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Oecologia

, Volume 177, Issue 1, pp 223–234 | Cite as

Geometry of nutrition in field studies: an illustration using wild primates

  • David RaubenheimerEmail author
  • Gabriel E. Machovsky-Capuska
  • Colin A. Chapman
  • Jessica M. Rothman
Physiological ecology - Original research

Abstract

Nutritional geometry has shown the benefits of viewing nutrition in a multidimensional context, in which foraging is viewed as a process of balancing the intake and use of multiple nutrients. New insights into nutrient regulation have been generated in studies performed in a laboratory context, where accurate measures of amounts (e.g. eaten, converted to body mass, excreted) can be made and analysed using amounts-based nutritional geometry. In most field situations, however, proportional compositions (e.g. of foods, diets, faeces) are the only measures readily available, and in some cases are more relevant to the problem at hand. For this reason, a complementary geometric method was recently introduced for analysing multi-dimensional data on proportional compositions in nutritional studies, called the right-angled mixture triangle (RMT). We use literature data from field studies of primates to demonstrate how the RMT can provide insight into a variety of important concepts in nutritional ecology. We first compare the compositions of foods, using as an example primate milks collected in both the wild and the laboratory. We next compare the diets of different species of primates from the same habitat and of the same species (mountain gorillas) from two distinct forests. Subsequently, we model the relationships between the composition of gorilla diets in these two habitats and the foods that comprise these diets, showing how such analyses can provide evidence for active nutrient-specific regulation in a field context. We provide a framework to relate concepts developed in laboratory studies with field-based studies of nutrition.

Keywords

Nutritional ecology Nutritional geometry Mixture triangles Primates Gorillas 

Notes

Acknowledgments

We are grateful to Dr Alistair Senior for assistance with the comparative analysis of primate milk compositions. This research was partially funded by Faculty of Veterinary Science Research Fund, The University of Sydney. D.R. is part-funded by Gravida, The National Research Centre for Growth and Development, New Zealand.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer, BerlinCrossRefGoogle Scholar
  2. Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Natl Acad Sci USA 105:1977–1982PubMedCentralPubMedCrossRefGoogle Scholar
  3. Blumfield M, Hure A, Macdonald-Wicks LK, Smith R, Simpson SJ, Raubenheimer D, Collins C (2012) The association between the macronutrient content of maternal diet, adequacy of micronutrients during pregnancy. Nutrients 4:1958–1976PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bowen SH, Lutz EV, Ahlgren MO (1995) Dietary protein and energy as determinants of food quality: trophic strategies compared. Ecology 76:899–907CrossRefGoogle Scholar
  5. Bryer MAH, Chapman CA, Rothman JM (2013) Diet and polyspecific associations affect spatial patterns among redtail monkeys (Cercopithecus ascanius). Behaviour 150:277–293Google Scholar
  6. Chambers PG, Simpson SJ, Raubenheimer D (1995) Behavioural mechanisms of nutrient balancing in Locusta migratoria. Anim Behav 50:1513–1523CrossRefGoogle Scholar
  7. Conklin-Brittain NL, Wrangham RW, Hunt KD (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II: macronutrients. Int J Primatol 19:971–998CrossRefGoogle Scholar
  8. Dearing MD, Schall JJ (1992) Testing models of optimal diet assembly by the generalist herbivorous lizard Cnemidophorus murinus. Ecology 73:845–858CrossRefGoogle Scholar
  9. DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, Wallis IR, Johnson CN, Foley WJ (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. doi: 10.1111/j.1600-0706.2013.00727.x CrossRefGoogle Scholar
  10. Despland E, Noseworthy M (2006) How well do specialist feeders regulate nutrient intake? Evidence from a gregarious tree-feeding caterpillar. J Exp Biol 209:1301–1309PubMedCrossRefGoogle Scholar
  11. Erlenbach JA, Rode KD, Raubenheimer D, Robbins CT (2014) Macronutrient optimization and energy maximization determine diets of brown bears. J Mammal 95:160–168CrossRefGoogle Scholar
  12. Fagan WF, Siemann E, Denno RF, Mitter C, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802PubMedCrossRefGoogle Scholar
  13. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT, Wallis IR, Lindenmayer DB (2009a) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20:685–690CrossRefGoogle Scholar
  14. Felton AM, Felton A, Wood JT, Foley WJ, Raubenheimer D, Wallis IR, Lindenmayer DB (2009b) Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. Int J Primatol 30:675–696CrossRefGoogle Scholar
  15. Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, Mcneilage A (2004) Dietary variability of mountain gorillas in Bwindi impenetrable national park, Uganda. Int J Primatol 25:1043–1072CrossRefGoogle Scholar
  16. Giri S, Aryal A, Koirala RK, Adhikari B, Raubenheimer D (2011) Feeding ecology and distribution of Himalayan serow (Capricornis thar) in Annapurna conservation area. Nepal World J Zool 6:80–85Google Scholar
  17. Gosby AK, Conigrave AD, Lau NS, Iglesias MA, Hall RM, Jebb SA, Brand-Miller JI, Caterson D, Raubenheimer D, Simpson SJ (2011) Testing protein leverage in lean humans: a randomised controlled experimental study. PLoS ONE 6:e25929PubMedCentralPubMedCrossRefGoogle Scholar
  18. Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23:494–508Google Scholar
  19. Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556PubMedCrossRefGoogle Scholar
  20. 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 214:1039–1051PubMedCrossRefGoogle Scholar
  21. Hewson-Hughes AK, Hewson-Hughes VL, Colyer A, Miller AT, Hall SR, Raubenheimer D, Simpson SJ (2012) Consistent proportional macronutrient intake selected by adult domestic cats (Felis catus), despite variations in dietary macronutrient and moisture content of foods offered. J Comp Physiol B, pp 1–12Google Scholar
  22. Hewson-Hughes AK, Hewson-Hughes VL, Colyer A, Miller AT, McGrane SJ, Hall SR, Butterwick RF, Simpson S (2013) Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris. Behav Ecol 24:293–304PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthr 20:9–23CrossRefGoogle Scholar
  24. Hyslop EJ (1980) Stomach contents analysis––a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  25. Jensen K, Mayntz D, Toft S, Clissold FJ, Hunt J, Raubenheimer D, Simpson SJ (2012) Optimal foraging for specific nutrients in predatory beetles. Proc R Soc Lond B 279:2212–2218CrossRefGoogle Scholar
  26. Johnson CA, Raubenheimer D, Rothman JM, Clarke D, Swedell L (2013) 30 Days in the life: daily nutrient balancing in a wild chacma baboon. PLoS ONE 8:e70383. doi: 10.1371/journal.pone.0070383 PubMedCentralPubMedCrossRefGoogle Scholar
  27. Kamler JF, Pope KL (2001) nonlethal methods of examining fish stomach contents. Rev Fish Sci 9:1–11CrossRefGoogle Scholar
  28. Kearney M, Simpson SJ, Raubenheimer D, Helmuth B (2010) Modelling the ecological niche from functional traits. Philos Trans R Soc Lond B 365:3469–3483CrossRefGoogle Scholar
  29. Kearney MR, Simpson SJ, Raubenheimer D, Kooijman SALM (2012) Balancing heat, water and nutrients under environmental change: a thermodynamic niche framework. Funct Ecol 4:950–966Google Scholar
  30. Klare U, Kamler JF, Macdonald DW (2011) A comparison and critique of different scat-analysis methods for determining carnivore diet. Mammal Rev 41:294–312CrossRefGoogle Scholar
  31. Lambert, JE (2010) Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder S (eds) Primates in Perspective, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  32. Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JWO, Taylor PW, Soran N, Raubenheimer D (2008) Lifespan and reproduction in drosophila: new insights from nutritional geometry. Proc Natl Acad Sci USA 105:2498–2503PubMedCentralPubMedCrossRefGoogle Scholar
  33. Machovsky-Capuska GE, Dwyer SL, Alley MR, Stockin KA, Raubenheimer D (2011) Evidence for fatal collisions and kleptoparasitism while plunge diving in Gannets. Ibis 153:631–635CrossRefGoogle Scholar
  34. Maklakov AA, Hall MD, Simpson SJ, Dessmann J, Clissold FJ, Zajitschek F, Lailvaux SP, Raubenheimer D, Bonduriansky R, Brooks RC (2009) Sex differences in nutrient-dependent reproductive ageing. Aging Cell 8:324–330PubMedCrossRefGoogle Scholar
  35. Milligan LA (2010) Milk composition of captive tufted capuchins (Cebus apella). Am J Primatol 72:81–86PubMedCrossRefGoogle Scholar
  36. National Research Council (2003) Nutrient requirements of nonhuman primates, 2nd edn. National Academic Press, WashingtonGoogle Scholar
  37. Nie Y, Zhang Z, Raubenheimer D, Elser JJ, Wei W, Wei F (2014) Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Funct Ecol. doi: 10.1111/1365-2435.12302 Google Scholar
  38. Paddack MJ, Cowen RK, Sponaugle S (2006) Grazing pressure of herbivorous coral reef fishes on low coral-cover reefs. Coral Reefs 25:461–472CrossRefGoogle Scholar
  39. Panthi S, Aryal A, Lord J, Adhikari B, Raubenheimer D (2012) Summer diet and habitat ecology of red panda (Ailurus fulgens fulgens) in Dhopatan hunting reserve. Nepal Zool Stud 51:701–709Google Scholar
  40. Parker KL (2003) Advances in the nutritional ecology of cervids at different scales. Ecoscience 10:395–411Google Scholar
  41. Petry MV, Fonseca VSD, Scherer AL (2007) Analysis of stomach contents from the black-browed albatross, Thalassarche melanophris, on the coast of Rio grande do sul, southern brazil. Polar Biol 30:321–325CrossRefGoogle Scholar
  42. Plumptre AJ (1995) The chemical composition of montane plants and its influence on the diet of large mammalian herbivores in the Pare National des Volcans, Rwanda. J Zool 235:323–337CrossRefGoogle Scholar
  43. Power ML, Verona C, Ruiz-Miranda CE, Oftedal OT (2008) The composition of milk from free-living common marmosets (Callithrix jacchus) in Brazil. Am J Primatol 70:78–83PubMedCrossRefGoogle Scholar
  44. Raubenheimer D (2011) Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecol Monogr 81:407–427CrossRefGoogle Scholar
  45. Raubenheimer D, Jones SA (2006) Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Anim Behav 71:1253–1262CrossRefGoogle Scholar
  46. Raubenheimer D, Rothman JM (2013) The nutritional ecology of entomophagy in humans and other primates. Annu Rev Entomol 58:141–160PubMedCrossRefGoogle Scholar
  47. Raubenheimer D, Simpson SJ (1993) The geometry of compensatory feeding in the locust. Anim Behav 45:953–964CrossRefGoogle Scholar
  48. Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10:151–179PubMedCrossRefGoogle Scholar
  49. Raubenheimer D, Simpson SJ (2006) The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis 53:100–111Google Scholar
  50. Raubenheimer D, Mayntz D, Simpson SJ, Toft S (2007) Nutrient-specific compensation following overwintering diapause in a generalist predatory invertebrate: implications for intraguild predation. Ecology 88:2598–2608PubMedCrossRefGoogle Scholar
  51. Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct Ecol 23:4–16CrossRefGoogle Scholar
  52. Raubenheimer D, Simpson SJ, Tait AH (2012) Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation. Philos Trans R Soc Lond B 367:1628–1646CrossRefGoogle Scholar
  53. Raubenheimer D, Machovsky-Capuska GE, Gosby AK, Simpson S (2014) The nutritional ecology of obesity: from humans to companion animals. Br J Nutr. doi: 10.1017/S0007114514002323 Google Scholar
  54. Remis MJ (2000) Initial studies on the contributions of body size and gastrointestinal passage rates to dietary flexibility among gorillas. Am J Phys Anthropol 112:171–180PubMedCrossRefGoogle Scholar
  55. Remis MJ, Dierenfeld ES (2004) Digesta passage, digestibility and behavior in captive gorillas under two dietary regimens. Int J Primatol 25:825–845CrossRefGoogle Scholar
  56. Robbins CT, Fortin JK, Rode KD, Farley SD, Shipley LA, Felicetti LA (2007) Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos 116:1675–1682CrossRefGoogle Scholar
  57. Rode KD, Chapman CA, Mcdowell LR, Stickler C (2006) Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica 38:625–634CrossRefGoogle Scholar
  58. Rothman JM, Dierenfeld ES, Molina DO, Shaw AV, Hintz HF, Pell AN (2006) Nutritional chemistry of foods eaten by gorillas in Bwindi impenetrable national park, Uganda. Am J Primatol 68:675–691PubMedCrossRefGoogle Scholar
  59. Rothman JM, Plumptre AJ, Dierenfeld ES, Pell AN (2007) Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. J Trop Ecol 23:673–682CrossRefGoogle Scholar
  60. Rothman JM, Dierenfeld ES, Hintz HF, Pell AN (2008) Nutritional quality of gorilla diets: consequences of age, sex, and season. Oecologia 155:111–122PubMedCrossRefGoogle Scholar
  61. Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol Lett 7:847–849PubMedCentralPubMedCrossRefGoogle Scholar
  62. Ruohonen K, Simpson SJ, Raubenheimer D (2007) A new approach to diet optimisation: a re-analysis using European whitefish (Coregonus lavaretus). Aquaculture 267:147–156CrossRefGoogle Scholar
  63. Saravanan S, Schrama JW, Figueiredo-Silva AC, Kaushik SJ, Verreth JAJ, Geurden I (2012) Constraints on Energy Intake in Fish: the Link between Diet Composition, Energy Metabolism, and Energy Intake in Rainbow Trout. PLoS ONE 7:e34743PubMedCentralPubMedCrossRefGoogle Scholar
  64. Schuckard R, Melville D, Cook W, Machovsky-Capuska GE (2012) Diet of the Australasian gannet (Morus serrator) at Farewell Spit, New Zealand. Notornis 59:66–70Google Scholar
  65. Shrader AM, Owen-Smith N, Ogutu JO (2006) How a mega-grazer copes with the dry season: food, nutrient intake rates by white rhinoceros in the wild. Funct Ecol 20:376–384CrossRefGoogle Scholar
  66. Simpson SJ, Raubenheimer D (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond B 342:381–402CrossRefGoogle Scholar
  67. Simpson SJ, Raubenheimer D (1997) The geometric analysis of macronutrient selection in the rat. Appetite 28:201–213PubMedCrossRefGoogle Scholar
  68. Simpson SJ, Raubenheimer D (2005) Obesity: the protein leverage hypothesis. Obes Rev 6:133–142PubMedCrossRefGoogle Scholar
  69. Simpson SJ, Raubenheimer D (2010) The nutritional geometry of aging. Springer, BerlinGoogle Scholar
  70. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, PrincetonGoogle Scholar
  71. Simpson SJ, Batley R, Raubenheimer D (2003) Geometric analysis of macronutrient intake in humans: the power of protein? Appetite 41:123–140PubMedCrossRefGoogle Scholar
  72. Simpson SJ, Raubenheimer D, Charleston MA, Clissold FJ (2010) Modelling nutritional interactions: from individuals to communities. Trends Ecol Evol 25:53–60PubMedCrossRefGoogle Scholar
  73. Skibiel AL, Downing LM, Orr TJ, Hood WR (2013) The evolution of the nutrient composition of mammalian milks. J Anim Ecol 82:1254–1264PubMedCrossRefGoogle Scholar
  74. Solon-Biet SM, Aisling CM, Ballard JWO, Ruohonen K, Wu LE, Cogger VC, Warren A (2014) The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab 19:418–430PubMedCrossRefGoogle Scholar
  75. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  76. Tait A, Raubenheimer D, Stockin KA, Merriman M, Machovsky-Capuska GE (2014) Nutritional geometry of gannets and the challenges in field studies. Mar Biol 12:2791–2801. doi: 10.1007/s00227-014-2544-1 CrossRefGoogle Scholar
  77. Van Soest PJ (1994) Nutritional ecology of the ruminant. Cornell University Press, IthacaGoogle Scholar
  78. Westoby M (1974) An analysis of diet selection by large generalist herbivores. Am Nat 108:290–304CrossRefGoogle Scholar
  79. Whittier CA, Milligan LA, Nutter FB, Cranfield MR, Power ML (2010) Proximate composition of milk from free-ranging mountain gorillas (Gorilla beringei beringei). Zool Biol 29:1–10Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • David Raubenheimer
    • 1
    Email author
  • Gabriel E. Machovsky-Capuska
    • 1
  • Colin A. Chapman
    • 2
    • 3
  • Jessica M. Rothman
    • 4
    • 5
  1. 1.Faculty of Veterinary Science, The Charles Perkins Centre, School of Biological SciencesUniversity of SydneySydneyAustralia
  2. 2.Department of Anthropology McGill School of EnvironmentMcGill UniversityMontrealCanada
  3. 3.Wildlife Conservation SocietyNew YorkUSA
  4. 4.Department of AnthropologyHunter College of the City University of New YorkNew YorkUSA
  5. 5.New York Consortium of Evolutionary PrimatologyNew YorkUSA

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