Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling

Kyle H. Elliott, Maryline Le Vaillant, Akiko Kato, Anthony J. Gaston, Yan Ropert-Coudert, James F. Hare, John R. Speakman, Donald Croll

Research output: Contribution to journalArticlepeer-review

61 Citations (Scopus)


1. Energy expenditure in wild animals can be limited (i) intrinsically by physiological processes that constrain an animal’s capacity to use energy, (ii) extrinsically by energy availability
in the environment and/or (iii) strategically based on trade-offs between elevated metabolism and survival. Although these factors apply to all individuals within a population, some individuals
expend more or less energy than other individuals.
2. To examine the role of an energy ceiling in a species with a high and individually repeatable metabolic rate, we compared energy expenditure of thick-billed murres (Uria lomvia) with and without handicaps during a period of peak energy demand (chick-rearing, N = 16). We also compared energy expenditure of unencumbered birds (N = 260) across 8 years exhibiting contrasting environmental conditions and correlated energy expenditure with fitness (reproductive success and survival).
3. Murres experienced an energy ceiling mediated through behavioural adjustments. Handicapped birds decreased time spent flying/diving and chick-provisioning rates such that overall
daily energy expenditure remained unchanged across the two treatments. The energy ceiling did not reflect energy availability or trade-offs with fitness, as energy expenditure was similar
across contrasting foraging conditions and was not associated with reduced survival or increased reproductive success.
4. We found partial support for the trade-off hypothesis as older murres, where prospects for future reproduction would be relatively limited, did overcome an energy ceiling to invest more
in offspring following handicapping by reducing their own energy reserves. The ceiling therefore appeared to operate at the level of intake (i.e. digestion) rather than expenditure (i.e. thermal constraint, oxidative stress).
5. A meta-analysis comparing responses of breeding animals to handicapping suggests that our results are typical: animals either reduced investment in themselves or in their offspring to remain below an energy ceiling. Across species, whether a handicapped individual invested in its own energy stores or its offspring’s growth was not explained by life history (future vs. current reproductive potential). Many breeding animals apparently experience an intrinsic energy ceiling, and increased energy costs lead to a decline in self-maintenance and/or offspring provisioning.
Original languageEnglish
Pages (from-to)136-146
Number of pages11
JournalJournal of Animal Ecology
Issue number1
Early online date18 Dec 2013
Publication statusPublished - Jan 2014


  • device effects
  • doubly labelled water
  • energy ceiling
  • extrinsic limitation
  • intrinsic limitation
  • repeatability
  • thick-billed murre
  • Uria lomvia


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