Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Research Note
  • Published:

The effect of environmental enrichment on the behavior of captive tufted capuchin monkeys (Cebus apella)

Lab Animal volume 39, pages 269–277 (2010)Cite this article

Abstract

The authors provided different forms of environmental enrichment to six old laboratory male tufted capuchin monkeys (Cebus apella) and studied the behavior of the monkeys during a baseline period and during three enrichment periods. Each observation period lasted 5 d, with an interval of 6 d between periods. During the first enrichment period, the authors provided Buster cubes and wood cylinders with drilled holes filled with gum arabic. During the second enrichment period, monkeys were provided with a deep litter of bark shavings, and during the third enrichment period, they were given Buster cubes, wood cylinders and bark shavings. When provided with enrichment, the monkeys engaged in natural, species-specific activities and began to exhibit behavioral profiles that more closely resembled those of their natural counterparts. This suggests that their psychological well-being had improved and that group housing combined with environmental enrichment can improve the welfare of old laboratory tufted capuchin monkeys that were previously housed individually.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Enrichment provided for tufted capuchin monkeys.
Figure 2: Average amount of time spent on different behavioral categories (affiliative behavior, object manipulation, vigilance, foraging and abnormal behavior) during the four testing periods.

Similar content being viewed by others

References

  1. Institute for Laboratory Animal Research. The Psychological Well-Being of Nonhuman Primates (National Academy Press, Washington, DC, 1998).

  2. Mason, G., Clubb, R., Latham, N.R. & Vickery, S. Why and how should we use environmental enrichment to tackle stereotypic behavior? Appl. Anim. Behav. Sci. 102, 163–188 (2007).

    Article  Google Scholar 

  3. Fekete, J.M., Norcross, J.L. & Newman, J.D. Artificial turf foraging boards as environmental enrichment for pair-housed female squirrel monkeys. Contemp. Top. Lab. Anim. Sci. 39, 22–26 (2000).

    CAS  PubMed  Google Scholar 

  4. Mason, G.J. & Latham, N.R. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator? Anim. Welfare 13, 57–69 (2004).

    Google Scholar 

  5. Bayne, K. et al. The use of artificial turf as a foraging substrate for individually housed rhesus monkeys (Macaca mulata). Anim. Welfare 1, 39–53 (1992).

    Google Scholar 

  6. Line, S.W. Environmental enrichment for laboratory primates. J. Am. Vet. Med. Assoc. 190, 854–859 (1987).

    CAS  PubMed  Google Scholar 

  7. Lindburg, D.G. Improving the feeding of captive felines through application of field data. Zoo Biol. 7, 211–218 (1988).

    Article  Google Scholar 

  8. Fragaszy, D.M., Boinski, S. & Whipple, J. Behavioral sampling in the field: Comparison of individual and group sampling methods. Am. J. Primatol. 26, 259–275 (1992).

    Article  Google Scholar 

  9. Martin, P. & Bateson, P. Measuring Behaviour: An Introductory Guide 2nd edn. (Cambridge University Press, Cambridge, 1993).

    Book  Google Scholar 

  10. Veasey, J.S., Waran, N.K. & Young, R.J. On comparing the behaviour of zoo housed animals with wild conspecifics as a welfare indicator, using the giraffe (Giraffa camelopardalis) as a model. Anim. Welfare 5, 139–153 (1996).

    Google Scholar 

  11. Boinski, S., Swing, S.P., Gross, T.S. & Davis, J.K. Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness. Am. J. Primatol. 48, 49–68 (1999).

    Article  CAS  Google Scholar 

  12. Carlstead, K., Brown, J.L. & Seidensticker, J. Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo Biol. 12, 321–331 (1993).

    Article  Google Scholar 

  13. Snowdon, C.T. The significance of naturalistic environments for primate behavioral research. in Naturalistic Environment in Captivity for Animal Behavior Research (eds. Gibbons Jr., E.F., Wyers, E.J., Waters, E. & Menzel Jr., E.W.) 217–235 (State University of New York Press, Albany, NY, 1994).

    Google Scholar 

  14. Chamove, A.S. Environmental enrichment: A review. Anim. Technol. 40, 155–178 (1989).

    Google Scholar 

  15. Celli, M.L., Tomonaga, M., Udono, T., Teramoto, M. & Nagano, K. Tool use task as environmental enrichment for captive chimpanzees. Appl. Anim. Behav. Sci. 81, 171–182 (2003).

    Article  Google Scholar 

  16. Honess, P.E. & Marin, C.M. Enrichment and aggression in primates. Neurosci. Biobehav. Rev. 30, 413–436 (2006).

    Article  CAS  Google Scholar 

  17. Bayne, K. et al. The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. Am. J. Primatol. 23, 23–35 (1991).

    Article  Google Scholar 

  18. Ludes-Fraulob, E. & Anderson, J.R. Behavior and preferences among deep litters in captive capuchin monkeys (Cebus capucinus). Anim. Welfare 8, 127–134 (1999).

    Google Scholar 

  19. Baker, K.C. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees. Zoo Biol. 16, 225–236 (1997).

    Article  Google Scholar 

  20. Boccia, M.L. Preliminary report on the use of a natural foraging task to reduce aggression and stereotypies in socially housed pigtail macaques. Laboratory Primate Newsletter 28, 3–4 (1989).

    Google Scholar 

  21. Byrne, G.D. & Suomi, S.J. Effects of woodchip and buried food on behavior patterns and psychological well-being of captive rhesus monkeys. Am. J. Primatol. 23, 141–152 (1991).

    Article  Google Scholar 

  22. Blois-Heulin, C. & Jubin, R. Influence of the presence of seeds and litter on the behaviour of captive red-capped mangabeys Cercocebus torquatus torquatus. Appl. Anim. Behav. Sci. 85, 349–362 (2004).

    Article  Google Scholar 

  23. Izawa, K. Social behavior of the wild black-capped Capuchin (Cebus apella). Primates 21, 443–467 (1980).

    Article  Google Scholar 

  24. Fragaszy, D.M., Visalberghi, E. & Fedigan, L.M. The Complete Capuchin: The Biology of the Genus Cebus (Cambridge University Press, Cambridge, 2004).

    Google Scholar 

  25. Fragaszy, D.M., Izar, P., Visalberghi, E., Ottoni, E.B. & de Oliveira, M.G. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am. J. Primatol. 64, 359–366 (2004).

    Article  Google Scholar 

  26. Chevalier-Skolnikoff, S. Tool use by wild cebus monkeys at Santa Rosa National Park, Costa Rica. Primates 31, 375–383 (1990).

    Article  Google Scholar 

  27. Anderson, J.R. Use of objects as hammers to open nuts by capuchin monkeys (Cebus apella). Folia Primatol. 54, 138–145 (1990).

    Article  CAS  Google Scholar 

  28. Westergaard, G.C. & Fragaszy, D.M. The manufacture and use of tools by capuchin monkeys (Cebus apella). J. Comp. Psychol. 101, 159–168 (1987).

    Article  Google Scholar 

  29. Westergaard, G.C. & Fragaszy, D.M. Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella). Zoo Biol. 4, 317–327 (1985).

    Article  Google Scholar 

  30. Hayes, S.L. Increasing foraging opportunities for a group of captive capuchin monkeys (Cebus capucinus). Lab. Anim. Sci. 40, 515–519 (1990).

    CAS  PubMed  Google Scholar 

  31. Parker, S.T. & Gibson, K.R. Object manipulation, tool use and sensorimotor intelligence as feeding adaptions in cebus monkeys and great apes. J. Hum. Evol. 6, 623–641 (1977).

    Article  Google Scholar 

  32. Schapiro, S.J., Brent, L., Bloomsmith, M.A. & Satterfield, W.C. Enrichment devices for nonhuman primates. Lab. Anim. (NY) 20, 22–28 (1991).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Beisner, B.A. & Isbell, L.A. Ground substrate affects activity budgets and hair loss in outdoor captive groups of rhesus macaques (Macaca mulatta). Am. J. Primatol. 70, 1160–1168 (2008).

    Article  Google Scholar 

  35. Fragaszy, D.M. & Adams-Curtis, L.E. Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella). J. Comp. Psychol. 105, 387–397 (1991).

    Article  CAS  Google Scholar 

  36. Westergaard, G.C., Lundquist, A.L., Haynie, M.K., Kuhn, H.E. & Suomi, S.J. Why some capuchin monkeys (Cebus apella) use probing tools (and others do not). J. Comp. Psychol. 112, 207–211 (1998).

    Article  CAS  Google Scholar 

  37. Westergaard, G. & Fragaszy, D. Self-treatment of wounds by a capuchin monkey (Cebus apella). Hum. Evolution 1, 557–562 (1987).

    Article  Google Scholar 

  38. Ritchie, B.G. & Fragaszy, D.M. Capuchin monkey (Cebus apella) grooms her infant's wound with tools. Am. J. Primatol. 16, 345–348 (1988).

    Article  Google Scholar 

  39. Tarou, L.R. & Bashaw, M.J. Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior. Appl. Anim. Behav. Sci. 102, 189–204 (2007).

    Article  Google Scholar 

  40. Walsh, S., Bramblett, C.A. & Alford, P.L. A vocabulary of abnormal behaviors in restrictively reared chimpanzees. Am. J. Primatol. 3, 315–319 (1982).

    Article  Google Scholar 

  41. Baker, K.C. & Eisele, S.P. An analysis of regurgitation and reingestion in captive chimpanzees. Appl. Anim. Behav. Sci. 49, 403–415 (1996).

    Article  Google Scholar 

  42. Gould, E. & Bres, M. Regurgitation and reingestion in captive gorillas: Description and intervention. Zoo Biol. 5, 241–250 (1986).

    Article  Google Scholar 

  43. Akers, J.S. & Schildkraut, D.S. Regurgitation/reingestion and coprophagy in captive gorillas. Zoo Biol. 4, 99–109 (1985).

    Article  Google Scholar 

  44. Marriner, L.M. & Drickamer, L.C. Factors influencing stereotyped behavior of primates in a zoo. Zoo Biol. 13, 267–275 (1994).

    Article  Google Scholar 

  45. Hughes, B.O. & Duncan, I.J.H. The notion of ethological 'need', models of motivation and animal wellfare. Anim. Behav. 36, 1696–1707 (1988).

    Article  Google Scholar 

  46. Vick, S.-J., Anderson, J.R. & Young, R. Maracas for Macaca? Evaluation of three potential enrichment objects in two species of zoo-housed macaques. Zoo Biol. 19, 181–191 (2000).

    Article  Google Scholar 

  47. Visalberghi, E., Valenzano, D.R. & Preuschoft, S. Facial displays in Cebus apella. Int. J. Primatol. 27, 1689–1707 (2006).

    Article  Google Scholar 

  48. De Marco, A. & Visalberghi, E. Facial displays in young tufted capuchin monkeys (Cebus apella): Appearance, meaning, context and target. Folia Primatol. 78, 118–137 (2007).

    Article  Google Scholar 

  49. Augustsson, H. & Hau, J. A simple ethological monitoring system to assess social stress in group-housed laboratory rhesus macaques. J. Med. Primatol. 28, 84–90 (1999).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was done in collaboration with Ree Park – Ebeltoft Safari.

Author information

Authors and Affiliations

  1. Department of Experimental Medicine, Faculty of Health Sciences, University of Copenhagen, Copenhagen N, Denmark

    Kirsten R. Jacobsen &  J. Hau

  2. Animal Unit, Management, Novo Nordisk A/S, Novo Nordisk Park, Måløv, Denmark

    L.F. Mikkelsen

Authors
  1. Kirsten R. Jacobsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L.F. Mikkelsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Hau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kirsten R. Jacobsen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jacobsen, K., Mikkelsen, L. & Hau, J. The effect of environmental enrichment on the behavior of captive tufted capuchin monkeys (Cebus apella). Lab Anim 39, 269–277 (2010). https://doi.org/10.1038/laban0910-269

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/laban0910-269

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing