Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone, Dihydrotestosterone, and Glucocorticoids

International Journal of Primatology

Volumn 35, Issue 3-4, 2014, Pages 643-660

  Schoof, Valérie A M ^a   Jack, Katharine M ^a   Ziegler, Toni E ^b  

^a TULANE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Allostatic load; Androgens; Dominance; Fertile females; Reproductive strategies

Indexed keywords

ADULT; BEHAVIORAL RESPONSE; DOMINANCE; FEMALE; FERTILITY; MALE; PRIMATE; REPRODUCTIVE EFFORT; REPRODUCTIVE SUCCESS; SEASON; TESTOSTERONE;

CAMEROON; COSTA RICA; GUANACASTE; NORD OUEST PROVINCE; SANTA;

CEBUS; CEBUS CAPUCINUS; PRIMATES;

EID: 84906054036     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-013-9742-4     Document Type: Article

References (76)

1. Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Salzman, W., Snowdon, C. T., Ziegler, T. E., Banjevic, M., Garland, T. J., & Sapolsky, R. M. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior, 43, 67-82.
2. Arlet, M. E., Grote, M. N., Molleman, F., Isbell, L. A., & Carey, J. R. (2009). Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena). Hormones and Behavior, 55, 210-216.
3. Arlet, M. E., Kaasik, A., Molleman, F., Isbell, L., Carey, J. R., & Mänd, R. (2011). Social factors increase fecal testosterone levels in wild male gray-cheeked mangabeys (Lophocebus albigena). Hormones and Behavior, 59, 605-611.
4. Bales, K. L., French, J. A., McWilliams, J., Lake, R. A., & Dietz, J. M. (2006). Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leotopithecus rosalia). Hormones and Behavior, 49, 88-95.
5. Beehner, J. C., Bergman, T. J., Cheney, D. L., Seyfarth, R. M., & Whitten, P. L. (2006). Testosterone predicts future dominance rank and mating activity among male chacma baboons. Behavioral Ecology and Sociobiology, 59, 469-479.
6. Bergman, T. J., Beehner, J. C., Cheney, D. L., Seyfarth, R. M., & Whitten, P. L. (2005). Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Animal Behaviour, 70, 703-713.
7. Braude, S., Tang-Martinez, Z., & Taylor, G. (1999). Stress, testosterone, and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345-350.
8. Brockman, D. K., Whitten, P. L., Richard, A. F., & Schneider, A. (1998). Reproduction in free ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression. American Journal of Physical Anthropology, 105, 137-151.
9. Carnegie, S. D., Fedigan, L. M., & Ziegler, T. E. (2005). Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus). American Journal of Primatology, 67, 51-68.
10. Carnegie, S. D., Fedigan, L. M., & Ziegler, T. E. (2006). Post-conceptive mating in white-faced capuchins, Cebus capucinus: Hormonal and sociosexual patterns of cycling, noncycling, and pregnant females. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior, and conservation (pp. 387-409). New York: Springer Science + Business Media.
11. Carnegie, S. D., Fedigan, L. M., & Melin, A. D. (2011a). Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. International Journal of Primatology, 32, 1076-1090.
12. Carnegie, S. D., Fedigan, L. M., & Ziegler, T. E. (2011b). Social and environmental factors affecting fecal glucocorticoids in wild, female white-faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 861-869.
13. Charpentier, M., Peignot, P., Hossaert-McKey, M., Gimenez, O., Setchell, J. M., & Wickings, E. J. (2005). Constraints on control: Factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behavioral Ecology, 16, 614-623.
14. Creel, S. (2001). Social dominance and stress hormones. Trends in Ecology and Evolution, 16, 491-497.
15. Di Fiore, A. (2003). Molecular genetic approaches to the study of primate behavior, social organization, and reproduction. Yearbook of Physical Anthropology, 46, 62-99.
16. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans (2nd ed.). Oxford: Oxford University Press.
17. Fedigan, L. M. (1993). Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus). International Journal of Primatology, 14, 853-877.
18. Fedigan, L. M., Carnegie, S. D., & Jack, K. M. (2008). Predictors of reproductive success in female white-faced capuchins. American Journal of Physical Anthropology, 137, 82-90.
19. Fedigan, L. M., & Jack, K. M. (2012). Tracking monkeys in Santa Rosa: Lessons from a regenerating tropical dry forest. In P. M. Kappeler & D. Watts (Eds.), Long-term field studies of primates (pp. 165-184). New York: Springer Science + Business Media.
20. Fichtel, C., Kraus, C., Ganswindt, A., & Heistermann, M. (2007). Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Hormones and Behavior, 51, 640-648.
21. Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge, U. K.: Cambridge University Press.
22. Gangestad, S. W., & Thornhill, R. (2008). Human oestrus. Proceedings of the Royal Society Biological Sciences, 275, 991-1000.
23. Gesquiere, L. R., Learn, N. H., Carolina, M., Simao, M. C. M., Onyango, P. O., Alberts, S. C., & Altmann, J. (2011). Life at the top: Rank and stress in wild male baboons. Science, 333, 357-360.
24. Ginther, A. J., Ziegler, T. E., Carlson, A. A., & Snowdon, C. T. (2002). Sexual development in cotton-top tamarin males. Biology of Reproduction, 66, 282-290.
25. Ginther, A. J., Ziegler, T. E., & Snowdon, C. T. (2001). Reproductive biology of captive male cotton-top tamarin monkeys as a function of social environment. Animal Behaviour, 61, 65-78.
26. Girard-Buttoz, C., Heistermann, M., Krummel, S., & Engelhardt, A. (2009). Seasonal and social influences fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiology and Behavior, 98, 168-175.
27. Gould, L., & Ziegler, T. E. (2007). Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta). American Journal of Primatology, 69, 1-15.
28. Gould, L., Ziegler, T. E., & Wittwer, D. J. (2005). Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar. American Journal of Primatology, 67, 5-23.
29. Goymann, W., & Wingfield, J. C. (2004). Allostatic load, social status and stress hormones: The costs of social status matter. Animal Behaviour, 67, 591-602.
30. Griffin, J. E., & Wilson, J. D. (1998). Disorders of the testis and male reproductive tract. In J. D. Wilson, D. W. Foster, H. M. Kronenberg, & P. R. Larsen (Eds.), Williams textbook of endocrinology (9th ed., pp. 819-875). Philadelphia: W. B. Saunders.
31. Hirschenhauser, K., & Oliveira, R. I. (2006). Social modulation of androgens in vertebrates: meta-analyses of the challenge hypothesis. Animal Behaviour, 71, 265-277.
32. Hirschfield, M. F., & Tinkle, D. W. (1975). Natural selection and the evolution of reproductive effort. Proceedings of the National Academy of Sciences of the USA, 72, 2227-2231.
33. Jack, K. M. (2003). Explaining variation in affiliative relationships among male white-faced capuchins (Cebus capucinus). Folia Primatologica, 74, 1-16.
34. Jack, K. M., & Fedigan, L. M. (2006). Why be alpha male? Dominance and reproductive success in wild white-faced capuchins (Cebus capucinus). In A. Estrada, P. Garber, M. A. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior and conservation (pp. 367-386). New York: Springer Science + Business Media.
35. Kraus, C., Heistermann, M., & Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: A subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiology and Behavior, 66, 855-861.
36. Lynch, J. W., Ziegler, T. E., & Strier, K. B. (2002). Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus paella nigritus. Hormones and Behavior, 41, 275-287.
37. Maggioncalda, A., Sapolsky, R., & Czekala, N. (1999). Reproductive hormone profiles in captive male orangutans: Implications for understanding developmental arrest. American Journal of Physical Anthropology, 109, 19-32.
38. Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness-related benefits of dominance in primates. American Journal of Physical Anthropology, 147, 652-660.
39. Manson, J. H., Perry, S., & Parish, A. R. (1997). Nonconceptive sexual behavior in bonobos and capuchins. International Journal of Primatology, 18, 767-786.
40. McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2-15.
41. Meusy-Dessolle, N., & Dang, D. C. (1985). Plasma concentrations of testosterone, dihydrotestosterone, delta 4-androstenedione, dehydroepiandrosterone and oestradiol-17 beta in the crab-eating monkey (Macaca fascicularis) from birth to adulthood. Journal of Reproduction and Fertility, 74, 347-359.
42. Miller, S. L., & Maner, J. K. (2010). Scent of a woman: men's testosterone responses to ovulatory ovulation cues. Psychological Science, 21, 276-284.
43. Muller, M. N., & Wrangham, R. W. (2004a). Dominance, aggression and testosterone in wild chimpanzees: A test of the "challenge hypothesis. Animal Behaviour, 67, 113-123.
44. Muller, M. N., & Wrangham, R. W. (2004b). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 55, 332-340.
45. Muniz, L., Perry, S., Manson, J. H., Gilkenson, H., Gros-Louis, J., & Vigilant, L. (2010). Male dominance and reproductive success in wild white-faced capuchins (Cebus capucinus) at Lomas Barbudal, Costa Rica. American Journal of Primatology, 72, 1118-1130.
46. Ostner, J., Kappeler, P. M., & Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 52, 485-495.
47. Ostner, J., Kappeler, P. M., & Heistermann, M. (2008a). Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 62, 627-638.
48. Ostner, J., Heistermann, M., & Schülke, O. (2008b). Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior, 54, 613-619.
49. Ostner, J., Heistermann, M., & Schülke, O. (2011). Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis). Hormones and Behavior, 59, 105-113.
50. Perry, S. (1996). Intergroup encounters in wild white-faced capuchins (Cebus capucinus). International Journal of Primatology, 17, 309-330.
51. Perry, S. (1997). Male-female relationships in wild white-faced capuchins, Cebus capucinus. Behaviour, 134, 477-510.
52. Perry, S. (1998). Male-male social relationships in wild white-faced capuchins, Cebus capucinus. Behaviour, 135, 139-172.
53. Plant, T. M., & Witchel, S. F. (2006). Puberty in non-human primates and humans. In J. D. Neill (Ed.), Knobil and Neill's physiology of reproduction (3rd edition, Vol. 2, pp. 2177-2230). St. Louis: Elsevier Academic Press.
54. Rose, L. M. (1998). Behavioral ecology of white-faced capuchins (Cebus capucinus) in Costa Rica. PhD dissertation, Washington University, St. Louis.
55. Rose, L. M., & Fedigan, L. M. (1995). Vigilance in white-faced capuchins, Cebus capucinus, in Costa Rica. Animal Behaviour, 49, 63-70.
56. Rostal, D. C., Glick, B. B., Eaton, G. G., & Resko, J. A. (1986). Seasonality of adult male Japanese macaques (Macaca fuscata): Androgens and behavior in a confined troop. Hormones and Behavior, 20, 452-462.
57. Sapolsky, R. M. (1993). The physiology of dominance in stable versus unstable social hierarchies. In W. A. Mason & S. P. Mendoza (Eds.), Primate social conflict (pp. 171-204). Albany, NY: State University of New York Press.
58. Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648-652.
59. Schoof, V. A. M., & Jack, K. M. (2013). The association of intergroup encounters, dominance status, and fecal androgen and glucocorticoid profiles in wild male white-faced capuchins (Cebus capucinus). American Journal of Primatology, 75, 107-115.
60. Schoof, V. A. M., & Jack, K. M. (in press). Male social bonds: Strength and quality among coresident white-faced capuchin monkeys (Cebus capucinus). Behaviour.
61. Schoof, V. A. M., Jack, K. M., & Carnegie, S. D. (2011). Rise to power: A case study of male fecal androgen and cortisol levels before and after a non-aggressive rank change in a group of wild white-faced capuchins (Cebus capucinus). Folia Primatologica, 82, 299-307.
62. Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2008). Social correlates of testosterone and ornamentation in male mandrills. Hormones and Behavior, 54, 365-372.
63. Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior, 58, 720-728.
64. Stocco, D. M., & McPhaul, J. M. (2006). Physiology of testicular steroidogenesis. In J. D. Neill (Ed.), Knobil and Neill's physiology of reproduction (3rd ed., pp. 977-1016). St. Louis: Elsevier.
65. Strier, K. B., Lynch, J. W., & Ziegler, T. E. (2003). Hormonal changes during the mating and conception seasons of wild Northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology, 61, 85-99.
66. Strier, K. B., Ziegler, T. E., & Wittwer, D. J. (1999). Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Hormones and Behavior, 35, 125-134.
67. Surbeck, M., Deschner, T., Weltring, A., & Hohmann, G. (2012). Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Hormones and Behavior, 62, 27-35.
68. van Belle, S., Estrada, A., Ziegler, T. E., & Strier, K. B. (2009). Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra). Hormones and Behavior, 56, 355-363.
69. van Schaik, C. P., van Noordwijk, M. A., & Nunn, C. L. (1999). Sex and social evolution in primates. In P. Lee (Ed.), Comparative primate socioecology (pp. 204-231). Cambridge, U. K.: Cambridge University Press.
70. Wallen, K. (2005). Hormonal influences on sexually differentiated behavior in nonhuman primates. Frontiers in Neuroendocrinology, 26, 7-26.
71. Weiner, J. S., Marcelli, M., & Lamb, D. J. (1996). Molecular determinants of sexual differentiation. World Journal of Urology, 14, 278-294.
72. Wingfield, J. C., Hegner, R. E., Dufty, A. M. J., & Ball, G. F. (1990). The "challenge hypothesis": Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136, 829-846.
73. Wingfield, J. C., Lynn, S. E., & Soma, K. K. (2001). Avoiding the 'costs' of testosterone: ecological basis of hormone-behavior interactions. Brain, Behavior and Evolution, 57, 239-251.
74. 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.
75. Ziegler, T. E., Bridson, W., Snowdon, C., & Eman, S. (1987). Urinary gonadotropin and estrogen excretion during the postpartum estrus, conception, and pregnancy in the cotton-top tamarin (Saguinus oedipus oedipus). American Journal of Primatology, 12, 127-140.
76. Ziegler, T. E., Schultz-Darken, N. J., Scott, J. J., Snowdon, C. T., & Ferris, C. F. (2005). Neuroendocrine response to female ovulatory odors upon social condition in male common marmosets, Callithrix jacchus. Hormones and Behavior, 47, 56-64.