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Methods in Primate Nutritional Ecology: A User’s Guide

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Abstract

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.

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References

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.

    Article  PubMed  CAS  Google Scholar 

  • Altmann, S. A. (1998). Foraging for survival: Yearling baboons in Africa. Chicago: University of Chicago Press.

    Google Scholar 

  • Altmann, J., & Alberts, S. C. (2005). Growth rates in a wild primate population: Ecological influences and maternal effects. Behavioral Ecology and Sociobiology, 57, 490–501.

    Article  Google Scholar 

  • AOAC (1990). Official methods of analysis, 15th ed.Association of Analytical Chemists.

  • Banta, C. A., Warner, R. G., & Robertson, J. B. (1975). Protein nutrition of the golden hamster. Journal of Nutrition, 105, 38–45.

    CAS  Google Scholar 

  • Barboza, P. S., Parker, K. L., & Hume, I. D. (2009). Integrative wildlife nutrition. Berlin: Springer-Verlag.

    Book  Google Scholar 

  • Barton, R. A., & Whiten, A. (1994). Reducing complex diets to simple rules: Food selection by olive baboons. Behavioral Ecology and Sociobiology, 35, 283–293.

    Article  Google Scholar 

  • Cameron, J. L. (1996). Regulation of reproductive hormone secretion in primates. Reproduction, 1, 117–126.

    Article  CAS  Google Scholar 

  • Campbell, J. L. (2000). Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variecia, Hapalemur grisus, and Lemur catta. American Journal of Primatology, 52, 133–142.

    Article  PubMed  CAS  Google Scholar 

  • Campbell, J. L., Williams, C. V., & Eismann, J. H. (2002). Fecal inoculum can be used to determine the rate and extent of in vitro fermentation of dietary fiber sources across three lemur species that differ in dietary profile: Varecia variegata, Eulemur fulvus, and Hapalemur griseus. Journal of Nutrition, 132, 3073–3080.

    PubMed  CAS  Google Scholar 

  • Camperio Ciani, A., Martinoli, L., Capiluppi, C., Arahou, M., & Mouna, M. (2001). Effects of water availability and habitat quality on bark-stripping behavior in Barbary macaques. Conservation Biology, 15, 259–265.

    Google Scholar 

  • Caton, J. M. (1999). A preliminary report on the digestive strategy of the western lowland gorilla. Australian Journal of Ecology, 13, 2–7.

    Google Scholar 

  • Caton, J. M., Lawes, M., & Cunningham, C. (2000). Digestive strategy of the south-east African lesser bushbaby, Galago moholi. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 127, 39–48.

    Article  CAS  Google Scholar 

  • Chamberlain, J., Nelson, G., & Milton, K. (1993). Fatty-acid profiles of major food sources of howler monkeys (Alouatta palliata) in the Neotropics. Experientia, 49(9), 820–824.

    Article  PubMed  CAS  Google Scholar 

  • Chancellor, R. L., & Isbell, L. A. (2009). Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology and Sociobiology, 63, 1447–1458.

    Article  PubMed  Google Scholar 

  • Chapman, C. A. (1995). Primate seed dispersal: Coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.

    Article  Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (2002). Foraging challenges of red colobus monkeys: Influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology. Part A, Physiology, 133, 861–875.

    Article  Google Scholar 

  • Chapman, C. A., & Rothman, J. M. (2009). Within-species differences in primate social structure: Evolution of plasticity and phylogenetic constraints. Primates, 50, 12–22.

    Article  PubMed  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002). Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Rode, K. D., Hauck, E. M., & McDowell, L. R. (2003). Variation in the nutritional value of primate foods: Among trees, time periods, and areas. International Journal of Primatology, 24, 317–333.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Naughton-Treves, L., Lawes, M. J., & McDowell, L. R. (2004). Predicting folivorous primate abundance: Validation of a nutritional model. American Journal of Primatology, 62, 55–69.

    Article  PubMed  Google Scholar 

  • Chivers, D. J. (1998). Measuring food intake in wild animals: Primates. Proceedings of the Nutrition Society, 57, 321–332.

    Article  PubMed  CAS  Google Scholar 

  • 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, 137–151.

    Article  Google Scholar 

  • Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. International Journal of Primatology, 19, 971–998.

    Article  Google Scholar 

  • Conklin-Brittain, N. L., Dierenfeld, E. S., Wrangham, R. W., Norconk, M., & Silver, S. C. (1999). Chemical protein analysis: A comparison of Kjeldahl crude protein and total ninhydrin protein from wild, tropical vegetation. Journal of Chemical Ecology, 25, 2601–2622.

    Article  CAS  Google Scholar 

  • Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2006). Energy intake by wild chimpanzees and orangutans: Methodological considerations and a preliminary comparison. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates. Ecological, physical and behavioral aspects (pp. 445–571). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Cork, S. J., & Krockenberger, A. K. (1991). Methods and pitfalls of extracting condensed tannins and other phenolics from plants: Insights from investigations on Eucalyptus leaves. Journal of Chemical Ecology, 17, 123–134.

    Article  CAS  Google Scholar 

  • Curtis, D. J. (2004). Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. American Journal of Physical Anthropology, 124, 234–247.

    Article  PubMed  Google Scholar 

  • Dammhahn, M., & Kappeler, P. M. (2008). Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29, 1567–1589.

    Article  Google Scholar 

  • Deblauwe, I., & Janssens, G. P. J. (2008). New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: The role of nutritional value. American Journal of Physical Anthropology, 135, 42–55.

    Article  PubMed  Google Scholar 

  • DeGabriel, J. L., Wallis, I. R., Moore, B. D., & Foley, W. J. (2008). A simple, integrative assay to quanity nutritional quality of browses for herbivores. Oecologia, 156, 107–116.

    Article  PubMed  Google Scholar 

  • Deinum, B., & Maassen, A. (1994). Effects of drying temperature on chemical composition and in vitro digestibility of forages. Animal Feed Science and Technology, 46, 75–86.

    Article  Google Scholar 

  • Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.

    Article  CAS  Google Scholar 

  • Edwards, M. S., & Ullrey, D. E. (1999a). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. I. Ruffed lemurs (Varecia variegata vauiegata and V-v. rubra). Zoo Biology, 18, 529–536.

    Article  Google Scholar 

  • Edwards, M. S., & Ullrey, D. E. (1999b). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut and foregut fermenting folivores. Zoo Biology, 18, 537–549.

    Article  Google Scholar 

  • Eitenmiller, R. R., Landen, W. O., & Ye, L. (2007). Vitamin analysis for the health and food sciences (2nd ed.). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Fahey, G. C., & Jung, H. G. (1983). Lignin as a marker in digestion studies: A review. Journal of Animal Science, 57, 220–225.

    CAS  Google Scholar 

  • Fashing, P. J., Dierenfeld, E., & Mowry, C. B. (2007). Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. International Journal of Primatology, 28, 673–703.

    Article  Google Scholar 

  • Fedigan, L. M. (2010). Ethical issues faced by field primatologists: Asking the relevant questions. American Journal of Primatology, 71, 1–18.

    Google Scholar 

  • Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009a). Nutritional goals of wild primates. Functional Ecology, 23, 70–78.

    Article  Google Scholar 

  • Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., et al. (2009b). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioural Ecology, 20, 685–690.

    Article  Google Scholar 

  • Felton, A. M., Felton, A., Foley, W. J., & Lindenmayer, D. B. (2010). The role of timber tree species in the nutritional ecology of spider monkeys in a certified logging concession, Bolivia. Forest Ecology and Management, 259, 1642–1649.

    Article  Google Scholar 

  • Foley, W. J., & Moore, B. D. (2005). Plant secondary metabolites and vertebrate herbivores—from physiological regulation to ecosystem function. Current Opinion in Plant Biology, 8, 430–435.

    Article  PubMed  CAS  Google Scholar 

  • 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, 293–305.

    Article  Google Scholar 

  • Food and Nutrition Board of the Institute of Medicine of the National Academy. (2005). Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. Washington, DC: National Academies Press.

    Google Scholar 

  • Frey, J. C., Rothman, J. M., Pell, A. N., Nizeyi, J. B., Cranfield, M. R., & Angert, E. A. (2006). Fecal bacterial diversity in a wild gorilla (Gorilla beringei). Applied and Environmental Microbiology, 72, 3789–3792.

    Article  CAS  Google Scholar 

  • Ganas, J., Ortmann, S., & Robbins, M. M. (2008). Food preferences of wild mountain gorillas. American Journal of Primatology, 70, 927–938.

    Article  PubMed  Google Scholar 

  • Ganzhorn, J. U. (1988). Food partitioning among Malagasy primates. Oecologia, 75, 436–450.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1995). Low level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084–2096.

    Article  Google Scholar 

  • Ganzhorn, J. U., Arrigo-Nelson, S., Boinski, S., Bollen, A., Carrai, V., Derby, A., et al. (2009). Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PloS One, 4, e8253.

    Article  PubMed  CAS  Google Scholar 

  • Glander, K. E. (1982). The impact of plant secondary compounds on primate feeding behavior. Yearbook of Physical Anthropology, 25, 1–18.

    Article  Google Scholar 

  • Goering, H. K., & Van Soest, P. J. (1970). Forage fiber analysis: United States Department of Agriculture.

  • Goodall, J. (1986). The chimpanzees of Gombe. Boston: Houghton Mifflin.

    Google Scholar 

  • Gould, L., Power, M. L., Ellwanger, N., & Rambeloarivony, H. (in press). Feeding behavior and nutrient intake in spiny forest-dwelling ring-tailed lemurs (Lemur catta) during early gestation and early to mid-lactation periods: Compensating in a harsh environment. American Journal of Physical Anthropology.

  • Hall, M. B., & Keuler, N. S. (2009). Factors affecting accuracy and time requirements of a glucose oxidase-peroxidates assay for determination of glucose. Journal of AOAC International, 92, 50–60.

    PubMed  CAS  Google Scholar 

  • Hall, M. B., & Mertens, D. R. (2008). Effect of sample processing procedures on measurement of starch in corn silage and corn grain. Journal of Dairy Science, 91, 4830–4833.

    Article  PubMed  CAS  Google Scholar 

  • Hall, M. B., Hoover, W. H., Jennings, J. P., & Webster, T. K. M. (1999). A method for partitioning neutral detergent-soluble carbohydrates. Journal of the Science of Food and Agriculture, 79, 2079–2086.

    Article  CAS  Google Scholar 

  • Harris, T. R., & Chapman, C. A. (2007). Variation in the diet and ranging behavior of black-and-white colobus monkeys: Implications for theory and conservation. Primates, 28, 208–221.

    Article  Google Scholar 

  • Harrison, M. E., Vogel, E. R., Morrogh-Bernard, H. C., & van Noordwijk, M. A. (2009). Methods for calculating activity budgets compared: A case study using orangutans. American Journal of Primatology, 71, 353–358.

    Article  PubMed  Google Scholar 

  • Hohmann, G., Fowler, A., Sommer, V., & Ortmann, S. (2006). Frugivory and gregariousness of Salonga bonobos and Gashaka chimpanzees: The influence of abundance and nutritional quality of fruit. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioural aspects (pp. 123–159). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Houle, A., Chapman, C. A., & Vickery, W. L. (2004). Tree climbing strategies for primate ecological studies. International Journal of Primatology, 25, 237–260.

    Article  Google Scholar 

  • Houle, A., Chapman, C. A., & Vickery, W. L. (2007). Intratree variation in fruit production and implication for primate foraging. International Journal of Primatology, 28, 1197–1271.

    Article  Google Scholar 

  • Isbell, L. A. (1991). Contest and scramble competition: Patterns of female aggression and ranging behaviour among primates. Behavioral Ecology, 2, 143–155.

    Article  Google Scholar 

  • Isbell, L. A. (1998). Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). American Journal of Primatology, 45, 381–398.

    Article  PubMed  CAS  Google Scholar 

  • Janson, C. H. (1988). Intra-specific food competition and primate social structure: A synthesis. Behaviour, 105, 1–17.

    Article  Google Scholar 

  • Janson, C. H. (2007). What wild primates know about resources: Opening up the black box. Animal Cognition, 10, 357–367.

    Article  PubMed  Google Scholar 

  • Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure. In J. G. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 237–267). Cambridge, UK: Cambridge University Press.

    Chapter  Google Scholar 

  • Janson, C. H., & van Schaik, C. P. (1988). Recognizing the many faces of primate food competition: Methods. Behaviour, 105, 165–186.

    Article  Google Scholar 

  • Janson, C. H., & Vogel, E. R. (2006). Estimating the effects of hunger on primate social ecology. In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 285–312). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Julkunen-Tiitto, R., & Sorsa, S. (2002). Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. Journal of Chemical Ecology, 27, 779–789.

    Article  Google Scholar 

  • Karasov, W. H. (1986). Energetics, physiology and vertebrate ecology. Trends in Ecology & Evolution, 1, 101–104.

    Article  CAS  Google Scholar 

  • Kay, R. F., & Davies, A. G. (1994). Digestive physiology. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys (pp. 229–250). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Kisidayova, S., Varadyova, Z., Pristas, P., Piknova, M., Nigutova, K., Petrzelkova, K. J., Profousova, I., Schovancova, K., Kamler, J., & Modry, D. (2009). Effects of high- and low-fiber diets on fecal fermentation and fecal microbial populations of captive chimpanzees. American Journal of Primatology, 71, 548–557.

    Article  PubMed  CAS  Google Scholar 

  • Knott, C. D. (1998). Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. International Journal of Primatology, 19, 1061–1079.

    Article  Google Scholar 

  • Koenig, A. (2000). Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behavioral Ecology and Sociobiology, 48, 93–109.

    Article  Google Scholar 

  • Lambert, J. E. (1998). Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology, 7, 8–20.

    Article  Google Scholar 

  • Lambert, J. E. (in press). In vitro fermentation of dietary carbohydrates consumed by African apes and monkeys: Preliminary results for interpreting microbial and digestive strategy. International Journal of Primatology. in press

  • Lee, S. C., Prosky, L., & DeVries, J. W. (1992). Determination of total, soluble, and insoluble fiber in foods- enzymatic- gravimetric method, MES-TRIS buffer: Collaborative study. Journal of AOAC International, 75, 395–416.

    CAS  Google Scholar 

  • Leighton, M. (1993). Modeling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection. International Journal of Primatology, 14, 257–313.

    Article  Google Scholar 

  • Levey, D. J. (2000). Conversion of nitrogen to protein and amino acids in wild fruits. Journal of Chemical Ecology, 26, 1749–1763.

    Article  CAS  Google Scholar 

  • Licitra, G., Hernandez, T. M., & VanSoest, P. J. (1996). Standardization of procedures for nitrogen fractionation of ruminant feeds. Animal Feed Science and Technology, 57, 347–358.

    Article  Google Scholar 

  • Link, A., Galvis, N., Fleming, E., & Di Fiore, A. (2011). Patterns of mineral lick visitation by spider monkeys and holwer monkeys in Amazonia: Are licks perceived as risky areas? American Journal of Primatology, 73, 286–396.

    Article  Google Scholar 

  • Lucas, P., Osorio, D., Yamashita, N., Prinz, J. F., Dominy, N. J., & Darvell, B. J. (2011). Dietary analysis II: Food chemistry. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology (2nd ed., pp. 255–270). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Malenky, R. K., & Wrangham, R. W. (1994). A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. American Journal of Primatology, 32, 1–12.

    Article  Google Scholar 

  • Marks, D. L., Swain, T., Goldstein, S., Richards, A. F., & Leighton, M. (1988). Chemical correlates of rhesus monkey food choice: The influence of hydrolyzable tannins. Journal of Chemical Ecology, 14, 213–235.

    Article  CAS  Google Scholar 

  • Martin, P., & Bateson, P. (1986). Measuring behaviour (2nd ed.). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Martinek, R. G. (1964). Stabilized tungstic acid reagent for blood deproteinization and glucose stabilization. Chemist-Analyst, 53, 108–109.

    CAS  Google Scholar 

  • Mau, M., Sudekum, K. H., Johann, A., Sliwa, A., & Kaiser, T. M. (2009). Saliva of the graminivorous Theropithecus gelada lacks proline-rich proteins and tannin-binding capacity. American Journal of Primatology, 71, 663–669.

    Article  PubMed  CAS  Google Scholar 

  • Mau, M., Martinho de Almeida, A., Coelho, A. V., & Sudekum, K. (2011). First identification of tannin-binding proteins in saliva of Papio hamadryas using MS/ MS mass spectroscopy. American Journal of Primatology, 73, 1–7.

    Google Scholar 

  • McCabe, G. M., & Fedigan, L. M. (2007). Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. International Journal of Primatology, 28, 837–851.

    Article  Google Scholar 

  • Mertens, D. R. (1992). Critical conditions in determining detergent fibers. Paper presented at the Proceedings of the NFTA Forage Analysis Workshop, September 16–17, Denver, CO.

  • Milton, K. (1979). Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. American Naturalist, 114, 362–378.

    Article  CAS  Google Scholar 

  • Milton, K. (1980). The foraging strategies of howler monkeys: A study in primate economics. New York: Columbia University Press.

    Google Scholar 

  • Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species. American Naturalist, 117, 496–505.

    Article  Google Scholar 

  • Milton, K. (1991). Pectic substances in neotropical plant parts. Biotropica, 23, 90–92.

    Article  Google Scholar 

  • Milton, K. (1993). Diet and primate evolution. Scientific American, 269, 86–93.

    Article  PubMed  CAS  Google Scholar 

  • Milton, K. (1998). Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the Colobinae. International Journal of Primatology, 19, 513–548.

    Article  Google Scholar 

  • Milton, K. (2006). Analyzing primate nutritional ecology. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioural aspects (pp. 381–396). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Milton, K. (2008). Macronutrient patterns of 19 species of Panamanian fruits from Barro Colorado Island. Neotropical Primates, 15, 1–7.

    Article  Google Scholar 

  • Milton, K., & Demment, M. W. (1988). Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with humans. Journal of Nutrition, 118, 1082–1088.

    PubMed  CAS  Google Scholar 

  • Milton, K., & Dintzis, F. (1981). Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica, 12, 177–181.

    Article  Google Scholar 

  • Milton, K., & Jenness, R. (1987). Ascorbic acid content of neotropical plant parts available to wild monkeys and bats. Experentia, 43, 339–342.

    Article  CAS  Google Scholar 

  • Milton, K., & McBee, R. H. (1983). Rates of fermentative digestion in the howler monkey, Alouatta palliata (Primates, Ceboidea). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 74, 29–31.

    CAS  Google Scholar 

  • Milton, K., Van Soest, P. J., & Robertson, J. B. (1980). Digestive efficiences of wild howler monkeys. Physiological Zoology, 53, 402–409.

    Google Scholar 

  • Mole, S., Butler, L. G., & Ianson, G. (1990). Defense against dietary tannin in herbivores: A survey for proline rich salivary proteins in mammals. Biochemistry, Systematics and Ecology, 18, 287–293.

    Article  CAS  Google Scholar 

  • Mould, F. L., Kliem, K. E., Morgan, R., & Mauricio, R. M. (2005). In vitro microbial inoculum: A review of its function and properties. Animal Feed Science and Technology, 123–124, 31–50.

    Article  Google Scholar 

  • Mowry, C. B., Decker, B. S., & Shure, D. J. (1996). The role of phytochemistry in dietary choices of Tana River red colobus monkeys (Procolobus badius rufomitratus). International Journal of Primatology, 17, 63–84.

    Article  Google Scholar 

  • Mueller-Harvey, I. (2001). Analysis of hydrolysable tannins. Animal Feed Science and Technology, 91, 3–20.

    Article  CAS  Google Scholar 

  • Muetzel, S., & Becker, K. (2006). Extractibility and biological activity of tannins from various tree leaves determined by chemical and biological assays as affected by drying procedure. Animal Feed Science and Technology, 125, 139–149.

    Article  CAS  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 baboon populations. Oecologia, 87, 467–472.

    Article  Google Scholar 

  • Nagy, K. A., & Milton, K. (1979). Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology, 60, 475–480.

    Article  Google Scholar 

  • National Research Council. (1998). Nutrient requirements of swine. Washington, DC: National Academies Press.

    Google Scholar 

  • National Research Council. (2003). Nutrient requirements of nonhuman primates (2nd ed.). Washington, DC: National Academies Press.

    Google Scholar 

  • National Research Council. (2007). Nutrient requirements of small ruminants: Sheep, goats, cervids, and New World camelids. Washington, DC: National Academies Press.

    Google Scholar 

  • Norconk, M. A., & Conklin, N. L. (2004). Variation on frugivory: The diet of Venezuelan white-faced sakis. International Journal of Primatology, 25, 1–26.

    Article  Google Scholar 

  • Norconk, M. A., Wright, B. W., Conklin-Brittain, N. L., & Vinyard, C. J. (2009). Mechanical and nutritional properties of foods as factors in platyrrhine dietary adaptations. In P. A. Garber, A. Estrada, C. Bicca-Marques, E. Heymann, & K. Strier (Eds.), South American primates: Testing new theories in the study of primate behavior, ecology and conservation (pp. 279–319). New York: Springer.

    Google Scholar 

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

    Article  Google Scholar 

  • Oftedal, O. T. (1992). The nutritional consequences of foraging in primates: The relationship of nutrient intakes to nutrient requirements. Philosophical Transactions of the Royal Society B: Biological Sciences, 334, 161–170.

    Article  Google Scholar 

  • Ortmann, S., Bradley, B. J., Stolter, C., & Ganzhorn, J. U. (2006). Estimating the quality and composition of wild animal diets: A critical survey of methods. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioral aspects (pp. 397–420). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Ozanne, C. M. P., Bell, J. R., & Weaver, D. G. (2011). Collecting arthropods and arthropod remains for primate studies. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology (2nd ed., pp. 271–285). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Palmer, B., Jones, R. J., Wina, E., & Tangendjaja, B. (2000). The effect of sample drying conditions on estimates of condensed tannin and fibre content, dry matter digestibility, nitrogen digestibility and PEG binding of Calliandra calothyrsus. Animal Feed Science and Technology, 87, 29–40.

    Article  Google Scholar 

  • Palmquist, D. L., & Jenkins, T. C. (2003). Challenges with fats and fatty acid methods. Journal of Animal Science, 81, 3250–3254.

    PubMed  CAS  Google Scholar 

  • Perry, J. M. G., & Harstone-Rose, A. (2010). Maximum ingested food size in captive strepsirrhine primates: Scaling and the effects of diet. American Journal of Physical Anthropology, 142, 625–635.

    Article  PubMed  Google Scholar 

  • Powzyk, J. A., & Mowry, C. B. (2003). Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. International Journal of Primatology, 24(6), 1143–1162.

    Article  Google Scholar 

  • Raubenheimer, D. (2011). Towards a quantitative nutritional ecology: The right-angled mixture triangle. Ecological Monographs, 81, 407–427.

    Article  Google Scholar 

  • Rautio, P., Bergvall, U. A., Karonen, M., & Salminen, J. P. (2007). Bitter problems in ecological feeding experiments: Commercial tannin preparations and common methods for tannin quantifications. Biochemical Systematics and Ecology, 35, 257–262.

    Article  CAS  Google Scholar 

  • Reiner, W. B., & Rothman, J. M. (2011). Fatty acids in gorilla diets: Implications for primate nutrition and human health. American Journal of Physical Anthropology, 52, 99.

    Google Scholar 

  • Remis, M. J., Dierenfeld, E. S., Mowry, C. B., & Carroll, R. W. (2001). Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. International Journal of Primatology, 22, 807–836.

    Article  Google Scholar 

  • Reynolds, V., Plumptre, A. J., Greenham, J., & Harborne, J. (1998). Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia, 115, 331–336.

    Article  Google Scholar 

  • Riba-Hernandez, P., Stoner, K. E., & Lucas, P. W. (2005). Sugar concentration of fruits and their detection via color in the central American spider monkey (Ateles geoffroyi). American Journal of Primatology, 67, 411–423.

    Article  PubMed  Google Scholar 

  • Robbins, C. T. (1993). Wildlife feeding and nutrition. San Diego, CA: Academic Press.

    Google Scholar 

  • Robbins, C. T., Hanley, T. A., Hagerman, A. E., Hjeljord, O., Baker, D. L., Schwartz, C. C., et al. (1987a). Role of tannins in defending plants against ruminants: Reduction in protein availability. Ecology, 68, 98–107.

    Article  CAS  Google Scholar 

  • Robbins, C. T., Mole, S., Hagerman, A. E., & Hanley, T. A. (1987b). Role of tannins in defending plants against ruminants: Reduction in dry matter digestion. Ecology, 68, 1606–1615.

    Article  CAS  Google Scholar 

  • Rode, K. D., Chapman, C. A., Chapman, L. J., & McDowell, L. R. (2003). Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. International Journal of Primatology, 24, 541–573.

    Article  Google Scholar 

  • Rode, K. D., Chapman, C. A., McDowell, L. R., & Stickler, C. (2006). Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica, 38, 625–634.

    Article  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Molina, D. O., Shaw, A. V., Hintz, H. F., & Pell, A. N. (2006a). Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. American Journal of Primatology, 68, 675–691.

    Article  CAS  Google Scholar 

  • Rothman, J. M., Van Soest, P. J., & Pell, A. N. (2006b). Decaying wood is a sodium source for mountain gorillas. Biology Letters, 2, 321–324.

    Article  CAS  Google Scholar 

  • Rothman, J. M., Plumptre, A. J., Dierenfeld, E. S., & Pell, A. N. (2007). Nutritional composition of the diet of the gorilla (Gorilla beringei): A comparison between two mountain habitats. Journal of Tropical Ecology, 23, 673–682.

    Article  Google Scholar 

  • Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008a). Fiber-bound protein in gorilla diets: Implications for estimating the intake of dietary protein by primates. American Journal of Primatology, 70, 690–694.

    Article  CAS  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Hintz, H. F., & Pell, A. N. (2008b). Nutritional quality of gorilla diets: Consequences of age, sex and season. Oecologia, 155, 111–122.

    Article  Google Scholar 

  • Rothman, J. M., Chapman, C. A., Hansen, J. L., Cherney, D. J., & Pell, A. N. (2009a). Rapid assessment of the nutritional value of foods eaten by mountain gorillas: Applying near-infrared reflectance spectroscopy to primatology. International Journal of Primatology, 30, 729–742.

    Article  Google Scholar 

  • Rothman, J. M., Dusinberre, K., & Pell, A. N. (2009b). Condensed tannins in the diets of primates: A matter of methods. American Journal of Primatology, 71, 70–76.

    Article  Google Scholar 

  • Rothman, J. M., Raubenheimer, D., & Chapman, C. A. (2011). Nutritional geometry: Gorillas prioritize non-protein energy while consuming surplus protein. Biology Letters, 7, 847–849.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, D. A., Kerley, M. S., Dempsey, J. L., Porton, I. J., Porter, J. H., Griffen, M. E., Ellersieck, M. R., & Sadler, W. C. (2005). Fiber digestibility by the orangutan (Pongo abelii) in vitro and in vivo. Journal of Zoo and Wildlife Medicine, 36, 571–580.

    Article  PubMed  Google Scholar 

  • Shipley, L. A., Gross, J. E., Spalinger, D. E., Hobbs, N. T., & Wunder, B. A. (1994). The scaling intake rate in mammalian herbivores. American Naturalist, 143, 1055–1082.

    Article  Google Scholar 

  • Simmen, B., & Sabatier, D. (1996). Diets of some French Guianan primates: Food composition and food choices. International Journal of Primatology, 17, 661–693.

    Article  Google Scholar 

  • Simpson, S. J., & Raubenheimer, D. (1999). Assuaging nutritional complexity: A geometrical approach. Proceedings of the Nutrition Society, 58, 779–789.

    Article  PubMed  CAS  Google Scholar 

  • Smith, A. C. (2000). Composition and proposed nutritional importance of exudates eaten by saddleback (Sanguinus fuscicollis) and mustached (Saguinus mystax) tamarins. International Journal of Primatology, 21, 69–83.

    Article  Google Scholar 

  • Snaith, T. V., & Chapman, C. A. (2005). Towards an ecological solution to the folivore paradox: Patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behavioral Ecology and Sociobiology, 59, 185–190.

    Article  Google Scholar 

  • Snaith, T. V., & Chapman, C. A. (2007). Primate group size and interpreting socioecological models: Do primates really play by different rules? Evolutionary Anthropology, 16, 95–106.

    Article  Google Scholar 

  • Sommer, V., Bauer, J., Fowler, A., & Ortmann, S. (2011). Patriarchal chimpanzees, matriarchal bonobos: Potential ecological causes of a Pan dichotomy. In V. Sommer & C. Ross (Eds.), Primates of Gashaka: Sociology and conservation in Nigeria’s biodiversity hotspot (pp. 469–501). New York: Springer.

    Google Scholar 

  • Spalinger, D. E., & Hobbs, N. T. (1992). Mechanisms of foraging in mammalian herbivores: New models of functional response. American Naturalist, 140, 325–348.

    Article  PubMed  CAS  Google Scholar 

  • Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291–309.

    Article  Google Scholar 

  • Sterling, E. J., Dierenfeld, E. S., Ashbourne, C. J., & Feistner, A. T. C. (1994). Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatologica, 62, 115–124.

    Article  CAS  Google Scholar 

  • Stewart, J. L., Mould, F., & Mueller-Harvey, I. (2000). The effect of drying treatment on the fodder quality and tannin content of two provenances of Calliandra calothyrsus Meissner. Journal of the Science of Food and Agriculture, 80, 1461–1468.

    Article  CAS  Google Scholar 

  • Stork, N. E. (1991). The composition of the arthropod fauna of Bornean lowland rain forest trees. Journal of Tropical Ecology, 7, 161–180.

    Article  Google Scholar 

  • Sukhija, P. S., & Palmquist, D. L. (1988). Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. Journal of Agricultural and Food Chemistry, 36, 1202–1206.

    Article  CAS  Google Scholar 

  • Tsuji, Y., & Takatsuki, S. (2008). Effects of a typhoon on foraging behavior and foraging success of Macaca fuscata on Kinkazan Island, Northern Japan. International Journal of Primatology, 29, 1203–1217.

    Article  Google Scholar 

  • Urquiza-Haas, T., Serio-Silva, J. C., & Hernandez-Salazar, L. T. (2008). Traditional nutritional analyses of figs overestimates intake of most nutrient fractions: A study of Ficus perforata consumed by howler monkeys (Alouatta palliata mexicana). American Journal of Primatology, 70, 432–438.

    Article  PubMed  CAS  Google Scholar 

  • van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 195–218). Boston: Blackwell.

    Google Scholar 

  • Van Soest, P. (1963). Use of detergents in the analysis of fibrous feeds: II. A rapid method for the determination of fiber and lignin. Journal of the Association of Official Agricultural Chemists, 46, 829–835.

    Google Scholar 

  • Van Soest, P. J. (1994). Nutritional ecology of the ruminant. Ithaca, NY: Cornell University Press.

    Google Scholar 

  • Van Soest, P. J. (1996). Allometry and ecology of feeding behavior and digestive capacity in herbivores: A review. Zoo Biology, 15, 455–479.

    Article  Google Scholar 

  • Van Soest, P. J., Robertson, J. B., & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.

    Article  PubMed  Google Scholar 

  • Vogel, E. R. (2005). Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: The effects of contest competition. Behavioral Ecology and Sociobiology, 58, 333–344.

    Article  Google Scholar 

  • Vogel, E. R., Crowley, B. E., Knott, C. D., Blakely, M. D., Larsen, M. D., & Dominy, N. J. (2012). Non-invasive method for quantifying nitrogen balance in free-ranging primates. International Journal of Primatology.

  • Waterman, P. G., & Mole, S. (1994). Analysis of phenolic plant metabolites. Oxford: Blackwell.

    Google Scholar 

  • Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the central Virungas. American Journal of Primatology, 7, 323–356.

    Article  Google Scholar 

  • Worman, C. O., & Chapman, C. A. (2005). Seasonal variation in the quality of tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology, 21, 689–697.

    Article  Google Scholar 

  • Wrangham, R. W., & Waterman, P. G. (1981). Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea with special reference to reproductive strategies and tannin production. Journal of Animal Ecology, 50, 715–731.

    Article  Google Scholar 

  • Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.

    Article  Google Scholar 

  • Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949–970.

    Article  Google Scholar 

  • Zinner, D. (1999). Relationship between feeding time and food intake in hamadryas baboons (Papio hamadryas) and the value of feeding time as predictor of food intake. Zoo Biology, 18, 495–505.

    Article  Google Scholar 

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Acknowledgments

We thank Erin Vogel and Janine Chalk for inviting us to contribute this article. We also thank Erin Vogel, Janine Chalk, and Peter Lucas for organizing a fruitful workshop on Innovative Methods in Feeding Ecology, and we thank the participants of the workshop for inspiring discussions about nutritional methods. We thank Deborah Cherney, Ellen Dierenfeld, Mary Beth Hall, Skip Hintz, Caley Johnson, Joanna Lambert, Alice Pell, James Robertson, Deborah Ross, and Michael Van Amburgh for insights into the nutritional methods outlined here. We appreciate the very helpful comments provided by Caley Johnson, Erin Vogel, and 3 anonymous reviewers. We also thank our funding agencies, including the National Science Foundation under grant 0922709, Hunter College, Canada Research Chair program, and the National Science and Engineering Research Council.

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Rothman, J.M., Chapman, C.A. & Van Soest, P.J. Methods in Primate Nutritional Ecology: A User’s Guide. Int J Primatol 33, 542–566 (2012). https://doi.org/10.1007/s10764-011-9568-x

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