doi:

DOI: 10.3724/SP.J.1141.2013.E02E42

Zoological Research (动物学研究) 2013/34:2 PP.E42-E49

Social rank and cortisol among female rhesus macaques (Macaca mulatta)


Abstract:
In animal societies, some stressful events can lead to higher levels of physiological stress. Such stressors, like social rank, also predict an increased vulnerability to an array of diseases. However, the physiological relationship between social rank and stress varies between different species, as well as within groups of a single species. For example, dominant individuals are more socially stressed at times, while at other times it is the subordinate ones who experience this stress. Together, these variations make it difficult to assess disease vulnerability as connected to social interactions. In order to learn more about how physiological rank relationships vary between groups of a single species, cortisol measurements from hair samples were used to evaluate the effects of dominance rank on long-term stress levels in despotic and less stringent female rhesus macaque hierarchal groups. In despotic groups, cortisol levels were found not to be correlated with social rank, but a negative correlation was found between social rank and cortisol levels in less stringent hierarchies. Low ranking monkeys in less stringent groups secreted elevated levels of cortisol compared to higher ranking animals. These data suggest that variations in the strictness of the dominance hierarchy are determining factors in rank related stress physiology. The further consideration of nonhuman primate social system diversity and the linear degree of their hierarchies may allow for the development of valid rank-related stress models that will help increase our understanding and guide the development of new therapeutics for diseases related to human socioeconomic status.

Key words:Social rank,Hypothalamus-pituitary-adrenal axis,Cortisol,Female,Rhesus macaques

ReleaseDate:2015-04-16 19:34:20



Abbott D, Keverne E, Bercovitch F, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM. 2003. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior, 43(1): 67-82.

Adams MR, Kaplan JR, Koritnik DR. 1985. Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiology & Behavior, 35(6): 935-940.

Ader R, Cohen N. 2001. Conditioning and immunity. // Ader R, Felten D, Vohen N, eds. Psychoneuroimmunology. New York: Scademic Press, 2: 3-34.

Adler NE, Epel ES, Castellazzo G, Ickovics JR. 2000. Relationship of subjective and objective social status with psychological and physiological functioning: Preliminary data in healthy, White women. Health Psychology, 19(6): 586-532.

Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour, 49(3-4): 227-267.

Beerda B, Schilder MBH, Janssen NS, Mol JS. 1996. The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a noninvasive assessment of stress responses in dogs. Hormones and Behavior, 30(3): 272-279.

Bercovitch FB, Clarke AS. 1995. Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiology & Behavior, 58(2): 215-221.

Brunner E. 1997. Socioeconomic determinants of health: stress and the biology of inequality. BMJ, 314(7092): 1472.

Burch WM. 1982. Urine free-cortisol determination-a useful tool in the management of chronic hypoadrenal states. JAMA: the Journal of the American Medical Association, 247(14): 2002-2004.

Cattet M, Christison K, Caulkett NA, Stenhouse GB. 2003. Physiologic responses of grizzly bears to different methods of capture. Journal of Wildlife Diseases, 39(3): 649-654.

Cavogelli S A. 1999. Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Animal Behaviour, 57(4): 935-944.

Chamove AS, Bowman RE. 1976. Rank, rhesus social behavior, and stress. Folia Primatologica, 26(1): 57-66.

Chase ID, Tovey C, Spangler-Martin D, Manfredonia M. 2002. Individual differences versus social dynamics in the formation of animal dominance hierarchies. Proceedings of the National Academy of Sciences, 99(8): 5744-5749.

Coe CL, Mendoza SP, Levine S. 1979. Social status constrains the stress response in the squirrel monkey. Physiology & Behavior, 23(4): 633-638.

Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR. 1997. Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosomatic Medicine, 59(3): 213-221.

Constable S, Parslow A, Dutton G, Rogers T, Hogg C. 2006. Urinary cortisol sampling: a non-invasive technique for examining cortisol concentrations in the Weddell seal, Leptonychotes weddellii. Zoo Biology, 25(2): 137-144.

Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS. 2006. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. General and Comparative Endocrinology, 147(3): 255-261.

Dhabhar FS, Mcewen BS. 1999. Enhancing versus suppressive effects of stress hormones on skin immune function. Proceedings of the National Academy of Sciences, 96(3): 1059-1064.

Ekkel ED, Dieleman SJ, Schouten WGP, Portela A, Cornélissen G, Tielen MJ, Halberg F. 1996. The circadian rhythm of cortisol in the saliva of young pigs. Physiology & Behavior, 60(3): 985-989.

Feng X, Wang L, Yang S, Qin D, Wang J, Li C, Lü L, Ma Y, Hu X. 2011. Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys. Proceedings of the National Academy of Sciences, 108(34): 14312-14317.

Gammell MP, De Vries H, Jennings DJ, Carlin CM, Hayden TJ. 2003. David's score: a more appropriate dominance ranking method than Clutton-Brock et al. 's index. Animal Behaviour, 66(3): 601-605.

Gatti R, Antonelli G, Prearo M, Spinella P, Cappellin E, De Palo EF. 2009. Cortisol assays and diagnostic laboratory procedures in human biological fluids. Clinical Biochemistry, 42(12): 1205-1217.

Gow R, Thomson S, Rieder M, Van Unm S, Koren G. 2010. An assessment of cortisol analysis in hair and its clinical applications. Forensic Science International, 196(1-3): 32-37.

Gust DA, Gordon TP, Hambright MK, Wilson ME. 1993. Relationship between social factors and pituitary-adrenocortical activity in female rhesus monkeys (Macaca mulatta). Hormones and Behavior, 27(3): 318-331.

Gust DA, Gordon TP, Wilson ME, Ahmed-Ansari A, Brodie AR, McClure HM. 1991. Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain, Behavior, and Immunity, 5(3): 296-307.

Kawachi I, Kennedy BP. 2006. The Health of Nations: Why Inequality is Harmful to Your Health. New York: New Press.

Keay JM, Singh J, Gaunt MC, Kaur T. 2006. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. Journal of Zoo and Wildlife Medicine, 37(3): 234-244.

Keverne EB, Meller RE, Eberhart A. 1982. Dominance and subordination: concepts or physiological states. // Chiarelli AB, Corruccini RS. Advanced Views in Primate Biology. Berlin: Springer-Verlag: 81-94.

Li HQ, Zhang YH, Li BG. 2004. Review on dominance hierarchy of Non-human Primates. Acta Theriologica Sinica, 24(1): 53-60 (in Chinese).

Manogue KR, Leshner AI, Candland DK. 1975. Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus). Primates, 16(4): 457-463.

Manuck SB, Marsland AL, Kaplan JR, Williams JK. 1995. The pathogenicity of behavior and its neuroendocrine mediation: An example from coronary artery disease. Psychosomatic Medicine, 57(3): 275-283.

Mcewen BS, Lasley EN. 2004. The End of Stress as We Know It. Washington: Joseph Henry Press.

Mendoza SP, Mason WA. 1991. Breeding readiness in squirrel monkeys: female-primed females are triggered by males. Physiology & Behavior, 49(3): 471-479.

Mendoza SP, Coe CL, Lowe EL, Levine S. 1978. The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology, 3(3-4): 221-229.

Millspaugh JJ, Washburn BE, Milanick MA, Beringer J, Hansen LP, MeyerTM. 2002. Non-invasive techniques for stress assessment in white-tailed deer. Wildlife Society Bulletin, 30(3): 899-907.

Mormède P, Andanson S, Aupérin B, Beerdad B, Guémenée D, Malmkvistf J, Mantecag X, Manteuffelh G, Prunetc P, van Reenend CG, Richarde S, Veissierb I. 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior, 92(3): 317-339.

Owen MA, Czekala NM, Swaisgood RR, Steinman K, Lindburg DG. 2005. Seasonal and diurnal dynamics of glucocorticoids and behavior in giant pandas. Ursus, 16(2): 208-221.

Russell E, Koren G, Rieder M, Van Uum S. 2011. Hair cortisol as a biological marker of chronic stress: Current status, future directions and unanswered questions. Psychoneuroendocrinology, 37(5): 589-601.

Saltzman W, Schultz-Darken NJ, Scheffler G, Wegner FH, Abbott DH. 1994. Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiology & Behavior, 56(4): 801-810.

Saltzman W, Schultz-Darken NJ, Wegner FH, Wittwer DJ, Abbott DH. 1998. Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Hormones and Behavior, 33(1): 58-74.

Sapolsky RM. 1990. Adrenocortical function, social rank, and personality among wild baboons. Biological Psychiatry, 28(10): 862-878.

Sapolsky RM. 2004a. Social status and health in humans and other animals. Annual Review of Anthropology, 33: 393-418.

Sapolsky RM. 2004b. Why Zebras Don't Get Ulcers: The Acclaimed Guide to Stress, Stress-Related Diseases, and Coping-Now Revised and Updated. New York: Holt Paperbacks.

Sapolsky RM. 2005. The influence of social hierarchy on primate health. Science, 308(5722): 648-652.

Sapolsky RM, Share L J. 1994. Rank-related differences in cardiovascular function among wild baboons: Role of sensitivity to glucocorticoids. American Journal of Primatology, 32(4): 261-275.

Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1): 55-89.

Schilling A, Perret M. 1987. Chemical signals and reproductive capacity in a male prosimian primate (Microcebus murinus). Chemical Senses, 12(1): 143-157.

Shively CA. 1998. Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biological Psychiatry, 44(9): 882-891.

Shively CA, Clarkson TB. 1994. Social status and coronary artery atherosclerosis in female monkeys. Arteriosclerosis, Thrombosis, and Vascular Biology, 14(5): 721-726.

Shively CA, Laber-Laird K, Anton RF. 1997. Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biological Psychiatry, 41(8): 871-882.

Shively CA, Register TC, Friedman DP, Morgan TM, Thompson J, Lanier T. 2005. Social stress-associated depression in adult female cynomolgus monkeys (Macaca fascicularis). Biological Psychology, 69(1): 67-84.

Siegrist J, Marmot M. 2004. Health inequalities and the psychosocial environment--two scientific challenges. Social Science & Medicine, 58(8): 1463-1473.

Singh M, D'souza L, Singh M. 1992. Hierarchy, kinship and social interaction among Japanese monkeys (Macaca fuscata). Journal of Biosciences, 17(1): 15-27.

Singh M, Sharma A, Krishna B. 2003. Methodological considerations in measurement of dominance in primates. Current Science, 84(5): 709-713.

Snowdon CT, Savage A, Mcconnell PB. 1985. A breeding colony of cotton-top tamarins (Saguinus oedipus). Laboratory Animal Science, 35(5): 477-480.

Steklis HD, Raleigh MJ, Kling AS, Tachiki K. 1986. Biochemical and hormonal correlates of dominance and social behavior in all-male groups of squirrel monkeys (Saimiri sciureus). American Journal of Primatology, 11(2): 133-145.

Van Schaik C, Van Noordwijk M, Van Bragt T, Blankenstein MA. 1991. A pilot study of the social correlates of levels of urinary cortisol, prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis). Primates, 32(3): 345-356.

Vining RF, Mcginley RA, Maksvytis JJ, Ho KY. 1983. Salivary cortisol: a better measure of adrenal cortical function than serum cortisol. Annals of Clinical Biochemistry, 20(P6): 329-335.

Von Der Ohe CG, Servheen C. 2002. Measuring stress in mammals using fecal glucocorticoids: opportunities and challenges. Wildlife Society Bulletin, 30(4): 1215-1225.

Wallner B, M?stl E, Dittami J, Prossinger H. 1999. Fecal glucocorticoids document stress in female Barbary macaques (Macaca sylvanus). General and Comparative Endocrinology, 113(1): 80-86.

Weingrill T, Gray DA, Barrett L, Henzi SP. 2004. Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Hormones and Behavior, 45(4): 259-269.

Wennig R. 2000. Potential problems with the interpretation of hair analysis results. Forensic Science International, 107(1-3): 5-12.

Whitten PL, Stavisky R, Aureli F, Rusell E. 1999. Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). American Journal of Primatology, 44(1): 57-69.

Wilkinson RG. 2001. Mind the Gap: Hierarchies, Health and Human Evolution. New Haven: Yale University Press.

Willard SL, Shively CA. 2011. Modeling depression in adult female cynomolgus monkeys (Macaca fascicularis). American Journal of Primatology, 74(6): 528-542.

Yodyingyuad U, De La Riva C, Abbott D, Herbert J, Keverne EB. 1985. Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys. Neuroscience, 16(4): 851-858.

Zhao HT, Zhang J, Zhu ZR, Li BG, Wang XW. 2011. The methods of research on the dominance of female in non-human primates. Acta Anthropologica Sinica, 30(4): 415-424 (in Chinese).