Animal Cognition

, Volume 13, Issue 6, pp 871–880 | Cite as

Leaf swallowing behavior in chimpanzees (Pan troglodytes): biased learning and the emergence of group level cultural differences

  • Michael A. Huffman
  • Caterina Spiezio
  • Andrea Sgaravatti
  • Jean-Baptiste Leca
Original Paper

Abstract

Demonstrating the ability to ‘copy’ the behavior of others is an important aspect in determining whether social learning occurs and whether group level differences in a given behavior represent cultural differences or not. Understanding the occurrence of this process in its natural context is essential, but can be a daunting task in the wild. In order to test the social learning hypothesis for the acquisition of leaf swallowing (LS), a self-medicative behavior associated with the expulsion of parasites, we conducted semi-naturalistic experiments on two captive groups of parasite-free, naïve chimpanzees (Pan troglodytes). Individuals in the group were systematically provided appropriate stimuli (rough hispid leaves) identical to those used by chimpanzees in the wild. Individuals initially responded in a variety of ways, ranging from total aversion to normal chewing and swallowing. Over time, however, the two groups adopted different variants for inserting and folding the leaves in the mouth prior to swallowing them (complete and partial LS), following the specific method spontaneously displayed by the first and primary LS models in their respective groups. These variants were similar to LS displayed by chimpanzees in the wild. Using the option-bias method, we found evidence for social learning leading to group-level biased transmission and group-level stabilization of these two variants. This is the first report on two distinct cultural variants innovated in response to the introduction of natural stimuli that emerged and spread spontaneously and concurrently within two adjacent groups of socially housed primates. These observations support the assertion that LS may reflect a generalized propensity for ingesting rough hispid leaves, which can be socially induced and transmitted within a group. Ingesting an adequate number of these leaves induces increased gut motility, which is responsible for the subsequent expulsion of particular parasite species in the wild. Cultural transmission and maintenance of LS within a group and associative learning by the individual of the positive consequences of this otherwise non-nutritive mode of ingestion is proposed to be the pivotal link between this feeding propensity and its maintenance as a self-medicative behavior by great apes in the wild.

Keywords

Captive chimpanzees Leaf swallowing Pan troglodytes Social learning Self-medication 

Notes

Acknowledgments

We are grateful to the director Dr. Cesare Avesani Zaborra, Ms Donata Grassi, and other staff of Parco Natura Viva for their tireless support of this research and for their dedication to the well-being of the chimpanzees. Special thanks to Prof. Emanuela Prato Previde and Prof. Giorgio Vallortigara for their advice and encouragement. During the later stages of the preparation of this manuscript, JBL was supported by a JSPS (Japan Society for the Promotion of Science) postdoctoral fellowship (No. 07421). We are also grateful to the reviewers of this manuscript, who both challenged and encouraged the development of our ideas. This study complies with the current laws of the country in which it was performed, and was approved in advance by the Parco Natura Viva administration.

References

  1. Baker KC, Aureli F (1996) The neighbor effect: other groups influence intragroup behavior in captive chimpanzees. Am J Primatol 40:283–291CrossRefGoogle Scholar
  2. Bond R, Smith PB (1996) Culture and conformity: a meta-analysis of studies using Asch’s (1952, 1956) line judgement task. Psychol Bull 119:111–137CrossRefGoogle Scholar
  3. Bonnie KE, de Waal FBM (2006) Affiliation promotes the transmission of social custom: handclasp grooming among captive chimpanzees. Primates 47:27–34CrossRefPubMedGoogle Scholar
  4. Bonnie KE, Horner V, Whiten A, de Waal FBM (2007) Spread of arbitrary conventions among chimpanzees: a controlled experiment. Proc R Soc B-Biol Sci 274:367–372CrossRefGoogle Scholar
  5. Byrne RW, Russon AE (1998) Learning by imitation: a hierarchical approach. Behav Brain Sci 21:667–721PubMedGoogle Scholar
  6. Day RL, Macdonald R, Brown C, Laland KN, Reader SM (2001) Interactions between shoal size and conformity in guppy social foraging. Anim Behav 62:917–925CrossRefGoogle Scholar
  7. de Waal FBM (2001) The ape and the Sushi-Master: cultural reflections of a primatologist. Harvard University Press, CambridgeGoogle Scholar
  8. de Waal FBM, Boesch C, Horner V, Whiten A (2008) Comparing social skills of children and apes. Science 319:569CrossRefPubMedGoogle Scholar
  9. Fessler DMT (1999) Toward an understanding of the universality of second order emotions. In: Hinton AL (ed) Biocultural approaches to the emotions. Cambridge University Press, New York, pp 75–116Google Scholar
  10. Fragaszy DM, Perry S (2003) Towards a biology of traditions. In: Fragaszy DM, Perry S (eds) The biology of tradition: models and evidence. Cambridge University Press, Cambridge, pp 1–32CrossRefGoogle Scholar
  11. Galef BG, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–499CrossRefGoogle Scholar
  12. Galef BG, Whiskin EE (2008) ‘Conformity’ in Norway rats? Anim Behav 75:2035–2039CrossRefGoogle Scholar
  13. Ghiglieri MP (1984) The chimpanzees of Kibale forest: a field study of ecology and social structure. Columbia University Press, New YorkGoogle Scholar
  14. Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiol 8:4–15Google Scholar
  15. Henrich J, McElreath R (2003) The evolution of cultural evolution. Evol Anthropol 12:123–135CrossRefGoogle Scholar
  16. Herrman E, Call J, Hernandez-Lloreda MV, Hare B, Tomasello M (2007) Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science 317:1360–1366CrossRefGoogle Scholar
  17. Huffman MA (1997) Current evidence for self-medication in primates: a multidisciplinary perspective. Yearb Phys Anthropol 40:171–200CrossRefGoogle Scholar
  18. Huffman MA (2001) Self-medicative behavior in the African great apes—an evolutionary perspective into the origins of human traditional medicine. Bioscience 51:651–661CrossRefGoogle Scholar
  19. Huffman MA, Caton JM (2001) Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees. Int J Primatol 22:329–346CrossRefGoogle Scholar
  20. Huffman MA, Hirata S (2003) Biological and ecological foundations of primate behavioral traditions. In: Fragaszy DM, Perry S (eds) The biology of tradition: models and evidence. Cambridge University Press, Cambridge, pp 267–296CrossRefGoogle Scholar
  21. Huffman MA, Hirata S (2004) An experimental study of leaf swallowing in captive chimpanzees—insights into the origin of a self-medicative behavior and the role of social learning. Primates 45:113–118CrossRefPubMedGoogle Scholar
  22. Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, Towers GHN (1996) Leaf-swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections. Int J Primatol 72:475–503CrossRefGoogle Scholar
  23. Kendal RL, Coolen I, Laland KN (2004) The role of conformity in foraging when personal and social information conflict. Behav Ecol 15:269–277CrossRefGoogle Scholar
  24. Kendal RL, Kendal JR, Hoppitt W, Laland KN (2009) Identifying social learning in animal populations: a new ‘option-bias’ method. PLoS One 4(8):e6541CrossRefPubMedGoogle Scholar
  25. Levy DA, Nail PR (1993) Contagion: a theoretical and empirical review and reconceptualization. Genet Soc Gen Psychol Monogr 119:233–284PubMedGoogle Scholar
  26. Perry S (2009) Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus). Anim Cogn 12:705–716CrossRefPubMedGoogle Scholar
  27. Price E, Caldwell CA (2007) Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis. Behav Proc 74:13–20CrossRefGoogle Scholar
  28. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, SingaporeGoogle Scholar
  29. Sweeting MP, Houpt CE, Houpt ICA (1985) Social facilitation of feeding and time budgets in stabled ponies. J Anim Sci 60:369–374PubMedGoogle Scholar
  30. Thorpe WH (1963) Learning and instinct in animals. Methuen, LondonGoogle Scholar
  31. Tomasello M (1996) Do apes ape? In: Heyes CM, Galef BG (eds) Social learning in animals: the roots of culture. Academic Press, London, pp 319–346CrossRefGoogle Scholar
  32. Tomasello M, Davis-Dasilva M, Camak L, Bard K (1987) Observational learning of tool-use by young chimpanzees. Hum Evol 2:175–183CrossRefGoogle Scholar
  33. Whiten A (2000) Primate culture and social learning. Cogn Sci 24:477–508CrossRefGoogle Scholar
  34. Whiten A, Ham R (1992) On the nature and evolution of imitation in the animal kingdom: reappraisal of a century of research. Adv Stud Behav 11:239–283CrossRefGoogle Scholar
  35. Whiten A, van Schaik CP (2007) The evolution of animal ‘cultures’ and social intelligence. Phil Trans R Soc B 362:603–620CrossRefPubMedGoogle Scholar
  36. Whiten A, Horner V, de Waal FBM (2005) Conformity to cultural norms of tool use in chimpanzees. Nature 437:737–740CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Michael A. Huffman
    • 1
  • Caterina Spiezio
    • 2
    • 3
  • Andrea Sgaravatti
    • 4
  • Jean-Baptiste Leca
    • 1
  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Research DepartmentParco Natura Viva, Garda Zoological ParkBussolengo, VeronaItaly
  3. 3.Cognitive Neuroscience SectorInternational School for Advanced StudiesTriesteItaly
  4. 4.Psychology DepartmentUniversity of TriesteTriesteItaly

Personalised recommendations