International Journal of Primatology

, Volume 31, Issue 3, pp 457–470 | Cite as

Wild Capuchins Show Male-Biased Feeding Tool Use



Relatively few studies have explored sex differences in the use of foraging tools among primates other than apes. Although male primates are thought to be more innovative, researchers have reported a female sex bias in the use of feeding tools in wild chimpanzees. We investigate here the nature and extent of sex differences in foraging tool use over 12 mo in a free-ranging group of bearded capuchins (2 males, 5 females, and 3 juveniles) living in the dry Caatinga forests of the Serra da Capivara National Park, Piaui, Brazil. These capuchins used 3 major types of feeding tools: 1) tools for probing; 2) tools for pounding/cracking; and 3) digging stones to extract tubers or roots. Adult males performed 63% (n = 134) of all events of tool use and used tools significantly more frequently than did females, although male bout lengths across all tools (57 s ± 7.9 SE) were equivalent to those of adult females (47.3 s ± 12.6 SE). Both sexes used digging and cracking tools, although at different rates, whereas adult males used sticks to probe for prey and other rewards far more than females. Differential opportunities to use tools were not apparent: >71% of tool-use events occurred on the ground, and males and females spent equal time on the ground. We suggest that sex differences in tool use may function as opportunities for male signaling of investment quality.


Cebus sex differences sexual selection tool use 



We thank Niede Guidon for logistical support that made this work possible, the Brazilian Research Council (CNPq) for the PhD scholarship (A. C. de A. Moura) and FAPESB-Bahia for a post-doc fellowship grant and a partial travel grant to A. C. de A. Moura to attend the 2008 IPS and present this paper. A. C. de A. Moura thanks Stephen Shapiro, who waived his registration fees during the IPS 2008 meeting. This research conformed to the ethical and legal requirements of the Government of Brazil, and ASAB guidelines for working with animals. We thank several reviewers for their many comments on earlier drafts.


  1. Boesch, C., & Boesch, H. (1984). Possible causes of sex differences in the use of natural hammers by wild chimpanzees. Journal of Human Evolution, 13, 415–440.CrossRefGoogle Scholar
  2. Boinski, S. (2004). The beats of different drummers: percussion as sexual signaling among brown capuchins at Raleighvallen, Suriname. Folia Primatologica, 75, 238.Google Scholar
  3. Clinebell, R. R., Phillips, O. L., Gentry, A. H., Stark, N., & Zuuring, H. (1995). Prediction of neotropical tree and liana species richness from soil and climatic data. Biodiversity Conservervation, 4, 56–90.CrossRefGoogle Scholar
  4. Emperaire, L. (1984). A regiao da Serra da Capivara (sudeste do Piaui) e sua Vegetacao. Brasil Florestal, 60, 4–21.Google Scholar
  5. Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39, 175–191.PubMedGoogle Scholar
  6. Fragaszy, D. M. (1990). Sex and age differences in the organization of behavior in wedge-capped capuchins, Cebus olivaceus. Behavioural Ecology, 1, 81–94.CrossRefGoogle Scholar
  7. Gunther, M. M., & Boesch, C. (1993). Energetic cost of nut-cracking behaviour in wild chimpanzees. In H. Preuschoft, D. J. Chivers (Eds.), Hands of Primates (pp. 109–129). Vienna: Springer-Verlag.Google Scholar
  8. Jalles-Filho, E. (1995). Manipulative propensity and tool use in capuchin monkeys. Current Anthropology, 36, 664–667.CrossRefGoogle Scholar
  9. Jalles-Filho, E., & Cunha, R. G. T. (2008). Manipulation and tool use in captive yellow-breasted capuchin monkeys (Cebus xanthosternos). International Journal of Comparative Psychology, 21, 12–18.Google Scholar
  10. Jalles-Filho, E., Cunha, R. G. T., & Salm, R. A. (2001). Transport of tools and mental representation: is capuchin monkey tool behavior a useful model of Plio-Pleistocene hominid technology? Journal of Human Evolution, 40, 365–377.CrossRefPubMedGoogle Scholar
  11. Janson, C. H. (1984). Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). Zeitschrift furTierpsychologi, 65, 177–200.Google Scholar
  12. Kohn, M., & Mithen, S. (1999). Handaxes: Products of sexual selection? Antiquity, 73, 518–526.Google Scholar
  13. Kuhn, S. L., & Stiner, M. C. (2006). What’s a mother to do? Current Anthropology, 47, 953–976.CrossRefGoogle Scholar
  14. Laden, G., & Wrangham, R. (2005). The rise of the hominids as an adaptive shift in fallback foods: Plant underground storage organs (USOs) and australopith origins. Journal of Human Evolution, 49, 482–498.CrossRefPubMedGoogle Scholar
  15. Leger, D. W., & Didrichsons, A. I. (1994). An assessment of data pooling and some alternatives. Animal Behaviour, 48, 823–832.CrossRefGoogle Scholar
  16. Liu, Q., Simpson, K., Izar, P., Ottoni, E., Visalberghi, E., & Fragaszy, D. (2009). Kinematics and energetic of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piaui, Brazil. American Journal of Physical Anthropology, 138, 210–220.CrossRefPubMedGoogle Scholar
  17. Lonsdorf, E. V., Eberly, L. E., & Pusey, A. E. (2004). Sex differences in learning in chimpanzees. Nature, 428, 715.CrossRefPubMedGoogle Scholar
  18. Mannu, M., & Ottoni, E. (2009). The enhanced tool-kit of two groups of wild bearded capuchin monkeys in the Caatinga: Tool making, associative use, and secondary tools. American Journal of Primatology, 70, 1–10.Google Scholar
  19. Martin, P. S., & Bateson, P. P. G. (1986). Measuring behaviour. Cambridge: Cambridge University Press.Google Scholar
  20. McGrew, W. C. (1992). Chimpanzee material culture. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  21. Miller, L. E. (1996). The behavioral ecology of wedge-capped capuchin monkeys (Cebus olivaceus). In M. A. Norconk, P. A. Garder, A. F. Rosenberger (Eds.), Adaptive radiations of Neotropical Primates (pp. 271–288). New York: Plenum Press.Google Scholar
  22. Moura, A. C. de. A. (2003). Ecological pressure driving tool use in capuchin monkeys. Folia Primatologica, 74, 209.Google Scholar
  23. Moura, A. C. de. A. (2004). The capuchin monkey and the Caatinga dry forest: A hard life in a harsh habitat. PhD Thesis, University of Cambridge.Google Scholar
  24. Moura, A. C. de. A. (2007a). Primate group size and abundance in the Caatinga dry forest, Northeastern Brazil. International Journal of Primatology, 28, 1279–1297.CrossRefGoogle Scholar
  25. Moura, A. C. de. A. (2007b). Stone banging by wild capuchin monkeys: A unusual auditory display. Folia Primatologica, 78, 36–45.CrossRefGoogle Scholar
  26. Moura, A. C. de. A., & Lee, P. C. (2004). Capuchin stone tool use in Caatinga dry forest. Science, 306, 1909.CrossRefPubMedGoogle Scholar
  27. Moura, A. C. de. A., & McConkey, K. R. (2007). The capuchin, the howler and the Caatinga forest: Seed dispersal by monkeys in a threatened Brazilian biome. American Journal of Primatolology, 69, 220–226.CrossRefGoogle Scholar
  28. O’Connell, J. F., Hawkes, K., & Blurton-Jones, N. G. (1999). Grandmothering and the evolution of Homo erectus. Journal of Human Evolution, 36, 461–485.CrossRefPubMedGoogle Scholar
  29. Ottoni, E. B., & Izar, P. (2008). Capuchin monkey tool use: Overview and implications. Evolutionary Anthropology, 17, 171–178.CrossRefGoogle Scholar
  30. Ottoni, E. B., & Mannu, M. (2001). Semifree-ranging tufted capuchins (Cebus apella) spontaneously use tools to crack open nuts. International Journal of Primatology, 22, 310–328.CrossRefGoogle Scholar
  31. Ottoni, E. B., Resende, B. D., & Izar, P. (2005). Watching the best nutcrackers: What capuchin monkeys (Cebus apella) know about others’ tool-using skills. Animal Cognition, 24, 215–219.CrossRefGoogle Scholar
  32. Reader, S. M., & Laland, K. N. (2001). Primate innovation: Sex, age and social rank differences. International Journal of Primatology, 22, 787–805.CrossRefGoogle Scholar
  33. Robinson, J. G. (1986). Seasonal variation in use of time and space by the wedge-capped capuchin monkey, Cebus olivaceus: Implications for foraging theory. Smithsonian Contribution to Zoology, 431, 1–60.Google Scholar
  34. Tebbich, S., Taborsky, M., Fessl, B., & Dvorak, M. (2002). The ecology of tool-use in the woodpecker finch (Cactospiza pallida). Ecological Letters, 5, 656–664.CrossRefGoogle Scholar
  35. Trejo, I., & Dirzo, R. (2002). Floristic diversity of Mexican seasonally dry tropical forests. Biodiversity and Conservation, 11, 2063–2048.CrossRefGoogle Scholar
  36. Visalberghi, E. (1987). Acquisition of nut-cracking behaviour by 2 capuchin monkeys (Cebus apella). Folia Primatologica, 49, 168–181.CrossRefGoogle Scholar
  37. Visalberghi, E., Addessi, E., Truppa, V., Spagnoletti, N., Ottoni, E., Izar, P., et al. (2009). Selection of effective stone tools by wild bearded capuchin monkeys. Current Biology, 19, 213–217.CrossRefPubMedGoogle Scholar
  38. Westergaard, G. C., Lundquist, A. L., Haynie, M. K., Kuhn, H. E., & Suomi, S. J. (1998). Why some capuchin monkeys (Cebus apella) use probing tools (and others do not). Journal of Comparative Psychology, 112, 207–211.CrossRefPubMedGoogle Scholar
  39. Yamakoshi, G. (1998). Dietary response to fruit scarcity of wild chimpanzees at Bossou, Guinea: Possible implications for ecological importance of tool use. American Journal of Physical Anthropology, 106, 283–295.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Centro de Ciencias Aplicadas e Educacao, Departamento de Engenharia e Meio AmbienteUniversidade Fedaral da ParabaRio TintoBrazil
  2. 2.Department of Psychology, Behaviour and Evolution Research GroupUniversity of StirlingStirlingScotland

Personalised recommendations