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Learned vocal and breathing behavior in an enculturated gorilla

Animal Cognition volume 18, pages 1165–1179 (2015)Cite this article

Abstract

We describe the repertoire of learned vocal and breathing-related behaviors (VBBs) performed by the enculturated gorilla Koko. We examined a large video corpus of Koko and observed 439 VBBs spread across 161 bouts. Our analysis shows that Koko exercises voluntary control over the performance of nine distinctive VBBs, which involve variable coordination of her breathing, larynx, and supralaryngeal articulators like the tongue and lips. Each of these behaviors is performed in the context of particular manual action routines and gestures. Based on these and other findings, we suggest that vocal learning and the ability to exercise volitional control over vocalization, particularly in a multimodal context, might have figured relatively early into the evolution of language, with some rudimentary capacity in place at the time of our last common ancestor with great apes.

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Notes

  1. We limit our review of the literature to primates, but there is of course extensive and highly relevant research on vocal abilities in non-primate species too, including cetaceans, pinnipeds, and birds, among others (e.g., Janik and Slater 1997; Marler 2000; Schusterman 2008).

  2. Her production of voicing specifically when performing talk on phone and when vocalizing into an object tip, often referred to as her microphone, hints at the possibility that Koko is doing her “imitation” of human speech.

References

  • Arbib MA (2012) How the brain got language: the mirror system hypothesis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Arbib MA, Liebal K, Pika S (2008) Primate vocalization, gesture and the evolution of human language. Curr Anthropol 49:1053–1076

    Article  PubMed  Google Scholar 

  • Bickerton D (1990) Language and species. University of Chicago Press, Chicago

    Google Scholar 

  • Birdwhistell R (1970) Kinesics and context: essays on body motion communication. University of Pennsylvania Press, Philadelphia

    Google Scholar 

  • Burling R (1993) Primate calls, human language, and nonverbal communication. Curr Anthropol 34:25–53

    Article  Google Scholar 

  • Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Taylor and Francis, New York

    Google Scholar 

  • Cheney DL, Seyfarth RM (1985) Vervet monkey alarm calls: manipulation through shared information? Behaviour 94:150–166

    Article  Google Scholar 

  • Corballis M (2002) From hand to mouth: the origins of language. Princeton University Press, Princeton

    Google Scholar 

  • Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243

    Article  Google Scholar 

  • Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22:142–146

    CAS  Article  PubMed  Google Scholar 

  • Fitch WT (2006) Production of vocalizations in mammals. In: Brown K (ed) Encyclopedia of language and linguistics. Oxford University Press, Oxford, pp 115–121

    Chapter  Google Scholar 

  • Fitch WT (2010) The evolution of language. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Furness WH (1916) Observations on the mentality of chimpanzees and orang-utans. Proc Am Philos Soc 55:281–290

    Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Hardus ME, Lameira AR, Van Schaik CP, Wich SA (2009) Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation? Philos Trans R Soc B 276:3689–3694

    Google Scholar 

  • Hauser MD (1996) The evolution of communication. MIT Press, Cambridge

    Google Scholar 

  • Hayes C (1951) The ape in our house. Harper, New York

    Google Scholar 

  • Hewes GW (1973) Primate communication and the gestural origins of language. Curr Anthropol 14:5–24

    Article  Google Scholar 

  • Hopkins WD, Savage-Rumbaugh S (1991) Vocal communication as a function of differential rearing experiences in Pan paniscus: a preliminary report. Int J Primatol 12:559–583

    Article  Google Scholar 

  • Hopkins WD, Taglialatela JP, Leavens DA (2007) Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim Behav 73:281–286

    PubMed Central  Article  PubMed  Google Scholar 

  • Janik VM, Slater PJB (1997) Vocal learning in mammals. Adv Study Behav 26:59–99

    Article  Google Scholar 

  • Kellogg WN, Kellogg LA (1933) The ape and the child: a study of environmental influence upon early behavior. Whittelsey House, Oxford

    Google Scholar 

  • Kendon A (2004) Gesture: visible action as utterance. Cambridge University Press, Cambridge

    Google Scholar 

  • Kendon A (2009) Language’s matrix. Gesture 9:352–372

    Article  Google Scholar 

  • Krauss MA, Fouts RS (1997) Chimpanzee (Pan troglodytes) pointing: hand shapes, accuracy, and the role of eye gaze. J Comp Psychol 11:330–336

    Article  Google Scholar 

  • Laidler K (1980) The talking ape. Stein and Day, New York

    Google Scholar 

  • Lancaster JB (1968) Primate communication systems and the emergence of human language. In: Jay PC (ed) Primates: studies in adaptation and variability. Holt, Rinehart & Winston, New York, pp 439–457

    Google Scholar 

  • Laporte MNC, Zuberbühler K (2010) Vocal greeting behavior in wild chimpanzee females. Anim Behav 80:467–473

    Article  Google Scholar 

  • Leavens DA (2003) Integration of visual and vocal communication: evidence for Miocene origins. Behav Brain Sci 26:232–233

    Article  Google Scholar 

  • Leavens DA, Hostetter AB, Wesley MJ, Hopkins WD (2004) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 80:467–476

    Article  Google Scholar 

  • Leavens DA, Russell JL, Hopkins WD (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40

    PubMed Central  Article  PubMed  Google Scholar 

  • Levinson SC, Holler J (2014) The origin of human multi-modal communication. Philos Trans R Soc B 369:20130302. doi:10.1098/rstb.2013.0302

    Article  Google Scholar 

  • Lieberman P (1969) On the acoustic analysis of primate vocalizations. Behav Res Methods Instrum 1:169–174

    Article  Google Scholar 

  • Marler P (2000) Origins of music and speech: insights from animals. In: Wallin NL, Merker B, Brown S (eds) The origins of music. MIT Press, Cambridge, pp 31–48

    Google Scholar 

  • Marshall AJ, Wrangham RW, Arcadi AC (1999) Does learning affect the structure of vocalizations in chimpanzees? Anim Behav 58:825–830

    Article  PubMed  Google Scholar 

  • McNeill D (1992) Hand and mind. University of Chicago Press, Chicago

    Google Scholar 

  • McNeill D (2012) How language began: gesture and speech in human evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mitani JC, Gros-Louis J (1998) Chorusing and call convergence in chimpanzees: tests of three hypotheses. Behaviour 135:1041–1064

    Article  Google Scholar 

  • Myers RE (1976) Comparative neurology of vocalization and speech: proof of a dichotomy. Ann N Y Acad Sci 280:745–757

    CAS  Article  PubMed  Google Scholar 

  • Owren MJ, Amoss RT, Rendall D (2011) Two organizing principles of vocal production: implications for nonhuman and human primates. Am J Primatol 73:530–544

    Article  PubMed  Google Scholar 

  • Patterson FG, Linden E (1981) The education of Koko. Holt, Rinehart &Winston, New York

    Google Scholar 

  • Perlman MS, Gibbs RW Jr (2013) Pantomimic gestures reveal the sensorimotor imagery of a human-fostered gorilla. J Ment Imaging 37:73–96

    Google Scholar 

  • Perlman MS, Patterson FG, Cohn RH (2012) The human-fostered gorilla Koko shows breath control in play with wind instruments. Biolinguistics 6:433–444

    Google Scholar 

  • Pierce JD (1985) A review of attempts to condition operantly alloprimate vocalizations. Primates 26:202–213

    Article  Google Scholar 

  • Pinker S (1994) The language instinct. William Morrow & Co., New York

    Book  Google Scholar 

  • Pinker S, Bloom P (1990) Natural language and natural selection. Behav Brain Sci 13:707–727

    Article  Google Scholar 

  • Pollick AS, de Waal FBM (2007) Ape gestures and language evolution. Proc Natl Acad Sci 104:8184–8189

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Premack D (2004) Is language the key to human intelligence? Science 303:318–320

    CAS  Article  PubMed  Google Scholar 

  • Salmi R, Hammerschmidt K, Doran-Sheehy DM (2013) Western gorilla vocal repertoire and contextual use of vocalization. Ethology 119:831–847

    Article  Google Scholar 

  • Schel AM, Townsend SW, Machanda Z, Zuberbühler K, Slocombe K (2013) Chimpanzee alarm call production meets key criteria for intentionality. PLoS One 8:e76674. doi:10.1371/journal.pone.0076674

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Schusterman RJ (2008) Vocal learning in mammals with a special emphasis on pinnipeds. In: Oller DK, Gribel U (eds) The evolution of communicative flexibility: complexity, creativity, and adaptability in human and animal communication. MIT Press, Cambridge, pp 41–70

    Chapter  Google Scholar 

  • Skinner BF (1957) Verbal behavior. Appleton-Century-Crofts, New York

    Book  Google Scholar 

  • Sutton D, Larson C, Taylor EM, Lindeman RC (1973) Vocalization in rhesus monkeys: conditionability. Brain Res 52:225–231

    CAS  Article  PubMed  Google Scholar 

  • Taglialatela JP, Savage-Rumbaugh S, Baker LA (2003) Vocal production by a language-competent Pan paniscus. Int J Primatol 24:1–17

    Article  Google Scholar 

  • Taglialatela JP, Russell JL, Schaeffer JA, Hopkins WD (2011) Chimpanzee vocal signaling points to a multimodal origin of human language. PLoS One 6:e18852. doi:10.1371/journal.pone.0018852

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suzuki A, Utami SS, Merrill M (2003) Orangutan cultures and the evolution of material culture. Science 3:102–105

    Article  Google Scholar 

  • van Schaik CP, van Noordwijk MA, Wich SA (2006) Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour 143:839–876

    Article  Google Scholar 

  • Waller B, Liebal K, Burrows A, Slocombe K (2013) How can a multimodal approach to primate communication help us understand the evolution of communication? Evol Psychol 11:538–549

    Article  PubMed  Google Scholar 

  • Watson SK, Townsend SW, Schel AM, Wilke C, Wallace EK, Cheng L, West V, Slocombe KE (2015) Vocal learning in the functionally referential food grunts of chimpanzees. Curr Biol 25:495–499

    CAS  Article  PubMed  Google Scholar 

  • Wich SA, Swartz KB, Hardus ME, Lameira AR, Stromberg E, Shumaker RW (2009) A case of spontaneous acquisition of a human sound by an orangutan. Primates 50:56–64

    Article  PubMed  Google Scholar 

  • Wilson ML, Hauser MD, Wrangham RW (2001) Does participation in intergroup conflict depend on numerical assessment, range location, or rank for wild chimpanzees? Anim Behav 61:1203–1216

    Article  Google Scholar 

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Acknowledgments

We are grateful to videographer Dr. Ronald Cohn and the Gorilla Foundation for providing the video on which this article is based, and for their permission to post the video clips in Supplementary Information. We are also grateful to Katarina Noelle for her assistance with the research.

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Authors and Affiliations

  1. Department of Psychology, University of Wisconsin-Madison, 1202 W. Johnson St., Madison, WI, 53707, USA

    Marcus Perlman

  2. Department of Psychology, University of California, Santa Cruz, Santa Cruz, CA, USA

    Nathaniel Clark

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  1. Marcus Perlman
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  2. Nathaniel Clark
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Correspondence to Marcus Perlman.

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All applicable national guidelines for the care and use of animals were followed. All the procedures performed were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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The authors of the article relied on certain information and materials made available by The Gorilla Foundation. The authors are solely responsible for the content of the article, and the article shall not constitute any representation by The Gorilla Foundation that the data presented therein are correct or sufficient to support the conclusions reached.

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Perlman, M., Clark, N. Learned vocal and breathing behavior in an enculturated gorilla. Anim Cogn 18, 1165–1179 (2015). https://doi.org/10.1007/s10071-015-0889-6

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Keywords

  • Breath control
  • Gorilla
  • Koko
  • Multimodal communication
  • Primate vocalization
  • Vocal learning