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 journalArticle

50 Citations (Scopus)

Abstract

Summary
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
Volume83
Issue number1
Early online date18 Dec 2013
DOIs
Publication statusPublished - Jan 2014

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energy expenditure
expenditure
bird
birds
energy
energy costs
animal breeding
animal
chicks
fitness
breeding
wild animals
meta-analysis
reproductive potential
animals
oxidative stress
rearing
flight
diving
digestion

Keywords

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

Cite this

Elliott, K. H., Le Vaillant, M., Kato, A., Gaston, A. J., Ropert-Coudert, Y., Hare, J. F., ... Croll, D. (2014). Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling. Journal of Animal Ecology, 83(1), 136-146. https://doi.org/10.1111/1365-2656.12126

Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling. / Elliott, Kyle H.; Le Vaillant, Maryline; Kato, Akiko; Gaston, Anthony J.; Ropert-Coudert, Yan; Hare, James F.; Speakman, John R.; Croll, Donald.

In: Journal of Animal Ecology, Vol. 83, No. 1, 01.2014, p. 136-146.

Research output: Contribution to journalArticle

Elliott, KH, Le Vaillant, M, Kato, A, Gaston, AJ, Ropert-Coudert, Y, Hare, JF, Speakman, JR & Croll, D 2014, 'Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling', Journal of Animal Ecology, vol. 83, no. 1, pp. 136-146. https://doi.org/10.1111/1365-2656.12126
Elliott, Kyle H. ; Le Vaillant, Maryline ; Kato, Akiko ; Gaston, Anthony J. ; Ropert-Coudert, Yan ; Hare, James F. ; Speakman, John R. ; Croll, Donald. / Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling. In: Journal of Animal Ecology. 2014 ; Vol. 83, No. 1. pp. 136-146.
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abstract = "Summary1. 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 availabilityin 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 individualsexpend 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 overalldaily 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 similaracross 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 morein 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.",
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author = "Elliott, {Kyle H.} and {Le Vaillant}, Maryline and Akiko Kato and Gaston, {Anthony J.} and Yan Ropert-Coudert and Hare, {James F.} and Speakman, {John R.} and Donald Croll",
note = "Acknowledgements We thank our field companions (2006: K. Ashbrook, M. Barrueto, J. Nakoolak, P. Redman, P. Woodward; 2009: J. Nakoolak, J. Provencher, P. Smith and K. Woo; other years: B. Addison, A. Hargreaves, M. Hipfner, G. Langston, S. Jacobs, A. Moody, J. Nakoolak, J. Provencher, A. Ronston, K. Woo), G. Anderson, J. Green, T. Williams and two anonymous reviewers for insightful comments and J. Akearok, C. Eberl and M. Mallory (Environment Canada) and R. Armstrong (Nunavut Research Institute) for assistance with logistics. The study is part of KHE’s PhD thesis, and he benefitted from input by committee members G. Anderson, J. Anderson, K. Campbell and F. Schweizer. P Redman and P.J. Thomson provided technical support for the isotope analyses. Financial support came from Environment Canada, JFH’s NSERC Discovery Grant, the Polar Continental Shelf Project Natural Resources Canada), the Northern Contaminants Programme (Indian Affairs and Northern Development Canada), the Frank Chapman Fund (American Museum of Natural History), the Taverner and James Baillie Awards (Bird Studies Canada/Society of Canadian Ornithologists), a Sigma Xi grant-in-aid of research, the Animal Behaviour Society and American Ornithologists’ Union Research Grants, the Northern Scientific Training Program and the Fondation Prince Albert II de Monaco. KHE was supported by an NSERC Vanier Scholarship, a Garfield Weston Northern Studies Award and the Jennifer Robinson Scholarship (Arctic Institute of North America). MLV was supported by a CNRS and the Fondation des Treilles grant.",
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T1 - Age-related variation in energy expenditure in a longlived bird within the envelope of an energy ceiling

AU - Elliott, Kyle H.

AU - Le Vaillant, Maryline

AU - Kato, Akiko

AU - Gaston, Anthony J.

AU - Ropert-Coudert, Yan

AU - Hare, James F.

AU - Speakman, John R.

AU - Croll, Donald

N1 - Acknowledgements We thank our field companions (2006: K. Ashbrook, M. Barrueto, J. Nakoolak, P. Redman, P. Woodward; 2009: J. Nakoolak, J. Provencher, P. Smith and K. Woo; other years: B. Addison, A. Hargreaves, M. Hipfner, G. Langston, S. Jacobs, A. Moody, J. Nakoolak, J. Provencher, A. Ronston, K. Woo), G. Anderson, J. Green, T. Williams and two anonymous reviewers for insightful comments and J. Akearok, C. Eberl and M. Mallory (Environment Canada) and R. Armstrong (Nunavut Research Institute) for assistance with logistics. The study is part of KHE’s PhD thesis, and he benefitted from input by committee members G. Anderson, J. Anderson, K. Campbell and F. Schweizer. P Redman and P.J. Thomson provided technical support for the isotope analyses. Financial support came from Environment Canada, JFH’s NSERC Discovery Grant, the Polar Continental Shelf Project Natural Resources Canada), the Northern Contaminants Programme (Indian Affairs and Northern Development Canada), the Frank Chapman Fund (American Museum of Natural History), the Taverner and James Baillie Awards (Bird Studies Canada/Society of Canadian Ornithologists), a Sigma Xi grant-in-aid of research, the Animal Behaviour Society and American Ornithologists’ Union Research Grants, the Northern Scientific Training Program and the Fondation Prince Albert II de Monaco. KHE was supported by an NSERC Vanier Scholarship, a Garfield Weston Northern Studies Award and the Jennifer Robinson Scholarship (Arctic Institute of North America). MLV was supported by a CNRS and the Fondation des Treilles grant.

PY - 2014/1

Y1 - 2014/1

N2 - Summary1. 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 availabilityin 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 individualsexpend 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 overalldaily 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 similaracross 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 morein 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.

AB - Summary1. 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 availabilityin 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 individualsexpend 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 overalldaily 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 similaracross 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 morein 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.

KW - device effects

KW - doubly labelled water

KW - energy ceiling

KW - extrinsic limitation

KW - intrinsic limitation

KW - repeatability

KW - thick-billed murre

KW - Uria lomvia

U2 - 10.1111/1365-2656.12126

DO - 10.1111/1365-2656.12126

M3 - Article

VL - 83

SP - 136

EP - 146

JO - Journal of Animal Ecology

JF - Journal of Animal Ecology

SN - 0021-8790

IS - 1

ER -