1932

Abstract

Eating is a risky affair. All animals have to offset risks of feeding such as exposure to plant toxins, increased vulnerability to predation, or conspecific aggression with a food's energetic and nutritional return. What, when, and where an individual eats can impact fitness and, ultimately, species-level adaptations. Here, we explore the variables that influence primate feeding preference: food availability, chemical defense, and nutrient content. We present information demonstrating that consumers manipulate nutrient and energy intake, indicating that what may be a less-than-optimal food for one state of an animal's phenotype may not be for another. This evidence suggests that factors previously assumed to be constraints in Optimal Foraging Theory, Functional Response, and—recently—Fallback Food feeding models would be better categorized as variables. We conclude that “fallback” is not an intrinsic state of the food or the consumer and that this conclusion complicates the application of this concept to morphological features in the fossil record.

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2015-10-21
2024-10-12
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Literature Cited

  1. Afik D, Karasov WH. 1995. The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76:2247–57 [Google Scholar]
  2. Altmann SA. 1998. Foraging for Survival: Yearling Baboons in Africa Chicago: Univ. Chicago Press [Google Scholar]
  3. Altmann SA. 2009. Fallback foods, eclectic omnivores, and the packaging problem. Am. J. Phys. Anthropol. 140:615–29 [Google Scholar]
  4. Amato K. 2013. Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci. Med. 1:10–29 [Google Scholar]
  5. Amato K, Leigh SR, Kent A, Mackie R, Yeoman C. et al. 2015. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69:2434–43 [Google Scholar]
  6. Ballhorn DJ, Kautz S, Rakotoarivelo S. 2009. Quantitative variability of cyanogenesis in Cathariostachys madagascariensis—the main food plant of bamboo lemurs in Southeastern Madagascar. Am. J. Primatol. 71:305–15 [Google Scholar]
  7. Barboza PS, Parker KL, Hume ID. 2009. Integrative Wildlife Nutrition Berlin: Springer-Verlag342 [Google Scholar]
  8. Behmer ST, Simpson SJ, Raubenheimer D. 2002. Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–501 [Google Scholar]
  9. Benson A, Kelly SA, Legge R, Ma F, Low SJ. et al. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS 107:18933–38 [Google Scholar]
  10. Boyle WA, Bronstein JL. 2012. Phenology of tropical understory trees: patterns and correlates. Rev. Biol. Trop. 60:1415–30 [Google Scholar]
  11. Brockman DK, van Schaik CP. 2005. Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  12. Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR. 2003. Variation in the nutritional value of primate foods: among trees, time periods, and areas. Int. J. Primatol. 24:317–33 [Google Scholar]
  13. Chapman CA, Rothman JM, Lambert JE. 2012. Food as a selective force in primates. The Evolution of Primate Societies JC Mitani, J Call, PM Kappeler, RA Palombit, JB Silk 149–68 Chicago: Univ. Chicago Press [Google Scholar]
  14. Chapman CA, Wrangham RW, Chapman LJ. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav. Ecol. Sociobiol. 36:59–70 [Google Scholar]
  15. Chapman CA, Wrangham RW, Chapman LJ, Kennard DK, Zanne AE. 1999. Fruit and flower phenology at two sites in Kibale National Park, Uganda. J. Trop. Ecol. 15:189–211 [Google Scholar]
  16. Charnov EL. 1976. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9:129–36 [Google Scholar]
  17. Clutton-Brock TH, Harvey PH. 1977. Primate ecology and social organization. J. Zool. Soc. Lond. 183:1–39 [Google Scholar]
  18. Clutton-Brock TH, Janson CH. 2012. Primate socioecology at the crossroads: past, present and future. Evol. Anthropol. 21:136–50 [Google Scholar]
  19. Conklin NL, Wrangham RW. 1994. The value of figs to a hind-gut fermenting frugivore: a nutritional analysis. Biochem. Syst. Ecol. 22:137–51 [Google Scholar]
  20. Constantino PJ, Lucas PW, Lee JJ-W, Lawn BR. 2009. The influence of fallback foods on great ape tooth enamel. Am. J. Phys. Anthropol. 140:653–60 [Google Scholar]
  21. Constantino PJ, Wright PW. 2009. The importance of fallback foods in primate ecology and evolution. Am. J. Phys. Anthropol. 140:599–602 [Google Scholar]
  22. Crofoot MC. 2013. The cost of defeat: Capuchin groups travel further, faster and later after losing conflicts with neighbors. Am. J. Phys. Anthropol. 152:79–85 [Google Scholar]
  23. David L, Maurice C, Carmody R, Gootenberg D, Button J. et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–63 [Google Scholar]
  24. DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C. et al. 2014. Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 123:298–308 [Google Scholar]
  25. Dillis C, Beaudrot L, Feilen KL, Clink DJ, Wittmer HU, Marshall AJ. 2013. Modeling the ecological and phenological predictors of fruit consumption by gibbons (Hylobates albibarbis). Biotropica 47:85–93 [Google Scholar]
  26. Dominy NJ, Lucas PW, Osorio D, Yamashita N. 2001. The sensory ecology of primate food perception. Evol. Anthropol. 10:171–86 [Google Scholar]
  27. Dussutour A, Latty T, Beekman M, Simpson SJ. 2010. Amoeboid organism solves complex nutritional challenges. PNAS 107:4607–11 [Google Scholar]
  28. Feeny P. 1976. Plant apparency and chemical defense. Recent Adv. Phytochem. 10:1–40 [Google Scholar]
  29. Felton AM, Felton A, Lindenmayer DB, Foley WJ. 2009a. Nutritional goals of wild primates. Funct. Ecol. 23:70–78 [Google Scholar]
  30. Felton AM, Felton A, Wood JT, Foley WJ, Raubenheimer D. et al. 2009b. Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. Int. J. Primatol. 30:675–96 [Google Scholar]
  31. Fenner M. 1998. The phenology of growth and reproduction in plants. Perspect. Plant Ecol. Evol. Syst. 1:78–91 [Google Scholar]
  32. Foster R. 1993. Famine on Barro Colorado Island. The Ecology of a Neotropical Forest: Season Rhythms and Long-Term Changes EG Leigh, AS Rand, DM Windsor 201–12 Washington, DC: Smithsonian Inst. Press [Google Scholar]
  33. Fox EA, van Schaik CP, Sitompul A, Wright DN. 2004. Intra- and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use. Am. J. Phys. Anthropol. 125:162–74 [Google Scholar]
  34. Freeland WJ, Janzen DH. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108:269–89 [Google Scholar]
  35. Furuichi T, Hashimoto C, Tashiro Y. 2001. Fruit availability and habitat use by chimpanzees in the Kalinzu Forest, Uganda: examination of fallback foods. Int. J. Primatol. 22:929–45 [Google Scholar]
  36. Ganas J, Ortmann S, Robbins MM. 2008. Food preferences of wild mountain gorillas. Am. J. Primatol. 70:927–38 [Google Scholar]
  37. Ganzhorn JU. 1995. Low-level forest disturbance effects on primary production, leaf chemistry and lemur populations. Ecology 76:2084–96 [Google Scholar]
  38. Gautier-Hion A, Michaloud G. 1989. Are figs always keystone resources for tropical frugivorous vertebrates? A test in Gabon. Ecology 70:1826–33 [Google Scholar]
  39. Glander KE, Wright PC, Seigler DS, Randrianasolo V, Randrianasolo B. 1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. Am. J. Primatol. 19:199–24 [Google Scholar]
  40. Grueter CC, Li D, Ren B, Wei F, Xiang Z, van Schaik CP. 2009. Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am. J. Phys. Anthropol. 140:700–15 [Google Scholar]
  41. Gursky S. 2000. Effect of seasonality on the behavior of an insectivorous primate, Tarsius spectrum. Int. J. Primatol. 21:477–95 [Google Scholar]
  42. Harborne JB. 2001. Twenty-five years of chemical ecology. Nat. Prod. Rep. 18:361–79 [Google Scholar]
  43. Hawes JP, Peres CA. 2014. Ecological correlates of trophic status and frugivory in neotropical primates. Oikos 123:365–77 [Google Scholar]
  44. Hemingway CA, Bynum N. 2005. The influence of seasonality on primate diet and ranging. See Brockman & van Schaik 2005 57–104
  45. Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K. et al. 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. PNAS 105:4792–95 [Google Scholar]
  46. Hewson-Hughes AK, Hewson-Hughes VL, Miller AT, Hall SR, Simpson SJ, Raubenheimer D. 2011. Geometric analysis of macronutrient selection in the adult domestic cat, Felis catus. J. Exp. Biol. 214:1039–51 [Google Scholar]
  47. Hill DA. 1999. Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. Am. J. Primatol. 43:305–20 [Google Scholar]
  48. Hladik CM. 1973. Alimentation et activite d'un groupe de chimpanzes reintroduit en foret gabonaise. Terre Vie 27:343–443 [Google Scholar]
  49. Hladik CM. 1977. Chimpanzees of Gabon and chimpanzees of Gombe: some comparative data on the diet. Primate Ecology TH Clutton-Brock 487–501 New York: Academic [Google Scholar]
  50. Holling CS. 1959. Some characteristics of simple types of predation and parasitism. Can. Entomol. 91:385–98 [Google Scholar]
  51. Holling CS. 1965. The functional response of predators to prey density and its role in mimicry and population regulation. Mem. Entomol. Soc. Can. 97:5–60 [Google Scholar]
  52. Houle A, Conklin-Brittain NL, Wrangham RW. 2014. Vertical stratification of the nutritional value of fruit: macronutrients and condensed tannins. Am. J. Primatol. 76:1207–32 [Google Scholar]
  53. Iason GR, Dicke M, Hartley SE. 2013. The Ecology of Plant Secondary Metabolites: From Genes to Global Processes Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  54. Isbell LA, Rothman JM, Young PJ, Rudolph K. 2013. Nutritional benefits of Crematogaster mimosae ants and Acacia drepanolobium gum for patas monkeys and vervets in Laikipia, Kenya. Am. J. Phys. Anthropol. 150:286–300 [Google Scholar]
  55. Janson CH, Chapman CA. 1999. Resources and primate community structure. Primate Communities JG Fleagle, CH Janson, KE Reed 237–67 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  56. Janson CH, van Schaik CP. 1988. Recognizing the many faces of primate food competition: methods. Behaviour 105:165–86 [Google Scholar]
  57. Johnson CA, Raubenheimer D, Rothman JM, Clarke D, Swedell L. 2013. 30 days in the life: nutrient balancing in a wild chacma baboon. PLOS ONE 8:270383 [Google Scholar]
  58. Jolly A. 2009. Coat condition of ringtailed lemurs, Lemur catta, at Berenty Reserve, Madagascar: II. Coat and tail alopecia associated with Leucaena leucocephala, 2001–2006. Am. J. Primatol. 71:199–205 [Google Scholar]
  59. Karasov WH, Martinez del Rio C. 2007. Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins Princeton, NJ: Princeton Univ. Press [Google Scholar]
  60. Knott CD. 2005. Energetic responses to food availability in the great apes: implications for hominin evolution. See Brockman & van Schaik 2005 351–78
  61. Kohler A, Raubenheimer D, Nicholson SW. 2012. Regulation of nutrient intake in nectar-feeding birds: insights from the geometric framework. J. Comp. Physiol. B 182:603–11 [Google Scholar]
  62. Koricheva J, Barton KE. 2013. Temporal changes in plant secondary metabolite production: patterns, causes, and consequences. See Iason et al. 2013 34–55
  63. Krebs J, McCleery R. 1984. Optimization in behavioural ecology. Behavioural Ecology: An Evolutionary Approach JR Krebs, NB Davies 9–21 Sunderland, MA: Sinauer, 2nd ed.. [Google Scholar]
  64. Laden G, Wrangham RW. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J. Hum. Evol. 49:482–98 [Google Scholar]
  65. Lambert JE. 2007. Seasonality, fallback strategies, and natural selection: a chimpanzee and cercopithecoid model for interpreting the evolution of hominin diet. Evolution of the Human Diet: The Known, the Unknown, and the Unknowable PS Ungar 324–43 Oxford, UK: Oxford Univ. Press [Google Scholar]
  66. Lambert JE. 2009. Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity—scale, pattern, and process. Am. J. Phys. Anthropol. 140759–66 [Google Scholar]
  67. Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am. J. Phys. Anthropol. 125:4363–68 [Google Scholar]
  68. Lambert JE, Fellner V. 2012. In vitro fermentation of dietary carbohydrates in African apes and monkeys: preliminary results on digestive and microbial strategy. Int. J. Primatol. 33:263–81 [Google Scholar]
  69. Lambert JE, Fellner V, McKenney E, Hartstone-Rose A. 2014. Binturong (Arctictis binturong) and Kinkajou (Potos flavus) digestive strategy: implications for interpreting frugivory in carnivora and primates. PLOS ONE 9:8e105415 [Google Scholar]
  70. Laska M, Schull E, Scheuber HP. 1999. Taste preference thresholds for food-associated sugars in baboons (Papio hamadryas anubis). Int. J. Primatol. 20:25–34 [Google Scholar]
  71. Le Gros Clark WE. 1957. History of the Primates: An Introduction to the Study of Fossil Man Chicago: Univ. Chicago Press [Google Scholar]
  72. Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JWO. et al. 2008. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. PNAS 105:2498–503 [Google Scholar]
  73. Lee WB, Houston DC. 1993. The effect of diet quality on gut anatomy in British voles. J. Comp. Physiol. 163:337–39 [Google Scholar]
  74. Leighton M. 1993. Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. Int. J. Primatol. 14:257–313 [Google Scholar]
  75. Lucas PW, Constantino PJ, Chalk J, Ziscovici C, Wright BW. et al. 2009. Indentation as a technique to assess the mechanical properties of fallback foods. Am. J. Phys. Anthropol. 140:643–52 [Google Scholar]
  76. Lucas PW, Copes L, Constantino PJ, Vogel ER, Chalk J. et al. 2012. Measuring the toughness of primate foods and its ecological value. Int. J. Primatol. 33:598–610 [Google Scholar]
  77. MacArthur RH, Pianka E. 1966. On optimal use of a patchy environment. Am. Nat. 100:603–9 [Google Scholar]
  78. Marlowe FW, Berbesque JC. 2009. Tubers as fallback foods and their impact on Hadza hunter-gatherers. Am. J. Phys. Anthropol. 140:751–58 [Google Scholar]
  79. Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M. 2009. Defining fallback foods and assessing their importance in primate ecology and evolution. Am. J. Phys. Anthropol. 140:603–14 [Google Scholar]
  80. Marshall AJ, Wrangham RW. 2007. Evolutionary consequences of fallback foods. Int. J. Primatol. 28:119–26 [Google Scholar]
  81. Martin RD, Chivers DJ, MacLarnon AM, Hladik CM. 1985. Gastrointestinal allometry in primates and other mammals. Size and Scaling in Primate Biology WL Jungers 61–89 New York: Plenum [Google Scholar]
  82. Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ. 2005. Nutrient-specific foraging in invertebrate predators. Science 307:111–13 [Google Scholar]
  83. McCord AI, Chapman C, Weny G, Tumukunde A, Hyeroba D. et al. 2014. Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am. J. Primatol. 76:347–54 [Google Scholar]
  84. McGraw WS, Daegling DJ. 2012. Primate feeding and foraging: integrating studies of behavior and morphology. Annu. Rev. Anthropol. 41:203–19 [Google Scholar]
  85. Mertl-Millhollen A, Moret E, Felantsoa D, Rasamimanana H, Blumenfeld-Jones KC, Jolly A. 2003. Ring-tailed lemur home ranges correlate with food abundance and nutritional content at a time of environmental stress. Int. J. Primatol. 24:969–85 [Google Scholar]
  86. Milton K. 1999. Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us?. Nutrition 15:488–98 [Google Scholar]
  87. Milton K, Demment M. 1988. Digestive and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. J. Nutr. 118:91082–88 [Google Scholar]
  88. Moura AC, Lee PC. 2004. Capuchin stone tool use in Caatinga dry forest. Science 306:1909 [Google Scholar]
  89. Napier JR, Napier PH. 1967. A Handbook of Living Primates New York: Academic [Google Scholar]
  90. Oates JF. 1987. Food distribution and foraging behavior. Primate Societies BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, TT Struhsaker 197–209 Chicago: Univ. Chicago Press [Google Scholar]
  91. Oftedal OT. 1991. The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philos. Trans. R. Soc. Lond. B 334:161–70 [Google Scholar]
  92. Potts R. 1999. Variability selection in hominid evolution. Evol. Anthropol. 7:81–96 [Google Scholar]
  93. Rathcke B, Lacey EP. 1985. Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst. 16:179–214 [Google Scholar]
  94. Raubenheimer D, Machovsky-Capuska GE, Chapman CA, Rothman JM. 2015. Geometry of nutrition in field studies: an illustration using wild primates. Oecologia 177:223–34 [Google Scholar]
  95. Raubenheimer D, Simpson SJ. 1997. Integrative models of nutrient balancing: application to insects and vertebrates. Nutr. Res. Rev. 10:151–79 [Google Scholar]
  96. Raubenheimer D, Simpson SJ, Mayntz D. 2009. Nutrition, ecology, and nutritional ecology: toward an integrated framework. Funct. Ecol. 23:4–16 [Google Scholar]
  97. Ravosa MJ, Lopez EK, Menegaz RA, Stock SR, Stack MS, Hamrick MW. 2008. Adaptive plasticity in the mammalian masticatory complex: You are what, and how, you eat. Primate Craniofacial Function and Biology C Vinyard, M Ravosa, C Wall 293–329 New York: Springer [Google Scholar]
  98. Reynolds V, Lloyd AW, Babweteera F, English CJ. 2009. Decaying Raphia farinifera palm trees provide a source of sodium for wild chimpanzees in the Budongo Forest, Uganda. PLOS ONE 4:7e6194 [Google Scholar]
  99. Reynolds V, Plumptre AJ, Greenham J, Harborne J. 1998. Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia 115:331–36 [Google Scholar]
  100. Ripple WJ, Beschta RL. 2004. Wolves, elk, willows, and trophic cascades in the upper Gallatin Range of southwestern Montana, USA. Forest Ecol. Manag. 200:161–81 [Google Scholar]
  101. Rosenberger AL. 2013. Fallback foods, preferred foods, adaptive zones, and primate origins. Am. J. Primatol. 75:883–90 [Google Scholar]
  102. Ross C, Iriarte-Diaz J, Nunn CL. 2012. Innovative approaches to the relationship between diet and mandibular morphology in primates. Int. J. Primatol. 33:632–60 [Google Scholar]
  103. Rothman JM, Chapman CA, van Soest PJ. 2012. Methods in primate nutritional ecology: a user's guide. Int. J. Primatol. 33:542–66 [Google Scholar]
  104. Rothman JM, Raubenheimer D, Bryer MAH, Takahashi M, Gilbert CC. 2014. Nutritional contributions of insects to primate diets: implications for primate evolution. J. Hum. Evol. 71:59–69 [Google Scholar]
  105. Rothman JM, Raubenheimer D, Chapman CA. 2011. Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol. Lett. 7:847–49 [Google Scholar]
  106. Rothman JM, van Soest PJ, Pell AN. 2006. Decaying wood is a sodium source for mountain gorillas. Biol. Lett. 2:321–24 [Google Scholar]
  107. Saunders DS. 2002. Insect Clocks Amsterdam, Neth: Elsevier [Google Scholar]
  108. Sauther ML, Cuozzo F. 2009. The impact of fallback foods on wild ring-tailed lemur biology: a comparison of intact and anthropogenically disturbed habitats. Am. J. Phys. Anthropol. 140:671–86 [Google Scholar]
  109. Schoener TW. 1971. Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2:369–404 [Google Scholar]
  110. Schowalter TD. 2006. Insect Ecology: An Ecosystem Approach New York: Academic [Google Scholar]
  111. Scott JE, McAbee KR, Eastman MM, Ravosa MJ. 2014. Experimental perspective on fallback foods and dietary adaptations in early hominins. Biol. Lett. 10:1 doi: 10.1098/rsbl.2013.0789 [Google Scholar]
  112. Simpson SJ, Raubenheimer D. 1995. The geometric analysis of feeding and nutrition: a user's guide. J. Insect Physiol. 41:545–53 [Google Scholar]
  113. Simpson SJ, Raubenheimer D. 2005. Obesity: the protein leverage hypothesis. Obes. Rev. 6:133–42 [Google Scholar]
  114. Simpson SJ, Raubenheimer D. 2012. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity Princeton, NJ: Princeton Univ. Press [Google Scholar]
  115. Snaith TV, Chapman CA. 2007. Primate group size and socioecological models: Do folivores really play by different rules?. Evol. Anthropol. 16:94–106 [Google Scholar]
  116. Stalenberg E, Wallis IR, Cunningham RB, Allen C, Foley WJ. 2014. Nutritional correlates of koala persistence in a low-density population. PLOS ONE 9:e113930 [Google Scholar]
  117. Stanford CB, Nkurunungi JB. 2003. Behavioral ecology of sympatric chimpanzees and gorillas in Bwindi Impenetrable National Park, Uganda: diet. Int. J. Primatol. 24:901–18 [Google Scholar]
  118. Stephens CE, Krebs J. 1986. Foraging Theory Princeton, NJ: Princeton Univ. Press [Google Scholar]
  119. Strier KB. 2009. Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Curr. Anthropol. 50:213–28 [Google Scholar]
  120. Struhsaker TT. 2010. The Red Colobus Monkeys: Variation in Demography, Behavior, and Ecology of Endangered Species Oxford, UK: Oxford Univ. Press [Google Scholar]
  121. Terborgh JW. 1984. Five New World Primates: A Study in Comparative Ecology Princeton, NJ: Princeton Univ. Press [Google Scholar]
  122. Terborgh JW, Stern M. 1987. The surreptitious life of the saddle-backed tamarin. Am. Sci. 75:260–69 [Google Scholar]
  123. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon HA. 2009. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1:6ra14 [Google Scholar]
  124. Tutin C, Hamm RM, White L, Harrison M. 1997. The primate community of Lopé Reserve, Gabon: diets, response to fruit scarcity, and effects on biomass. Am. J. Primatol. 42:1–24 [Google Scholar]
  125. Ungar PS. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. J. Hum. Evol. 46:605–22 [Google Scholar]
  126. Ungar PS. 2012. Dental evidence for the reconstruction of diet in African early Homo. Curr. Anthropol. 53:S318–29 [Google Scholar]
  127. Ungar PS, Grine FE, Teaford MF. 2008. Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLOS ONE 3e2044 [Google Scholar]
  128. van Schaik CP, Brockman DK. 2005. Seasonality in primate ecology, reproduction, and life history: an overview. See Brockman & van Schaik 2005 3–20
  129. van Schaik CP, Terborgh JW, Wright SJ. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu. Rev. Ecol. Syst. 24:353–77 [Google Scholar]
  130. Verlinden C, Wiley R. 1989. The constraints of digestive rate: an alternative model of diet selection. Evol. Ecol. 3:264–72 [Google Scholar]
  131. Villalba JJ, Provenza FD. 1999. Effects of food structure and nutritional quality and animal nutritional state on intake behaviour and food preferences of sheep. Appl. Anim. Behav. Sci. 63:145–63 [Google Scholar]
  132. Vogel ER, Haag L, Mitra-Setia T, van Schaik CP, Dominy NJ. 2009. Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. Am. J. Phys. Anthropol. 140:716–26 [Google Scholar]
  133. Waterman PG, Kool KM. 1994. Colobine food selection and plant chemistry. Colobine Monkeys: Their Ecology, Behaviour and Evolution AG Davies, JF Oates 251–73 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  134. Watts DP. 1984. Composition and variability of mountain gorilla diets in the central Virungas. Am. J. Primatol. 7:323–56 [Google Scholar]
  135. Watts DP. 1988. Environmental influences on mountain gorilla time budgets. Am. J. Primatol. 15:195–211 [Google Scholar]
  136. West-Eberhard MJ. 2003. Developmental Plasticity and Evolution Oxford, UK: Oxford Univ. Press [Google Scholar]
  137. Witte F. 1984. Consistency and functional significance of morphological differences between wild-caught and domestic Haplochromis squamipinnis (Pisces, Cichlidae). J. Zool. 34:596–612 [Google Scholar]
  138. Worman CO, Chapman CA. 2005. Seasonal variation in the quality of tropical ripe fruit and the response of three frugivores. 216689–97
  139. Wrangham RW, Cheney D, Seyfarth R, Sarmiento E. 2009. Shallow-water habitats as sources of fallback foods for hominins. Am. J. Phys. Anthropol. 140:630–42 [Google Scholar]
  140. Wrangham RW, Conklin NL, Hunt KD. 1998. Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance: I. Antifeedants. Int. J. Primatol. 19:949–70 [Google Scholar]
  141. Wrangham RW, Waterman PG. 1981. Feeding behaviour of vervet monkeys on Acacia tortilis and Acadi xanthophloea: with special reference to reproductive strategies and tannin production. J. Anim. Ecol. 50:715–31 [Google Scholar]
  142. Wright B, Wright K, Chalk J, Verderane M, Fragaszy D. et al. 2009. Fallback foraging as a way of life: using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation. Am. J. Phys. Anthropol. 140:687–99 [Google Scholar]
  143. Yamagiwa J, Basabose AK. 2009. Fallback foods and dietary partitioning among Pan and Gorilla. Am. J. Phys. Anthropol. 140:739–50 [Google Scholar]
  144. Yamakoshi G. 1998. Dietary response to fruit scarcity of wild chimpanzees in Boussou, Guinea: possible implication for ecological importance of tool use. Am. J. Phys. Anthropol. 106:283–95 [Google Scholar]
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