Abstract
All free-living animals must make choices regarding which foods to eat, with the choices influencing their health and fitness. An important goal in nutritional ecology is therefore to understand what governs animals’ diet selection. Despite large variation in the availability of different food items, Peruvian spider monkeys (Ateles chamek) maintain a relatively stable daily protein intake, but allow total energy intake to vary as a function of the composition of available food items. This is referred to as protein-dominated macronutrient balancing. Here we assess the influence of this nutritional strategy on daily and seasonal nutritional intakes, estimate the nutritional value of different foods, and interpret unusual food choices. We conducted continuous all-day observations of focal spider monkeys inhabiting a semideciduous forest in Bolivia. We recorded feeding events, collected foods, and analyzed their nutrient content. By using the Geometric Framework for nutrition, we show that individuals reached their daily end-point in nutrient space —balance between protein and nonprotein energy intake— by consuming nutritionally balanced foods or by alternating between nutritionally complementary foods. The macronutritionally balanced figs of Ficus boliviana were their primary staple food and therefore dominated their overall nutritional intake. Our results also demonstrate that spider monkeys consumed a diverse array of ripe fruits to overcome periods of fig scarcity rather than vice versa; they could obtain sufficient protein on a diet of pure fruit; and unripe figs constituted a nutritionally rewarding and reliable food resource. We hope that the approaches taken and the conclusions reached in this study will catalyze further inquiries into the nutritional ecology of frugivorous primates.
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References
Altmann, S. A. (1998). Foraging for survival. Chicago: University of Chicago Press.
ANON. (1995). Standard practices for infrared multivariate quantitative analysis (designation E1655–00). West Conshohocken, PA.: American Society for Testing and Materials.
Beehner, J. C., Onderdonk, D. A., Alberts, S. C., & Altmann, J. (2006). The ecology of conception and pregnancy failure in wild baboons. Behavioral Ecology, 17(5), 741–750.
Campbell, C. J. (2008). Spider monkeys: Behavior, ecology and evolution of the genus Ateles. Cambridge, UK: Cambridge University Press.
Castellanos, H. G. (1995). Feeding behaviour of Ateles belzebuth E. Geoffroy 1806 (Cebidae: Atelinae) in Tawadu Forest Southern Venezuela. Ph.D dissertation, The University of Exeter, UK.
Chambers, P. G., Simpson, S. J., & Raubenheimer, D. (1995). Behavioural mechanisms of nutrient balancing in Locusta migratoria nymphs. Animal Behaviour, 50, 1513–1523.
Chapman, C. A., & Russo, S. E. (2007). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger & S. K. Bearder (Eds.), Primates in perspective (pp. 510–524). Oxford: Oxford University Press.
Cipollini, M. L., & Levey, D. J. (1997a). Secondary metabolites of fleshy vertebrate-dispersed fruits: Adaptive hypotheses and implications for seed dispersal. American Naturalist, 150(3), 346–372.
Cipollini, M. L., & Levey, D. J. (1997b). Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology, 78(3), 782–798.
Conklin, N. L., & Wrangham, R. W. (1994). The value of figs to a hind-gut fermenting frugivore—a nutritional analysis. Biochemical Systematics and Ecology, 22(2), 137–151.
De Gabriel, J. L., Wallis, I. R., Moore, B. D., & Foley, W. J. (2008). A simple, integrative assay to quantify nutritional quality for browsing herbivores. Oecologia, 156(1), 107–116.
Dearing, M. D., Foley, W. J., & McLean, S. (2005). The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annual Review of Ecology Evolution and Systematics, 36, 169–189.
Dew, J. L. (2005). Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. International Journal of Primatology, 26(5), 1107–1135.
Di Fiore, A., & Rodman, P. S. (2001). Time allocation patterns of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terra firma forest. International Journal of Primatology, 22(3), 449–480.
Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 81–137). Cambridge, UK: Cambridge University Press.
Dufour, D. L. (1987). Insects as food—a case study from the Northwest Amazon. American Anthropologist, 89(2), 383–397.
Duhan, A., Chauhan, B. M., & Punia, D. (1992). Nutritional value of some nonconventional plant foods of India. Plant Foods for Human Nutrition, 42(3), 193–200.
Dunbar, R. I. M. (1988). Primate social systems. London and Sydney: Croom Helm Ltd.
Felton, A. M., Felton, A., Wood, J. T., & Lindenmayer, D. B. (2008). Diet and feeding ecology of the Peruvian spider monkey (Ateles chamek) in a Bolivian semi-humid forest: the importance of Ficus as a staple food resource. International Journal of Primatology, 29, 379–403.
Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23(1), 70–78.
Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., et al. (2009). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology,. doi:10.1093/beheco/arp021.
Foley, W. J., McIlwee, A., Lawler, I., Aragones, L., Woolnough, A. P., & Berding, N. (1998). Ecological applications of near infrared reflectance spectroscopy a tool for rapid, cost-effective prediction of the composition of plant and animal tissues and aspects of animal performance. Oecologia, 116(3), 293–305.
Freeland, W. J., & Janzen, D. H. (1974). Strategies in herbivory by mammals - role of plant secondary compounds. American Naturalist, 108(961), 269–289.
Herbst, L. H. (1986). The role of nitrogen from fruit pulp in the nutrition of the frugivorous bat Carollia perspicillata. Biotropica, 18(1), 39–44.
Jordano, P. (1983). Fig-seed predation and dispersal by birds. Biotropica, 15(1), 38–41.
Kinnaird, M. F., & O’Brien, T. G. (2005). Fast foods of the forest: The influence of figs on primates and hornbills across Wallace’s line. In J. L. Dew & J. P. Bouble (Eds.), Tropical fruits and frugivores: The search for strong predictors (pp. 155–184).
Kinzey, W. G. (1997). Ateles. In W. G. Kinzey (Ed.), New World primates: Ecology, evolution, and behavior (pp. 192–199). New York: Aldine de Gruyter.
Lambert, J. E. (2007). Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger & S. K. Bearder (Eds.), Primates in perspective (pp. 482–495). Oxford: Oxford University Press.
Mattson, W. J. (1980). Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics, 11, 119–161.
Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species. American Naturalist, 117(4), 496–505.
Milton, K. (1982). Dietary quality and demographic regulation in a howler monkey population. In E. G. Leigh, A. S. Rand & D. M. Windsor (Eds.), The ecology of a tropical forest: Seasonal rhythms and long-term changes (pp. 273–289). Washington, DC: Smithsonian Institution Press.
Milton, K. (1993). Diet and primate evolution (pp.86–93). Scientific American, Aug.
Milton, K. (1998). Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the Colobinae. International Journal of Primatology, 19(3), 513–548.
Milton, K. (1999). A hypothesis to explain the role of meat-eating in human evolution. Evolutionary Anthropology, 8(1), 11–21.
Milton, K., & Dintzis, F. R. (1981). Nitrogen-to-protein conversion factors for tropical plant-samples. Biotropica, 13(3), 177–181.
Milton, K., Windsor, D. M., Morrison, D. W., & Estribi, M. A. (1982). Fruiting phenologies of two Neotropical Ficus species. Ecology, 63(3), 752–762.
Norconk, M. A., Grafton, B. W., & Conklin-Brittain, N. L. (1998). Seed dispersal by Neotropical seed predators. American Journal of Primatology, 45(1), 103–126.
Oates, J. F. (1987). Food distribution and foraging behavior. In B. B. Smuts, D. L. Cheyney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker (Eds.), Primate Societies (pp. 197–209). Chicago: University of Chicago Press.
O’Brien, T. G., Kinnaird, M., & Dierenfeld, E. S. (1998). What’s so special about figs? Nature, 392, 668.
Oftedal, O. T. (1991). The nutritional consequences of foraging in primates—the relationship of nutrient intakes to nutrient-requirements. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 334(1270), 161–170.
Peres, C. A. (1994). Diet and feeding ecology of gray woolly monkeys (Lagothrix lagotricha cana) in Central Amazonia—comparisons with other atelines. International Journal of Primatology, 15(3), 333–372.
Raubenheimer, D., & Simpson, S. J. (1997). Integrative models of nutrient balancing: Application to insects and vertebrates. Nutrition Research Reviews, 10, 151–179.
Raubenheimer, D., & Simpson, S. J. (2004). Organismal stoichiometry: quantifying non-independence among food components. Ecology, 85(5), 1203–1216.
Raubenheimer, D., & Simpson, S. J. (2006). The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis, 53, 100–111.
Robbins, C. T. (1993). WIldlife feeding and nutrition (2nd edition ed.): Academic Press.
Robbins, C. T., Fortin, J. K., Rode, K. D., Farley, S. D., Shipley, L. A., & Felicetti, L. A. (2007). Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos, 116(10), 1675–1682.
Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the ateline primates. Journal of Human Evolution, 18(7), 717–750.
Ruby, J., Nathan, P. T., Balasingh, J., & Kunz, T. H. (2000). Chemical composition of fruits and leaves eaten by short-nosed fruit bat, Cynopterus sphinx. Journal of Chemical Ecology, 26(12), 2825–2841.
Ruohonen, K., Simpson, S. J., & Raubenheimer, D. (2007). A new approach to diet optimisation: A re-analysis using European whitefish (Coregonus lavaretus). Aquaculture, 267(1–4), 147–156.
Schaefer, H. M., & Schaefer, V. (2006). The fruits of selectivity: How birds forage on Goupia glabra fruits of different ripeness. Journal of Ornithology, 147(4), 638–643.
Schaefer, H. M., Schmidt, V., & Winkler, H. (2003). Testing the defense trade-off hypothesis: How contents of nutrients and secondary compounds affect fruit removal. Oikos, 102(2), 318–328.
Schoener, T. W. (1971). Theory of feeding strategies. Annual Review of Ecology and Systematics, 2, 369–404.
Shanahan, M., So, S., Compton, S. G., & Corlett, R. (2001). Fig-eating by vertebrate frugivores: A global review. Biological Reviews, 76(4), 529–572.
Silver, S. C., Ostro, L. E. T., Yeager, C. P., & Dierenfeld, E. S. (2000). Phytochemical and mineral components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize. Zoo Biology, 19(2), 95–109.
Simpson, S. J., & Raubenheimer, D. (1993). A multilevel analysis of feeding behavior - the geometry of nutritional decisions. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 342(1302), 381–402.
Simpson, S. J., & Raubenheimer, D. (1995). The geometric analysis of feeding and nutrition—a user’s guide. Journal of Insect Physiology, 41(7), 545–553.
Simpson, S. J., & Raubenheimer, D. (2001). The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology, 82(2), 422–439.
Simpson, S. J., & Raubenheimer, D. (2005). Obesity: the protein leverage hypothesis. Obesity Reviews, 6(2), 133–142.
Stevenson, P. (2005). Potential keystone plant species for the frugivore community at Tinigua Park, Colombia. In J. L. Dew & J. P. Bouble (Eds.), Tropical fruits and frugivores: The Search for Strong Predictors (pp. 37–57): Springer.
Strier, K. B. (1992). Atelinae adaptations—behavioral strategies and ecological constraints. American Journal of Physical Anthropology, 88(4), 515–524.
Strier, K. B. (2007). Primate behavioral ecology (3rd ed.). Columbus, OH: Allyn & Bacon.
Venu, D. K., Munjal, S. V., Waskar, D. P., Patil, S. R., & Kale, A. A. (2005). Biochemical changes during growth and development of fig (Ficus carica L.) fruits. Journal of Food Science and Technology-Mysore, 42(3), 279–282.
Wallace, R. B. (2005). Seasonal variations in diet and foraging behavior of Ateles chamek in a southern Amazonian tropical forest. International Journal of Primatology, 26(5), 1053–1075.
Wendeln, M. C., Runkle, J. R., & Kalko, E. K. V. (2000). Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica, 32(3), 489–501.
White, T. C. R. (1993). The inadequate environment: Nitrogen and the abundance of animals. Berlin/Heidelberg/New York: Springer.
Acknowledgments
This project was supported through the generous financial assistance of the Wildlife Conservation Society, Conservation International, the Rufford Foundation, and the Primate Society of Great Britain. We thank the personnel of Instituto Boliviano de Investigación Forestal (IBIF), Agroindustría Forestal La Chonta Ltda, and el Proyecto de Manejo Forestal Sostenible (BOLFOR) for providing logistical support and expert advice, especially Marielos Peña-Claros, Todd Fredericksen, and Joaquin Justiniano. José and Genaro Chuviña provided integral assistance during all phases of the field work. We also thank Renna Short, Helga Peters, Petter König, and all other volunteers and field workers. We thank Nancy Conklin-Brittain, Francis Marsh, and Rositta Shun Ting Au for guidance and assistance in laboratory work. Advice from Robert Wallace, Ross Cunningham, and Colin Groves contributed to the design of this project and Clive Hilliker helped with graphics. We also thank Stephen Simpson for providing mentorship on the use of the Geometric Framework, and 2 anonymous reviewers for improving on an earlier version of this paper.
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Felton, A.M., Felton, A., Wood, J.T. et al. Nutritional Ecology of Ateles chamek in lowland Bolivia: How Macronutrient Balancing Influences Food Choices. Int J Primatol 30, 675–696 (2009). https://doi.org/10.1007/s10764-009-9367-9
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DOI: https://doi.org/10.1007/s10764-009-9367-9