Abstract
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.
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References
Asensio, N., Brockelman, W. Y., Malaivijitnond, S., & Reichard, U. H. (2011). Gibbon travel paths are goal oriented. Animal Cognition, 14(3), 395–405.
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.
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.
Cunningham, E. (2003). The use of memory in Pithecia pithecia’s foraging strategy. Ph.D. thesis, City University of New York.
Cunningham, E. P., & Janson, C. H. (2006). Pithecia pithecia's behavioral response to decreasing fruit abundance. American Journal of Primatology, 68(5), 491–497.
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.
Garber, P. A. (1988). Foraging decisions during nectar-feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis). Biotropica, 20, 100–106.
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.
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.
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.
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.
Janson, C. H. (1998). Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus apella. Animal Behaviour, 55(5), 1229–1243.
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.
Joly, M., & Zimmermann, E. (2011). Do solitary foraging nocturnal mammals plan their routes? Biology Letters, 7, 638–640.
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.
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.
Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219–1235.
Milton, K. (1981). Distribution patterns of tropical food plants as an evolutionary stimulus to primate mental development. American Anthropologist, 83, 534–548.
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.
Moura, A. C., & Lee, P. C. (2004). Capuchin stone tool use in Caatinga dry forest. Science, 306(5703), 1909.
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.
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.
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.
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.
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.
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.
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.
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.
Sokal, R. R., & Rohlf, F. J. (1995). Biometry. New York: W. H. Freeman.
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.
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.
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.
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.
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.
Acknowledgments
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.
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Cunningham, E.P., Janson, C.H. Effect of Fruit Scarcity on Use of Spatial Memory in a Seed Predator, White-faced Saki (Pithecia pithecia). Int J Primatol 34, 808–822 (2013). https://doi.org/10.1007/s10764-013-9697-5
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DOI: https://doi.org/10.1007/s10764-013-9697-5