Animal Cognition

, Volume 18, Issue 1, pp 333–344 | Cite as

Emotionality and intentionality in bonobo playful communication

  • Elisa Demuru
  • Pier F. Ferrari
  • Elisabetta Palagi
Original Paper

Abstract

Great apes show very complex systems for communicating emotions and intentions. Whereas gestures are intentional signals, facial expressions can disclose both emotions and intentions. The playful context is a good field to explore the possible dichotomy between intentionally and emotionally driven signals as it has been suggested that one of its functions is to learn producing and decoding communicative patterns. To understand how signals are produced during play and how they are modified in the course of ontogeny, we investigated the use of playful facial expressions and gestures in bonobos (Pan paniscus), a tolerant species showing a high propensity to play even as adults. Our results showed that the use of play faces and gestures is strongly influenced by the characteristics of the play session. Both play faces and gestures were more often performed when social play involved physical contact and when the receiver was visually attending, thus suggesting that both signals can be strategically employed when communicating becomes more urgent. Compared to play faces, gestures were more frequent during dyadic than polyadic sessions, when a unique receiver was involved. Being gestures not context specific, they are probably used more selectively by the sender. On the contrary, play faces are context specific and transmit an unequivocal positive message that cannot be misconceived. These features legitimize a broad use of playful facial expressions, independently of the number of playmates. The similarities and differences in the production of these signals are probably linked to the different degree of emotionality and intentionality characterizing them.

Keywords

Pan paniscus Gestures Facial expressions Social and solitary play 

Notes

Acknowledgments

We thank the Apenheul Primate Park (Apeldoorn, The Netherlands), General Curator Frank Rietkerk, and the bonobo keepers for allowing and facilitating this work. We also thank Francesca Coppola for her assistance. We thank Walter Rapitalà and Roscoe Stanyon for their important clarifying input to the discussion and critical revision of the manuscript. This research was supported exclusively by private funding. This research complies with current laws of the Netherlands and Italy.

Supplementary material

10071_2014_804_MOESM1_ESM.jpg (1.6 mb)
Play Face (male subject on the left) and Full Play Face (female subject on the right) shown by two adult bonobos during a face-to-face interaction while playing in contact. (JPEG 1670 kb)
10071_2014_804_MOESM2_ESM.jpg (895 kb)
An immature female (on the right) is performing a Play Face and a Beg With Hand gesture during a playful contact with an adult male (on the left) (for the description of the gestural item see Pollick and de Waal 2007) (JPEG 895 kb)
10071_2014_804_MOESM3_ESM.jpg (175 kb)
An immature female puts her finger into the mouth of an adult male (for the description of the gestural item see Pollick and de Waal 2007). (JPEG 175 kb)
10071_2014_804_MOESM4_ESM.docx (18 kb)
Supplementary material 4 (DOCX 17 kb)

Playful invitation of an adult male towards a newborn. The adult male, after engaging the gaze of the newborn, performs a Full Play Face and slightly shakes its head in front of him. Then, the adult male engages in self-handicapping behaviours (putting on its own back). (AVI 10728 kb)

An adult male performs a Flap and Reach Out Up gestures to invite to play an infant male, who responds to the invitation (for the description of the gestural item see Pollick and de Waal 2007) (MPG 8343 kb)

An adult male manage a polyadic playful interaction with two immatures, a male and a female. At the very beginning of the video, the juvenile female (on the right) performs a Full Play Face (AVI 10010 kb)

Immediately after the interruption of a contact play session two subjects, an adult male (ADm) and an immature female (IMf) engage in a facial expression and gestural “dialogue”. IMf: pout face, silent bared-teeth (Pollick and de Waal 2007); ADm: Head Nod (Hobaiter and Byrne 2011a); IMf: Reach Out Up (Pollick and de Waal 2007) (AVI 13200 kb)

References

  1. Altmann J (1974) Observational study of behavior sampling methods. Behaviour 49:227–265PubMedCrossRefGoogle Scholar
  2. Arbib MA, Liebal K, Pika S (2008) Primate vocalization, gesture, and the evolution of human language. Curr Anthropol 49:1053–1075PubMedCrossRefGoogle Scholar
  3. Bakeman R, Adamson LB (1986) Infants’ conventionalized acts: gestures and words with mothers and peers. Infant Behav Dev 9:215–230CrossRefGoogle Scholar
  4. Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (1979) The emergence of symbols: cognition and communication in infancy. Academic Press, New YorkGoogle Scholar
  5. Bekoff M (1974) Social play and play-soliciting by infant canids. Am Zool 14:323–340Google Scholar
  6. Bekoff M (1995) Play signals as punctuation: the structure of social play in canids. Behaviour 132:5–6CrossRefGoogle Scholar
  7. Bekoff M, Allen C (2002) The evolution of social play: interdisciplinary analyses of cognitive processes. In: Bekoff M, Allen C, Burghardt GM (eds) The cognitive animal: empirical and theoretical perspectives on animal cognition. MIT Press, Cambridge Massachusetts, pp 429–435Google Scholar
  8. Brosnan SF (2010) Behavioral development: timing is everything. Curr Biol 20:98–100CrossRefGoogle Scholar
  9. Burghardt GM (2005) The genesis of animal play: testing the limits. MIT Press, CambridgeGoogle Scholar
  10. Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317PubMedCrossRefGoogle Scholar
  11. Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  12. Cartmill EA, Byrne RW (2011) Addressing the problems of intentionality and granularity in non-human primate gesture. In: Stam G, Ishino M (eds) Integrating gestures: the interdisciplinary nature of gesture. John Benjamins Publishing Company, AmsterdamGoogle Scholar
  13. Cattaneo L, Pavesi G (2014) The facial motor system. Neurosci Biobehav R 38:135–159CrossRefGoogle Scholar
  14. 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 84:1313–1322CrossRefGoogle Scholar
  15. Darwin C (1872) The expression of the emotions in man and animals. Oxford University Press, OxfordCrossRefGoogle Scholar
  16. Davila Ross M, Owren MJ, Zimmermann E (2009) Reconstructing the evolution of laughter in great apes and humans. Curr Biol 19:1106–1111PubMedCrossRefGoogle Scholar
  17. Davila-Ross M, Allcock B, Thomas C, Bard KA (2011) Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion 11:1013–1020PubMedCrossRefGoogle Scholar
  18. De Marco A, Visalberghi E (2007) Facial displays in young tufted capuchin monkeys (Cebus apella): appearance, meaning, context and target. Folia Primatol 78:118–137PubMedCrossRefGoogle Scholar
  19. de Waal FBM (2003) Darwin’s legacy and the study of primate visual communication. Ann NY Acad Sci 1000:7–31PubMedCrossRefGoogle Scholar
  20. de Waal FBM, van Hooff JARAM (1981) Side-directed communication and agonistic interactions in chimpanzees. Behaviour 77:164–198CrossRefGoogle Scholar
  21. Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347PubMedCrossRefGoogle Scholar
  22. Ekman P (1993) Facial expression and emotion. Am Psychol 48:384–392PubMedCrossRefGoogle Scholar
  23. Ekman P, Rosenberg EL (1997) What the face reveals: basic and applied studies of spontaneous expression using the facial action coding system (FACS). Oxford University Press, OxfordGoogle Scholar
  24. Ekman P, Davidson RJ, Friesen WV (1990) The Duchenne smile: emotional expression and brain physiology II. J Pers Soc Psychol 58:342–353PubMedCrossRefGoogle Scholar
  25. Fagen RM (1981) Animal play behavior. Oxford University Press, OxfordGoogle Scholar
  26. Fagen R (1993) Primate juveniles and primate play. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. University of Chicago Press, Chicago, pp 182–196Google Scholar
  27. Flack JC, Jeannotte LA, de Waal FBM (2004) Play signaling and the perception of social rules by juvenile chimpanzees (Pan troglodytes). J Comp Psychol 118:149–159PubMedCrossRefGoogle Scholar
  28. Fredrickson BL (2004) The broaden-and-build theory of positive emotions. Philos T R Soc B 359:1367–1378CrossRefGoogle Scholar
  29. Freeberg TM, Robin IM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos T R Soc B 367:1785–1801CrossRefGoogle Scholar
  30. Genty E, Byrne RW (2010) Why do gorillas make sequences of gestures? Anim Cogn 13:287–301PubMedCrossRefGoogle Scholar
  31. Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn 12:527–546PubMedCentralPubMedCrossRefGoogle Scholar
  32. Gervais M, Wilson DS (2005) The evolution and functions of laughter and humor: a synthetic approach. Q Rev Biol 80:395–430PubMedCrossRefGoogle Scholar
  33. Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785PubMedCrossRefGoogle Scholar
  34. Hare B, Melis AP, Woods V, Hastings S, Wrangham RW (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623PubMedCrossRefGoogle Scholar
  35. Hare B, Wobber V, Wrangham R (2012) The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Anim Behav 83:573–585CrossRefGoogle Scholar
  36. Hayaki H (1985) Social play of juvenile and adolescent chimpanzees in the Mahale Mountains National Park, Tanzania. Primates 26:343–360CrossRefGoogle Scholar
  37. Hobaiter C, Byrne RW (2011a) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767PubMedCrossRefGoogle Scholar
  38. Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cogn 14:827–838PubMedCrossRefGoogle Scholar
  39. Hobaiter C, Byrne RW (2014) The meanings of chimpanzee gestures. Curr Biol 24:1596–1600PubMedCrossRefGoogle Scholar
  40. Hostetter AB, Cantero M, Hopkins WD (2001) Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). J Comp Psychol 115:337–343PubMedCentralPubMedCrossRefGoogle Scholar
  41. Leavens DA, Hopkins WD, Bard KA (1996) Indexical and referential pointing in chimpanzees (Pan troglodytes). J Comp Psychol 110:346–353PubMedCentralPubMedCrossRefGoogle Scholar
  42. Leavens DA, Hopkins WD, Thomas RK (2004a) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57PubMedCrossRefGoogle Scholar
  43. Leavens DA, Hostetter AB, Wesley MJ, Hopkins WD (2004b) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 67:467–476CrossRefGoogle Scholar
  44. Leavens DA, Russel JL, Hopkins WD (2005) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76:291–306PubMedCentralPubMedCrossRefGoogle Scholar
  45. Liebal K (2007) Gestures in orangutans. In: Call J, Tomasello M (eds) The gestural communication of apes and monkeys. Lawrence Erlbaum Associates, Mahwah, pp 69–98Google Scholar
  46. Liebal K, Pika S, Call J, Tomasello M (2004) To move or not to move. How apes adjust to the attentional state of others. Interact Stud 5:199–219CrossRefGoogle Scholar
  47. Liebal K, Pika S, Tomasello M (2006) Gestural communication of orangutans (Pongo pygmaeus). Gesture 6:1–38CrossRefGoogle Scholar
  48. Lieberman DE, Carlo J, de Leon M, Zollikofer CP (2007) A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos. J Hum Evol 52:647–662PubMedCrossRefGoogle Scholar
  49. Maestripieri D (1999) Primate social organization, gestural repertoire size, and communication dynamics. In: King BJ (ed) The origins of language: what non-human primates can tell. School of American Research Press, Santa Fe, pp 55–77Google Scholar
  50. Mancini G, Ferrari PF, Palagi E (2013) Rapid facial mimicry in geladas. Sci Rep 3:1527. doi:10.1038/srep01527 PubMedCentralPubMedCrossRefGoogle Scholar
  51. Matsusaka T (2004) When does play panting occur during social play in wild chimpanzees? Primates 45:221–229PubMedCrossRefGoogle Scholar
  52. McComb K, Semple S (2005) Co-evolution of vocal communication and sociality in primates. Biol Lett 1:381–385PubMedCentralPubMedCrossRefGoogle Scholar
  53. Mundry R, Fisher J (1998) Use of statistical programs for nonparametric tests of small samples often leads to incorrect P values: examples from animal behaviour. Anim Behav 56:256–259PubMedCrossRefGoogle Scholar
  54. O’Neill DK (1996) Two-year-old children’s sensitivity to a parent’s knowledge state when making requests. Child Dev 67:659–677CrossRefGoogle Scholar
  55. 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 129:418–426PubMedCrossRefGoogle Scholar
  56. Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75:887–896CrossRefGoogle Scholar
  57. Palagi E (2009) Adult play fighting and potential role of tail signals in ring-tailed lemurs (Lemur catta). J Comp Psychol 123:1–9PubMedCrossRefGoogle Scholar
  58. Palagi (2014) 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, Hoboken, pp 461–482Google Scholar
  59. Palagi E, Cordoni G (2012) The right time to happen: play developmental divergence in the two Pan species. PLoS ONE 7:e52767. doi:10.1371/journal.pone.0052767 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Palagi E, Mancini G (2011) Playing with the face: playful facial “chattering” and signal modulation in a monkey species (Theropithecus gelada). J Comp Psychol 125:11–21PubMedCrossRefGoogle Scholar
  61. Palagi E, Paoli T (2007) Play in adult bonobos (Pan paniscus): modality and potential meaning. Am J Phys Anthropol 134:219–225PubMedCrossRefGoogle Scholar
  62. Palagi E, Antonacci D, Cordoni G (2007) Fine-tuning of social play in juvenile Lowland gorillas (Gorilla gorilla gorilla). Dev Psychobiol 49:433–445PubMedCrossRefGoogle Scholar
  63. Panksepp J, Panksepp JB (2013) Toward a cross-species understanding of empathy. Trends Neurosci 36:489–496PubMedCrossRefGoogle Scholar
  64. Parker ST, McKinney ML (1999) Origins of intelligence: the evolution of cognitive development in monkeys, apes, and humans. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  65. Parr LA, Waller BM, Fugate J (2005) Emotional communication in primates: implications for neurobiology. Curr Opin Neurobiol 15:716–720PubMedCentralPubMedCrossRefGoogle Scholar
  66. Pellis SM, Pellis VC (1996) On knowing it’s only play: the role of play signals in play fighting. Aggress Violent Behav 1:249–268CrossRefGoogle Scholar
  67. Pellis SM, Pellis VC (1997) Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggress Behav 23:41–57CrossRefGoogle Scholar
  68. Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Publications, Oxford, UKGoogle Scholar
  69. Pereira ME, Preisser MC (1998) Do strong primates players “self-handicap” during competitive social play? Folia Primatol 69:177–180CrossRefGoogle Scholar
  70. Pika S (2007a) Gestures in subadult bonobos (Pan paniscus). In: Call J, Tomasello M (eds) The gestural communication of apes and monkeys. Lawrence Erlbaum Associates, Mahwah, pp 41–67Google Scholar
  71. Pika S (2007b) Gestures in subadult gorillas (Gorilla gorilla). In: Call J, Tomasello M (eds) The gestural communication of apes and monkeys. Lawrence Erlbaum Associates, Mahwah, pp 99–130Google Scholar
  72. Pika S, Liebal K, Tomasello M (2003) Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire, learning, and use. Am J Primatol 60:95–111PubMedCrossRefGoogle Scholar
  73. Pika S, Liebal K, Tomasello M (2005) Gestural communication in subadult bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61PubMedCrossRefGoogle Scholar
  74. Pollick AS, de Waal FMB (2007) Ape gestures and language evolution. P Natl Acad Sci USA 104:8184–8189CrossRefGoogle Scholar
  75. Poss SR, Kuhar C, Stoinski TS, Hopkins WD (2006) Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human. Am J Primatol 68:978–992PubMedCentralPubMedCrossRefGoogle Scholar
  76. Power TG (2000) Play and exploration in children and animals. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  77. Provine RR (2000) Laughter: a scientific investigation. Penguin Group, New YorkGoogle Scholar
  78. Rilling JK, Scholz J, Preuss TM, Glasser MF, Errangi BK, Behrens TE (2012) Differences between chimpanzees and bonobos in neural systems supporting social cognition. Soc Cogn Affect Neur 7:369–379CrossRefGoogle Scholar
  79. Rothbart MK (1973) Laughter in young children. Psychol Bull 80:247–256PubMedCrossRefGoogle Scholar
  80. Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearb Phys Anthropol 44:3–24CrossRefGoogle Scholar
  81. Schyns PG, Petro LS, Smith ML (2009) Transmission of facial expression of emotion co-evolved with their efficient decoding in the brain: behavioral and brain evidence. PLoS ONE 4:e5625. doi:10.1371/journal.pone.0005625 PubMedCentralPubMedCrossRefGoogle Scholar
  82. Seyfarth RM, Cheney DL (2003) Signalers and receivers in animal communication. Annu Rev Psychol 54:145–173PubMedCrossRefGoogle Scholar
  83. Sherwood CC, Holloway RL, Erwin JF, Hof PR (2004) Cortical orofacial motor representation in old world monkeys, great apes and humans. Brain Behav Evolut 63:82–106CrossRefGoogle Scholar
  84. Sherwood CC, Hof PR, Holloway RL, Semendeferi K, Gannon PJ, Frahm HD, Zilles K (2005) Evolution of the brainstem orofacial motor system in primates: a comparative study of trigeminal, facial and hypoglossal nuclei. J Hum Evol 48:45–84PubMedCrossRefGoogle Scholar
  85. Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Company, New YorkGoogle Scholar
  86. Surakka V, Hietanen JK (1998) Facial and emotional reactions to Duchenne and non-Duchenne smiles. Int J Psychophysiol 29:23–33PubMedCrossRefGoogle Scholar
  87. Tacconi G, Palagi E (2009) Play behavioural tactics under space reduction: social challenges in bonobos (Pan paniscus). Anim Behav 78:469–476CrossRefGoogle Scholar
  88. Tanner JE, Byrne RW (1993) Concealing facial evidence of mood: evidence for perspective-taking in a captive gorilla? Primates 34:451–456CrossRefGoogle Scholar
  89. 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 183–204Google Scholar
  90. Tomasello M, Gust D, Frost TA (1989) A longitudinal investigation of gestural communication in young chimpanzees. Primates 30:35–50CrossRefGoogle Scholar
  91. Tomasello M, Call J, Nagell C, Olguin R, Carpenter M (1994) The learning and use of gestural signals by young chimpanzees: a trans-generational study. Primates 35:137–154CrossRefGoogle Scholar
  92. Tomasello M, Call J, Warren J, Frost JT, Carpenter M, Nagell K (1997) The ontogeny of chimpanzee gestural signals: a comparison across groups and generations. Evol Comm 1:223–259CrossRefGoogle Scholar
  93. 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 209–238Google Scholar
  94. van Hooff JARAM (1973) A structural analysis of the social behaviour of a semi-captive group of chimpanzees. In: von Cranach M, Vine I (eds) Expressive movement and non-verbal communication. Academic Press, London, pp 75–162Google Scholar
  95. van Hooff JARAM, Preuschoft S (2003) Laughter and smiling: the intertwining of nature and culture. In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, pp 261–287Google Scholar
  96. Waller B, Dunbar RIM (2005) Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111:129–142CrossRefGoogle Scholar
  97. Wild B, Rodden FA, Grodd W, Ruch W (2003) Neural correlates of laughter and humour. Brain 126:2121–2138PubMedCrossRefGoogle Scholar
  98. Wilson SC, Kleiman DG (1974) Eliciting play: a comparative study. Am Zool 14:341–370Google Scholar
  99. Wobber V, Wrangham R, Hare B (2010a) Application of the heterochrony framework to the study of behavior and cognition. Comm Integr Biol 3:337–339CrossRefGoogle Scholar
  100. Wobber V, Wrangham R, Hare B (2010b) Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. Curr Biol 20:226–230PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Elisa Demuru
    • 1
    • 2
  • Pier F. Ferrari
    • 3
  • Elisabetta Palagi
    • 2
    • 4
  1. 1.Dipartimento di BioscienzeUniversità di ParmaParmaItaly
  2. 2.Centro Ateneo Museo di Storia Naturale, CalciUniversità di PisaPisaItaly
  3. 3.Dipartimento di NeuroscienzeUniversità di ParmaParmaItaly
  4. 4.Unità di Primatologia Cognitiva, Istituto di Scienze e Tecnologie della CognizioneConsiglio Nazionale delle RicercheRomeItaly

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