Social capital and physiological stress levels in free-ranging adult female rhesus macaques

Physiology and Behavior

Volumn 102, Issue 1, 2011, Pages 76-83

  Brent, L J N ^a   Semple, S ^a   Dubuc, C ^b,c   Heistermann, M ^c   MacLarnon, A ^a  

^a UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c GERMAN PRIMATE CENTER   (Germany)

Author keywords

Affiliation; Fecal glucocorticoids; Indirect connections; Rhesus macaques; Social capital; Social networks

Indexed keywords

GLUCOCORTICOID;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOMINANCE BEHAVIOR; FECES LEVEL; FEMALE; GROOMING; NONHUMAN; PHYSIOLOGICAL STRESS; PREGNANCY; PRIORITY JOURNAL; RHESUS MONKEY; SOCIAL CAPITAL; SOCIAL INTERACTION; SOCIAL NETWORK; VOCALIZATION;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; FECES; FEMALE; GLUCOCORTICOIDS; GROOMING; MACACA MULATTA; MALE; SOCIAL DOMINANCE; SOCIAL SUPPORT; STRESS, PHYSIOLOGICAL;

EID: 78149314631     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.09.022     Document Type: Article

References (90)

1. deVries A.C., Glasper E.R., Detillion C.E. Social modulation of stress responses. Physiol Behav 2003, 79:399-407.
2. Kikusui T., Winslow J.T., Mori Y. Social buffering: relief from stress and anxiety. Philos Trans Roy Soc B Biol Sci 2006, 361:2215-2228.
3. Thorsteinsson E.B., James J.E. A meta-analysis of the effects of experimental manipulations of social support during laboratory stress. Psychol Health 1999, 14:869-886.
4. Reeder D.M., Kramer K.M. Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 2005, 86:225-235.
5. Field J. Social capital 2009, Routledge, New York. 2nd ed.
6. Cohen S., Gottlieb B.H., Underwood L.G. Social relationships and health: challenges for measurement and intervention. Adv Mind Body Med 2001, 17:129-141.
7. Cameron J.L. Stress and behaviorally induced reproductive dysfunction in primates. Semin Reprod Endocrinol 1997, 15:37-45.
8. Tamashiro K.L.K., Nguyen M.M.N., Sakai R.R. Social stress: from rodents to primates. Front Neuroendocrinol 2005, 26:27-40.
9. Cohen S., Kaplan J.R., Cunnick J.E., Manuck S.B., Rabin B.S. Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psychol Sci 1992, 3:301-304.
10. Cohen S., Line S., Manuck S.B., Rabin B.S., Heise E.R., Kaplan J.R. Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 1997, 59:213-221.
11. Baum A., Posluszny D.M. Health psychology: mapping biobehavioral contributions to health and illness. Ann Rev Psychol 1999, 50:137-163.
12. Silk J.B., Beehner J.C., Bergman T.J., Crockford C., Engh A.L., Moscovice L.R., et al. The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc Roy Soc B 2009, 276:3099-3104.
13. Holt-Lunstad J., Smith T.B., Layton J.B. Social relationships and mortality risk: a meta-analytic review. PLoS Med 2010, 7:e1000316.
14. Rosal M.C., King J., Ma Y., Reed G.W. Stress, social support, and cortisol: inverse associations?. Behav Med 2004, 30:11-21.
15. Rice M., Kang D.H., Weaver M., Howell C.C. Relationship of anger, stress, and coping with school connectedness in fourth-grade children. J Sch Health 2008, 78:149-156.
16. Taxis J.C., Rew L., Jackson K., Kouzekanani K. Protective resources and perceptions of stress in a multi-ethnic sample of school-age children. Pediatr Nurs 2004, 30:477-482. 87.
17. Seeman T.E., Singer B.H., Ryff C.D., Love G.D., Levy-Storms L. Social relationships, gender, and allostatic load across two age cohorts. Psychosom Med 2002, 64:395-406.
18. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Mendoza S.P., Saltzman W., et al. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 2003, 43:67-82.
19. Sapolsky R.M., Alberts S.C., Altmann J. Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatry 1997, 54:1137-1143.
20. Ray J.C., Sapolsky R.M. Styles of male social behavior and their endocrine correlates among high ranking wild baboons. Am J Primatol 1992, 28:231-250.
21. Sapolsky R.M., Ray J.C. Styles of dominance and their endocrine correlates among wild olive baboons (Papio anubis). Am J Primatol 1989, 18:1-13.
22. Shutt K., MacLarnon A., Heistermann M., Semple S. Grooming in Barbary macaques: better to give than receive?. Biol Lett 2007, 3:231-233.
23. Setchell J.M., Smith T., Wickings E.J., Knapp L.A. Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Madrillus sphinx). Am J Primatol 2008, 70:1-10.
24. Emery Thompson M., Muller M.N., Kahlenberg S.M., Wrangham R.W. Dynamics of social and energetic stress in wild female chimpanzees. Horm Behav 2010, 58:440-449.
25. McDonald D.B. Young-boy networks without kin clusters in a lek-mating manakin. Behav Ecol Sociobiol 2009, 63:1029-1034.
26. Fowler J.H., Christakis N.A. Dynamic spread of happiness in a large social network: longitudinal analysis over 20years in the Framingham Heart Study. Br Med J 2008, 337:9.
27. Rosenquist, JN, Fowler, JH, Christakis, NA. Social network determinants of depression. Mol Psychiatry 2010;In press:. doi:10.1038/mp.2010.13.
28. Rosenquist J.N., Murabito J., Fowler J.H., Christakis N.A. The spread of alcohol consumption behavior in a large social network. Ann Intern Med 2010, 152:426-433.
29. McDonald D.B. Predicting fate from early connectivity in a social network. Proc Natl Acad Sci USA 2007, 104:10910-10914.
30. Ryder T.B., Parker P.G., Blake J.G., Loiselle B.A. It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird. Proc Roy Soc B 2009, 76:2377-2384.
31. Ryder T.B., McDonald D.B., Blake J.G., Parker P.G., Loiselle B.A. Social networks in the lek-mating wire-tailed manakin (Pipra filicauda). Proc Roy Soc B 2008, 275:1367-1374.
32. Blumstein D.T., Wey T.W., Tang K. A test of the social cohesion hypothesis: interactive female marmots remain at home. Proc Roy Soc B 2009, 276:3007-3012.
33. Cheney D.L., Seyfarth R.M. Recognition of other individuals' social relationships by female baboons. Anim Behav 1999, 58:67-75.
34. Flombaum J.I., Santos L.R. Rhesus monkeys attribute perceptions to others. Curr Biol 2005, 15:447-452.
35. Hare B., Call J., Tomasello M. Do chimpanzees know what conspecifics know?. Anim Behav 2001, 61:139-151.
36. Krause J., James R., Lusseau D. Animal social networks: an introduction. Behav Ecol Sociobiol 2009, 63:967-973.
37. Croft D.P., James R., Krause J. Exploring animal social networks 2008, Princeton University Press, Princeton, New Jersey.
38. Wey T., Blumstein D.T., Shen W., Jordan F. Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 2008, 75:333-344.
39. Rawlings R.G., Kessler M.J. The Cayo Santiago macaques: history, behavior & biology 1986, State University of New York Press, Albany.
40. Malik I. Time budgets and activity patterns in free-ranging rhesus monkeys. Primate ecology and conservation 1986, 105-114. Cambridge University Press, New York. J.G. Else, P.C. Lee (Eds.).
41. Cockrem J.F., Silverin B. Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen Comp Endocrinol 2002, 125:248-255.
42. Engh A.L., Beehner J.C., Bergman T.J., Whitten P.L., Hoffmeier R.R., Seyfarth R.M., et al. Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc Roy Soc B 2006, 273:707-712.
43. Monclus R., Palomares F., Tablado Z., Martinez-Fonturbel A., Palme R. Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 2009, 158:615-623.
44. Ange-van Heugten K.D., van Heugten E., Timmer S., Bosch G., Elias A., Whisnant S., et al. Fecal and salivary cortisol concentrations in woolly (Lagothrix ssp.) and spider monkeys (Ateles spp.). Int J Zool 2009, 10.1155/2009/127852.
45. Wasser S.K., Thomas R., Nair P.P., Guidry C., Southers J., Lucas J., et al. Effects of dietary fiber on fecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J Reprod Fertil 1993, 97:569-574.
46. Gesquiere L.R., Khan M., Shek L., Wango T.L., Wango E.O., Alberts S.C., et al. Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 2008, 54:410-416.
47. Weingrill T., Gray D.A., Barrett L., Henzi P.S. Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm Behav 2004, 45:259-269.
48. Chikazawa D., Gordon T.P., Bean C.A., Bernstein I.S. Mother -daughter dominance reversals in rhesus monkeys (Macaca mulatta). Primates 1979, 20:301-305.
49. McLean M., Smith R. Corticotropin-releasing hormone in human pregnancy and parturition. Trends Endocrinol Metab 1999, 10:174-178.
50. Engh A.L., Beehner J.C., Bergman T.J., Whitten P.L., Hoffmeier R.R., Seyfarth R.M., et al. Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons. Anim Behav 2006, 71:1227-1237.
51. Dubuc C., Brent L.J.N., Accamando A., Gerald M., MacLarnon A., Semple S., et al. Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. Int J Primatol 2009, 13:777-789.
52. Silk J.B., Short J., Roberts J., Kusnitz J. Gestation length in rhesus macaques (Macaca mulatta). Int J Primatol 1993, 14:95-104.
53. Fitchel C., Krause C., Ganswindt A., Heistermann M. Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm Behav 2007, 51:640-648.
54. Heistermann M., Palme R., Ganswindt A. Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am J Primatol 2006, 68:257-273.
55. Ostner J., Heistermann M., Schulke O. Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 2008, 54:613-619.
56. Beehner J.C., Bergman T.J., Cheney D.L., Seyfarth R.M., Whitten P.L. The effect of new alpha males on female stress in free-ranging baboons. Anim Behav 2005, 69:1211-1221.
57. Anestis S.F. Urinary cortisol responses to unusual events in captive chimpanzees (Pan troglodytes). Stress 2009, 12:49-57.
58. Nepomnaschy P.A., Welch K.B., McConnell D.S., Low B.S., Strassmann B.I., England B.G. Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA 2006, 103:3938-3942.
59. Beehner J.C., Nguyen N., Wango E.O., Alberts S.C., Altmann J. The endocrinology of pregnancy and fetal loss in wild baboons. Horm Behav 2006, 49:688-699.
60. French J.A., Koban T., Rukstalis M., Ramirez S.M., Bardi M., Brent L. Excretion of urinary steroids in pre- and postpartum female baboons. Gen Comp Endocrinol 2004, 137:69-77.
61. Barrett L., Henzi P.S. Constraints on relationship formation among female primates. Behaviour 2002, 139:263-289.
62. Cords M. Friendships, alliances, reciprocity and repair. Machiavellian intelligence II: extensions and evaluations 1997, 24-49. Cambridge University Press, Cambridge. A. Whiten, R.W. Byrne (Eds.).
63. Dunbar R.I.M., Shultz S. Bondedness and sociality. Behaviour 2010, 147:775-803.
64. Borgatti S.P., Everett M.G., Freeman L.C. UCINET for Windows: software for social network analysis 2002, Analytic Technologies, Harvard, Massachusetts.
65. Whitehead H. Socprog 2.3 (for MATLAB 7.4) 2007, Dalhousie University, Halifax, Canada.
66. Kapsalis E., Berman C.M. Models of affiliative relationships among free-ranging rhesus monkeys (Macaca mulatta).1. Criteria for kinship. Behaviour 1996, 133:1209-1234.
67. Widdig A., Nürnberg P., Krawczak M., Streich W.J., Bercovitch F.B. Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 2002, 139:371-391.
68. Berman C.M. Early agonistic experience and rank acquisition among free-ranging infant rhesus monkeys. Int J Primatol 1980, 1:153-170.
69. Altmann J. Age cohorts as paternal sibships. Behav Ecol Sociobiol 1979, 6:161-164.
70. Crockford C., Wittig R.M., Whitten P.L., Seyfarth R.M., Cheney D.L. Social stressors and coping mechanism in wild female baboons (Papio hamadryas ursinus). Horm Behav 2008, 53:254-265.
71. Wallner B., Möstl E., Dittami J., Prossinger H. Fecal glucocorticoids document stress in female Barbary macaques (Macaca sylvanus). Gen Comp Endocrinol 1999, 113:80-86.
72. Gust D.A., Gordon T.P., Hambright K., Wilson M.E. Relationship between social factors and pituitary-adrenocortical activity in female rhesus monkeys (Macaca mulatta). Horm Behav 1993, 27:318-331.
73. de Weerth C., Buitelaar J.K. Physiological stress reactivity in human pregnancy - a review. Neurosci Biobehav Rev 2005, 29:295-312.
74. Tabachnick B.G., Fidell L.S. Using multivariate statistics 2007, Allyn & Bacon, Boston, MA. 5th ed.
75. Rasbash J., Steele F., Browne W.J., Goldstein H. A user's guide to MLwiN, version 2.10 2009, Centre for Multilevel Modelling, University of Bristol.
76. Wasserman S., Faust K. Social network analysis: methods and applications 1994, Cambridge University Press, Cambridge.
77. Browne W.J. MCMC estimation in MLwiN, version 2.10 2009, Centre for Multilevel Modelling, University of Bristol.
78. Rasbash J., Charlton C., Jones K., Pillinger R. Manual supplement for MLwiN, version 2.10 2009, Centre for Multilevel Modelling, University of Bristol.
79. Thierry B. Social epigenesis. Macaque societies: a model for the study of social organization 2004, 267-290. Cambridge University Press, Cambridge. B. Thierry, M. Singh, W. Kaumanns (Eds.).
80. van Schaik C.P., van Noordwijk M.A., van Bragt T., Blankenstein M.A. A pilot-study of the social correlates of levels of urinary cortisol, prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis). Primates 1991, 32:345-356.
81. Aureli F., Preston S.D., de Waal F.B.M. Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. J Comp Psychol 1999, 113:59-65.
82. Boccia M.L., Reite M., Laudenslager M. On the physiology of grooming in a pigtail macaque. Physiol Behav 1989, 45:667-670.
83. Aureli F., Yates K. Distress prevention by grooming others in crested black macaques. Biol Lett 2009, 10.1098/rsbl.2009.0513.
84. Brunton P.J., Russell J.A., Douglas A.J. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 2008, 20:764-776.
85. Kudielka B.M., Hellhammer D.H., Wust S. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 2009, 34:2-18.
86. McLean M., Smith R. Corticotrophin-releasing hormone and human parturition. Reproduction 2001, 121:493-501.
87. Whitehead H. Analyzing animal societies 2008, University of Chicago Press, Chicago.
88. Newman M.E.J. Mathematics of networks. The new Palgrave encyclopedia of economics 2008, Palgrave Macmillan, Basingstoke. 2nd ed. L.E. Blume, S.N. Durlauf (Eds.).
89. Ganswindt A., Palme R., Heistermann M., Borragan S., Hodges J.K. Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol 2003, 134:156-166.
90. Heistermann M., Ademmer C., Kaumanns W Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int J Primatol 2004, 25:689-708.