Does behavioral flexibility contribute to successful play among juvenile rhesus macaques?

Abstract

Animal play often resembles aggressive interactions, making it difficult for players and third parties to distinguish between the two types of behavior or to concur on aspects of play. In this sense, social play involves some degree of social risk, and players may benefit by behaving flexibly particularly when playing with unmatched partners. Here, we ask (1) whether social play among free-ranging juvenile rhesus monkeys (Macaca mulatta) is more likely to fail when partners are unmatched by sex, age, rank/kinship, or when their mothers are nearby and (2) whether juveniles behave flexibly to overcome these social risks. We first identify the factors contributing to play failure, by describing social attributes that are associated with negative outcomes of play. We then compare behavior for matched vs. unmatched partners by examining tendencies to (1) refrain from play, (2) engage in short play durations, and (3) use enhanced play signaling. Males were responsive to several play failure factors; they disproportionately used enhanced play signaling and played for short durations with unmatched partners, suggesting that they have social knowledge that supports attempts to cope flexibly with diverse play partners/situations. Females were less actively responsive to these factors. Although they refrained from playing with many unmatched partners, they did not adjust play tactics to the same degree. These sex differences may be related to differences in life histories; males preparing to disperse eventually may benefit from expanding their social networks through play, while philopatric females may have less need to do so.

Significance statement

While social play provides many benefits for animals, play attempts may also involve risks of failure, from refusal by partners to escalation into aggression, particularly when players are mismatched physically or socially. Growing juveniles in despotic societies may be especially vulnerable to such risk. We ask whether juvenile rhesus monkeys behave flexibly when playing with mismatched partners in a way that may help them overcome such risks. We demonstrate that males, who typically emigrate from their natal groups, are indeed sensitive to mismatches in social characteristics or situations; they play in short durations and enhance their play signaling during play sessions involving mismatches. Females, who permanently remain in their maternal groups are less responsive. These sex differences suggest that juvenile males may hone social skills via playful interaction in preparation for emigration, while females have less need to do so.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aldis O (1975) Play fighting. Academic Press, New York

    Google Scholar 

  2. Altmann SA (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann N Y Acad Sci 102:338–435

    CAS  PubMed  Article  Google Scholar 

  3. Altmann SA (1967) The structure of primate social communication. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 325–362

    Google Scholar 

  4. Antonacci D, Norscia I, Palagi E (2010) Stranger to familiar: wild strepsirhines manage xenophobia by playing. PLoS One 5:e13218

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  5. Aureli F, Das M, Veenema HC (1997) Differential kinship effect on reconciliation in three species of macaques (Macaca fascicularis, M. fuscata, and M. sylvanus). J Comp Psychol 111:91–99

    CAS  PubMed  Article  Google Scholar 

  6. Baldwin JD (1969) The ontogeny of social behavior of squirrel monkeys (Saimiri sciureus) in a seminatural environment. Folia Primatol 11:35–79

    CAS  PubMed  Article  Google Scholar 

  7. Baldwin JD, Baldwin JJ (1972) The ecology and behavior of squirrel monkeys (Saimiri oerstedi) in a natural forest in western Panama. Folia Primatol 18:161–184

    CAS  PubMed  Article  Google Scholar 

  8. Baldwin JD, Baldwin JI (1977) The role of learning phenomena in the ontogeny of exploration and play. In: Chevalier-Skolnikoff S, Poirier FE (eds) Primate Biosocial Development: Biological, Social, and Ecological Determinants. Garland, New York, pp 343–406

    Google Scholar 

  9. Bardi M, Borgognini-Tarli SM (2006) Social play and solitary play in immature macaques: sex differences and maternal role (abstract). Folia Primatol 77:284

    Google Scholar 

  10. Bateson G (1972) A theory of play and fantasy. In: Bateson G (ed) Steps to an ecology of mind. Ballantine Books, New York, pp 177–193

    Google Scholar 

  11. Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs, Canis familiaris. Anim Behav 73:489–499

    Article  Google Scholar 

  12. Bekoff M (1972) The development of social interaction, play, and metacommunication in mammals: an ethological perspective. Q Rev Biol 47:412–434

    Article  Google Scholar 

  13. Bekoff M (1974) Social play and play soliciting by infant canids. Am Zool 14:323–340

    Article  Google Scholar 

  14. Bekoff M (1995) Play signals as punctuation: the structure of social play in canids. Behaviour 132:419–429

    Article  Google Scholar 

  15. Bekoff M, Allen C (1998) Intentional communication and social play: how and why animals negotiate and agree to play. In: Bekoff M, Byers JA (eds) Animal play: evolutionary, comparative, and ecological approaches. Cambridge University Press, Cambridge, pp 97–114

    Google Scholar 

  16. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  17. Berman CM (1978) Social relationships among free-ranging infant rhesus monkey. Dissertation, University of Cambridge

  18. Berman CM (1980) Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Anim Behav 28:860–873

    Article  Google Scholar 

  19. Biben M (1986) Individual- and sex-related strategies of wrestling play in captive squirrel monkeys. Ethology 71:229–241

    Article  Google Scholar 

  20. Biben M (1998) Squirrel monkey play fighting: making the case for a cognitive training function for play. In: Bekoff M, Byers JA (eds) Animal play: evolutionary, comparative, and ecological approaches. Cambridge University Press, Cambridge, pp 161–182

    Google Scholar 

  21. Box HO (1975) Quantitative studies of behavior within captive groups of marmoset monkeys (Callithrix jacchus). Primates 16:155–174

    Article  Google Scholar 

  22. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer, Sunderland

    Google Scholar 

  23. Brennan J, Anderson JR (1988) Primates, varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta). Primates 29:353–360

    Article  Google Scholar 

  24. Burghardt GM (2005) The genesis of animal play: testing the limits. MIT Press, Cambridge

    Google Scholar 

  25. Byers JA (1980) Play partner preferences in Siberian ibex, Capra ibex sibirica. Ethology 53:23–40

    Google Scholar 

  26. Caine N, Mitchell G (1979) The relationship between maternal rank and companion choice in immature macaques (Macaca mulatta and M. radiate). Primates 20:583–590

    Article  Google Scholar 

  27. Cao TT, Hyland KM, Malechuk A, Lewis LA, Schneider SS (2009) The effect of repeated vibration signals on worker behaviour in established and newly founded colonies of the honey bee, Apis mellifera. Behav Ecol Sociobiol 63:521–529

    Article  Google Scholar 

  28. Chauhan A, Pitra RS (2010) Agonistic interactions between humans and two species of monkeys (rhesus monkey Macaca mulatta and hanuman langur Semnopithecus entellus) in Shimla, Himachal Pradesh. J Psychol 1:9–14

    Article  Google Scholar 

  29. Chamove A, Harlow HF, Mitchell G (1967) Sex differences in the infant-directed behavior of preadolescent rhesus monkeys. Child Dev 38:329–335

    CAS  PubMed  Article  Google Scholar 

  30. Cheney DL (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging baboons. Behav Ecol Sociobiol 2:303–318

    Article  Google Scholar 

  31. Cheney DL (1978) The play partner of immature baboon. Anim Behav 26:1038–1050

    Article  Google Scholar 

  32. Cheney DL, Seyfarth RM (1977) Behavior of immature and adult male baboons during inter-group encounters. Nature 269:404–406

    Article  Google Scholar 

  33. Clark FE (2011) Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management. Am J Primatol 73:748–757

    PubMed  Article  Google Scholar 

  34. Cordoni G, Palagi E (2011) Ontogenetic trajectories of chimpanzee social play: similarities with humans. PLoS One 6:e27344

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Deutsch JC, Lee PC (1991) Dominance and feeding competition in captive rhesus monkeys. Int J Primatol 12:615–628

    Article  Google Scholar 

  36. DeVore IT (1963) Mother-infant relations in baboons. In: Rheingold H (ed) Maternal behavior in mammals. Wiley, New York, pp 305–335

    Google Scholar 

  37. Dolhinow P (1999) Play: a critical process in the developmental system. In: Dolhinow P, Fuentes A (eds) The Non-Human Primates. Mayfield Publishing Co., Mountain Oven, pp 231–236

    Google Scholar 

  38. Eaton GG, Johnson DF, Glick BB, Worlein JM (1986) Japanese macaque (Macaca fusucata) social development: sex differences in juvenile behavior. Primates 27:141–150

    Article  Google Scholar 

  39. Ehardt CL, Bernstein IS (1987) Patterns of affiliation among immature rhesus monkeys (Macaca mulatta). Am J Primatol 13:255–269

    Article  Google Scholar 

  40. Fagen R (1981) Animal play behavior. Oxford University Press, New York

    Google Scholar 

  41. Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 9:425–441

    Google Scholar 

  42. Fedigan LM (1972) Social and solitary play in a colony of vervet monkeys (C. aethiops). Primates 13:347–364

    CAS  PubMed  Article  Google Scholar 

  43. Flack JC, Jeannotte LA, de Waal FBM (2004) Play signaling and the perception of social rules by juvenile chimpanzees (Pan troglodytes). J Comp Psychol 118:149–159

    PubMed  Article  Google Scholar 

  44. Fröhlich M, Wittig RM, Pika S (2016) Play-solicitation gestures in chimpanzees in the wild: flexible adjustment to social circumstances and individual matrices. R Soc Open Sci 3:160278

    PubMed  PubMed Central  Article  Google Scholar 

  45. Glick BB, Eaton GG, Johnson DF, Worlein J (1986) Development of partner preferences in Japanese macaques (Macaca fuscata): effects of gender and kinship during the second year of life. Int J Primatol 7:467–479

    Article  Google Scholar 

  46. Gouzoules H, Gouzoules S, Marler P (1984) Rhesus monkey (Macaca mulatta) screams: representational signalling in the recruitment of agonistic aid. Anim Behav 32:182–193

    Article  Google Scholar 

  47. Harlow HF (1969) Age-mate or peer affectional system. Adv Stud Behav 2:333–383

    Article  Google Scholar 

  48. Hassett JM, Rupp HA, Wallen K (2010) Social segregation in male, but not in female yearling rhesus macaques (Macaca mulatta). Am J Primatol 72:87–92

    PubMed  PubMed Central  Google Scholar 

  49. Hausfater G (1972) Intergroup behaviour of free-ranging rhesus monkeys (Macaca mulatta). Folia Primatol 18:78–107

    CAS  PubMed  Article  Google Scholar 

  50. Hayaki H (1983) The social interactions of juvenile Japanese monkeys on Koshima islet. Primates 24:139–153

    Article  Google Scholar 

  51. Hayaki H (1985) Social play of juvenile and adolescent chimps in the Mahale mountains national park, Tanzania. Primates 26:343–360

    Article  Google Scholar 

  52. Hernandez-Pacheco R, Delgado DL, Ralins RG, Kessler MJ, Ruiz-Lambides AV, Maldonado E, Sabat AM (2016) Managing the Cayo Santiago Rhesus Macaque population: the role of density. Am J Primatol 78:167–181

    PubMed  Article  Google Scholar 

  53. van Hooff JARAM (1972) A comparative approach to the phylogeny of laughter and smiling. In: Hinde RA (ed) Nonverbal communication. Cambridge University Press, Cambridge, pp 209–241

    Google Scholar 

  54. Kahlenberg SM, Wrangham RW (2010) Sex differences in chimpanzees’ use of sticks as play objects resemble those of children. Curr Biol 20:R1067–R1068

    CAS  PubMed  Article  Google Scholar 

  55. Katsukake N, Castles DN (2001) Reconciliation and variation in post-conflict stress in Japanese macaques (Macaca fuscata fuscata): testing the integrated hypothesis. Anim Cogn 4:259–268

    Article  Google Scholar 

  56. Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS ONE 11:e015845

    Article  CAS  Google Scholar 

  57. Kummer H (1968) Social organization of hamadryas baboons. University of Chicago Press, Chicago

    Google Scholar 

  58. Lancaster JB (1971) Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol 15:161–182

    Article  Google Scholar 

  59. Levy J (1979) Play behavior and its decline during development in rhesus monkeys (Macaca mulatta). Doctoral dissertation, University of Chicago

  60. Lewis KP (2005) Social play in the great apes. In: Pellegrini AD, Smith PK (eds) The nature of play: great apes and humans. Guilford, New York, pp 27–53

    Google Scholar 

  61. Lovejoy J, Wallen K (1988) Sexually dimorphic behavior in group-housed rhesus monkeys (Macaca mulatta) at 1 year of age. Psychobiology 16:348–356

    Google Scholar 

  62. Maestripieri D, Ross SR (2004) Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure. Am J Phys Anthropol 123:52–61

    PubMed  Article  Google Scholar 

  63. Maestripieri D, Hoffman CL (2012) Behavior and social dynamics of rhesus macaques on Cayo Santiago. In: Wang Q (ed) Bones, Genetics, and Behavior of Rhesus Macaques. Springer, Berlin, pp 247–262

    Google Scholar 

  64. Mancini G, Palagi E (2009) Play and social dynamics in a captive herd of gelada baboons (Theropithecus gelada). Behav Process 82:286–292

    Article  Google Scholar 

  65. Martin P, Caro TM (1985) On the functions of play and its role in behavioral development. Adv Stud Behav 15:59–103

    Article  Google Scholar 

  66. Meaney MJ, Stewart J, Beatty WW (1985) Sex differences in social play: the socialization of sex roles. Adv Study Behav 15:1–58

    Article  Google Scholar 

  67. Mendoza-Granados D, Sommer V (1995) Play in chimpanzees of the Arnhem zoo: self-serving compromises. Primates 36:57–68

    Article  Google Scholar 

  68. Miller MN, Byers JA (1991) Energetic cost of locomotor play in pronghorn fawns. Anim Behav 41:1007–1013

    Article  Google Scholar 

  69. Montgomery SH (2014) The relationship between play, brain growth and behavioural flexibility in primates. Anim Behav 90:281–286

    Article  Google Scholar 

  70. Nadler RD, Wallis J, Roth-Meyer C, Cooper RW, Baulieu EE (1987) Hormones and behavior of prepubertal chimpanzees. Horm Behav 21:118–131

    CAS  PubMed  Article  Google Scholar 

  71. de Oliveira CR, Ruiz-Miranda CR, Kleiman DG, Beck BB (2003) Play behavior in juvenile golden lion tamarins (Callitrichidae: primates): organization in relation to costs. Ethology 109:593–612

    Article  Google Scholar 

  72. Owens NW (1975a) Social play behavior in free-living baboons, Papio anubis. Anim Behav 23:387–408

    Article  Google Scholar 

  73. Owens NW (1975b) A comparison of aggressive play and aggression in free-living baboons, Papio anubis. Anim Behav 23:757–765

    CAS  PubMed  Article  Google Scholar 

  74. Palagi E (2006) Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): implications for natural social systems and interindividual relationships. Am J Phys Anthropol 129:418–426

    PubMed  Article  Google Scholar 

  75. Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75:887–896

    Article  Google Scholar 

  76. Palagi E (2009) Adult play fighting and potential role of tail signals in ringtailed lemurs (Lemur catta). J Comp Psychol 123:1–9

    PubMed  Article  Google Scholar 

  77. Palagi E, Cordoni G (2012) The right time to happen: play developmental divergence in the two Pan species. PLoS One 7:e52767

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. Palagi E, Paoli T (2007) Play in adult bonobos (Pan paniscus): modality and potential meaning. Am J Phys Anthropol 134:219–225

    PubMed  Article  Google Scholar 

  79. Palagi E, Cordoni G, Borgognini Tarli S (2004) Immediate and delayed benefits of play behaviour: new evidence from chimpanzees (Pan troglodytes). Ethology 110:949–962

    Article  Google Scholar 

  80. Palagi E, Antonacci D, Cordoni G (2007) Fine-tuning of social play by juvenile lowland gorillas (Gorilla gorilla gorilla). Dev Psychobiol 49:433–445

    PubMed  Article  Google Scholar 

  81. Palagi E, Burghardt GM, Smuts B, Cordoni G, Dall’Olio S, Fouts HN, Rehakova-Petru M, Siviy SM, Pellis SM (2016) Rough-and-tumble play as a window on animal communication. Biol Rev 91:311–327

    PubMed  Article  Google Scholar 

  82. Paquette D (1994) Fighting and playfighting in captive adolescent chimpanzees. Aggress Behav 20:49–65

    Article  Google Scholar 

  83. Pellegrini AD (2009) The role of play in human development. Oxford University Press, Oxford

    Google Scholar 

  84. Pellegrini AD, Dupuis D, Smith PK (2007) Play in evolution and development. Dev Rev 27:261–276

    Article  Google Scholar 

  85. Pellis SM, Iwaniuk AN (1999) The problem of adult play-fighting: a comparative analysis of play and courtship in primates. Ethology 105:783–806

    Article  Google Scholar 

  86. Pellis SM, Iwaniuk AN (2000) Adult-adult play in primates: comparative analyses of its origin, distribution and evolution. Ethology 106:1083–1104

    Article  Google Scholar 

  87. Pellis SM, Pellis VC (1997) Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggress Behav 23:41–57

    Article  Google Scholar 

  88. Pellis SM, Pellis VC (1998) The structure-function interface in the analysis of play fighting. In: Bekoff M, Byers JA (eds) Animal play: evolutionary, comparative, and ecological perspectives. Cambridge University Press, Cambridge, pp 115–140

    Google Scholar 

  89. Pellis SM, Pellis VC (2006) Play and the development of social engagement: a comparative perspective. In: Marshall PJ, Fox NA (eds) The Development of Social Engagement: Neurobiological Perspectives. Oxford University Press, Oxford, pp 247–274

    Google Scholar 

  90. Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Publications, Oxford

    Google Scholar 

  91. Pellis SM, Pellis VC, Bell HC (2010) The function of play in the development of the social brain. Am J Play 2:278–296

    Google Scholar 

  92. Pereira ME (1984) Age changes and sex differences in the social behavior of juvenile yellow baboons (Papio cynocephalus). Doctoral dissertation. University of Chicago, Chicago, IL

  93. Pereira ME, Preisser MC (1998) Do strong primate players “self-handicap” during competitive social play? Folia Primatol 69:177–180

    Article  Google Scholar 

  94. Petit O, Bertrand F, Thierry B (2008) Social play in crested and Japanese macaques: testing the covariation hypothesis. Dev Psychobiol 50:399–407

    CAS  PubMed  Article  Google Scholar 

  95. Preuschoft S (1992) “Laughter” and “smile” in barbary macaques (Macaca sylvanus). Ethology 91:220–236

    Article  Google Scholar 

  96. Radhakrishna S, Huffman MA, Sinha A (2013) The macaque connection: cooperation and conflict between humans and macaques. Springer, New York

    Google Scholar 

  97. Reinhart CJ, Pellis VC, Thierry B, Gauthier C, Vanderlaan DP, Vasey PL, Pellis SM (2010) Targets and tactics of play fighting: competitive versus cooperative styles of play in Japanese and Tonkean macaques. Int J Comp Psychol 23:166–200

    Google Scholar 

  98. Rijksen HD (1978) A field study on Sumatran orangutans (Pongo pygmaeus abelii, lesson 1827): ecology, behavior, and conservation. Wageningen, H. Veenman and Zonen

    Google Scholar 

  99. Rodman PS, Mitani JC (1987) Orangutans: sexual dimorphism in a solitary species. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate Societies. University of Chicago Press, Chicago, pp 146–154

    Google Scholar 

  100. Sade DS (1972) A longitudinal study of social behavior in rhesus monkeys. In: Tuttle R (ed) The functional and evolutionary biology of primates. Aldine Publishing Co., Chicago, pp 378–398

    Google Scholar 

  101. Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698

    CAS  PubMed  Article  Google Scholar 

  102. Smith PK, Boulton M (1990) Rough-and-tumble play, aggression, and dominance: perceptions and behavior in children’s encounters. Hum Dev 33:271–282

    Article  Google Scholar 

  103. Smith JE, Chung LK, Blumstein DT (2013) Ontogeny and symmetry of social partner choice among free-living yellowbellied marmots. Anim Behav 85:715–725

    Article  Google Scholar 

  104. Spijkerman RP, Dienske H, van Hooff JARAM, Jens W (1996) Differences in variability, interactivity and skills in social play of young chimpanzees living in peer groups and in a large family zoo group. Behaviour 133:717–739

    Article  Google Scholar 

  105. Špinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168

    PubMed  Article  Google Scholar 

  106. Symons D (1978) Play and aggression: a study of rhesus monkeys. Columbia University Press, New York

    Google Scholar 

  107. Tacconi G, Palagi E (2009) Play behavioural tactics under space reduction: social changes in bonobos, Pan paniscus. Anim Behav 78:469–476

    Article  Google Scholar 

  108. Thierry B (2006) The macaques: a double-layered social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 224–239

  109. Thompson KV (1996) Behavioral development and play. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, Harris H (eds) Wild Mammals in Captivity: Principles and Techniques. University of Chicago Press, Chicago, pp 352–371

    Google Scholar 

  110. Thompson KV (1998) Self assessment in juvenile play. In: Bekoff M, Byers JA (eds) Animal Play: Evolutionary. Comparative and Ecological Perspectives. Cambridge University Press, Cambridge, pp 183–204

    Google Scholar 

  111. Todt D (1997) The codex of social play: a system of rules that can prevent in-group violence. Schriften Rechtspsychol 3:305–315

    Google Scholar 

  112. Tomasello M, Call J (1997) Primate Cognition. Oxford University Press, New York

    Google Scholar 

  113. Ward C, Trisko R, Smuts BB (2009) Third-party interventions in dyadic play between littermates of domestic dogs, Canis lupus familiaris. Anim Behav 78:1153–1160

    Article  Google Scholar 

  114. Watson DM (1993) The play associations of rednecked wallabies (Macropus rufogriseus banksianus) and relation to other social contexts. Ethology 94:1–20

    Article  Google Scholar 

  115. Watson DM, Croft DB (1996) Age-related differences in playfighting strategies of captive male red-necked wallabies (Macropus rufogriseus banksianus). Ethology 102:33–346

    Google Scholar 

  116. Widdig A, Langos D, Kulik L (2016) Sex differences in kin bias at maturation: male rhesus macaques prefer paternal kin prior to natal dispersal. Am J Primatol 78:78–91

    PubMed  Article  Google Scholar 

  117. Yanagi A, Berman CM (2014a) Body signals during social play in free-ranging rhesus macaques (Macaca mulatta): a systematic analysis. Am J Primatol 76:168–179

    PubMed  Article  Google Scholar 

  118. Yanagi A, Berman CM (2014b) Functions of multiple play signals in free-ranging juvenile rhesus macaques (Macaca mulatta). Behaviour 151:1983–2014

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the National Science Foundation (Award ID 0622357), the Leakey Foundation, and Mark Diamond Research Fund, the Department of Anthropology and the Graduate Program in Evolution, Ecology, and Behavior at the State University of New York at Buffalo for the funds we received for this study. We are also grateful to the Caribbean Primate Research Center, University of Puerto Rico, for permission to conduct research at Cayo Santiago (Protocol No. A3460107), to the staff for their friendly assistance, and to the resident scientists at the time of the study, Melissa Gerald and Adaris Mas Rivera. This study would not have been possible without our field assistants, Jessika Ava and Julien De Leval. We would like to give special thanks to Anja Widdig for providing AY a valuable fieldwork experience on Cayo Santiago and AY’s dissertation committee members, Ted Steegmann and Eduardo Mercado, for their helpful suggestions. Finally, we wish to thank the associate editor and two anonymous reviewers who helped us improve this manuscript.

Funding

This study was funded by the National Science Foundation (AY and CMB), the Leakey Foundation (AY and CMB), and Mark Diamond Fund, Department of Anthropology and Graduate Program in Evolution, Ecology, and Behavior, The State University of New York at Buffalo (AY).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Akie Yanagi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Institutional Animal Care and Use Committees (IACUC) at the Caribbean Primate Research Center, University of Puerto Rico (Protocol No. A3460107), as well as the State University of New York at Buffalo (Protocol No. N/A).

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Additional information

Communicated by E. Huchard

Electronic supplementary material

ESM 1

(DOCX 48 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yanagi, A., Berman, C.M. Does behavioral flexibility contribute to successful play among juvenile rhesus macaques?. Behav Ecol Sociobiol 71, 156 (2017). https://doi.org/10.1007/s00265-017-2377-2

Download citation

Keywords

  • Animal social play
  • Play signals
  • Juvenile primates
  • Despotic primates
  • Sex differences