CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Australian Journal of Zoology   
Australian Journal of Zoology
Journal Banner
  Evolutionary, Molecular and Comparative Zoology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Sample Issue
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow Supplementary Series
blank image
All volumes of the Australian Journal of Zoology Supplementary Series are online and available to subscribers of Australian Journal of Zoology.

 

Article << Previous     |     Next >>   Contents Vol 59(6)

The nature of nutrition: a unifying framework

Stephen J. Simpson A C and David Raubenheimer B C

A School of Biological Sciences & The Charles Perkins Centre, The University of Sydney, Sydney, NSW 2006, Australia.
B Institute of Natural Sciences, Massey University, Albany, Private Bag 102 904, North Shore Mail Centre, Auckland, New Zealand.
C Corresponding authors. Email: stephen.simpson@sydney.edu.au; d.raubenheimer@massey.ac.nz

Australian Journal of Zoology 59(6) 350-368 http://dx.doi.org/10.1071/ZO11068
Submitted: 31 August 2011  Accepted: 18 April 2012   Published: 9 May 2012


 
 Full Text
 PDF (337 KB)
 Export Citation
 Print
  
Abstract

We present a graphical approach, which we believe can help to integrate nutrition into the broader biological sciences, and introduce generality into the applied nutritional sciences. This ‘Geometric Framework’ takes account of the fact that animals need multiple nutrients in changing amounts and balance, and that nutrients come packaged in foods that are often hard to find, dangerous to subdue and costly to process. We then show how the Geometric Framework has been used to understand the links between nutrition and relevant aspects of the biology of individual animals. These aspects include the physiological mechanisms that direct the nutritional interactions of the animal with its environment, and the fitness consequences of these interactions. Having considered the implications of diet for individuals, we show that these effects can translate into the collective behaviour of groups and societies, and in turn ramify throughout food webs to influence the structure of ecosystems.

Additional keywords: ageing, cannibalism, conservation, Geometric Framework.


References

Abisgold, J. D., Simpson, S. J., and Douglas, A. E. (1994). Nutrient regulation in the pea aphid Acyrthosiphon pisum: application of a novel geometric framework to sugar and amino acid consumption. Physiological Entomology 19, 95–102.
CrossRef | CAS |

Altmann, J., Schoeller, D., Altmann, S. A., Muruthi, P., and Sapolsky, R. M. (1993). Body size and fatness of free-living baboons reflect food availability and activity levels. American Journal of Primatology 30, 149–161.
CrossRef |

Andrew, R., Wallis, I. R., Harwood, C. E., Henson, M., and Foley, W. J. (2007). Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia 153, 891–901.
CrossRef |

Angilletta, M. J. (2009). ‘Thermal Adaptation: a Theoretical and Empirical Synthesis.’ (Oxford University Press: Oxford.)

Archer, C. R., Royle, N., South, S., Selman, C., and Hunt, J. (2009). Nutritional geometry provides food for thought. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 64A, 956–959.
CrossRef |

Aubert, A., Goodall, G., and Dantzer, R. (1995). Compared effects of cold ambient temperature and cytokines on macronutrient intake in rats. Physiology & Behavior 57, 869–873.
CrossRef | CAS |

Barker, D. J. P. (1998), ‘Mothers, Babies and Health in Later Life.’ 2nd edn. (Churchill Livingstone: London.)

Barton Browne, L. (1995). Ontogenetic changes in feeding behavior. In ‘Regulatory Mechanisms in Insect Feeding’. (Eds R. F. Chapman and G. de Boer.) pp. 307–342. (Chapman and Hall: New York.)

Bazazi, S., Buhl, J., Hale, J. J., Anstey, M. L., Sword, G. A., Simpson, S. J., and Couzin, I. D. (2008). Collective motion and cannibalism in locust migratory bands. Current Biology 18, 735–739.
CrossRef | CAS |

Bazazi, S., Romanczuk, P., Thomas, S., Schimansky-Geier, L., Hale, J. J., Miller, G. A., Sword, G. A., Simpson, S. J., and Couzin, I. D. (2011). Nutritional state and collective motion: from individuals to mass migration. Proceedings. Biological Sciences 278, 356–363.
CrossRef |

Behmer, S. T. (2009). Insect herbivore nutrient regulation. Annual Review of Entomology 54, 165–187.
CrossRef | CAS |

Behmer, S. T., Simpson, S. J., and Raubenheimer, D. (2002). Herbivore foraging strategies in chemically heterogeneous environments: allelochemical–nutrient interactions. Ecology 83, 2489–2501.
CrossRef |

Berenbaum, M. R. (1995). Turnabout is fair play: secondary roles for primary compounds. Journal of Chemical Ecology 21, 925–940.
CrossRef | CAS |

Bernays, E. A. (1993). Food aversion learning. In ‘Insect Learning’. (Eds A. C. Lewis and D. Papaj.) pp. 1–17. (Chapman and Hall: New York.)

Boersma, M., and Elser, J. J. (2006). Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87, 1325–1330.
CrossRef |

Booth, D. A., and Thibault, L. (2000). Macronutrient-specific hungers and satieties and their neural bases, learnt from pre- and postingestinal effects of eating particular foodstuffs. In ‘Neural and Metabolic Control of Macronutrient Intake’. (Eds H.-R. Berthoud and R. J. Seeley.) pp. 61–91. (CRC Press: Boca Raton, FL.)

Burke, C. J., and Waddell, S. (2011). Remembering nutrient quality of sugar in Drosophila. Current Biology 21, 746–750.
CrossRef | CAS |

Calabrese, E. J. (2005). Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environmental Pollution 138, 379–412.
CrossRef |

Calabrese, E. J., and Baldwin, L. A. (2003). Toxicology rethinks its central belief – hormesis demands a reappraisal of the way risks are assessed. Nature 421, 691–692.
CrossRef | CAS |

Calabrese, E. J., Baldwin, L. A., and Holland, C. D. (1999). Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment. Risk Analysis 19, 261–281.
CrossRef | CAS |

Carey, J. R., Harshman, L. G., Liedo, P., Müller, H.-G., Wang, J.-L., and Zhang, Z. (2008). Longevity–fertility trade-offs in the tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell 7, 470–477.
CrossRef | CAS |

Carleton, A., Accolla, R., and Simon, S. A. (2010). Coding in the mammalian gustatory system. Trends in Neurosciences 33, 326–334.
CrossRef | CAS |

Cassill, D. L., and Tschinkel, W. R. (1999). Regulation of diet in the fire ant, Solenopsis invicta. Journal of Insect Behavior 12, 307–328.
CrossRef |

Chambers, P. G., Simpson, S. J., and Raubenheimer, D. (1995). Behavioural mechanisms of nutrient balancing in Locusta migratoria. Animal Behaviour 50, 1513–1523.
CrossRef |

Chambers, P. G., Simpson, S. J., and Raubenheimer, D. (1997). The functional significance of switching interval in food mixing by Locusta migratoria. Journal of Insect Physiology 44, 77–85.
CrossRef |

Clissold, F. J., Tedder, B. J., Conigrave, A. D., and Simpson, S. J. (2010). The gastrointestinal tract as a nutrient balancing organ. Proceedings. Biological Sciences 277, 1751–1759.
CrossRef |

Coggan, N., Clissold, F. J., and Simpson, S. J. (2011). Locusts use dynamic thermoregulatory behaviour to optimise nutritional outcomes. Proceedings. Biological Sciences 278, 2745–2752.
CrossRef |

Colman, R. J., Anderson, R. M., Johnson, S. C., Kastman, E. K., Kosmatka, K. J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., and Weindruch, R. (2009). Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201–204.
CrossRef | CAS |

Cook, S. C., Eubanks, M. D., Gold, R. E., and Behmer, S. T. (2010). Colony-level macronutrient regulation in ants: mechanisms, hoarding and associated costs. Animal Behaviour 79, 429–437.
CrossRef |

Cota, D., Proulx, K., and Seeley, R. J. (2007). The role of CNS fuel sensing in energy and glucose regulation. Gastroenterology 132, 2158–2168.
CrossRef | CAS |

Cotter, S. C., Simpson, S. J., Raubenheimer, D., and Wilson, K. (2011). Macronutrient balance mediates trade-offs between immune function and life history traits. Functional Ecology 25, 186–198.
CrossRef |

Crespi, E. J., and Denver, R. J. (2006). Leptin (ob gene) of the South African clawed frog Xenopus laevis. Proceedings of the National Academy of Sciences of the United States of America 103, 10 092–10 097.
CrossRef | CAS |

Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y.-H., Doria, A., Kolodny, G. M., and Kahn, C. R. (2009). Identification and importance of brown adipose tissue in adult humans. The New England Journal of Medicine 360, 1509–1517.
CrossRef | CAS |

De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccinie, G., and Lionetti, P. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America 107, 14 691–14 696.
CrossRef |

DeAngelis, D. L., Mulholland, P. J., Palumbo, A. V., Steinmen, A. D., Huston, M. A., and Elwood, J. W. (1989). Nutrient dynamics and food-web stability. Annual Review of Ecology and Systematics 20, 71–95.
CrossRef |

Dearing, M. D., Forbey, J. S., McLister, J. D., and Santos, L. (2008). Ambient temperature influences diet selection and physiology of an herbivorous mammal, Neotoma albigula. Physiological and Biochemical Zoology 81, 891–897.
CrossRef | CAS |

Denno, R. F., and Fagan, W. F. (2003). Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84, 2522–2531.
CrossRef |

Dethier, V. G. (1976). ‘The Hungry Fly.’ (Princeton University Press: Princeton, NJ.)

Dong, D., Jones, G., and Zhang, S. (2009). Dynamic evolution of bitter taste receptor genes in vertebrates. BMC Evolutionary Biology 9, 1–9.
CrossRef |

Douglas, A. E. (2010). ‘The Symbiotic Habit.’ (Princeton University Press: Princeton, NJ.)

Dukas, R. (2008). Evolutionary biology of insect learning. Annual Review of Entomology 53, 145–160.
CrossRef | CAS |

Dussutour, A., and Simpson, S. J. (2008). Carbohydrate regulation in relation to colony growth in ants. The Journal of Experimental Biology 211, 2224–2232.
CrossRef | CAS |

Dussutour, A., and Simpson, S. J. (2009). Communal nutrition in ants. Current Biology 19, 740–744.
CrossRef | CAS |

Everitt, A. V., Rattan, S., Le Couteur, D., and de Cabo, R. (Eds) (2010). ‘Calorie Restriction, Aging, and Longevity.’ (Springer: Dordrecht.)

Fagan, W. F., and Denno, R. F. (2004). Stoichiometry of actual vs. potential predator–prey interactions: insights into nitrogen limitation for arthropod predators. Ecology Letters 7, 876–883.
CrossRef |

Fanson, B. G., and Taylor, P. W. (2011). Protein: carbohydrate ratios explain lifespan patterns found in Queensland fruit fly on diets varying in yeast : sugar ratios. Age , .
CrossRef |

Fanson, B. G., Weldon, C. W., Pérez-Staples, D., Simpson, S. J., and Taylor, P. W. (2009). Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell 8, 514–523.
CrossRef | CAS |

Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., Wallis, I. R., and Lindenmayer, D. B. (2009a). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology 20, 685–690.
CrossRef |

Felton, A. M., Felton, A., Wood, J. T., Foley, W. J., Raubenheimer, D., Wallis, I. R., and Lindenmayer, D. B. (2009b). Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. International Journal of Primatology 30, 675–696.
CrossRef |

Finger, T. E. (1997). Evolution of taste and solitary chemoreceptor cell systems. Brain, Behavior and Evolution 50, 234–243.
CrossRef | CAS |

Flatt, T. (2011). Survival costs of reproduction in Drosophila. Experimental Gerontology 46, 369–375.
CrossRef |

Fujita, M., and Tanimura, T. (2011). Drosophila evaluates and learns the nutritional value of sugars. Current Biology 21, 751–755.
CrossRef | CAS |

Galef, B. G., and Laland, K. N. (2005). Social learning in animals: empirical studies and theoretical models. Bioscience 55, 489–499.
CrossRef |

Gluckman, P. D., and Hanson, M. A. (2004). The developmental origins of the metabolic syndrome. Trends in Endocrinology and Metabolism 15, 183–187.
CrossRef | CAS |

Gluckman, P. D., and Hanson, M. A. (Eds) (2006a). ‘Developmental Origins of Health and Disease.’ (Cambridge University Press: Cambridge.)

Gluckman, P. D., and Hanson, M. A. (2006b). ‘Mismatch: why Our World No Longer Fits Our Bodies.’ (Oxford University Press: Oxford.)

Gluckman, P. D., Hanson, M. A., Bateson, P., Beedle, A. S., Law, C. M., Bhutta, Z. A., Anokhin, K. V., Bougnères, P., Chandak, G. R., Dasgupta, P., Smith, G. D., Ellison, P. T., Forrester, T., Gilbert, S. F., Jablonka, E., Kaplan, H., Prentice, A. M., Simpson, S. J., Uauy, R., and West-Eberhard, M. J. (2009). Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet 373, 1654–1657.
CrossRef |

Gosby, A. K., Conigrave, A. D., Lau, N. S., Iglesias, M. A., Hall, R. M., Jebb, S. A., Brand-Miller, J., Caterson, I. D., Raubenheimer, D., and Simpson, S. J. (2011). Testing protein leverage in lean humans: a randomised controlled experimental study. PLoS ONE 6, e25929.
CrossRef | CAS |

Grandison, R. C., Piper, M. D. W., and Partridge, L. (2009). Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061–1064.
CrossRef | CAS |

Grimm, V., and Railsback, S. F. (2005). ‘Individual-based Modeling and Ecology.’ (Princeton University Press: Princeton, NJ.)

Hansen, B. C. (2001). Causes of obesity and consequences of obesity prevention in non-human primates and other animals. In ‘International Textbook of Obesity’. (Ed. P. Björntorp.) pp. 181–201. (John Wiley and Sons: Chichester, UK.)

Hansen, M. J., Buhl, J., Bazazi, S., Simpson, S. J., and Sword, G. A. (2011). Cannibalism in the lifeboat – collective movement in Australian plague locusts. Behavioral Ecology and Sociobiology 65, 1715–1720.
CrossRef |

Hawlena, D., and Schmitz, O. J. (2010). Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proceedings of the National Academy of Sciences of the United States of America 107, 15503–15507.
CrossRef | CAS |

Hayes, D. P. (2007). Nutritional hormesis. European Journal of Clinical Nutrition 61, 147–159.
CrossRef | CAS |

Hewson-Hughes, A. K., Hewson-Hughes, V. L., Miller, A. T., Hall, S. R., Simpson, S. J., and Raubenheimer, D. (2011). Geometric analysis of macronutrient selection in the adult domestic cat, Felis catus. The Journal of Experimental Biology 214, 1039–1051.
CrossRef |

Hölldobler, B., and Wilson, E. O. (2009). ‘The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies.’ (W.W. Norton & Co.: New York.)

Houston, A., and Sumida, B. (1985). A positive feedback model for switching between two activities. Animal Behaviour 33, 315–325.
CrossRef |

Huffman, M. A. (2001). Self-medicative behavior in the African great apes: an evolutionary perspective into the origins of human traditional medicine. Bioscience 51, 651–661.
CrossRef |

Huffman, M. A. (2003). Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants. The Proceedings of the Nutrition Society 62, 371–381.
CrossRef |

Hunt, J. H., and Nalepa, C. A. (Eds) (1994). ‘Nourishment and Evolution in Insect Societies.’ (Westview Press: Boulder, CO.)

Hutchings, M. R., Athanasiadou, S., Kyriazakis, I., and Gordon, I. J. (2003). Can animals use foraging behaviour to combat parasites? The Proceedings of the Nutrition Society 62, 361–370.
CrossRef |

Hutchinson, G. E. (1957). Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 22, 415–427.
CrossRef |

Ja, W. W., Carvalho, G. B., Zid, B. M., Mak, E. M., Brummel, T., and Benzer, S. (2009). Water- and nutrient-dependent effects of dietary restriction on Drosophila lifespan. Proceedings of the National Academy of Sciences of the United States of America 106, 18 633–18 637.
CrossRef | CAS |

Jensen, K., Mayntz, D., Tøft, S., Raubenheimer, D., and Simpson, S. J. (2011). Nutrient regulation in a predator, the wolf spider Pardosa prativaga. Animal Behaviour 81, 993–999.
CrossRef |

Jensen, K., Mayntz, D., Tøft, S., Clissold, F. J., Hunt, J., Raubenheimer, D., and Simpson, S. J. (2012). Optimal foraging for specific nutrients in predatory beetles. Proceedings of the Royal Society B: Biological Sciences. 10.1098/rspb.2011.2410

Kamakura, M. (2011). Royalactin induces queen differentiation in honeybees. Nature 473, 478–483.
CrossRef | CAS |

Karban, R., and Baldwin, I. T. (1997). ‘Induced Responses to Herbivory.’ (University of Chicago Press: Chicago, IL.)

Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., and Gordon, J. I. (2011). Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336.
CrossRef | CAS |

Kearney, M. (2006). Habitat, environment and niche: what are we modelling? Oikos 115, 186–191.
CrossRef |

Kearney, M., and Porter, W. P. (2009). Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecology Letters 12, 334–350.
CrossRef |

Kearney, M., Simpson, S. J., Raubenheimer, D., and Helmuth, B. (2010). Modelling the ecological niche from functional traits. Philosophical Transactions of the Royal Society B. Biological Sciences 365, 3469–3483.
CrossRef |

Kirkwood, T. B. L. (2005). Understanding the odd science of aging. Cell 120, 437–447.
CrossRef | CAS |

Kooijman, S. A. L. M. (2009). ‘Dynamic Energy Budget Theory for Metabolic Organisation.’ (Cambridge University Press: Cambridge.)

Kuijper, L. D. J., Anderson, T. R., and Kooijman, S. A. L. M. (2004). C and N gross growth efficiencies of copepod egg production studied using a dynamic energy budget model. Journal of Plankton Research 26, 213–226.
CrossRef | CAS |

Kytö, M., Niemelä, P., and Larsson, S. (1996). Insects on trees: population and individual response to fertilization. Oikos 75, 148–159.
CrossRef |

Le Rohellec, M., and Le Bourg, É. (2009). Contrasted effects of suppressing live yeast from food on longevity, aging and resistance to several stresses in Drosophila melanogaster. Experimental Gerontology 44, 695–707.
CrossRef |

Lee, K. P., Behmer, S. T., Simpson, S. J., and Raubenheimer, D. (2002). A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology 48, 655–665.
CrossRef | CAS |

Lee, K. P., Raubenheimer, D., and Simpson, S. J. (2003). A correlation between nutrient balancing and insect host-plant range: evidence from the specialist caterpillar Spodoptera exempta. Journal of Insect Physiology 49, 1161–1171.
CrossRef | CAS |

Lee, K. P., Simpson, S. J., and Raubenheimer, D. (2004). A comparison of nutrient regulation between solitarious and gregarious phases of the specialist caterpillar, Spodoptera exempta (Walker). Journal of Insect Physiology 50, 1171–1180.
CrossRef | CAS |

Lee, K. P., Cory, J. S., Wilson, K., Raubenheimer, D., and Simpson, S. J. (2006a). Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proceedings. Biological Sciences 273, 823–829.
CrossRef | CAS |

Lee, K. P., Behmer, S. T., and Simpson, S. J. (2006b). Nutrient regulation in relation to diet breadth: a comparison of Heliothis sister species and a hybrid. The Journal of Experimental Biology 209, 2076–2084.
CrossRef | CAS |

Lee, K. P., Simpson, S. J., Clissold, F. J., Brooks, R., Ballard, J. W. O., Taylor, P. W., Soran, N., and Raubenheimer, D. (2008a). Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Sciences of the United States of America 105, 2498–2503.
CrossRef | CAS |

Lee, K. P., Simpson, S. J., and Wilson, K. (2008b). Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology 22, 1052–1061.
CrossRef |

Leibowitz, S. F., Lucas, D. J., Leibowitz, K. L., and Jhanwar, Y. S. (1991). Developmental patterns of macronutrient intake in female and male rats from weaning to maturity. Physiology & Behavior 50, 1167–1174.
CrossRef | CAS |

Lorch, P. D., Sword, G. A., Gwynne, D. T., and Anderson, G. L. (2005). Radiotelemetry reveals differences in individual movement patterns between outbreak and non-outbreak Mormon cricket populations. Ecological Entomology 30, 548–555.
CrossRef |

Lozano, G. A. (1998). Parasitic stress and self-medication. Advances in the Study of Behavior 27, 291–317.
CrossRef |

Luckey, T. D., and Stone, P. C. (1960). Hormology in nutrition. Science 132, 1891–1893.
CrossRef | CAS |

Mair, W., Piper, M. D. W., and Partridge, L. (2005). Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biology 3, e223.
CrossRef |

Maklakov, A. A., Simpson, S. J., Zajitschek, F., Hall, M. D., Dessmann, J., Clissold, F., Raubenheimer, D., Bonduriansky, R., and Brooks, R. C. (2008). Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Current Biology 18, 1062–1066.
CrossRef | CAS |

Masoro, E. J. (2005). Overview of caloric restriction and ageing. Mechanisms of Ageing and Development 126, 913–922.
CrossRef | CAS |

Mayntz, D., Raubenheimer, D., Salomon, M., Tøft, S., and Simpson, S. J. (2005). Nutrient-specific foraging in invertebrate predators. Science 307, 111–113.
CrossRef | CAS |

Mayntz, D., Nielsen, V. H., Sørensen, A., Tøft, S., Raubenheimer, D., Hejlesen, C., and Simpson, S. J. (2009). Balancing of protein and lipid intake by a mammalian carnivore, the mink, Mustela vison. Animal Behaviour 77, 349–355.
CrossRef |

McCay, C. M., Crowell, M. F., and Maynard, L. A. (1935). The effect of retarded growth upon the length of life and upon ultimate size. Journal of Nutrition 10, 63–79.
| CAS |

McMillen, C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571–633.
CrossRef | CAS |

Mertz, W. (1981). The essential trace elements. Science 213, 1332–1338.
CrossRef | CAS |

Miller, R. A., Buehner, G., Chang, Y., Harper, J. M., Sigler, R., and Smith-Wheelock, M. (2005). Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4, 119–125.
CrossRef | CAS |

Miller, G. A., Clissold, F. J., Mayntz, D., and Simpson, S. J. (2009). Speed over efficiency: locusts select body temperatures that favour growth rate over efficient nutrient utilization. Proceedings. Biological Sciences 276, 3581–3589.
CrossRef |

Morton, G. J., and Schwartz, M. W. (2011). Leptin and the central nervous system control of glucose metabolism. Physiological Reviews 91, 389–411.
CrossRef | CAS |

Musten, B., Peace, D., and Anderson, G. H. (1974). Food intake regulation in the weanling rat: self-selection of protein and energy. The Journal of Nutrition 104, 563–572.
| CAS |

Newland, P. L., and Yates, P. (2008). Nitric oxide modulates salt and sugar responses via different signaling pathways. Chemical Senses 33, 347–356.
CrossRef | CAS |

Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., and Morris, M. J. (2010). Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offsrping. Nature 467, 963–966.
CrossRef | CAS |

Nonaka, E., and Holme, P. (2007). Agent-based model approach to optimal foraging in heterogeneous landscapes: effects of patch clumpiness. Ecography 30, 777–788.
CrossRef |

O’Brien, D. M., Min, K.-J., Larsen, T., and Tatar, M. (2008). Use of stable isotopes to examine how dietary restriction extends Drosophila lifespan. Current Biology 18, R155–R156.
CrossRef | CAS |

Oom, S. P., Beecham, J. A., Legg, C. J., and Hester, A. J. (2004). Foraging in a complex environment: from foraging strategies to emergent spatial properties. Ecological Complexity 1, 299–327.
CrossRef |

Orentreich, N., Matias, J. R., DeFelice, A., and Zimmerman, J. A. (1993). Low methionine ingestion by rats extends life span. The Journal of Nutrition 123, 269–274.
| CAS |

Peck, M. D., Babcock, G. F., and Alexander, J. W. (1992). The role of protein and calorie restriction in outcome from Salmonella infection in mice. Journal of Parenteral and Enteral Nutrition 16, 561–565.
CrossRef | CAS |

Pincebourde, S., and Casas, J. (2006). Multitrophic biophysical budgets: thermal ecology of an intimate herbivore insect plant interaction. Ecological Monographs 76, 175–194.
CrossRef |

Pirk, C. W. W., Boodhoo, C., Human, H., and Nicolson, S. W. (2010). The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41, 62–72.
CrossRef | CAS |

Ponton, F., Lalubin, F., Fromont, C., Wilson, K., Behm, C., and Simpson, S. J. (2011a). Hosts use altered macronutrient intake to circumvent parasite-induced reduction in fecundity. International Journal for Parasitology 41, 43–50.
CrossRef | CAS |

Ponton, F., Wilson, K., Cotter, S. C., Raubenheimer, D., and Simpson, S. J. (2011b). Nutritional immunology: a multi-dimensional approach. PLoS Pathogens 7, e1002223.
CrossRef | CAS |

Porter, W. P., and Gates, D. M. (1969). Thermodynamic equilibria of animals with environment. Ecological Monographs 39, 227–244.
CrossRef |

Povey, S., Cotter, S. C., Simpson, S. J., Lee, K. P., and Wilson, K. (2009). Can the protein costs of bacterial resistance be offset by altered feeding behaviour? Journal of Animal Ecology 78, 437–446.
CrossRef |

Raubenheimer, D., and Bassil, K. (2007). Separate effects of macronutrient concentration and balance on plastic gut responses in locusts. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 177, 849–855.
CrossRef | CAS |

Raubenheimer, D., and Jones, S. A. (2006). Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Animal Behaviour 71, 1253–1262.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (1992). Analysis of covariance: an alternative to nutritional indices. Entomologia Experimentalis et Applicata 62, 221–231.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (1993). The geometry of compensatory feeding in the locust. Animal Behaviour 45, 953–964.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (1994). The analysis of nutrient budgets. Functional Ecology 8, 783–791.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (1995). Constructing nutrient budgets. Entomologia Experimentalis et Applicata 77, 99–104.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (1999). Integrating nutrition: a geometrical approach. Entomologia Experimentalis et Applicata 91, 67–82.
CrossRef |

Raubenheimer, D., and Simpson, S. J. (2003). Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. The Journal of Experimental Biology 206, 1669–1681.
CrossRef | CAS |

Raubenheimer, D., and Simpson, S. J. (2006). The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis 53, 100–111.

Raubenheimer, D., and Simpson, S. J. (2009). Nutritional pharmecology: doses, nutrients, toxins, and medicines. Integrative and Comparative Biology 49, 329–337.
CrossRef | CAS |

Raubenheimer, D., and Tucker, D. (1997). Associative learning by locusts: pairing of visual cues with consumption of protein and carbohydrate. Animal Behaviour 54, 1449–1459.
CrossRef |

Raubenheimer, D., Lee, K. P., and Simpson, S. J. (2005). Does Bertrand’s rule apply to macronutrients? Proceedings. Biological Sciences 272, 2429–2434.
CrossRef | CAS |

Raubenheimer, D., Mayntz, D., Simpson, S. J., and Tøft, S. (2007). Nutrient specific compensation following overwintering diapause in a generalist predatory invertebrate: implications for intraguild predations. Ecology 88, 2598–2608.
CrossRef |

Raubenheimer, D., Simpson, S. J., and Mayntz, D. (2009). Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology 23, 4–16.
CrossRef |

Ribeiro, C., and Dickson, B. J. (2010). Sex peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Current Biology 20, 1000–1005.
CrossRef | CAS |

Rodriguez, E., and Wrangham, R. (1993). Zoopharmacognosy: the use of medicinal plants by animals. In ‘Recent Advances in Phytochemistry. Phytochemical Potential of Tropical Plants. Vol. 27’. (Eds K. R. Downum, J. T. Romeo, and H. A. Stafford.) pp. 89–105. (Plenum Press: New York.)

Romano, M. D., Piatt, J. F., and Roby, D. D. (2006). Testing the junk-food hypothesis on marine birds: effects of prey type on growth and development. Waterbirds 29, 407–414.
CrossRef |

Rosen, D. A. S., and Trites, A. W. (2000). Pollock and the decline of Steller sea lions: testing the junk-food hypothesis. Canadian Journal of Zoology 78, 1243–1250.
CrossRef |

Ross, M. H. (1961). Length of life and nutrition in the rat. The Journal of Nutrition 75, 197–210.
| CAS |

Rubio, V. C., Sánchez-Vázquez, F. J., and Madrid, J. A. (2003). Macronutrient selection through postingestive signals in sea bass fed on gelatine capsules. Physiology & Behavior 78, 795–803.
CrossRef | CAS |

Sánchez-Vázquez, F. J., Yamamoto, T., Akiyama, T., Madrid, J. A., and Tabata, M. (1999). Macronutrient self-selection through demand-feeders in rainbow trout. Physiology & Behavior 66, 45–51.
CrossRef |

Schoonhoven, L. M., van Loon, J. J. A., and Dicke, M. (2005). ‘Insect–Plant Biology.’ (Oxford University Press: Oxford.)

Schwartz, S. M., Kemnitz, J. W., and Howard, C. F. (1993). Obesity in free-ranging rhesus macaques. International Journal of Obesity 17, 1–9.
| CAS |

Schwartz, M. W., Woods, S. C., Porte, D., Seeley, R. J., and Baskin, D. G. (2000). Central nervous control of food intake. Nature 404, 661–671.
| CAS |

Sclafani, A. (2000). Macronutrient-conditioned flavor preferences. In ‘Neural and Metabolic Control of Macronutrient Intake’. (Eds H.-R. Berthoud and R. J. Seeley.) pp. 93–107. (CRC Press: Boca Raton, FL.)

Shuster, S. M., Lonsdorf, E. V., Wimp, G. M., Bailey, J. K., and Whitham, T. G. (2006). Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60, 991–1003.
| CAS |

Silva, J. E. (2006). Thermogenic mechanisms and their hormonal regulation. Physiological Reviews 86, 435–464.
CrossRef | CAS |

Simpson, S. J., and Raubenheimer, D. (1993). A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philosophical Transactions of the Royal Society B. Biological Sciences 342, 381–402.
CrossRef |

Simpson, S. J., and Raubenheimer, D. (1995). The geometric analysis of feeding and nutrition: a user’s guide. Journal of Insect Physiology 41, 545–553.
CrossRef | CAS |

Simpson, S. J., and Raubenheimer, D. (1997). The geometric analysis of feeding and nutrition in the rat. Appetite 28, 201–213.
CrossRef | CAS |

Simpson, S. J., and Raubenheimer, D. (2000). The hungry locust. Advances in the Study of Behavior 29, 1–44.
CrossRef |

Simpson, S. J., and Raubenheimer, D. (2001). The geometric analysis of nutrient–allelochemical interactions: a case study using locusts. Ecology 82, 422–439.

Simpson, S. J., and Raubenheimer, D. (2005). Obesity: the protein leverage hypothesis. Obesity Reviews 6, 133–142.
CrossRef | CAS |

Simpson, S. J., and Raubenheimer, D. (2007). Caloric restriction and aging revisited: the need for a geometric analysis of the nutritional bases of aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 62, 707–713.
CrossRef |

Simpson, S. J., and Raubenheimer, D. (2009). Macronutrient balance and lifespan. Aging 1, 875–880.
| CAS |

Simpson, S. J., and Raubenheimer, D. (2012). ‘The Nature of Nutrition: a Unifying Framework from Animal Adaptation to Human Obesity.’ (Princeton University Press: Princeton, NJ.)

Simpson, S. J., and White, P. R. (1990). Associative learning and locust feeding: evidence for a ‘learned hunger’ for protein. Animal Behaviour 40, 506–513.
CrossRef |

Simpson, S. J., Raubenheimer, D., Behmer, S. T., Whitworth, A., and Wright, G. A. (2002). A comparison of nutritional regulation in solitarious and gregarious phase nymphs of the desert locust, Schistocerca gregaria. The Journal of Experimental Biology 205, 121–129.
| CAS |

Simpson, S. J., Sibly, R. M., Lee, K. P., Behmer, S. T., and Raubenheimer, D. (2004). Optimal foraging when regulating intake of multiple nutrients. Animal Behaviour 68, 1299–1311.
CrossRef |

Simpson, S. J., Sword, G. A., Lorch, P. D., and Couzin, I. D. (2006). Cannibal crickets on a forced march for protein and salt. Proceedings of the National Academy of Sciences of the United States of America 103, 4152–4156.
CrossRef | CAS |

Simpson, S. J., Raubenheimer, D., Charleston, M. A., Clissold, F. J., ARC-NZ Vegetation Function Network Herbivory Working Group. (2010). Modelling nutritional interactions: from individuals to communities. Trends in Ecology & Evolution 25, 53–60.
CrossRef |

Skorupa, D. A., Dervisefendic, A., Zwiener, J., and Pletcher, S. D. (2008). Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7, 478–490.
CrossRef | CAS |

Slansky, F. (1992). Allelochemical–nutrient interactions in herbivore nutritional ecology. In ‘Herbivores: Their Interaction with Secondary Plant Metabolites’. (Eds G. A. Rosenthal and M. R. Berenbaum.) pp. 135–174. (Academic Press: New York.)

Smith, V. H., and Holt, R. D. (1996). Resource competition and within-host disease dynamics. Trends in Ecology & Evolution 11, 386–389.
CrossRef | CAS |

Sørensen, A., Mayntz, D., Simpson, S. J., and Raubenheimer, D. (2010). Dietary ratio of protein to carbohydrate induces plastic responses in the gastrointestinal tract of mice. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 180, 259–266.
CrossRef |

Sotka, E. E., Forbey, J., Horn, M., Poore, A., Raubenheimer, D., and Whalen, K. (2009). The emerging role of pharmacology in understanding marine and freshwater consumer–prey interactions. Integrative and Comparative Biology 49, 291–313.
CrossRef | CAS |

Sousa, T., Domingos, T., and Kooijman, S. A. L. M. (2008). From empirical patterns to theory: a formal metabolic theory of life. Philosophical Transactions of the Royal Society B. Biological Sciences 363, 2453–2464.
CrossRef |

South, S. H., House, C. M., Moore, A. J., Simpson, S. J., and Hunt, J. (2011). Male cockroaches prefer a high carbohydrate diet that makes them more attractive to females: implications for the study of condition-dependence. Evolution 65, 1594–1606.
CrossRef | CAS |

Stephens, D. W., and Krebs, J. R. (1986). ‘Foraging Theory.’ (Princeton University Press: Princeton, NJ.)

Stephens, D. W., Brown, J. S., and Ydenberg, R. C. (2007). ‘Foraging: Behavior and Ecology.’ (The University of Chicago Press: Chicago, IL.)

Sterner, R. W., and Elser, J. J. (2002). ‘Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere.’ (Princeton University Press: Princeton, NJ.)

Sterner, R. W., Elser, J. J., Chrzanowski, T. H., Schampel, J. H., and George, N. B. (1996). Biogeochemistry and trophic ecology: a new food web diagram. In ‘Food Webs: Integration of Patterns and Dynamics’. (Eds G. A. Polis and K. O. Winemiller.) pp. 72–80. (Chapman and Hall: New York.)

Stock, M. J. (1999). Gluttony and thermogenesis revisited. International Journal of Obesity 23, 1105–1117.
CrossRef | CAS |

Sword, G. A., Lorch, P. D., and Gwynne, D. T. (2005). Migratory bands give crickets protection. Nature 433, 703.
CrossRef | CAS |

Tatar, M. (2007). Diet restriction in Drosophila melanogaster. In ‘Mechanisms of Dietary Restriction in Aging and Disease’. (Eds C. V. Mobbs, K. Yen, and P. R. Hof.) pp. 115–136. (Karger: Basel.)

Tatar, M. (2011). The plate half-full: status of research on the mechanisms of dietary restriction in Drosophila melanogaster. Experimental Gerontology 46, 363–368.
CrossRef | CAS |

Tilman, D. (1982). ‘Resource Competition and Community Structure.’ (Princeton University Press: Princeton, NJ.)

Tomé, D. (2004). Protein, amino acids and the control of food intake. The British Journal of Nutrition 92, S27–S30.
CrossRef |

Torregrossa, A.-M., and Dearing, D. (2009). Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Functional Ecology 23, 48–56.
CrossRef |

Touzani, K., and Sclafani, A. (2005). Critical role of amygdala in flavor but not taste preference learning in rats. The European Journal of Neuroscience 22, 1767–1774.
CrossRef |

Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., and Gordon, G. I. (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine 1, 6–14.

Vargas, M. A., Luo, N., Yamaguchi, A., and Kapahi, P. (2010). A role for S6 kinase and serotonin in postmating dietary switch and balance of nutrients in D. melanogaster. Current Biology 20, 1006–1011.
CrossRef | CAS |

Vigne, P., and Frelin, C. (2010). Hypoxia modifies the feeding preferences of Drosophila. Consequences for diet dependent hypoxic survival. BMC Physiology 10, 1–9.
CrossRef |

Villalba, J. J., and Provenza, F. D. (2007). Self-medication and homeostatic behaviour in herbivores: learning about the benefits of nature’s pharmacy. Animal 1, 1360–1370.
CrossRef | CAS |

Warbrick-Smith, J., Behmer, S. T., Lee, K. P., Raubenheimer, D., and Simpson, S. J. (2006). Evolving resistance to obesity in an insect. Proceedings of the National Academy of Sciences of the United States of America 103, 14 045–14 049.
CrossRef | CAS |

Weindruch, R., and Walford, R. L. (1988). ‘The Retardation of Aging and Disease by Dietary Restriction.’ (Charles C. Thomas: Springfield, IL.)

White, T. C. R. (1983). ‘The Inadequate Environment: Nitrogen and the Abundance of Animals.’ (Springer: Berlin.)

Wilder, S. M., and Eubanks, M. D. (2010). Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 91, 3114–3117.
CrossRef |

Withers, P. C., and Cooper, C. E. (2010). Metabolic depression: a historical perspective. In ‘Aestivation: molecular and Physiological Aspects. Progress in Molecular and Subcellular Biology. Vol. 49’. (Eds C. A. Navas and J. E. Carvalho.) pp. 1–23. (Springer: Berlin.)

Yarmolinsky, D. A., Zuker, C. S., and Ryba, N. J. (2009). Common sense about taste: from mammals to insects. Cell 139, 234–244.
CrossRef | CAS |

Zanotto, F. P., Simpson, S. J., and Raubenheimer, D. (1993). The regulation of growth by locusts through post-ingestive compensation for variation in the levels of dietary protein and carbohydrate. Physiological Entomology 18, 425–434.
CrossRef |

Zanotto, F. P., Gouveia, S. M., Simpson, S. J., Raubenheimer, D., and Calder, P. C. (1997). Nutritional homeostasis in locusts: is there a mechanism for increased energy expenditure during carbohydrate overfeeding? The Journal of Experimental Biology 200, 2437–2448.

Zera, A. J., and Harshman, L. G. (2001). The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 32, 95–126.
CrossRef |

Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.
CrossRef | CAS |

Zimmerman, J. A., Malloy, V., Krajcik, R., and Orentreich, N. (2003). Nutritional control of aging. Experimental Gerontology 38, 47–52.
CrossRef | CAS |


   
 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014