Bonobos use call combinations to facilitate inter-party travel recruitment

  • Isaac SchambergEmail author
  • Dorothy L. Cheney
  • Zanna Clay
  • Gottfried Hohmann
  • Robert M. Seyfarth
Original Article


Many primates produce vocalizations when initiating travel. These “travel calls” are often acoustically similar to vocalizations unrelated to travel, and listeners appear to rely on a shared context with callers to correctly interpret the calls. When individuals use vocalizations to coordinate movement with out-of-sight group mates, however, such pragmatic cues are unavailable. Under these circumstances, effective communication may depend on more informative acoustic signals. Here, we investigate travel-related vocalizations that occur when callers and listeners cannot see one another: long-distance calls given by wild bonobos (Pan paniscus). We find that production of a specific call combination, the “low hoot-high hoot,” is more likely than a high hoot alone to be produced prior to travel. Furthermore, the low hoot-high hoot combination is more likely to result in inter-party recruitment—that is, individuals from other parties are more likely to approach the caller. We also compare these observations with previous research and find that bonobos appear to use distinct call combinations to facilitate specific movement patterns common in fission-fusion social structures. These results suggest that use of call combinations allow bonobos to convey more specific information than do single call types alone and that this additional information allows for effective communication between out-of-sight parties.

Significance statement

When an animal hears a conspecific vocalization, it is able to respond appropriately by integrating information about the call type itself and the context in which it was given. Vocalizations produced by out-of-sight individuals, therefore, present a challenge: how can a listener respond appropriately with only partial information about the context of the call? In situations where distant bonobos are communicating with one another, we find that call combinations are potentially more informative to listeners than single call types alone. The use of call combinations in such situations may allow listeners to respond appropriately to conspecific vocalizations even with ambiguous information about the context in which the call was produced.


Bonobo Call combination Fission-fusion Travel coordination Vocal communication 



We thank the Institut Congolais pour la Conservation de la Nature (ICCN) for permission to conduct research in the Democratic Republic of Congo. We are grateful to Lys Alcayna for data collection in the field and three anonymous reviewers for comments and suggestions.

Compliance with ethical standards

Ethical approval

The study was conducted in accordance with the current laws in the USA, Germany, and the Democratic Republic of the Congo. Research was approved by the Animal Care and Use Committee of the University of Pennsylvania (Protocol no. 804117).

Conflict of interest

The authors declare that they have no conflicts of interest.


This research was funded by the National Science Foundation Graduate Research Fellowship (IS) and grants from the Leaky Foundation (IS and ZC), the Department of Psychology at the University of Pennsylvania (IS), National Geographic Society (RMS and ZC) (Grant #9115-12).

Supplementary material

265_2017_2301_MOESM1_ESM.docx (64 kb)
ESM 1 (DOCX 63 kb)


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  2. Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654Google Scholar
  3. Bermejo M, Omedes A (1999) Preliminary vocal repertoire and vocal communication of wild bonobos (Pan paniscus) at Lilungu (Democratic Republic of Congo). Folia Primatol 70:328–357CrossRefPubMedGoogle Scholar
  4. Boinski S (1993) Vocal coordination of troop movement among white-faced capuchin monkeys, Cebus capucinus. Am J Primatol 30:85–100CrossRefGoogle Scholar
  5. Boinski S, Garber PA (2000) On the move: how and why animals travel in groups. University of Chicago Press, ChicagoGoogle Scholar
  6. Bousquet CAH, Sumpter DJT, Manser MB (2011) Moving calls: a vocal mechanism underlying quorum decisions in cohesive groups. Proc R Soc Lond B 278:1482–1488CrossRefGoogle Scholar
  7. Clay Z, Archbold J, Zuberbühler (2015) Functional flexibility in wild bonobo vocal behaviour. Peer J 3:e1124CrossRefPubMedPubMedCentralGoogle Scholar
  8. da Cunha RGT, Byrne RW (2009) The use of vocal communication in keeping the spatial cohesion of groups: intentionality and specific functions. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American Primates. Springer, New York, pp 341–363Google Scholar
  9. de Waal FBM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251Google Scholar
  10. Fedurek P, Donnellan E, Slocombe KE (2014) Social and ecological correlates of long-distance pant hoot calls in male chimpanzees. Behav Ecol Sociobiol 68:1345–1355CrossRefGoogle Scholar
  11. Fischer J, Zinner D (2011) Communication and cognition in primate group movement. Int J Primatol 32:1279–1295CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gersick AS, Cheney DL, Schneider JM, Seyfarth RM, Holekamp KE (2015) Long-distance communication facilitates cooperation among wild spotted hyaenas, Crocuta crocuta. Anim Behav 103:107–116CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gruber T, Zuberbühler K (2013) Vocal recruitment for joint travel in wild chimpanzees. PLoS One 8:e76073CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hohmann G, Fruth B (1994) Structure and use of distance calls in wild bonobos (Pan paniscus). Int J Primatol 15:767–782CrossRefGoogle Scholar
  15. Hohmann G, Fruth B (2003) Lui Kotal—a new site for field research on bonobos in the Salonga National Park. Pan Africa News 10:25–27Google Scholar
  16. Kalan AK, Mundry R, Boesch C (2015) Wild chimpanzees modify food call structure with respect to tree size for a particular fruit species. Anim Behav 101:1–9CrossRefGoogle Scholar
  17. Kanō T (1992) The last ape: pygmy chimpanzee behavior and ecology. Stanford University Press, StanfordGoogle Scholar
  18. Kondo N, Watanabe S (2009) Contact calls: information and social function. Jpn Psychol Res 51:197–208CrossRefGoogle Scholar
  19. Lammers MO, Schotten M, Au WW (2006) The spatial context of free-ranging Hawaiian spinner dolphins (Stenella longirostris) producing acoustic signals. J Acoust Soc Am 119:1244–1250CrossRefPubMedGoogle Scholar
  20. Lehmann J, Boesch C (2004) To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behav Ecol Sociobiol 56:207–216CrossRefGoogle Scholar
  21. Leighty KA, Soltis J, Wesolek CM, Savage A (2008) Rumble vocalizations mediate interpartner distance in African elephants, Loxodonta africana. Anim Behav 76:1601–1608CrossRefGoogle Scholar
  22. Mitani JC, Nishida T (1993) Contexts and social correlates of long-distance calling by male chimpanzees. Anim Behav 45:735–746CrossRefGoogle Scholar
  23. Mitra S, van Schaik CP (2007) The response of adult orangutans to flanged male long calls: inferences about their function. Folia Primatol 78:215–226CrossRefGoogle Scholar
  24. Poole JH (2011) Behavioral contexts of elephant acoustic communication. In: Moss CJ, Croze HJ, Less PC (eds) The Amboseli elephants: a long-term perspective on a long-lived mammal. University of Chicago Press, Chicago, pp 125–161CrossRefGoogle Scholar
  25. Price T, Wadewitz P, Cheney DL, Seyfarth RM, Hammerschmidt K, Fischer J (2015) Vervets revisited: a quantitative analysis of alarm call structure and context specificity. Sci Rep 5:13220CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ramos-Fernández G (2005) Vocal communication in a fission–fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077–1092CrossRefGoogle Scholar
  27. Rendall D, Seyfarth RM, Cheney DL, Owren MJ (1999) The meaning and function of grunt variants in baboons. Anim Behav 57:583–592CrossRefPubMedGoogle Scholar
  28. Schamberg I, Cheney DL, Clay Z, Hohmann G, Seyfarth RM (2016) Call combinations, vocal exchanges and interparty movement in wild bonobos. Anim Behav 122:109–116CrossRefGoogle Scholar
  29. Schlenker P, Chemla E, Schel AM, Fuller J, Gautier JP, Kuhn J, Veselinović D, Arnold K, Cäsar C, Keenan S, Lemasson A, Ouattara K, Ryder R, Zuberbühler K (2016) Formal monkey linguistics. Theoretical Linguistics 42:1–90Google Scholar
  30. Seyfarth RM, Cheney DL (2016a) The origin of meaning in animal signals. Anim Behav 124:339–346CrossRefGoogle Scholar
  31. Seyfarth RM, Cheney DL (2016b) Schlenker et al.’s informativity principle. Theor Linguist 42:155–158CrossRefGoogle Scholar
  32. Spehar SN, Di Fiore A (2013) Loud calls as a mechanism of social coordination in a fission–fusion taxon, the white-bellied spider monkey (Ateles belzebuth). Behav Ecol Sociobiol 67:947–961CrossRefGoogle Scholar
  33. Stewart KJ, Harcourt AH (1994) Gorillas’ vocalizations during rest periods: signals of impending departure? Behaviour 130:29–40CrossRefGoogle Scholar
  34. Sueur C, King AJ, Conradt L, Kerth G, Lusseau D, Mettke-Hofmann C, Schaffner CM, Williams L, Zinner D, Aureli F (2011) Collective decision-making and fission–fusion dynamics: a conceptual framework. Oikos 120:1608–1617CrossRefGoogle Scholar
  35. Tabachnick BG, Fidell LS (2007) Using multivariate statistics. Pearson Education, BostonGoogle Scholar
  36. Wheeler BC, Fischer J (2012) Functionally referential signals: a promising paradigm whose time has passed. Evol Anthropol 21:195–205CrossRefPubMedGoogle Scholar
  37. White FJ, Waller M, Boose K, Merrill MY, Wood KD (2015) Function of loud calls in wild bonobos. J Anthropol Sci 93:1–13Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  3. 3.Department of PsychologyUniversity of BirminghamBirminghamUK
  4. 4.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany

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