Animal Cognition

, Volume 17, Issue 4, pp 997–1005 | Cite as

Socially learned habituation to human observers in wild chimpanzees

  • Liran Samuni
  • Roger Mundry
  • Joseph Terkel
  • Klaus Zuberbühler
  • Catherine Hobaiter
Original Paper


Habituation to human observers is an essential tool in animal behaviour research. Habituation occurs when repeated and inconsequential exposure to a human observer gradually reduces an animal’s natural aversive response. Despite the importance of habituation, little is known about the psychological mechanisms facilitating it in wild animals. Although animal learning theory offers some account, the patterns are more complex in natural than in laboratory settings, especially in large social groups in which individual experiences vary and individuals influence each other. Here, we investigate the role of social learning during the habituation process of a wild chimpanzee group, the Waibira community of Budongo Forest, Uganda. Through post hoc hypothesis testing, we found that the immigration of two well-habituated, young females from the neighbouring Sonso community had a significant effect on the behaviour of non-habituated Waibira individuals towards human observers, suggesting that habituation is partially acquired via social learning.


Female transfer Social referencing Social learning Culture Dispersal Observational conditioning 



We would like to thank the Waibira chimpanzee field assistants, Simon Lokuyu, Gerald Mayanga, Gideon Atayo and Robert Eguma, and the group of international habituation volunteers; as well as to all the staff of the Budongo Conservation Field Station, the Uganda National Council for Science and Technology, the President’s Office, the Uganda Wildlife Authority, and the National Forestry Authority. We thank Naomi Paz for her assistance in proofreading the manuscript. We also thank two anonymous reviewers for their thoughtful and helpful comments and one in particular for the discussion point that larger groups may dilute the effect of the habituated females. Fieldwork of CH and LS was funded by grants from the British Academy and a Leverhulme Trust’s Research Leadership Award.

Supplementary material

10071_2014_731_MOESM1_ESM.docx (104 kb)
Supplementary material 1 (DOCX 104 kb)


  1. Akins CK, Zentall TR (1996) Imitative learning in male Japanese quail (Coturnix japonica) using the two-action method. J Comp Psychol 110(3):316PubMedCrossRefGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  3. Baar 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. Baayen RH (2008) Analyzing linguistic data. A practical introduction to statistics using R. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. Barsalou LW, Breazeal C, Smith LB (2007) Cognition as coordinated non-cognition. Cogn Process 8:79–91PubMedCrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2Google Scholar
  7. Bertolani P, Boesch C (2008) Habituation of wild chimpanzees (Pan troglodytes) of the South Group at Tai Forest, Côte d’Ivoire: empirical measure of progress. Folia Primatol 79:162–171PubMedCrossRefGoogle Scholar
  8. Boesch C, Boesch H (1990) Tool use and tool making in wild chimpanzees. Folia Primatol 54:86–99PubMedCrossRefGoogle Scholar
  9. Burrell BD, Sahley CL (2001) Learning in simple systems. Curr Opin Neurobiol 11:757–764PubMedCrossRefGoogle Scholar
  10. Byrne RW, Byrne JME (1993) The complex lead-gathering skills of mountain gorillas (Gorilla g. beringei): variability and standardization. Am J Primatol 31:241–261CrossRefGoogle Scholar
  11. Caldwell CA, Whiten A (2002) Evolutionary perspectives on imitation: is a comparative psychology of social learning possible? Anim Cogn 5:193–2002PubMedCrossRefGoogle Scholar
  12. Cheney DL, Seyfarth RM (2010) Primate communication and human language: continuities and discontinuities. In: Kappeler P, Silk J (eds) Mind the gap: tracing the origins of human universals. Springer, Berlin, pp 283–298CrossRefGoogle Scholar
  13. Cook M, Mineka S (1989) Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys. J Abnorm Psychol 98:448PubMedCrossRefGoogle Scholar
  14. Custance D, Whiten A, Fredman T (1999) Social learning of an artificial fruit task in capuchin monkeys (Cebus paella). J Comp Psychol 113:13CrossRefGoogle Scholar
  15. Dobson AJ (2002) An Introduction to generalized linear models. Chapman & Hall/CRC, New YorkGoogle Scholar
  16. Eggling WJ (1969) Observations on the ecology of the Budongo rain forest, Uganda. J Ecol 34:20–87CrossRefGoogle Scholar
  17. Feinman S, Roberts D, Hsieh KF, Sawyer D, Swanson D (1992) A critical review of social referencing in infancy. In: Feinman S (ed) Social referencing and the social construction of reality in infancy. Plenum Press, New York, pp 15–54CrossRefGoogle Scholar
  18. Field A (2005) Discovering statistics using SPSS. Sage Publications, LondonGoogle Scholar
  19. Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55PubMedCentralPubMedCrossRefGoogle Scholar
  20. Fox B, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand OaksGoogle Scholar
  21. Frith CD, Frith U (2007) Social cognition in humans. Curr Biol 17(16):R724–R732PubMedCrossRefGoogle Scholar
  22. Galef BG, Laland KN (2004) Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–499CrossRefGoogle Scholar
  23. Ghiglieri MP (1984) The Chimpanzees of Kibale forest. Columbia University Press, New YorkGoogle Scholar
  24. Goldsmith ML (2005) Habituating primates for field study: ethical considerations for African great apes. In: Turner TR (ed) Biological anthropology and ethics. State University of New York Press, Albany, pp 49–64Google Scholar
  25. Hamilton WD (1971) Geometry of the selfish herd. J Theor Biol 31(2):295–311PubMedCrossRefGoogle Scholar
  26. Heyes CM, Dawson GR (1990) A demonstration of observational learning in rats using a bidirectional control. Q J Exp Psychol 42:59–71Google Scholar
  27. Hobaiter C, Byrne RW (2010) Able-bodied chimpanzees imitate a motor procedure used by a disabled individual to overcome handicap. PLoS One 5(8):e11959PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  29. Jack KM, Lenz BB, Healan E, Rudman S, Schoof VAM, Fedigan L (2008) The effects of observer presence on the behavior of Cebus capucinus in Costa Rica. Am J Primatol 70:490–494PubMedCrossRefGoogle Scholar
  30. Johns B (1996) Responses of chimpanzees to habituation and tourism in the Kibale forest, Uganda. Biol Conserv 78:257–262CrossRefGoogle Scholar
  31. Kasereka B, Muhigwa JBB, Shalukoma C, Kahekwa JM (2006) Vulnerability of habituated Grauer’s gorilla to paoching in the Kahuzi-Biega National Park, DRC. Afr Stud Monogr 27:5–26Google Scholar
  32. Kawai M (1965) Newly-acquired pre-cultural behaviour of the natural troop of Japanese monkeys on Koshima Islet. Primates 6:1–30CrossRefGoogle Scholar
  33. Köndgen S, Kühl H, N’Goran PK, Walsh PD, Schenk S, Ernst N et al (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18:260–264PubMedCrossRefGoogle Scholar
  34. Kosheleff VP, Anderson CNK (2008) Temperature’s influence on the activity budget, terrestriality, and sun exposure of chimpanzees in the Budongo Forest, Uganda. Am J Phys Anthropol 139:172–181CrossRefGoogle Scholar
  35. Mackintosh NJ (1987) Neurobiology, psychology and habituation. Behav Res Ther 25:81–97PubMedCrossRefGoogle Scholar
  36. Magurran AE, Girling S (1986) Predator recognition and response habituation in shoaling minnows. Anim Behav 34:510–518CrossRefGoogle Scholar
  37. McGrew WC, Tutin CEG (1978) Evidence for a social custom in wild chimpanzees. Man 13:234–251CrossRefGoogle Scholar
  38. Mineka S, Davidson M, Cook M, Keir R (1984) Fear of snakes in wild and lab-reared rhesus monkeys. J Abnorm Psychol 93:355–372PubMedCrossRefGoogle Scholar
  39. Morgan D, Sanz C (2003) Naive encounters with chimpanzees in the Goualougo triangle, Republic of Congo. Int J Primatol 24:369–381CrossRefGoogle Scholar
  40. Newton-Fisher NE (1999) The diet of chimpanzees in the Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354CrossRefGoogle Scholar
  41. Nishida T (1987) Local traditions and cultural transmission. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 462–474Google Scholar
  42. Nishida T, Kawanaka K (1972) Inter-unit-group relationships among wild chimpanzees of the Mahale Mountains. Afr Stud 7:131–169Google Scholar
  43. Petrinovich L, Patterson TL (1981) Field studies of habituation: IV. Sensitization as a function of the distribution and novelty of song playback to white-crowned sparrows. J Comp Physiol Psychol 95:805CrossRefGoogle Scholar
  44. Plumptre AJ, Behangana M, Davenport TRB, Kahindo C, Kityo R, Ndomba E et al. (2003) The biodiversity of the Albertine Rift, Albertine Rift technical reports No. 3, p 105Google Scholar
  45. Pusey A (1979) Intercommunity transfer of chimpanzees in Gombe National Park. In: Hamburg D, McCown E (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 405–427Google Scholar
  46. Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  47. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. Raderschall CA, Magrath RD, Hemmi JM (2011) Habituation under natural conditions: model predators are distinguished by approach direction. J Exp Biol 214:4209–4216PubMedCrossRefGoogle Scholar
  49. Reynolds V (2005) The Chimpanzees of the Budongo Forest: ecology, behaviour, and conservation: ecology, behaviour, and conservation. Oxford University Press, OxfordGoogle Scholar
  50. Romanes GJ (1882) Animal intelligence. Kegan Paul Trench & Co., LondonGoogle Scholar
  51. Russell CL, Bard KA, Adamson LB (1997) Social referencing by young chimpanzees (Pan troglodytes). J Comp Psychol 111:185PubMedCrossRefGoogle Scholar
  52. Schaller GB (1963) The mountain gorilla; ecology and behavior. University of Chicago Press. xvii, Chicago, p 431Google Scholar
  53. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Method Ecol Evol 1:103–113CrossRefGoogle Scholar
  54. Sherry DF, Galef BG (1984) Cultural transmission without imitation: milk bottle opening by birds. Anim Behav 32:937–938CrossRefGoogle Scholar
  55. Sommer V, Adanu J, Faucher I, Fowler A (2004) Nigerian Chimpanzees (Pan troglodytes vellerosus) at Gashaka: 2 years of habituation efforts. Folia Primatol 75:295–316PubMedCrossRefGoogle Scholar
  56. Stein L (1966) Habituation and stimulus novelty: a model based on classical conditioning. Psychol Rev 73:352–356PubMedCrossRefGoogle Scholar
  57. Tennie C, Call J, Tomasello M (2006) Push or pull: imitation versus emulation in great apes and human children. Ethology 112:1159–1169CrossRefGoogle Scholar
  58. Thorndike EL (1898) Animal intelligence: an experimental study of the associative process in animals. Psychol Rev Monogr 2:551–553CrossRefGoogle Scholar
  59. Thorpe W (1963) Learning and instinct in animals. Methuen, LondonGoogle Scholar
  60. Tomasello M (1990) Cultural transmission in the tool use and communicatory signalling of chimpanzees? In: Parker S, Gibson K (eds) Language and Intelligence in monkeys and apes: comparative developmental perspectives. Cambridge University Press, Cambridge, pp 274–311CrossRefGoogle Scholar
  61. Tomasello M, Davis-Dasilva M, Camak L, Bard K (1987) Observational learning of tool-use by young chimpanzees. Primates 30:35–50CrossRefGoogle Scholar
  62. Tutin CEG, Fernandez M (1991) Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation. In: Box HO (ed) Primates responses to environmental change. Chapman & Hall, London, pp 187–197CrossRefGoogle Scholar
  63. 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 21:239–283CrossRefGoogle Scholar
  64. Whiten A, Horner V, Litchfield CA, Marshall-Pescini S (2004) How do apes ape? Learn Behav 32:36–52PubMedCrossRefGoogle Scholar
  65. Williams J (1999) Female strategies and the reasons for territoriality in chimpanzees: lessons from three decades of research at Gombe. Ph.D. thesis, University of MinnesotaGoogle Scholar
  66. Williamson EA, Feistner ATC (2011) Habituating primates: processes, techniques, variables and ethics. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology: a practical guide, 2nd edn. Cambridge University Press, Cambridge, pp 25–39Google Scholar
  67. Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36(02):153–160CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Liran Samuni
    • 1
    • 2
    • 5
  • Roger Mundry
    • 1
  • Joseph Terkel
    • 2
  • Klaus Zuberbühler
    • 3
    • 4
    • 5
  • Catherine Hobaiter
    • 3
    • 5
  1. 1.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.Department of ZoologyUniversity of Tel AvivTel AvivIsrael
  3. 3.Centre for Social Learning and Cognitive Evolution and Scottish Primate Research Group, School of Psychology and NeuroscienceUniversity of St AndrewsSt AndrewsScotland, UK
  4. 4.Department of Comparative Cognition, Institute of BiologyUniversity of NeuchatelNeuchâtelSwitzerland
  5. 5.Budongo Conservation Field StationMasindiUganda

Personalised recommendations