Animal Cognition

, Volume 15, Issue 3, pp 327–339 | Cite as

Context-related call combinations in female Diana monkeys

  • Agnès Candiotti
  • Klaus Zuberbühler
  • Alban Lemasson
Original Paper


Non-human primates possess species-specific repertoires of acoustically distinct call types that can be found in adults in predictable ways. Evidence for vocal flexibility is generally rare and typically restricted to acoustic variants within the main call types or sequential production of multiple calls. So far, evidence for context-specific call sequences has been mainly in relation to external disturbances, particularly predation. In this study, we investigated extensively the vocal behaviour of free-ranging and individually identified Diana monkeys in non-predatory contexts. We found that adult females produced four vocal structures alone (‘H’, ‘L’, ‘R’ and ‘A’ calls, the latter consisting of two subtypes) or combined in non-random ways (‘HA’, ‘LA’ and ‘RA’ call combinations) in relation to ongoing behaviour or external events. Specifically, the concatenation of an introductory call with the most frequently emitted and contextually neutral ‘A’ call seems to function as a contextual refiner of this potential individual identifier. Our results demonstrate that some non-human primates are able to increase the effective size of their small vocal repertoire not only by varying the acoustic structure of basic call types but also by combining them into more complex structures. We have demonstrated this phenomenon for a category of vocalisations with a purely social function and discuss the implications of these findings for evolutionary theories of primate vocal communication.


Social calls Call combination Vocal flexibility Non-human primates 



This research was funded by the French Ministry of Research, IUF, PICS-CNRS and ANR ‘Orilang’. In Côte d’Ivoire, we thank the minister of scientific research and the ‘Office Ivoirien des Parcs et Réserves’ (OIPR) for permission to conduct research in Taï National Park. We also thank the Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS) for logistic support. We are very thankful to our field assistants F. Belé and F. Gnepa for their invaluable help with data collection and to members of the Taï Chimpanzee Project (TCP) and the ‘Centre de Recherche en Ecologie’ (CRE) for their support in the field. We are grateful for comments and thoughts by K. Ouattara, K. Arnold, T. Aubin and H. Bouchet as well as for the referees’ valuable comments on the manuscript. We thank the Wissenschaftskolleg zu Berlin as well as the Institut Universitaire de France for additional support.


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  2. Arnold K, Zuberbühler K (2006) The alarm-calling system of adult male putty-nosed monkeys, Cercopithecus nictitans martini. Anim Behav 72:643–653CrossRefGoogle Scholar
  3. Arnold K, Zuberbühler K (2008) Meaningful call combinations in a non-human primate. Curr Biol 18:R202–R203PubMedCrossRefGoogle Scholar
  4. Bickerton D, Szathmáry E (2009) Biological foundations and origin of syntax. MIT Press, CambridgeGoogle Scholar
  5. Bouchet H, Pellier A, Blois-Heulin C, Lemasson A (2010) Sex differences in the vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus): a multi-level acoustic analysis. Am J Primatol 72:360–375PubMedCrossRefGoogle Scholar
  6. Catchpole CK, Slater PJ (1995) Bird song. Biological themes and variations. Press Syndicate University of Cambridge, CambridgeGoogle Scholar
  7. Chomsky N (1981) Knowledge of language: its elements and origins. Philos Trans R Society of Lond B Biol Sci 295:223–234CrossRefGoogle Scholar
  8. Clarke E, Reichard UH, Zuberbühler K (2006) The syntax and meaning of wild gibbon songs. PLoS One 1:e73PubMedCrossRefGoogle Scholar
  9. Clay Z, Zuberbühler K (2009) Food-associated calling sequences in bonobos. Anim Behav 77:1387–1396CrossRefGoogle Scholar
  10. Clay Z, Zuberbühler K (2011) Bonobos extract meaning from call sequences. PloS One 6:e18786PubMedCrossRefGoogle Scholar
  11. Cleveland J, Snowdon CT (1982) The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). Zeitschrift für Tierpsychologie 58:231–270CrossRefGoogle Scholar
  12. Corballis MC (2003) From hand to mouth: the origins of language. Princeton University Press, PrincetonGoogle Scholar
  13. Crockford C, Boesch C (2005) Call combinations in wild chimpanzees. Behaviour 142:397–421CrossRefGoogle Scholar
  14. Dunbar R (1998) Theory of mind and evolution of language. In: Hurford JR, Studdert-Kennedy M, Knight C (eds) Approaches to the evolution of language. Cambridge University Press, Cambridge, pp 92–110Google Scholar
  15. Elowson AM, Snowdon CT (1994) Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Anim Behav 47:1267–1277CrossRefGoogle Scholar
  16. Enard W, Przeworski M, Fisher SE, Lai CSL, Wiebe V, Kitano T, Monaco AP, Pääbo S (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869–872PubMedCrossRefGoogle Scholar
  17. Ey E, Rahn C, Hammerschmidt K, Fischer J (2009) Wild female olive baboons adapt their grunt vocalizations to environmental conditions. Ethology 115:493–503CrossRefGoogle Scholar
  18. Gautier JP (1988) Interspecific affinities among guenons as deduced from vocalizations. In: Gautier-Hion A, Bourlière F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 194–226Google Scholar
  19. Gautier JP, Gautier A (1977) Communication in old world monkeys. In: Sebeok TE (ed) How animals communicate. Indiana University Press, Bloomington, pp 890–964Google Scholar
  20. Gautier-Hion A (1988) Polyspecific associations among forest guenons: ecological, behavioural and evolutionary aspects. In: Gautier-Hion A, Bourlière F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 452–476Google Scholar
  21. Gerhardt HC, Roberts JD, Bee MA, Schwartz JJ (2000) Call matching in the quacking frog (Crinia georgiana). Behav Ecol Sociobiol 48:243–251CrossRefGoogle Scholar
  22. Green S (1975) Dialects in Japanese monkeys: vocal learning and cultural transmission of locale-specific vocal behavior? Zeitschrift für Tierpsychologie 38:304–314PubMedCrossRefGoogle Scholar
  23. Harcourt AH, Stewart KJ (1996) Function and meaning of wild gorilla ‘close’ calls 2. Correlations with rank and relatedness. Behaviour 133:827–845CrossRefGoogle Scholar
  24. Hauser MD (2000) A primate dictionary? Decoding the function and meaning of another species’ vocalizations. Cognit Sci 24:445–475CrossRefGoogle Scholar
  25. Hauser MD, Chomsky N, Fitch W (2002) The faculty of language: what is it, who has it, and how did it evolve? Science 298:1569–1579PubMedCrossRefGoogle Scholar
  26. Hill CM (1994) The role of female diana monkeys, Cercopithecus diana, in territorial defence. Anim Behav 47:425–431CrossRefGoogle Scholar
  27. Koda H, Shimooka Y, Sugiura H (2008) Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata). Am J Primatol 70:1055–1063PubMedCrossRefGoogle Scholar
  28. Kroodsma DE (1982) Song repertoires: problems in their definition and use. In: Kroodsma DE, Miller HE (eds) Acoustic communication in birds. New York Academic Press, New York, pp 125–141Google Scholar
  29. Lemasson A (2011) What can forest guenons “tell” us about the origin of language? In: Vilain A, Schwartz JL, Abry C, Vauclair J (eds) Primate communication and human language vocalisation, gestures, imitation and deixis in humans and non-humans. John Benjamins Publishing Company, Amsterdam, pp 39–70Google Scholar
  30. Lemasson A, Hausberger M (2004) Patterns of vocal sharing and social dynamics in a captive group of Campbell’s monkeys (Cercopithecus campbelli campbelli). J Comp Psychol 118:347–359PubMedCrossRefGoogle Scholar
  31. Lemasson A, Hausberger M (2011) Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). J Acoust Soc Am 129:3341–3352PubMedCrossRefGoogle Scholar
  32. Lemasson A, Richard JP, Hausberger M (2004) A new methodological approach to context analysis of call production. Bioacoustics 14:111–125Google Scholar
  33. Lemasson A, Hausberger M, Zuberbühler K (2005) Socially meaningful vocal plasticity in adult Campbell’s monkeys (Cercopithecus campbelli). J Comp Psychol 119:220–229PubMedCrossRefGoogle Scholar
  34. Lemasson A, Gandon E, Hausberger M (2010) Attention to elder’s voice in non-human primates. Biol Lett 6:325–338Google Scholar
  35. Marler P (1977) The structure of animal communication sounds. In: Bullock TH (ed) Recognition of complex acoustic signals. Springer, Berlin, pp 17–35Google Scholar
  36. McGraw WS (2007) Positional behavior and habitat use of Tai forest monkeys. In: McGraw WS, Zuberbühler K, Noë R (eds) Monkeys of the Taı forest: an African primate community. Cambridge University Press, Cambridge, pp 223–253CrossRefGoogle Scholar
  37. Ouattara K, Lemasson A, Zuberbühler K (2009a) Campbell’s monkeys use affixation to alter call meaning. PLoS One 4:e7808PubMedCrossRefGoogle Scholar
  38. Ouattara K, Lemasson A, Zuberbühler K (2009b) Campbell’s monkeys concatenate vocalizations into context-specific call sequences. Proc Nat Acad Sci 106:22026–22031PubMedCrossRefGoogle Scholar
  39. Owings DH, Morton ES (1998) Animal vocal communication: a new approach. Cambridge University Press, CambridgeGoogle Scholar
  40. 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 10:58–71CrossRefGoogle Scholar
  41. Owren MJ, Seyfarth RM, Cheney DL (1997) The acoustic features of vowel-like grunt calls in chacma baboons (Papio cyncephalus ursinus): implications for production processes and functions. J Acoust Soc Am 101:2951–2963PubMedCrossRefGoogle Scholar
  42. Payne RS, McVay S (1971) Songs of humpback whales. Science 173:585–597PubMedCrossRefGoogle Scholar
  43. Pola YV, Snowdon CT (1975) The vocalizations of pygmy marmosets (Cebuella pygmaea). Anim Behav 23:826–842PubMedCrossRefGoogle Scholar
  44. Robinson JG (1984) Syntactic structures in the vocalizations of wedge-capped capuchin monkeys, Cebus olivaceus. Behaviour 90:46–79CrossRefGoogle Scholar
  45. Rowell TE (1988) The social system of guenons, compared with baboons, macaques and mangabeys. In: Gautier- Hion A, Bourlière F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 437–451Google Scholar
  46. Rowell TE, Olson DK (1983) Alternative mechanisms of social organization in monkeys. Behaviour 86:31–54Google Scholar
  47. Schel AM, Tranquilli S, Zuberbühler K (2009) The alarm call system of two species of black-and-white colobus monkeys (Colobus polykomos and Colobus guereza). J Comp Psychol 123:136–150PubMedCrossRefGoogle Scholar
  48. Schel AM, Candiotti A, Zuberbühler K (2010) Predator-deterring alarm call sequences in Guereza colobus monkeys are meaningful to conspecifics. Anim Behav 80:799–808CrossRefGoogle Scholar
  49. Seyfarth RM, Cheney DL (1984) The acoustic features of vervet monkey grunts. J Acoust Soc Am 75:1623–1628PubMedCrossRefGoogle Scholar
  50. Shapiro AD, Tyack PL, Seneff S (2010) Comparing call-based versus subunit-based methods for categorizing Norwegian killer whale, Orcinus orca, vocalizations. Anim Behav 81:377–386CrossRefGoogle Scholar
  51. Slocombe KE, Taller T, Call J, Zuberbühler K (2010) Chimpanzees extract social information from agnonistic screams. PLoS ONE 5(7):e11473Google Scholar
  52. Snowdon CT (2009) Chapter 7: Plasticity of communication in nonhuman primates. In: Naguib M, Janick VM (eds) Advances in the study of behaviour, vol 40. Academic press, New York, pp 239–276Google Scholar
  53. Snowdon CT, Elowson AM (1999) Pygmy marmosets modify call structure when paired. Ethology 105:893–908CrossRefGoogle Scholar
  54. Uster D, Zuberbühler K (2001) The functional significance of Diana monkey’s clear calls. Behaviour 138:741–756CrossRefGoogle Scholar
  55. Williams DA (1976) Improved likelihood ratio tests for complete contingency tables. Biometrika 63:33–37CrossRefGoogle Scholar
  56. Zuberbühler K (2000a) Causal knowledge of predators’ behaviour in wild Diana monkeys. Anim Behav 59:209–220PubMedCrossRefGoogle Scholar
  57. Zuberbühler K (2000b) Referential labelling in Diana monkeys. Anim Behav 59:917–927PubMedCrossRefGoogle Scholar
  58. Zuberbühler K (2002) A syntactic rule in forest monkey communication. Anim Behav 63:293–299CrossRefGoogle Scholar
  59. Zuberbühler K, Noë R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604CrossRefGoogle Scholar
  60. Zuberbühler K, Cheney DL, Seyfarth RM (1999) Conceptual semantics in a nonhuman primate. J Comp Psychol 113:33–42CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Agnès Candiotti
    • 1
    • 2
    • 3
    • 5
  • Klaus Zuberbühler
    • 2
    • 3
  • Alban Lemasson
    • 1
    • 4
  1. 1.Université de Rennes 1, Laboratoire EthoS ‘Ethologie Animale et Humaine’, U.M.R. 6552-C.N.R.S., Station BiologiquePaimpontFrance
  2. 2.Centre Suisse de Recherches Scientifiques, Taï Monkey ProjectAbidjanIvory Coast
  3. 3.School of PsychologyUniversity of St AndrewsSt AndrewsScotland, UK
  4. 4.Institut Universitaire de FranceParisFrance
  5. 5.Université de Rennes 1, Laboratoire EthoS ‘Ethologie Animale et Humaine’, U.M.R. 6552-C.N.R.S., Station BiologiquePaimpontFrance

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