Skip to main content
Log in

Socially learned habituation to human observers in wild chimpanzees

Animal Cognition Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Akins CK, Zentall TR (1996) Imitative learning in male Japanese quail (Coturnix japonica) using the two-action method. J Comp Psychol 110(3):316

    Article  CAS  PubMed  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

  • Baar DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278

    Article  Google Scholar 

  • Baayen RH (2008) Analyzing linguistic data. A practical introduction to statistics using R. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Barsalou LW, Breazeal C, Smith LB (2007) Cognition as coordinated non-cognition. Cogn Process 8:79–91

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2

  • 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 79:162–171

    Article  PubMed  Google Scholar 

  • Boesch C, Boesch H (1990) Tool use and tool making in wild chimpanzees. Folia Primatol 54:86–99

    Article  CAS  PubMed  Google Scholar 

  • Burrell BD, Sahley CL (2001) Learning in simple systems. Curr Opin Neurobiol 11:757–764

    Article  CAS  PubMed  Google Scholar 

  • Byrne RW, Byrne JME (1993) The complex lead-gathering skills of mountain gorillas (Gorilla g. beringei): variability and standardization. Am J Primatol 31:241–261

    Article  Google Scholar 

  • Caldwell CA, Whiten A (2002) Evolutionary perspectives on imitation: is a comparative psychology of social learning possible? Anim Cogn 5:193–2002

    Article  PubMed  Google Scholar 

  • 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 283–298

    Chapter  Google Scholar 

  • Cook M, Mineka S (1989) Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys. J Abnorm Psychol 98:448

    Article  CAS  PubMed  Google Scholar 

  • Custance D, Whiten A, Fredman T (1999) Social learning of an artificial fruit task in capuchin monkeys (Cebus paella). J Comp Psychol 113:13

    Article  Google Scholar 

  • Dobson AJ (2002) An Introduction to generalized linear models. Chapman & Hall/CRC, New York

    Google Scholar 

  • Eggling WJ (1969) Observations on the ecology of the Budongo rain forest, Uganda. J Ecol 34:20–87

    Article  Google Scholar 

  • 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 15–54

    Chapter  Google Scholar 

  • Field A (2005) Discovering statistics using SPSS. Sage Publications, London

    Google Scholar 

  • Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55

    Article  PubMed Central  PubMed  Google Scholar 

  • Fox B, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Frith CD, Frith U (2007) Social cognition in humans. Curr Biol 17(16):R724–R732

    Article  CAS  PubMed  Google Scholar 

  • Galef BG, Laland KN (2004) Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–499

    Article  Google Scholar 

  • Ghiglieri MP (1984) The Chimpanzees of Kibale forest. Columbia University Press, New York

    Google Scholar 

  • 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 49–64

    Google Scholar 

  • Hamilton WD (1971) Geometry of the selfish herd. J Theor Biol 31(2):295–311

    Article  CAS  PubMed  Google Scholar 

  • Heyes CM, Dawson GR (1990) A demonstration of observational learning in rats using a bidirectional control. Q J Exp Psychol 42:59–71

    CAS  Google Scholar 

  • Hobaiter C, Byrne RW (2010) Able-bodied chimpanzees imitate a motor procedure used by a disabled individual to overcome handicap. PLoS One 5(8):e11959

    Article  PubMed Central  PubMed  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • 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 70:490–494

    Article  PubMed  Google Scholar 

  • Johns B (1996) Responses of chimpanzees to habituation and tourism in the Kibale forest, Uganda. Biol Conserv 78:257–262

    Article  Google Scholar 

  • 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 27:5–26

    Google Scholar 

  • Kawai M (1965) Newly-acquired pre-cultural behaviour of the natural troop of Japanese monkeys on Koshima Islet. Primates 6:1–30

    Article  Google Scholar 

  • 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 18:260–264

    Article  PubMed  Google Scholar 

  • 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 139:172–181

    Article  Google Scholar 

  • Mackintosh NJ (1987) Neurobiology, psychology and habituation. Behav Res Ther 25:81–97

    Article  CAS  PubMed  Google Scholar 

  • Magurran AE, Girling S (1986) Predator recognition and response habituation in shoaling minnows. Anim Behav 34:510–518

    Article  Google Scholar 

  • McGrew WC, Tutin CEG (1978) Evidence for a social custom in wild chimpanzees. Man 13:234–251

    Article  Google Scholar 

  • Mineka S, Davidson M, Cook M, Keir R (1984) Fear of snakes in wild and lab-reared rhesus monkeys. J Abnorm Psychol 93:355–372

    Article  CAS  PubMed  Google Scholar 

  • Morgan D, Sanz C (2003) Naive encounters with chimpanzees in the Goualougo triangle, Republic of Congo. Int J Primatol 24:369–381

    Article  Google Scholar 

  • Newton-Fisher NE (1999) The diet of chimpanzees in the Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354

    Article  Google Scholar 

  • 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 462–474

    Google Scholar 

  • Nishida T, Kawanaka K (1972) Inter-unit-group relationships among wild chimpanzees of the Mahale Mountains. Afr Stud 7:131–169

    Google Scholar 

  • 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 95:805

    Article  Google Scholar 

  • 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 105

  • 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 405–427

    Google Scholar 

  • Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Raderschall CA, Magrath RD, Hemmi JM (2011) Habituation under natural conditions: model predators are distinguished by approach direction. J Exp Biol 214:4209–4216

    Article  PubMed  Google Scholar 

  • Reynolds V (2005) The Chimpanzees of the Budongo Forest: ecology, behaviour, and conservation: ecology, behaviour, and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Romanes GJ (1882) Animal intelligence. Kegan Paul Trench & Co., London

    Google Scholar 

  • Russell CL, Bard KA, Adamson LB (1997) Social referencing by young chimpanzees (Pan troglodytes). J Comp Psychol 111:185

    Article  CAS  PubMed  Google Scholar 

  • Schaller GB (1963) The mountain gorilla; ecology and behavior. University of Chicago Press. xvii, Chicago, p 431

    Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Method Ecol Evol 1:103–113

    Article  Google Scholar 

  • Sherry DF, Galef BG (1984) Cultural transmission without imitation: milk bottle opening by birds. Anim Behav 32:937–938

    Article  Google Scholar 

  • Sommer V, Adanu J, Faucher I, Fowler A (2004) Nigerian Chimpanzees (Pan troglodytes vellerosus) at Gashaka: 2 years of habituation efforts. Folia Primatol 75:295–316

    Article  PubMed  Google Scholar 

  • Stein L (1966) Habituation and stimulus novelty: a model based on classical conditioning. Psychol Rev 73:352–356

    Article  CAS  PubMed  Google Scholar 

  • Tennie C, Call J, Tomasello M (2006) Push or pull: imitation versus emulation in great apes and human children. Ethology 112:1159–1169

    Article  Google Scholar 

  • Thorndike EL (1898) Animal intelligence: an experimental study of the associative process in animals. Psychol Rev Monogr 2:551–553

    Article  Google Scholar 

  • Thorpe W (1963) Learning and instinct in animals. Methuen, London

    Google Scholar 

  • 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 274–311

    Chapter  Google Scholar 

  • Tomasello M, Davis-Dasilva M, Camak L, Bard K (1987) Observational learning of tool-use by young chimpanzees. Primates 30:35–50

    Article  Google Scholar 

  • 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 187–197

    Chapter  Google Scholar 

  • 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 21:239–283

    Article  Google Scholar 

  • Whiten A, Horner V, Litchfield CA, Marshall-Pescini S (2004) How do apes ape? Learn Behav 32:36–52

    Article  PubMed  Google Scholar 

  • 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 Minnesota

  • 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 25–39

    Google Scholar 

  • Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36(02):153–160

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine Hobaiter.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 104 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Samuni, L., Mundry, R., Terkel, J. et al. Socially learned habituation to human observers in wild chimpanzees. Anim Cogn 17, 997–1005 (2014). https://doi.org/10.1007/s10071-014-0731-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-014-0731-6

Keywords

Navigation