What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago

American Journal of Primatology

Volumn 78, Issue 1, 2016, Pages 92-105

  Maestripieri, Dario ^a   Georgiev, Alexander V ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Competition; Cortisol; Reproduction; Rhesus macaques; Social evolution; Stress

Indexed keywords

ABUNDANCE; COMPETITION (ECOLOGY); CONCENTRATION (COMPOSITION); EXPERIMENTAL STUDY; PHYSIOLOGICAL RESPONSE; PRIMATE; PROTEIN; REPRODUCTION; REPRODUCTIVE EFFORT; SEASONAL VARIATION; SOCIAL BEHAVIOR; SURVIVAL;

CAYO SANTIAGO; PUERTO RICO;

MACACA; MACACA MULATTA; PRIMATES;

HYDROCORTISONE;

ANIMAL; BLOOD; FEMALE; PHYSIOLOGY; PUERTO RICO; REPRODUCTION; RHESUS MONKEY; SOCIAL DOMINANCE;

ANIMALS; FEMALE; HYDROCORTISONE; MACACA MULATTA; PUERTO RICO; REPRODUCTION; SOCIAL DOMINANCE;

EID: 84954377074     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22368     Document Type: Review

References (95)

1. Abbott DH, Keverne EB, Bercovitch FB, et al. 2003. Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior 43:67-82.
2. Altizer S, Nunn CL, Thrall PH, et al. 2003. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology. Evolution and Systematics 34:517-547.
3. Ansar Ahmed S, Karpuzoglu E, Khan D. 2009. Effects of sex steroids on innate and adaptive immunity. In sex hormones and immunity to infection. Berlin, Heidelberg: Springer. 19-51.
4. Archie EA, Tung J, Clark M, Altmann J, Alberts SC. 2014. Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proceedings of the Royal Society B: Biological Sciences 281:20141261-20141261.
5. Balasubramaniam KN, Dunayer ES, Gilhooly LJ, Rosenfield KA, Berman CM. 2014. Group size, contest competition, and social structure. In Cayo Santiago Rhesus Macaques. DOI: 10.1163/1568539X-00003216.
6. Bell AW, Bauman DE. 1997. Adaptations of glucose metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia 2:265-278.
7. Bercovitch FB. 1991. Social stratification, social strategies, and reproductive success in primates. Ethology and Sociob iology 12:315-333.
8. Blomquist GE, Sade DS, Berard JD. 2011. Rank-related fitness differences and their demographic pathways in semi-free-ranging rhesus macaques (Macaca mulatta). International Journal of Primatology 32:193-208.
9. Blomquist GE. 2009a. Environmental and genetic causes of maturational differences among rhesus macaque matrilines. Behavioral Ecology and Sociobiology 63:1345-1352.
10. Blomquist GE. 2009b. Trade-off between age of first reproduction and survival in a female primate. Biology Letters 5:339-342.
11. Brent LJN, Semple S, Dubuc C, Heistermann M, MacLarnon A. 2011. Social capital and physiological stress levels in free-ranging adult female rhesus macaques. Physiology & Behavior 102:76-83.
12. Brockman DK, van Schaik CP. 2006. Seasonality and reproductive function. In: Brockman DK, van Schaik CP, editors. Seasonality in Primates. Cambridge: Cambridge University Press. p 269-305.
13. Chapais B. 2004. How kinship generates dominance structures: a comparative perspective. In: Thierry B, Singh M, Kaumanns W, editors. Macaque Societies: A Model for the Study of Social Organization. Cambridge: Cambridge University Press. p 186-204.
14. Clutton-Brock TH, Parker GA. 1995. Sexual coercion in animal societies. Animal Behaviour 49:1345-1365.
15. Cords M. 2012. The behavior, ecology, and social evolution of cercopithecine monkeys. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago: The University of Chicago Press. p 91-112.
16. Creel S, Dantzer B, Goymann W, Rubenstein DR. 2012. The ecology of stress: effects of the social environment. Functional Ecology 27:66-80.
17. Crofoot MC, Wrangham RW. 2009. Intergroup aggression in primates and humans: the Case for a Unified Theory. In: Kappeler PM, Silk JB, editors. Mind The Gap. Berlin Heidelberg: Springer. p 171-197.
18. de Waal FBM. 1986. The integration of dominance and social bonding in primates. Quarterly Review of Biology 61:459-479.
19. de Waal FBM, Luttrell LM. 1985. The formal hierarchy of rhesus macaques: an investigation of the bared-teeth display. American Journal of Primatology 9:73-85.
20. Drickamer LC. 1974. A ten-year summary of reproductive data for free-ranging macaca mulatta. Folia Primatologica 21:61-80.
21. Dubuc C, Ruiz-Lambides AV, Widdig A. 2014. Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate. Behavioral Ecology.
22. Ehardt CL, Bernstein IS. 1986. Matrilineal overthrows in rhesus monkey groups. International Journal of Primatology 7:157-181.
23. Ellison PT. 2003. Energetics and reproductive effort. American Journal of Human Biology 15:342-351.
24. Emery Thompson M, Georgiev AV. 2014. The high price of success: costs of mating effort in male primates. International Journal of Primatology 35:609-627.
25. Emery Thompson M, Muller MN, Kahlenberg SM, Wrangham RW. 2010. Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior 58:440-449.
26. Emery Thompson M, Muller MN, Wrangham RW. 2012. The energetics of lactation and the return to fecundity in wild chimpanzees. Behavioral Ecology 23:1234-1241.
27. Emery Thompson M. 2013. Comparative reproductive energetics of human and nonhuman primates. Annual Review of Anthropology 42:287-304.
28. Foerster S, Cords M, Monfort SL. 2012. Seasonal energetic stress in a tropical forest primate: proximate causes and evolutionary implications. PLoS ONE 7:e50108.
29. Fürtbauer I, Heistermann M, Schülke O, Ostner J. 2014. Low female stress hormone levels are predicted by same- or opposite-sex sociality depending on season in wild Assamese macaques. Psychoneuroendocrinology 48:19-28.
30. Georgiev AV. 2012. Energetic Costs of Reproductive Effort in Male Chimpanzees, PhD dissertation. Harvard University: Cambridge MA.
31. Gesquiere LR, Learn NH, Simao MCM, et al. 2011. Life at the top: rank and stress in wild male baboons. Science 333:357-360.
32. Goymann W, Wingfield JC. 2004. Allostatic load, social status and stress hormones: the costs of social status matter. Animal Behaviour 67:591-602.
33. Gómez-Espinosa E, Rangel-Negrín A, Chavira R, Canales-Espinosa D, Dias PAD. 2013. The effect of energetic and psychosocial stressors on glucocorticoids in mantled howler monkeys (Alouatta palliata). American Journal of Primatology 76:362-373.
34. Harshman LG, Zera AJ. 2007. The cost of reproduction: the devil in the details. Trends in Ecology & Evolution 22:80-86.
35. Hernández-Pacheco R, Rawlins RG, Kessler MJ, et al. 2013. Demographic variability and density-dependent dynamics of a free-ranging rhesus macaque population. American Journal of Primatology 75:1152-1164.
36. Higham JP, Heistermann M, Maestripieri D. 2011. The energetics of male-male endurance rivalry in free-ranging rhesus macaques, Macaca mulatta. Animal Behaviour 81:1001-1007.
37. Higham JP, Maestripieri D. 2014. The costs of reproductive success in male rhesus macaques (Macaca mulatta) on Cayo Santiago. International Journal of Primatology. 35:661-676.
38. Hoffman CL, Ayala JE, Mas-Rivera A. 2010a. Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free-ranging female rhesus macaques. American journal of Primatology 72:559-565.
39. Hoffman CL, Higham JP, Heistermann M, et al. 2011. Immune function and HPA axis activity in free-ranging rhesus macaques. Physiology & Behavior 104:507-514.
40. Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D. 2010b. Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behavioral Ecology 21:972-978.
41. Hoffman CL, Maestripieri D. 2011. Costs of reproduction among rhesus macaque females on cayo santiago. In: Wang Q, editor. Bones, Genetics, and Behavior of Rhesus Macaques. Berlin: Springer. p 209-226.
42. Hoffman CL, Ruiz-Lambides AV, Davila E, et al. 2008. Sex differences in survival costs of reproduction in a promiscuous primate. Behavioral Ecology and Sociobiology 62:1711-1718.
43. Holekamp KE, Smale L. 1991. Dominance acquisition during mammalian social development: the "inheritance" of maternal rank. Integrative and Comparative Biology 31:306-317.
44. Jaimez NA, Bribiescas RG, Aronsen GP, Anestis SA, Watts DP. 2011. Urinary cortisol levels of gray-cheeked mangabeys are higher in disturbed compared to undisturbed forest areas in Kibale National Park, Uganda. Animal Conservation 15:242-247.
45. Juster R-P, McEwen BS, Lupien SJ. 2010. Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews 35:2-16.
46. Kaufmann JH. 1983. On the definitions and functions of dominance and territoriality. Biological Reviews 58:1-20.
47. Kessler MJ, Berard JD, Rawlins RG, et al. 2006. Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta). American Journal of Primatology 68:725-731.
48. Kotrschal A, Ilmonen P, Penn DJ. 2007. Stress impacts telomere dynamics. Biology Letters 3:128-130.
49. Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews 10:434-445.
50. Maestripieri D, Hoffman CL, Fulks R, Gerald MS. 2008. Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Hormones and Behavior 53:170-176.
51. Maestripieri D, Hoffman CL. 2012. Behavior and social dynamics of rhesus macaques on Cayo Santiago. In: Wang Q, editor. Bones, Genetics, and Behavior of Rhesus Macaques. Berlin: Springer. p 247-262.
52. Maestripieri D. 1995. First steps in the macaque world: do rhesus mothers encourage their infants' independent locomotion?. Animal Behaviour 49:1541-1549.
53. Maestripieri D. 2005. Gestural communication in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides): use of signals in relation to dominance and social context. Gesture 5:57-73.
54. Majolo B, de Bortoli Vizioli, Schino A. 2008. Costs and benefits of group living in primates: group size effects on behaviour and demography. Animal Behaviour 76:1235-1247.
55. Martin LB. 2009. Stress and immunity in wild vertebrates: timing is everything. General and Comparative Endocrinology 163:70-76.
56. McEwen BS. 2007. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 87:873-904.
57. Muehlenbein MP, Bribiescas RG. 2005. Testosterone-mediated immune functions and male life histories. American Journal of Human Biology 17:527-558.
58. Muehlenbein MP. 2006. Intestinal parasite infections and fecal steroid levels in wild chimpanzees. American Journal of Physical Anthropology 130:546-550.
59. Muller MN, Kahlenberg SM, Emery Thompson, Wrangham M. 2007. Male coercion and the costs of promiscuous mating for female chimpanzees. Proceedings of the Royal Society B: Biological Sciences 274:1009-1014.
60. Muller MN, Wrangham RW. 2009. Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Cambridge, MA: Harvard University Press.
61. Novak MA, Hamel AF, Kelly BJ, Dettmer AM, Meyer JS. 2013. Stress, the HPA axis, and nonhuman primate well-being: a review. Applied Animal Behaviour Science 143:135-149.
62. Oates-O'Brien RS, Farver TB, Anderson-Vicino KC, McCowan B, Lerche NW. 2010. Predictors of matrilineal overthrows in large captive breeding groups of rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science 49:196-201.
63. Otali E, Gilchrist JS. 2006. Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: the infant safety hypothesis. Behavioral Ecology and Sociobiology 59:561-570.
64. Penn DJ, Smith KR. 2007. Differential fitness costs of reproduction between the sexes. Proceedings of the National Academy of Sciences USA 104:553-558.
65. Prall SP, Muehlenbein MP. 2014. Testosterone and immune function in primates: a brief summary with methodological considerations. International Journal of Primatology. 35:805-824.
66. Prentice AM, Prentice A. 1988. Energy costs of lactation. Annual Review of Nutrition 8:63-79.
67. Pusey A. 2012. Magnitude and sources of variation in female reproductive performance. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago: The University of Chicago Press. p 343-366.
68. Rawlins RG, Kessler MJ. 1986. The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ, editors. The Cayo Santiago Macaques. Albany: SUNY Press. p 13-45.
69. Rhine RJ, Norton GW, Wasser SK. 2000. Lifetime reproductive success, longevity, and reproductive life history of female yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. American Journal of Primatology 51:229-241.
70. Rifkin JL, Nunn CL, Garamszegi LZ. 2012. Do animals living in larger groups experience greater parasitism? A meta-analysis. The American Naturalist 180:70-82.
71. Robbins AM, Stoinski T, Fawcett K, Robbins MM. 2011. Lifetime reproductive success of female mountain gorillas. Yearbook of Physical Anthropology 146:582-593.
72. Roberts S-J, Cords M. 2013. Group size but not dominance rank predicts the probability of conception in a frugivorous primate. Behavioral Ecology and Sociobiology 67:1995-2009.
73. Ruiz-Lambides AV, Aure B, Caraballo G, Platt ML, Brent LJN. 2013. Matrilineal overthrow followed by high mortality levels in free-ranging rhesus macaques. American Journal of Primatology 75S1:98.
74. Sapolsky RM, Krey LC, McEwen BS. 1986. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocrine Reviews 7:284-301.
75. Sapolsky RM, Uno H, Rebert CS, Finch CE. 1990. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. The Journal of Neuroscience 10:2897-2902.
76. Sapolsky RM. 1999. Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Experimental Gerontology 34:721-732.
77. Sapolsky RM. 2005. The influence of social hierarchy on primate health. Science 308:648-652.
78. Schulke O, Ostner J. 2012. Ecological and social influences on sociality. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago: The University of Chicago Press. p 193-219.
79. Silk JB, Alberts SC, Altmann J. 2003. Social bonds of female baboons enhance infant survival. Science 302:1231-1234.
80. Silk JB, Beehner JC, Bergman TJ, et al. 2009. The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society B: Biological Sciences 276:3099-3104.
81. Silk JB, Beehner JC, Bergman TJ, et al. 2010. Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20:1359-1361.
82. Smuts BB, Smuts RW. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior 22(22):1-63.
83. Steptoe A, Kivimäki M. 2013. Stress and csrdiovascular disease: an update on current knowledge. Annual Review of Public Health 34:337-354.
84. Sterck E, Watts DP, van Schaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41:291-309.
85. Stockley P, Bro-Jørgensen J. 2011. Female competition and its evolutionary consequences in mammals. Biological Reviews 86:341-366.
86. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM. 1989. Hippocampal damage associated with prolonged and fatal stress in primates. The Journal of Neuroscience 9:1705-1711.
87. van Noordwijk MA, van Schaik CP. 2004. Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP, editor. Sexual Selection in Primates: New and Comparative Perspectives. Cambridge: Cambridge University Press, p 208-229.
88. van Schaik CP. 1983. Why are diurnal primates living in groups?. Behaviour 87:120-144.
89. Vandenbergh JG, Vessey S. 1968. Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. Journal of Reproduction and Fertility. 15:71-79.
90. Varley MA, Vessey SH. 1977. Effects of geographic transfer on the timing of seasonal breeding of rhesus monkeys. Folia Primatologica 28:52-59.
91. Wade GN, Schneider JE. 1992. Metabolic fuels and reproduction in female mammals. Neuroscience & Biobehavioral Reviews 16:235-272.
92. Webster Marketon, Glaser JI. 2008. Stress hormones and immune function. Cellular Immunology 252:16-26.
93. Wheeler BC, Scarry CJ, Koenig A. 2013. Rates of agonism among female primates: a cross-taxon perspective. Behavioral Ecology 24:1369-1380.
94. Wilson AP, Boelkins RC. 1970. Evidence for seasonal variation in aggressive behaviour by Macaca mulatta. Animal Behaviour 18:719-724.
95. Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75:262-300.