Dominance rank reversals and rank instability among male lemur catta: The effects of female behavior and ejaculation

American Journal of Physical Anthropology

Volumn 138, Issue 3, 2009, Pages 293-305

  Parga, Joyce A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Female mate choice; Male male competition; Proceptivity; Ring tailed lemur; Sexual behavior

Indexed keywords

ANIMALS; BREEDING; CONSERVATION OF NATURAL RESOURCES; EJACULATION; FEMALE; GEORGIA; LEMUR; MALE; REPRODUCTION; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

EID: 61449095620     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.20927     Document Type: Article

References (115)

1. Alberts SC, Buchan JC, Altmann J. 2006. Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177-1196.
2. Alberts SC, Sapolsky RM, Altmann J. 1992. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav 26:167-178.
3. Alberts SC, Watts HE, Altmann J. 2003. Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821-840.
4. Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49:227-267.
5. Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacey RC, Bruford MW. 1996. Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93:5797-5801.
6. Altmann SA. 1962. A field study of the sociobiology of the rhesus monkey, Macaca mulatta. Ann NY Acad Sci 102:338-435.
7. Andelman SJ. 1987. Evolution of concealed ovulation in vervet monkeys (Cercopithecus aethiops). Am Nat 129:785-799.
8. Andersson MB. 1994. Sexual selection. Princeton: Princeton University Press.
9. Beach FA. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105-138.
10. Berard J. 1999. A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta). Primates 40:159-175.
11. Bercovitch FB. 1988. Coalitions, cooperation and reproductive tactics among adult male baboons. Anim Behav 36:1198-1209.
12. Bernstein IS. 1976. Dominance, aggression and reproduction in primate societies. J Theor Biol 60:459-472.
13. Bernstein IS. 1981. Dominance: the baby and the bathwater. Behav Brain Sci 4:419-457.
14. Bernstein IS. 2007. Social mechanisms in the control of primate aggression. In: Campbell CJ, Fuentes A, MacKinnon KC, Pan-ger M, Bearder SK, editors. Primates in perspective. New York: Oxford University Press. p 562-571.
15. Brockman DK. 1999. Reproductive behavior of female Propithe-cus verreauxi at Beza Mahafaly, Madagascar. Int J Primatol 20:375-398.
16. Budnitz N, Dainis K. 1975. Lemur catta: ecology and behavior. In: Tattersall I, Sussman RW, editors. Lemur biology. New York: Plenum. p 219-235.
17. Bulger JB. 1993. Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67-103.
18. Bulger JB, Hamilton WJ III. 1988. Inbreeding and reproductive success in a natural chacma baboon, Papio cynocephalus ursi-nus, population. Anim Behav 36:574-578.
19. Cavigelli SA. 1999. Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim Behav 57:935-944.
20. Cavigelli SA, Pereira ME. 2000. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm Behav 37:246-255.
21. Chapais B. 1983. Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12:215-228.
22. Clutton-Brock TH, Harvey PH. 1976. Evolutionary rules and primate societies. In: Bateson PPG, Hinde RA, editors. Growing points in ethology. Cambridge: Cambridge University Press. p 195-237.
23. Colquhoun IC. 1987. Dominance and "fall-fever": the reproductive behaviour of male brown lemurs (Lemur fulvus). Can Rev Phys Anthropol 6:10-19.
24. Cox CR, Le Boeuf BJ. 1977. Female incitation of male competition: a mechanism in sexual selection. Am Nat 111:317-335.
25. de Ruiter JR, Scheffrahn W, Trommelen GJJM, Uitterlinden AG, Martin RD, van Hooff JARAM. 1992. Male social rank and reproductive success in wild long-tailed macaques. In: Martin RD, Dixson AF, Wickings EJ, editors. Paternity in primates: genetic tests and theories-Implications of human DNA fingerprinting. Basel: Karger. p 175-191.
26. de Waal F. 1982. Chimpanzee politics: power and sex among apes. Baltimore: Johns Hopkins University Press.
27. de Waal FBM. 1989. Dominance 'style' and primate social organization. In: Standen V, Foley RA, editors. Comparative socioecology: the behavioural ecology of humans and other mammals. Oxford: Blackwell Scientific Publications. p 243-263.
28. Dhabhar FS, McEwen BS. 2007. Bi-directional effects of stress on immune function: possible explanations for salubrious as well as harmful effects. In: Ader R, editor. Psychoneuroimmu-nology, 4th ed. Burlington: Academic Press. p 723-760.
29. Dierenfeld ES, McCann CM. 1999. Nutrient composition of selected plant species consumed by semi free-ranging lion-tailed macaques (Macaca silenus) and ringtailed lemurs (Lemur catta) on St. Catherines Island, Georgia, USA. Zoo Biol 18:481-494.
30. Dixson AF. 1998. Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press.
31. Evans CS, Goy RW. 1968. Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J Zool 156:181-197.
32. Gachot-Neveu H, Petit M, Roeder JJ. 1999. Paternity determination in two groups of Eulemur fulvus mayottensis: implications for understanding mating strategies. Int J Primatol 20:107-119.
33. Goodall J. 1986. The chimpanzees of Gombe. Cambridge: Harvard University Press.
34. Gould L. 1994. Patterns of affiliative behavior in adult male ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar, Ph.D. dissertation. St. Louis: Washington University.
35. Gould L. 1996. Male-female affiliative relationships in naturally occurring ringtailed lemurs (Lemur catta) at the Beza-Maha-faly Reserve, Madagascar. Am J Primatol 39:63-78.
36. Gould L. 1997. Intermale affiliative behavior in ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar. Primates 38:15-30.
37. Gould L. 2006. Male sociality and integration during the dispersal process in Lemur catta: a case study. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H, editors. Ringtailed lemur biology: Lemur catta in Madagascar. New York: Springer. p 296-310.
38. Gould L, Ziegler TE. 2007. 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 69:1325-1339.
39. Gould L, Ziegler TE, Wittwer DJ. 2005. 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 67:5-23.
40. Hauser MD. 1990. Do chimpanzee copulatory calls incite male-male competition? Anim Behav 39:596-597.
41. Hausfater G. 1975. Dominance and reproduction in baboons (Papio cynocephalus). Contrib Primatol 7:1-150.
42. Henzi P, Barrett L. 2003. Evolutionary ecology, sexual conflict, and behavioral differentiation among baboon populations. Evol Anthropol 12:217-230.
43. Huffman MA. 1987. Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology 75:221-234.
44. Huffman MA. 1992. Influences of female partner preference on potential reproductive outcome in Japanese macaques. Folia Primatol 59:77-88.
45. Hungerford H, Taylor L, Lessnau R. 2001. Troop fission among free-ranging ring-tailed lemurs (Lemur catta) on St. Catherines Island. Am J Primatol 54 (Suppl 1):100-101.
46. Janson CH. 1984. Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). Z Tierpsychol 65:177-200.
47. Jolly A. 1966. Lemur behavior. Chicago: University of Chicago Press.
48. Jolly A. 1967. Breeding synchrony in wild Lemur catta. In: Alt-mann SA, editor. Social communication among primates. Chicago: The University of Chicago. p 3-14.
49. Kappeler PM. 1990. Female dominance in Lemur catta: more than just female feeding priority? Folia Primatol 55:92-95.
50. Kappeler PM, Port M. 2008. Mutual tolerance or reproductive competition? Patterns of reproductive skew among male red-fronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 62:1477-1488.
51. Kappeler PM, Schaffler L. 2008. The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propi-thecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol 62:1007-1015.
52. Keith-Lucas T, White FJ, Keith-Lucas L, Vick LG. 1999. Changes in behavior in free-ranging Lemur catta following release in a natural habitat. Am J Primatol 47:15-28.
53. Koyama N. 1988. Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty, Madagascar. Primates 29:163-175.
54. Lawler RR. 2007. Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989 to 1999. Am J Phys Anthropol 132:267-277.
55. Lawler RR, Richard AF, Riley MA. 2005. Intrasexual selection in Verreaux's sifaka (Propithecus verreauxi verreauxi). J Hum Evol 48:259-277.
56. Lewis RJ. 2002. Beyond dominance: the importance of leverage. Q Rev Biol 77:149-164.
57. Lewis RJ, van Schaik CP. 2007. Bimorphism in male Verreaux's sifaka in the Kirindy forest of Madagascar. Int J Primatol 28:159-182.
58. Lynch Alfaro JW. 2005. Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus). Am J Primatol 67:313-328.
59. Maestripieri D, Leoni M, Raza SS, Hirsch EJ, Whitham JC. 2005. Female copulation calls in guinea baboons: evidence for postcopulatory female choice? Int J Primatol 26:737-758.
60. Manson JH. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44:405-416.
61. Manson JH. 1994. Male aggression: a cost of female mate choice in Cayo Santiago rhesus macaques. Anim Behav 48:473-475.
62. Martin RD. 1992. Female cycles in relation to paternity in primate societies. In: Martin RD, Dixson AF, Wickings EJ, editors. Paternity in primates: genetic tests and theories-implications of human DNA fingerprinting. Basel: Karger. p 238-274.
63. Nakamichi M, Koyama N. 1997. Social relationships among ring-tailed lemurs (Lemur catta) in two free-ranging troops at Berenty Reserve, Madagascar. Int J Primatol 18:73-93.
64. Nishida T, Hosaka K. 1996. Coalition strategies among adult male chimpanzees of the Mahale Mountains, Tanzania. In: McGrew WC, Marchant LF, Nishida T, editors. Great ape societies. Cambridge: Cambridge University Press. p 114-134.
65. Noe R. 1992. Alliance formation among male baboons: shopping for profitable partners. In: Harcourt AH, de Waal FBM, editors. Coalitions and alliances in humans and other animals. Oxford: Oxford University Press. p 285-321.
66. Noe R, Sluijter AA. 1990. Reproductive tactics of male savanna baboons. Behaviour 113:117-170.
67. Ostner J, Kappeler PM. 1999. Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)? Anim Behav 58:1069-1078.
68. Ostner J, Kappeler PM, Heistermann M. 2002. Seasonal variation and social correlates of androgen excretion in male red-fronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 54:485-495.
69. Overdorff DJ. 1998. Are Eulemur species pair-bonded? Social organization and mating strategies in Eulemur fulvus rufus from 1988 to 1995 in Southeast Madagascar. Am J Phys Anthropol 105:153-166.
70. Packer C. 1977. Reciprocal altruism in Papio anubis. Nature 265:441-443.
71. Packer C. 1979. Male dominance and reproductive activity in Papio anubis. Anim Behav 27:37-45.
72. Parga JA. 2003. Copulatory plug displacement evidences sperm competition in Lemur catta. Int J Primatol 24:889-899.
73. Parga JA. 2006a. Male mate choice in Lemur catta. Int J Primatol 27:107-131.
74. Parga JA. 2006b. Sexual selection in the ring-tailed lemur (Lemur catta): female choice, male mating strategies, and male mating success in a female dominant primate, Ph.D. dissertation. Austin: University of Texas-Austin.
75. Parga JA, Lessnau RG. 2005. Female age-specific reproductive rates, birth seasonality, and infant mortality of ring-tailed lemurs on St. Catherines Island: 17-year reproductive history of a free-ranging colony. Zoo Biol 24:295-309.
76. Parga JA, Lessnau RG. 2008. Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Island. Am J Primatol 70:650-66 0.
77. Parga JA, Maga M, Overdorff DJ. 2006. High-resolution X-ray computed tomography scanning of primate copulatory plugs. Am J Phys Anthropol 129:567-576.
78. Parker GA. 1974. Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223-243.
79. Pereira ME, Kappeler PM. 1997. Divergent systems of agonistic behaviour in lemurid primates. Behaviour 134:225-274.
80. Pereira ME, Kaufman R, Kappeler PM, Overdorff DJ. 1990. Female dominance does not characterize all of the lemuridae. Folia Primatol 55:96-103.
81. Pereira ME, McGlynn CA. 1997. Special relationships instead of female dominance for redfronted lemurs, Eulemur fulvus rufus. Am J Primatol 43:239-258.
82. Pereira ME, Weiss ML. 1991. Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behav Ecol Sociobiol 28:141-152.
83. Perry S. 1998. A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus). Primates 39:51-70.
84. Petter JJ, Charles-Dominique P. 1979. Vocal communication in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 247-305.
85. Popp JL, DeVore I. 1979. Aggressive competition and social dominance theory. In: Hamburg DA, McCown ER, editors. Perspectives on human evolution, Vol. 5: Behavior of great apes. Menlo Park: Benjamin/Cummings. p 316-338.
86. Pride RE. 2005a. Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behav Ecol 16:550-560.
87. Pride RE. 2005b. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol Lett 1:60-63.
88. Raleigh MJ, McGuire MT. 1989. Female influence on male dominance acquisition in captive vervet monkeys, Ceropithecus aethiops sabaeus. Anim Behav 38:59-67.
89. Rasmussen DT. 1985. A comparative study of breeding seasonal-ity and litter size in eleven taxa of captive lemurs (Lemur and Varecia). Int J Primatol 6:501-517.
90. Richard A. 1974. Patterns of mating in Propithecus verreauxi verreauxi. In: Martin RD, Doyle GA, Walker AC, editors. Pro-simian biology. London: Duckworth. p 49-74.
91. Richard AF. 1992. Aggressive competition between males,emale-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J Hum Evol 22: 395-406.
92. Rowell TE. 1974. The concept of social dominance. Behav Biol 11:131-154.
93. Sapolsky RM. 1983. Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 5:365-379.
94. Sapolsky RM. 2004. Social status and health in humans and other animals. Annu Rev Anthropol 33:393-418.
95. Sapolsky RM. 2005. The influence of social hierarchy on primate health. Science 308:648-652.
96. Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, sup-pressive, stimulatory, and preparative actions. Endocr Rev 21:55-89.
97. Sauther ML. 1991. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am J Phys Anthropol 84:463-477.
98. Sauther ML. 1992. The effects of reproductive state, social rank and roup size of resource use among free-ranging ringtailed lemurs (Lemur catta) of Madagascar, Ph.D. dissertation. St. Louis: Washington University.
99. Sauther ML, Sussman RW. 1993. A new interpretation of the social organization and mating system of the ringtailed lemur (Lemur catta). In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum. p 111-121.
100. Sauther ML, Sussman RW, Gould L. 1999. The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthropol 8:120-132.
101. Smuts BB. 1985. Sex and friendship in baboons. Hawthorne: Al-dine.
102. Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y, Domingo-Roura X, Takenaka O. 1997. Sexual selection in Japanese macaques. II. Female mate choice and male-male competition. Anim Behav 54:737-746.
103. Soltis J, Thomsen R, Takenaka O. 2001. The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62:485-494.
104. Strum SC. 1982. Agonistic dominance in male baboons: an alternative view. Int J Primatol 5:93-109.
105. Sussman RW. 1992. Male life history and intergroup mobility among ringtailed lemurs (Lemur catta). Int J Primatol 13:395-413.
106. Takahata Y. 1982. The socio-sexual behavior of Japanese monkeys. Z Tierpsychol 59:89-108.
107. Taylor LL. 1986. Kinship, dominance, and social organization in a semi-free ranging group of ringtailed lemurs (Lemur catta), Ph.D. dissertation. St. Louis: Washington University.
108. Taylor L, Sussman RW. 1985. A preliminary study of kinship and social organization in a semi-free-ranging group of Lemur catta. Int J Primatol 6:601-614.
109. Thomas DH, Jones GD, Durham RS, Larsen CS. 1978. The anthropology of St. Catherines Island, Part 1: Natural and cultural history. Anthropol Pap Am Mus Nat Hist 55:157-248.
110. Van Horn RN. 1975. Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatol 24:203-220.
111. Van Horn RN, Resko JA. 1977. The reproductive cycle of the ring-tailed lemur (Lemur catta), sex steroid levels and sexual receptivity under controlled photoperiods. Endocrinol 101: 1579-1586.
112. van Noordwijk MA. 1985. Sexual behavior of Sumatran long-tailed macaques (Macaca fascicularis). Z Tierpsychol 70:277-296.
113. van Noordwijk MA, van Schaik CP. 2004. Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates: new and comparative perspectives. Cambridge: Cambridge University Press. p 208-229.
114. Watts DP. 1998. Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43-55.
115. Weingrill T, Lycett JE, Henzi SP. 2000. Consortship and mating success in chacma baboons (Papio cynocephalus ursinus). Ethology 106:1033-1044.