Testosterone in juvenile and adolescent male chimpanzees (Pan troglodytes): Effects of dominance rank, aggression, and behavioral style

American Journal of Physical Anthropology

Volumn 130, Issue 4, 2006, Pages 536-545

  Anestis, Stephanie F ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Androgens; Hormones; Personality; Primates; Social behavior

Indexed keywords

TESTOSTERONE;

ADOLESCENT; AGGRESSION; ANIMAL BEHAVIOR; ARTICLE; DOMINANCE BEHAVIOR; MALE; MALE GENITAL SYSTEM; MATING; NONHUMAN; PAN TROGLODYTES; PRIMATE; SOCIAL BEHAVIOR; TESTOSTERONE BLOOD LEVEL; URINALYSIS;

AGGRESSION; AGING; ANIMALS; ANIMALS, ZOO; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; CREATININE; MALE; PAN TROGLODYTES; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; TESTOSTERONE;

EID: 33746265441     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.20387     Document Type: Article

References (110)

1. Albertsson-Wikland K, Rosberg S, Lannering B, Dunkel L, Selstam G, Norjavaara E. 1997. Twenty-four-hour profiles of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol levels: a semilongitudinal study throughout puberty in healthy boys. J Clin Endocrinol Metab 82:541-549.
2. Anestis SF. 2005. Behavioral style, dominance rank, and urinary cortisol in young chimpanzees (Pan troglodytes). Behaviour 142:1245-1268.
3. Baker KC, Aureli F. 2000. Coping with conflict during initial encounters in chimpanzees. Ethology 106:527-541.
4. Baker KC, Smuts BB. 1994. Social relationships of female chimpanzees. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne P, editors. Chimpanzee cultures. Cambridge, MA: Harvard University Press, p 227-242.
5. Bardin CW. 1996. The anabolic action of testosterone. N Engl J Med 335:52-53.
6. Bardin CW, Catterall JF. 1981. Testosterone: major determinant of extragenital sexual dimorphism. Science 211:1285-1294.
7. Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A. 2002. Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca, fuscata). Horm Behav 42:85-96.
8. Ben Saad M, Bayle J-D. 1985. Seasonal changes in plasma testosterone, thyroxine, and cortisol levels in wild rabbits (Oryctolagus cuniculus algirus) of Zembra Island. Gen Comp Endocrinol 57:388.
9. Bercovitch FB, Strum SC. 1993. Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313-318.
10. Bermond B, Mos J, Meelis W, van der Poel AM, Kruk MR. 1982. Aggression induced by stimulation of the hypothalamus: effects of androgens. Pharmacol Biochem Behav 16:41-45.
11. Bernhardt PC, Dabbs JM Jr, Fielden JA, Lutter CD. 1998. Testosterone changes during vicarious experiences of winning and losing among fans at sporting events. Physiol Behav 65: 59-62.
12. Bernstein IS, Rose RM, Gordon TP. 1977. Behavioural and hormonal responses of male rhesus monkeys introduced to females in the breeding and non-breeding seasons. Anim Behav 25:609-614.
13. Blank MS, Murphy JR. 1991. Luteinizing hormone sensitivity to naloxone in maturing male chimpanzees. Brain Res Bull 27:241-245.
14. Bloomsmith MA, Baker KC. 2001. Social management of captive chimpanzees. In: Brent L, editor. The care and management of captive chimpanzees. San Antonio: American Society of Primatologists. p 205-241.
15. Boehm C. 1994. Pacifying interventions at Arnhem Zoo and Gombe. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne P, editors. Chimpanzee cultures. Cambridge, MA: Harvard University Press, p 211-226.
16. Boesch C, Boesch-Achermann H. 2000. The chimpanzees of the Tai forest: behavioural ecology and evolution. Oxford: Oxford University Press.
17. Booth A, Shelley G, Mazur A, Tharp G, Kittok R. 1989. Testosterone, and winning and losing in human competition. Horm Behav 23:556-571.
18. Bradley A, Stoddart D. 1992. Seasonal changes in plasma androgens, glucocorticoids and glucocorticoid-binding proteins in the marsupial sugar glider Petaurus breviceps. J Endocrinol 132:21-31.
19. Bremner WJ, Vitello MV, Prinz PN. 1983. Loss of circadian rhythmicity in blood testosterone levels with aging in normal men. J Clin Endocrinol Metab 56:1278-1281.
20. Bribiescas RG. 1996. Testosterone levels among Ache huntergatherer men: a functional interpretation of population variation among adult males. Hum Nat 7:163-188.
21. Bribiescas RG. 2001a. Reproductive ecology and life history of the human male. Yrbk Phys Anthropol 44:148-176.
22. Bribiescas RG. 2001b. Reproductive physiology of the human male: an evolutionary and life history perspective. In: Ellison PT, editor. Reproductive ecology and human evolution. New York: Aldine de Gruyter. p 107-135.
23. Brockman DK, Whitten PL, Richard AF, Schneider A. 1998. Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. Am J Phys Anthropol 105:137-151.
24. Brockman DK, Whitten PL, Richard AF, Benander B. 2001. Birth season testosterone levels in male Verreaux's sifaka, Propithecus verreauxi: insights into socio-demographic factors mediating seasonal testicular function. Behav Ecol Sociobiol 49:117-127.
25. Bruce J, Davis EP, Gunnar MR. 2002. Individual differences in children's cortisol response to the beginning of a new school year. Psychoneuroendocrinology 27:635-650.
26. Catling P, Sutherland R. 1980. Effect of gonadectomy, season and the presence of female tammar wallabies (Macropus eugenii) on concentrations of testosterone, luteinizing hormone and follicle-stimulating hormone in the plasma of male tammar wallabies. J Endocrinol 86:25-33.
27. Cavigelli SA, Pereira ME. 2000. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm Behav 37:246-255.
28. Coe CL, Smith ER, Mendoza SP, Levine S. 1983. Varying influence of social status on hormone levels in male squirrel monkeys. In: Steklis HD, Kling AS, editors. Hormones, drugs, and social behavior in primates. New York: Spectrum Publications, p 7-32.
29. Copeland KC, Eichberg JW, Parker CRJ, Bartke A. 1985. Puberty in the chimpanzee: somatomedin-C and its relationship to somatic growth and steroid hormone concentrations. J Clin Endocrinol Metabol 60:1154-1160.
30. Gumming DC, Quigley ME, Yen SSC. 1983. Acute suppression of circulating testosterone levels by cortisol in men. J Clin Endocrinol Metab 57:671-673.
31. de Vries H. 1995. An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50:1375-1389.
32. de Waal FBM. 1982. Chimpanzee politics. Baltimore: Johns Hopkins University Press.
33. de Waal FBM. 1994. Chimpanzee's adaptive potential: a comparison of social life under captive and wild conditions. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG, editors. Chimpanzee cultures. Cambridge, MA: Harvard University Press, p 243-260.
34. Dinzburg AL, Chirkov AM, Chirkova SK, Voit IS. 1992. Stress-induced changes in behavior and function of the neurohormonal systems in monkeys differing in social rank. Bull Exp Biol Med 114:1579-1581.
35. Dufty AMJ. 1989. Testosterone and survival: a cost of aggressiveness? Horm Behav 23:185-193.
36. Eaton GG, Resko JA. 1974. Plasma testosterone and male dominance in a Japanese macaque troop compared with repeated measures of testosterone in laboratory males. Horm Behav 5:251-259.
37. Elia M. 1992. Organ and tissue contribution to metabolic rate. In: Kinney JM, Tucker HN, editors. Energy metabolism: tissue determinants and cellular corollaries. New York: Raven Press, p 61-79.
38. Ellison PT. 2001. On fertile ground: a natural history of human reproduction. Cambridge, MA: Harvard University Press.
39. Ellison PT. 2003. Energetics and reproductive effort. Am J Human Biol 15:342-351.
40. Forger NG, Breedlove M. 1987. Seasonal variation in mammalian striated muscle mass and motoneuron morphology. J Neurobiol 18:155-165.
41. George FW. 1996. Sexual differentiation. In: Griffin JE, Ojeda SR, editors. Textbook of endocrine physiology. New York: Oxford University Press, p 147-163.
42. Gonzales-Bono E, Salvador A, Ricarte J, Serrano MA, Arnedo M. 2000. Testosterone and attribution of successful competition. Aggr Behav 26:235-240.
43. Goodall J. 1984. The nature of the mother-child bond and the influence of the family on the social development of free-living chimpanzees. In: Kobayashi N, Brazelton T, editors. The growing child in family and society. Tokyo: University of Tokyo Press, p 47-66.
44. Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior. Boston: Bellknap Press.
45. Griffin JE. 1996. Male reproductive function. In: Griffin JE, Ojeda SR, editors. Textbook of endocrine physiology. New York: Oxford University Press, p 201-222.
46. Hagey LR, Czekala NM. 2003. Comparative urinary androstanes in the great apes. Gen Comp Endocrinol 130:64-69.
47. Hayaki H. 1988. Association partners of young chimpanzees in the Mahale Mountains National Park, Tanzania. Primates 29:147-161.
48. Hayaki H, Huffman MA, Nishida T. 1989. Dominance among male chimpanzees in the Mahale Mountains National Park, Tanzania: a preliminary study. Primates 30:187-197.
49. Hirata S, Celli ML. 2003. Role of mothers in the acquisition of tool-use behaviours by captive infant chimpanzees. Anim Cogn 6:235-244.
50. Hirschenhauser K, Winkler H, Oliveira RF. 2003. Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm Behav 43:519.
51. Kagan J. 1989. Temperamental contributions to social behavior. Am Psychol 44:668-674.
52. Kalin NH, Shelton SE, Davidson RJ. 2000. Cerebrospinal fluid corticotropin-releasing hormone levels are elevated in monkeys with patterns of brain activity associated with fearful temperament. Biol Psychiatry 47:579-585.
53. Kawanaka K. 1989. Age differences in social interactions of young males in a chimpanzee unit-group at the Mahale Mountains National Park, Tanzania. Primates 30:285-305.
54. Ketterson ED, Nolan VJ. 1992. Hormones and life histories: an integrative approach. Am Nat 140:33-62.
55. Kirkwood RN, Cumming DC, Aherne FX. 1987. Nutrition and puberty in the female. Proc Nutr Soc 46:177-192.
56. Kjeld JM, Puah CM, Joplin GE. 1977. Rise of unconjugated sex hormones in human urine on storage. Clin Chim Acta 80:285-291.
57. Klinkova E, Heistermann M, Hodges JK. 2004. Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes). Horm Behav 46:474-481.
58. Knapp R, Wingfield JC, Bass AH. 1999. Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Horm Behav 35:89.
59. Knott CD. 1997. Field collection and preservation of urine in orangutans and chimpanzees. Trop Biodivers 4:95-102.
60. Kondo M, Udono T, Jin W, Shimizu K, Funakoshi M, Itoh M, Watanabe G, Groome NP, Taya K. 2000. Changes in plasma concentrations of inhibin A and inhibin B throughout sexual maturation in the male chimpanzee. Endocr J 47:707-714.
61. Kraemer HC, Horvat JR, Doering C, McGinnis PR. 1982. Male chimpanzee development focusing on adolescence: integration of behavioral with physiological changes. Primates 23:393-405.
62. Kutsukake N, Castles DL. 2004. Reconciliation and post-conflict third-party affiliation among wild chimpanzees in the Mahale Mountains, Tanzania. Primates 45:157-165.
63. Marier CA, Moore MC. 1988. Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behav Ecol Sociobiol 23:21-26.
64. Marshall A, Hohmann G. 2005. Urinary testosterone levels of wild male bonobos (Pan paniscus) in the Lomako Forest, Democratic Republic of Congo. Am J Primatol 65:87-92.
65. Marson J, Meuris S, Cooper RW, Jouannet P. 1991. Puberty in the male chimpanzee: time-related variations in luteinizing hormone, follicle-stimulating hormone, and testosterone. Biol Reprod 44:456-460.
66. Martin DE, Swenson RB, Collins DC. 1977. Correlation of serum testosterone levels with age in male chimpanzees. Steroids 29:471-481.
67. Mazur A, Booth A, Dabbs JMJ. 1992. Testosterone and chess competition. Soc Psychol Q 55:70-77.
68. Mitamura R, Yano K, Suzuki N, Ito Y, Makita Y, Okuno A. 2000. Diurnal rhythms of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol secretion before the onset of female puberty in short children. J Clin Endocrinol Metab 85:1074-1080.
69. Mohle U, Heistermann M, Palme R, Hodges JK. 2002. Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen Comp Endocrinol 129:135-145.
70. Moore SL, Wilson K. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297: 2015-2018.
71. Muehlenbein M. 2004. Testosterone-mediated immune function: an energetic allocation mechanism in human and non-human primate males. Ph.D. dissertation, Yale University.
72. Muehlenbein M, Watts DP, Whitten PL. 2004. Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol 64:71-82.
73. Muller MN. 2002. Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press, p 112-124.
74. Muller MN, Lipson SF. 2003. Diurnal patterns of urinary steroid excretion in wild chimpanzees. Am J Primatol 60:161-166.
75. Muller MN, Wrangham RW. 2004. Dominance, aggression and testosterone in wild chimpanzees: a test of the "challenge hypothesis." Anim Behav 67:113-123.
76. Nadler RD, Wallis J, Roth-Meyer C, Cooper RW, Baulieu E-E. 1987. Hormones and behavior of prepubertal and peripubertal chimpanzees. Horm Behav 21:118-131.
77. Neave N, Wolfson S. 2003. Testosterone, territoriality, and the "home advantage." Physiol Behav 78:269-275.
78. Nieuwenhuijsen K, de Neef KJ, van der Werff ten Bosch JJ, Slob AK. 1987. Testosterone, testis size, seasonality, and behavior in group-living stumptail macaques (Macaca arctoides). Horm Behav 21:153-169.
79. Nishida T, Hosaka K. 1996. Coalition strategies among adult male chimpanzees of the Mahale Mountains. In: McGrew WC, Marchant LF, Nishida T, editors. Great ape societies. Cambridge: Cambridge University Press, p 114-135.
80. Nishida T, Kano T, Goodall J, McGrew WC, Nakamura M. 1999. Ethogram and ethnography of Mahale chimpanzees. Anthropol Sci 107:141-188.
81. Nunes S, Fite JE, French JA. 2000. Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Anim Behav 60:857-865.
82. Olsen N, Kovacs W. 1996. Gonadal steroids and immunity. Endocr Rev 17:369-384.
83. Ostner J, Kappeler P, Heistermann M. 2002. Seasonal variation and social correlates of androgen excretion in male red-fronted lemurs (Lemur fulvus rufus). Behav Ecol Sociobiol 52: 485-495.
84. Perret M, 1992. Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol (Basel) 59:1-25.
85. Pusey AE. 1990. Behavioural changes at adolescence in chimpanzees. Behaviour 115:203-246.
86. Robbins MM, Czekala NM. 1997. A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas. Am J Primatol 43:51-64.
87. Roberts ML, Buchanan KL, Evans MR. 2004, Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227-239.
88. Rose RM, Holaday JW, Bernstein IS. 1971. Plasma testosterone, dominance rank and aggressive behaviour in male rhesus monkeys. Nature 231:366-368.
89. Sannen A, van Eisacker L, Heistermann M, Eens M. 2004. Urinary testosterone-metabolite levels and dominance rank in male and female bonobos (Pan paniscus). Primates 45:89-96.
90. Sapolsky RM. 1985. Stress-induced suppression of testicular function in the wild-baboon: role of glucocorticoids. Endocrinology 116:2273-2278.
91. Sapolsky RM, Ray JC. 1989. Styles of dominance and their endocrine correlates among wild olive baboons (Papio anubis). Am J Primatol 18:1-13.
92. Setchell JM, Dixson AF. 2001. Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177-184.
93. Setchell JM, Dixson AF. 2002. Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx). Am J Primatol 56:9-25.
94. Spijkerman RP, van Hooff JARAM, Dienske H, Jens W. 1997. Differences in subadult behaviours of chimpanzees living in peer groups and in family groups. Int J Primatol 18:439-454.
95. Spratt DI, O'Dea LS, Schoenfeld D, Butler J, Rao PN, Crowley WFJ. 1988. Neuroendocrine-gonadal axis in men: frequent sampling of LH, FSH, and testosterone. Am J Phys Endocrinol Metab 254:658-666.
96. 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). Am J Primatol 11:133-145.
97. Stoinski TS, Czekala N, Lukas KE, Maple TL. 2002. Urinary androgen and corticoid levels in captive, male western low-land gorillas (Gorilla g. gorilla): age- and social group-related differences. Am J Primatol 56:73-87.
98. Storey AE, Walsh CJ, Quintan RL, Wynne-Edwards KE. 2000. Hormonal correlates of paternal responsiveness in new and expectant fathers. Evol Hum Behav 21:79-95.
99. Strier KB, Ziegler TE, Wittwer DJ. 1999. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm Behav 35:125-134.
100. Tanriverdi F, Silveira L, MacColl G, Bouloux P. 2003. The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 176:293-304.
101. Taussky HH. 1954. A microcolormetric determination of creatinine in urine by the Jaffe reaction. J Biol Chem 208:853-861.
102. Vleck CM, Brown JL. 1999. Testosterone and social and reproductive behaviour in Aphelocoma jays. Anim Behav 58:943-951.
103. Whalen RE. 1968. Differentiation of the neural mechanisms which control gonadotropin secretion and sexual behavior. In: Diamond M, editor. Reproduction and sexual behavior. Bloomington, IN: Indiana University Press, p 303-340.
104. Whitten P, Turner T. 2004. Male residence and the patterning of serum testosterone in vervet monkeys (Cercopithecus aethiops). Behav Ecol Sociobiol 56:565-578.
105. Wingfield JC, Hegner RE, Dufty AMJ, Ball GF. 1990. The "challenge hypothesis;" theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829-846.
106. Wynne-Edwards KE. 2001. Hormonal changes in mammalian fathers. Horm Behav 40:139-145.
107. Young LG, Gould KG, Smithwick EB. 1993. Selected endocrine parameters of the adult male chimpanzee. Am J Primatol 31:287-297.
108. Ziegler TE. 2000. Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatol (Basel) 71:6-21.
109. Zihlman A, Bolter D, Boesch C. 2004. Wild chimpanzee dentition and its implications for assessing life history in immature hominin fossils. Proc Natl Acad Sci USA 101:10541-10543.
110. Zuk M, McKean KA. 1996. Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009-1024.