Relationship between social rank and cortisol and testosterone concentrations in male cynomolgus monkeys (macaca fascicularis)

Journal of Neuroendocrinology

Volumn 21, Issue 1, 2009, Pages 68-76

  Czoty, P W ^a   Gould, R W ^a   Nader, Michael A ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Cortisol; Dexamethasone suppression; Dominance hierarchy; Nonhuman primates; Testosterone

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; DEXAMETHASONE; HYDROCORTISONE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEXAMETHASONE SUPPRESSION TEST; HYDROCORTISONE RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MACACA; MALE; NONHUMAN; PRIORITY JOURNAL; SOCIAL DOMINANCE; SOCIAL STATUS;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BEHAVIOR, ANIMAL; DEXAMETHASONE; HIERARCHY, SOCIAL; HOUSING, ANIMAL; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MACACA FASCICULARIS; MALE; PITUITARY-ADRENAL SYSTEM; SOCIAL DOMINANCE; STRESS, PSYCHOLOGICAL; TESTOSTERONE;

EID: 57749168382     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01800.x     Document Type: Article

References (56)

1. Cameron JL. Stress and behaviorally induced reproductive dysfunction in primates. Semin Reprod Endocrinol 1997; 15: 37-45.
2. Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR. Chronic stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 1997; 59: 213-221.
3. Kaplan JR, Manuck SB. Status, stress, and atherosclerosis: The role of environment and individual behavior. Ann NY Acad Sci 1998; 896: 145-161.
4. Kaplan JR, Manuck SB. Ovarian dysfunction, stress, and disease: A primate continuum. ILAR J 2004; 45: 89-115.
5. Sapolsky RM. The influence of social hierarchy on primate health. Science 2005; 308: 648-652.
6. Czoty PW, McCabe C, Nader MA. Assessment of the relative reinforcing strength of cocaine in socially housed monkeys using a choice procedure. J Pharmacol Exp Ther 2005; 312: 96-102.
7. Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA. Social dominance in monkeys: dopamine D 2 receptors and cocaine self-administration. Nat Neurosci 2002; 5: 169-174.
8. Shively CA, Laber-Liard K, Anton RF. Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 1997; 41: 871-882.
9. Shively CA, Register TC, Friedman DP, Morgan TM, Thompson J, Lanier T. Social stress-associated depression in adult female cynomolgus monkeys. Biol Psychol 2005; 69: 67-84.
10. Amick BC III, McDonough P, Chang H, Rogers WH, Pieper CF, Duncan G. Psychological and physical exposures in the United States labor market from 1968 to 1992. Psychosom Med 2002; 64: 370-381.
11. Wohlfarth T, van den Brink W. Social class and substance use disorder: the value of social class as distinct from socioeconomic status. Soc Sci Med 1998; 47: 51-58.
12. Adler NE, Matthews K. Health physiology: Why do some people get sick and some stay well? Ann Rev Psychol 1993; 45: 229-259.
13. Krantz DS, McCeney MK. Effects of psychological and social factors on organic disease: A critical assessment of research on coronary heart disease. Ann Rev Psychol 2002; 53: 341-369.
14. Kaplan JR, Manuck SB, Clarkson TB, Lusso FM, Taub DM. Social status, environment, and atherosclerosis in cynomolgus monkeys. Atherosclerosis 1982; 2: 359-368.
15. Henry JP, Stephens PM. Stress, Health and the Social Environment: A Sociobiologic Approach to Medicine. New York, NY: Sprenger-Verlag, 1977.
16. Goymann W, Wingfield JC. Allostatic load, social status and stress hormones: The costs of social status matter. Anim Behav 2004; 67: 591-602.
17. Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 2003; 43: 67-82.
18. Clarke AS, Czekala NM, Lindburg DG. Behavioral and adrenocortical responses of male cynomolgus monkeys and lion-tailed macaques to social stimulation and group formation. Primates 1995; 36: 41-56.
19. Kaplan JR, Adams MR, Koritnik DR, Rose JC, Manuck SB. Adrenal responsiveness and social status in intact and ovariectomized Macaca fascicularis. Am J Primatol 1986; 11: 181-193.
20. Sassenrath EN. Increased adrenal responsiveness related to social stress in rhesus monkeys. Horm Behav 1970; 1: 283-298.
21. Shively CA. Social subordination stress, behavior and central monoaminergic function in female cynomolgus monkeys. Biol Psychiatry 1998; 44: 882-891.
22. Shively CA, Kaplan JR. Effects of social factors on adrenal weight and related physiology of Macaca fascicularis. Physiol Behav 1984; 33: 777-782.
23. Hayama S. Correlation between adrenal weight and dominance rank in caged crab-eating monkeys (Macaca fascicularis). Primates 1966; 7: 22-26.
24. Kimura K, Shimizu K, Hayashi M, Ishikawa T, Ago Y. Pituitary-adrenocortical responses to the first dyadic encounters in male rhesus monkeys: Effect of dominance relationship. Am J Primatol 2000; 50: 247-256.
25. Sapolsky RM. The endocrine stress-response and social status in the wild baboon. Horm Behav 1982; 16: 279-292.
26. Sapolsky RM. Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 1983; 5: 365-379.
27. Sapolsky RM. Hypercortisolism among socially subordinate wild baboons originates at the CNS level. Arch Gen Psychiatry 1989; 46: 1047-1051.
28. Sapolsky RM. Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 1992; 17: 701-709.
29. Yodyingyuad U, de la Riva C, Abbott DH, Herbert J, Keverne EB. Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys. Neuroscience 1985; 16: 851-858.
30. Sapolsky RM, Alberts SC, Altmann J. Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatry 1997; 54: 1137-1143.
31. Bercovitch FB, Clarke S. Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiol Behav 1995; 58: 215-221.
32. Chamove AS, Bowman RE. Rank, rhesus social behavior, and stress. Folia Primatol 1976; 26: 57-66.
33. McGuire MT, Brammer GL, Raleigh MJ. Resting cortisol levels and the emergence of dominant status among male vervet monkeys. Horm Behav 1986; 20: 106-117.
34. Morgan D, Grant KA, Prioleau OA, Nader SH, Kaplan JR, Nader MA. Predictors of social status in cynomolgus monkeys (Macaca fascicularis) after group formation. Am J Primatol 2000; 52: 115-131.
35. Stavisky RC, Adams MR, Watson SL, Kaplan JR. Dominance, cortisol and behavior in small groups of female cynomolgus monkeys (Macaca fascicularis). Horm Behav 2001; 39: 232-238.
36. Yodyingyuad U, Eberhart JA, Keverne EB. Effects of rank and novel females on behaviour and hormones in male talapoin monkeys. Physiol Behav 1982; 28: 995-1005.
37. Eberhart JA, Yodyingyuad U, Keverne EB. Subordination in male talapoin monkeys lowers sexual behavior in the absence of dominants. Physiol Behav 1985; 35: 673-677.
38. Goo GP, Sassenrath EN. Persistent adrenocortical activation in female rhesus monkeys after new breeding groups formation. J Med Primatol 1980; 9: 325-334.
39. Mendoza SP, Coe CL, Lowe EL, Levine S. The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology 1979; 3: 221-229.
40. Berstein IS, Gordon CP, Rose RM. The interaction of hormones, behavior, and social context in nonhuman primates. In: Savre BB, ed. Hormones and Aggressive Behavior. New York, NY: Plenum, 1983: 535-561.
41. Clarke AS, Kaplan JR, Bumsted PT, Koritnik DR. Social dominance and serum. testosterone concentrations in dyads of male Macaca fascicularis. J Med Primatol 1986; 15: 419.
42. Rose RM, Berstein IS, Gordon TP. Consequences of social conflict on plasma testosterone levels in rhesus monkeys. Psychosom Med 1975; 37: 50-61.
43. Kaplan JR, Heise ER, Manuck SB, Shively CA, Cohen S, Rabin BS, Kasprowicz AL. The relationship of agonistic and affiliative behavior patterns to cellular immune function among cynomolgus monkeys (Macaca fascicularis) living in unstable social groups. Am J Primatol 1991; 25: 157-173.
44. Coe CL, Franklin D, Smith ER, Levine S. Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol Behav 1982; 29: 1051-1057.
45. Golub MS, Sassenrath EN, Goo GP. Plasma cortisol levels and dominance in peer groups of rhesus monkey weanlings. Horm Behav 1979; 12: 50-59.
46. Gust DA, Gordon TP, Wilson ME, Ahmed-Ansari A, Brodie AR, McClure HM. Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav Immun 1991; 5: 296-307.
47. Sapolsky RM. Endocrinology of the stress response. In: Becker J, Breedlove S, Crews D, McCarthy M, eds. Behavioral Endocrinology, 2nd edn. Cambridge, MA: MIT Press, 2002: 409-450.
48. Xiao E, Xia-Zhang L, Ferin M. Inadequate luteal function is the initial clinical cyclic defect in a 12-day stress model than includes a psychogenic component in the rhesus monkey. J Clin Endocrinol Metab 2002; 87: 2232-2237.
49. Manogue KR, Leshner AI, Candland DK. Dominance status and adrenocortical reactivity to stress in squirrel monkeys. Primates 1975; 16: 457-463.
50. Winslow JT, Miczek KA. Androgen dependency of alcohol effects on aggressive behavior: A seasonal rhythm in high-ranking squirrel monkeys. Psychopharmacology 1988; 95: 92-98.
51. Beehner JC, Phillips-Conroy JE, Whitten PL. Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons. Am J Primatol 2005; 67: 101-119.
52. Batty KA, Herbert J, Keverne EB, Velluci SV. Differences in blood levels of androgens in female talapoin monkeys related to their social status. Neuroendocrinology 1986; 44: 347-354.
53. Coe CL, Mendoza SP, Levine S. Social status constrains the stress response in the squirrel monkey. Physiol Behav 1979; 23: 633-638.
54. Gonzalez CA, Coe CL, Levine S. Cortisol responses under different housing conditions in female squirrel monkeys. Psychoneuroendocrinology 1982; 7: 209-216.
55. Leshner AI, Candland DK. Endocrine effects of grouping and dominance rank in squirrel monkeys. Physiol Behav 1972; 8: 441-445.
56. Creel S. Social dominance and stress hormones. Trends Ecol Evol 2001; 16: 491-497.