International Journal of Primatology

, Volume 38, Issue 6, pp 1032–1057 | Cite as

Modeling Developmental Class Provides Insights into Individual Contributions to Infant Survival in Callitrichids

  • Mrinalini WatsaEmail author
  • Gideon Erkenswick
  • Efstathia Robakis


Cooperative breeders live in social groups in which individuals in an age–sex class vary in reproductive development due to reproductive dominance by a few individuals in each group. Among callitrichids, adult males have been implicated in driving group reproductive output, but uneven sampling efforts, the underlying effects of group size, and pseudoreplication at the group and species levels are confounding variables in these analyses. We examined the drivers of group reproductive output in callitrichids by 1) conducting a meta-analysis of published studies of callitrichid group composition; 2) assigning developmental class based on reproductive morphology; and 3) using multivariate modeling to test whether the proportion of individuals of each developmental class predicts the presence and the number of surviving offspring among free-ranging Weddell’s saddleback tamarins (Leontocebus weddelli) and emperor tamarins (Saguinus imperator) in Peru. The meta-analysis revealed that the number of adult females and group size, but not the number of adult males, are significantly correlated with group reproductive output. Statistical models of the new dataset revealed that the proportion of primary breeding males, primary breeding females, and group size predicted whether groups had surviving infants, and that only the proportion of primary breeding females and group size predicted the number of surviving infants. Thus, primary breeding males appear to be necessary for groups to raise any infants, but a higher proportion of primary breeding females and a larger group size increase group reproductive output overall.


Callitrichid Cooperative breeding Development Group composition Reproductive output 



This study was funded by Field Projects International, the American Society of Mammalogists, Idea Wild, the Animal Behavior Society, Lambda Alpha, the International Primatological Society, the American Society of Primatologists, the Society for Integrative and Comparative Biology, Sigma Xi, and Trans World Airlines. We would like to acknowledge the logistical support of the Amazon Conservation Association, staff at EBLA, and the Ministry of Agriculture in Peru. In addition, we want to thank all wildlife handling research assistants who assisted in putting together this dataset with FPI and PrimatesPeru over the years. We also thank three reviewers and the editor of the International Journal of Primatology for their comments on a previous version of this manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10764_2017_9995_MOESM1_ESM.docx (33 kb)
ESM 1 (DOCX 32 kb)
10764_2017_9995_MOESM2_ESM.xlsx (89 kb)
ESM 2 (XLSX 88 kb)


  1. Akaike, H. (1994). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723.CrossRefGoogle Scholar
  2. Altmann, J. (1990). Primate males go where the females are. Animal Behaviour, 39(1), 193–195.CrossRefGoogle Scholar
  3. Arruda, M. F., Araújo, A., Sousa, M. B. C., Albuquerque, F. S., Albuquerque, A. C. S. R., & Yamamoto, M. E. (2005). Two breeding females within free-living groups may not always indicate polygyny: Alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatologica, 76(1), 10–20.CrossRefGoogle Scholar
  4. Baker, A. J., Dietz, J. M., & Kleiman, D. G. (1993). Behavioural evidence for monopolization of paternity in multi-male groups of golden lion tamarins. Animal Behaviour, 46(6), 1091–1103.CrossRefGoogle Scholar
  5. Bales, K., Dietz, J., Baker, A., Miller, K., & Tardif, S. D. (2000). Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatologica, 71(1–2), 27–38.CrossRefGoogle Scholar
  6. Bales, K., O’Herron, M., Baker, A. J., & Dietz, J. M. (2001). Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 54(4), 211–221.CrossRefPubMedGoogle Scholar
  7. Bales, K. L., French, J. A., McWilliams, J., Lake, R. A., & Dietz, J. M. (2006). Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia). Hormones and Behavior, 49(1), 88–95.CrossRefPubMedGoogle Scholar
  8. Barrett, J., Abbott, D. H., & George, L. M. (1990). Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. Journal of Reproduction and Fertility, 90(2), 411–418.CrossRefPubMedGoogle Scholar
  9. Bates, D., Mächler, M., Bolker, B., & Walker, S. (2014). Fitting linear mixed-effects models using lme4. doi:arXiv:1406.5823.
  10. Beehner, J. C., & Lu, A. (2013). Reproductive suppression in female primates: A review. Evolutionary Anthropology: Issues News and Reviews, 22(5), 226–238.CrossRefGoogle Scholar
  11. Bezerra, B. M., Da Silva Souto, A., & Schiel, N. (2007). Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrix jacchus). American Journal of Primatology, 69(8), 945–952.CrossRefPubMedGoogle Scholar
  12. Boulton, R. A., & Fletcher, A. W. (2015). Do mothers prefer helpers or smaller litters? Birth sex ratio and litter size adjustment in cotton-top tamarins (Saguinus oedipus). Ecology and Evolution, 5(3), 598–606.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buckner, J. C., Lynch Alfaro, J. W., Rylands, A. B., & Alfaro, M. E. (2015). Biogeography of the marmosets and tamarins (Callitrichidae). Molecular Phylogenetics and Evolution, 82, 413–425.CrossRefPubMedGoogle Scholar
  14. Calegaro-Marques, C., & Bicca-Marques, J. C. (1995). Two breeding females in a Saguinus fuscicollis weddelli group. Neotropical Primates, 3(4), 183.Google Scholar
  15. Campbell, C. J. (2006). Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi). American Journal of Primatology, 68(5), 507–511.CrossRefPubMedGoogle Scholar
  16. Carnes, L. M., Nunn, C. L., & Lewis, R. J. (2011). Effects of the distribution of female primates on the number of males. PLoS One, 6(5), e19853.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Clutton-Brock, T. (2012). Long-term, individual-based field studies. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 437–449). Berlin and Heidelberg: Springer Verlag.CrossRefGoogle Scholar
  18. Clutton-Brock, T., & Sheldon, B. C. (2010). Individuals and populations: The role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution, 25(10), 562–573.CrossRefGoogle Scholar
  19. Culot, L., Lledo-Ferrer, Y., Hoelscher, O., Muñoz Lazo, F. J. J., Huynen, M.-C., & Heymann, E. W. (2011). Reproductive failure, possible maternal infanticide, and cannibalism in wild moustached tamarins, Saguinus mystax. Primates, 52(2), 179–186.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Díaz-Muñoz, S. L. (2011). Paternity and relatedness in a polyandrous nonhuman primate: Testing adaptive hypotheses of male reproductive cooperation. Animal Behaviour, 82, 563–571.CrossRefGoogle Scholar
  21. Díaz-Muñoz, S. L. (2015). Complex cooperative breeders: Using infant care costs to explain variability in callitrichine social and reproductive behavior. American Journal of Primatology, 78(3), 372–387.CrossRefPubMedGoogle Scholar
  22. Digby, L. J. (1994). Social organization and reproductive strategies in a wild population of common marmosets (Callithrix jacchus). Doctoral thesis, University of California, Davis.Google Scholar
  23. Digby, L. (1995). Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus). Behavioral Ecology and Sociobiology, 37(1), 51–61.CrossRefGoogle Scholar
  24. Digby, L. J., & Ferrari, S. F. (1994). Multiple breeding females in free-ranging groups of Callithrix jacchus. International Journal of Primatology, 15(3), 389–397.CrossRefGoogle Scholar
  25. Digby, L., & Saltzman, W. (2009). Balancing cooperation and competition in callitrichid primates: Examining the relative risk of infanticide across species. In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The smallest anthropoids, 1st ed. (pp. 135–153). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.Google Scholar
  26. Dunbar, R. I. M. (2000). Male mating strategies: A modeling approach. In Primate males: Causes and consequences of variation in group composition (pp. 259–268). Cambridge: Cambridge University Press.Google Scholar
  27. Erb, W. M., & Porter, L. M. (2017). Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines. Evolutionary Anthropology, 26(1), 25–37.CrossRefPubMedGoogle Scholar
  28. Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., et al (2017). Impending extinction crisis of the world's primates: Why primates matter. Science Advances, 3(1), e1600946.PubMedPubMedCentralGoogle Scholar
  29. Fedigan, L. M., & Jack, K. M. (2011). Tracking Neotropical monkeys in Santa Rosa: Lessons from a regenerating Costa Rican dry forest. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 165–184). Berlin and Heidelberg: Springer-Verlag.Google Scholar
  30. Ferrari, S. F., & Digby, L. J. (1996). Wild Callithrix groups: Stable extended families?, 38, 19–27.Google Scholar
  31. French, J. A. (1997). Proximate regulation of singular breeding in callitrichid primates. In J. A. French & N. G. Solomon (Eds.), Cooperative breeding in mammals (pp. 34–75). New York: Cambridge University Press.Google Scholar
  32. French, J. A., & Cleveland, J. (1984). Scent-marking in the tamarin, Saguinus oedipus: Sex differences and ontogeny. Animal Behaviour, 32(2), 615–623.CrossRefGoogle Scholar
  33. French, J. A., Bales, K. L., Baker, A. J., & Dietz, J. M. (2003). Endocrine monitoring of wild dominant and subordinate female Leontopithecus rosalia. International Journal of Primatology, 24(6), 1281–1300.CrossRefGoogle Scholar
  34. Garber, P. A. (1997). One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy. Evolutionary Anthropology: Issues, News, and Reviews, 5(6), 187–199.CrossRefGoogle Scholar
  35. Garber, P. A., Moya, L., & Malaga, C. (1984). A preliminary field study of the moustached tamarin monkey (Saguinus mystax) in northeastern Peru: Questions concerned with the evolution of a communal breeding system. Folia Primatologica, 42(1), 17–32.CrossRefGoogle Scholar
  36. Garber, P. A., Ón, F. E., Moya, L., & Pruetz, J. D. (1993). Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems. American Journal of Primatology, 29(4), 235–254.CrossRefGoogle Scholar
  37. Garber, P. A., Moya, L., Pruetz, J. D., & Ique, C. (1996). Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax). American Journal of Primatology, 38(1), 29–46.CrossRefGoogle Scholar
  38. Garber, P. A., Porter, L. M., Spross, J., & Di Fiore, A. (2015). Tamarins: Insights into monogamous and non-monogamous single female social and breeding systems. American Journal of Primatology, 78(3), 298–314.CrossRefPubMedGoogle Scholar
  39. Ginther, A. J., Ziegler, T. E., & Snowdon, C. T. (2001). Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment. Animal Behaviour, 61(1), 65–78.CrossRefPubMedGoogle Scholar
  40. Goldizen, A. (1988). Tamarin and marmoset mating systems: Unusual flexibility. Trends in Ecology & Evolution, 3(2), 36–40.CrossRefGoogle Scholar
  41. Goldizen, A. W., & Terborgh, J. (1986). Cooperative polyandry and helping behavior in saddle-backed tamarins (Saguinus fuscicollis). In J. G. Else & P. C. Lee (Eds.), Proceedings of the Xth Congress of the International Primatological Society: Primate Ecology and Conservation (pp. 191–198). Chicago: University of Chicago Press.Google Scholar
  42. Goldizen, A. W., & Terborgh, J. (1989). Demography and dispersal patterns of a tamarin population: Possible causes of delayed breeding. The American Naturalist, 134(2), 208–224.CrossRefGoogle Scholar
  43. Goldizen, A. W., 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. American Journal of Primatology, 38(1), 57–83.CrossRefGoogle Scholar
  44. Gurevitch, J., Morrow, L. L., Wallace, A., & Walsh, J. S. (1992). A meta-analysis of competition in field experiments. American Naturalist, 140(4), 539–572.CrossRefGoogle Scholar
  45. Heymann, E. W. (2000). The number of adult males in callitrichine groups and its implications for callitrichine social evolution. In P. Kappeler (Ed.), Primate males: Causes and consequences of variation in group composition (pp. 64–71). Cambridge: Cambridge University Press.Google Scholar
  46. Heymann, E. W., & Soini, P. (1999). Offspring number in pygmy marmosets. Cebuella pygmaea, in relation to group size and the number of adult males, 46(6), 400–404.Google Scholar
  47. Huck, M., Lottker, P., & Heymann, E. W. (2004). The many faces of helping: Possible costs and benefits of infant carrying and food transfer in wild moustached tamarins (Saguinus mystax). Behaviour, 141(7), 915–934.CrossRefGoogle Scholar
  48. Huck, M., Löttker, P., Böhle, U.-R., & Heymann, E. W. (2005a). Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax). American Journal of Physical Anthropology, 127(4), 449–464.CrossRefPubMedGoogle Scholar
  49. Huck, M., Löttker, P., Heymann, E., & Heistermann, M. (2005b). Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguinus mystax. International Journal of Primatology, 26(1), 159–179.CrossRefGoogle Scholar
  50. Huck, M., Roos, C., & Heymann, E. W. (2007). Spatio-genetic population structure in mustached tamarins, Saguinus mystax. American Journal of Physical Anthropology, 132(4), 576–583.CrossRefPubMedGoogle Scholar
  51. Isler, K., & van Schaik, C. P. (2012). Allomaternal care, life history and brain size evolution in mammals. Journal of Human Evolution, 63(1), 52–63.CrossRefPubMedGoogle Scholar
  52. Jennions, M. (1994). Cooperative breeding in mammals. Trends in Ecology & Evolution, 9(3), 89–93.CrossRefGoogle Scholar
  53. Kappeler, P. M. (2000). Primate males: Causes and consequences of variation in group composition. Cambridge: Cambridge University Press.Google Scholar
  54. Kappeler, P., & van Schaik, C. (2002). Evolution of primate social systems. International Journal of Primatology, 23(4), 707–740.CrossRefGoogle Scholar
  55. Koenig, A. (1995). Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus). American Journal of Primatology, 35(4), 311–317.CrossRefGoogle Scholar
  56. Kostrub, C. E. (2003). The social organization and behavior of golden-mantled tamarins, Saguinus tripartitus, in Eastern Ecuador. Ph.D. thesis. University of California, Davis.Google Scholar
  57. Lazaro-Perea, C., Arruda, M. d. F., & Snowdon, C. T. (2004). Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets. Animal Behaviour, 67(4), 627–636.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Löttker, P., Huck, M., Heymann, E., & Heistermann, M. (2004). Endocrine correlates of reproductive status in breeding and nonbreeding wild female moustached tamarins. International Journal of Primatology, 25(4), 919–937.CrossRefGoogle Scholar
  59. MacLeod, K. (2013). Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. Animal Behaviour, 86(5), 1059–1067.CrossRefGoogle Scholar
  60. Martins, M. M., Nascimento, A., & Nali, C. (2015). A test for sex-biased dispersal in the black-faced lion tamarin (Leontopithecus caissara): Inferences from microsatellite markers. Studies on Neotropical Fauna and Environment, 50(1), 14–20.CrossRefGoogle Scholar
  61. Matauschek, C., Roos, C., & Heymann, E. W. (2010). Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. American Journal of Physical Anthropology, 144(4), 564–574.CrossRefPubMedGoogle Scholar
  62. Mitani, J. C., Gros-Louis, J., & Manson, J. H. (1996). Number of males in primate groups: Comparative tests of competing hypotheses. American Journal of Primatology, 38, 315–332.CrossRefGoogle Scholar
  63. Moreira, L. A. A., de Oliveira, D. G. R., de Sousa, M. B. C., & Pessoa, D. M. A. (2015). Parturition signaling by visual cues in female marmosets (Callithrix jacchus). PLoS One, 10(6), e0129319.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Moreno, P. G., Eberhardt, M. A. T., Lamattina, D., Previtali, M. A., & Beldomenico, P. M. (2013). Intra-phylum and inter-phyla associations among gastrointestinal parasites in two wild mammal species. Parasitology Research, 112(9), 3295–3304.CrossRefPubMedGoogle Scholar
  65. Nievergelt, C. M., Digby, L. J., Ramakrishnan, U., & Woodruff, D. S. (2000). Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. International Journal of Primatology, 21(1), 1–20.CrossRefGoogle Scholar
  66. Nunn, C. L. (1999). The number of males in primate social groups: A comparative test of the socioecological model. Behavioral Ecology and Sociobiology, 46(1), 1–13.CrossRefGoogle Scholar
  67. Pontes, A., & da Cruz, M. (1995). Home range, intergroup transfers, and reproductive status of common marmosets Callithrix jacchus in a forest fragment in north-eastern Brazil. Primates, 36(3), 335–347.CrossRefGoogle Scholar
  68. Porter, L. M. (2001). Social organization, reproduction and rearing strategies of Callimico goeldii: New clues from the wild. Folia Primatologica, 72(2), 69–79.CrossRefGoogle Scholar
  69. Poulin, R. (1994). Meta-analysis of parasite-induced behavioural changes. Animal Behaviour, 48(1), 137–146.CrossRefGoogle Scholar
  70. R Development Core Team. (2015). R: A language and environment for statistical computing. Vienna, Austria.
  71. Ramirez, M. M. (1989). Feeding ecology and demography of the moustached tamarin Saguinus mystax in northeastern Peru. Ph.D. dissertation, The City University of New York.Google Scholar
  72. Ridley, M. (1986). The number of males in a primate troop. Animal Behaviour, 34(6), 1848–1858.CrossRefGoogle Scholar
  73. Robbins, M. M. (2010). Long-term field studies of primates: Considering the past, present, and future. Evolutionary Anthropology: Issues News and Reviews, 19, 87–88.Google Scholar
  74. Roda, S. A. (1989). Ocorrência de duas fêmeas reprodutivas em grupos selvagens de Callithrix jacchus (Primates, Callitrichidae). In M. L. Cristoffersen & D. S. Amorim (Eds.), Resumos do XVI Congresso Brasileiro de Zoologia (p. 122). Resumos do XVI congresso Brasileiro de zoologia.Google Scholar
  75. Rollin, B. E., & Kessel, M. L. (2006). Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour, 71, 245–253.CrossRefGoogle Scholar
  76. Savage, A., & Baker, A. J. (1996). Callitrichid social structure and mating system: Evidence from field studies. American Journal of Primatology, 38(1), 1–3.CrossRefGoogle Scholar
  77. Savage, A., Giraldo, L., Blumer, E., Soto, L., & Burger, W. (1993). Field techniques for monitoring cotton-top tamarins (Saguinus oedipus oedipus) in Colombia. American Journal of Primatology, 31(3), 189–196.CrossRefGoogle Scholar
  78. Savage, A., Snowdon, C. T., Giraldo, L. H., & Soto, L. H. (1996). Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus). In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of Neotropical primates (pp. 187–199). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  79. Scanlon, C., Chalmers, N., & Monteiro Da Cruz, M. (1988). Changes in the size, composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in north east Brazil. Primates, 29(3), 295–305.CrossRefGoogle Scholar
  80. Scheiner, S. M., & Gurevitch, J. (2001). Design and analysis of ecological experiments. Oxford: Oxford University Press.Google Scholar
  81. Sikes, R. S., & Gannon, W. L. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92(1), 235–253.CrossRefGoogle Scholar
  82. Smith, A. C., Tirado Herrera, E., Buchanan-Smith, H. M., & Heymann, E. W. (2001). Multiple breeding females and allo-nursing in a wild group of moustached tamarins (Saguinus mystax). Neotropical Primates, 9(2), 67–69.Google Scholar
  83. Soini, P. (1988). The pygmy marmoset, genus Cebuella. In R. A. Mittermeier, A. Rylands, A. Coimbra-Filho, & G. da Fonseca (Eds.), Ecology and behavior of neotropical primates (Vol. 2, pp. 79–129). Washington, DC: World Wildlife Fund.Google Scholar
  84. Soini, P., & Cóppula, M. (1981). Ecologia y dinamica poblacional del pichio Saguinus fuscicollis (Primates, Calltrichidae): Informe de Pacaya No. 4 (No. 4). Centro de Dators Para La conservación (pp. 1–31). Direccion Regional de Agricultura.Google Scholar
  85. Soini, P., & de Soini, M. (1990). Distribución geografica y ecologia poblacional de Saguinus mystax. In La primatologia en el Peru: Proyecto Peruano de Primatología “Manuel Moro Sommo” (pp. 1–31). Lima: Proyecto Peruana de Primatología.Google Scholar
  86. Sousa, M. B. C., Albuquerque, A. C. S. D. R., Albuquerque, F. D. S., Araujo, A., Yamamoto, M. E., & Arruda, M. d. F. (2005). Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups. American Journal of Primatology, 67(1), 37–50.CrossRefPubMedGoogle Scholar
  87. Suárez, S. S. (2007). Paternity, relatedness, and socio-reproductive behavior in a population of wild red-bellied tamarins (Saguinus labiatus). Doctoral Dissertation, New York University. Retrieved from
  88. Sussman, R. W., & Garber, P. A. (1987). A new interpretation of the social organization and mating system of the Callitrichidae. International Journal of Primatology, 8(1), 73–92.CrossRefGoogle Scholar
  89. Tardif, S. D. (1994). Relative energetic cost of infant care in small-bodied neotropical primates and its relation to infant-care patterns. American Journal of Primatology, 34(2), 133–143.CrossRefGoogle Scholar
  90. Tardif, S. D. (1997). The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In N. G. Solomon & J. A. French (Eds.), Cooperative breeding in mammals (pp. 11–33). New York: Cambridge University Press.Google Scholar
  91. Terborgh, J., & Goldizen, A. W. (1985). On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis ). Behavioral Ecology and Sociobiology, 16, 293–299.CrossRefGoogle Scholar
  92. Tirado Herrera, E. R., Knogge, C., & Heymann, E. W. (2000). Infanticide in a group of wild saddle-back tamarins, Saguinus fuscicollis. American Journal of Primatology, 50(2), 153–157.CrossRefGoogle Scholar
  93. van Schaik, C. P., & Hörstermann, M. (1994). Predation risk and the number of adult males in a primate group: A comparative test. Behavioral Ecology and Sociobiology, 35(4), 261–272.CrossRefGoogle Scholar
  94. Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S-plus, 4 ed. (pp. 1–498). New York: Springer Science+Business Media.Google Scholar
  95. Watsa, M. (2013). Growing up tamarin: Morphology, reproduction, and population demography of sympatric free-ranging Saguinus fuscicollis and S. imperator. Doctoral thesis, Washington University in St. Louis. Retrieved from
  96. Watsa, M., Erkenswick, G. A., Halloran, D., Kane, E. E., Poirier, A., et al (2015). A field protocol for the capture and release of callitrichids. Neotropical Primates, 22(2), 59–68.Google Scholar
  97. Windfelder, T. L. (2000). Observations on the birth and subsequent care of twin offspring by a lone pair of wild emperor tamarins (Saguinus imperator). American Journal of Primatology, 52(2), 107–113.CrossRefPubMedGoogle Scholar
  98. Wislocki, G. B. (1939). Observations on twinning in marmosets. American Journal of Anatomy, 64(3), 445–483.CrossRefGoogle Scholar
  99. Zeller, U., Epple, G., Küderling, I., & Kuhn, H. (1988). The anatomy of the circumgenital scent gland of Saguinus fuscicollis (Callitrichidae, Primates). Journal of Zoology, 214(1), 141–156.CrossRefGoogle Scholar
  100. Ziegler, T. E., Savage, A., Scheffler, G., & Snowdon, C. T. (1987). The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. Biology of Reproduction, 37(3), 618–627.CrossRefPubMedGoogle Scholar
  101. Ziegler, T. E., Epple, G., Snowdon, C. T., Porter, T. A., Belcher, A. M., & Kuderling, I. (1993). Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Animal Behaviour, 45(2), 313–322.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of AnthropologyWashington University in St. LouisSt. LouisUSA
  2. 2.Field Projects InternationalSt. LouisUSA
  3. 3.Department of BiologyUniversity of Missouri–St. LouisSt. LouisUSA

Personalised recommendations