Fat storage influences fasting endurance more than body size in an ungulate

L. Monica Trondrud; Gabriel Pigeon; Elżbieta Król; Steve Albon; Alina L. Evans; Walter Arnold; Catherine Hambly; R. Justin Irvine; Erik Ropstad; Audun Stien; Vebjørn Veiberg; John R. Speakman; Leif Egil Loe

doi:10.1111/1365-2435.13816

Fat storage influences fasting endurance more than body size in an ungulate

L. Monica Trondrud^*, Gabriel Pigeon, Elżbieta Król, Steve Albon, Alina L. Evans, Walter Arnold, Catherine Hambly, R. Justin Irvine, Erik Ropstad, Audun Stien, Vebjørn Veiberg, John R. Speakman^*, Leif Egil Loe

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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4 Downloads (Pure)

Abstract

The fasting endurance hypothesis (FEH) predicts strong selection for large body size in mammals living in environments where food supply is interrupted over prolonged periods of time. The Arctic is a highly seasonal and food‐restricted environment, but contrary to predictions from the FEH, empirical evidence shows that Arctic mammals are often smaller than their temperate conspecifics. Intraspecific studies integrating physiology and behaviour of different‐sized individuals may shed light on this paradox. We tested the FEH in free‐living Svalbard reindeer Rangifer tarandus platyrhynchus. We measured daily energy expenditure (DEE), subcutaneous body temperature (Tsc) and activity levels during the late winter in 14 adult females with body masses ranging from 46.3 to 57.8 kg. Winter energy expenditure (WEE) and fasting endurance (FE) were modelled dynamically by combining these data with body composition measurements of culled individuals at the onset of winter (14 years, n = 140) and variation in activity level throughout winter (10 years, n = 70). Mean DEE was 6.3 ± 0.7 MJ/day. Lean mass, Tsc and activity had significantly positive effects on DEE. Across all 140 individuals, mean FE was 85 ± 17 days (range 48–137 days). In contrast to the predictions of the FEH, the dominant factor affecting FE was initial fat mass, while body mass and FE were not correlated. Furthermore, lean mass and fat mass were not correlated. FE was on average 80% (45 days) longer in fat than lean individuals of the same size. Reducing activity levels by ~16% or Tsc by ~5% increased FE by 7% and 4% respectively. Our results fail to support the FEH. Rather, we demonstrate that (a) the size of fat reserves can be independent of lean mass and body size within a species, (b) ecological and environmental variation influence FE via their effects on body composition and (c) physiological and behavioural adjustments can improve FE within individuals. Altogether, our results suggest that there is a selection in Svalbard reindeer to accumulate body fat, rather than to grow structurally large. A free Plain Language Summary can be found within the Supporting Information of this article.

Original language	English
Pages (from-to)	1470-1480
Number of pages	11
Journal	Functional Ecology
Volume	35
Issue number	7
Early online date	14 May 2021
DOIs	https://doi.org/10.1111/1365-2435.13816
Publication status	Published - 1 Jul 2021

Bibliographical note

ACKNOWLEDGEMENTS
The authors thank two anonymous reviewers for constructive and insightful feedback which substantially improved their manuscript. They thank the Governor of Svalbard for permission to carry out the research. they are especially grateful to Mads Forchhammer, and the logistical and technical staff at the University Centre in Svalbard for supporting the field campaigns. They thank Marina Stamatiou and Peter Thompson for technical assistance in conducting the isotope analyses. The work was supported by the Norwegian Research Council (KLIMAFORSK project number 267613) and NMBU through the PhD grant of L.M.T. Equipment used for the detailed monitoring of animal movement and activity was supported by a grant to COAT from Tromsø Research Foundation. The animal handling protocol was approved by the Norwegian Food Safety Authority (permit no. 17/237024) and the Governor of Svalbard (permit no.16/01632‐9). The authors have no conflict of interest.

Keywords

activity
biologging
daily energy expenditure
doubly labelled water
intraspecific scaling
subcutaneous body temperature
Svalbard reindeer
the Arctic

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Trondrud_etal_FE_Fat_storage_influences_VOR
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.https://creativecommons.org/licenses/by-nc-nd/4.0/
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Fat storage influences fasting endurance more than body size in an ungulate
Trondrud, L. M. (Creator), Pigeon, G. (Creator), Król, E. (Creator), Albon, S. (Creator), Evans, A. L. (Creator), Arnold, W. (Creator), Hambly, C. (Creator), Irvine, R. J. (Creator), Ropstad, E. (Creator), Stien, A. (Creator), Veiberg, V. (Creator), Speakman, J. R. (Creator) & Loe, L. E. (Creator), Zenodo, 2021
DOI: 10.5281/zenodo.4682654, https://zenodo.org/record/4682654 and 2 more links, https://zenodo.org/record/4711725, https://datadryad.org/stash/dataset/doi:10.5061/dryad.83bk3j9qv (show fewer)
Dataset

Cite this

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title = "Fat storage influences fasting endurance more than body size in an ungulate",

abstract = "The fasting endurance hypothesis (FEH) predicts strong selection for large body size in mammals living in environments where food supply is interrupted over prolonged periods of time. The Arctic is a highly seasonal and food‐restricted environment, but contrary to predictions from the FEH, empirical evidence shows that Arctic mammals are often smaller than their temperate conspecifics. Intraspecific studies integrating physiology and behaviour of different‐sized individuals may shed light on this paradox. We tested the FEH in free‐living Svalbard reindeer Rangifer tarandus platyrhynchus. We measured daily energy expenditure (DEE), subcutaneous body temperature (Tsc) and activity levels during the late winter in 14 adult females with body masses ranging from 46.3 to 57.8 kg. Winter energy expenditure (WEE) and fasting endurance (FE) were modelled dynamically by combining these data with body composition measurements of culled individuals at the onset of winter (14 years, n = 140) and variation in activity level throughout winter (10 years, n = 70). Mean DEE was 6.3 ± 0.7 MJ/day. Lean mass, Tsc and activity had significantly positive effects on DEE. Across all 140 individuals, mean FE was 85 ± 17 days (range 48–137 days). In contrast to the predictions of the FEH, the dominant factor affecting FE was initial fat mass, while body mass and FE were not correlated. Furthermore, lean mass and fat mass were not correlated. FE was on average 80% (45 days) longer in fat than lean individuals of the same size. Reducing activity levels by ~16% or Tsc by ~5% increased FE by 7% and 4% respectively. Our results fail to support the FEH. Rather, we demonstrate that (a) the size of fat reserves can be independent of lean mass and body size within a species, (b) ecological and environmental variation influence FE via their effects on body composition and (c) physiological and behavioural adjustments can improve FE within individuals. Altogether, our results suggest that there is a selection in Svalbard reindeer to accumulate body fat, rather than to grow structurally large. A free Plain Language Summary can be found within the Supporting Information of this article.",

keywords = "activity, biologging, daily energy expenditure, doubly labelled water, intraspecific scaling, subcutaneous body temperature, Svalbard reindeer, the Arctic",

author = "Trondrud, {L. Monica} and Gabriel Pigeon and El{\.z}bieta Kr{\'o}l and Steve Albon and Evans, {Alina L.} and Walter Arnold and Catherine Hambly and Irvine, {R. Justin} and Erik Ropstad and Audun Stien and Vebj{\o}rn Veiberg and Speakman, {John R.} and Loe, {Leif Egil}",

note = "ACKNOWLEDGEMENTS The authors thank two anonymous reviewers for constructive and insightful feedback which substantially improved their manuscript. They thank the Governor of Svalbard for permission to carry out the research. they are especially grateful to Mads Forchhammer, and the logistical and technical staff at the University Centre in Svalbard for supporting the field campaigns. They thank Marina Stamatiou and Peter Thompson for technical assistance in conducting the isotope analyses. The work was supported by the Norwegian Research Council (KLIMAFORSK project number 267613) and NMBU through the PhD grant of L.M.T. Equipment used for the detailed monitoring of animal movement and activity was supported by a grant to COAT from Troms{\o} Research Foundation. The animal handling protocol was approved by the Norwegian Food Safety Authority (permit no. 17/237024) and the Governor of Svalbard (permit no.16/01632‐9). The authors have no conflict of interest.",

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T1 - Fat storage influences fasting endurance more than body size in an ungulate

AU - Trondrud, L. Monica

AU - Pigeon, Gabriel

AU - Król, Elżbieta

AU - Albon, Steve

AU - Evans, Alina L.

AU - Arnold, Walter

AU - Hambly, Catherine

AU - Irvine, R. Justin

AU - Ropstad, Erik

AU - Stien, Audun

AU - Veiberg, Vebjørn

AU - Speakman, John R.

AU - Loe, Leif Egil

N1 - ACKNOWLEDGEMENTS The authors thank two anonymous reviewers for constructive and insightful feedback which substantially improved their manuscript. They thank the Governor of Svalbard for permission to carry out the research. they are especially grateful to Mads Forchhammer, and the logistical and technical staff at the University Centre in Svalbard for supporting the field campaigns. They thank Marina Stamatiou and Peter Thompson for technical assistance in conducting the isotope analyses. The work was supported by the Norwegian Research Council (KLIMAFORSK project number 267613) and NMBU through the PhD grant of L.M.T. Equipment used for the detailed monitoring of animal movement and activity was supported by a grant to COAT from Tromsø Research Foundation. The animal handling protocol was approved by the Norwegian Food Safety Authority (permit no. 17/237024) and the Governor of Svalbard (permit no.16/01632‐9). The authors have no conflict of interest.

PY - 2021/7/1

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N2 - The fasting endurance hypothesis (FEH) predicts strong selection for large body size in mammals living in environments where food supply is interrupted over prolonged periods of time. The Arctic is a highly seasonal and food‐restricted environment, but contrary to predictions from the FEH, empirical evidence shows that Arctic mammals are often smaller than their temperate conspecifics. Intraspecific studies integrating physiology and behaviour of different‐sized individuals may shed light on this paradox. We tested the FEH in free‐living Svalbard reindeer Rangifer tarandus platyrhynchus. We measured daily energy expenditure (DEE), subcutaneous body temperature (Tsc) and activity levels during the late winter in 14 adult females with body masses ranging from 46.3 to 57.8 kg. Winter energy expenditure (WEE) and fasting endurance (FE) were modelled dynamically by combining these data with body composition measurements of culled individuals at the onset of winter (14 years, n = 140) and variation in activity level throughout winter (10 years, n = 70). Mean DEE was 6.3 ± 0.7 MJ/day. Lean mass, Tsc and activity had significantly positive effects on DEE. Across all 140 individuals, mean FE was 85 ± 17 days (range 48–137 days). In contrast to the predictions of the FEH, the dominant factor affecting FE was initial fat mass, while body mass and FE were not correlated. Furthermore, lean mass and fat mass were not correlated. FE was on average 80% (45 days) longer in fat than lean individuals of the same size. Reducing activity levels by ~16% or Tsc by ~5% increased FE by 7% and 4% respectively. Our results fail to support the FEH. Rather, we demonstrate that (a) the size of fat reserves can be independent of lean mass and body size within a species, (b) ecological and environmental variation influence FE via their effects on body composition and (c) physiological and behavioural adjustments can improve FE within individuals. Altogether, our results suggest that there is a selection in Svalbard reindeer to accumulate body fat, rather than to grow structurally large. A free Plain Language Summary can be found within the Supporting Information of this article.

AB - The fasting endurance hypothesis (FEH) predicts strong selection for large body size in mammals living in environments where food supply is interrupted over prolonged periods of time. The Arctic is a highly seasonal and food‐restricted environment, but contrary to predictions from the FEH, empirical evidence shows that Arctic mammals are often smaller than their temperate conspecifics. Intraspecific studies integrating physiology and behaviour of different‐sized individuals may shed light on this paradox. We tested the FEH in free‐living Svalbard reindeer Rangifer tarandus platyrhynchus. We measured daily energy expenditure (DEE), subcutaneous body temperature (Tsc) and activity levels during the late winter in 14 adult females with body masses ranging from 46.3 to 57.8 kg. Winter energy expenditure (WEE) and fasting endurance (FE) were modelled dynamically by combining these data with body composition measurements of culled individuals at the onset of winter (14 years, n = 140) and variation in activity level throughout winter (10 years, n = 70). Mean DEE was 6.3 ± 0.7 MJ/day. Lean mass, Tsc and activity had significantly positive effects on DEE. Across all 140 individuals, mean FE was 85 ± 17 days (range 48–137 days). In contrast to the predictions of the FEH, the dominant factor affecting FE was initial fat mass, while body mass and FE were not correlated. Furthermore, lean mass and fat mass were not correlated. FE was on average 80% (45 days) longer in fat than lean individuals of the same size. Reducing activity levels by ~16% or Tsc by ~5% increased FE by 7% and 4% respectively. Our results fail to support the FEH. Rather, we demonstrate that (a) the size of fat reserves can be independent of lean mass and body size within a species, (b) ecological and environmental variation influence FE via their effects on body composition and (c) physiological and behavioural adjustments can improve FE within individuals. Altogether, our results suggest that there is a selection in Svalbard reindeer to accumulate body fat, rather than to grow structurally large. A free Plain Language Summary can be found within the Supporting Information of this article.

KW - activity

KW - biologging

KW - daily energy expenditure

KW - doubly labelled water

KW - intraspecific scaling

KW - subcutaneous body temperature

KW - Svalbard reindeer

KW - the Arctic

U2 - 10.1111/1365-2435.13816

DO - 10.1111/1365-2435.13816

M3 - Article

SN - 0269-8463

VL - 35

SP - 1470

EP - 1480

JO - Functional Ecology

JF - Functional Ecology

IS - 7

ER -

Fat storage influences fasting endurance more than body size in an ungulate

Abstract

Bibliographical note

Keywords

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Fat storage influences fasting endurance more than body size in an ungulate

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