When Dads Help: Male Behavioral Care During Primate Infant Development

  • Maren Huck
  • Eduardo Fernandez-Duque
Part of the Developments in Primatology: Progress and Prospects book series (DIPR, volume 37)


In contrast to birds, male mammals rarely help to raise the offspring. Of all mammals, only among rodents, carnivores, and primates, males are sometimes intensively engaged in providing infant care (Kleiman and Malcolm 1981). Male caretaking of infants has long been recognized in nonhuman primates (Itani 1959). Given that infant care behavior can have a positive effect on the infant’s development, growth, well-being, or survival, why are male mammals not more frequently involved in “building babies”? We begin the chapter defining a few relevant terms and introducing the theory and hypotheses that have historically addressed the evolution of paternal care. We then review empirical findings on male care among primate taxa, before focusing, in the final section, on our own work on paternal care in South American owl monkeys (Aotus spp.). We conclude the chapter with some suggestions for future studies.


Aotus Carrying Dispersal Development Male care Mating effort Night monkeys Owl monkeys Paternal care 



Thanks to all students, volunteers, and assistants who helped us to collect the data. We also thank Mr. F. Middleton, Manager of Estancia Guaycolec, and Alfredo Casaretto (Director of Bellamar Estancias) for the continued support of the Owl Monkey Project. All research presented here is approved by the Formosa Province Council of Veterinarian Doctors, the Directorate of Wildlife, the Subsecretary of Ecology and Natural Resources, and the Ministry of Production. At the national level, the procedures were approved by the National Wildlife Directorate in Argentina and by the IACUC committees of the Zoological Society of San Diego (2000–2005) and of the University of Pennsylvania (2006–2010). MH was funded by the Deutsche Forschungsgemeinschaft (HU 1746/2-1). EFD acknowledges the financial support from the Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), the University of Pennsylvania Research Foundation, and the Zoological Society of San Diego. We thank the editors Kathryn Clancy, Katie Hinde, and Julienne Rutherford for inviting us to contribute to this volume, and the editors and anonymous reviewers for their comments.


  1. Achenbach GG, Snowdon CT (2002) Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. International Journal of Primatology 23(1):179–189PubMedGoogle Scholar
  2. Allman J, Rosin A, Kumar R, Hasenstaub A (1998) Parenting and survival in anthropoid primates: caretakers live longer. Proc Natl Acad Sci USA 95:6866–6869PubMedGoogle Scholar
  3. Anderson CM (1992) Male investment under changing conditions among Chacma baboons at Suikerbosrand. Am J Phys Anthropol 87:479–496PubMedGoogle Scholar
  4. Anderson KG, Kaplan H, Lancaster J (1999) Paternal care by genetic fathers and stepfathers I: reports from Albuquerque men. Evol Hum Behav 20:405–431Google Scholar
  5. Austad SN, Rabenold KN (1986) Demography and the evolution of cooperative breeding in the bicolored wren, Campylorhynchus griseus. Behaviour 97:308–324Google Scholar
  6. Bales KL, O’Herron M, Baker AJ, Dietz JM (2001) Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 54(4):211–221PubMedGoogle Scholar
  7. Bales KL, Kim AJ, Lewis-Reese AD, Sue Carter C (2004) Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 45(5):354–361PubMedGoogle Scholar
  8. Bastian ML, Brockman DK (2007) Paternal care in Propithecus verreauxi coquereli. Int J Primatol 28(2):305–313Google Scholar
  9. Bateman AJ (1948) Intrasexual selection in Drosophila. Heredity 2:349–368PubMedGoogle Scholar
  10. Bercovitch FB (2002) Sex-biased parental investment in primates. Int J Primatol 23(4):905–921Google Scholar
  11. Birnie AK, Smith AS, Nali C, French JA (2011) Social and developmental influences on urinary androgen levels in young male white-faced marmosets (Callithrix geoffroyi). Am J Primatol 73:378–385PubMedGoogle Scholar
  12. Brockmann 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 49:117–127Google Scholar
  13. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181PubMedGoogle Scholar
  14. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008) Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci USA 105(6):1988–1992PubMedGoogle Scholar
  15. Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60PubMedGoogle Scholar
  16. Dawkins R, Carlisle TR (1976) Parental investment, mate desertion and a fallacy. Nature 262:131–133Google Scholar
  17. Dixson AF, Fleming D (1981) Parental behaviour and infant development in owl monkeys (Aotus trivirgatus griseimembra). J Zool Lond 194:25–39Google Scholar
  18. Dixson AF, Gardner JS, Bonney RC (1980) Puberty in the male owl monkeys (Aotus trivirgatus griseimembra): a study of physical and hormonal development. Int J Primatol 1(2):129–139Google Scholar
  19. Drea CM (2007) Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally ‘masculinized’? Horm Behav 51(4):555–567PubMedGoogle Scholar
  20. Dunbar RIM (1995) The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim Behav 50:1057–1070Google Scholar
  21. Erkert HG, Cramer B (2006) Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea). Folia Primatol 77:87–103PubMedGoogle Scholar
  22. Feistner ATC, Price EC (2000) Food sharing in black lion tamarins (Leontopithecus chrysophygus). Am J Primatol 52:47–54Google Scholar
  23. Fernandez-Duque E (2002) Environmental determinants of birth seasonality in night monkeys (Aotus azarai) of the Argentinian Chaco. Int J Primatol 23(3):639–656Google Scholar
  24. Fernandez-Duque E (2003) Influences of moonlight, ambient temperature, and food availability on the diurnal and nocturnal activity of owl monkeys (Aotus azarai). Behav Ecol Sociobiol 54:431–440Google Scholar
  25. Fernandez-Duque E (2007) Costs and benefits of paternal care in free-ranging owl monkeys (Aotus azarai). Am J Phys Anthropol Suppl 44:108Google Scholar
  26. Fernandez-Duque E. 2009. Natal dispersal in monogamous owl monkeys (Aotus azarai) of the Argentinean Chaco. Behaviour 146(4–5):583–606Google Scholar
  27. Fernandez-Duque E (2011a) Aotinae: social monogamy in the only nocturnal anthropoid. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf R (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 139–154Google Scholar
  28. Fernandez-Duque E (2011b) Rensch’s rule, Bergmann’s effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina. Am J Phys Anthropol 146(1):38–48PubMedGoogle Scholar
  29. Fernandez-Duque E, Juárez CP, Di Fiore A (2008) Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (Aotus azarai). Primates 49:81–84PubMedGoogle Scholar
  30. Fernandez-Duque E, Valeggia CR, Mendoza SP (2009) The biology of paternal care in human and nonhuman primates. Annu Rev Anthropol 38:115–130Google Scholar
  31. Fernandez-Duque E, de la Iglesia H, Erkert HG (2010) Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment. PLoS One 5(9):e12572PubMedGoogle Scholar
  32. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  33. Fite JE, Patera KJ, French JA, Rukstalis M, Hopkins EC, Ross CN (2005) Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can. J Hum Evol 49:122–142PubMedGoogle Scholar
  34. Fragaszy DM, Schwarz S, Shimosaka D (1982) Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch). Am J Primatol 2(2):191–200Google Scholar
  35. Fuentes A (2000) Hylobatid communities: changing views on pair bonding and social organization in hominoids. Yearbook Phys Anthropol 43:33–60Google Scholar
  36. Garber PA (1994) Phylogenetic approach to the study of tamarin and marmoset social systems. Am J Primatol 34:199–219Google Scholar
  37. Garber PA (1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive strategy. Evol Anthropol 6:187–199Google Scholar
  38. Geary DC (2000) Evolution and proximate expression of human paternal investment. Psychol Bull 126:55–77PubMedGoogle Scholar
  39. Geary DC (2005) Evolution of paternal investment. In: Buss DM (ed) The evolutionary psychology handbook. Wiley, Hoboken, pp 483–505Google Scholar
  40. Gettler LT (2010) Direct male care and hominin evolution: why male-child interaction is more than a nice social idea. Am Anthropol 112(1):7–21Google Scholar
  41. Gettler LT, McDade TW, Feranil AB, Kuzawa CW. 2011. Longitudinal evidence that fatherhood decreases testosterone in human males. Proceedings of the National Academy of Sciences USA 108(39):16194–16199Google Scholar
  42. Goldizen AW (1987a) Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis). Behav Ecol Sociobiol 20:99–109Google Scholar
  43. Goldizen AW (1987b) Tamarins and marmosets: communal care of offspring. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 34–43Google Scholar
  44. Goldizen AW (1990) A comparative perspective on the evolution of tamarin and marmoset social systems. Int J Primatol 11(1):63–83Google Scholar
  45. Goldizen A, Mendelson J, van Vlaardingen M, Terborgh J (1996) Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: evidence from a thirteen-year study of a marked population. Am J Primatol 38:57–83Google Scholar
  46. Goymann W, Landys MM, Wingfield JC (2007) Distinguishing seasonal androgen responses from male-male androgen responsiveness-revisiting the challenge hypothesis. Horm Behav 51:463–476PubMedGoogle Scholar
  47. Gozalo A, Montoya E (1990) Reproduction of the owl monkey (Aotus nancymai) (primates:Cebidae) in captivity. Am J Primatol 21(1):61–68Google Scholar
  48. Gray PB, Parkin JC, Samms-Vaughan ME (2007) Hormonal correlates of human paternal interactions: a hospital-based investigation in urban Jamaica. Horm Behav 52(4):499–507PubMedGoogle Scholar
  49. Gubernick DJ, Teferi T (2000) Adaptive significance of male parental care in a monogamous mammal. Proc R Soc Lond B 267(1439):147–150Google Scholar
  50. Gursky S (2000) Allocare in a nocturnal primate: data on the spectral tarsier, Tarsius spectrum. Folia Primatol 71(1–2):39–54PubMedGoogle Scholar
  51. Härdling R, Kaitala A (2004) Male brood care without paternity increases mating success. Behav Ecol 15(5):715–721Google Scholar
  52. Harris TR, Chapman CA, Monfort SL (2010) Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21(1):46–56Google Scholar
  53. Hewlett BS (1989) Multiple caretaking among African pygmies. Am Anthropol 91:186–191Google Scholar
  54. Hewlett BS (2004) Fathers in forager, farmer, and pastoral cultures. In: Lamb ME (ed) The role of the father in child development, 4th edn. Wiley, New York, pp 182–195Google Scholar
  55. Heymann EW (2000) The number of adult males in callitrichine groups and its implications for callitrichine social evolution. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 64–71Google Scholar
  56. Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277Google Scholar
  57. Hoage RJ (1977) Parental care in Leontopithecus rosalia rosalia: sex and age differences in carrying behavior and the role of prior experience. In: Kleiman DG (ed) The biology and conservation of the callitrichidae. Smithsonian Institution Press, Washington, pp 293–305Google Scholar
  58. Hoffman KA, Mendoza SP, Hennessy MB, Mason WA (1995) Responses of infant titi monkeys, Callicebus moloch, to removal of one or both parents: evidence for paternal attachment. Dev Psychobiol 28(7):399–407PubMedGoogle Scholar
  59. Houston AI, McNamara JM (2002) A self-consistent approach to paternity and parental effort. Phil Trans R Soc Lond B 357:351–362Google Scholar
  60. Houston AI, McNamara JM (2005) John Maynard Smith and the importance of consistency in evolutionary game theory. Biol Phil 20:933–950Google Scholar
  61. Houston AI, Székely T, McNamara JM (2005) Conflict between parents over care. Trends Ecol Evol 20(1):33–38PubMedGoogle Scholar
  62. Hrdy SB (2008) Cooperative breeding and the paradox of facultative fathering. In: Bridges R (ed) Neurobiology of the parental brain. Academic, New York, pp 407–416Google Scholar
  63. Huck M, Fernandez-Duque E (2012) Children of divorce: effects of adult replacements on previous offspring in Argentinean owl monkeys. Behav Ecol Sociobiol 66(3):505–517Google Scholar
  64. Huck M, Löttker P, Heymann EW (2004) The many faces of helping: possible costs and benefits of infant carrying and food transfer in moustached tamarins (Saguinus mystax). Behaviour 141:915–934Google Scholar
  65. Huck M, Löttker P, Heymann EW, Heistermann M (2005) Characterization and social correlates of fecal testosterone and cortisol levels in wild male moustached tamarins (Saguinus mystax). Int J Primatol 26(1):159–179Google Scholar
  66. Huck M, Rotundo M, Fernandez-Duque E (2011) Growth and development in wild owl monkeys (Aotus azarai) of Argentina. Int J Primatol 32(5):1133–1152Google Scholar
  67. Hurtado AM, Hill KR (1992) Paternal effect on offspring survivorship among Ache and Hiwi hunter-gatherers: implications for modeling pair-bond stability. In: Hewlett BS (ed) Father–child relations - cultural and biosocial Contexts. Aldine de Gruyter, New York, pp 31–55Google Scholar
  68. Itani J (1959) Paternal care in the wild Japanese monkey, Macaca fuscata fuscata. Primates 2:61–93Google Scholar
  69. Jantschke B, Welker C, Klaiber-Schuh A (1998) Rearing without paternal help in the Bolivian owl monkey Aotus azarae boliviensis: a case study. Folia Primatol 69:115–120Google Scholar
  70. Kappeler PM (1998) Nests, tree holes, and the evolution of primate life histories. Am J Primatol 46:7–33PubMedGoogle Scholar
  71. Kappeler PM (2012) Behavioral ecology of strepsirrhines and tarsiers. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J. The Evolution of Primate Societies. University of Chicago Press, Chicago (in press)Google Scholar
  72. Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23(4):707–740Google Scholar
  73. Keddy Hector AC, Seyfarth RM, Raleigh MJ (1989) Male parental care, female choice and the effect of an audience in vervet monkeys. Anim Behav 38:262–271Google Scholar
  74. Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79(4):757–768PubMedGoogle Scholar
  75. Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Gubernick DG, Klopfer PH (eds) Parental care in mammals. Plenum Press, New York, pp 347–387Google Scholar
  76. Kokko H, Jennions MD (2008) Parental investment, sexual selection and sex ratios. J Evol Biol 21(4):919–948PubMedGoogle Scholar
  77. Komers PE, Brotherton PNM (1997) Female space use is the best predictor of monogamy in mammals. Proc R Soc Lond B 264:1261–1270Google Scholar
  78. Kostan KM, Snowdon CT (2002) Attachment and social preferences in cooperatively-reared cotton-top tamarins. Am J Primatol 57:131–139PubMedGoogle Scholar
  79. Kramer KL (2010) Cooperative breeding and its significance to the demographic success of humans. Annu Rev Anthropol 39(1):417–436Google Scholar
  80. Lappan S (2008) Male care of infants in a siamang (Symphalangus syndactylus) population including socially monogamous and polyandrous groups. Behav Ecol Sociobiol 62:1307–1317Google Scholar
  81. Leutenegger W (1973) Maternal-fetal weight relationships in primates. Folia Primatol 20:280–293PubMedGoogle Scholar
  82. Löttker P, Huck M, Heymann EW (2004) Demographic parameters and events in wild moustached tamarins (Saguinus mystax). Am J Primatol 64:425–449PubMedGoogle Scholar
  83. Marlowe F (1999) Male care and mating effort among Hadza foragers. Behav Ecol Sociobiol 46:57–64Google Scholar
  84. Marlowe F (2000) Paternal investment and the human mating system. Behav Processes 51:45–61PubMedGoogle Scholar
  85. Martin JK, Handasyde KA, Taylor AC, Coulson G (2007) Long-term pair-bonds without mating fidelity in a mammal. Behaviour 144(11):1419–1445Google Scholar
  86. Maynard Smith S (1977) Parental investment: a prospective analysis. Anim Behav 25:1–9Google Scholar
  87. McGrew WC (1988) Parental division of infant caretaking varies with family composition in cotton-top tamarins. Anim Behav 36:285–310Google Scholar
  88. Mendoza SP, Mason WA (1986) Parental division of labour and differentiation of attachments in a monogamous primate (Callicebus moloch). Anim Behav 34:1336–1347Google Scholar
  89. Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40:213–220Google Scholar
  90. Mitani J, Merriwether DA, Zhang C (2000) Male affiliation, cooperation and kinship in wild chimpanzees. Anim Behav 59:885–893PubMedGoogle Scholar
  91. Morcillo A, Sánchez S, Fidalgo A, Gil-Bürman C, Peláez F (2003) Effects of enclosure size on weight loss after the birth of infants in cotton-top tamarins (Saguinus oedipus). Primate Report 66–1:32–33Google Scholar
  92. Moreno J, Veiga JP, Cordero PJ, Mínguez E (1999) Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor. Behav Ecol Sociobiol 47:47–53Google Scholar
  93. Morland HS (1990) Parental behavior and infant development in ruffed lemurs (Varecia variegata) in a northeast Madagascar rain forest. Am J Primatol 20(4):253–265Google Scholar
  94. Nekaris KAI (2003) Observations of mating, birthing and parental behaviour in three subspecies of slender loris (Loris tardigradus and Loris lydekkerianus) in India and Sri Lanka. Folia Primatol 74:312–336PubMedGoogle Scholar
  95. Nicolson N (1987) Infants, mothers and other females. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsacker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 330–342Google Scholar
  96. Nievergelt CM, Digby LJ, Ramkrishnan U, Woodruff DS (2000) Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. Int J Primatol 21(1):1–20Google Scholar
  97. Norconk MA (2007) Sakis, uakaris, and titi monkeys: behavioral diversity in a radiation of seed predators. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 123–138Google Scholar
  98. O’Brien TG, Robinson JG (1991) Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. Behaviour 119:30–50Google Scholar
  99. Palombit R, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614PubMedGoogle Scholar
  100. Parker GA, Baker RR, Smith VGF (1972) The origin and evolution of gamete dimorphism and the male–female phenomenon. J Theor Biol 36:529–553PubMedGoogle Scholar
  101. Patel ER (2007) Non-maternal infant care in wild silky sifakas (Propithecus candidus). Lemur News 12:39–42Google Scholar
  102. Paul A (1999) The socioecology of infant handling in primates: is the current model convincing? Primates 40(1):33–46Google Scholar
  103. Perry S (1998) Male–male social relationships in wild white-faced capuchins, Cebus capucinus. Behaviour 135(2):139–172Google Scholar
  104. Porter LM (2001) Social organization, reproduction and rearing strategies of Callimico goeldii: new clues from the wild. Folia Primatol 72(2):69–79PubMedGoogle Scholar
  105. Porter LM, Garber PA (2009) Social behavior of Callimicos: mating strategies and infant care. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids - the marmoset/callimico radiation. Springer, New York, pp 87–101Google Scholar
  106. Price EC (1990) Infant carrying as a courtship strategy of breeding male cotton-top tamarins. Anim Behav 40(4):784–786Google Scholar
  107. Price EC (1992a) The benefits of helpers: effects of group and litter size on infant care in tamarins (Saguinus oedipus). Am J Primatol 26:179–190Google Scholar
  108. Price EC (1992b) The costs of infant carrying in captive cotton-top tamarins. Am J Primatol 26:23–33Google Scholar
  109. Price EC, Feistner ATC (2001) Food sharing in pied bare-faced tamarins (Saguinus bicolor bicolor): Development and individual differences. Int J Primatol 22(2):231–241Google Scholar
  110. Pryce CR (1988) Individual and group effects on early caregiver-infant relationships in red-bellied tamarin monkeys. Anim Behav 36:1455–1464Google Scholar
  111. Rafacz ML, Margulis SUE, Santymire RM (2012) Hormonal correlates of paternal care differences in the Hylobatidae. Am J Primatol 74(3):247–260Google Scholar
  112. Reichard U, Barelli C 2008 Life history and reproductive strategies of Khao Yai Hylobates lar: implications for social evolution in apes. Int J Primatol 29(4):823–844Google Scholar
  113. Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113PubMedGoogle Scholar
  114. Rotundo M, Fernandez-Duque E, Dixon AF (2005) Infant development and parental care in free-ranging Aotus azarai azarai in Argentina. Int J Primatol 26(6):1459–1473Google Scholar
  115. Sánchez S, Peláez F, Gil-Bürmann C, Kaumanns W (1999) Costs of infant-carrying in cotton-top tamarin (Saguinus oedipus). Am J Primatol 48:99–111PubMedGoogle Scholar
  116. Savage A, Snowdon CT, Giraldo LH, Soto LH (1996) Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus). In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of neotropical primates. Plenum Press, New York, pp 187–199Google Scholar
  117. Schmitt C, Di Fiore A, Hurst D, Fernandez-Duque E (2005) Maternally-initiated babysitting by wild adult male equatorial sakis (Pithecia aequatorialis) in Yasuní National Park, Ecuador. 1st Annual NYCEP Symposium: ‘Monkeys: Old and New’: New YorkGoogle Scholar
  118. Schradin C, Anzenberger G (2002) Why do New World monkey fathers have enhanced prolactin levels? Evol Anthropol 11(S1):122–125Google Scholar
  119. Schradin C, Reeder DM, Mendoza SP, Anzenberger G (2003) Prolactin and paternal care: comparison of three species of monogamous New World monkeys (Callicebus cupreus, Callithrix jacchus, and Callimico goeldii). J Comp Psychol 117(2):166–175PubMedGoogle Scholar
  120. Sheldon BC (2002) Relating paternity to paternal care. Phil Trans R Soc Lond B 357(1419):341–350Google Scholar
  121. Sherry DS, Ellison PT (2007) Potential applications of urinary C-peptide of insulin for comparative energetics research. Am J Phys Anthropol 133(1):771–778PubMedGoogle Scholar
  122. Small MF (1990) Alloparental behaviour in Barbary macaques, Macaca sylvanus. Anim Behav 39(2):297–306Google Scholar
  123. Smuts BB, Gubernick DJ (1992) Male–infant relationships in nonhuman primates: paternal investment or mating effort? In: Hewlett BS (ed) Father–child relations. cultural and biosocial contexts. Aldine de Gruyter, New York, pp 1–30Google Scholar
  124. Snowdon CT, Soini P (1988) The tamarins, genus Saguinus. In: Mittermeier RA, Rylands AB, Coimbra-Filho A, Fonseca GAB (eds) Ecology and behavior of neotropical primates. World Wildlife Fund, Washington, pp 223–298Google Scholar
  125. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, CambridgeGoogle Scholar
  126. Stallcup JA, Woolfenden GE (1978) Family status and contributions to breeding by Florida scrub jays. Anim Behav 26:1144–1156Google Scholar
  127. Starin ED (1978) Food transfer by wild titi monkeys (Callicebus torquatus torquatus). Folia Primatol 30(2):145–151PubMedGoogle Scholar
  128. Tardif SD, Carson RL, Gangaware BL (1992) Infant-care behavior of non-reproductive helpers in a communal-care primate, the cotton-top tamarin (Saguinus oedipus). Ethology 92:155–167PubMedGoogle Scholar
  129. Tardif SD (1994) Relative energetic cost of infant care in small-bodied Neotropical primates and its relation to infant-care patterns. Am J Primatol 34:133–143Google Scholar
  130. Tardif S, Bales K (1997) Is infant-carrying a courtship strategy in callitrichid primates? Anim Behav 53:1001–1007Google Scholar
  131. Tecot SR et al (2012) Reproductive strategies and infant care in the Malagasy primates. In: Hinde K, Clancy KBH, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New YorkGoogle Scholar
  132. Trainor BC, Marler CA (2001) Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm Behav 40:32–42PubMedGoogle Scholar
  133. Trainor BC, Marler CA (2002) Testosterone promotes paternal behavior in a monogamous mammal via conversion to oestrogen. Proc R Soc Lond B 269:823–829Google Scholar
  134. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  135. Wade MJ, Shuster SM (2002) The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory. Am Nat 160(3):285–292PubMedGoogle Scholar
  136. Wade MJ, Shuster SM (2005) Don’t throw Bateman out with the bathwater! Integr Comp Biol 45:945–951PubMedGoogle Scholar
  137. Welker C, Schäfer-Witt C (1986) On the carrying behaviour of basic South American primates. Hum Evol 2(5):459–473Google Scholar
  138. Whitten PL (1987) Infants and adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsacker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 343–357Google Scholar
  139. Wickler W, Seibt U (1983) Monogamy: an ambiguous concept. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 33–50Google Scholar
  140. 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(6):829–846Google Scholar
  141. Wolovich CK, Feged A, Evans S, Green SM (2006) Social patterns of food sharing in monogamous owl monkeys. Am J Primatol 68:1–12Google Scholar
  142. Wolovich CK, Perea-Rodriguez JP, Fernandez-Duque E (2007) Food transfers to young and mates in wild owl monkeys (Aotus azarai). Am J Primatol 69:1–16Google Scholar
  143. Wolovich CK, Evans S, French JA (2008) Dads do not pay for sex but do buy the milk: food sharing and reproduction in owl monkeys (Aotus spp.). Anim Behav 75:1155–1163Google Scholar
  144. Wright PC (1984) Biparental care in Aotus trivirgatus and Callicebus moloch. In: Small MF (ed) Female primates: studies by women primatologists. Alan R. Liss, New York, pp 59–75Google Scholar
  145. Wright PC (1989) The nocturnal primate niche in the New World. J Hum Evol 18:635–658Google Scholar
  146. Wright PC (1990) Patterns of paternal care in primates. Int J Primatol 11(2):89–102Google Scholar
  147. Wuensch KL (1985) Effects of early paternal presence upon nonhuman offsprings’ development. Am Zool 25(3):911–923Google Scholar
  148. Xiang ZF, Sayers K, Grueter CC (2009) Direct paternal care in black-and-white snub-nosed monkeys. J Zool 278(2):157–162Google Scholar
  149. Yamamoto ME, Md FA, Irene Alencar A, Sousa MBCd, Araújo A (2009) Mating systems and female–female competition in the common marmoset, Callithrix jacchus. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids – the marmoset/callimico radiation. Springer, New YorkGoogle Scholar
  150. Ziegler TE (2000) Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatol 71(1–2):6–21PubMedGoogle Scholar
  151. Ziegler TE, Wegner FH, Snowdon CT (1996) Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a new world primate. Horm Behav 30:287–297PubMedGoogle Scholar
  152. Ziegler TE, Wegner FH, Carlson AA, Lazaro-Perea C, Snowdon CT (2000) Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): interactions with gender, androgen levels, and parenting. Horm Behav 38:111–122PubMedGoogle Scholar
  153. Ziegler TE, Prudom SL, Zahed SR (2009) Variations in male parenting behavior and physiology in the common marmoset. Am J Hum Biol 21(6):739–744PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Centro de Ecología Aplicada del LitoralConicetArgentina

Personalised recommendations