"friendships" between new mothers and adult males: Adaptive benefits and determinants in wild baboons (Papio cynocephalus)

Behavioral Ecology and Sociobiology

Volumn 63, Issue 9, 2009, Pages 1331-1344

  Nguyen, Nga ^a,b,c   Van Horn, Russell C ^d   Alberts, Susan C ^e,f   Altmann, Jeanne ^f,g,h  

^a Cleveland Metroparks Zoo ^*  (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

^d ZOOLOGICAL SOCIETY OF SAN DIEGO   (United States)

^e DUKE UNIVERSITY   (United States)

^f INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^g PRINCETON UNIVERSITY   (United States)

^h UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

Infant harassment; Male female associations; Mating effort; Parental care

Indexed keywords

FEMALE BEHAVIOR; FERTILITY; INTERSEXUAL INTERACTION; LACTATION; MALE BEHAVIOR; MONOGAMY; PARENTAL CARE; PRIMATE;

AFRICA; AMBOSELI NATIONAL PARK; EAST AFRICA; KENYA; RIFT VALLEY; SUB-SAHARAN AFRICA;

MAMMALIA; PAPIO; PAPIO CYNOCEPHALUS; PRIMATES;

EID: 67650438899     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-009-0786-6     Document Type: Article

References (113)

1. SC Alberts 1999 Paternal kin discrimination in wild baboons Proc R Soc Lond B Biol Sci 266 1501 1506
2. SC Alberts J Altmann 1995 Preparation and activation-determinants of age at reproductive maturity in male baboons Behav Ecol Sociobiol 36 397 406 (Pubitemid 26448298)
3. Alberts SC, Altmann J (2003) Matrix models for primate life history analysis. In: Kappeler P, Pereira ME (eds) Primate life history and socioecology. University of Chicago Press, Chicago, pp 66-102
4. SC Alberts JC Buchan J Altmann 2006 Sexual selection in wild baboons: from mating opportunities to paternity success Anim Behav 72 1177 1196 (Pubitemid 44634363)
5. SC Alberts RM Sapolsky J Altmann 1992 Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group Horm Behav 26 167 178
6. SC Alberts HE Watts J Altmann 2003 Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus Anim Behav 65 821 840 (Pubitemid 36453601)
7. J Altmann 1974 Observational study of behavior: sampling methods Behaviour 49 227 267
8. Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge
9. Altmann J, Alberts SC (2003) Intraspecific variability in fertility and offspring survival in a nonhuman primate: behavioral control of ecological and social sources. In: Wachter KW, Bulatao RA (eds) Offspring: the biodemography of fertility and family behavior. National Academy Press, Washington, DC, pp 140-169
10. Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, Chicago
11. CM Anderson 1983 Levels of social organization and male female bonding in the genus Papio Am J Phys Anthropol 60 15 22 (Pubitemid 13155270)
12. DP Armstrong 1991 Aggressive of breeding territorial honeyeaters corresponds to seasonal changes in nectar availability Behav Ecol Sociobiol 29 103 111
13. Aureli F, de Waal FBM (2000) Why natural conflict resolution? In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 3-10
14. KB Bales 1980 Cumulative scaling of paternalistic behavior in primates Am Nat 116 454 461
15. L Barrett SP Henzi T Weingrill JE Lycett RA Hill 1999 Market forces predict grooming reciprocity in female baboons Proc R Soc Lond B Biol Sci 266 665 670 (Pubitemid 29161041)
16. JC Beehner TJ Bergman DL Cheney RM Seyfarth PL Whitten 2005 The effect of new alpha males on female stress in free-ranging baboons Anim Behav 69 1211 1221 (Pubitemid 40588798)
17. FB Bercovitch 1987 Reproductive success in male savanna baboons Behav Ecol Sociobiol 21 163 72
18. FB Bercovitch 1991 Mate selection, consortship formation, and reproductive tactics in adult female savanna baboons Primates 32 437 452
19. L Berenstain TD Wade 1983 Intrasexual selection and male mating strategies in baboons and macaques Int J Primatol 4 201 235
20. Blumstein DT (2000) The evolution of infanticide in rodents: A comparative analysis. In: van Schaik CP, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 178-197
21. C Borries K Launhardt C Epplen JT Epplen P Winkler 1999 DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys Proc R Soc Lond B Biol Sci 266 901 904 (Pubitemid 29237681)
22. C Borries K Launhardt C Epplen JT Epplen P Winkler 1999 Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups - defence pattern, paternity and sexual behaviour Behav Ecol Sociobiol 46 350 356 (Pubitemid 129748806)
23. JC Buchan SC Alberts JB Silk J Altmann 2003 True paternal care in a multi-male primate society Nature 425 179 181 (Pubitemid 37150895)
24. JB Bulger 1993 Dominance rank and access to estrous females in male savanna baboons Behaviour 127 67 103 (Pubitemid 24416857)
25. Buss DM (1994) The evolution of desire. Harper Collins, New York
26. B Chapais 1983 Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys Behav Ecol Sociobiol 12 215 228
27. Chapais B (1983b) Structure of the birth season relationship among adult male and female rhesus monkeys. In: Hinde RA (ed) Primate social relationships. Blackwell Scientific, Oxford, pp 200-208
28. Chapais B (1986a) Why do adult male and female rhesus monkeys affiliate during the birth season? In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior, and biology. State University of New York Press, Albany, pp 173-200
29. Chapais B (1986b) Why do adult male and female rhesus monkeys affiliate during the birth season? In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, pp 173-200
30. MJE Charpentier RC Van Horn J Altmann SC Alberts 2008 Paternal effects on offspring fitness in a multimale primate society Proc Natl Acad Sci U S A 105 1988 1992
31. DL Cheney RM Seyfarth J Fischer J Beehner T Bergman SE Johnson DM Kitchen RA Palombit D Rendall JB Silk 2004 Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana Int J Primatol 25 401 428 (Pubitemid 38498013)
32. HC Chuang-Dobbs MS Webster RT Holmes 2001 Paternity and parental care in the black-throated blue warbler, Dendroica caerulescens Anim Behav 62 83 92 (Pubitemid 32731616)
33. TH Clutton-Brock 1989 Mammalian mating systems Proc R Soc Lond B Biol Sci 236 339 372
34. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
35. A Dixon D Ross SLC Omalley T Burke 1994 Paternal investment inversely related to degree of extra pair paternity in the reed bunting Nature 371 698 700 (Pubitemid 24327327)
36. LC Drickamer PA Gowaty CM Holmes 2000 Free female mate choice in house mice affects reproductive success and offspring viability and performance Anim Behav 59 371 378 (Pubitemid 30656494)
37. RIM Dunbar 1991 Functional significance of social grooming in primates Folia Primatol 57 121 131
38. Estes RD (1992) The behavior guide to african mammals: including hoofed mammals, carnivores. University of California Press, Berkeley, Primates
39. Eggert AK, Muller JK (1997) Biparental care and social evolution in burying beetles: lessons from the larder. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 216-236
40. CR Freeman-Gallant 1997 Parentage and paternal care: consequences of intersexual selection in Savannah sparrows? Behav Ecol Sociobiol 40 395 400 (Pubitemid 27275091)
41. Gerald CN (1995) Demography of the Virunga mountain gorilla (Gorilla gorilla beringei). MSc thesis. Princeton University, Princeton
42. DF Gori S Rohwer J Caselle 1996 Accepting unrelated broods helps replacement male yellow-headed blackbirds attract mates Behav Ecol 7 49 54
43. Gubernick DJ (1994) Biparental care and male-female relations in mammals. In: Parmigiani S, von Saal FS (eds) Infanticide and parental care. Harwood, Chur, Switzerland, pp 427-463
44. AH Harcourt 1979 Social relationships between adult male and female mountain gorillas in the wild Anim Behav 27 325 342
45. Hausfater G (1975) Dominance and reproduction in baboons (Papio cynocephalus). Karger, Basel
46. G Hausfater J Altmann S Altmann 1982 Long-term consistency of dominance relations among female baboons (Papio cynocephalus) Science 217 752 755 (Pubitemid 12049582)
47. Hausfater G, Hrdy SB (1984) Infanticide: comparative and evolutionary perspectives. Aldine de Gruyter, New York
48. AG Hendrickx DC Kraemer 1969 Observations on the menstrual cycle, optimal mating time and pre-implantation embryos in the baboon, Papio anubis and Papio cynocephalus J Reprod Fertil Supp 6 119 128
49. DA Hill 1990 Social relationships between adult male and female rhesus macaques.2. Nonsexual affiliative behavior Primates 31 33 50
50. K Hill C Boesch J Goodall A Pusey J Williams R Wrangham 2001 Mortality rates among wild chimpanzees J Hum Evol 40 437 450 (Pubitemid 32511857)
51. M Hiraiwa 1981 Maternal and alloparental care in a troop of free-ranging Japanese monkeys Primates 22 309 329
52. SB Hrdy 1979 Infanticide among animals - Review, classification, and examination of the implications for the reproductive strategies of females Ethol Sociobiol 1 13 40
53. AC Keddy-Hector RM Seyfarth MJ Raleigh 1989 Male parental care, female choice and the effect of an audience in vervet monkeys Anim Behav 38 262 271 (Pubitemid 20419963)
54. EB Keverne ND Martensz B Tuite 1989 Beta endorphin concentrations in cerebrospinal-fluid of monkeys are influenced by grooming relationships Psychoneuroendocrinology 14 155 161 (Pubitemid 19110840)
55. Kingdon J (2003) The Kingdon field guide to african mammals. Black, London
56. Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Gubernick DJ, Klopfer PH (eds) Parental care in mammals. Plenum, New York, pp 347-387
57. S Kleindorfer SK Wasser 2004 Infant handling and mortality in yellow baboons (Papio cynocephalus): evidence for female reproductive competition? Behav Ecol Sociobiol 56 328 337 (Pubitemid 39098597)
58. Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, London
59. A Lemasson RA Palombit R Jubin 2008 Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments Behav Ecol Sociobiol 62 1027 1035
60. D Maestripieri 2000 Determinants of affiliative interactions between adult males and lactating females in pigtail macaques (Macaca nemestrina nemestrina) Ethology 106 425 439 (Pubitemid 30329599)
61. JH Manson 1994 Mating patterns, mate choice, and birth season heterosexual relationships in free-ranging rhesus macaques Primates 35 417 433
62. TC Marshall J Slate LEB Kruuk JM Pemberton 1998 Statistical confidence for likelihood-based paternity inference in natural populations Mol Ecol 7 639 655 (Pubitemid 28235973)
63. JH Mason 1994 Mating patterns, mate choice, and birth season heterosexual relationships in free-ranging rhesus macaques Primates 35 417 433
64. N Menard F von Segesser W Scheffrahn J Pastorini D Vallet B Gaci RD Martin A Gautier-Hion 2001 Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? C R Acad Sci SeÂr 3 Sci Vie 324 601 610 (Pubitemid 32605742)
65. AP Moller TR Birkhead 1993 Certainty of paternity covaries with paternal care in birds Behav Ecol Sociobiol 33 261 268 (Pubitemid 24411860)
66. Morris D (1967) The naked ape. Cape, London
67. Nicolson NA (1987) Infants, mothers, and other females. In: Smuts B, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Unversity of Chicago Press, Chicago, pp 330-342
68. R Noe AA Sluijter 1990 Reproductive tactics of male savanna baboons Behaviour 113 117 170
69. DJ Overdorff 1998 Are Eulemur species pair-bonded? Social organization and mating strategies in Eulemur fulvus rufus from 1988-1995 in southeast Madagascar Am J Phys Anthropol 105 153 166 (Pubitemid 28110398)
70. Palombit RA (2000) Infanticide and the evolution of male-female bonds in animals. In: van Schaik CP, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 239-268
71. RA Palombit RM Seyfarth DL Cheney 1997 The adaptive value of 'friendships' to female baboons: experimental and observational evidence Anim Behav 54 599 614 (Pubitemid 27413941)
72. Parmigiani S, Palanza P, Mainardi D, Brain PF (1994) Infanticide and protection of young in house mice (Mus domesticus): female and male strategies. In: Parmigiani S, von Saal FS (eds) Infanticide and parental care. Harwood, Chur, Switzerland, pp 341-363
73. A Paul 1999 The socioecology of infant handling in primates: is the current model convincing? Primates 40 33 46 (Pubitemid 29303346)
74. A Paul J Kuester J Arnemann 1996 The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus Anim Behav 51 155 170
75. EC Price 1990 Infant carrying as a courtship strategy of breeding male cotton-top tamarins Anim Behav 40 784 786
76. Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts B, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 250-266
77. Pusey AE, Packer C (1994) Infanticide in lions: consequences and counterstrategies. In: Parmigiani S, von Saal FS (eds) Infanticide and parental care. Harwood, London, pp 277-299
78. TW Ransom BS Ransom 1971 Adult male-infant relations among baboons (Papio anubis) Folia Primatol 16 179 195
79. O Rios-Cardenas AS Webster 2005 Paternity and paternal effort in the pumpkinseed sunfish Behav Ecol 16 914 921 (Pubitemid 41191531)
80. TE Rowell DK Olson 1983 Alternative mechanisms of social organization in monkeys Behaviour 86 31 54
81. M Sandvik G Rosenqvist A Berglund 2000 Male and female mate choice affects offspring quality in a sex-role-reversed pipefish Proc R Soc Lond B Biol Sci 267 2151 2155 (Pubitemid 30846429)
82. Sapolsky RM (1993) Neuroendocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D (eds) Behav Endocrinol. MIT Press, Cambridge, pp 287-324
83. RM Seyfarth 1978 Social relationships among adult male and female baboons. I. Behaviour during sexual consortship Behaviour 64 204 226
84. RM Seyfarth 1978 Social relationships among adult male and female baboons. II. Behavior throughout the female reproductive cycle. Behaviour 64 227 247
85. Seyfarth RM (1983) Grooming and social competition in primates. In: Hinde RA (ed) Primate Social relationships: an integrated approach. Blackwell, London, pp 182-189
86. AA Shaikh CL Celaya I Gomez SA Shaikh 1982 Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon Primates 23 444 452
87. JM Shopland J Altmann 1987 Fatal intragroup kidnapping in yellow baboons Am J Primatol 13 61 65
88. P Sicotte 1994 Effect of male competition on male female relationships in bi male groups of mountain gorillas Ethology 97 47 64
89. JB Silk 1980 Kidnapping and female competition in captive bonnet macaques Primates 21 100 110
90. JB Silk 1999 Why are infants so attractive to others? The form and function of infant handling in bonnet macaques Anim Behav 57 1021 1032 (Pubitemid 29228689)
91. K Smith SC Alberts J Altmann 2003 Wild female baboons bias their social behaviour towards paternal half-sisters Proc R Soc Lond B Biol Sci 270 503 510 (Pubitemid 36308227)
92. Smuts B (1985) Sex and friendship in baboons. Cambridge University Press, Cambridge
93. Smuts B, Gubernick DJ (1992) Male-infant relationships in nonhuman primates: paternal investment or mating effort? In: Hewlett BS (ed) Father-child relations. Aldine de Guyter, New York, pp 1-30
94. J Soltis R Thomsen K Matsubayashi O Takenaka 2000 Infanticide by resident males and female counter-strategies in wild Japanese macaques (Macaca fuscata) Behav Ecol Sociobiol 48 195 202 (Pubitemid 30686452)
95. Y Takahata 1982 Social relations between adult males and females of Japanese monkeys in the Arashiyama B troop Primates 23 1 23
96. I Tanaka H Takefushi 1993 Elimination of external parasites (lice) is the primary function of grooming in free-ranging japanese macaques Anthropol Sci 101 187 193
97. Taub DM (1990) The functions of primate paternalism: a cross-species review. In: Feierman JR (ed) Pedophilia: biosocial dimensions. Springer, New York, pp 338-377
98. Taub DM, Mehlman PT (1991) Primate paternalistic investment: a cross-species view. In: Loy JD, Peters CB (eds) Understanding behavior: what primate studies tell us about human behavior. Oxford, New York, pp 51-89
99. RC Van Horn SA Wahaj KE Holekamp 2004 Role-reversed nepotism among cubs and sires in the spotted hyena (Crocuta crocuta) Ethology 110 413 426 (Pubitemid 38700198)
100. van Schaik CP (2000) Infanticide by male primates: The sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27-60
101. van Schaik CP, Janson CH (2000) Infanticide by males and its implications. Cambridge University Press, Cambridge
102. CP van Schaik PM Kappeler 1997 Infanticide risk and the evolution of male-female association in primates Proc R Soc Lond B Biolog Sci 264 1687 1694 (Pubitemid 27504150)
103. CP van Schaik A Paul 1996 Male care in primates: does it ever reflect paternity? Evol Anthropol 5 152 156
104. SK Wasser DP Barash 1981 The selfish allomother-a comment Ethol Sociobiol 2 91 93
105. Watts DP (1996) Comparative socio-ecology of gorillas. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 16-28
106. PJ Weatherhead R Montgomerie HL Gibbs PT Boag 1994 The cost of extra-pair fertilizations to female red-winged blackbirds Proc R Soc Lond B Biol Sci 258 315 320
107. A Widdig P Nurnberg M Krawczak WJ Streich FB Bercovitch 2001 Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques Proc Natl Acad Sci U S A 98 13769 13773 (Pubitemid 33115973)
108. DE Wildt LL Doyle SC Stone RM Harrison 1977 Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle Primates 18 261 270
109. Wilson EO (1975) Sociobiology. Belknap, Cambridge
110. JF Wittenberger RL Tilson 1980 The evolution of monogamy-hypotheses and evidence Annu Rev Ecol Syst 11 197 232
111. JO Wolff DM Cicirello 1991 Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae) Behav Ecol 2 38 45
112. BBM Wong 2004 Superior fighters make mediocre fathers in the Pacific blue-eye fish Anim Behav 67 583 590 (Pubitemid 38319289)
113. PC Wright 1995 Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar Int J Primatol 16 835 854 (Pubitemid 3018060)