Advertisement

The development of gestural communication in great apes

  • Marlen FröhlichEmail author
  • Catherine Hobaiter
Review
Part of the following topical collections:
  1. An evolutionary perspective on the development of primate sociality

Abstract

Great apes deploy gestural signals in goal-directed and flexible ways across a wide range of social contexts. Despite growing evidence for profound effects of developmental experience on social cognition, socio-ecological factors shaping gesture use are still poorly understood, particularly in apes living in their natural environment. After discussing current ambiguities in terminology and methods, we review recent work implementing a longitudinal and/or cross-sectional approach in great ape gesture acquisition (phylogenetic and ontogenetic origins) and development (ontogenetic trajectories). To understand whether and to what extent the socio-ecological environment influences gestural communication, it is essential to distinguish between the gestural repertoire and gesture usage, which represent different levels of analysis. While the majority of the apes’ gestural repertoire seems to be innate, accumulating evidence shows that the communicative usage of these signals is substantially affected by interactional experiences throughout ontogeny. Nevertheless, since great ape communication is intrinsically multimodal, future developmental research on gesture should incorporate other modes of communication.

Significance statement

Great apes navigate their differentiated social relationships by means of a large and flexible repertoire of gestures. However, gestural ontogeny is still poorly understood, particularly in primates living in their natural environment. We first discuss how the different usages of the term ‘gesture’ have led to a number of apparently disparate views, but highlight that these perspectives each provide their own contribution and may be reconciled by considering them as different levels of explanation. We then review recent studies on the various individual and social factors shaping the gestural use in great apes throughout development, highlighting the impact of socio-ecological factors. While the majority of the apes’ gestural repertoire seems to be innate, the communicative usage of these signals is substantially affected by interactional experiences throughout ontogeny. Given that ape gestural signals are inherently multimodal and are then often combined with other communicative signals, a broad multimodal perspective on gesture is important in order to gain a thorough understanding of the developmental processes underlying great ape communication.

Keywords

Gesture Communication Development Repertoire Usage Great apes 

Notes

Acknowledgments

We are grateful to Federica Amici and Anja Widdig for their invitation to the topical collection “An evolutionary perspective on the development of primate sociality”. We thank Simone Pika, Carel van Schaik, Richard Byrne, and both the St Andrews Gesture group and the former Humboldt Research group for many insightful discussions on great ape gestures. We also thank Anja Widdig, Jaap van Schaik and two anonymous reviewers for helpful comments on earlier versions of this manuscript.

Funding

MF was supported by the Forschungskredit of the University of Zurich (grant no. FK-17-106) and by the German Research Foundation (grant no. FR 3986/1-1).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

References

  1. Arbib M, Gasser B (in press) A dyadic brain model of ape gestural learning, production and representation. Anim CognGoogle Scholar
  2. Arbib MA, Liebal K, Pika S (2008) Primate vocalization, gesture, and the evolution of human language. Curr Anthropol 49:1053–1063PubMedGoogle Scholar
  3. Arcadi AC, Robert D, Boesch C (1998) Buttress drumming by wild chimpanzees: temporal patterning, phrase integration into loud calls, and preliminary evidence for individual distinctiveness. Primates 39:505–518Google Scholar
  4. Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics. Curr Anthropol 49:627–654Google Scholar
  5. Bard KA (1992) Intentional behavior and intentional communication in young free-ranging orangutans. Child Dev 63:1186–1197PubMedGoogle Scholar
  6. Bard KA, Bakeman R, Boysen ST, Leavens DA (2014a) Emotional engagements predict and enhance social cognition in young chimpanzees. Dev Sci 17:682–696PubMedPubMedCentralGoogle Scholar
  7. Bard KA, Dunbar S, Maguire-Herring V, Veira Y, Hayes KG, McDonald K (2014b) Gestures and social-emotional communicative development in chimpanzee infants. Am J Primatol 76:14–29PubMedGoogle Scholar
  8. Bard KA, Maguire-Herring V, Tomonaga M, Matsuzawa T (2017) The gesture ‘Touch’: Does meaning-making develop in chimpanzees’ use of a very flexible gesture? Anim Cogn.  https://doi.org/10.1007/s10071-017-1136-0)
  9. Bar-On D (2013) Origins of meaning: must we ‘go Gricean’? Mind Lang 28:342–375Google Scholar
  10. Bates E, Camaioni L, Volterra V (1975) The acquisition of performatives prior to speech. Merrill Palmer Q 21:205–226Google Scholar
  11. 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
  12. Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20:143–149PubMedGoogle Scholar
  13. Boesch C (2007) What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison. J Comp Psychol 3:227–240Google Scholar
  14. Brainard MS, Doupe AJ (2002) What songbirds teach us about learning. Nature 417:351–358PubMedGoogle Scholar
  15. Byrne RW, Tanner JE (2006) Gestural imitation by a gorilla: evidence and nature of the capacity. Int J Psychol Psychol Ther 6:215–231Google Scholar
  16. Byrne RW, Cartmill E, Genty E, Graham KE, Hobaiter C, Tanner J (2017) Great ape gestures: intentional communication with a rich set of innate signals. Anim Cogn 20:755–769PubMedPubMedCentralGoogle Scholar
  17. Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  18. Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience's comprehension. Curr Biol 17:1345–1348PubMedGoogle Scholar
  19. Cartmill EA, Byrne RW (2010) Semantics of primate gestures: intentional meanings of orangutan gestures. Anim Cogn 13:793–804PubMedGoogle Scholar
  20. Cheney DL, Seyfarth RM (2018) Flexible usage and social function in primate vocalizations. Proc Natl Acad Sci U S A 115:1974–1979PubMedPubMedCentralGoogle Scholar
  21. Davila-Ross M, Jesus G, Osborne J, Bard KA (2015) Chimpanzees (Pan troglodytes) produce the same types of ‘laugh faces’ when they emit laughter and when they are silent. PLoS One 10:e0127337PubMedPubMedCentralGoogle Scholar
  22. Douglas PH, Moscovice LR (2015) Pointing and pantomime in wild apes? Female bonobos use referential and iconic gestures to request genito-genital rubbing. Sci Rep 5:13999PubMedPubMedCentralGoogle Scholar
  23. Dunn JC, Halenar LB, Davies TG, Cristobal-Azkarate J, Reby D, Sykes D, Dengg S, Fitch WT, Knapp LA (2015) Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys. Curr Biol 25:2839–2844PubMedPubMedCentralGoogle Scholar
  24. Fröhlich M (2017) Taking turns across channels: conversation-analytic tools in animal communication. Neurosci Biobehav Rev 80:201–209PubMedGoogle Scholar
  25. Fröhlich M, van Schaik CP (2018) The function of primate multimodal communication. Anim Cogn 21:619–629Google Scholar
  26. Fröhlich M, Kuchenbuch P, Müller G, Fruth B, Furuichi T, Wittig RM, Pika S (2016a) Unpeeling the layers of language: bonobos and chimpanzees engage in cooperative turn-taking sequences. Sci Rep 6:25887PubMedPubMedCentralGoogle Scholar
  27. Fröhlich M, Wittig RM, Pika S (2016b) Play-solicitation gestures in chimpanzees in the wild: flexible adjustment to social circumstances and individual matrices. R Soc Open sci 3:160278PubMedPubMedCentralGoogle Scholar
  28. Fröhlich M, Wittig RM, Pika S (2016c) Should I stay or should I go? Initiation of joint travel in mother–infant dyads of two chimpanzee communities in the wild. Anim Cogn 19:483–500PubMedPubMedCentralGoogle Scholar
  29. Fröhlich M, Müller G, Zeiträg C, Wittig RW, Pika S (2017) Gestural development of chimpanzees in the wild: the impact of interactional experience. Anim Behav 134:271–282Google Scholar
  30. Fröhlich M, Wittig RM, Pika S (2018) The ontogeny of intentional communication in wild chimpanzees. Dev Sci 29:e12716Google Scholar
  31. Genty E, Zuberbühler K (2014) Spatial reference in a bonobo gesture. Curr Biol 24:1601–1605PubMedGoogle Scholar
  32. Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn 12:527–546PubMedPubMedCentralGoogle Scholar
  33. Genty E, Clay Z, Hobaiter C, Zuberbühler K (2014) Multi-modal use of a socially directed call in bonobos. PLoS One 9:e84738PubMedPubMedCentralGoogle Scholar
  34. Gillespie-Lynch K, Greenfield P, Feng Y, Savage-Rumbaugh S, Lyn H (2013) A cross-species study of gesture and its role in symbolic development: implications for the gestural theory of language evolution. Front Psychol 4:160PubMedPubMedCentralGoogle Scholar
  35. Gillespie-Lynch K, Greenfield PM, Lyn H, Savage-Rumbaugh S (2014) Gestural and symbolic development among apes and humans: support for a multimodal theory of language evolution. Front Psychol 5:1228PubMedPubMedCentralGoogle Scholar
  36. Goodall J (1986) The chimpanzees of Gombe: patterns of behaviour. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  37. Graham KE, Furuichi T, Byrne RW (2016) The gestural repertoire of the wild bonobo (Pan paniscus): a mutually understood communication system. Anim Cogn 20:171–177PubMedPubMedCentralGoogle Scholar
  38. Graham K, Hobaiter C, Ounsley J, Furuichi T, Byrne RW (2018) Bonobo and chimpanzee gestures overlap extensively in meaning. PLoS Biol 16:e2004825PubMedPubMedCentralGoogle Scholar
  39. Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol Lett 11:20141051PubMedPubMedCentralGoogle Scholar
  40. Halfwerk W, Page RA, Taylor RC, Wilson PS, Ryan MJ (2014) Crossmodal comparisons of signal components allow for relative-distance assessment. Curr Biol 24:1751–1755PubMedGoogle Scholar
  41. Halina M, Rossano F, Tomasello M (2013) The ontogenetic ritualization of bonobo gestures. Anim Cogn 16:653–666PubMedGoogle Scholar
  42. Hamilton SF (2010) Apprenticeship for adulthood. Simon and Schuster, New YorkGoogle Scholar
  43. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214Google Scholar
  44. Hebets EA, Vink CJ (2007) Experience leads to preference: experienced females prefer brush-legged males in a population of syntopic wolf spiders. Behav Ecol 18:1010–1020Google Scholar
  45. Hewes GW (1973) Primate communication and the gestural origin of language. Curr Anthropol 12:5–24Google Scholar
  46. Higham JP, Hebets EA (2013) An introduction to multimodal communication. Behav Ecol Sociobiol 67:1381–1388Google Scholar
  47. Hobaiter C, Byrne R (2011a) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767PubMedGoogle Scholar
  48. Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cogn 14:827–838PubMedGoogle Scholar
  49. Hobaiter C, Byrne RW (2012) Gesture use in consortship: wild chimpanzees’ use of gesture for an ‘evolutionarily urgent’purpose. In: Pika S, Liebal K (eds) Developments in primate gesture research. John Benjamins Publishing Company, Amsterdam, pp 129–146Google Scholar
  50. Hobaiter C, Byrne RW (2013) Laterality in the gestural communication of wild chimpanzees. Ann N Y Acad Sci 1288:9–16PubMedGoogle Scholar
  51. Hobaiter C, Byrne RW (2014) The meanings of chimpanzee gestures. Curr Biol 24:1596–1600PubMedGoogle Scholar
  52. Hobaiter C, Byrne RW (2017) What is a gesture? A meaning-based approach to defining gestural repertoires. Neurosci Biobehav Rev 82:3–12PubMedGoogle Scholar
  53. Hobaiter C, Leavens DA, Byrne RW (2014) Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases. J Comp Psychol 128:82–87PubMedGoogle Scholar
  54. Hobaiter C, Byrne RW, Zuberbühler K (2017) Wild chimpanzees’ use of single and combined vocal and gestural signals. Behav Ecol Sociobiol 71:96PubMedPubMedCentralGoogle Scholar
  55. Jacob S, Rieucau G, Heeb P (2011) Multimodal begging signals reflect independent indices of nestling condition in European starlings. Behav Ecol 22:1249–1255Google Scholar
  56. Katsu N, Yamada K, Nakamichi M (2017) Influence of social interactions with nonmother females on the development of call usage in Japanese macaques. Anim Behav 123:267–276Google Scholar
  57. Kendon A (2004) Gesture: visible action as utterance. Cambridge University Press, CambridgeGoogle Scholar
  58. Kersken V, Gómez J, Liszkowski U, Soldati A, Hobaiter C (2018) A gestural repertoire of 1–2 year old human children: in seach of the ape gestures. Anim Cogn.  https://doi.org/10.1007/s10071-018-1213-z)
  59. Kuhl PK (2003) Human speech and birdsong: communication and the social brain. Proc Natl Acad Sci U S A 100:9645–9646PubMedPubMedCentralGoogle Scholar
  60. Kuhl PK (2004) Early language acquisition: cracking the speech code. Nat Rev Neurosci 5:831–843PubMedGoogle Scholar
  61. Ladygina-Kohts NN, de Waal FBM (2002) Infant chimpanzee and human child: a classic 1935 comparative study of ape emotions and intelligence. Oxford University Press, New YorkGoogle Scholar
  62. Laporte MNC, Zuberbühler K (2011) The development of a greeting signal in wild chimpanzees. Dev Sci 14:1220–1234PubMedGoogle Scholar
  63. Leavens DA, Bard KA (2011) Environmental influences on joint attention in great apes: implications for human cognition. J Cogn Educ Psychol 10:9–31Google Scholar
  64. Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822PubMedPubMedCentralGoogle Scholar
  65. Leavens DA, Hopkins WD (2005) Multimodal concomitants of manual gesture by chimpanzees: influence of food size and distance. Gesture 5:73–88Google Scholar
  66. Leavens DA, Hopkins WD, Bard KA (2005a) Understanding the point of chimpanzee pointing: epigenesis and ecological validity. Curr Dir Psychol Sci 14:185–189PubMedPubMedCentralGoogle Scholar
  67. Leavens DA, Russell JL, Hopkins WD (2005b) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76:291–306PubMedPubMedCentralGoogle Scholar
  68. Leavens DA, Russell J, Hopkins W (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40PubMedGoogle Scholar
  69. Leavens DA, Bard KA, Hopkins WD (2017) The mismeasure of ape social cognition. Anim Cogn.  https://doi.org/10.1007/s10071-017-1119-1
  70. Liebal K, Call J (2012) The origins of non-human primates' manual gestures. Phil Trans R Soc B 367:118–128PubMedGoogle Scholar
  71. Liebal K, Call J, Tomasello M (2004a) Use of gesture sequences in chimpanzees. Am J Primatol 64:377–396PubMedGoogle Scholar
  72. Liebal K, Pika S, Call J, Tomasello M (2004b) To move or not to move. How apes adjust to the attentional state of others. Interact Stud 5:199–219Google Scholar
  73. Liebal K, Pika S, Tomasello M (2006) Gestural communication of orangutans (Pongo pygmaeus). Gesture 6:1–38Google Scholar
  74. Liebal K, Waller BM, Burrows AM, Slocombe KE (2013) Primate communication: a multimodal approach. Cambridge University Press, CambridgeGoogle Scholar
  75. Liebal K, Schneider C, Errson-Lembeck M (2018) How primates acquire their gestures: evaluating current theories and evidence. Anim Cogn.  https://doi.org/10.1007/s10071-018-1187-x
  76. Lonsdorf EV, Anderson KE, Stanton MA, Shender M, Heintz MR, Goodall J, Murray CM (2014a) Boys will be boys: sex differences in wild infant chimpanzee social interactions. Anim Behav 88:79–83PubMedPubMedCentralGoogle Scholar
  77. Lonsdorf EV, Markham AC, Heintz MR, Anderson KE, Ciuk DJ, Goodall J, Murray CM (2014b) Sex differences in wild chimpanzee behavior emerge during infancy. PLoS One 9:e99099PubMedPubMedCentralGoogle Scholar
  78. Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. Chicago University Press, Chicago, pp 256–291Google Scholar
  79. Marler P (1961) The logical analysis of animal communication. J Theor Biol 1:295–317PubMedGoogle Scholar
  80. Marler P (1965) Communication in monkeys and apes. In: DeVore I (ed) Primate behaviour. Field studies of monkeys and apes. Holt, Rinehart and Winston, New York, pp 544–584Google Scholar
  81. Marler P (1997) Three models of song learning: evidence from behavior. Dev Neurobiol 33:501–516Google Scholar
  82. Matsumoto-Oda A, Tomonaga M (2005) "intentional" control of sound production found in leaf-clipping display of Mahale chimpanzees. J Ethol 23:109–112Google Scholar
  83. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  84. McCarthy MS, Jensvold MLA, Fouts DH (2013) Use of gesture sequences in captive chimpanzee (Pan troglodytes) play. Anim Cogn 16:471–481PubMedGoogle Scholar
  85. Mitani JC, Hunley KL, Murdoch ME (1999) Geographic variation in the calls of wild chimpanzees: a reassessment. Am J Primatol 47:133–151PubMedGoogle Scholar
  86. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
  87. Moore R (2015) Meaning and ostension in great ape gestural communication. Anim Cogn 19:223–231PubMedGoogle Scholar
  88. Munoz NE, Blumstein DT (2012) Multisensory perception in uncertain environments. Behav Ecol 23:457–462Google Scholar
  89. Murray CM, Lonsdorf EV, Stanton MA, Wellens KR, Miller JA, Goodall J, Pusey AE (2014) Early social exposure in wild chimpanzees: mothers with sons are more gregarious than mothers with daughters. Proc Natl Acad Sci U S A 111:18189–18194PubMedPubMedCentralGoogle Scholar
  90. Nishida T (1968) The social group of wild chimpanzees in the Mahali Mountains. Primates 9:167–224Google Scholar
  91. Nishida T (1980) The leaf-clipping display: a newly-discovered expressive gesture in wild chimpanzees. J Hum Evol 9:117–128Google Scholar
  92. Parker JG, Asher SR (1987) Peer relations and later personal adjustment: are low-accepted children at risk? Psychol Bull 102:357–389PubMedGoogle Scholar
  93. Partan SR (2013) Ten unanswered questions in multimodal communication. Behav Ecol Sociobiol 67:1523–1539PubMedPubMedCentralGoogle Scholar
  94. Partan SR, Marler P (1999) Communication goes multimodal. Science 283:1272–1273PubMedGoogle Scholar
  95. Partan SR, Marler P (2005) Issues in the classification of multimodal communication signals. Am Nat 166:231–245PubMedPubMedCentralGoogle Scholar
  96. Perlman M, Tanner JE, King BJ (2012) A mother gorilla’s variable use of touch to guide her infant. In: Pika S, Liebal K (eds) Developments in primate gesture research. John Benjamins Publishing Company, Amsterdam, pp 55–72Google Scholar
  97. Pika S (2008) Gestures of apes and pre-linguistic human children: similar or different? First Lang 28:116–140Google Scholar
  98. Pika S (2012) The case of referential gestural signaling: where next? Commun Integr Biol 5:578–582PubMedPubMedCentralGoogle Scholar
  99. Pika S, Fröhlich M (2018) Gestural acquisition in great apes: the social negotiation hypothesis. Anim Cogn.  https://doi.org/10.1007/s10071-017-1159-6
  100. Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16:R191–R192PubMedGoogle Scholar
  101. Pika S, Zuberbühler K (2008) Social games between bonobos and humans: evidence for shared intentionality? Am J Primatol 70:207–210PubMedGoogle Scholar
  102. Pika S, Liebal K, Tomasello M (2003) Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire, learning, and use. Am J Primatol 60:95–111PubMedGoogle Scholar
  103. Pika S, Liebal K, Tomasello M (2005) Gestural communication in subadult bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61PubMedGoogle Scholar
  104. Plooij FX (1978) Some basic traits of language in wild chimpanzees? In: Lock A (ed) Action, gesture and symbol. Academic Press, London, pp 111–131Google Scholar
  105. Plooij FX (1979) How wild chimpanzee babies trigger the onset of mother-infant play. In: Bullowa M (ed) Before speech. University Press, Cambridge, pp 223–243Google Scholar
  106. Plooij FX (1984) The behavioral development of free-living chimpanzee babies and infants. In: Praeger publishers Inc. USA, WestportGoogle Scholar
  107. Pollick AS, de Waal FBM (2007) Ape gestures and language evolution. P Natl Acad Sci USA 104:8184–8189Google Scholar
  108. Pollick AS, Jeneson A, de Waal FBM (2008) Gestures and multimodal signaling in bonobos. In: Furuichi T, Thompson J (eds) The bonobos. Developments in primatology: Progress and prospects. Springer, New York, pp 75–94Google Scholar
  109. Roberts AI, Vick S-J, Buchanan-Smith HM (2012) Usage and comprehension of manual gestures in wild chimpanzees. Anim Behav 84:459–470Google Scholar
  110. Roberts AI, Roberts SGB, Vick S-J (2014a) The repertoire and intentionality of gestural communication in wild chimpanzees. Anim Cogn 17:317–336PubMedGoogle Scholar
  111. Roberts AI, Vick S-J, Roberts SGB, Menzel CR (2014b) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun 5:3088PubMedPubMedCentralGoogle Scholar
  112. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931PubMedGoogle Scholar
  113. Ruben RJ (1997) A time frame of critical/sensitive periods of language development. Acta Otolaryngol 117:202–205PubMedGoogle Scholar
  114. Ruxton GD, Schaefer HM (2011) Resolving current disagreements and ambiguities in the terminology of animal communication. J Evol Biol 24:2574–2585PubMedGoogle Scholar
  115. Savage-Rumbaugh ES, Wilkerson BJ, Bakeman R (1977) Spontaneous gestural communication among conspecifics in the pygmy chimpanzee (Pan paniscus). In: Bourne GH (ed) Progress in ape research. Academic Press, New York, pp 97–116Google Scholar
  116. Schaller GB (1963) The mountain Gorilla: ecology and behavior. University of Chicago Press, ChicagoGoogle Scholar
  117. Schaller GB (1965) The behaviour of the mountain gorilla. In: de Vore I (ed) Primate behaviour: field studies of monkeys and apes. Holt. Rinehart and Winston, New York, pp 324–367Google Scholar
  118. Scherer KR (1995) Expression of emotion in voice and music. J Voice 9:235–248PubMedGoogle Scholar
  119. Schneider C, Call J, Liebal K (2012a) Onset and early use of gestural communication in nonhuman great apes. Am J Primatol 74:102–113PubMedGoogle Scholar
  120. Schneider C, Call J, Liebal K (2012b) What role do mothers play in the gestural acquisition of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes)? Int J Primatol 33:246–262Google Scholar
  121. Scott-Phillips TC (2015) Meaning in animal and human communication. Anim Cogn 18:801–805PubMedGoogle Scholar
  122. Seyfarth RM, Cheney DL (2017) The origin of meaning in animal signals. Anim Behav 124:339–346Google Scholar
  123. Snowdon CT, Hausberger M (eds) (1997) Social influences on vocal development. Cambridge University Press, CambridgeGoogle Scholar
  124. Tanner JE, Byrne R (1996) Representation of action through iconic gesture in a captive lowland gorilla. Curr Anthropol 37:162–173Google Scholar
  125. Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433Google Scholar
  126. Tomasello M (1990) Cultural transmission in the tool use and communicatory signalling of chimpanzees. In: Parker ST, Gibson KR (eds) Language' and intelligence in monkeys and apes: comparative developmental perspectives. Cambridge University Press, Cambridge, pp 274–311Google Scholar
  127. Tomasello M (2008) Origins of human communication vol 2008. MIT press, Cambridge, MAGoogle Scholar
  128. Tomasello M, Call J (2018) Thirty years of great ape gestures. Anim Cogn.  https://doi.org/10.1007/s10071-018-1167-1)
  129. Tomasello M, George BL, Kruger AC, Jeffrey M, Farrar EA (1985) The development of gestural communication in young chimpanzees. J Hum Evol 14:175–186Google Scholar
  130. Tomasello M, Gust D, Frost GT (1989) A longitudinal investigation of gestural communication in young chimpanzees. Primates 30:35–50Google Scholar
  131. Tomasello M, Call J, Nagell K, Olguin R, Carpenter M (1994) The learning and use of gestural signals by young chimpanzees: a trans-generational study. Primates 35:137–154Google Scholar
  132. Tomasello M, Call J, Warren J, Frost GT, Carpenter M, Nagell K (1997) The ontogeny of chimpanzee gestural signals: a comparison across groups and generations. Evol Commun 1:223–259Google Scholar
  133. Townsend SW, Koski SE, Byrne RW, Slocombe KE, Bickel B, Boeckle M, Braga Goncalves I, Burkart JM, Flower T, Gaunet F, Glock HJ, Gruber T, Jansen DAWAM, Liebal K, Linke A, Miklósi Á, Moore R, van Schaik CP, Stoll S, Vail A, Waller BM, Wild M, Zuberbühler K, Manser MB (2017) Exorcising Grice's ghost: an empirical approach to studying intentional communication in animals. Biol Rev 92:1427–1433PubMedGoogle Scholar
  134. van Lawick-Goodall J (1967) Mother–offspring relationships in free-ranging chimpanzees. In: Morris D (ed) Primate ethology. Weidenfeld and Nicolson, London, pp 287–346Google Scholar
  135. van Lawick-Goodall J (1968) The behavior of free-ranging chimpanzees in the Gombe stream reserve. Anim Behav Monogr 1:161–311Google Scholar
  136. van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94PubMedGoogle Scholar
  137. van Schaik CP, Deaner RO, Merrill MY (1999) The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol 36:719–741PubMedGoogle Scholar
  138. van Schaik CP, Marshall AJ, Wich SA (2009) Geographic variation in orangutan behavior and biology. In: Wich S, Utami-Atmoko S, Setia T, van Schaik C (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 351–361Google Scholar
  139. Waller BM, Liebal K, Burrows AM, Slocombe KE (2013) How can a multimodal approach to primate communication help us understand the evolution of communication? Evol Psychol 11:538–549PubMedGoogle Scholar
  140. Whiten A, Goodall J, McGrew C, Nishida T, Reynolds V, Sugiyama Y, Tutin CES, Wrangham R, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685PubMedGoogle Scholar
  141. Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schürmann C, van Hooff JARAM, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398PubMedGoogle Scholar
  142. Wilke C, Kavanagh E, Donnellan E, Waller BM, Machanda ZP, Slocombe KE (2017) Production of and responses to unimodal and multimodal signals in wild chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 123:305–316Google Scholar
  143. Wilson EO (1976) Sociobiology. Cambridge, BelknapGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of ZurichZurichSwitzerland
  2. 2.School of Psychology and Neuroscience, St Marys CollegeUniversity of St AndrewsSt AndrewsScotland

Personalised recommendations