangham RW. 2012. Ecological and social factors affect the occurrence and outcomes of intergroup encounters in chimpanzees. Anim Behav 83:277-291.
171. Wilson ML, Wrangham RW. 2003. Intergroup relations in chimpanzees. Ann Rev Anthropol 32:363-392.
172. Wittig RM, Boesch C. 2003. Food competition and linear dominance hierarchy among female chimpanzees of the Taï National Park. Int J Primatol 24:847-867.
173. Wrangham RW. 1993. The evolution of sexuality in chimpanzees and bonobos. Hum Nat 4:47-79.
174. Wrangham RW. 2000. Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler PM, editor. Primate males: causes and consequences of variation in group composition. Cambridge: Cambridge University Press. p 248-258.
175. Wrangham RW. 2002. The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 204-215.
176. Wrangham RW, Chapman CA, Clark AP, Isabirye-Basuta G. 1996. Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great ape groups. In: McGrew WC, Marchant LF, Nishida T, editors. Great ape societies. Cambridge: Cambridge University Press. p 45-57.
177. Wroblewski EE, Murray CM, Keele BF, Schumaker-Stankey JC, Hahn BH, Pusey AE. 2009. Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77:873-885.
178. Young WC, Yerkes RM. 1943. Factors influencing the reproductive cycle in the chimpanzee; the period of adolescent sterility and related problems. Endocrinology 33:121-154.