Advertisement

Animal Cognition

, Volume 18, Issue 3, pp 581–591 | Cite as

An intentional vocalization draws others’ attention: A playback experiment with wild chimpanzees

  • Catherine Crockford
  • Roman M. Wittig
  • Klaus Zuberbühler
Original Paper

Abstract

A vital step in the evolution of language is likely to have been when signalers explicitly intended to direct recipients’ attention to external objects with the use of referential signals. Although animal signals can direct the attention of others to external events, such as in monkey predator alarm calls, there is little evidence that this is the result of an intention to inform the recipient. Two recent studies, however, indicate that the production of chimpanzee quiet alarm calls, given to snakes, complies with some standard behavioral markers of intentional signaling, such as gaze alternation. But it is currently unknown whether the calls alone direct receivers’ attention to the threat. To address this, we carried out a playback experiment with free-ranging chimpanzees in Budongo Forest, Uganda, using a within-subjects design. From a hidden speaker, we broadcast either quiet alarm ‘hoos’ (‘alert hoos’) or acoustically distinguishable hoos produced while resting (‘rest hoos’) and found a significant increase in search behavior after ‘alert’ compared with ‘rest’ hoos, with subjects monitoring either the call provider or the area near the call provider. In sum, chimpanzee ‘alert hoos’ represent a plausible case of an intentionally produced animal vocalization (other studies) that refers recipients to signalers and/or to an external event (this study).

Keywords

Evolution of language Chimpanzee Reference Intention Directed attention Alarm calls 

Notes

Acknowledgments

We thank S. Adue, J. Alyo, M. Gideon and J. Okuti, for their hard work in the field, Mike Tomasello and Dorothy Cheney for very insightful comments, and Budongo Conservation Field Station and the Ugandan Authorities (UWA, UNCST) for permission to conduct the study. The study was funded by the Leverhulme Trust, the British Academy and the Leakey Foundation. We thank the Royal Zoological Society of Scotland for providing core support for the Budongo Conservation Field Station.

Supplementary material

10071_2014_827_MOESM1_ESM.wav (128 kb)
Supplementary material 1 (WAV 128 kb)
10071_2014_827_MOESM2_ESM.wav (189 kb)
Supplementary material 2 (WAV 189 kb)
10071_2014_827_MOESM3_ESM.wav (190 kb)
Supplementary material 3 (WAV 190 kb)
10071_2014_827_MOESM4_ESM.wav (353 kb)
Supplementary material 4 (WAV 352 kb)

Supplementary material 5 (MP4 8900 kb)

Supplementary material 6 (MP4 5485 kb)

Supplementary material 7 (MP4 10518 kb)

10071_2014_827_MOESM8_ESM.docx (822 kb)
Supplementary material 8 (DOCX 822 kb)

References

  1. Arnold K, Zuberbühler K (2013) Female putty-nosed monkeys use experimentally altered contextual information to disambiguate the cause of male alarm calls. PLoS One 8(6):e65660CrossRefPubMedCentralPubMedGoogle Scholar
  2. Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  3. Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-5Google Scholar
  5. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302(5648):1234–1236CrossRefPubMedGoogle Scholar
  6. Boersma P, Weenink D (2009) Praat: doing phonetics by computer (Version 5.1. 05) [Computer program]. Retrieved May 1, 2009Google Scholar
  7. Bruner JS (1974) Organization of early skilled action. Child Dev 44:1–11CrossRefGoogle Scholar
  8. Cäsar C, Byrne R, Young RJ, Zuberbühler K (2012) The alarm call system of wild black-fronted titi monkeys, Callicebus nigrifrons. Behav Ecol Sociobiol 66(5):653–667CrossRefGoogle Scholar
  9. Cheney DL, Seyfarth RM (1985) Vervet monkey alarm calls: manipulation through shared information? Behaviour 94:150–166CrossRefGoogle Scholar
  10. Cheney DL, Seyfarth RM (1990) How monkeys see the world: inside the mind of another species. University of Chicago Press, ChicagoGoogle Scholar
  11. Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58(1):67–75CrossRefPubMedGoogle Scholar
  12. Cheney DL, Seyfarth RM (2007) Baboon metaphysics: the evolution of a social mind. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  13. Cheney DL, Seyfarth RM, Silk JB (1995) The role of grunts in reconciling opponents and facilitating interactions among adult female baboons. Anim Behav 50(1):249–257CrossRefGoogle Scholar
  14. Clay Z, Zuberbühler K (2011) Bonobos extract meaning from call sequences. PLoS One 6(4):e18786CrossRefPubMedCentralPubMedGoogle Scholar
  15. Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  16. Crockford C (2005) Vocal communication in West African wild chimpanzees (Pan troglodytes verus): similarities to and differences with humans. PhD Dissertation, University of LeipzigGoogle Scholar
  17. Crockford C, Wittig RM, Seyfarth RM, Cheney DL (2007) Baboons eavesdrop to deduce mating opportunities. Anim Behav 73(5):885–890CrossRefGoogle Scholar
  18. Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22(2):142–146CrossRefPubMedGoogle Scholar
  19. Crockford C, Wittig RM, Langergraber K, Ziegler TE, Zuberbühler K, Deschner T (2013) Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc R Soc B Biol Sci 280(1755):20122765CrossRefGoogle Scholar
  20. Dennett DC (1983) Intentional systems in cognitive ethology: the “Panglossian paradigm” defended. Behav Brain Sci 6(03):343–355CrossRefGoogle Scholar
  21. Engh AL, Hoffmeier RR, Cheney DL, Seyfarth RM (2006) Who, me? Can baboons infer the target of vocalizations? Anim Behav 71(2):381–387CrossRefGoogle Scholar
  22. Fischer J (1998) Barbary macaques categorize shrill barks into two call types. Anim Behav 55(4):799–807CrossRefPubMedGoogle Scholar
  23. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
  24. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  25. Gruber T, Zuberbühler K (2013) Vocal recruitment for joint travel in wild chimpanzees. PLoS One 8(9):e76073CrossRefPubMedCentralPubMedGoogle Scholar
  26. Hoogland JL (1983) Nepotism and alarm calling in the black-tailed prairie dog (Cynomys ludovicianus). Anim Behav 31(2):472–479CrossRefGoogle Scholar
  27. Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7(4):216–223CrossRefPubMedGoogle Scholar
  28. Karakashian SJ, Gyger M, Marler P (1988) Audience effects on alarm calling in chickens (Gallus gallus). J Comp Psychol 102(2):129CrossRefPubMedGoogle Scholar
  29. Le Roux A, Cherry MI, Manser MB (2008) The audience effect in a facultatively social mammal, the yellow mongoose (Cynictis penicillata). Anim Behav 75(3):943–949CrossRefGoogle Scholar
  30. McCullagh P, Nelder JA (2008) Generalized linear models. Chapman and Hall, LondonGoogle Scholar
  31. Mennill DJ, Ratcliffe LM, Boag PT (2002) Female eavesdropping on male song contests in songbirds. Science 296(5569):873CrossRefPubMedGoogle Scholar
  32. Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20(12):R507–R508CrossRefPubMedGoogle Scholar
  33. Morton ES (1977) On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am Nat 111:855–869CrossRefGoogle Scholar
  34. Owren MJ, Rendall D (2001) Sound on the rebound: bringing form and function back to the forefront in understanding nonhuman primate vocal signaling. Evol Anthropol Issues News Rev 10(2):58–71CrossRefGoogle Scholar
  35. Papworth S, Barker J, Bose A-S, Schell AM, Zuberbühler K (2008) Male blue monkeys alarm call in response to danger experienced by others. Biol Lett 4:472–475. doi: 10.1098/rsbl.2008.0299 CrossRefPubMedCentralPubMedGoogle Scholar
  36. Price T, Fischer J (2014) Meaning attribution in the West African green monkey: influence of call type and context. Anim Cogn 17(2):277–286CrossRefPubMedCentralPubMedGoogle Scholar
  37. Rainey HJ, Zuberbühler K, Slater PJ (2004) Hornbills can distinguish between primate alarm calls. Proc R Soc B Biol Sci 271(1540):755CrossRefGoogle Scholar
  38. Reynolds V (2005) The chimpanzees of the Budongo Forest. Oxford University Press, OxfordCrossRefGoogle Scholar
  39. Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209(4455):523–525CrossRefPubMedGoogle Scholar
  40. Schel AM, Candiotti A, Zuberbühler K (2010) Predator-deterring alarm call sequences in Guereza colobus monkeys are meaningful to conspecifics. Anim Behav 80(5):799–808CrossRefGoogle Scholar
  41. Schel AM, Townsend SW, Machanda Z, Zuberbühler K, Slocombe KE (2013a) Chimpanzee alarm call production meets key criteria for intentionality. PLoS One 8(10):e76674CrossRefPubMedCentralPubMedGoogle Scholar
  42. Schel AM, Machanda Z, Townsend SW, Zuberbühler K, Slocombe KE (2013b) Chimpanzee food calls are directed at specific individuals. Anim Behav 86(5):955–965CrossRefGoogle Scholar
  43. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420CrossRefPubMedCentralPubMedGoogle Scholar
  44. Seyfarth RM, Cheney DL (2003) Meaning and emotion in animal vocalizations. Ann N Y Acad Sci 1000(1):32–55CrossRefPubMedGoogle Scholar
  45. Seyfarth RM, Cheney DL, Marler P (1980a) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210(4471):801–803CrossRefPubMedGoogle Scholar
  46. Seyfarth RM, Cheney DL, Marler P (1980b) Vervet monkey alarm calls: semantic communication in a free-ranging primate. Anim Behav 28(4):1070–1094CrossRefGoogle Scholar
  47. Seyfarth RM, Cheney DL, Bergman T, Fischer J, Zuberbühler K, Hammerschmidt K (2010) The central importance of information in studies of animal communication. Anim Behav 80(1):3–8CrossRefGoogle Scholar
  48. Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15(19):1779–1784CrossRefPubMedGoogle Scholar
  49. Tomasello M (2008) Why don’t apes point? Trends Linguist Stud Monogr 197:375Google Scholar
  50. Wheeler BC, Fischer J (2012) Functionally referential signals: a promising paradigm whose time has passed. Evol Anthropol Issues News, Rev 21(5):195–205CrossRefGoogle Scholar
  51. Wich SA, de Vries H (2006) Male monkeys remember which group members have given alarm calls. Proc R Soc B Biol Sci 273(1587):735–740CrossRefGoogle Scholar
  52. Wittig RM, Crockford C, Wikberg E, Seyfarth RM, Cheney DL (2007a) Kin-mediated reconciliation substitutes for direct reconciliation in female baboons. Proc R Soc B Biol Sci 274(1613):1109–1115CrossRefGoogle Scholar
  53. Wittig RM, Crockford C, Seyfarth RM, Cheney DL (2007b) Vocal alliances in chacma baboons (Papio hamadryas ursinus). Behav Ecol Sociobiol 61(6):899–909CrossRefGoogle Scholar
  54. Wittig RM, Crockford C, Deschner T, Langergraber KE, Ziegler TE, Zuberbühler K (2014) Triadic social interactions operate across time: a field experiment with wild chimpanzees. Proc R Soc B Biol Sci 281(1779):20133155CrossRefGoogle Scholar
  55. Zuberbühler K (2000a) Causal cognition in a non-human primate: field playback experiments with Diana monkeys. Cognition 76(3):195–207CrossRefPubMedGoogle Scholar
  56. Zuberbühler K (2000b) Interspecies semantic communication in two forest primates. Proc R Soc Lond Ser B Biol Sci 267(1444):713–718CrossRefGoogle Scholar
  57. Zuberbühler K (2009) Survivor signals: the biology and psychology of animal alarm calling. Adv Study Behav 40:277–322CrossRefGoogle Scholar
  58. Zuberbühler K, Wittig RM (2011) Field experiments with nonhuman primates: a tutorial. In: Curtis DJ, Setchell JM (eds) Field and laboratory methods in primatology: a practical guide. Cambridge University Press, Cambridge, pp 207–224CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.School of PsychologyUniversity of St AndrewsSt AndrewsUK
  3. 3.Budongo Conservation Field StationMasindiUganda
  4. 4.Cognitive Science CentreUniversity of NeuchâtelNeuchâtelSwitzerland

Personalised recommendations