International Journal of Primatology

, Volume 34, Issue 4, pp 808–822 | Cite as

Effect of Fruit Scarcity on Use of Spatial Memory in a Seed Predator, White-faced Saki (Pithecia pithecia)

  • Elena P. Cunningham
  • Charles H. Janson


Many studies have shown that primates use spatial memory to travel efficiently between important resources such as trees with ripe fruit or water holes. White-faced sakis (Pithecia pithecia) have shown strong evidence of spatial memory as they travel efficiently to feed on the seeds of highly productive fruit trees and the ripe fruit of a highly preferred tree species and to drink from natural cisterns in trees. Researchers theorize that primates rely less on memory when they feed on more evenly dispersed food. Here we examine the use of spatial memory in a group of wild white-faced sakis during a month of fruit scarcity when they foraged for desiccated seeds, leaves, insect material, and flowers. We used logistic regression and three computer models (the geometric model, the step model, and the change point model) to analyze their movement patterns. We find that the focal group does not demonstrate the use of memory. These results are in contrast to results from a study of spatial memory with the same focal group in the two immediately preceding months. The results conform to theories on the role of nutritionally dense and patchy foods in driving the use of memory during travel between feeding sites. They demonstrate that, within a short time, a group of primates can vary from a strong reliance on spatial memory to no demonstrable use of spatial memory.


Cognition Fallback foods Platyrrhine Ranging Scarcity White-faced saki 



E. P. Cunningham is grateful to the City University of New York Graduate School, L. S. B. Leakey Foundation, W. G. Kinzey Fund, and Wenner-Gren Foundation for funding this research. E. Cunningham thanks Karyl Swartz whose support made this research possible. We are grateful to the administration of EDELCA for allowing us to study the primates of Guri Lake. We thank Marilyn Norconk for helping E. P. Cunningham work at the study site. E. Cunningham thanks Amy Levine for her hard work and friendship in the field. We also thank John Robinson, Eric Delson, and Sharon Himmanen for their comments and logistical support. E. P. Cunningham thanks Johanna Warshaw for helping her navigate Adobe Illustrator CS2. We are grateful to Joanna Setchell and two anonymous reviewers for insightful comments.


  1. Asensio, N., Brockelman, W. Y., Malaivijitnond, S., & Reichard, U. H. (2011). Gibbon travel paths are goal oriented. Animal Cognition, 14(3), 395–405.Google Scholar
  2. Barton, R. A. (1996). Neocortex size and behavioural ecology in primates. Proceedings of the Royal Society of London B: Biological Sciences, 263(1367), 173–177.CrossRefGoogle Scholar
  3. Byrne, R. W., Noser, R., Bates, L. A., & Jupp, P. E. (2009). How did they get here from there? Detecting changes of direction in terrestrial ranging. Animal Behaviour, 77, 619–631.CrossRefGoogle Scholar
  4. Cunningham, E. (2003). The use of memory in Pithecia pithecia’s foraging strategy. Ph.D. thesis, City University of New York.Google Scholar
  5. Cunningham, E. P., & Janson, C. H. (2006). Pithecia pithecia's behavioral response to decreasing fruit abundance. American Journal of Primatology, 68(5), 491–497.PubMedCrossRefGoogle Scholar
  6. Cunningham, E., & Janson, C. (2007). Integrating information about location and value of resources by white-faced saki monkeys (Pithecia pithecia). Animal Cognition, 10(3), 293–304.PubMedCrossRefGoogle Scholar
  7. Garber, P. A. (1988). Foraging decisions during nectar-feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis). Biotropica, 20, 100–106.CrossRefGoogle Scholar
  8. Hemingway, C. A., & Bynum, N. (2005). The influence of seasonality on primate diet and ranging. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 57–104). New York: Cambridge University Press.CrossRefGoogle Scholar
  9. Hopkins, M. E. (2008). Spatial foraging patterns and ranging behavior of mantled howler monkeys (Alouatta palliata), Barro Colorado Island, Panama Ph.D. thesis, University of California, Berkeley.Google Scholar
  10. Janmaat, K. R. L., Byrne, R. W., & Zuberbühler, K. (2006). Evidence for a spatial memory of fruiting states of rainforest trees in wild mangabeys. Animal Behaviour, 72, 797–807.CrossRefGoogle Scholar
  11. Janmaat, K., Chapman, C., Meijer, R., & Zuberbühler, K. (2012). The use of fruiting synchrony by foraging mangabey monkeys: A ‘simple tool’ to find fruit. Animal Cognition, 15(1), 83–96.PubMedCrossRefGoogle Scholar
  12. Janson, C. H. (1998). Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus apella. Animal Behaviour, 55(5), 1229–1243.PubMedCrossRefGoogle Scholar
  13. Janson, C. H. (2000). Spatial movement strategies: Theory, evidence, and challenges. In S. Boinksi & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 165–203). Chicago: Chicago University Press.Google Scholar
  14. Joly, M., & Zimmermann, E. (2011). Do solitary foraging nocturnal mammals plan their routes? Biology Letters, 7, 638–640.PubMedCrossRefGoogle Scholar
  15. Kinzey, W. G., & Norconk, M. A. (1993). Physical and chemical properties of fruit and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. International Journal of Primatology, 14(2), 207–227.CrossRefGoogle Scholar
  16. Lambert, J. E. (2007). Seasonality, fallback strategies, and natural selection: A chimpanzee and circopithecoid model for interpreting the evolution of hominin diet. In P. S. Ungar (Ed.), Evolution of the human diet: The known, the unknown, and the unknowable (pp. 324–343). Oxford: Oxford University Press.Google Scholar
  17. Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219–1235.CrossRefGoogle Scholar
  18. Milton, K. (1981). Distribution patterns of tropical food plants as an evolutionary stimulus to primate mental development. American Anthropologist, 83, 534–548.CrossRefGoogle Scholar
  19. Milton, K. (1988). Foraging behaviour and the evolution of primate intelligence. In R. Byrne & A. Whiten (Eds.), Machiavellian intelligence (pp. 285–305). Oxford: Clarendon Press.Google Scholar
  20. Moura, A. C., & Lee, P. C. (2004). Capuchin stone tool use in Caatinga dry forest. Science, 306(5703), 1909.PubMedCrossRefGoogle Scholar
  21. Norconk, M. A. (1996). Seasonal variation in the diets of white-faced and bearded sakis (Pithecia pithecia and Chiropotes satanas) in Guri Lake, Venezuela. In M. A. Norconk, A. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of neotropical primates (pp. 403–425). New York: Plenum Press.CrossRefGoogle Scholar
  22. Norconk, M. A., & Conklin-Brittain, N. L. (2004). Variation on frugivory: The diet of Venezuelan white-faced sakis. International Journal of Primatology, 25(1), 1–26.CrossRefGoogle Scholar
  23. Norconk, M. A., & Veres, M. (2011). Physical properties of fruit and seeds ingested by primate seed predators with emphasis on sakis and bearded sakis. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 294(12), 2092–2111.CrossRefGoogle Scholar
  24. Norconk, M. A., Oftedal, O. T., Power, M. L., Jakubasz, M., & Savage, A. (2002). Digesta passage and fiber digestibility in captive white-faced sakis (Pithecia pithecia). American Journal of Primatology, 58(1), 23–34.PubMedCrossRefGoogle Scholar
  25. Normand, E., Ban, S., & Boesch, C. (2009). Forest chimpanzees (Pan troglodytes verus) remember the location of numerous fruit trees. Animal Cognition, 12(6), 797–807.PubMedCrossRefGoogle Scholar
  26. Noser, R., & Byrne, R. W. (2007a). Mental maps in chacma baboons (Papio ursinus): Using intergroup encounters as a natural experiment. Animal Cognition, 10(3), 331–340.PubMedCrossRefGoogle Scholar
  27. Noser, R., & Byrne, R. W. (2007b). Travel routes and planning of visits to out of sight resources in wild chacma baboons, Papio ursinus. Animal Behaviour, 73, 257–266.CrossRefGoogle Scholar
  28. Sawaguchi, T. (1992). The size of the neocortex in relation to ecology and social structure in monkeys and apes. Folia Primatologica, 58(3), 131–145.CrossRefGoogle Scholar
  29. Sokal, R. R., & Rohlf, F. J. (1995). Biometry. New York: W. H. Freeman.Google Scholar
  30. Valero, E., & Byrne, R. W. (2007). Spider monkey ranging patterns in Mexican subtropical forest: Do travel routes reflect planning? Animal Cognition, 10(3), 305–315.PubMedCrossRefGoogle Scholar
  31. van Schaik, C. P., & Knott, C. D. (2001). Geographic variation in tool use on Nesia fruits in orangutans. American Journal of Physical Anthropology, 114, 331–342.PubMedCrossRefGoogle Scholar
  32. van Woerden, J.T., Willems, E.P., van Schaik C.P., & Isler, K. (2012). Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution, 66(1), 191–199.Google Scholar
  33. Willems, E. P., & Hill, R. A. (2009). Predator-specific landscapes of fear and resource distribution: Effects on spatial range use. Ecology, 90(2), 546–555.PubMedCrossRefGoogle Scholar
  34. Yamakoshi, G. (1998). Dietary responses 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Basic Science and Craniofacial BiologyNew York University College of DentistryNew YorkUSA
  2. 2.Division of Biological SciencesUniversity of MontanaMissoulaUSA

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