Testosterone dynamics during encounter: Role of emotional factors

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 198, Issue 7, 2012, Pages 485-494

  Chichinadze, Konstantin ^a,b   Lazarashvili, Ann ^c   Chichinadze, Nodar ^c   Gachechiladze, Ledi ^c  

^a Tbilisi St Andrew the First Called Georgian University of Georgian Patriarchate   (Georgia)

^b TBILISI STATE UNIVERSITY   (Georgia)

^c A Natishvili Institute of Morphology   (Georgia)

Author keywords

Aggressive behavior; Dominant; Emotions; Testosterone; Winner

Indexed keywords

BIOLOGICAL MARKER; TESTOSTERONE;

AFFECT; AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; ANTICIPATION; ASSERTIVENESS; BLOOD; COMPETITIVE BEHAVIOR; EMOTION; HUMAN; MALE; REVIEW; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; TIME;

AFFECT; AGGRESSION; ANIMALS; ANTICIPATION, PSYCHOLOGICAL; ASSERTIVENESS; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; COMPETITIVE BEHAVIOR; DOMINANCE-SUBORDINATION; EMOTIONS; HUMANS; MALE; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; TESTOSTERONE; TIME FACTORS;

EID: 84862652243     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-012-0726-1     Document Type: Review

References (125)

1. Adkins-Regan E (2005) Hormones and animal social behaviour. Princeton University Press, Princeton.
2. Aikey JL, Nyby JG, Anmuth DM, James PJ (2002) Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm Behav 42: 448-460.
3. Almeida OP, Waterreus A, Spry N, Flicker L, Martins RN (2004) One year follow-up study of the association between chemical castration, sex hormones, beta-amyloid, memory and depression in men. Psychoneuroendocrinology 29: 1071-1081.
4. Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30(3): 319-345.
5. Barrett-Connor E, Goodman-Gruen D, Patay B (1999) Endogenous sex hormones and cognitive function in older men. J Clin Endocrinol Metab 84: 3681-3685.
6. Bateup HS, Booth A, Shirtcliff EA, Granger DA (2002) Testosterone, cortisol, and women's competition. Evol Hum Behav 23: 181-192.
7. Bayer HM, Glimcher PW (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47: 129-141.
8. Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2006) Testosterone predicts future dominance rank and mating activity among male chacma baboons. Behav Ecol Sociobiol 59: 469-479.
9. 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.
10. Bonson KR, Garrick NA, Murphy DL (1994) Evidence for a withdrawal syndrome following chronic administration of an anabolic steroid to rats. Soc Neurosci Abstr 20: 1527.
11. Booth A, Shelley G, Mazur A, Tharp G, Kittok R (1989) Testosterone, and winning and losing in human competition. Horm Behav 23: 556-571.
12. Bouissou MF, Vandenheede M (1996) Long-term effects of androgen treatment on fear reactions in ewes. Horm Behav 30: 93-99.
13. Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc B 268: 1337-1344.
14. Buck CL, Barnes BM (2003) Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm Behav 43: 318-326.
15. Campbell B, O'Rourke M, Rabow M (1988) Pulsatile response of salivary testosterone and cortisol to aggressive competition in young males. In: Annual meeting of the American Association of Physical Anthropologists, Kansas City, Missouri.
16. Carre JM (2009) No place like home: testosterone responses to victory depend on game location. Am J Hum Biol 21: 392-394.
17. Carre J, Muir C, Belanger J, Putnam SK (2006) Pre-competition hormonal and psychological levels of elite hockey players: relationship to the 'home advantage'. Physiol Behav 89: 392-398.
18. Castro WL, Matt KS (1997) Neuroendocrine correlates of separation stress in the Siberian dwarf hamster (Phodopus sungorus). Physiol Behav 61: 477-484.
19. Cavigelli SA, Pereira ME (2000) Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm Behav 37: 246-255.
20. Chichinadze K, Chichinadze N (2008) Stress-induced increase of testosterone: Contributions of social status and sympathetic reactivity. Physiol Behav 94: 595-603.
21. Chichinadze K, Chichinadze N, Lazarashvili A (2009) New classification and neurobiology of aggressive behavior. In: Quin C, Tawse S (eds) Handbook of aggressive behavior research. Nova Publishers, New York, pp 183-213.
22. Chichinadze KN, Domianidze TR, Matitaishvili TTs, Chichinadze NK, Lazarashvili AG (2010) Possible relation of plasma testosterone level to aggressive behavior of male prisoners. B Exp Biol Med 149: 7-9.
23. Chichinadze K, Chichinadze N, Lazarashili A (2011) Hormonal and neurochemical mechanisms of aggression and a new classification of aggressive behavior. Aggress Violent Behav 16: 461-471.
24. Christiansen K (2001) Behavioural effects of androgen in men and women. J Endocrinol 170: 39-48.
25. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N (2012) Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482: 85-88.
26. Consten D, Lambert JG, Goos HJ (2001) Cortisol affects testicular development in male common carp, Cyprinus carpio L., but not via an effect on LH secretion. Comp Biochem Physiol B Biochem Mol Biol 129: 671-677.
27. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16: 491-497.
28. Creel S, Sands JL (2003) Is social stress a consequence of subordination or a cost of dominance? In: de Waal F, Tyack P (eds) Animal social complexity. Harvard University Press, Cambridge, pp 153-179.
29. De Ridder E, Pinxten R, Eens M (2000) Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird. Behav Ecol Sociobiol 49: 24-30.
30. Denk AG, Kempenaers B (2005) Testosterone and testes size in mallards (Anas platyrhynchos). J Ornithol 147: 436-440.
31. Dong Q, Salva A, Sottas CM, Niu E, Holmes M, Hardy MP (2004) Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl 25: 973-981.
32. Ebinger M, Sievers C, Ivan D, Schneider HJ, Stalla GK (2009) Is there a neuroendocrinological rationale for testosterone as a therapeutic option in depression? J Psychopharmacol 23: 841-853.
33. Esch T, Stefano GB (2004) The neurobiology of pleasure, reward processes, addiction and their health implications. Neuroendocrinol Lett 25: 235-251.
34. Fenske M (1997) Role of cortisol in the ACTH-induced suppression of testicular steroidogenesis in guinea pigs. J Endocrinology 154: 407-414.
35. Fielden J, Lutter C, Dabbs J (1994) Basking in glory: testosterone changes in world cup soccer fans, Psychology Department, Georgia State University.
36. Foerster K, Poesel A, Kunc H, Kempenaers B (2002) The natural plasma testosterone profile of male blue tits during the breeding season and its relation to song output. J Avian Biol 33: 269-275.
37. Frye C (2007) Some rewarding effects of androgens may be mediated by actions of its 5α-reduced metabolite 3α-Androstanediol. Pharmacol Biochem Behav 86: 354-367.
38. Frye CA, Seliga AM (2001) Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn Affect Behav Neurosci 1: 371-381.
39. Frye CA, Rhodes ME, Rosellini R, Svare B (2002) The nucleus accumbens as a site of action for rewarding properties of testosterone and its 5a-reduced metabolites. Pharmacol Biochem Behav 74: 119-127.
40. Fusani L, Day LB, Canoine V, Reinemann D, Hernandez E, Schlinger BA (2007) Androgen and the elaborate courtship behavior of a tropical lekking bird. Horm Behav 51: 62-68.
41. Fuxjager M, Marler C (2010) How and why the winner effect forms: influences of contest environment and species differences. Behav Ecol 21: 37-45.
42. Fuxjager MJ, Mast G, Becker EA, Marler CA (2009) The 'home advantage' is necessary for a full winner effect and changes in postencounter testosterone. Horm Behav 56: 214-219.
43. Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP (2002) Glucocorticoid induces apoptosis in rat leydig cells. Endocrinology 143: 130-138.
44. Garamszegi LZ, Eens M, Hurtrez-Bousses S, Møller AP (2005) Testosterone, testes size, and mating success in birds: a comparative study. Horm Behav 47: 389-409.
45. Giammanco M, Tabacchi G, Giammano S, Di Majo D, La Guardia M (2005) Testosterone and aggressiveness. Med Sci Monitor 11: RA 136-RA 145.
46. Gleason ED, Fuxjager MJ, Oyegbile TO, Marler CA (2009) Testosterone release and social context: when it occurs and why. Front Neuroendocrinol 30: 460-469.
47. Goldstat R, Briganti E, Tran J, Wolfe R, Davis S (2003) Transdermal testosterone improves mood, well being and sexual function in premenopausal women. Menopause 10: 390-398.
48. Gonzalez-Bono E, Salvador A, Serrano MA, Ricarte J (1999) Testosterone, cortisol, and mood in a sports team competition. Horm Behav 35: 55-62.
49. Hardy MP, Sottas CM, Ge R, McKittrick CR, Tamashiro KL, McEwen BS, Haider SG, Markham CM, Blanchard RJ, Blanchard DC, Sakai RR (2002) Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biol Reprod 67: 1750-1755.
50. Hardy MP, Gao HB, Dong Q, Ge R, Wang Q, Chai WR, Feng X, Sottas C (2005) Stress hormone and male reproductive function. Cell Tissue Res 322: 147-153.
51. Hermans E, Ramsey N, van Honk J (2008) Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol Psychiat 63: 263-270.
52. Heuser I (2002) Depression, endocrinologically a syndrome of premature aging. Maturitas 41: S19-S23.
53. Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71: 265-277.
54. Isovich E, Mijnster MJ, Flugge G, Fuchs E (2000) Chronic psychosocial stress reduces the density of dopamine transporters. Eur J Neurosci 12: 1071-1078.
55. Jara M, Carballada R, Esponda P (2004) Age-induced apoptosis in the male genital tract of the mouse. Reproduction 127: 359-366.
56. Johnson LR, Wood RI (2001) Oral testosterone self-administration in male hamsters. Neuroendocrinology 73: 285-292.
57. Josephs RA, Newman ML, Brown RP, Beer JM (2003) Status, testosterone, and human intellectual performance: stereotype threat as status concern. Psychol Sci 14: 158-163.
58. Josephs RA, Sellers JG, Newman ML, Mehta PH (2006) The mismatch effect: when testosterone and status are at odds. J Pers Soc Psychol 90: 999-1013.
59. Kempenaers B, Peters A, Foerster K (2008) Sources of individual variation in plasma testosterone levels. Philos Trans R Soc Lond B Biol Sci 363: 1711-1723.
60. King BE, Packard MG, Alexander GM (1999) Affective properties of intra-medial preoptic area injections of testosterone in male rats. Neurosci Lett 269: 149-152.
61. Kollack-Walker S, Watson SJ, Akil H (1997) Social stress in hamsters: defeat activates specific neurocircuits within the brain. J Neurosci 17: 8842-8855.
62. Koob GF, Le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278: 52-58.
63. Kraus C, Heistermann M, Kappeler PM (1999) Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithesuc verreauxi). Physiol Behav 66: 855-861.
64. Lai JC, Evans PD, Ng SH, Chong AM, Siu OT, Chan CL, Ho SM, Ho RT, Chan P, Chan CC (2005) Optimism, positive affectivity, and salivary cortisol. Br J Health Psychol 10: 467-484.
65. Mazur A (1985) A biosocial model of status in face-to-face primate groups. Soc Forces 64: 377-402.
66. Mazur A (2006) The role of testosterone in male dominance contests that turn violent. Biodemography Social Biol 53: 24-29.
67. Mazur A (2009) A hormonal interpretation of Collins's micro-sociological theory of violence. J Theor Soc Behav 39: 434-447.
68. Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21: 353-397.
69. Mazur A, Lamb T (1980) Testosterone, status, and mood in human males. Horm Behav 14: 236-246.
70. Mazur A, Susman EJ, Edelbrock S (1997) Sex difference in testosterone response to a video game contest. Evol Hum Behav 18: 317-326.
71. McCaul K, Gladue B, Joppa M (1992) Winning, losing, mood, and testosterone. Horm Behav 26: 486-506.
72. Mehta PH, Josephs RA (2010) Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Horm Behav 58: 898-906.
73. Mehta PH, Jones AC, Josephs RA (2008) The social endocrinology of dominance: basal testosterone predicts cortisol changes and behavior following victory and defeat. J Pers Soc Psychol 94: 1078-1093.
74. Mehta PH, Wuehrmann EV, Josephs RA (2009) When are low testosterone levels advantageous? The moderating role of individual versus intergroup competition. Horm Behav 56: 158-162.
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. Neave N, Wolfson S (2003) Testosterone, territoriality, and the 'home advantage'. Physiol Behav 78: 269-275.
77. Newman ML, Sellers JG, Josephs RA (2005) Testosterone, cognition, and social status. Horm Behav 47: 205-211.
78. Oliveira T, Gouveia MJ, Oliveira RF (2009) Testosterone responsiveness to winning and losing experiences in female soccer players. Psychoneuroendocrinology 34: 1056-1064.
79. Ostner J, Kappeler P, Heistermann M (2008) Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 62: 627-638.
80. Ovsiukova MV, Amikishieva AV, Kudriavtseva NN, Obut TA (2003) Anxiolytic effect of dehydroepiandrosterone sulfate in male mice with high anxiety level. Zh Vyssh Nerv Deiat Im I P Pavlova 53: 789-793 Russian.
81. Oyegbile TO, Marler CA (2005) Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm Behav 48: 259-267.
82. Packard M, Cornell A, Alexander G (1997) Rewarding affective properties of intra-nucleus accumbens injections of testosterone. Behav Neurosci 111: 219-224.
83. Packard M, Schroeder J, Alexander G (1998) Expression of testosterone conditioned place preference is blocked by peripheral or intra-accumbens injection of α-flupenthixol. Horm Behav 34: 39-47.
84. Rabkin JG, Wagner G, Rabkin R (1996) Treatment of depression in HIV+ men: literature review and report of an ongoing study of testosterone replacement therapy. Ann Behav Med 18: 24-29.
85. Raouf SA, Parker PG, Ketterson ED, Nolan V, Ziegenfus C (1997) Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proc R Soc B 264: 1599-1603.
86. Redpath SM, Mougeot F, Leckie FM, Evans SA (2006) The effects of autumn testosterone on survival and productivity in red grouse, Lagopus lagopus scoticus. Anim Behav 71: 1297-1305.
87. Richardson HN, Nelson AL, Ahmed EI, Parfitt DB, Romeo RD, Sisk CL (2004) Female pheromones stimulate release of luteinizing hormone and testosterone without altering GnRH mRNA in adult male Syrian hamsters (Mesocricetus auratus). Gen Comp Endocrinol 138: 211-217.
88. Rivera-Woll LM, Papalia M, Davis SR, Burger HG (2004) Androgen insufficiency in women: diagnostic and therapeutic implications. Hum Reprod Update 10: 421-432.
89. Ruiz-de-la-Torre JL, Manteca X (1999) Effects of testosterone on aggressive behaviour after social mixing in male lambs. Physiol Behav 68: 109-113.
90. Salvador A, Costa R (2009) Coping with competition: neuroendocrine responses and cognitive variables. Neurosci Biobehav Rev 33: 160-170.
91. Salvador A, Martinez S, Suay F, Borras JJ, Perez M, Montoro JB (1991) Relationship between testosterone and psychological mood states. II Congre s Mundial del COI de Cie'ncies de l'Esport, Barcelona.
92. Salvador A, Suay F, Gonzalez-Bono E, Serrano MA (2003) Anticipatory cortisol, testosterone and psychological responses to judo competition in young men. Psychoneuroendocrinology 28: 364-375.
93. Sapolsky RM (1991) Testicular function, social rank, and personality among wild baboons. Psychoneuroendocrinology 16: 281-293.
94. Sato SM, Schulz KM, Sisk CL, Wood RI (2008) Adolescents and androgens, receptors and rewards. Horm Behav 53: 647-658.
95. Schmidt PJ, Daly RE, Bloch M, Smith MJ, Danaceau MA, St Clair LS, Murphy JH, Haq N, Rubinow DR (2005) Dehydroepiandrosterone monotherapy in midlife-onset major and minor depression. Arch Gen Psychiat 62: 154-162.
96. Schroeder JP, Packard MG (2000) Role of dopamine receptor subtypes in the acquisition of a testosterone conditioned place preference in rats. Neurosci Lett 282: 17-20.
97. Schultheiss OC, Rohde W (2002) Implicit power motivation predicts men's testosterone changes and implicit learning in a contest situation. Horm Behav 41: 195-202.
98. Schultheiss OC, Wirth MM, Torges CM, Pang JS, Villacorta MA, Welsh KM (2005) Effects of implicit power motivation on men's and women's implicit learning and testosterone changes after social victory or defeat. J Pers Soc Psychol 88: 174-188.
99. Schultz W (2006) Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 57: 87-115.
100. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275: 1593-1599.
101. Scotti MA, Belén J, Jackson JE, Demas GE (2008) The role of androgens in the mediation of seasonal territorial aggression in male Siberian hamsters (Phodopus sungorus). Physiol Behav 95: 633-640.
102. Seidman SN, Araujo AB, Roose SP, Devanand DP, Xie S, Cooper TB, McKinlay JB (2002) Low testosterone levels in elderly men with dysthymic disorder. Am J Psychiatry 159: 456-459.
103. Shores MM, Kivlahan DR, Sadak TI, Li EJ, Matsumoto AM (2009) A randomized, double-blind, placebo-controlled study of testosterone treatment in hypogonadal older men with subthreshold depression (dysthymia or minor depression). J Clin Psychiatry 70: 1009-1016.
104. Sidibe M, Franco LA, Fredriksson G, Madej A, Malmgren L (1992) Effects on testosterone, LH and cortisol concentrations, and on testicular ultrasonographic appearance of induced testicular degeneration in bulls. Acta Vet Scand 33: 191-196.
105. Simon NG, Lu S-F (2006) Androgens and aggression. In: Nelson RJ (ed) Biology of aggression. Oxford University Press, New York, pp 211-230.
106. Soma KK (2006) Testosterone and aggression: berthold, birds and beyond. J Neuroendocrinol 18: 543-551.
107. Stefanski V (2001) Social stress in laboratory rats: behavior, immune function, and tumor metastasis. Physiol Behav 73: 385-391.
108. Suay F, Salvador A, Gonzalez-Bono E, Sanchis C, Martinez M, Martinez-Sanchis S, Simon VM, Montoro JB (1999) Effects of competition and its outcome on serum testosterone, cortisol and prolactin. Psychoneuroendocrinology 24: 551-566.
109. van der Meij L, Buunk AP, Almela M, Salvador A (2010) Testosterone responses to competition: The opponent's psychological state makes it challenging. Biol Psychol 84: 330-335.
110. van Honk J, Tuiten A, Verbaten R, van den Hout M, Koppeschaar H, Thijssen J, de Haan E (1999) Correlations among salivary testosterone, mood, and selective attention to threat in humans. Horm Behav 36: 17-24.
111. van Honk J, Tuiten A, Hermans E, Putnam P, Koppeschaar H, Thijssen J, Verbaten R, van Doornen L (2001) A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. Behav Neurosci 115: 238-242.
112. van Honk J, Peper J, Schutter D (2005) Testosterone reduces unconscious fear but not consciously experienced anxiety: Implications for the disorders of fear and anxiety. Biol Psychiat 58: 218-225.
113. Vervaecke H, de Vries H, van Elsacker L (2000) Dominance and its behavioral measures in a captive group of bonobos (Pan paniscus). Int J Primatol 21: 47-68.
114. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15: 711-724.
115. Wingfield JC, Jacobs JD, Tramontin AD, Perfito N, Meddle S, Maney DL, Soma K (2000) Toward an ecological basis of hormone-behavior interactions in reproduction of birds. In: Wallen K, Schneider JE (eds) Reproduction in context: social and environmental influences on reproduction. MIT Press, Cambridge, pp 85-128.
116. Wingfield JC, Moore IT, Goymann W, Wacker DW, Sperry T (2006) Contexts and ethology of vertebrate aggression: implications for the evolution of hormone-behavior interactions. In: Nelson RJ (ed) Biology of Aggression. Oxford University Press, New York, pp 179-210.
117. Wirth MM, Schultheiss OC (2007) Basal testosterone moderates responses to anger faces in humans. Physiol Behav 90: 496-505.
118. Wirth MM, Welsh KM, Schultheiss OC (2006) Salivary cortisol changes in humans after winning or losing a dominance contest depend on implicit power motivation. Horm Behav 49: 346-352.
119. Wobber V, Hare B, Maboto J, Lipson S, Wrangham R, Ellison PT (2010) Differential changes in steroid hormones before competition in bonobos and chimpanzees. Proc Natl Acad Sci USA 107: 12457-12462.
120. Wolkowitz OM, Reus VI, Keebler A, Nelson N, Friedland M, Brizendine L, Roberts E (1999) Double-blind treatment of major depression with dehydroepiandrosterone. Am J Psychiatry 156: 646-649.
121. Wood RI (2002) Oral testosterone self-administration in male hamsters: dose-response, voluntary exercise, and individual differences. Horm Behav 41: 247-258.
122. Wood RI (2004) Reinforcing aspects of androgens. Physiol Behav 83: 279-289.
123. Wood RI (2008) Anabolic-androgenic steroid dependence? Insights from animals and humans. Front Neuroendocrin 29: 490-506.
124. Wood RI, Johnson LR, Chu L, Schad CA, Self DW (2004) Testosterone reward: intravenous and intracerebroventricular self-administration. Psychopharmacology 171: 298-305.
125. Wrangham R, Pilbeam D (2001) African apes as time machines. In: Galdikas B, Briggs N, Sheeran L, Shapiro G, Goodall J (eds) All apes great and small. Kluwer Publishers, New York, pp 5-17.