Limits to sustained energy intake. XIII. Recent progress and future perspectives

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Abstract

Several theories have been proposed to explain limits on the maximum rate at which animals can ingest and expend energy. These limits are likely to be intrinsic to the animal, and potentially include the capacity of the alimentary tract to assimilate energy - the 'central limitation' hypothesis. Experimental evidence from lactating mice exposed to different ambient temperatures allows us to reject this and similar ideas. Two alternative ideas have been proposed. The 'peripheral limitation' hypothesis suggests that the maximal sustained energy intake reflects the summed demands of individual tissues, which have their own intrinsic limitations on capacity. In contrast, the 'heat dissipation limit' (HDL) theory suggests that animals are constrained by the maximal capacity to dissipate body heat. Abundant evidence in domesticated livestock supports the HDL theory, but data from smaller mammals are less conclusive. Here, we develop a novel framework showing how the HDL and peripheral limitations are likely to be important in all animals, but to different extents. The HDL theory makes a number of predictions - in particular that there is no fixed limit on sustained energy expenditure as a multiple of basal metabolic rate, but rather that the maximum sustained scope is positively correlated with the capacity to dissipate heat.

Original languageEnglish
Pages (from-to)230-241
Number of pages12
JournalJournal of Experimental Biology
Volume214
Issue number2
DOIs
Publication statusPublished - 1 Jan 2011

Bibliographical note

We are grateful to Hans Hoppeler and Raul Suarez for the invitation to attend the conference on ‘The Biology of Energy Expenditure’ held at Murren, enlightening discussions at the meeting with colleagues, and for the support from The Company of Biologists to attend this meeting. The HDL theory has grown from many interesting discussions with colleagues including Don Thomas, Henk Visser, Simon Verhulst, Serge Daan, Lobke Vaanholt, Colin Selman, Kim Hammond, Teresa Valencak, Thomas Ruf, Pawel Koteja, Marek Konarzewski, Zhijun Zhao and Dehua Wang. Our work on energetics of lactation has been funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC grant BB/C504794/1), Natural Environmental Research Council (NERC grant NE/C004159/1) and the Royal Society (International Joint Project JP071172). We are grateful to the numerous honours, Erasmus exchange, masters and PhD students and postdoctoral fellows that have worked on these projects. We also thank two anonymous reviewers for their extensive comments on earlier drafts of the article.

Keywords

  • Central limitation
  • Heat dissipation limit theory
  • Heat transfer
  • Lactation
  • Metabolic theory of ecology
  • Milk production
  • Peripheral limitation
  • Sustained energy expenditure
  • Sustained metabolic scope

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