Multi-male groups positively linked to infant survival and growth in a cooperatively breeding primate

  • Laura A. Heslin PiperEmail author
  • James M. Dietz
  • Becky E. Raboy
Original Article


Cooperative breeding is a system where helper individuals care for breeding individuals’ offspring. As a result, social environment is likely to play a key role in regulating reproductive success. In primates, cooperative breeding is only found in the family Callitrichidae. Callitrichid males typically provide more infant care than non-breeding females, and in many callitrichid species, the presence of multiple males has been linked to infant survival. Leontopithecus chrysomelas (the golden-headed lion tamarin) is an endangered callitrichid found in the Atlantic Forest of Brazil. We used long-term data for wild L. chrysomelas to assess the influence of social group composition on reproductive success. Our survival model found that infant survival was negatively associated with group size, but this cost was mitigated by the presence of multiple adult males vs a single adult male. We also found that infants raised in groups with multiple adult males exhibited faster growth rates and higher adult weights than infants raised with a single adult male. This study adds novel evidence for the positive influence of adult males on callitrichid reproduction, demonstrating that adult males influence infant growth, as well as survival, in wild populations of cooperatively breeding primates. We suggest that social group composition, particularly the presence of adult males, be considered in future conservation strategies given its importance for reproductive success.

Significance statement

In cooperatively breeding species, group members care for breeding individuals’ offspring. Due to this care, group composition may have a strong influence on infant success. In cooperatively breeding primates, males often provide more infant care than females. We investigated the influence of group composition on infant success in a cooperatively breeding primate, the golden-headed lion tamarin. Using long-term field data, we found that infant survival decreased as group size increased. However, this effect was reduced when multiple adult males were present in the group compared to a single male. We also found that infants grew faster and reached larger adult weights in the presence of multiple adult males compared to a single male. Our results demonstrate the importance of group composition for cooperative breeders and provide new evidence for the positive influence of adult males on cooperatively breeding primate infants.


Leontopithecus chrysomelas Callitrichid Primate Cooperative breeding Social behavior Reproductive success 



We thank the Brazilian Institute for the Environment and Renewable Natural Resources (IBAMA), the Brazilian Science Council (CNPq), and the owners of Fazenda Incon for permission to conduct work in and around Una Biological Reserve. We are especially grateful for the instrumental support of Saturnino N. de Souza and Paulo Cesar Cruz. The University of Maryland, Smithsonian Institution, and Instituto de Estudos Socioambientais do Sul da Bahia (IESB) provided institutional support during the field portion of this study. We are grateful to our field assistants Jose Renato, Daniel Batista, Gilvan Gomes Mota, Gilvánio Gomes Mota, and Jiomário Santos Sousa. We thank our veterinarians Lilian Catenacci and Rafael Monteiro. Nayara Cardoso, Carlos Guidorizzi, Kristel De Vleeschouwer, Cecilia Keirulff, Leonardo Oliveira, and Leonardo Neves gave invaluable assistance in the field. Further thanks to Sarah Hankerson and to Lily Hu for data entry and organization. We also thank Diane Chan, Nathan Taback, and Marty Krkosek for advice on statistics, and Deborah McLennan and Helen Rodd for their guidance and advice during the analysis stage of this research. We thank the anonymous reviewers for their helpful comments and feedback.

Funding information

This work was supported by the World Wildlife Fund, the Durrell Wildlife Conservation Trust, the Margot Marsh Biodiversity Foundation, the Lion Tamarins of Brazil Fund, the Tulsa Zoo, a National Science Foundation Research and Training Grant (BIR-9602266 to the University of Maryland), Sigma Xi (to BER), and a Eugenie Clark Fellowship (to BER). The analysis portion of this study was funded by a National Sciences and Engineering Research Council Discovery Grant (RGPIN-2014-04964 to BER).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This research complied with the guidelines of the University of Maryland Animal Care and Use Committee (under protocol numbers: R-91-07, R-93-39, R-01-13A, R-01-13B, R-04-43, R-07-75) and all applicable Brazilian laws.


  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. Int J Primatol 23(1):179–189. PubMedCentralCrossRefPubMedGoogle Scholar
  2. Aitken EH, Bueno MG, Ortolan LS, Alvaréz JM, Pissinatti A, Kierulff MCM, Catão-Dias JL, Epiphanio S (2016) Survey of Plasmodium in the golden-headed lion tamarin (Leontopithecus chrysomelas) living in urban Atlantic forest in Rio de Janeiro, Brazil. Malar J 15(1):93. PubMedCentralCrossRefPubMedGoogle Scholar
  3. 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: human fertility behavior in biodemographic perspective: proceedings of a workshop. National Academies Press, WashingtonGoogle Scholar
  4. Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57(5):490–501. CrossRefGoogle Scholar
  5. Baker AJ, Dietz JM, Kleiman DG (1993) Behavioural evidence for monopolization of paternity in multi-male groups of golden lion tamarins. Anim Behav 46(6):1091–1103. CrossRefGoogle Scholar
  6. Bales K, Dietz J, Baker A, Miller K, Tardif S (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71(1-2):27–38. CrossRefPubMedGoogle Scholar
  7. Bales K, 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):211–221. CrossRefPubMedGoogle Scholar
  8. Brouwer L, Richardson DS, Eikenaar C, Komdeur J (2006) The role of group size and environmental factors on survival in a cooperatively breeding tropical passerine. J Anim Ecol 75(6):1321–1329. CrossRefPubMedGoogle Scholar
  9. Buckner JC, Alfaro JWL, Rylands AB, Alfaro ME (2015) Biogeography of the marmosets and tamarins (Callitrichidae). Mol Phylogenet Evol 82:413–425. CrossRefPubMedGoogle Scholar
  10. Bueno MG, Iovine RO, Torres LN, Catão-Dias JL, Pissinatti A, Kierulff MC, Carvalho VM (2015) Pneumonia and bacteremia in a golden-headed lion tamarin (Leontopithecus chrysomelas) caused by Klebsiella pneumoniae subsp. pneumoniae during a translocation program of free-ranging animals in Brazil. J Vet Diagn Investig 27(3):387–391. CrossRefGoogle Scholar
  11. Burkart JM, Fehr E, Efferson C, van Schaik CP (2007) Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. P Natl Acad Sci USA 104(50):19762–19766. CrossRefGoogle Scholar
  12. Calcagno V, de Mazancourt C (2010) glmulti: an R package for easy automated model selection with (generalized) linear models,
  13. Canestrari D, Marcos JM, Baglione V (2008) Reproductive success increases with group size in cooperative carrion crows, Corvus corone corone. Anim Behav 75(2):403–416. CrossRefGoogle Scholar
  14. Catenacci LS, Pessoa MS, Nogueira-Filho SL, De Vleeschouwer KM (2016) Diet and feeding behavior of Leontopithecus chrysomelas (Callitrichidae) in degraded areas of the Atlantic forest of South-Bahia, Brazil. Int J Primatol 37(2):136–157. CrossRefGoogle Scholar
  15. Childress MJ, Lung MA (2003) Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics? Anim Behav 66(2):389–398. CrossRefGoogle Scholar
  16. Cleveland J, Snowdon CT (1984) Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus). Anim Behav 32(2):432–444. CrossRefGoogle Scholar
  17. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296(5565):69–72. CrossRefPubMedGoogle Scholar
  18. Clutton-Brock TH (2006) Cooperative breeding in mammals. In: Kappeler PM, van Schaik CP (eds) Cooperation in primates and humans: mechanisms and evolution. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 173–190. CrossRefGoogle Scholar
  19. Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293(5539):2446–2449. CrossRefPubMedGoogle Scholar
  20. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444(7122):1065–1068. CrossRefPubMedGoogle Scholar
  21. Courchamp F, Macdonald DW (2001) Crucial importance of pack size in the African wild dog Lycaon pictus. Anim Conserv 4(2):169–174. CrossRefGoogle Scholar
  22. Covas R, Deville A-S, Doutrelant C, Spottiswoode CN, Grégoire A (2011) The effect of helpers on the postfledging period in a cooperatively breeding bird, the sociable weaver. Anim Behav 81:121–126CrossRefGoogle Scholar
  23. Creel SR, Rabenold KN (1994) Inclusive fitness and reproductive strategies in dwarf mongooses. Behav Ecol 5(3):339–348. CrossRefGoogle Scholar
  24. de Almeida Rocha JM, De Vleeschouwer KM, Reis PP, Grelle CEV, Oliveira LC (2015) Do habitat use and interspecific association reflect predation risk for the golden-headed lion tamarin (Leontopithecus chrysomelas)? Int J Primatol 36(6):1198–1215. CrossRefGoogle Scholar
  25. De Vleeschouwer KM, Oliveira LC (2017) Report on the presence of a group of golden-headed lion tamarins (Leontopithecus chrysomelas), an endangered primate species in a rubber plantation in southern Bahia, Brazil. Primate Biol 4:61CrossRefGoogle Scholar
  26. De Vleeschouwer KM, Raboy BE (2013) Multilevel and transdisciplinary approaches to understanding endangered primates in complex landscapes: golden-headed lion tamarins in Southern Bahia, Brazil. In: Marsh L, Chapman C (eds) Primates in fragments. Springer, New York, pp 275–297. CrossRefGoogle Scholar
  27. Díaz-Muñoz SL (2011) Paternity and relatedness in a polyandrous nonhuman primate: testing adaptive hypotheses of male reproductive cooperation. Anim Behav 82(3):563–571. CrossRefGoogle Scholar
  28. Díaz-Muñoz SL (2016) Complex cooperative breeders: using infant care costs to explain variability in callitrichine social and reproductive behavior. Am J Primatol 78(3):372–387. CrossRefPubMedGoogle Scholar
  29. Dietz JM, Baker AJ (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Anim Behav 46(6):1067–1078. CrossRefGoogle Scholar
  30. Dietz JM, DeSousa SN, Billerbeck R (1996) Population dynamics of golden-headed lion tamarins Leontopithecus chrysomelas in Una Reserve, Brazil. Dodo 32:115–122Google Scholar
  31. Digby L (1995) Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus). Behav Ecol Sociobiol 37(1):51–61. CrossRefGoogle Scholar
  32. Digby LJ, Ferrari SF (1994) Multiple breeding females in free-ranging groups of Callithrix jacchus. Int J Primatol 15(3):389–397. CrossRefGoogle Scholar
  33. Dunbar R (1995) The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim Behav 50(4):1057–1070. CrossRefGoogle Scholar
  34. English S, Huchard E, Nielsen JF, Clutton-Brock TH (2013) Early growth, dominance acquisition and lifetime reproductive success in male and female cooperative meerkats. Ecol Evol 3(13):4401–4407. PubMedCentralCrossRefPubMedGoogle Scholar
  35. English S, Bateman AW, Mares R, Ozgul A, Clutton-Brock TH (2014) Maternal, social and abiotic environmental effects on growth vary across life stages in a cooperative mammal. J Anim Ecol 83(2):332–342. CrossRefPubMedGoogle Scholar
  36. Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11(6):633–639. CrossRefGoogle Scholar
  37. Fortin D, Fortin M-E, Beyer HL, Duchesne T, Courant S, Dancose K (2009) Group-size-mediated habitat selection and group fusion–fission dynamics of bison under predation risk. Ecology 90(9):2480–2490. CrossRefPubMedGoogle Scholar
  38. Garber PA, 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 Primatol 42(1):17–32. CrossRefGoogle Scholar
  39. Garber P, Porter L, Spross J, Fiore AD (2015) Tamarins: insights into monogamous and non-monogamous single female social and breeding systems. Am J Primatol 78(3):298–314. CrossRefPubMedGoogle Scholar
  40. Goldizen AW (1987) Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis). Behav Ecol Sociobiol 20(2):99–109. CrossRefGoogle Scholar
  41. 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):57–83.<57::AID-AJP6>3.0.CO;2-S CrossRefGoogle Scholar
  42. Guy C, Cassano CR, Cazarre L, De Vleeschouwer KM, Kierulff MCM, Neves LG, Oliveira LC, Tardio BMR, Zeigler SL, Raboy BE (2016) Evaluating landscape suitability for golden-headed lion tamarins (Leontopithecus chrysomelas) and Wied’s black tufted-ear marmosets (Callithrix kuhlii) in the Bahian Atlantic Forest. Trop Conserv Sci 9(2):735–757. CrossRefGoogle Scholar
  43. Hankerson S, Dietz J (2014) Predation rate and future reproductive potential explain home range size in golden lion tamarins. Anim Behav 96:87–95. CrossRefGoogle Scholar
  44. Hatchwell BJ, Komdeur J (2000) Ecological constraints, life history traits and the evolution of cooperative breeding. Anim Behav 59(6):1079–1086. CrossRefPubMedGoogle Scholar
  45. Hauber ME, Lacey EA (2005) Bateman’s principle in cooperatively breeding vertebrates: the effects of non-breeding alloparents on variability in female and male reproductive success. Integr Comp Biol 45(5):903–914. CrossRefPubMedGoogle Scholar
  46. Henry MD, Hankerson SJ, Siani JM, French JA, Dietz JM (2013) High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia). Horm Behav 63:675–683PubMedCentralCrossRefGoogle Scholar
  47. Heymann EW (1990) Social behaviour and infant carrying in a group of moustached tamarins, Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla, Peruvian Amazonia. Primates 31(2):183–196. CrossRefGoogle Scholar
  48. 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
  49. Heymann EW, Soini P (1999) Offspring number in pygmy marmosets, Cebuella pygmaea, in relation to group size and the number of adult males. Behav Ecol Sociobiol 46(6):400–404. CrossRefGoogle Scholar
  50. Hodge SJ, Manica A, Flower T, Clutton-Brock T (2008) Determinants of reproductive success in dominant female meerkats. J Anim Ecol 77(1):92–102. CrossRefPubMedGoogle Scholar
  51. Huck M, Löttker P, Böhle UR, Heymann EW (2005) Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax). Am J Phys Anthropol 127(4):449–464. CrossRefPubMedGoogle Scholar
  52. IUCN (2014) The IUCN red list of threatened species, version 2014.3,
  53. Jorgenson JT, Festa-Bianchet M, Lucherini M, Wishart WD (1993) Effects of body size, population density, and maternal characteristics on age at first reproduction in bighorn ewes. Can J Zool 71(12):2509–2517. CrossRefGoogle Scholar
  54. Keane B, Waser P, Creel S, Creel N, Elliott L, Minchella D (1994) Subordinate reproduction in dwarf mongooses. Anim Behav 47(1):65–75. CrossRefGoogle Scholar
  55. Key C, Ross C (1999) Sex differences in energy expenditure in non–human primates. Proc R Soc Lond B 266(1437):2479–2485. CrossRefGoogle Scholar
  56. Kierulff MCM, Rylands AB, Mendes SL, de Oliveira MM (2008) Leontopithecus chrysomelas. In: The IUCN red list of threatened species 2008,
  57. Koenig A (1995) Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus). Am J Primatol 35(4):311–317. CrossRefGoogle Scholar
  58. Koenig WD, Dickinson JL (2016) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge. CrossRefGoogle Scholar
  59. Koenig WD, Mumme RL, Pitelka FA (1983) Female roles in cooperatively breeding acorn woodpeckers. In: Wasser SK (ed) Social behavior of female vertebrates. Academic Press, New York, pp 235–261. CrossRefGoogle Scholar
  60. Legge S (2000) The effect of helpers on reproductive success in the laughing kookaburra. J Anim Ecol 69(4):714–724. CrossRefGoogle Scholar
  61. Leutenegger W (1973) Maternal-fetal weight relationships in primates. Folia Primatol 20(4):280–293. CrossRefPubMedGoogle Scholar
  62. Lewis R, Kappeler P (2005) Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. Am J Primatol 67(3):347–364. CrossRefPubMedGoogle Scholar
  63. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14(9):343–348. CrossRefPubMedGoogle Scholar
  64. Lukas D, Clutton-Brock T (2012a) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 279(1736):2151–2156. CrossRefGoogle Scholar
  65. Lukas D, Clutton-Brock T (2012b) Life histories and the evolution of cooperative breeding in mammals. Proc R Soc Lond B 279(1744):4065–4070. CrossRefGoogle Scholar
  66. MacNulty DR, Tallian A, Stahler DR, Smith DW (2014) Influence of group size on the success of wolves hunting bison. PLoS One 9(11):e112884. PubMedCentralCrossRefPubMedGoogle Scholar
  67. Magrath RD (2001) Group breeding dramatically increases reproductive success of yearling but not older female scrubwrens: a model for cooperatively breeding birds? J Anim Ecol 70(3):370–385. CrossRefGoogle Scholar
  68. McAdam AG, Millar JS (1999) The effects of dietary protein content on growth and maturation in deer mice. Can J Zool 77(11):1822–1828. CrossRefGoogle Scholar
  69. Mumme RL, Bowman R, Pruett MS, Fitzpatrick JW (2015) Natal territory size, group size, and body mass affect lifetime fitness in the cooperatively breeding Florida Scrub-Jay. Auk 132(3):634–646. CrossRefGoogle Scholar
  70. Nascimento AT, Nali C, da Fonseca GA (2014) Dispersal, group formation and kinship in the black-faced lion tamarin (Leontopithecus caissara). Folia Primatol 85(4):216–227. CrossRefPubMedGoogle Scholar
  71. Nievergelt CM, Martin RD (1998) Energy intake during reproduction in captive common marmosets (Callithrix jacchus). Physiol Behav 65(4-5):849–854. CrossRefGoogle Scholar
  72. 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):1–20. CrossRefGoogle Scholar
  73. Oliveira LC, Dietz JM (2011) Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest. Am J Primatol 73(9):852–860. CrossRefPubMedGoogle Scholar
  74. Oliveira LC, Neves LG, Raboy BE, Dietz JM (2011) Abundance of jackfruit (Artocarpus heterophyllus) affects group characteristics and use of space by golden-headed lion tamarins (Leontopithecus chrysomelas) in Cabruca agroforest. Environ Manag 48(2):248–262. CrossRefGoogle Scholar
  75. Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1–128,
  76. Price EC (1992) Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): the influence of age, sex, and reproductive status. Int J Primatol 13(2):125–141. CrossRefGoogle Scholar
  77. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  78. Raboy BE, Dietz JM (2004) Diet, foraging, and use of space in wild golden-headed lion tamarins. Am J Primatol 63(1):1–15. CrossRefPubMedGoogle Scholar
  79. Raboy BE, Christman MC, Dietz JM (2004) The use of degraded and shade cocoa forests by endangered golden-headed lion tamarins Leontopithecus chrysomelas. Oryx 38:75–83CrossRefGoogle Scholar
  80. Rapaport LG (2011) Progressive parenting behavior in wild golden lion tamarins. Behav Ecol 22(4):745–754. PubMedCentralCrossRefPubMedGoogle Scholar
  81. Richardson D, Burke T, Komdeur J (2003) Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler. J Evol Biol 16(5):854–861. CrossRefPubMedGoogle Scholar
  82. Rödel HG, Prager G, Stefanski V, von Holst D, Hudson R (2008) Separating maternal and litter-size effects on early postnatal growth in two species of altricial small mammals. Physiol Behav 93(4-5):826–834. CrossRefPubMedGoogle Scholar
  83. Rood JP (1990) Group size, survival, reproduction, and routes to breeding in dwarf mongooses. Anim Behav 39(3):566–572. CrossRefGoogle Scholar
  84. Rothe H, Koenig A, Darms K (1993) Infant survival and number of helpers in captive groups of common marmosets (Callithrix jacchus). Am J Primatol 30(2):131–137. CrossRefGoogle Scholar
  85. Russell AF (2004) Mammals: comparisons and contrasts. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 210–227. CrossRefGoogle Scholar
  86. Russell AF, Clutton-Brock TH, Brotherton PNM, Sharpe LL, McIlrath GM, Dalerum FD, Cameron EZ, Barnard JA (2002) Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta. J Anim Ecol 71(4):700–709. CrossRefGoogle Scholar
  87. Russell AF, Brotherton PNM, McIlrath GM, Sharpe LL, Clutton-Brock TH (2003) Breeding success in cooperative meerkats: effects of helper number and maternal state. Behav Ecol 14(4):486–492. CrossRefGoogle Scholar
  88. Sanchez S, Pelaez F, Gil-Bürmann C, Kaumanns W (1999) Costs of infant-carrying in the cotton-top tamarin (Saguinus oedipus). Am J Primatol 48(2):99–111.<99::AID-AJP2>3.0.CO;2-6 CrossRefPubMedGoogle Scholar
  89. Santos CV, French JA, Otta E (1997) Infant carrying behavior in callitrichid primates: Callithrix and Leontopithecus. Int J Primatol 18(6):889–907. CrossRefGoogle Scholar
  90. Sparkman AM, Adams J, Beyer A, Steury TD, Waits L, Murray DL (2011) Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus). Proc R Soc Lond B 278(1710):1381–1389. CrossRefGoogle Scholar
  91. Tardif SD, Carson RL, Gangaware BL (1986) Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus). Am J Primatol 11(2):103–110. CrossRefGoogle Scholar
  92. Therneau TM (2015) Survival: a package for survival analysis in S. R Package version 2:38 Google Scholar
  93. Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer, New York. CrossRefGoogle Scholar
  94. Verhulst S, Perrins C, Riddington R (1997) Natal dispersal of great tits in a patchy environment. Ecology 78(3):864–872.[0864:NDOGTI]2.0.CO;2 CrossRefGoogle Scholar
  95. Watts DP (1985) Relations between group size and composition and feeding competition in mountain gorilla groups. Anim Behav 33(1):72–85. CrossRefGoogle Scholar
  96. Wauters L, Dhondt AA (1989) Body weight, longevity and reproductive success in red squirrels (Sciurus vulgaris). J Anim Ecol 58(2):637–651. CrossRefGoogle Scholar
  97. Woxvold IA, Magrath MJ (2005) Helping enhances multiple components of reproductive success in the cooperatively breeding apostlebird. J Anim Ecol 74(6):1039–1050. CrossRefGoogle Scholar
  98. Wright PC (1990) Patterns of paternal care in primates. Int J Primatol 11(2):89–102. CrossRefGoogle Scholar
  99. Yamamoto ME, Albuquerque FS, Lopes NA, Ferreira ES (2008) Differential infant carrying in captive and wild common marmosets (Callithrix jacchus). Acta Ethol 11(2):95–99. CrossRefGoogle Scholar
  100. Yamamoto ME, Arruda M, Alencar AI, de Sousa MBC, Araújo A (2009) Mating systems and female–female competition in the common marmoset, Callithrix jacchus. In: Ford S, Porter L, Davis L (eds) The smallest anthropoids. Springer, Boston, pp 119–133. CrossRefGoogle Scholar
  101. Zeigler SL, De Vleeschouwer KM, Raboy BE (2013) Assessing extinction risk in small metapopulations of golden-headed lion tamarins (Leontopithecus chrysomelas) in Bahia State, Brazil. Biotropica 45(4):528–535. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Laura A. Heslin Piper
    • 1
    Email author
  • James M. Dietz
    • 2
    • 3
  • Becky E. Raboy
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  2. 2.Program in Behavior, Ecology, Evolution, & SystematicsUniversity of MarylandCollege ParkUSA
  3. 3.Save the Golden Lion TamarinSilver SpringUSA

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