Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T18:32:31.317Z Has data issue: false hasContentIssue false

Integrative models of nutrient balancing: application to insects and vertebrates

Published online by Cambridge University Press:  14 December 2007

D. Raubenheimer
Affiliation:
Department of Zoology and University Museum, Oxford University, South Parks Road, Oxford, OX1 3PS, UK
S. J. Simpson
Affiliation:
Department of Zoology and University Museum, Oxford University, South Parks Road, Oxford, OX1 3PS, UK
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

We present and apply to data for insects, chickens and rats a conceptual and experimental framework for studying nutrition as a multi-dimensional phenomenon. The framework enables the unification within a single geometrical model of several nutritionally relevant measures, including: the optimal balance and amounts of nutrients required by an animal in a given time (the intake target), the animal's current state in relation to these requirements, available foods, the amounts of ingested nutrients which are retained and eliminated, and animal performance. Animals given a nutritionally balanced food, or two or more imbalanced but complementary foods, can satisfy their nutrient requirements, and hence optimize performance. However, animals eating noncomplementary imbalanced foods must decide on a suitable compromise between overingesting some nutrients and underingesting others. The geometrical models provide a means of measuring nutritional targets and rules of compromise, and comparing these among different animals and within similar animals at different developmental stages or in different environments. They also provide a framework for designing and interpreting experiments on the regulatory and metabolic mechanisms underlying nutritional homeostasis.

Type
Research Article
Copyright
Copyright © The Nutrition Society 1997

References

Abisgold, J. D. & Simpson, S. J. (1988). The effect of dietary protein levels and haemolymph composition on the sensitivity of the maxillary palp chemoreceptors of locusts. Journal of Experimental Biology 135, 215230.CrossRefGoogle Scholar
Abisgold, J. D., Simpson, S. J. & Douglas, A. E. (1994). Nutrient regulation in the pea aphid Acynhosiphon pisum: application of a novel geometric framework to sugar and amino acid consumption. Physiological Entomology 19, 95102.CrossRefGoogle Scholar
Armsby, H. P. & Fries, J. A. (1915). Net energy values of feeding stuff for cattle. Journal of Agricultural Research III, 435491.Google Scholar
Belovsky, G. E. (1990). How important are nutrient constraints in optimal foraging models or are spatial/temporal factors more important? In Behavioural Mechanisms of Food Selection (NATO AS1 Series vol. 20) pp. 255278 [Hughes, R. N., editor]. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Bernays, E. A. (1997). Feeding by lepidopteran larvae is dangerous. Ecological Entomology 22, 121123.CrossRefGoogle Scholar
Bernays, E. A. & Raubenheimer, D. (1991). Dietary mixing in grasshoppers: changes in acceptability of different plant secondary compounds associated with low levels of dietary proteins. Journal of Insect Behaviour 4, 545556.CrossRefGoogle Scholar
Chambers, P. G.Raubenheimer, D. & Simpson, S. J. (1997). The rejection of nutritionally unbalanced foods by Locusra migratoria: the interaction between food nutrients and added flavours. Physiological Entomology, in press.CrossRefGoogle Scholar
Chambers, P. G., Simpson, S. J. & Raubenheimer, D. (1995). Behavioural mechanisms of nutrient balancing in Locusta rnigratoria nymphs. Animal Behaviour 50, 15131523.CrossRefGoogle Scholar
Champagne, D. E. & Bemays, E. A. (1991). Phytosterol unsuitability as a factor mediating food aversion learning in the grasshopper Schistocerca americana. Physiological Entomology 16, 391400.CrossRefGoogle Scholar
Chyb, S. & Simpson, S. J. (1990). Dietary selection in adult Locusta migratoria L. Entomologia Experimentalis et Applicata 56. 4760.CrossRefGoogle Scholar
Emmans, G. C. (1987). Growth, body composition and feed intake. World's Poultry Science 43, 208227.CrossRefGoogle Scholar
Emmans, G. C. (1991). Diet selection by animals: theory and experimental design. Proceedings of the Nutrition Society 50. 5964.CrossRefGoogle ScholarPubMed
Friggens, N. C., Hay, D. E. F. & Oldham, J. D. (1993). Interactions between major nutrients in the diet and the lactational performance of rats. British Journal of Nutrition 69, 5971.CrossRefGoogle ScholarPubMed
Hughes, R. N. (1993). Introduction. In Diet Selection: an interdisciplinary approach to foraging behaviour. pp. 19 [Hughes, R. N., editor]. Oxford: Blackwell Scientific Publications.Google Scholar
Islam, M. S.Roessingh, P., Simpson, S. J. & McCaffery, A. R. (1994). Parental effects on the behaviour and colouration of nymphs of the desert locust, Schisrocerca gregaria. Journal of Insect Physiology 40,173181.CrossRefGoogle Scholar
Kennedy, J. S. (1992). The New Anthropomorphism. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Leibowitz, S. F., Lucas, D. J.. Leibowitz, K. L. & Jhanwar, Y. S. (1991). Developmental patterns of macronutrient intake in female and male rats from weaning to maturity. Physiology & Behaviour 50, 11671174.CrossRefGoogle ScholarPubMed
McFarland, D. I. & Sibly, R. (1972). ‘Unitary drives’ revisited. Animal Behaviour 20, 548563.CrossRefGoogle ScholarPubMed
Moon, P. & Spencer, D. E. (1974). A geometry of nutrition. Journal of nutrition 104. 15351542.CrossRefGoogle ScholarPubMed
Musten, B., Peace, D. & Anderson, G. H. (1974). Food intake regulation in the weanling rat: self-selection of protein and energy. Journal of Nutrition 104, 563572.CrossRefGoogle ScholarPubMed
Parks, J. R. (1982). A Theory of Feeding and Growth of Animals. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Provenza, F. D. & Cincotta, R. P. (1993). Foraging as a self-organizational learning process: accepting adaptability at the expense of predictability. In Diet Selection; an interdisciplinary approach to foraging behaviour, pp. 78101[Hughes, R. N., editor]. Oxford: Blackwell Scientific Publications.Google Scholar
Pulliam, H. R. (1975). Diet optimization with nutrient constraints. American Naturalist 109, 765768.CrossRefGoogle Scholar
Raubenheimer, D. (1992). Tannic acid, protein, and digestible carbohydrate: dietary imbalance and nutritional compensation in the African migratory locust. Ecology 73, 10121027.CrossRefGoogle Scholar
Raubenheimer, D. (1995). Problems with ratio analysis in nutritional studies. Functional Ecology 9, 2129.CrossRefGoogle Scholar
Raubenheimer, D. & Blackshaw, J. (1994). Locusts learn to associate visual stimuli with drinking. Journal of Insect Behaviour 7, 569575.CrossRefGoogle Scholar
Raubenheimer, D. & Simpson, S. J. (1992). Analysis of covariance: an alternative to nutritional indices. Entomologia Experimentalis et Applicata 62, 221231.CrossRefGoogle Scholar
Raubenheimer, D. & Simpson, S. J. (1993). The geometry of compensatory feeding in the locust. Animal Behaviour 45, 953964.CrossRefGoogle Scholar
Raubenheimer, D. & Simpson, S. J. (1994). The analysis of nutrient budgets. Functional Ecology 8, 783791.CrossRefGoogle Scholar
Raubenheimer, D. & Simpson, S. J. (1995). Constructing nutrient budgets. Entomologia Experimentalis et Applicata 77, 99104.CrossRefGoogle Scholar
Raubenheimer, D. & Simpson, S. J. (1996). Meeting nutrient requirements: the roles of power and efficiency. Entomologia Experimentalis et Applicata 80, 6568.CrossRefGoogle Scholar
Raubenheimer, D. & Tucker, D. (1997). Associative learning in locusts: pairing of visual cues with consumption of protein and carbohydrate. Animal Behaviour, in press.CrossRefGoogle ScholarPubMed
Rogers, S. & Simpson, S. J. (1997). Experience-dependent changes in the number of chemosensitive sensillae on the mouthparts of Locusfa migratoria. Journal of Experimental Biology, in press.CrossRefGoogle Scholar
Rossiter, M. C. (1996). Incidence and consequences of inherited environmental effects. Annual Review of Entomology 27, 451476.CrossRefGoogle Scholar
Rothwell, N. J. & Stock, M. J. (1979). A role of brown adipose tissue in diet-induced thermogenesis. Nature 281, 3135.CrossRefGoogle ScholarPubMed
Rothwell, N. J. & Stock, M. J. (1983). Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour. Clinical Science 64, 1923.CrossRefGoogle Scholar
Shariatmadari, F. & Forbes, J. M. (1993). Growth and food intake responses to diets of different protein contents and a choice between diets containing two concentrations of protein in broiler and layer strains of chicken. British Poultry Science 34, 959970.CrossRefGoogle Scholar
Sibly, R. M. (1981). Strategies of digestion and defecation. In Physiological Ecology: an evolutionary approach to resource use, pp. 109139 [Townsend, C. R. and Calow, P.. editors]. Oxford: Blackwell.Google Scholar
Simmonds, M. S. J.Simpson, S. J. & Blaney, W. M. (1992). Dietary selection behaviour in Spodoptera littoralis: the effects of conditioning diet and conditioning period on neural responsiveness and selection behaviour. Journal of Experimental Biology 162, 7390.CrossRefGoogle Scholar
Simpson, S. J. (1994). Experimental support for a model in which innate taste responses contribute to regulation of salt intake by nymphs of Locusta migratoria. Journal of Insect Physiology 40, 555559.CrossRefGoogle Scholar
Simpson, S. J. & Raubenheimer, D. (1993 a). A multi-level analysis of feeding behaviour: the geomeuy of nutritional decisions. Philosophical Transacrions of the Royal Society of London B: Biological Sciences 342, 381402.Google Scholar
Simpson, S. J. & Raubenheimer, D. (1993 b). The central role of the haemolymph in the regulation of nutrient intake in insects. Physiological Entomology 18. 395403.CrossRefGoogle Scholar
Simpson, S. J. & Raubenheimer, D. (1995). The geometric analysis of feeding and nutrition: a user's guide. Journal of Insect Physiology 41, 545553.CrossRefGoogle Scholar
Simpson, S. J. & Raubenheimer, D. (1995). Feeding behaviour, sensory physiology and nutrient feedback: unifying model. Entomologia Experimentalis et Applicata 80, 5564.CrossRefGoogle Scholar
Simpson, S. J. & Raubenheimer, D. (1997). Geometric analysis of macronutrient selection in the rat. Appetite 28, 201213.CrossRefGoogle ScholarPubMed
Simpson, S. J., Raubenheimer, D. & Chambers, P. G. (1995). Nutritional homeostasis. In Regulatory Mechanisms in Insect Feeding. pp. 251278 [Chapman, R. F. and de Boer, G., editors]. New York: Chapman and Hall.CrossRefGoogle Scholar
Simpson, S. J.James, S., Simmonds, M. S. J., & Blaney, W. M. (1991). Variation in chemosensitivity and the control of dietary selection behaviour in the locust. Appetite 17, 141154.CrossRefGoogle ScholarPubMed
Simpson, S. J. & Simpson, C. L. (1992). Mechanisms controlling modulation by haemolymph amino acids of gustatory responsiveness in the locust. Journal of Experimental Biology 168, 269287.CrossRefGoogle Scholar
Simpson, S. J. & White, P. R. (1990). Associative learning and locust feeding: evidence for a “learned hunger” for protein. Animal Behaviour 40, 506513.CrossRefGoogle Scholar
Slansky, F. & Feeny, P. P. (1977). Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecological Monographs 47, 209228.CrossRefGoogle Scholar
Stephens, D. W. & Krebs, J. R. (1986). Foraging Theory. Princeton, NJ: Princeton University Press.Google Scholar
Tews, J. K., Repa, J. J. & Harper, A. E. (1992). Protein selection by rats adapted to high or moderately low levels of dietary protein. Physiology & Behavior 51, 699712.CrossRefGoogle ScholarPubMed
Theall, C. L., Wurtman, J. J. & Wurtman, R. J. (1984). Self-selection and regulation of protein:carbohydrate ratio in foods adult rats eat. Journal of Nutrition 114, 711718.CrossRefGoogle ScholarPubMed
Trier, T. M. (1996). Diet-induced thermogenesis in the prairie vole, Microtus ochrogaster. Physiological Zoology 69, 14561468.CrossRefGoogle Scholar
Trumper, S. & Simpson, S. J. (1993). Regulation of salt intake by nymphs of Locusta migratoria. Journal of Insect Physiology 39, 857864.CrossRefGoogle Scholar
Trumper, S. & Simpson, S. J. (1994). Mechanisms regulating salt intake in fifth-instar nymphs of Locusfa migratoria. Physiological Entomology 19, 203215.CrossRefGoogle Scholar
Weiner, I. H. & Stellar, E. (1951). Salt preference of the rat determined by a single-stimulus method. Journal of Comparative and Physiological Psychology 44, 394401.CrossRefGoogle ScholarPubMed
Ydenberg, R. C., Welham, C. V. J., Schmid-Hempel, R., Schmid-Hempel, P. & Beauchamp, G. (1994). Time and energy constraints and the relationships between currencies in foraging theory. Behavioural Ecology 5, 2834.CrossRefGoogle Scholar
Zanotto, F. P., Gouveia, S. M., Simpson, S. J., Raubenheimer, D. & Calder, P. (1997). Nutritional homeostasis in locusts: is there a mechanism for increased energy expenditure during carbohydrate overfeeding? Journal of Experimental Biology. in press.CrossRefGoogle Scholar
Zanotto, F. P.Raubenheimer, D. & Simpson, S. J. (1994). Selective egestion of lysine by locusts fed nutritionally unbalanced foods. Journal of Insect Physiology 40, 259265.CrossRefGoogle Scholar
Zanotto, F. P.Simpson, S. J. & Raubenheimer, D. (1993). The regulatio of growth by locusts through post-ingestive compensation for variation in the levels of dietary protein and carbohydrate. Physiological Entomology 18 425434.CrossRefGoogle Scholar