Abstract
Comparing the communicative abilities of humans and great apes is a commonly used research strategy to understand the evolutionary foundation of modern human language. The ability to combine signals from different communicative modes (vocal, gestural, facial, etc.) is a universal and important feature of human language that is shared with great apes, although rarely investigated. Research on apes’ signal combination has usually studied the frequency, distribution, effectiveness, and function of combinations in comparison with single signals, but only seldom have studies addressed their functional specificity, i.e., their ability to convey specific signallers’ goals within contexts. Here, I suggest a new methodological approach to the investigation of functional specificity of signals, which consists of focusing on one call type and exploring its various patterns of production when combined with gestures. I illustrate the different methodological steps with a case study on infant bonobos’ combinations of ‘Pout moan’ calls with gestures in the context of infant-to-mother requests. The descriptive results indicate that at least three combinations seem functionally specific, i.e., specific to the infants’ desired goals. It suggests that combinations can be functionally specific from a young age and that learning how to combine signals efficiently might occur early in ontogeny. This suggested approach might provide insight to the on-going debate regarding the mechanisms underpinning the learning process of successful signal production and potentially further our understanding of the evolution of the combinatorial characteristics of human communication.
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Notes
The Ontogenetic ritualization hypothesis predicts that any action can be ritualized into a communicative gesture. Ontogenetic ritualization is described as a process through which functional behaviours are progressively abbreviated and shaped into a communicative signal following unintentional reinforcement by a partner during repetitive interactions, with partner-specific’s outcomes in different dyads for the same purpose (Tomasello 1996).
The Genetic channelling (or Phylogenetic ritualization) hypothesis predicts that gestures derive from an ape’s biological inheritance, shaped by evolution and not by learning (Genty et al. 2009; Hobaiter and Byrne 2011a). It predicts that gestures forms, and repertoire sizes, are quite constant throughout development and across species, although their contextual use is very flexible (Byrne et al. 2017; Graham et al. 2018).
The Social negotiation hypothesis postulates that gesture acquisition is a dynamic process through which interacting partners mutually shape the communicative outcome of gestures in real time. This process results in a shared understanding of the contextual use and function of each gesture, that can be generalized across dyads (Pika and Fröhlich 2018).
References
Acredolo L, Goodwyn S (1988) Symbolic gesturing in normal infants. Child Dev 59:450–466
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Arnold K, Zuberbühler K (2006) Language evolution: semantic combinations in primate calls. Nature 441:303. https://doi.org/10.1038/441303a
Bard KA, Dunbar S, Maguire-Herring V et al (2014) Gestures and social-emotional communicative development in chimpanzee infants. Am J Primatol 76:14–29. https://doi.org/10.1002/ajp.22189
Bates E, Benigni L, Bretherton I et al (1979) The emergence of symbols. Academic Press, New York
Bohn M, Call J, Tomasello M (2015) Communication about absent entities in great apes and human infants. Cognition 145:63–72. https://doi.org/10.1016/j.cognition.2015.08.009
Brosnan SF, de Waal FBM (2000) Regulation of vocal output by chimpanzees finding food in the presence or absence of an audience. Evol Commun 4:211–224. https://doi.org/10.1075/eoc.4.2.05bro
Byrne RW, Cartmill E, Genty E et al (2017) Great ape gestures: intentional communication with a rich set of innate signals. Anim Cogn 20:755–769. https://doi.org/10.1007/s10071-017-1096-4
Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Taylor and Francis Group/Lawrence Erlbaum Associates, New York
Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348. https://doi.org/10.1016/j.cub.2007.06.069
Cartmill EA, Byrne RW (2010) Semantics of primate gestures: intentional meanings of orangutan gestures. Anim Cogn 13:793–804. https://doi.org/10.1007/s10071-010-0328-7
Cäsar C, Byrne RW, Hoppitt W et al (2012) Evidence for semantic communication in titi monkey alarm calls. Anim Behav 84:405–411
Caselli MC, Volterra V (1990) From communication to language in hearing and deaf children. In: Caselli MC, Erting CJ (eds) From gesture to language in hearing and deaf children. Springer, Berlin, pp 263–277
Cassell J, McNeill D, McCullogh KE (1999) Speech-gesture mismatches: evidence for one underlying representation of linguistic and nonlinguistic information. Pragmact Cogn 7:1–33
Clay Z, Zuberbühler K (2012) Communication during sex among female bonobos: effects of dominance, solicitation and audience. Sci Rep 2:291. https://doi.org/10.1038/srep00291
Clay Z, Archbold J, Zuberbühler K (2015) Functional flexibility in wild bonobo vocal behaviour. PeerJ 3:e1124. https://doi.org/10.7717/peerj.1124
Cooper BG, Goller F (2004) Multimodal signals: enhancement and constraint of song motor patterns by visual display. Science 303:544–546. https://doi.org/10.1126/science.1091099
Corballis MC (2008) The gestural origins of language. In: Masataka N (ed) The origins of language. Springer, Tokyo, pp 11–23
Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243
Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22:142–146. https://doi.org/10.1016/j.cub.2011.11.053
Crockford C, Wittig RM, Zuberbühler K (2015) An intentional vocalization draws others’ attention: a playback experiment with wild chimpanzees. Anim Cogn 18:581–591. https://doi.org/10.1007/s10071-014-0827-z
de Luna AG, Hödl W, Amezquita A (2010) Colour, size and movement as visual subcomponents in multimodal communication by the frog Allobates femoralis. Anim Behav 79:739–745
de Rader NV, Zukow-Goldring P (2010) How the hands control attention during early word learning. Gesture 10:202–221. https://doi.org/10.1075/gest.10.2-3.05rad
de Waal FB (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251
Fischer J, Wheeler BC, Higham JP (2015) Is there any evidence for vocal learning in chimpanzee food calls? Curr Biol 25(21):1028–1029
Fitch WT (2010) The evolution of language. Cambridge University Press, Cambridge
Frank MC, Slemmer JA, Marcus GF, Johnson SP (2009) Information from multiple modalities helps 5-month-olds learn abstract rules. Dev Sci 12:504–509. https://doi.org/10.1111/j.1467-7687.2008.00794.x
Fröhlich M, van Schaik CP (2018) The function of primate multimodal communication. Anim Cogn 21:619–629. https://doi.org/10.1007/s10071-018-1197-8
Fröhlich M, Kuchenbuch P, Müller G et al (2016a) Unpeeling the layers of language: bonobos and chimpanzees engage in cooperative turn-taking sequences. Sci Rep 6:25887
Fröhlich M, Wittig RM, Pika S (2016b) Should I stay or should I go? Initiation of joint travel in mother–infant dyads of two chimpanzee communities in the wild. Anim Cogn 19:483–500. https://doi.org/10.1007/s10071-015-0948-z
Fröhlich M, Müller G, Zeiträg C et al (2017) Gestural development of chimpanzees in the wild: the impact of interactional experience. Anim Behav 134:271–282. https://doi.org/10.1016/j.anbehav.2016.12.018
Fusani L, Hutchison RE, Hutchison JB (1997) Vocal-postural co-ordination of a sexually dimorphic display in a monomorphic species: the Barbary dove. Behaviour 134:321–335
Gardner RA, Gardner BT (1969) Teaching sign language to a chimpanzee. Science 165:664–672
Genty E, Byrne RW (2009) Why do gorillas make sequences of gestures? Anim Cogn 13:287–301. https://doi.org/10.1007/s10071-009-0266-4
Genty E, Zuberbühler K (2014) Spatial reference in a bonobo gesture. Curr Biol 24:1601–1605. https://doi.org/10.1016/j.cub.2014.05.065
Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn 12:527–546. https://doi.org/10.1007/s10071-009-0213-4
Genty E, Clay Z, Hobaiter C, Zuberbühler K (2014) Multi-Modal use of a socially directed call in bonobos. PLoS One 9:e84738. https://doi.org/10.1371/journal.pone.0084738
Genty E, Neumann C, Zuberbühler K (2015a) Bonobos modify communication signals according to recipient familiarity. Sci Rep 5:85. https://doi.org/10.1038/srep16442
Genty E, Neumann C, Zuberbühler K (2015b) Complex patterns of signalling to convey different social goals of sex in bonobos, Pan paniscus. Sci Rep 5:16135. https://doi.org/10.1038/srep16135
Ghazanfar AA, Hauser MD (1999) The neuroethology of primate vocal communication: substrates for the evolution of speech. Trends Cogn Sci 3:377–384. https://doi.org/10.1016/S1364-6613(99)01379-0
Gillespie-Lynch K, Greenfield PM, Lyn H, Savage-Rumbaugh S (2011) The role of dialogue in the ontogeny and phylogeny of early symbol combinations: a cross-species comparison of bonobo, chimpanzee, and human learners. First Lang 31:442–460. https://doi.org/10.1177/0142723711406882
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. https://doi.org/10.3389/fpsyg.2014.01228
Gogate LJ, Bolzani LH, Betancourt EA (2006) Attention to maternal multimodal naming by 6- to 8-month-old infants and learning of word–object relations. Infancy 9:259–288. https://doi.org/10.1207/s15327078in0903_1
Goldin-Meadow S (1999) The role of gesture in communication and thinking. Trends Cogn Sci 3:419–429. https://doi.org/10.1016/S1364-6613(99)01397-2
Goldin-Meadow S, Wein D, Chang C (1992) Assessing knowledge through gesture: using children’s hands to read their minds. Cogn Instr 9:201–219
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press of Harvard University Press, Cambridge
Graham KE, Hobaiter C, Ounsley J et al (2018) Bonobo and chimpanzee gestures overlap extensively in meaning. PLoS Biol 16:e2004825. https://doi.org/10.1371/journal.pbio.2004825
Greenfield PM, Smith JH (1976) Structure of communication in early language development. Academic Press
Gruber T, Zuberbühler K (2013) Vocal recruitment for joint travel in wild chimpanzees. PLoS One 8:e76073
Halina M, Rossano F, Tomasello M (2013) The ontogenetic ritualization of bonobo gestures. Anim Cogn 16:653–666. https://doi.org/10.1007/s10071-013-0601-7
Hauser MD (1996) The evolution of communication. MIT Press, Cambridge
Hauser MD, Chomsky N, Fitch WT (2002) The faculty of language: what is it, who has it, and how did it evolve? Science 298:1569–1579
Hauser MD, Yang C, Berwick RC et al (2014) The mystery of language evolution. Front Psychol 5:85. https://doi.org/10.3389/fpsyg.2014.00401
Hennessy DF, Owings DH, Rowe MP et al (1981) The information afforded by a variable signal: constraints on snake-elicited tail flagging by California ground squirrels. Behaviour 78:188–226
Hewes HG (1973) Primate communication and the gestural origin of language. Curr Anthropol 14:5–24
Higham JP, Hebets EA (2013) An introduction to multimodal communication. Behav Ecol Sociobiol 67:1381–1388
Higham JP, Pfefferle D, Heistermann M et al (2013) Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior. Behav Ecol Sociobiol 67:1457–1469. https://doi.org/10.1007/s00265-013-1521-x
Hobaiter C, Byrne RW (2011a) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767. https://doi.org/10.1007/s10071-011-0409-2
Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cogn 14:827–838. https://doi.org/10.1007/s10071-011-0416-3
Hobaiter C, Leavens DA, Byrne RW (2014) Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases. J Comp Psychol 128:82
Hobaiter C, Byrne RW, Zuberbühler K (2017) Wild chimpanzees’ use of single and combined vocal and gestural signals. Behav Ecol Sociobiol 71:96. https://doi.org/10.1007/s00265-017-2325-1
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
Iverson JM, Capirci O, Longobardi E, Cristina Caselli M (1999) Gesturing in mother-child interactions. Cogn Dev 14:57–75. https://doi.org/10.1016/S0885-2014(99)80018-5
Kalan AK, Boesch C (2015) Audience effects in chimpanzee food calls and their potential for recruiting others. Behav Ecol Sociobiol 69:1701–1712. https://doi.org/10.1007/s00265-015-1982-1
Kano T (1992) The last ape: Pygmy chimpanzee behavior and ecology. Stanford University Press, Redwood City
Kuroda S (1989) Developmental retardation and behavioral characterisitcs of Pygmy chimpanzees. In: Heltne P, Marquardt A (eds) Understanding chimpanzees. Chicago Academy of Sciences, Chicago, pp 184–193
Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813
Leavens DA, Hopkins WD (2005) Multimodal concomitants of manual gesture by chimpanzees (Pan troglodytes): influence of food size and distance. Gesture 5:75–90. https://doi.org/10.1075/gest.5.1.07lea
Leavens DA, Hopkins WD, Thomas RK (2004a) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57. https://doi.org/10.1037/0735-7036.118.1.48
Leavens DA, Hostetter AB, Wesley MJ, Hopkins WD (2004b) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 67:467–476. https://doi.org/10.1016/j.anbehav.2003.04.007
Leavens DA, Russell JL, Hopkins WD (2005) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76:291–306. https://doi.org/10.1111/j.1467-8624.2005.00845.x
Leavens DA, Russell JL, Hopkins WD (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40. https://doi.org/10.1007/s10071-009-0242-z
Legerstee M (1990) Infants use multimodal information to imitate speech sounds. Infant Behav Dev 13:343–354. https://doi.org/10.1016/0163-6383(90)90039-B
Levinson SC, Holler J (2014) The origin of human multi-modal communication. Phil Trans R Soc B 369:20130302
Liebal K, Call J, Tomasello M, Pika S (2004) To move or not to move: how apes adjust to the attentional state of others. Interact Stud 5:199–219
Liebal K, Waller BM, Slocombe KE, Burrows AM (2013) Primate communication: a multimodal approach. Cambridge University Press, Cambridge
Liebal K, Schneider C, Errson-Lembeck M (2018) How primates acquire their gestures: evaluating current theories and evidence. Anim Cogn 15:85. https://doi.org/10.1007/s10071-018-1187-x
Lyn H, Greenfield PM, Savage-Rumbaugh ES (2011) Semiotic combinations in Pan: a comparison of communication in a chimpanzee and two bonobos. First Lang 31:300–325. https://doi.org/10.1177/0142723710391872
McNeill D (1992) Hand and Mind: What gestures reveal about thought. University of Chicago Press, Chicago
Micheletta J, Engelhardt A, Matthews L et al (2012) Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra). Am J Primatol 75:1–11
Miles HL (1990) The cognitive foundations for reference in a signing orangutan. In: Parker ST, Gibson KR (eds) “Language” and intelligence in monkeys and apes: Comparative developmental perspectives. Cambridge University Press, New York, pp 511–539
Papoušek M (1992) Early ontogeny of vocal communication in parent-infant interactions. In: Jürgens U, Papousek M, Papoušek H (eds) Nonverbal vocal communication: comparative and developmental approaches. Cambridge University Press, Cambridge, pp 230–261
Partan SR (2002) Single and multichannel signal composition: facial expressions and vocalizations of rhesus macaques (Macaca mulatta). Behaviour 139:993–1027
Partan SR, Marler P (2005) Issues in the classification of multimodal communication signals. Am Nat 166:231–245
Partan SR, Fulmer AG, Gounard MA, Redmond JE (2010) Multimodal alarm behavior in urban and rural gray squirrels studied by means of observation and a mechanical robot. Curr Zool 56:313–326
Perlman M, Clark N, Tanner JE (2014) Iconicity and ape gesture. In: Evolution of language: proceedings of the 10th international conference (EVOLANG10). World Scientific, New Jersey, pp 228–235
Pika S, Fröhlich M (2018) Gestural acquisition in great apes: the social negotiation hypothesis. Anim Cogn 1–15. https://doi.org/10.1007/s10071-017-1159-6
Pika S, Liebal K (2006) Differences and similarties between the natural gestural communication of the great apes and human children. In: Evolution of language: proceedings of the 6th international conference (EVOLAN6). World Scientific, London, pp 267–274
Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16:R191–R192. https://doi.org/10.1016/j.cub.2006.02.037
Pollick AS, de Waal F (2007) Ape gestures and language evolution. Proc Natl Acad Sci 104:8184–8189
Pollick A, Jeneson A, de Waal F (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 75–94
Rigaill L, Higham JP, Lee PC et al (2013) Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). Am J Primatol 75:774–787
Roberts AI, Vick S-J, Roberts SGB, Menzel CR (2014) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun. https://doi.org/10.1038/ncomms4088
Rossano F (2013) Sequence organization and timing of bonobo mother-infant interactions. Interact Stud 14:160–189
Rowe C, Guilford T (1996) Hidden colour aversions in domestic chicks triggered by pyrazine odours of insect warning displays. Nature 383:520–522. https://doi.org/10.1038/383520a0
Scheiner E, Hammerschmidt K, Jürgens U, Zwirner P (2002) Acoustic analyses of developmental changes and emotional expression in the preverbal vocalizations of infants. J Voice 16:509–529. https://doi.org/10.1016/S0892-1997(02)00127-3
Schel AM, Townsend SW, Machanda Z et al (2013) Chimpanzee alarm call production meets key criteria for intentionality. PLoS One 8:e76674. https://doi.org/10.1371/journal.pone.0076674
Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15:1779–1784. https://doi.org/10.1016/j.cub.2005.08.068
Slocombe KE, Kaller T, Turman L et al (2010) Production of food-associated calls in wild male chimpanzees is dependent on the composition of the audience. Behav Ecol Sociobiol 64:1959–1966
Slocombe KE, Waller BM, Liebal K (2011) The language void: the need for multimodality in primate communication research. Anim Behav 81:919–924. https://doi.org/10.1016/j.anbehav.2011.02.002
Taglialatela JP, Russell JL, Schaeffer JA, Hopkins WD (2011) Chimpanzee vocal signaling points to a multimodal origin of human language. PLoS One 6:e18852. https://doi.org/10.1371/journal.pone.0018852
Taglialatela JP, Russell JL, Pope SM et al (2015) Multimodal communication in chimpanzees. Am J Primatol 77:1143–1148. https://doi.org/10.1002/ajp.22449
Thompson LA, Massaro DW (1986) Evaluation and integration of speech and pointing gestures during referential understanding. J Exp Child Psychol 42:144–168
Tomasello M (1995) Language is not an instinct. Cogn Dev 10:131–156
Tomasello M (1996) Do apes ape? In: Heyes CM, Galef BG Jr (eds) Social learning in animals: the roots of culture. Academic Press, San Diego, pp 319–346
Townsend SW, Zuberbuhler K (2009) Audience effects in chimpanzee copulation calls. Commun Integr Biol 2:282–284. https://doi.org/10.4161/cib.2.3.6796
Tronick E, Brazelton TB, Als H (2013) The structure of face-to-face interaction and its developmental functions. Sign Lang Stud 18:1–16. https://doi.org/10.1353/sls.1978.0011
Uetz GW, Roberts JA, Taylor PW (2009) Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Anim Behav 78:299–305. https://doi.org/10.1016/j.anbehav.2009.04.023
Watson SK, Townsend SW, Schel AM et al (2015) Vocal learning in the functionally referential food grunts of chimpanzees. Curr Biol 25:495–499. https://doi.org/10.1016/j.cub.2014.12.032
Wilke C, Kavanagh E, Donnellan E et al (2017) Production of and responses to unimodal and multimodal signals in wild chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 123:305–316. https://doi.org/10.1016/j.anbehav.2016.10.024
Zuberbühler K (2005) The phylogenetic roots of language: evidence from primate communication and cognition. Curr Dir Psychol Sci 14:126–130. https://doi.org/10.1111/j.0963-7214.2005.00357.x
Acknowledgements
I would like to thank Klaus Zuberbühler for making this research possible and for his long-term collaboration and support. Thanks to Sarah McHugh for acting as a second rater and to Christof Neumann and Raphaela Heesen for their help in creating the figures. I am grateful to Claudine André and Brian Hare for permission to work at ‘Lola Ya Bonobo’, to Pierrot Mbonzo, Fanny Minesi and Raphaël Belais for their administrative support, and to the Ministry of Research and the Ministry of Environment in the Democratic Republic of Congo for giving me permission to carry out this research. I am grateful to all the Lola staff for their assistance. A very special thank you to E.A. Cartmill and Jacob G. Foster for fruitful discussions and invaluable comments and suggestions on this manuscript. Special thanks to E. A. Cartmill and C. Hobaiter for inviting me to contribute to this Special Issue.
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Studies from the author reported in this manuscript have received funding from the European Commission Sixth Framework Programme ‘Origins of Referential Communication’, contract 12787, the Leverhulme Research Leadership Award No F00268AP, the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement no 283871, and the Swiss National Science Foundation ‘Coordinating joint action in apes: Testing the boundaries of the human interaction engine’ CR31I3_159655.
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Genty, E. Vocal–gestural combinations in infant bonobos: new insights into signal functional specificity. Anim Cogn 22, 505–518 (2019). https://doi.org/10.1007/s10071-019-01267-0
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DOI: https://doi.org/10.1007/s10071-019-01267-0