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Balancing Cooperation and Competition in Callitrichid Primates: Examining the Relative Risk of Infanticide Across Species

  • Leslie Digby
  • Wendy Saltzman
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

At least eight cases of infanticide by females other than the mother have been observed in wild groups of common marmosets (Callithrix jacchus), with several more cases described for captive groups. Infanticide by females other than the mother has not, however, been documented for wild groups of other callitrichid species. Why might such overt aggression toward infants be more likely in one species than in others? In the common marmoset, a variety of social, reproductive and ecological characteristics – including short inter-birth intervals (and the resulting potential for overlap of pregnancies and births), habitat saturation, small home ranges, and low cost of infant care (including decreased travel costs and short dependency periods compared to other callitrichids) – may contribute to an increased likelihood of two breeding females being present in a group, which in turn may give rise to the potential for competition between breeding females and, ultimately, to infanticide. These conditions are less common in wild groups of most other callitrichid species. All callitrichids balance the need for cooperative care of young with the reproductive competition that results from limited reproductive opportunities; however, ecological and social conditions appear to tip the balance toward infanticide more frequently in common marmosets than in other callitrichid species.

Keywords

Common Marmoset Breeding Female Dominant Female Subordinate Female Reproductive Suppression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Resumen

Al menos ocho casos de infanticidio por hembras distintas a la madre han sido observados en grupos silvestres de marmosetas comunes (Callithrix jacchus), con muchos más casos descritos para grupos cautivos. Sin embargo, infanticidio por hembras distintas a la madre no ha sido documentado en grupos silvestres de otras especies de calitrícidos ¿Porqué podría la agresión tan evidente hacia infantes ser más probable en una especie que en otras? En las marmosetas comunes, una variedad de características sociales, reproductivas y ecológicas – incluyendo intervalos cortos entre nacimientos (y el resultado potencial de traslape de embarazos y nacimientos), la saturación del hábitat, ámbitos hogareños pequeños y bajo costo de cuidado infantil (incluyendo disminución de costos de viaje y períodos cortos de dependencia comparados con otros calitrícidos) – pueden contribuir al aumento de la posibilidad de que dos hembras reproductoras se presenten en un grupo, lo cual aumenta el potencial para competencia entre la hembras reproductoras y, ultimadamente, a cometer infanticidio. Dichas condiciones son menos comunes en los grupos silvestres de otras especies calitrícidos. Todos los calitrícidos equilibran la necesidad de cuidado cooperativo de los jóvenes con la competencia reproductiva que resulta de oportunidades reproductivas limitadas; no obstante, las condiciones ecológicas y sociales parecen inclinar la balanza hacia el infanticidio con más frecuencia en las marmosetas comunes que en otras especies de calitrícidos.

Resumo

Pelo menos oito casos de infanticídio realizados por fêmeas que não as mães foram observados em grupos de sagüi comum selvagens (Callithrix jacchus), com vários outros casos sendo descritos para grupos vivendo em cativeiro. Entretanto, infanticídios por fêmeas que não as mães não têm sido bem documentados em grupos selvagens de outras espécies de calitriquídeos. Por que esta agressão em relação aos infantes é mais comum em uma espécie do que em outras? Em sagüi comum, uma variedade de características sociais, reprodutivas e ecológicas – incluindo o intervalo curto entre nascimentos (e o resultante potencial de sobreposição de gestações e nascimentos) saturação de habitat, áreas de uso pequenas e baixo custo do cuidado parental (incluindo diminuição no custo do deslocamento e o período de dependência curto comparado com outros calitriquídeos) – podem contribuir para o aumento da probabilidade de duas fêmeas reprodutoras estarem presentes em um mesmo grupo, que por sua vez favorece o surgimento de competição potencial entre as fêmeas reprodutoras e, eventualmente, o infanticídio. Estas condições são menos comuns em grupos selvagens da maioria das demais espécies de calitriquídeos. Todos os calitriquídeos fazem o balanço entre a necessidade de cuidado cooperativo dos infantes e a competição reprodutiva que resulta das oportunidades limitadas de reprodução; entretanto, as condições ecológicas e sociais parecem inclinar a balança em relação ao infanticídio mais frequentemente em sagüis comuns do que em outras espécies de calitriquídeos.

References

  1. Abbott DH (1984) Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Am J Primatol 6:69–186CrossRefGoogle Scholar
  2. Abbott DH, Barrett J, George LM (1993) Comparative aspects of the social suppression of reproduction in female marmosets and tamarins. In: Rylands AB (ed) Marmosets and tamarins: systematics, behavior, and ecology. Oxford Science Publications, Oxford, pp 152–162Google Scholar
  3. Abbott DH, Digby L, Saltzman W (2009) Reproductive skew in female common marmosets: contributions on infanticide and subordinate self-restraint. In: Jones C, Hager R (eds) Reproductive skew in vertebrates: proximate ultimate causes. Cambridge University Press, CambridgeGoogle Scholar
  4. Albernaz AL, Magnusson WE (1999) Home-range size of the bare-ear marmoset (Callithrix argentata) at Alter do Chão, Central Amazonia, Brazil. Int J Primatol 20(5):665–677CrossRefGoogle Scholar
  5. Alonso C (1986) Fracasso no inibição da reprodução du uma fêmea subordinada e troca de hierarquia em um grupo familiar de Callithrix jacchus jacchus. In: Thiago de Mello M (ed) A primatologia no Brasil – 2. Sociedade Brasileira de Primatolgia, Campinas, p 203Google Scholar
  6. Altmann J (1997) Mate choice and intrasexual reproductive competition: contributions to reproduction that go beyond acquiring more mates. In: Gowaty PA (ed) Feminism and evolutionary biology: boundaries, intersections and frontiers. Chapman & Hall, New York, pp 320–333Google Scholar
  7. Arruda MF, Araujo A, Sousa MBC, Albuquerque FS, Albuquerque ACSR, Yamamoto ME (2005) Two breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatol 76:10–20CrossRefPubMedGoogle Scholar
  8. Baker AJ, Bales K, Dietz JM (2002) Mating system and group dynamics in lion tamarins. In: Kleiman DG, Rylands AB (eds) Lion tamarins: biology and conservation. Smithsonian Institution Press, Washington, DC, pp 188–212Google Scholar
  9. Bezerra BM, Souto AS, Schiel N (2007) Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrx jacchus). Am J Primatol 69:945–952CrossRefPubMedGoogle Scholar
  10. Calegaro-Marques C, Bicca-Marques JC, Azevado MAO (1995) Two breeding females in a Saguinus fuscicollis weddelli group. Neotrop Primates 3(4):183Google Scholar
  11. Christen A (1999) Survey of Goeldi’s monkeys (Callimico goeldii) in northern Bolivia. Folia Primatol 70(2):107–111CrossRefPubMedGoogle Scholar
  12. Coutinho PEG, Corrêa HKM (1995) Polygyny in a free-ranging group of buffy-tufted-ear marmosets, Callithrix aurita. Folia Primatol 65:25–29CrossRefPubMedGoogle Scholar
  13. de la Torre S, Snowdon CT, Bejarana M (2000) Effects of human activities on wild pygmy marmosets in Ecuadorian Amazonia. Biol Conserv 94(2):153–163CrossRefGoogle Scholar
  14. Dettling A, Price CR (1999) Hormonal monitoring of age at sexual maturation in female Goeldi’s monkey (Callimico goeldii) in their family groups. Am J Primatol 48:77–83CrossRefPubMedGoogle Scholar
  15. Dietz JM, Baker AJ (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Anim Behav 46:1067–1078CrossRefGoogle Scholar
  16. Dietz JM, Peres CA, Pinder, L (1997) Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). Amer J Primatol 41(4): 289–305CrossRefGoogle Scholar
  17. Dietz JM, Baker AJ, Ballou JD (2000) Demographic evidence of inbreeding depression in wild golden lion tamarins. In: Young AG, Clarke GM (eds) Genetics. Demography and Viability of Fragmented Populations. Cambridge University Press, Edinburgh, pp 203–211Google Scholar
  18. Digby L (1995) Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus). Behav Ecol Sociobiol 37:51–61CrossRefGoogle Scholar
  19. Digby LJ (2000) Infanticide by female mammals: implications for the evolution of social systems. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 423–446CrossRefGoogle Scholar
  20. Digby LJ, Barreto CE (1996) Activity and ranging patterns in common marmosets (Callithrix jacchus): implications for reproductive strategies. In: Norconk M, Rosenberger A, Garber PA (eds) Adaptive radiations of Neotropical Primates. Plenum, New York, pp 173–185Google Scholar
  21. Digby, L.J., Barreto CE (1993) Social organization in a wild population of Callithrix jacchus. Part I: group composition and dynamics. Folia Primatologica 61:123–134CrossRefGoogle Scholar
  22. Digby LJ, Ferrari SF, Saltzman W (2007) Callitrichines: the role of competition in a cooperatively breeding species. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder S (eds) Primates in perspective. Oxford, Oxford University Press, pp 85–105Google Scholar
  23. Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73:321–326CrossRefGoogle Scholar
  24. Ferrari SF (this volume) Social hierarchy and dispersal in free-ranging buffy-headed marmosets (Callithrix flaviceps). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 155–165Google Scholar
  25. Ferrari SF, Diego VH (1992) Long-term changes in a wild marmoset group. Folia Primatol 58(4):215–218CrossRefGoogle Scholar
  26. Ferrari SF, Rylands AB (1994) Activity budgets and differential visibility in three species of marmosets. Folia Primatol 63(2):78–83CrossRefGoogle Scholar
  27. Ferrari SF, Correa HKM, Coutinho PEG (1996) Ecology of the “southern” marmosets (Callithrix aurita and Callithrix flaviceps). In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of Neotropical Primates. Plenum, New York, pp 157–171Google Scholar
  28. French JA (1997) Proximate regulation of singular breeding in callitrichid primates. In: Soloman NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 34–75Google Scholar
  29. French JA, de Vleeschouwer K, Bales K, Heistermann M (2002) Lion tamarin reproductive biology. In: Kleiman DG, Rylands AB (eds) Lion tamarins: biology and conservation. Smithsonian Institution Press, Washington, DC, pp 133–156Google Scholar
  30. Garber PA (1988) Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour 105:18–34CrossRefGoogle Scholar
  31. Garber PA (1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive strategy. Evol Anthropol 5:187–199CrossRefGoogle Scholar
  32. Garber PA, Encarnacion F, Moya L, Pruetz JD (1993) Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): implications for reconstructing platyrrhine mating systems. Am J Primatol 29(4):235–254CrossRefGoogle Scholar
  33. Goldizen AW (2003) Social monogamy and its variations in callitrichids: do these relate to the costs of infant care? In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans, and other mammals. Cambridge University Press, Cambridge, pp 232–247Google Scholar
  34. Goldizen AW, 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(1):57–84CrossRefGoogle Scholar
  35. Gowaty P (1997) Sexual dialectics, sexual selection, and variation in female reproductive behavior. In: Gowaty PA (ed) Feminism and evolutionary biology: boundaries, intersections and frontiers. Chapman & Hall, New York, pp 351–84Google Scholar
  36. Guimarães A (1998) Ecology and social behavior of buffy-headed marmosets, Callithrix flaviceps. Neotrop Primates 6(2):51–52Google Scholar
  37. Hager R, Johnstone RA (2004) Infanticide and control of reproduction in cooperative and communal breeders. Anim Behav 67:941–949CrossRefGoogle Scholar
  38. Herrera ERT, Knogge C, Heymann EW (2000) Infanticide in a group of wild saddle-back tamarins, Saguinus fuscicollis. Am J Primatol 50:153–157CrossRefPubMedGoogle Scholar
  39. Heymann EW (2000) The number of adult males in callitrichine groups and its implications for callitrichine social evolution. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 64–71Google Scholar
  40. Heymann EW (2001) Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis. Folia Primatol 72:253–267CrossRefPubMedGoogle Scholar
  41. Heymann EW, Soini P (1999) Offspring number in pygmy marmosets, Cebuella pygmaea, in relation to group size and number of adult males. Behav Ecol Sociobiol 46:400–404CrossRefGoogle Scholar
  42. Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. University of Chicago Press, ChicagoGoogle Scholar
  43. Hrdy SB (1976) Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Rosenblatt L, Hinde RA, Shaw R, Beer C (eds) Advances in the study of behavior, vol 6. Academic, New York, pp 101–58Google Scholar
  44. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40CrossRefGoogle Scholar
  45. Hrdy SB (1981) The woman that never evolved. Harvard University Press, Cambridge, MAGoogle Scholar
  46. Hrdy SB (1999) Mother nature: maternal instincts and how they shape the human species. Ballantine Books, New YorkGoogle Scholar
  47. Hrdy SB, Hausfater G (1984) Comparative and evolutionary perspectives on infanticide: introduction and overview. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine de Gruyter, New York, pp xiii–xxxvGoogle Scholar
  48. Jones C (2003) Sexual selection and reproductive competition in Primates: new perspectives and directions. American Society of Primatologists, NormanGoogle Scholar
  49. Kirkpatrick-Tanner M, Aeschlimann C, Anzenberger G (1996) Occurrence of an infanticide within captive polygynous group of common marmosets, Callithrix jacchus. Folia Primatol 67(1):52–58PubMedGoogle Scholar
  50. Koenig A (1995) Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus). Am J Primatol 35:311–17CrossRefGoogle Scholar
  51. Kostrub CE (2003) The Social Organization and Behavior of Golden Mantled Tamarins, Saguinus tripartitus, in eastern Ecuador [PhD Thesis]. University of California DavisGoogle Scholar
  52. Lazaro-Perea C, Castro CSS, Harrison R, Araujo A, Arruda MF, Snowdon CT (2000) Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets. Behav Ecol Sociobiol 48:137–146CrossRefGoogle Scholar
  53. Löttker P, Huck M, Heymann EW (2004) Demographic parameters and events in wild moustached tamarins (Saguinus mystax). Am J Primatol 64:425–449CrossRefPubMedGoogle Scholar
  54. Maestripieri D, Carroll KA (1998) Risk factors for infant abuse and neglect in group-living rhesus monkeys. Psychol Sci 9:143–5CrossRefGoogle Scholar
  55. Martins MM (1998) Feeding ecology of Callithrix aurita in a forest fragment of Minas Gerais. Neotrop Primates 6(4):126–127Google Scholar
  56. Melo L, Mendes Pontes AR, Monteiro da Cruz MAO (2003) Infanticide and cannibalism in wild common marmosets. Folia Primatol 74(1):48–50CrossRefPubMedGoogle Scholar
  57. Nievergelt CM, Digby LJ, Ramakrishnan 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):1–20CrossRefGoogle Scholar
  58. Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New YorkGoogle Scholar
  59. Porter LM (2001) Social organization, reproduction and rearing strategies of Callimico goeldii: new clues from the wild. Folia Primatol 72(2):69–79CrossRefPubMedGoogle Scholar
  60. Porter LM, Garber PG (this volume) 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
  61. Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831CrossRefPubMedGoogle Scholar
  62. Raboy BE, Dietz JM (2004) Diet, foraging, and use of space in wild golden-headed lion tamarins. Am J Primatol 63:1–15CrossRefPubMedGoogle Scholar
  63. Roda SA, Mendes Pontes AR (1998) Polygyny and infanticide in common marmosets in a fragment of Atlantic Foreset of Brazil. Folia Primatol 69(6):372–376CrossRefPubMedGoogle Scholar
  64. Rylands AB (1986a) Ranging behaviour and habitat preference of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates) J. Zool Lond (A) 210:489–514CrossRefGoogle Scholar
  65. Rylands AB (1986b) Infant-carrying in a wild marmoset group, Callithrix humeralifer: evidence for a polyandrous mating system. In: Thiago de Mello M (ed) A primatologia No Brasil – 2. Sociedade Brasileira de Primatologia, Brasilia, pp 131–144Google Scholar
  66. Saltzman W (2003) Reproductive competition among female common marmosets (Callithrix jacchus): proximate and ultimate causes. In: Jones C (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 197–229Google Scholar
  67. Saltzman W, Abbott DH (2005) Diminished maternal responsiveness during pregnancy in multiparous female common marmosets. Horm Behav 47:151–163CrossRefPubMedGoogle Scholar
  68. Saltzman W, Schultz-Darken NJ, Abbott DH (1997) Familial influences on ovulatory function in common marmosets (Callithrix jacchus). Am J Primatol 41(3):159–177CrossRefPubMedGoogle Scholar
  69. Saltzman W, Pick RR, Salper OJ, Liedl KJ, Abbott DH (2004) Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male. Anim Behav 68:59–73CrossRefGoogle Scholar
  70. Saltzman W, Liedl KJ, Salper OJ, Pick RR, Abbott DH (2008) Post-conception reproductive competition in cooperatively breeding common marmosets. Horm Behav 53:274–286CrossRefGoogle Scholar
  71. Saltzman W, Digby LH, Abbott DH (2009) Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes? Proc Biol Sci 276:389–399Google Scholar
  72. Savage A, Giraldo LH, Soto LH, Snowdon CT (1996) Demography, group composition, and dispersal in wild cotton-top tamarins (Saguinus oedipus) groups. Am J Primatol 38(1):85–100CrossRefGoogle Scholar
  73. Savage A, Shideler SE, Soto LH, Causado J, Giraldo LH, Lasley BL, Snowdon CT (1997) Reproductive events of wild cotton-top tamarins (Saguinus Oedipus) in Colombia. Am J Primatol 43:329–337CrossRefPubMedGoogle Scholar
  74. Sherman PW (1981) Reproductive competition and infanticide in Belding’s ground squirrels and other animals. In: Alexander RD, Tinkle D (eds) Natural selection and social behavior: recent research and theory. Chiron Press, New York, pp 311–331Google Scholar
  75. Smith AC, Tirado Herrara ER, Buchanan-Smith HM (2001) Multiple breeding females and allo-nursing in a wild group of moustached tamarins (Saguinus mystax). Neotrop Primates 9(2):67–69Google Scholar
  76. Snowdon CT, Ziegler TE, Widowski TM (1993) Further hormonal suppression of eldest daughter cotton-top tamarins following birth of infants. Am J Primatol 31(1):11–21CrossRefGoogle Scholar
  77. Tardif SD (1997) The energetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In: Soloman NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 11–33Google Scholar
  78. Tardif SD, Harrison ML, Simek MA (1993) Communal infant care in marmosets and tamarins: relation to energetics, ecology, and social organization. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford Science Publications, Oxford, pp 220–234Google Scholar
  79. Tardif SD, Smucny DA, Abbott DH, Mansfield K, Schultz-Darken N, Yamamoto ME (2003) Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 53:364–368PubMedGoogle Scholar
  80. Tavares LI, Ferrari SF (2002) Diet of the silvery marmoset (Callithrix argentata) at CFPn: seasonal and longitudinal variation. In: Lisboar PLB (ed) Caxiuanã, Populações Tradicionais. Meio Físico e Diversidade Biológica. CNPq/MCT, Belèm, pp 707–719Google Scholar
  81. Treves A (2000) Prevention of infanticide: the perspective of infant primates. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 223–238CrossRefGoogle Scholar
  82. van Roosmalen MGM, van Roosmalen T (2003) The description of a new marmoset genus, Callibella, (Callitrichinae, Primates), including its molecular phylogenetic status. Neotrop Primates 11(1):1–10Google Scholar
  83. van Schaik CP, Janson CH (2000) Infanticide by males and its implications. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  84. Wasser SK, Barash DP (1983) Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol 58:513–538CrossRefPubMedGoogle Scholar
  85. Yamamoto ME, Arruda MF, de Sousa MBC, Alencar AI (1996) Mating systems and reproductive strategies in Callithrix jacchus females. Abstracts XVI Congress of the International Primatological Society and XIX Conferences American Society of Primatologists, p 56Google Scholar
  86. Yamamoto ME, Arruda MF, Alencar AI, de Sousa MBC, Araújo A (this volume) Mating systems and female–female competition in the common marmosets, Callithrix jacchus. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 119–133Google Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA

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