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Exploring New Areas: How Important is Long-Term Spatial Memory for Mangabey (Lophocebus albigena johnstonii) Foraging Efficiency?

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Abstract

Studies of primate foraging efficiency during the exploration of new areas can provide important insights into the adaptive value of long-term spatial memory. After 6 yr of observation of a group of gray-cheeked mangabeys (Lophocebus albigena johnstonii) in Kibale National Park, Uganda, we observed exploration of a new area, followed 7 mo later by a group split. We recorded their ranging and foraging behavior for 22 mo after the first exploration. Controlling for weather variables, we found that mangabeys moved longer daily travel distances, explored more area per day, and had larger group spreads in the new area compared to the old area in both parent and daughter groups. The increase in search swath in the new area likely enabled the monkeys to counteract their lack of knowledge of food locations in the new area, as the efficiency in finding fruit in general did not differ between the old and new areas. We did, however, find a lower efficiency in finding fruit from preferred fig trees whose edibility could not be assessed by visual cues in the new area. Fig finding efficiency remained lower, even when we controlled for potential differences in fig density. In addition, mangabeys traveled and foraged less often on the ground in the new compared to the old area. However, when the monkeys became more familiar with the new area, terrestrial behavior increased. Our results are consistent with the hypothesis that when monkeys move into an area in which they have no experience, an absence of knowledge acquired via long-term spatial memory decreases their foraging efficiency.

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References

  • Altmann, S. A., & Altmann, J. (1970). Baboon ecology: African field research. Basel: Karger.

    Google Scholar 

  • Aronsen, G. P. (2004). Locomotor energetics and forest canopy variation: implications for conservation and management. Folia Primatologica Supplement, 1, 233.

    Google Scholar 

  • Balda, R. P. & Kamil, A. C. (1998). The ecology and evolution of spatial memory in corvids of the Southwestern USA: The perplexing pinyon jay. In R. O. Balda, I. M. Pepperberg & A. C. Kamil (Eds.), Animal cognition in nature: The convergence of psychology and biology in laboratory and field (pp. 29–64). San Diego, CA: Academic Press.

    Google Scholar 

  • Barrett, L. (1995). Foraging strategies, ranging patterns and territoriality among gray-cheeked mangabeys in Kibale forest, Western Uganda. Ph.D. thesis, University College London.

  • Bronikowski, M., & Altmann, J. (1996). Foraging in a variable environment: weather patterns and the behavioral ecology of baboons. Behavioral Ecology and Sociobiology, 39, 11–25.

    Article  Google Scholar 

  • Brown, C. (2001). Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Animal Cognition, 4, 109–113.

    Article  Google Scholar 

  • Chalmers, N. R. (1968). Group composition, ecology and daily activities of free living mangabeys in Uganda. Folia Primatologica, 8, 247–262.

    Article  CAS  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Wrangham, R., Isabirye-Basuta, G., & Ben-David, K. (1997). Spatial and temporal variability in the structure of a tropical forest. African Journal of Ecology, 35, 341–436.

    Article  Google Scholar 

  • Chapman, C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K., & Zanne, A. E. (1999). Fruit and flower phenology at two sites in Kibale National Park, Uganda. Journal of Tropical Ecology, 15, 189–211.

    Article  Google Scholar 

  • Chepko-Sade, B. D., & Sade, D. S. (1979). Patterns of group splitting within matrilineal kinship groups: a study of social group structure in Macaca mulatta (Cercopithecine: Primates). Behavioral Ecology and Sociobiology, 5, 67–87.

    Article  Google Scholar 

  • Cords, M., & Rowell, T. E. (1986). Group fission in blue monkeys of the Kakamega Forest, Kenya. Folia Primatologica, 46, 70–82.

    Article  Google Scholar 

  • Crook, J. H. (1965). The adaptive significance of avian social organization. Symposia of the Zoological Society of London, 14, 181–218.

    Google Scholar 

  • Di Fiore, A., & Suarez, S. A. (2007). Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications. Animal Cognition, 10, 317–329.

    Article  PubMed  Google Scholar 

  • Doolan, S. P., & MacDonald, D. W. (1996). Dispersal and extra-territorial prospecting by slender tailed meerkats (Suricata suricatta) in the south-western Kalahari. Journal of Zoology, 240, 59–73.

    Article  Google Scholar 

  • Emery, N. J., & Clayton, N. S. (2004). Comparing the complex cognition of birds and primates. In L. J. Rogers & G. Kaplan (Eds.), Comparative vertebrate cognition (pp. 3–55). The Hague: Kluwer Academic Press.

    Google Scholar 

  • Forsman, J. T., Mönkkönen, M., Inkeröinen, J., & Reunanen, P. (1998). Aggregate dispersion of birds after encountering a predator: experimental evidence. Journal of Avian Biology, 29, 44–48.

    Article  Google Scholar 

  • Garber, P. A. (1989). Role of spatial memory in primate foraging patterns Saguinus mystax and Saguinus fuscicollis. American Journal of Primatology, 19, 203–216.

    Article  Google Scholar 

  • Girvan, J. R. & Braithwaite, V. A. (1997). Orientation mechanisms in different populations of the three spined stickleback. In Orientation and Navigation – birds, humans and other animals. Oxford: Royal institute of Navigation.

  • Hamilton, W. D. (1971). Geometry for the selfish herd. Journal of Theoretical Biology, 31, 295–311.

    Article  CAS  PubMed  Google Scholar 

  • Isbell, L. A., & van Vuren, D. (1996). Differential cost of locational and social dispersal and their consequences for female group-living primates. Behaviour, 133, 1–36.

    Article  Google Scholar 

  • Isbell, L. A., Cheney, D. L., & Seyfarth, R. M. (1990). Costs and benefits of home range shifts among vervet monkeys (Cercopithecus aethiops) in Amboseli National Park, Kenya. Behavioral Ecology and Sociobiology, 27, 351–358.

    Article  Google Scholar 

  • Janmaat, K. R. L. (2006). Fruits of enlightenment: Fruit finding strategies in wild mangabey monkeys. Ph.D. thesis, University of St. Andrews.

  • Janmaat, K. R. L., Byrne, R. W., & Zuberbühler, K. (2006a). Evidence for spatial memory of fruiting states of rain forest fruit in wild ranging mangabeys. Animal Behaviour, 71, 797–807.

    Article  Google Scholar 

  • Janmaat, K. R. L., Byrne, R. W., & Zuberbühler, K. (2006b). Primates take weather into account when searching for fruit. Current Biology, 16, 1232–1237.

    Article  CAS  PubMed  Google Scholar 

  • Janmaat, K. R. L., Olupot, W., Chancellor, R. L., Arlet, M. E., & Waser, P. M. (2009). Long-term site fidelity and individual home range shifts in Lophocebus albigena. International Journal of Primatology, 30, 443–466.

    Article  PubMed  Google Scholar 

  • Janmaat, K. R. L., Mijer, R., Chapman, C. A., & Zuberbuhler, K. (submitted). The use of fruiting synchrony in foraging mangabeys. Animal Cognition

  • Janson, C. H. (1998). Experimental evidence for spatial memory in foraging wild capuchin monkeys Cebus apella. Animal Behaviour, 55, 1229–1243.

    Article  PubMed  Google Scholar 

  • Janson, C. H., & Di Bitetti, M. S. (1997). Experimental analysis of food detection in capuchin monkeys: effects of distance, travel speed, and resource size. Behavioral Ecology and Sociobiology, 41, 17–24.

    Article  Google Scholar 

  • Knezevich, M. (1998). Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta). American Journal of Primatology, 44, 71–82.

    Article  CAS  PubMed  Google Scholar 

  • Krebs, C. J. (1988). Population ecology of individuals (pp. 1059–1060). Princeton: Princeton University Press.

  • Larsen, K. W., & Boutin, S. (1994). Movements, survival and settlement of red squirrel (Tamiasciurus hudsonicus) offspring. Ecology, 70, 214–223.

    Article  Google Scholar 

  • Manzer, M. B., & Bell, M. B. (2004). Spatial representation of shelter locations in meerkats, Suricata suricatta. Animal Behaviour, 68, 151–157.

    Article  Google Scholar 

  • Martin, P., & Bateson, P. (1986). Measuring behavior. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Menzel, E. W. (1973). Chimpanzee spatial memory organization. Science, 182, 943–945.

    Article  CAS  PubMed  Google Scholar 

  • Mermier, C. M., Robergs, R. A., McMinn, S. M., & Heyward, V. H. (1997). Energy expenditure and physiological responses during indoor rock climbing. British Journal of Sports Medicine, 31, 224–228.

    Article  CAS  PubMed  Google Scholar 

  • Metzgar, L. H. (1967). An experimental comparison of screech owl predation on resident and transient white-footed mice Peromyscus leucopus. Journal of Mammalogy, 48, 387–391.

    Article  Google Scholar 

  • Milton, K. (1988). Foraging behaviour and the evolution of primate intelligence. In R.W. Byrne and A. Whiten (Eds.), Machiavellian Intelligence: Social expertise and the evolution of intellect in monkeys, apes and humans (pp. 285–305). Oxford: Clarendon Press.

  • Murray, C. M., Gilby, I. C., Mane, S. V., & Pusey, A. E. (2008). Adult male chimpanzees inherit maternal ranging patterns. Current Biology, 18, 20–24.

    Article  CAS  PubMed  Google Scholar 

  • Muruthi, P., Altmann, J., & Altmann, S. (1991). Resource base, parity, and reproductive condition affect females’ feeding time and nutrient intake within and between groups of a baboon population. Oecologia, 87, 467–472.

    Article  Google Scholar 

  • Newton-Fisher, N. E. (2003). The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. African Journal of Ecology, 41, 150–156.

    Article  Google Scholar 

  • Nilsson, J. A. (1989). Causes and consequences of natal dispersal in marsh tit, Parus palustris. Journal of Animal Ecology, 58, 619–636.

    Article  Google Scholar 

  • Oates, J. F. (1978). Water-plant and soil consumption by guereza monkeys (Colobus guereza): a relationship with minerals and toxins in the diet? Biotropica, 10, 241–253.

    Article  Google Scholar 

  • Olupot, W. (1998). Long-term variation in mangabey (Cercocebus albigena johnstoni Lydekker) feeding in Kibale National Park, Uganda. African Journal of Ecology, 36, 96–101.

    Article  Google Scholar 

  • Olupot, W. (1999). Mangabey dispersal and conservation in Kibale National Park, Uganda. Ph.D. thesis, Purdue University.

  • Olupot, W. (2000). Body mass differences among male mangabeys inhabiting logged and unlogged forest compartments. Conservation Biology, 14, 833–843.

    Article  Google Scholar 

  • Perneger, T. V. (1998). What’s wrong with Bonferroni adjustments? British Medical Journal, 316, 1236–1238.

    CAS  PubMed  Google Scholar 

  • Poirier, F. E. (1968). Analysis of a Nilgiri langur (Presbytis johnii) home range change. Primates, 9, 29–43.

    Article  Google Scholar 

  • Poulsen, J. R., & Clark, C. J. (2007). Predation on mammals by the grey-cheeked mangabey Lophocebus albigena. Primates, 42, 391–394.

    Article  Google Scholar 

  • Reed, J. M., Boulinier, T., Danchin, E., & Oring, L. W. (1999). Prospecting by birds for breeding sites. Current Ornithology, 15, 189–259.

    Google Scholar 

  • Roper, T. J., Ostler, J. R., & Conradt, L. (2003). The process of dispersal in badgers Meles meles. Mammal Review, 33, 314–318.

    Article  Google Scholar 

  • Scheumann, M., & Call, J. (2006). Sumatran orangutans and a yellow-cheeked crested gibbon know what is where. International Journal of Primatology, 27, 575–601.

    Article  Google Scholar 

  • Shultz, S., Faurie, C., & Noe, R. (2003). Behavioral responses of Diana monkeys to male long-distance calls: changes in ranging, association patterns and activity. Behavioral Ecology and Sociobiology, 53, 238–245.

    Article  Google Scholar 

  • Singleton, I., & van Schaik, C. P. (2001). Orangutan home range size and its determinants in a Sumatran swamp forest. International Journal of Primatology, 22, 877–911.

    Article  Google Scholar 

  • Sokal, R. R., & Rohlf, F. J. (1981). Biometry: The principles and practice of statistics in biological research. San Francisco: W. H. Freeman.

    Google Scholar 

  • Steudel, K. (2000). The physiology and energetics of movement effects on individual and groups. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 9–23). Chicago: The University of Chicago Press.

    Google Scholar 

  • Stevens, J., Rosati, A., Ross, K., & Hauser, M. (2005). Will travel for food: spatial discounting in two new world monkeys. Current Biology, 15, 1855–1860.

    Article  CAS  PubMed  Google Scholar 

  • Struhsaker, T. T. (1997). Ecology of an African rainforest. Gainseville, FL: University Press of Florida.

    Google Scholar 

  • Struhsaker, T. T., & Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in Kibale Forest, Uganda. Behavioral Ecology and Sociobiology, 26, 435–443.

    Article  Google Scholar 

  • Struhsaker, T. T., & Leland, L. (1988). Group fission in redtail monkeys (Cercopithecus ascanius) in the Kibale forest, Uganda. In A. Gautier-Hion, F. Bourlière, J. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 364–388). New York: Cambridge University Press.

    Google Scholar 

  • Sugiyama, Y. (1960). On the division of a natural troop of Japanese monkeys at Takasakiyama. Primates, 2, 109–148.

    Article  Google Scholar 

  • Tolman, E. C. (1948). Cognitive maps in rats and men. The Psychological Review 55, 189–208.

    Google Scholar 

  • Tinbergen, N. (1972). The animal in its world. Cambridge: Harvard Press.

  • Wallis, S. J. (1979). The socioecology of Cercocebus albigena johnstonii (Lyddeker): An arboreal rainforest monkey. Ph.D. thesis, University of London.

  • Waser, P. M. (1974). Intergroup interactions in a forest monkey: The mangabey Cercocebus albigena. Ph.D. thesis, the Rockefeller University.

  • Waser, P. M. (1976). Cercocebus albigena: site attachment, avoidance, and intergroup spacing. American Naturalist, 11, 91–933.

    Google Scholar 

  • Waser, P. M. (1977). Individual recognition, intragroup cohesion, and intergroup spacing: evidence for sound playback to forest monkeys. Behaviour, 60, 28–74.

    Article  Google Scholar 

  • Waser, P. M. (1985). Spatial structure in mangabey groups. International Journal of Primatology, 6, 569–580.

    Article  Google Scholar 

  • Waser, P. M., & Floody, O. (1974). Ranging patterns of the mangabey Cercocebus albigena, in the Kibale Forest, Uganda. Zeitschrift fur Tierpsychologie, 35, 2–101.

    Google Scholar 

  • Waser, P. M., & Jones, W. T. (1983). Natal philopatry among solitary mammals. Quarterly Review of Biology, 58, 355–390.

    Article  Google Scholar 

  • Windberg, L. A. (1996). Coyote responses to visual and olfactory stimuli related to familiarity with an area. Canadian Journal of Zoology, 74, 2248–2253.

    Article  Google Scholar 

  • Zuberbühler K, Janmaat KRL (2010). Foraging cognition in non-human primates. In: Platt ML & Ghazanfar AA (Eds.), Primate Neuroethology (pp. 64–83). Oxford: Oxford University Press.

    Google Scholar 

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Acknowledgments

The Wenner-Gren and Leakey Foundation, the University of St. Andrews’ School of Psychology, the Schure-Bijerinck-Popping Foundation of the KNAW, the Stichting Kronendak, the Dobberke Stichting voor Vergelijkende Psychology, the Lucie Burger Stichting, and the Foundation Doctor Catharine van Tussenbroek provided funding to K. R. L. Janmaat. The Leakey Foundation and the University of California, Davis Department of Anthropology provided funding to R. L. Chancellor. We thank the Office of the President, the Uganda National Council for Science and Technology, the Uganda Wildlife Authority, the Makerere University Biological Field Station, and the Kibale Fish and Monkey Project, C. A. Chapman in particular, for logistic support, permission to conduct research in Kibale National Park, and the rainfall and temperature data needed to conduct our analyses. We thank W. Olupot and G. Arlet for sending us their ranging data and for training our assistants. We thank R. Meijer, L. B. Prevot, D. C. M. Wright, J. Rusoke, P. Irumba, R. Kaserengenyu, S. Katusabe, and R. Sabiiti for invaluable assistance in the field. We thank L. A. Isbell, K. Zuberbühler, C. H. Janson, G. Brown, 3 anonymous reviewers, and P. M. Waser in particular for comments and suggestions that significantly improved earlier drafts of the manuscript.

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  1. Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, 04103, Germany

    Karline R. L. Janmaat

  2. Department of Anthropology, University of California, Davis, CA, 95616, USA

    Rebecca L. Chancellor

  3. Gishwati Area Conservation Program, Great Ape Trust of Iowa, Des Moines, IA, USA

    Rebecca L. Chancellor

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  1. Karline R. L. Janmaat
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Correspondence to Karline R. L. Janmaat.

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Janmaat, K.R.L., Chancellor, R.L. Exploring New Areas: How Important is Long-Term Spatial Memory for Mangabey (Lophocebus albigena johnstonii) Foraging Efficiency?. Int J Primatol 31, 863–886 (2010). https://doi.org/10.1007/s10764-010-9433-3

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