, 50:131 | Cite as

Feeding rate as valuable information in primate feeding ecology

  • Naofumi NakagawaEmail author
Review Article Special contributions to commemorate the 60th anniversary of Japanese primatology


In this review I outline studies on wild non-human primates using information on feeding rate, which is defined as the food intake per minute on a dry-weight basis; further, I summarize the significance of feeding rate in primate feeding ecology. The optimal foraging theory has addressed three aspects of animal feeding: (1) optimal food patch choice, (2) optimal time allocation to different patches, and (3) optimal food choice. In order to gain a better understanding of these three aspects, the feeding rate itself or its relevance indices (e.g., rates of calorie and protein intake) could be appropriate measures to assess the quality of food and food patches. Moreover, the feeding rate plays an essential role in estimation of total food intake, because it varies greatly for different food items and the feeding time is not a precise measure. The feeding rate could also vary across individuals who simultaneously feed on the same food items in the same food patch. Body size-dependent and rank-dependent differences in the feeding rate sometimes cause individuals to take strategic behavioral options. In the closing remarks, I discuss the usefulness of even limited data on feeding rate obtained under adverse observational conditions in understanding primate feeding ecology.


Feeding rate Feeding success Food intake Food quality Optimal foraging 



I am much honored to have been given the opportunity to write a paper for the memorable issue of “Primates” that celebrates the 60th anniversary of Japanese Primatology and the 50th anniversary of the Japan Monkey Center. I am grateful to Toshisada Nishida, Editor-in-chief, and other editorial board members of Primates for their invitation. I also thank the three reviewers of “Primates” for their constructive comments. This research was financially supported in part by the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the Ministry of Education, Culture, Sports, and Technology (MEXT), Japan.


  1. Barton RA, Whiten A (1994) Reducing complex diets to simple rules: food selection by olive baboons. Behav Ecol Sociobiol 35:283–293CrossRefGoogle Scholar
  2. Byrne RW, Whiten A, Henzi SP, McCulloch FM (1993) Nutritional constraints on mountain baboons (Papio ursinus): implications for baboon socioecology. Behav Ecol Sociobiol 33:233–246CrossRefGoogle Scholar
  3. Chapman CA (1988) Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour 105:99–116CrossRefGoogle Scholar
  4. Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136PubMedCrossRefGoogle Scholar
  5. Chivers DJ (1998) Measuring food intake in wild animals: primates. Proc Nutr Soc 57:321–332PubMedCrossRefGoogle Scholar
  6. Clutton-Brock TH (ed) (1977) Primate ecology. Academic Press, LondonGoogle Scholar
  7. Conklin-Brittain NL, Knott CD, Wrangham RW (2006) Energy intake by wild chimpanzees and orangutans: methodological considerations and a preliminary comparison. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: Ecological, physical and behavioral aspects. Cambridge University Press, Cambridge, pp 445–471Google Scholar
  8. Dasilva GL (1992) The western black-and-white colobus as a low-energy strategist: activity budgets, energy expenditure and energy intake. J Anim Ecol 61:79–91CrossRefGoogle Scholar
  9. Davies AG, Bennett EL, Waterman PG (1988) Food selection by two south-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biol J Linn Soc 34:33–56CrossRefGoogle Scholar
  10. Fa JE (1986) Use of time and resources by provisioned troops of monkeys: social behaviour, time and energy in the Barbary macaque (Macaca sylvanus L.) at Gibraltar. Karger, BaselGoogle Scholar
  11. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289CrossRefGoogle Scholar
  12. Ganzhorn JU (2003) Habitat description and phenology. In: Curtis DJ, Setchell JM (eds) Field and laboratory methods in primatology. Cambridge University Press, Cambridge, pp 40–56Google Scholar
  13. Gaulin SJC, Gaulin CK (1982) Behavioral ecology of Alouatta seniculus in Andean cloud forest. Int J Primatol 3:1–32CrossRefGoogle Scholar
  14. Grether GF, Palombit RA, Rodman PS (1992) Gibbon foraging decisions and the marginal value model. Int J Primatol 13:1–18CrossRefGoogle Scholar
  15. Hanya G (2003) Age differences in food intake and dietary selection of wild male Japanese macaques. Primates 44:333–339PubMedCrossRefGoogle Scholar
  16. Hanya G, Kiyono M, Takafumi H, Tsujino R, Agetsuma N (2007) Mature leaf selection of Japanese macaques: effects of availability and chemical content. J Zool 273:140–147CrossRefGoogle Scholar
  17. Hladik CM (1977a) A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In: Clutton-Brock TH (ed) Primate ecology. Academic Press, London, pp 324–353Google Scholar
  18. Hladik CM (1977b) Chimpanzees of Gabon and chimpanzees of Gombe: some comparative data on the diet. In: Clutton-Brock TH (ed) Primate ecology. Academic Press, London, pp 481–501Google Scholar
  19. Imanishi K (1960) Gorilla. Bungeishunju-Shinsha, Tokyo (in Japanese)Google Scholar
  20. Iwamoto T (1974) A bioeconomic study on a provisioned troop of Japanese monkeys (Macaca fuscata fuscata) at Koshima Islet, Miyazaki. Primates 15:241–262CrossRefGoogle Scholar
  21. Iwamoto T (1979) Feeding ecology. In: Kawai M et al (eds) Ecological and sociological studies of Gelada baboons. Karger, Basel, pp 279–310Google Scholar
  22. Iwamoto T (1982) Food and nutritional condition of free ranging Japanese monkeys on Koshima Islet during winter. Primates 23:153–170CrossRefGoogle Scholar
  23. Janson CH (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138CrossRefGoogle Scholar
  24. Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76CrossRefGoogle Scholar
  25. Janson CH, Chapman CA (1999) Resources and primate community structure. In: Fleagle JG, Janson CH, Reed KE (eds) Primate community. Cambridge University Press, Cambridge, pp 237–267Google Scholar
  26. Janson CH, Vogel E (2006) Hunger and aggression in capuchin monkeys. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: ecological, physiological and behavioral aspects. Cambridge University Press, New York, pp 285–312Google Scholar
  27. Kazahari N, Agetsuma N (2008) Social factors enhancing foraging success of a wild group of Japanese macaques (Macaca fuscata) in a patchy food environment. Behaviour 145:843–860CrossRefGoogle Scholar
  28. Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079CrossRefGoogle Scholar
  29. Koenig A, Borries C, Chalise MK, Winker P (1997) Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J Zool 234:215–235CrossRefGoogle Scholar
  30. Kurland JA, Gaulin SJC (1987) Comparability among measures of primate diets. Primates 28:71–77CrossRefGoogle Scholar
  31. Lambert JE (2007) Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In: Campbell CH, Fuentes A, Mackinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 482–495Google Scholar
  32. Leighton M (1993) Modeling dietary selectivity by Bornean Orangutans: evidence for integration of multiple criteria in fruit selection. Int J Primatol 14:257–313CrossRefGoogle Scholar
  33. Matsumoto-Oda A, Hayashi Y (1999) Nutritional aspects of fruit choice by chimpanzees. Folia Primatol 70:154–162PubMedCrossRefGoogle Scholar
  34. McCabe GM, Fedigan LM (2007) Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. Int J Primatol 28:837–851CrossRefGoogle Scholar
  35. Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362–377CrossRefGoogle Scholar
  36. Mori A (1995) Rank and age related feeding strategy observed through field experiments in the Koshima group of Japanese macaques. Primates 36:11–26CrossRefGoogle Scholar
  37. Nakagawa N (1989a) Feeding strategies of Japanese monkeys against deterioration of habitat quality. Primates 30:1–16CrossRefGoogle Scholar
  38. Nakagawa N (1989b) Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island during winter. Primates 30:441–460CrossRefGoogle Scholar
  39. Nakagawa N (1990a) Choice of food patches by Japanese monkeys (Macaca fuscata). Am J Primatol 21:17–29CrossRefGoogle Scholar
  40. Nakagawa N (1990b) Decisions on time allocation to different food patches by Japanese monkeys (Macaca fuscata). Primates 31:459–469CrossRefGoogle Scholar
  41. Nakagawa N (1996) Reconsideration of optimal food selection in non-human primates. Jpn J Ecol 46:291–307 (in Japanese with english summary)Google Scholar
  42. Nakagawa N (1997a) Quantified food lists of the Japanese monkeys in Kinkazan Island. Primate Res 13:73–89 (in Japanese with english abstract)Google Scholar
  43. Nakagawa N (1997b) Determinants of the dramatic seasonal changes in the intake of energy and protein by Japanese monkeys in a cool temperate forest. Am J Primatol 41:267–288PubMedCrossRefGoogle Scholar
  44. Nakagawa N (2000a) Seasonal, sex, and interspecific differences in activity time budgets and diets of patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), living sympatrically in northern Cameroon. Primates 41:161–174CrossRefGoogle Scholar
  45. Nakagawa N (2000b) Foraging energetics in patas monkeys (Etythrocebus patas) and Tantalus monkeys (Cercopithecus aethiops tantalus): implications for reproductive seasonality. Am J Primatol 52:169–185PubMedCrossRefGoogle Scholar
  46. Nakagawa N (2003) Difference in food selection between patas monkeys (Erythrocebus patas) and Tantalus monkeys (Cercopithecus aethiops tantalus) in Kala Maloue National Park, Cameroon, in relation to nutrient content. Primates 44:3–11PubMedCrossRefGoogle Scholar
  47. Nakagawa N (2008) The scaling of feeding rate in wild primates: a preliminary analysis. Mammal Study 33:157–162CrossRefGoogle Scholar
  48. Nakagawa N, Iwamoto T, Yokota N, Soumah AG (1996) Inter-regional and inter-seasonal variations of food quality in Japanese macaques: with reference to the constraints of digestive volume and feeding time. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 207–234Google Scholar
  49. Nakayama Y, Matsuoka S, Watanuki Y (1999) Feeding rates and energy deficits of juvenile and adult Japanese monkeys in a cool temperate area with snow coverage. Ecol Res 14:291–301CrossRefGoogle Scholar
  50. Oates JF, Waterman PG, Choo GM (1980) Food selection by the South Indian leaf-monkey, Presbytis johnii, in relation to leaf chemistry. Oecologia 45:45–56CrossRefGoogle Scholar
  51. Perry G, Pianka ER (1997) Animal foraging: past, present and future. Trends Evol Ecol 12:360–364CrossRefGoogle Scholar
  52. Post DG, Hausfater G, McCuskey SA (1980) Feeding behavior of yellow baboons (Papio cynocephalus): relationship to age, gender and dominance rank. Folia Primatol 34:170–195PubMedCrossRefGoogle Scholar
  53. Pulliam HR (1974) On the theory of optimal diets. Am Nat 108:59–74CrossRefGoogle Scholar
  54. Pulliam HR (1975) Diet optimization with nutrient constraints. Am Nat 109:765–768CrossRefGoogle Scholar
  55. Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154CrossRefGoogle Scholar
  56. Reynolds V, Plumptre A, Greenham HJ (1998) Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo forest, Uganda. Oecologia 115:331–336CrossRefGoogle Scholar
  57. Robbins MM, Hohmann G (2006) Primate feeding ecology: an integrative approach. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: ecological, physiological and behavioral aspects. Cambridge University Press, New York, pp 1–13Google Scholar
  58. Rogers ME, Maisels F, Williamson EA, Fernandez M, Tutin CEG (1990) Gorilla diet in the Lope Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339Google Scholar
  59. Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Anim Behav 51:967–980CrossRefGoogle Scholar
  60. Schoener TW (1971) Theory of feeding strategy. Ann Rev Ecol Sys 2:369–404CrossRefGoogle Scholar
  61. Schülke O, Chalise MK, Koenig A (2006) The importance of ingestion rates for estimating food quality and energy intake. Am J Primatol 68:951–965PubMedCrossRefGoogle Scholar
  62. Shipley LA, Gross JE, Spalinger DE, Hobbs NT, Wunder BA (1994) The scaling of intake rate in mammalian herbivores. Am Nat 143:1055–1082CrossRefGoogle Scholar
  63. Shopland JM (1987) Food quality, spatial deployment, and the intensity of feeding interference in yellow baboons (Papio cynocephalus). Behav Ecol Sociobiol 21:149–156CrossRefGoogle Scholar
  64. Sih A, Christensen B (2001) Optimal diet theory: when does it work, and when and why does it fail. Anim Behav 61:379–390CrossRefGoogle Scholar
  65. Snaith TV, Chapman CA (2005) Towards an ecological solution the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behav Ecol Sociobiol 59:185–190CrossRefGoogle Scholar
  66. Soumah AG, Yokota N (1991) Female rank and feeding strategies in a free-ranging provisioned troop of Japanese macaques. Folia primatol 57:191–200CrossRefGoogle Scholar
  67. Stacey PB (1986) Group size and foraging efficiency in yellow baboons. Behav Ecol Sociobiol 18:175–187CrossRefGoogle Scholar
  68. Stammati M, Sabbatini G, Visalberghi E (2008) An experimental analysis of ingestion rates in an omnivorous species. Am J Primatol 70:1–4CrossRefGoogle Scholar
  69. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  70. Sterling EJ, Dierenfeld ES, Ashbourne CJ, Feistner ATC (1994) Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatol 62:115–124PubMedCrossRefGoogle Scholar
  71. Takemoto H (2003) Phytochemical determination for leaf food choice by wild chimpanzees in Guinea, Bossou. J Chem Ecol 29:2551–2573PubMedCrossRefGoogle Scholar
  72. Tsuji Y, Kazahari N, Kitahara M, Takatsuki S (2008) A more detailed seasonal division of the energy balance and the protein balance of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Primates 49:157–160PubMedCrossRefGoogle Scholar
  73. Urquiza-Haas T, Serio-Silva JC, Hernández-Salazar LT (2008) Traditional nutritional analyses of figs overestimates intake of most nutrient fractions: a study of Ficus perforata consumed by howler monkeys (Alouatta palliata mexicana). Am J Primatol 70:432–438CrossRefGoogle Scholar
  74. van Schaik CP, van Noordwijk MA (1988) Scramble and contest in feeding competition among female long-tailed macaques (Macaca fascicularis). Behaviour 105:77–98CrossRefGoogle Scholar
  75. Vogel ER (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344CrossRefGoogle Scholar
  76. Wasserman MD, Chapman CA (2003) Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. J Anim Ecol 72:650–659CrossRefGoogle Scholar
  77. Westoby M (1974) An analysis of diet selection by large generalist herbivores. Am Nat 108:290–304CrossRefGoogle Scholar
  78. Whitten PL (1988) Effects of patch quality and feeding subgroup size on feeding success in vervet monkeys (Cercopithecus aethiops). Behaviour 105:35–52CrossRefGoogle Scholar
  79. Wrangham RW, Conklin NL, Etot G, Obua J, Hunt KD, Hauser MD, Clark AP (1993) The value of figs to chimpanzees. Int J Primatol 14:243–256CrossRefGoogle Scholar
  80. 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. Zool Biol 18:495–505CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2009

Authors and Affiliations

  1. 1.Laboratory of Human Evolution Studies, Division of Biological Science, Department of Zoology, Graduate School of ScienceKyoto UniversityKyotoJapan

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