Behavioral Ecology and Sociobiology

, Volume 69, Issue 10, pp 1701–1712 | Cite as

Audience effects in chimpanzee food calls and their potential for recruiting others

  • Ammie K. KalanEmail author
  • Christophe Boesch
Original Article


One proposed benefit for the seemingly costly behaviour of food calling is the recruitment of social allies and mates by the signaller. In chimpanzees, food calls are only produced for approximately half of all feeding events. Therefore, we investigated the influence of social and ecological context on the probability of making a food call upon arriving to a food patch in a group of wild chimpanzees. First, we tested whether feeding events where food calls had been uttered did in fact attract more individuals to join the caller. Secondly, we examined the influence of two sources of audience effects: those who were physically present with the caller and those who were presumed nearby but out of sight, and thirdly the effect of various ecological factors. We found that when feeding on fruit species, events where food calls had been produced had a higher probability of group mates arriving, even whilst controlling for the effect of pant hoots. Furthermore, the probability of uttering a food call was motivated by social more than ecological context. Specifically, high-ranking males were more likely to make food calls when estrous females were nearby, while low-ranking males and females generally called more when more females were nearby, irrespective of their reproductive state. These effects were independent of the increase in food call probability when male callers were accompanied by more males. Our findings support the recruitment function of food calls and suggest that high-ranking males call to attract estrous females to food patches to obtain mating opportunities.


Audience effects Male signalling Pan troglodytes Primate communication Reciprocal altruism Recruitment call 



This study was funded by the Max Planck Society. We thank the Ministère de la Recherche Scientifique and the Ministère de l’Environnement et des Eaux et Forêts of Côte d’Ivoire and Office Ivorien des Parcs et Reserves for permission to conduct research in the country and Taï National Park. For logistical support, we thank the Centre Suisse de Recherche Scientifique and the Taï Chimpanzee Project, especially all field assistants and Roman Wittig. Thanks to Cathy Crockford for comments on earlier drafts as well as Roger Mundry and Colleen Stephens for statistical support. We also thank two anonymous reviewers for helpful comments that improved this manuscript.

Ethical standards

This research was conducted with permissions from the relevant Ivorian authorities in accordance with the national laws and animal care regulations of Côte d’Ivoire as well as Germany. The study complied with the ethical standards of the Max Planck Institute for Evolutionary Anthropology and the Primatology department’s ethical guidelines for non-invasive research.

Supplementary material

265_2015_1982_MOESM1_ESM.docx (181 kb)
Appendix 1 (DOCX 180 kb)


  1. Baayen RH (2008) Analyzing linguistic data: a practical introduction to statistics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  2. 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
  3. Bates D, Maechler M, Matrix LT (2014) lme4: Linear mixed effects models using S4 classes. CRAN.R project,
  4. Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour 117:220–242CrossRefGoogle Scholar
  5. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï Forest: behavioural ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  6. Boinski S, Campbell AF (1996) The huh vocalization of white-faced capuchins: a spacing call disguised as a food call? Ethology 102:826–840CrossRefGoogle Scholar
  7. Caine NG, Addington RL, Windfelder TL (1995) Factors affecting the rates of food calls given by red-bellied tamarins. Anim Behav 50:53–60CrossRefGoogle Scholar
  8. Chapman CA, Lefebvre L (1990) Manipulating foraging group size: spider monkey food calls at fruiting trees. Anim Behav 39:891–896CrossRefGoogle Scholar
  9. Chapman CA, Chapman LJ, Wangham R et al (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527CrossRefGoogle Scholar
  10. Chapman CA, Chapman LJ, Wrangham RW (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70CrossRefGoogle Scholar
  11. Clark AP (1993) Rank differences in the production of vocalizations by wild chimpanzees as a function of social context. Am J Primatol 31:159–179CrossRefGoogle Scholar
  12. Clark AP, Wrangham RW (1994) Chimpanzee arrival pant-hoots: do they signify food or status? Int J Primatol 15:185–205CrossRefGoogle Scholar
  13. Clay Z, Smith CL, Blumstein DT (2012) Food-associated vocalizations in mammals and birds: what do these calls really mean? Anim Behav 83:323–330CrossRefGoogle Scholar
  14. Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22:142–146CrossRefPubMedGoogle Scholar
  15. de Waal FBM (1989) Food sharing and reciprocal obligations among chimpanzees. J Hum Evol 18:433–459CrossRefGoogle Scholar
  16. Deschner T, Heistermann M, Hodges K, Boesch C (2003) Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim Behav 66:551–560CrossRefGoogle Scholar
  17. Di Bitetti MS (2003) Food-associated calls of tufted capuchin monkeys (Cebus apella nigritus) are functionally referential signals. Behaviour 140:565–592CrossRefGoogle Scholar
  18. Dittus WPJ (1984) Toque macaque food calls: semantic communication concerning food distribution in the environment. Anim Behav 32:470–477CrossRefGoogle Scholar
  19. Dobson AJ, Barnett AG (2008) An introduction to generalized linear models. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  20. Elgar MA (1986) The establishment of foraging flocks in house sparrows: risk of predation and daily temperature. Behav Ecol Sociobiol 19:433–438CrossRefGoogle Scholar
  21. Evans CS, Marler P (1994) Food calling and audience effects in male chickens, Gallus gallus: their relationships to food availability, courtship and social facilitation. Anim Behav 47:1159–1170CrossRefGoogle Scholar
  22. Fedurek P, Slocombe KE (2013) The social function of food-associated calls in male chimpanzees. Am J Primatol 75:726–739CrossRefPubMedGoogle Scholar
  23. Fedurek P, Machanda ZP, Schel AM, Slocombe KE (2013) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196CrossRefGoogle Scholar
  24. 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
  25. Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55PubMedCentralCrossRefPubMedGoogle Scholar
  26. Fox J, Weisberg S, Bates D, Fox MJ (2012) Package “car”.
  27. Fürtbauer I, Mundry R, Heistermann M, Schülke O, Ostner J (2011) You mate, I mate:macaque females synchronize sex not cycles. PLoS ONE 6:e26144Google Scholar
  28. Gomes CM, Mundry R, Boesch C (2009) Long-term reciprocation of grooming in wild West African chimpanzees. Proc R Soc Lond B 276:699–706CrossRefGoogle Scholar
  29. Goodall J (1986) The chimpanzees of gombe: patterns of behavior. Belknap Press of the Harvard University Press, CambridgeGoogle Scholar
  30. Hauser MD, Marler P (1993a) Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors. Behav Ecol 4:194–205CrossRefGoogle Scholar
  31. Hauser MD, Marler P (1993b) Food-associated calls in rhesus macaques (Macaca mulatta): II. Costs and benefits of call production and suppression. Behav Ecol 4:206–212CrossRefGoogle Scholar
  32. Hauser MD, Wrangham RW (1987) Manipulation of food calls in captive chimpanzees. Folia Primatol 48:207–210CrossRefPubMedGoogle Scholar
  33. Hauser MD, Teixidor P, Fields L, Flaherty R (1993) Food-elicited calls in chimpanzees: effects of food quantity and divisibility. Anim Behav 45:817–819CrossRefGoogle Scholar
  34. Heinrich B, Marzluff JM (1991) Do common ravens yell because they want to attract others? Behav Ecol Sociobiol 28:13–21CrossRefGoogle Scholar
  35. Hobaiter C, Byrne RW (2011) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767CrossRefPubMedGoogle Scholar
  36. Janik VM (2000) Food-related bray calls in wild bottlenose dolphins (Tursiops truncatus). Proc R Soc Lond B 267:923–927CrossRefGoogle Scholar
  37. 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
  38. Lehmann J, Boesch C (2009) Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Anim Behav 77:377–387CrossRefGoogle Scholar
  39. Marler P, Tenaza RR (1977) Signaling behavior of apes with special reference to vocalization. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, pp 965–1033Google Scholar
  40. Marler P, Dufty A, Pickert R (1986) Vocal communication in the domestic chicken: II. Is a sender sensitive to the presence and nature of a receiver? Anim Behav 34:194–198CrossRefGoogle Scholar
  41. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, LondonCrossRefGoogle Scholar
  42. Mitani JC, Nishida T (1993) Contexts and social correlates of long-distance calling by male chimpanzees. Anim Behav 45:735–746CrossRefGoogle Scholar
  43. Mundry R (2014) Statistical issues and assumptions of phylogenetic generalized least squares. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin, pp 131–153Google Scholar
  44. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  45. 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
  46. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  47. Riedel J, Franz M, Boesch C (2011) How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d’Ivoire. Am J Primatol 73:305–313CrossRefPubMedGoogle Scholar
  48. Roberts G (1998) Competitive altruism: from reciprocity to the handicap principle. Proc R Soc Lond B 265:427–431CrossRefGoogle Scholar
  49. Sayers K, Menzel CR (2012) Memory and foraging theory: chimpanzee utilization of optimality heuristics in the rank-order recovery of hidden foods. Anim Behav 84:795–803PubMedCentralCrossRefPubMedGoogle Scholar
  50. Schel AM, Machanda Z, Townsend SW et al (2013) Chimpanzee food calls are directed at specific individuals. Anim Behav 86:955–965CrossRefGoogle Scholar
  51. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  52. Seyfarth RM, Cheney DL (2003) Signalers and receivers in animal communication. Annu Rev Psychol 54:145–173CrossRefPubMedGoogle Scholar
  53. Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15:1779–1784CrossRefPubMedGoogle Scholar
  54. Slocombe KE, Zuberbühler K (2006) Food-associated calls in chimpanzees: responses to food types or food preferences? Anim Behav 72:989–999CrossRefGoogle Scholar
  55. Slocombe KE, Zuberbühler K (2007) Chimpanzees modify recruitment screams as a function of audience composition. Proc Natl Acad Sci U S A 104:17228–17233PubMedCentralCrossRefPubMedGoogle Scholar
  56. Slocombe KE, Kaller T, Turman L, Townsend SW, Papworth S, Squibbs P, Zuberbühler K (2010) Production of food-associated calls in wild male chimpanzees is dependent on the composition of the audience. Behav Ecol Sociobiol 64:1959–1966CrossRefGoogle Scholar
  57. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  58. Stokes AW, Williams HW (1972) Courtship feeding calls in gallinaceous birds. Auk 89:177–180CrossRefGoogle Scholar
  59. Townsend SW, Deschner T, Zuberbühler K (2008) Female chimpanzees use copulation calls flexibly to prevent social competition. PLoS ONE 3:e2431PubMedCentralCrossRefPubMedGoogle Scholar
  60. Trivers R (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57CrossRefGoogle Scholar
  61. Wakefield ML (2008) Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. Int J Primatol 29:907–929CrossRefGoogle Scholar
  62. Wilkinson GS, Boughman JW (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350CrossRefPubMedGoogle Scholar
  63. Wittig RM, Boesch C (2003) Food competition and linear dominance hierarchy among female chimpanzees of the Taï National Park. Int J Primatol 24:847–867CrossRefGoogle Scholar
  64. Wittiger L, Boesch C (2013) Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus. Behav Ecol Sociobiol 67:1097–1111CrossRefGoogle Scholar
  65. Wrangham RW (1977) Feeding behaviour of chimpanzees in Gombe national park, Tanzania. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behavior in lemurs monkeys and apes. Academic Press, London, pp 503–538Google Scholar
  66. Zuberbühler K (2008) Audience effects. Curr Biol 18:R189–R190CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany

Personalised recommendations