Social factors increase fecal testosterone levels in wild male gray-cheeked mangabeys (Lophocebus albigena)

Hormones and Behavior

Volumn 59, Issue 4, 2011, Pages 605-611

  Arlet, Małgorzata E ^a,b   Kaasik, Ants ^a   Molleman, Freerk ^a,b   Isbell, Lynne ^b   Carey, James R ^b   Mänd, Raivo ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aggression; Peak swelling females; Social status

Indexed keywords

RAIN; TESTOSTERONE;

AGGRESSION; ARTICLE; BABOON; CERCOCEBUS; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ESTRUS; FECES ANALYSIS; HORMONE DETERMINATION; IMMIGRANT; LOPHOCEBUS ALBIGENA; MALE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SEASONAL VARIATION; SEXUAL BEHAVIOR; SEXUAL SWELLING; SOCIAL ASPECT; TEMPERATURE; UGANDA;

AGGRESSION; ANIMALS; CERCOCEBUS; ENVIRONMENT; FECES; FEMALE; MALE; SEXUAL BEHAVIOR, ANIMAL; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; TESTOSTERONE;

EID: 79954661580     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.02.018     Document Type: Article

References (67)

1. Arlet M.E., Isbell L.A. Variation in behavioral and hormonal responses of adult male gray-cheeked mangabeys (Lophocebus albigena) to crowned eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behav. Ecol. Sociobiol. 2009, 63:491-499.
2. Arlet M.E., Carey J.R., Molleman F. Species and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park, Uganda. Primates 2009, 50:65-73.
3. Arlet M.E., Grote M., Molleman F., Isbell L.A., Carey J.R. Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena). Horm. Behav. 2009, 55:210-216.
4. Arlet M.E., Molleman F., Chapman C.A. Indications for female mate choice in grey-cheeked mangabeys Lophocebus albigena johnstoni in Kibale National Park, Uganda. Acta Ethologica 2007, 10:89-95.
5. Arlet M.E., Molleman F., Chapman C.A. Mating tactics in male grey-cheeked mangabeys (Lophocebus albigena). Ethology 2008, 114:851-862.
6. Bales K.L., French J.A., McWilliams J., Lake R.A., Dietz J.M. Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia). Horm. Behav. 2006, 49:88-95.
7. Balthazart J. Hormonal correlates of behaviour. Avian Biol. 1983, 7:221-365.
8. Barrett G.M., Shimizu K., Bardi M., Asaba S., Mori A. Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm. Behav. 2002, 42:85-96.
9. Bercovitch F.B. Dominance rank and reproductive maturation in rhesus macaques (Macaca mulatta). J. Reprod. Fertil. 1993, 99:113-120.
10. Booth A., Granger D.A., Mazur A., Kivlighan K.T. Testosterone and social behaviour. Soc. Forces 2006, 85:167-191.
11. Bribiescas R.G. Reproductive ecology and life history of the human male. Yearb. Phys. Anthropol. 2001, 44:148-176.
12. Briganti F., Seta D.D., Fontani G., Lodi L., Lupo C. Behavioral effects of testosterone in relation to social rank in the male rabbit. Aggress. Behav. 2003, 29:269-278.
13. Cavigelli S.A., Pereira M.E. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 2000, 37:246-255.
14. Celac P., Smreková L., Ostatníková D., Cabajová Z., Hodosy J., Kúdela M. Lack of evidence for meteorological effects on infradian dynamics of testosterone. Int. J. Biometeorol. 2009, 53:409-413.
15. Chancellor R.L., Isbell L.A. Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. Behav. Ecol. 2009, 20:79-86.
16. Chapman C.A., Wasserman M.D., Gillespie T.R., Speirs M.L., Lawes M.J., Saj T.L., Ziegler T.E. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am. J. Phys. Anthropol. 2006, 131:525-534.
17. Coe C.L., Smith E.R., Mendoza S.P., Levine S. Varying influence of social status on hormone levels in male squirrel monkeys. Hormones, Drugs, and Social Behaviour in Primates 1983, 7-21. SP Medical and Scientific Books, New York. H.D. Steklis, A.S. Kling (Eds.).
18. Creel S. Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 2005, 86:255-264.
19. Dixon A.F. Primate Sexuality. Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings 1998, Oxford University Press, Oxford.
20. Eberhart J.A., Yodyingyuad U., Keverne E.B. Subordination in male talapoin monkeys lowers sexual behaviour in the absence of dominants. Physiol. Behav. 1985, 35:673-677.
21. Gesquiere L.R., Onyango P.O., Alberts S.C., Altmann J. Endocrinology of year-round reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males. Am. J. Phys. Anthropol. 2011, 144:169-176.
22. Girard-Buttoz C., Heistermann M., Krummel S., Engelhardt A. Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiol. Behav. 2009, 98:168-175.
23. Gordon T.P., Rose R.M., Bernstein I.S. Seasonal rhythm in plasma testosterone levels in the rhesus monkey (Macaca mulatta): a three-year study. Horm. Behav. 1976, 7:229-243.
24. Griffin J.E. Male reproductive function. Textbook of Endocrine Physiology 1996, 201-222. Oxford University Press, Oxford. J.E. Griffin, S.R. Ojeda (Eds.).
25. Hansen P.J. Effect of heat stress on mammalian reproduction. Philos. Trans. R. Soc. 2009, 364:3341-3350.
26. Holekamp K.E., Smale L. Dispersal status influences hormones and behaviour in the male spotted hyena. Horm. Behav. 1998, 33:205-216.
27. Janmaat K.R., Byrne R.W., Zuberbühler K. Evidence for spatial memory of fruitive states of rainforest trees in wild mangabeys. Anim. Behav. 2006, 72:797-802.
28. Janmaat K.R., Olupot W., Chancellor R.L., Arlet M.E., Waser P.M. Long-term site fidelity and individual home range shifts in Lophocebus albigena. Int. J. Primatol. 2009, 30:443-466.
29. Kemnitz J.W., Sladky K.K., Flitsch T.J., Pomerantz S.M., Goy R.W. Androgenic influence on body size and composition of adult rhesus monkeys. Am. J. Physiol. 1988, 255:E857-E864.
30. Kraus C., Heistermann M., Kappeler P.M. Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)?. Physiol. Behav. 1999, 66:855-861.
31. Lambert J. Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol. Anthropol. 1998, 7:8-20.
32. Lynch J.W., Ziegler T.E., Strier K.B. Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm. Behav. 2002, 41:275-287.
33. McCaul K.D., Gladue B.A., Joppa M. Winning, losing, mood, and testosterone. Horm. Behav. 1992, 26:486-504.
34. Mendoza S.P., Coe C.L., Lowe E.L., Levine S. The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology 1979, 3:221-229.
35. Muehlenbein M.P. The immunosomatic metabolic diversion hypothesis and testosterone correlates with intestinal parasitemia in wild male chimpanzees. Am. J. Phys. Anthropol. 2004, 38:150. suppl.
36. Muehlenbein M.P., Watts D.P., Whitten P.L. Dominance rank and fecal testosterone in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am. J. Primatol. 2004, 64:71-82.
37. Muller M.N., Wrangham R.W. Dominance, aggression and testosterone in wild chimpanzees: a test of the 'challenge hypothesis'. Anim. Behav. 2004, 67:113-123.
38. Munro C., Stabenfeldt G. Development of cortisol enzyme immunoassay in plasma. Clin. Chem. 1984, 31:985.
39. Muroyama Y., Shimizu K., Sugiura H. Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques. Am. J. Primatol. 2007, 69:603-610.
40. Olupot, W., 1999. Mangabey dispersal and conservation in Kibale Forest National Park, Uganda. (Dissertation). Purdue University, USA.
41. Olupot W., Waser P.M. Correlates of intergroup transfer in male grey-cheeked mangabeys. Int. J. Primatol. 2001, 22:169-187.
42. Olupot W., Waser P.M. Patterns of male residency and inter-troop transfer in gray-cheeked mangabeys (Lophocebus albigena). Am. J. Primatol. 2005, 66:331-349.
43. Pinheiro J.C., Bates D.M. Mixed-effects Models in S and S-PLUS 2000, Springer.
44. Pinheiro J.C., Bates D.M., DebRoy S., Sarkar D. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-93 2009, the R Core team.
45. Rose R.M., Bernstein I.S., Gordon T.P. Consequences of social conflict on plasma testosterone levels in rhesus monkeys. Psychosom. Med. 1975, 37:50-60.
46. Sands J., Creel S. Social dominance, aggression and faecal glucocorticoid level in a wild population of wolves, Canis lupus. Anim. Behav. 2004, 67:387-396.
47. Sannen A., van Elsacker L., Heistermann M., Eens M. Urinary testosterone-metabolite levels and dominance rank in male and female bonobos (Pan paniscus). Primates 2004, 45:89-96.
48. Sapolsky R.M. Endocrine aspects of social instability in the olive baboon (Papio anubis). Am. J. Primatol. 1983, 5:365-379.
49. Sapolsky R.M. Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology 1991, 16:281-293.
50. Sapolsky R.M. The physiology of dominance in stable versus unstable social hierarchies. Primate Social Conflict 1993, 171-204. State University of New York Press, New York. W.A. Mason, S.P. Mendoza (Eds.).
51. Sapolsky R.M. Social status and health in humans and other animals. Annu. Rev. Anthropol. 2004, 33:393-418.
52. Seraphin, S.B., 2000. The reproductive ecology and stress physiology of free-ranging male chimpanzees in Budongo Forest, Uganda. Master's Thesis, Oxford University, Oxford, UK.
53. Silk J.B. Social behavior in evolutionary perspective. Primate Societies 1987, 318-329. University of Chicago Press, Chicago. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, T.T. Struhsaker (Eds.).
54. Steklis H.D., Raleigh M.J., Kling A.S., Tachiki K. Biochemical and hormonal correlates of dominance and social behaviour in all-male groups of squirrel monkeys (Saimiri sciureus). Am. J. Primatol. 1986, 11:133-145.
55. Strier K.B., Ziegler T.E. Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am. J. Primatol. 1997, 42:299-310.
56. Strier K.B., Ziegler T.E. Advances in field-based studies of primate behavioral endocrinology. Am. J. Primatol. 2005, 67:1-4.
57. Struhsaker T.T. The Red Colobus Monkey 1975, University of Chicago Press, Chicago.
58. Teichroeb J.A., Sicotte P. Social correlates of fecal testosterone in male ursine colobus monkeys (Colobus vellerosus): the effect of male reproductive competition in aseasonal breeders. Horm. Behav. 2008, 54:417-423.
59. Wallis S.J. Sexual behavior and reproduction of Cercocebus albigena johnstoni in Kibale Forest, western Uganda. Int. J. Primatol. 1983, 4:153-166.
60. Waser P. Feeding, ranging and group size in the mangabey (Cercocebus albigena). Primate Ecology 1977, 183-222. Academic Press, London. T.H. Clutton-Brock (Ed.).
61. Welle S., Jozefowicz R., Forbes G., Griggs R.C. Effect of testosterone on metabolic rate and body composition in normal men and men with muscular dystrophy. J. Clin. Endocrinol. Metab. 1992, 74:332-335.
62. Whitten P.L., Brockman D.K., Stavisky R.C. Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Amer. J. Phys. Anthropol. 1999, 107:1-23.
63. Wickings E.J., Dixson A.F. Testicular function, secondary sexual development and social status in male mandrills (Mandrillus sphinx). Physiol. Behav. 1992, 52:909-916.
64. Wingfield J.C., Hegner R.E., Ball G.F., Dufty A.M. The 'challenge hypothesis': theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 1990, 136:829-846.
65. Wolfe-Coote S. The Laboratory Primate 2005, 2038. Elsevier Academic Press.
66. Ziegler T.E., Scheffler G., Snowdon C.T. The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm. Behav. 1995, 29:407-424.
67. Zucker E.L., O'Neil J.A.S., Harrison R.M. Fecal testosterone values for free-ranging male mantled howling monkeys (Alouatta palliata) in Costa Rica. IPS/ASP Congress Abstracts 1996, 112.