Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra)

Hormones and Behavior

Volumn 56, Issue 4, 2009, Pages 355-363

  Belle, S Van ^a   Estrada, A ^b   Ziegler, T E ^c   Strier, K B ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Black howler monkey (Alouatta pigra); Fecal androgens; Fecal glucocorticoids; Indirect competition; Male immigration; Male female social relationships

Indexed keywords

ANDROGEN; GLUCOCORTICOID;

ALOUATTA; ALOUATTA PIGRA; ANIMAL EXPERIMENT; ARTICLE; COMPETITIVE BEHAVIOR; CONTROLLED STUDY; FECES ANALYSIS; FEMALE; GROUP DYNAMICS; HORMONAL REGULATION; MALE; MEXICO; MIGRATION; NONHUMAN; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION;

ALOUATTA; ANALYSIS OF VARIANCE; ANDROGENS; ANIMAL MIGRATION; ANIMALS; ANIMALS, WILD; COMPETITIVE BEHAVIOR; FECES; FEMALE; GLUCOCORTICOIDS; LINEAR MODELS; MALE; MENSTRUAL CYCLE; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SPATIAL BEHAVIOR;

EID: 70349753472     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.08.006     Document Type: Article

References (82)

1. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Mendoza S.P., Salzman W., Snowdon C.T., Ziegler T.E., Banjevic M., Garland T.J., and Sapolsky R.M. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 43 (2003) 67-82
2. Alberts S.C., Sapolsky R.M., and Altmann J. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm. Behav. 26 (1992) 167-178
3. Altmann J. Observational study of behavior: sampling methods. Behaviour 69 (1974) 227-267
4. Arlet M.E., Grote M.N., Molleman F., Isbell L.A., and Carey J.R. Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena). Horm. Behav. 55 (2009) 210-216
5. Arnold W., and Dittami J. Reproductive suppression in male alone marmots. Anim. Behav. 53 (1997) 53-66
6. Barrett G.M., Shimizu K., Bardi M., Asaba S., and Mori A. Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm. Behav. 42 (2002) 85-96
7. Beehner J.C., and Bergman T.J. The "bleeding-heart baboon": does chest patch color signal male quality in geladas?. Am. J. Phys. Anthropol. 48 (2009) 87
8. Beehner J.C., Bergman T.J., Cheney D.L., Seyfarth R.M., and Whitten P.L. Testosterone predicts future dominance rank and mating activity among male chacma baboons. Behav. Ecol. Sociobiol. 59 (2006) 469-479
9. Bercovitch F.B. The physiology of male reproductive strategies. In: Dolhinom P., and Fuentes A. (Eds). The Nonhuman Primates (1999), Mountain View, Mayfield, California 237-244
10. Bercovitch F.B., and Ziegler T.E. Current topics in primate socioendocrinology. Annu. Rev. Anthropol. 31 (2002) 45-67
11. Bergman T.J., Beehner J.C., Cheney D.L., Seyfarth R.M., and Whitten P.L. Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Anim. Behav. 70 (2005) 703-713
12. Booth A., Granger D.A., Mazur A., and Kivlighan K.T. Testosterone and social behavior. Soc. Forces 85 (2006) 167-191
13. Braude S., Tang-Martinez Z., and Taylor G. Stress, testosterone, and the immunoredistribution hypothesis. Behav. Ecol. 10 (1999) 345-350
14. Brockett R.C., Horwich R.H., and Jones C.B. Disappearance of infants following male takeovers in the Belizean black howler monkey (Alouatta pigra). Neotrop. Primates 7 (1999) 86-88
15. Brockman D.K., Whitten P.L., Richard A.F., and Schneider A. Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. Am. J. Phys. Anthropol. 105 (1998) 137-151
16. Brockman D.K., Whitten P.L., Richard A.F., and Benander B. Birth season testosterone levels in male Verreaux's sifaka, Propithecus verreauxi: insight into socio-demographic factors mediating seasonal testicular function. Behav. Ecol. Sociobiol. 49 (2001) 117-127
17. Carlson A.A., Young A.J., Russell A.F., Bennett N.C., McNeilly A.S., and Clutton-Brock T. Hormonal correlates of dominance in meerkats (Suricata suricatta). Horm. Behav. 46 (2004) 141-150
18. Cavigella S.A., and Pereira M.E. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37 (2000) 246-255
19. Creel S. Social dominance and stress hormones. Trends Ecol. Evol. 16 (2001) 491-497
20. Creel S., Creel N., Wildt D.E., and Monfort S.L. Behavioral and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. Anim. Behav. 43 (1992) 231-245
21. Creel S., Creel N.M., and Mills S.L. Social stress and dominance. Nature 379 (1996) 212
22. Creel S., Creel N.M., Mills M.G.L., and Monfort S.L. Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav. Ecol. 8 (1997) 298-306
23. Cristóbal-Azkarate J., Chavira R., Boeck L., Rodríguez-Luna E., and Veà J.J. Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis. Horm. Behav. 49 (2006) 261-267
24. Cristóbal-Azkarate J., Chavira R., Boeck L., Rodríguez-Luna E., and Veà J.J. Glucocorticoid levels in free ranging resident mantled howlers: a study of coping strategies. Am. J. Primatol. 69 (2007) 866-876
25. Crockett C.M. Re-evaluating the sexual selection hypothesis for infanticide by Alouatta males. In: Jones C.B. (Ed). Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. American Society of Primatology: Special Topics in Primatology 3 (2003), The American Society of Primatologists, Norman, Oklahoma 327-365
26. Díaz Gallegos, J.R., 1996. Estructura y composición florística de la vegetación del Parque Nacional Zona Arqueológica de Palenque, Chiapas, México. Bs. Thesis, Univ. Juárez Autónoma de Tabasco, Villahermosa, Tabasco, Mexico, 63 pp.
27. Dloniak S.M., French J.A., and Holekamp K.E. Faecal androgen concentrations in adult male spotted hyaenas, Crocuta crocuta, reflect interactions with socially dominant females. Anim. Behav. 71 (2006) 27-37
28. East M.L., and Hofer H. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav. Ecol. 12 (2001) 558-568
29. Estrada A., Castellanos L., Ibarra A., García del Valle Y., Muñoz D., Rivera A., Franco B., Fuentes E., and Jiménez C. Survey of the population of the black howler monkey, Alouatta pigra, at the Mayan site of Palenque, Chiapas, Mexico. Primates 44 (2002) 51-58
30. Fichtel C., Kraus C., Ganswindt A., and Heistermann M. Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm. Behav. 51 (2007) 640-648
31. Folstad I., and Karter A.J. Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139 (1992) 603-622
32. Ginther A.J., Ziegler T.E., and Snowdon C.T. Reproductive biology of captive male cotton-top tamarin monkeys as a function of social environment. Anim. Behav. 61 (2001) 65-78
33. Gould L., and Ziegler T.E. Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta). Am. J. Primatol. 69 (2007) 1-15
34. Gould L., Ziegler T.E., and Wittwer D.J. Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar. Am. J. Primatol. 67 (2005) 5-23
35. Goymann W., and Wingfield J.C. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 67 (2004) 591-602
36. Goymann W., East M.L., and Hofer H. Defense of females, but not social status, predicts plasma androgen levels in male spotted hyenas. Phys. Biochem. Zool. 76 (2003) 586-593
37. Goymann W., East M.L., Wachter B., Höner O.P., Möstl E., and Hofer H. Social status does not predict corticoid levels in male spotted hyenas. Horm. Behav. 43 (2003) 474-479
38. Grossman C.J., Roselle G.A., and Mendenhall C.L. Sex steroid regulation of autoimmunity. J. Steroid Biochem. Mol. Biol. 40 (1991) 649-659
39. Hau M. Regulation of male traits by testosterone: implications for the evolution of vertebrate life-histories. BioEssays 29 (2007) 133-144
40. Hill D.A. Social relationships between adult males and female rhesus macaques: II. Non-sexual affiliative behaviour. Primates 31 (1990) 33-50
41. Hinde R.A., and Atkinson S. Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. Anim. Behav. 18 (1970) 169-176
42. Hodges J.K., and Heistermann M. Field endocrinology: monitoring hormonal changes in free-ranging primates. In: Setchell J.M., and Curtis D.J. (Eds). Field and Laboratory Methods in Primatology. A Practical Guide (2003), Cambridge University Press, Cambridge 282-294
43. Horwich R.H. Breeding behaviors in the black howler monkey (Alouatta pigra) of Belize. Primates 24 (1983) 222-230
44. Horwich R.H., Brockett R.C., and Jones C.B. Alternative male reproductive behaviors in the Belizean black howler monkey (Alouatta pigra). Neotrop. Primates 8 (2000) 95-98
45. Huck M., Löttker P., Heymann E.W., and Heistermann M. Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguinus mystax. Int. J. Primatol. 26 (2005) 159-179
46. Koren L., Modady O., and Geffen E. Social status and cortisol levels in singing rock hyraxes. Horm. Behav. 54 (2008) 212-216
47. Lynch J.W., Ziegler T.E., and Strier K.B. Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm. Behav. 41 (2002) 275-287
48. Marler C.A., Walsberg G., White M.L., and Moore M. Increased energy expenditure due to increased territorial defense in male lizards after phenotypic manipulation. Behav. Ecol. Sociobiol. 37 (1995) 225-231
49. Martínez-Mota R., Valdespino C., Rivera Rebolledo A.R., and Palme R. Determination of fecal glucocorticoid metabolites to evaluate stress response in Alouatta pigra. Int. J. Primatol. 29 (2008) 1365-1373
50. Muehlenbein M.P., and Bribiescas R.G. Testosterone-mediated immune functions and male life histories. Am. J. Hum. Biol. 17 (2005) 527-558
51. Muehlenbein M.P., Watts D.P., and Whitten P.L. Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am. J. Primatol. 64 (2004) 71-82
52. Muller M.N., and Wrangham R.W. Dominance, aggression and testosterone in wild chimpanzees: a test of the "challenge hypothesis". Anim. Behav. 67 (2004) 113-123
53. Muller M.N., and Wrangham R.W. Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 55 (2004) 332-340
54. Neville M.K. Social relations within troops of red howler monkeys (Alouatta seniculus). Folia Primatol. 18 (1972) 47-77
55. Ostner J., Kappeler P.M., and Heistermann M. Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 52 (2002) 485-495
56. Ostner J., Kappeler P., and Heistermann M. Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 62 (2008) 627-638
57. Ostner J., Heistermann M., and Schülke O. Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm. Behav. 54 (2008) 613-619
58. Rasmussen H.B., Ganswindt A., Douglas-Hamilton I., and Vollrath F. Endocrine and behavioral changes in male African elephants: linking hormone changes to sexual state and reproductive tactics. Horm. Behav. 54 (2008) 539-548
59. Robbins M.M., and Czekala N.M. A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas. Am. J. Primatol. 43 (1997) 51-64
60. Sands J., and Creel S. Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav. 67 (2004) 387-396
61. Sapolsky R.M. The physiology of dominance in stable versus unstable social hierarchies. In: Mason W.A., and Mendoza S.P. (Eds). Primate Social Conflict (1993), State University of New York Press, Albany 171-204
62. Sapolsky R.M. Endocrinology of stress response. In: Becker J.B., Breedlove S.M., Crews D., and McCarthy M. (Eds). Behavioral Endocrinology. 2nd ed (2002), MIT Press, Cambridge 409-450
63. Sapolsky R.M. The influence of social hierarchy on primate health. Science 308 (2005) 648-652
64. Setchell J.M., Smith T., Wickings E.J., and Knapp L.A. Social correlates of testosterone and ornamentation in male mandrills. Horm. Behav. 54 (2008) 365-372
65. Sicotte P., and MacIntosh A.J. Inter-group encounters and male incursions in Colobus vellerosus in central Ghana. Behaviour 141 (2004) 533-553
66. Sousa M.B.C., and Ziegler T.E. Diurnal variation on the excretion patterns of fecal steroids in common marmosets (Callithrix jacchus) females. Am. J. Primatol. 46 (1998) 105-117
67. Strier K.B., and Ziegler T.E. Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am. J. Primatol. 42 (1997) 299-310
68. Strier K.B., Ziegler T.E., and Wittwer D.J. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm. Behav. 35 (1999) 125-134
69. Strier K.B., Lynch J.W., and Ziegler T.E. Hormonal changes during the mating and conception seasons of wild Northern muriquis (Brachyteles arachnoides hypoxanthus). Am. J. Primatol. 61 (2003) 85-99
70. Teichroeb J.A., and 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. 54 (2008) 417-423
71. Van Belle S., and Estrada A. Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A., Garber P.A., Pavelka M.S.M., and Leucke L.G. (Eds). New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation (2006), Springer Press, New York 121-142
72. Van Belle S., Estrada A., and Strier K.B. Social relationships among male Alouatta pigra. Int. J. Primatol. 29 (2008) 1481-1498
73. Van Belle S., Estrada A., Ziegler T.E., and Strier K.B. Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. Am. J. Primatol. 71 (2009) 153-164
74. Whitten P.L., Brockman D.K., and Stavisky R.C. Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yb. Phys. Anthropol. 41 (1998) 1-23
75. Wingfield J.C., Hegner R.E., Dufty A.M.J., and Ball G.F. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136 (1990) 829-846
76. Wingfield J.C., Jacobs J.D., Tramontin A.D., Perfito N., Meddle S., Meaney D.L., and Soma K. Toward and ecological basis of hormone-behavior interactions in reproduction of birds. In: Wallen K., and Schneider J. (Eds). Reproduction in Context-Social and Environmental Influences on Reproduction (2000), The MIT Press, Cambridge 85-128
77. Ziegler T.E., and Wittwer D.J. Fecal steroid research in the field and laboratory: improved methods for storage, transport, processing, and analysis. Am. J. Primatol. 67 (2005) 159-174
78. Ziegler T.E., Scheffler G., and Snowdon C.T. The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm. Behav. 29 (1995) 407-424
79. Ziegler T.E., Scheffler G., Wittwer D.J., Schultz-Darken N., Snowdon C.T., and Abbott D.H. Metabolism of reproductive steroids during the ovarian cycle in two species of callitrichids, Saguinus oedipus and Callithrix jacchus, and estimation of the ovulatory period from fecal steroids. Biol. Reprod. 54 (1996) 91-99
80. Ziegler T.E., Carlson A.A., Ginther A.J., and Snowdon C.T. Gonadal source of testosterone metabolites in urine of male cotton-top tamarin monkeys (Saguinus oedipus). Gen. Comp. Endocrinol. 118 (2000) 332-343
81. Ziegler T.E., Jacoris S., and Snowdon C.T. Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus), and its relationship to infant care. Am. J. Primatol. 64 (2004) 57-69
82. Ziegler T.E., Schultz-Darken N.J., Scott J.J., Snowdon C.T., and Ferris C.F. Neuroendocrine response to female ovulatory odors upon social condition in male common marmosets, Callithrix jacchus. Horm. Behav. 47 (2005) 56-64