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Not just for fun! Social play as a springboard for adult social competence in human and non-human primates

  • Elisabetta Palagi
Review
Part of the following topical collections:
  1. An evolutionary perspective on the development of primate sociality

Abstract

Play is one of the most difficult behaviors to quantify and for this reason, its study has had a very rocky history. Social play is ephemeral, difficult to distinguish from the other so-called serious behaviors, not so frequent (especially in sexually mature subjects), fast, and complex to describe. Due to its multifaceted nature, it has often been considered as a wastebasket category that has included all kinds of the behaviors not showing any immediate, obvious goal. Yet, play is widespread across the whole primate order and can have a strong impact on the development of cognitive, psychological, and social skills of many species, including humans. Unlike functional behaviors that are specifically and economically performed to reduce uncertainty and to increase the opportunity to gain resources, play seems to introduce and increase uncertainty, creating new challenges for the animals. For this reason, social play has been hypothesized to be the engine of behavioral innovation in ontogeny. From the first mild and gentle interactions with the mother to the most sophisticated play fighting sessions and acrobatic action sequences with peers, play represents for juveniles (and not only for them!) a window onto the social and physical environment. In this review, I focus on social play and its relation to adult social competence. By playing, juveniles acquire competence to manage interactions with conspecifics, enlarge their social networks, and test their physical power and motor skills (i.e., long-term benefits). At the same time, I propose the view that play—due to its plastic and versatile nature—can be used in an opportunistic way, as a joker behavior, throughout life to strategically obtain short-term or immediate benefits. I put forward the hypothesis that, during ontogeny, the joker function of play can be modulated according to the differing inter-individual relationships present in the diverse societies, characterizing the primate order.

Keywords

Play fighting Ontogenetic and evolutionary pathways Facial mimicry Emotional sharing Tolerant species 

Notes

Acknowledgements

I am grateful to Federica Amici and Anja Widdig for their kind invitation to contribute to this Topical Collection and the reviewers for improving the manuscript quality; I wish to thank Giada Cordoni for sharing most of the concepts of tolerance, play, cooperation, and fairness in animals; Ivan Norscia for a critical review of the manuscript and Nicola Cau for helping with the translation from Greek of the Eraclitus’ epigraph. Finally, I am grateful to all the colleagues of the NIMBioS Working Group (University of Tennessee) (www.nimbios.org/workinggroups/WG_play) for the stimulating input on one of the most controversial behaviors an ethologist can come across.

Compliance with ethical standards

Conflict of interest

The author declares that she has no conflict of interest.

Informed consent

For this type of study, formal consent is not required.

Ethical approval

This article does not contain studies with human participants or animals performed by any of the authors.

References

  1. Adams MJ, Majolo B, Ostner J, Schülke O, De Marco A, Thierry B, Engelhardt A, Widdig A, Gerald MS, Weiss A (2015) Personality structure and social style in macaques. J Pers Soc Psychol 109:338–353.  https://doi.org/10.1037/pspp0000041 PubMedGoogle Scholar
  2. Adamson L, Bakeman R (1984) Mother’s communication acts: changes during infancy. Infant Behav Dev 7:467–487Google Scholar
  3. Allen WL, Stevens M, Higham JP (2014) Character displacement of Cercopithecini primate visual signals. Nat Commun 5:4266.  https://doi.org/10.1038/ncomms5266 PubMedPubMedCentralGoogle Scholar
  4. Antonacci D, Norscia I, Palagi E (2010) Stranger to familiar: wild strepsirhines manage xenophobia by playing. PLoS One 5:e13218.  https://doi.org/10.1371/journal.pone.0013218 PubMedPubMedCentralGoogle Scholar
  5. Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs, Canis familiaris. Anim Behav 73:489–499.  https://doi.org/10.1016/j.anbehav.2006.09.006 Google Scholar
  6. Behncke I (2015) Play in the Peter Pan ape. Curr Biol 25:R24–R27PubMedGoogle Scholar
  7. Bekoff M (1995) Play signals as punctuation: the structure of social play in canids. Behaviour 132:419–429.  https://doi.org/10.1163/156853995X00649 Google Scholar
  8. Bekoff M (2001) Social play behavior: cooperation, fairness, trust, and the evolution of morality. J Conscious Stud 8:81–90Google Scholar
  9. 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 perspectives. Cambridge University Press, Cambridge, pp 97–114Google Scholar
  10. Berghänel A, Schulke O, Ostner J (2015) Locomotor play drives motor skill acquisition at the expense of growth: a life history trade-off. Sci Adv 1:e1500451PubMedPubMedCentralGoogle Scholar
  11. Bigelow AE, MacLean K, Proctor J (2004) The role of joint attention in the development of infants’ play with objects. Dev Sci 7:518–526PubMedGoogle Scholar
  12. Blumstein DT, Chung LK, Smith JE (2013) Early play may predict later dominance relationships in yellow-bellied marmots (Marmota flaviventris). Proc R Soc B 280:20130485.  https://doi.org/10.1098/rspb.2013.0485 PubMedGoogle Scholar
  13. Burghardt GM (1973) Instinct and innate behavior: toward an ethological psychology. In: Nevin JA, Reynolds GS (eds) The study of behavior: learning, motivation, emotion, and instinct. Scott Foresman, Glenview, pp 322–400Google Scholar
  14. Burghardt GM (2005) The genesis of animal play: testing the limits. MIT Press, CambridgeGoogle Scholar
  15. Burghardt GM (2017) The origins, evolution and interconnections of play and ritual: setting the stage. In: Renfrew C, Morley I, Boyd M (eds) Ritual, play and belief, in evolution and early human societies. Cambridge University Press, Cambridge, pp 23–39Google Scholar
  16. Butovskaya M (2004) Social space and degrees of freedom. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 182–185Google Scholar
  17. Calvo MG, Gutiérrez-García A, Avero P, Lundqvist D (2013) Attentional mechanisms in judging genuine and fake smiles: eye-movement patterns. Emotion 13:792–802.  https://doi.org/10.1037/a0032317 PubMedGoogle Scholar
  18. Ciani F, Dall'Olio S, Stanyon R, Palagi E (2012) Social tolerance and adult play in macaque societies: a comparison with different human cultures. Anim Behav 84:1313–1322.  https://doi.org/10.1016/j.anbehav.2012.09.002 Google Scholar
  19. Clay Z, de Waal FBM (2013) Bonobos respond to distress in others: consolation across the age spectrum. PLoS One 8:e55206.  https://doi.org/10.1371/journal.-pone.0055206 PubMedPubMedCentralGoogle Scholar
  20. Clay Z, Palagi E, de Waal FBM (2018) Ethological approaches to empathy in primates. In: Meyza KZ, Knapska E (eds) Neuronal correlates of empathy. Elsevier, San Diego (in press; ISBN:9780128053973)Google Scholar
  21. Cordoni G, Palagi E (2011) Ontogenetic trajectories of chimpanzee social play: similarities with humans. PLoS One 6:e27344.  https://doi.org/10.1371/journal.pone.0027344 PubMedPubMedCentralGoogle Scholar
  22. Cordoni G, Palagi E (2013) Smiling and primate play faces: origins and function. Hum Evol 28:1–12Google Scholar
  23. Cordoni G, Demuru E, Ceccarelli E, Palagi E (2016) Play, aggressive conflict and reconciliation in pre-school children: what matters? Behaviour 153:1075–1102.  https://doi.org/10.1163/1568539X-0003397 Google Scholar
  24. Cordoni G, Norscia I, Bobbio M, Palagi E (2018) Differences in play can illuminate differences in affiliation: a comparative study on chimpanzees and gorillas. PLoS One 13:e0193096.  https://doi.org/10.1371/journal.pone.0193096 PubMedPubMedCentralGoogle Scholar
  25. Demuru E, Ferrari PF, Palagi E (2015) Emotionality and intentionality in bonobo playful communication. Anim Cogn 18:333–344.  https://doi.org/10.1007/s10071-014-0804-6 PubMedGoogle Scholar
  26. Dettmer AM, Kaburu SS, Simpson EA et al (2016) Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nat Commun 7:11940.  https://doi.org/10.1038/ncomms11940 PubMedPubMedCentralGoogle Scholar
  27. Dobson SD (2012) Coevolution of facial expression and social tolerance in macaques. Am J Primatol 74:229–235.  https://doi.org/10.1002/ajp.21991 PubMedGoogle Scholar
  28. Fagen R (1993) Primate juvenile and primate play. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. Oxford University Press, Oxford, pp 182–196Google Scholar
  29. Fairbanks LA (2000) The developmental timing of primate play: a neural selection model. In: Parker ST, Langer J, McKinney ML (eds) Biology, brains, and behavior: the evolution of human development. School of American research press, Santa Fe, pp 131–158Google Scholar
  30. Feldman R, Greenbaum CW (1997) Affect regulation and synchrony in mother–infant play as precursors to the development of symbolic competence. Infant Ment Health J 18:4–23Google Scholar
  31. Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009a) Reciprocal face-to-face communication between rhesus macaque mothers and their infants. Curr Biol 19:1768–1772.  https://doi.org/10.1016/j.cub.2009.08.055 PubMedPubMedCentralGoogle Scholar
  32. Ferrari PF, Bonini L, Fogassi L (2009b) From monkey mirror neurons to primate behaviours: possible ‘direct’ and ‘indirect’ pathways. Phil Trans R Soc B 364:2311–2323.  https://doi.org/10.1098/rstb.2009.0062 PubMedGoogle Scholar
  33. Fischer A, Hess U (2017) Mimicking emotions. Curr Opin Psychol 17:151–155.  https://doi.org/10.1016/j.copsyc.2017.07.008 PubMedGoogle Scholar
  34. Flack JC, de Waal FBM (2004) Dominance style, social power, and conflict management: a conceptual framework. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 155–182Google Scholar
  35. Flack JC, Jeannotte LA, de Waal FBM (2004) Play signalling and the perception of social rules by juvenile chimpanzees (Pan troglodytes). J Comp Physiol 118:149–159.  https://doi.org/10.1037/0735-7036.118.2.149 Google Scholar
  36. Forcada-Guex M, Pierrehumbert B, Borghini A, Moessinger A, Muller-Nix C (2006) Early dyadic patterns of mother-infant interactions and outcomes of prematurity at 18 months. Pediatrics 118:e107–e114PubMedGoogle Scholar
  37. Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Phil Trans R Soc B 367:1785–1801.  https://doi.org/10.1098/rstb.2011.0213 PubMedGoogle Scholar
  38. Furuichi T (2011) Female contribution to the peaceful nature of bonobo society. Evol Anthropol 20:131–142.  https://doi.org/10.1002/evan.20308 PubMedGoogle Scholar
  39. Gallese V (2003) The manifold nature of interpersonal relations: the quest for a common mechanism. Phil Trans R Soc B 358:517–528.  https://doi.org/10.1098/rstb.2002.1234 PubMedGoogle Scholar
  40. Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trends Cogn Sci 8:396–403.  https://doi.org/10.1016/j.tics.2004.07.002 PubMedGoogle Scholar
  41. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Bellknap Press, BostonGoogle Scholar
  42. Graham KL, Burghardt GM (2010) Current perspectives on the biological study of play: signs of progress. Q Rev Biol 85:393–418PubMedGoogle Scholar
  43. Håkstada RB, Obstfeldera A, Øberga GK (2017) Let’s play! An observational study of primary care physical therapy with preterm infants aged 3–14 months. Infant Behav Dev 46:115–123Google Scholar
  44. Heesen R, Genty E, Rossano F, Zuberbühler K, Bangerter A (2017) Social play as joint action: a framework to study the evolution of shared intentionality as an interactional achievement. Learn Behav 45:390–405.  https://doi.org/10.3758/s13420-017-0287-9 PubMedGoogle Scholar
  45. Heintz MR, Murray CM, Markham AC, Pusey AE, Lonsdorf EV (2017) The relationship between social play and developmental milestones in wild chimpanzees (Pan troglodytes schweinfurthii). Am J Primatol 79:e22716.  https://doi.org/10.1002/ajp.22716 Google Scholar
  46. Henry JD, Herrero SM (1974) Social play in the American black bear: its similarity to canid social play and an examination of its identifying characteristics. Am Zool 14:371–389Google Scholar
  47. Hess U, Fischer A (2013) Emotional mimicry as social regulation. Personal Soc Psychol Rev 17:142–157.  https://doi.org/10.1177/1088868312472607 Google Scholar
  48. van Hooff JARAM (1967) The facial displays of the catarrhine monkeys and apes. In: Morris D (ed) Primate Ethology. Aldine de Gruyter, Chicago, pp 7–68Google Scholar
  49. van Hooff JARAM, Preuscholft S (2003) Laughter and smiling: the intertwining of nature and culture. In: de Waal FBM, Tyack PL (eds) Animal social complexity. Harvard University Press, Cambridge, pp 260–287Google Scholar
  50. Ishijima K, Negayama K (2013) Mother–infant interaction in tickling play: intention reading based on narrative sharing. Jpn J Dev Psychol 24:326–336.  https://doi.org/10.11201/jjdp.24.326 Google Scholar
  51. Ishizuka S, Kawamoto Y, Sakamaki T, Tokuyama N, Toda K, Okamura H, Furuichi T (2018) Paternity and kin structure among neighbouring groups in wild bonobos at Wamba. Proc R Soc B 5:171006.  https://doi.org/10.1098/rsos.171006 Google Scholar
  52. Kaburu SSK, Paukner A, Simpson EA, Suomi SJ, Ferrari PF (2016) Neonatal imitation predicts infant rhesus macaque (Macaca mulatta) social and anxiety-related behaviours at one year. Sci Rep 6:34997.  https://doi.org/10.1038/srep34997 PubMedPubMedCentralGoogle Scholar
  53. Kano T (1992) The last ape. Stanford University Press, Palo AltoGoogle Scholar
  54. Kulik L, Amici F, Langos D, Widdig A (2015) Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta). Int J Primatol 36:353–376.  https://doi.org/10.1007/s10764-015-9826-4 PubMedPubMedCentralGoogle Scholar
  55. Lifter K, Foster-Sanda S, Arzamarski C, Briesch J, McClure E (2011) Overview of play: its uses and importance in early intervention/early childhood special education. Infant Young Child 24:225–245Google Scholar
  56. Llamazares-Martín C, Scopa C, Guillén-Salazar F, Palagi E (2017a) Strong competition does not always predict play asymmetry: the case of South American sea lions (Otaria flavescens). Ethology 123:270–282.  https://doi.org/10.1111/eth.12594 Google Scholar
  57. Llamazares-Martín C, Scopa C, Guillén-Salazar F, Palagi E (2017b) Relaxed open mouth reciprocity favours playful contacts in south american sea lions (Otaria flavescens). Behav Process 140:87–95.  https://doi.org/10.1016/j.beproc.2017.04.007 Google Scholar
  58. Lutz MC, Judge PG (2017) Self-handicapping during play fighting in capuchin monkeys (Cebus apella). Behaviour 154:909–938.  https://doi.org/10.1163/1568539X-00003449 Google Scholar
  59. Mancini G, Palagi E (2009) Play and social dynamics in a captive herd of gelada baboons (Theropithecus gelada). Behav Process 82:286–292.  https://doi.org/10.1016/j.beproc.2009.07.007 Google Scholar
  60. Mancini G, Ferrari PF, Palagi E (2013a) Rapid facial mimicry in geladas. Sci Rep 3:1527.  https://doi.org/10.1038/srep01527 PubMedPubMedCentralGoogle Scholar
  61. Mancini G, Ferrari PF, Palagi E (2013b) In play we trust. Rapid facial mimicry predicts the duration of playful interactions in geladas. PLoS One 8:e66481.  https://doi.org/10.1371/journal.pone.0066481 PubMedPubMedCentralGoogle Scholar
  62. Martin P, Caro TM (1985) On the functions of play and its role in behavioral development. Adv Stud Behav 15:59–103Google Scholar
  63. Micheletta J, Engelhardt A, Matthews L, Agil M, Waller BM (2013) Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra). Am J Primatol 75:763–773.  https://doi.org/10.1002/ajp.22105 PubMedGoogle Scholar
  64. Monteiro de Almeida Rocha J, Pedreira dos Reis P, de Carvalho Oliveira L (2014) Play behavior of the golden-headed lion tamarin in Brazilian cocoa agroforests. Folia Primatol 85:192–199PubMedGoogle Scholar
  65. Montgomery SH (2014) The relationship between play, brain growth and behavioural flexibility in primates. Anim Behav 90:281–286.  https://doi.org/10.1016/j.anbehav.2014.02.004 Google Scholar
  66. Murray L, De Pascalis L, Bozicevic L, Hawkins L, Sclafani V, Ferrari PF (2016) The functional architecture of mother-infant communication, and the development of infant social expressiveness in the first two months. Sci Rep 6:39019.  https://doi.org/10.1038/srep39019 PubMedPubMedCentralGoogle Scholar
  67. Norscia I, Antonacci A, Palagi E (2009) Mating first, mating more: biological market fluctuation in a wild prosimian. PLoS ONE 4(3): e4679.  https://doi.org/10.1371/journal.pone.0004679
  68. Norscia I, Palagi E (2011) When play is a family business: adult play, hierarchy, and possible stress reduction in common marmosets. Primates 52:101–104.  https://doi.org/10.1007/s10329-010-0228-0 PubMedGoogle Scholar
  69. Norscia I, Palagi E (2015) The socio-matrix reloaded: from hierarchy to dominance profile in wild lemurs. PeerJ 3:e729.  https://doi.org/10.7717/peerj.729 PubMedPubMedCentralGoogle Scholar
  70. Norscia I, Palagi E (2016) The missing lemur link: an ancestral step in the evolution of human behaviour. Cambridge University Press, CambridgeGoogle Scholar
  71. Nunes S (2014) Juvenile social play and yearling behavior and reproductive success in female Belding’s ground squirrels. J Ethol 32:145–153.  https://doi.org/10.1007/s10164-014-0403-7 Google Scholar
  72. Palagi E (2006) Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): implications for natural social systems and inter-individual relationships. Am J Phys Anthropol 129:418–426.  https://doi.org/10.1002/ajpa.20289 PubMedGoogle Scholar
  73. Palagi E (2007) Play at work: revisiting data focussing on chimpanzees (Pan troglodytes). J Anthropol Sci 85:153–164Google Scholar
  74. Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75:887–896.  https://doi.org/10.1016/j.anbehav.2007.07.016 Google Scholar
  75. Palagi E (2009) Adult play fighting and potential role of tail signals in ringtailed lemurs (Lemur catta). J Comp Psychol 123:1–9.  https://doi.org/10.1037/0735-7036.123.1.1
  76. Palagi E (2011) Playing at every age: modalities and potential functions in non-human primates. In: Pellegrini A (ed) The Oxford handbook of the development of play. Oxford University Press, Oxford, pp 70–82Google Scholar
  77. Palagi E (2012) Playing alone and with others—a lesson from animals. In: Coplan RJ, Bowker JC (eds) The handbook of solitude: psychological perspectives on social isolation, social withdrawal, and being alone. Wiley Blackwell, Chichester, UK, pp 463–482Google Scholar
  78. Palagi E, Cordoni G (2012) The right time to happen: play developmental divergence in the two Pan species. PLoS One 7:e52767.  https://doi.org/10.1371/journal.pone.0052767 PubMedPubMedCentralGoogle Scholar
  79. Palagi E, Demuru E (2017) Pan paniscus or Pan ludens? Bonobos, playful attitude and social tolerance. In: Hare B, Yamamoto S (eds) Bonobos—unique in mind, brain and behaviour. Oxford University Press, Oxford, pp 65–77Google Scholar
  80. Palagi E, Mancini G (2011) Playing with the face: playful facial chattering and its modulation in a monkey species. J Comp Psychol 125:11–21.  https://doi.org/10.1037/a0020869 PubMedGoogle Scholar
  81. Palagi E, Norscia I (2013) Bonobos protect and console friends and kin. PLoS One 8:e79290.  https://doi.org/10.1371/journal.pone.0079290 PubMedPubMedCentralGoogle Scholar
  82. Palagi E, Norscia I (2018) Emotional contagion. In: Vonk J, Shackelford TK (eds) Encyclopedia of animal cognition and behavior,  https://doi.org/10.1007/978-3-319-47829-6_1866-195
  83. Palagi E, Scopa C (2017) Integrating Tinbergen’s inquiries: mimicry and play in humans and other social mammals. Learn Behav 45:378–389.  https://doi.org/10.3758/s13420-017-0278-x PubMedGoogle Scholar
  84. Palagi E, Cordoni G, Borgognini Tarli SM (2004) Immediate and delayed benefits of play behaviour: new evidences from chimpanzees (Pan troglodytes). Ethology 110:949–962.  https://doi.org/10.1111/j.1439-0310.2004.01035.x Google Scholar
  85. Palagi E, Paoli T, Borgognini Tarli S (2006) Short-term benefits of play behavior and conflict prevention in Pan paniscus. Int J Primatol 27:1257–1270Google Scholar
  86. Palagi E, Antonacci D, Cordoni G (2007) Fine-tuning of social play in juvenile lowland gorillas (Gorilla gorilla gorilla). Dev Psychobiol 49:433–445.  https://doi.org/10.1002/dev.20219 PubMedGoogle Scholar
  87. Palagi E, Norscia I, Spada G (2014) Relaxed open mouth as a playful signal in wild ring-tailed lemurs. Am J Primatol 76:1074–1083.  https://doi.org/10.1002/ajp.22294 PubMedGoogle Scholar
  88. Palagi E, Nicotra V, Cordoni G (2015) Rapid mimicry and emotional contagion in domestic dogs. R Soc Open Sci 2:150505.  https://doi.org/10.1098/rsos.150505 PubMedPubMedCentralGoogle Scholar
  89. Palagi E, Burghardt GM, Smuts B, Cordoni G, Dall'Olio S, Fouts HN, Řeháková-Petrů M, Siviy SM, Pellis SM (2016a) Rough-and-tumble play as a window on animal communication. Biol Rev 91:311–327.  https://doi.org/10.1111/brv.12172 PubMedGoogle Scholar
  90. Palagi E, Cordoni G, Demuru E, Bekoff M (2016b) Fair play and its connection with social tolerance, reciprocity and the ethology of peace. Behaviour 153:1195–1216.  https://doi.org/10.1163/1568539X-00003336 Google Scholar
  91. Pellegrini AD (2009) The role of play in human development. Oxford University Press, New YorkGoogle Scholar
  92. Pellis SM, Iwaniuk AN (1999) The problem of adult play-fighting: a comparative analysis of play and courtship in primates. Ethology 105:783–806.  https://doi.org/10.1046/j.1439-0310.1999.00457.x Google Scholar
  93. Pellis SM, Iwaniuk AN (2000) Adult-adult play in primates: comparative analyses of its origin, distribution and evolution. Ethology 106:1083–1104.  https://doi.org/10.1046/j.1439-0310.2000.00627.x Google Scholar
  94. Pellis SM, Pellis VC (1996) On knowing it’s only play: the role of play signals in play fighting. Aggress Violent Behav 1:249–268Google Scholar
  95. Pellis SM, Pellis VC (1998) The play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev 23:87–101PubMedGoogle Scholar
  96. Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld, OxfordGoogle Scholar
  97. Pellis SM, Pellis VC (2017) What is play fighting and what is it good for? Learn Behav 45:355–366.  https://doi.org/10.3758/s13420-017-0264-3 PubMedGoogle Scholar
  98. Pellis SM, Pellis VC, Reinhart CJ (2010) The evolution of social play. In: Worthman C, Plotsky P, Schechter D, Cummings C (eds) Formative experiences: the interaction of caregiving, culture, and developmental psychobiology. Cambridge University Press, Cambridge, pp 404–431Google Scholar
  99. Pellis SM, Pellis VC, Reinhart CJ, Thierry B (2011) The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): sometimes it is all about oneself. J Comp Psychol 125:393–403.  https://doi.org/10.1037/a0024514 PubMedGoogle Scholar
  100. Pellis SM, Williams LA, Pellis VC (2017) Adult-juvenile play fighting in rats: insight into the experiences that facilitate the development of socio-cognitive skills. Int J Comp Psychol 2017:30Google Scholar
  101. Petit O, Bertrand F, Thierry B (2008) Social play in crested and Japanese macaques: testing the covariation hypothesis. Dev Psychobiol 50:399–407.  https://doi.org/10.1002/dev.20305 PubMedGoogle Scholar
  102. Plooij FX (1979) How wild chimpanzee babies trigger the onset of mother-infant play and what the mother makes of it. In: Bullowa M (ed) Before speech: the beginning of interpersonal communication. Cambridge University press, Cambridge, pp 223–243Google Scholar
  103. Plooij FX (1984) The behavioral development of free-living chimpanzee babies and infants. Ablex, NorwoodGoogle Scholar
  104. Preuschoft S (1992) “Laughter” and “smile” in Barbary macaques, Macaca sylvanus. Ethology 91:220–236.  https://doi.org/10.1111/j.1439-0310.1992.tb00864.x Google Scholar
  105. Preuschoft S, van Hooff JARAM (1995) Homologizing primate facial displays: a critical review of methods. Folia Primatol 65:121–137PubMedGoogle Scholar
  106. Preuschoft S, van Hooff JARAM (1997) The social function of “smile” and “laugther”: variations across primate species and societies. In: Segerstrale U, Molnar P (eds) Nonverbal communication: where nature meets culture. Erlbaum, Mahwah, pp 171–189Google Scholar
  107. Prochazkova E, Kret ME (2017) Connecting minds and sharing emotions through mimicry: a neurocognitive model of emotional contagion. Neurosci Biobehav Rev 80:99–114.  https://doi.org/10.1016/j.neubiorev.2017.05.013 PubMedGoogle Scholar
  108. Provine RR (1996) Ticklish talk: a letter to the editor and reply. Am Sci 84:100–101Google Scholar
  109. Provine RR (1997) Yawns, laughs, smiles, tickles, and talking: naturalistic and laboratory studies of facial action and social communication. In: Russell JA, Fernández Dols JM (eds) The psychology of facial expression. Cambridge University, Cambridge, pp 158–175Google Scholar
  110. Provine RR (2004) Laughing, tickling, and the evolution of speech and self. Curr Dir Psychol Sci 13:215–218.  https://doi.org/10.1111/j.0963-7214.2004.00311.x Google Scholar
  111. 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 4:166–200Google Scholar
  112. Rossmanith N, Costall A, Reichelt AF, López B, Reddy V (2014) Jointly structuring triadic spaces of meaning and action: book sharing from 3 months on. Front Psychol 5:1390.  https://doi.org/10.3389/fpsyg.2014.01390 PubMedPubMedCentralGoogle Scholar
  113. Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearb Phys Anthropol 44:3–24.  https://doi.org/10.1002/ajpa.2001 Google Scholar
  114. Scopa C, Palagi E (2016) Mimic me while playing! Social tolerance and rapid facial mimicry in macaques (Macaca tonkeana and Macaca fuscata). J Comp Psychol 130(2):153–161.  https://doi.org/10.1037/com0000028 PubMedGoogle Scholar
  115. Seibt B, Mühlberger A, Likowski KU, Weyers P (2015) Facial mimicry in its social setting. Front Psychol 6:1122.  https://doi.org/10.3389/fpsyg.2015.01122 PubMedPubMedCentralGoogle Scholar
  116. Shimada M, Sueur C (2018) Social play among juvenile wild Japanese macaques (Macaca fuscata) strengthens their social bonds. Am J Primatol 80:e22728.  https://doi.org/10.1002/ajp.22728 Google Scholar
  117. Simpson EA, Sclafani V, Paukner A, Kaburu SSK, Suomi SJ, Ferrari PF (2017) Handling newborn monkeys alters later exploratory, cognitive, and social behaviors. Dev Cogn Neurosci-Neth S1878-9293(17):30044–30040.  https://doi.org/10.1016/j.dcn.2017.07.010 Google Scholar
  118. Špinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168PubMedGoogle Scholar
  119. Stanton MA, Lonsdorf EV, Pusey AE, Goodall J, Murray CM (2014) Maternal behavior by birth order in wild chimpanzees (Pan troglodytes) increased investment by first-time mothers. Curr Anthropol 55:483–489PubMedPubMedCentralGoogle Scholar
  120. Suomi SJ (2005) Mother-infant attachment, peer relationships, and the development of social networks in rhesus monkeys. Hum Dev 48:67–79.  https://doi.org/10.1159/000083216 Google Scholar
  121. Tan J, Ariely D, Hare B (2017) Bonobos respond prosocially toward members of other groups. Sci Rep 7:14733.  https://doi.org/10.1038/s41598-017-15320-w PubMedPubMedCentralGoogle Scholar
  122. Thompson ME, Muller MN, Wrangham RW (2012) The energetics of lactation and the return to fecundity in wild chimpanzees. Behav Ecol 23:1234–1241.  https://doi.org/10.1093/beheco/ars107 Google Scholar
  123. Tinbergen N (1952) Derived’ activities; their causation, biological significance, origin, and emancipation during evolution. Q Rev Biol 27:1–32PubMedGoogle Scholar
  124. Treyvaud K, Anderson VA, Howard K, Bear M, Hunt RW, Doyle LW, Inder TE, Woodward L, Anderson PJ (2009) Parenting behavior is associated with the early neurobehavioral development of very preterm children. Pediatrics 123:555–561PubMedGoogle Scholar
  125. de Waal FBM (2003) Darwin’s legacy and the study of primate visual communication. Ann N Y Acad Sci 1000:7–31.  https://doi.org/10.1196/annals.1280.003 PubMedGoogle Scholar
  126. de Waal FBM (2012) Empathy in primates and other mammals. In: Decety J (ed) Empathy—from bench to bedside. The MIT Press, Cambridge, pp 87–106Google Scholar
  127. de Waal FBM, Preston SD (2017) Mammalian empathy: behavioural manifestations and neural basis. Nat Rev Neurosci 18:498–509.  https://doi.org/10.1038/nrn.2017.72 PubMedGoogle Scholar
  128. Waller BM, Cherry L (2012) Facilitating play through communication: significance of teeth exposure in the gorilla play face. Am J Primatol 74:157–164.  https://doi.org/10.1002/ajp.21018 PubMedGoogle Scholar
  129. Waller BM, Dunbar RIM (2005) Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111:129–142.  https://doi.org/10.1111/j.1439-0310.2004.01045.x Google Scholar
  130. Waller BM, Whitehouse J, Micheletta J (2016) Macaques can predict social outcomes from facial expressions. Anim Cogn 19:1031–1036.  https://doi.org/10.1007/s10071-016-0992-3 PubMedPubMedCentralGoogle Scholar
  131. Watts DP, Pusey AE (1993) Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks LA (eds) Juvenile primates—life history, development, and behavior. Oxford University Press, New York, pp 148–167Google Scholar
  132. Weigel EA, Berman CM (2017) Body signals used during social play in captive immature western lowland gorillas. Primates (published online)  https://doi.org/10.1007/s10329-017-0646-3
  133. Wrangham RW (2018) Two types of aggression in human evolution. Proc Natl Acad Sci USA 115:245–253.  https://doi.org/10.1073/pnas.1713611115 PubMedGoogle Scholar
  134. Yanagi A, Berman CM (2017) Does behavioral flexibility contribute to successful play among juvenile rhesus macaques? Behav Ecol Sociobiol 71:156.  https://doi.org/10.1007/s00265-017-2377-2 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Natural History MuseumUniversity of PisaPisaItaly

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