Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

Edyta T. Sadowska, Elzbieta Krol, Katarzyna M. Chrzascik, Agata M. Rudolf, John R. Speakman, Paweł Koteja

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Abstract

Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day(-1), unshaved: 14.4±0.2 g day(-1); P<0.0001), average daily metabolic rate (shaved: 109±2 kJ day(-1), unshaved: 97±2 kJ day(-1); P<0.0001) and metabolisable energy intake (shaved: 215±4 kJ day(-1), unshaved: 185±4 kJ day(-1); P<0.0001), as well as the milk energy output (shaved: 104±4 kJ day(-1); unshaved: 93±4 kJ day(-1); P=0.021) and litter growth rate (shaved: 9.4±0.7 g 4 days(-1), unshaved: 7.7±0.7 g 4 days(-1); P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3%) than in unshaved ones (78.5±0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.

Original languageEnglish
Pages (from-to)805-815
Number of pages11
JournalJournal of Experimental Biology
Volume219
Issue number6
Early online date8 Jan 2016
DOIs
Publication statusPublished - 16 Mar 2016

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Arvicolinae
Clethrionomys glareolus
Budgets
Energy Intake
energy budget
dissipation
energy intake
Hot Temperature
lactation
heat
Lactation
energy
fur
basal metabolic rate
ecophysiology
reproductive traits
Basal Metabolism
Digestive System
metabolizable energy
food intake

Keywords

  • artificial selection
  • doubly labelled water
  • food consumption
  • maternal investment
  • milk energy output
  • thermal conductance

Cite this

Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles? / Sadowska, Edyta T.; Krol, Elzbieta; Chrzascik, Katarzyna M.; Rudolf, Agata M.; Speakman, John R.; Koteja, Paweł.

In: Journal of Experimental Biology, Vol. 219, No. 6, 16.03.2016, p. 805-815.

Research output: Contribution to journalArticle

Sadowska, Edyta T. ; Krol, Elzbieta ; Chrzascik, Katarzyna M. ; Rudolf, Agata M. ; Speakman, John R. ; Koteja, Paweł. / Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?. In: Journal of Experimental Biology. 2016 ; Vol. 219, No. 6. pp. 805-815.
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abstract = "Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day(-1), unshaved: 14.4±0.2 g day(-1); P<0.0001), average daily metabolic rate (shaved: 109±2 kJ day(-1), unshaved: 97±2 kJ day(-1); P<0.0001) and metabolisable energy intake (shaved: 215±4 kJ day(-1), unshaved: 185±4 kJ day(-1); P<0.0001), as well as the milk energy output (shaved: 104±4 kJ day(-1); unshaved: 93±4 kJ day(-1); P=0.021) and litter growth rate (shaved: 9.4±0.7 g 4 days(-1), unshaved: 7.7±0.7 g 4 days(-1); P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3{\%}) than in unshaved ones (78.5±0.2{\%}; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.",
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note = "Acknowledgements We are grateful to our technicians and several students for their help during this study and for animal care. We thank Catherine Hambly and Peter Thompson for technical assistance for the isotope analysis for the DLW measurements. We thank Ulf Bauchinger for stimulating discussion and his comments, and two anonymous referees for comments on the manuscript. Funding This project was supported by grants from the Polish Ministry of Science and Higher Education [0595/B/P01/2011/40 to E.T.S. and 8167/B/P01/2011/40 to P.K.], and Jagiellonian University [DS/WBINOZ/INOS/757 to P.K.].",
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T1 - Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

AU - Sadowska, Edyta T.

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AU - Chrzascik, Katarzyna M.

AU - Rudolf, Agata M.

AU - Speakman, John R.

AU - Koteja, Paweł

N1 - Acknowledgements We are grateful to our technicians and several students for their help during this study and for animal care. We thank Catherine Hambly and Peter Thompson for technical assistance for the isotope analysis for the DLW measurements. We thank Ulf Bauchinger for stimulating discussion and his comments, and two anonymous referees for comments on the manuscript. Funding This project was supported by grants from the Polish Ministry of Science and Higher Education [0595/B/P01/2011/40 to E.T.S. and 8167/B/P01/2011/40 to P.K.], and Jagiellonian University [DS/WBINOZ/INOS/757 to P.K.].

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N2 - Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day(-1), unshaved: 14.4±0.2 g day(-1); P<0.0001), average daily metabolic rate (shaved: 109±2 kJ day(-1), unshaved: 97±2 kJ day(-1); P<0.0001) and metabolisable energy intake (shaved: 215±4 kJ day(-1), unshaved: 185±4 kJ day(-1); P<0.0001), as well as the milk energy output (shaved: 104±4 kJ day(-1); unshaved: 93±4 kJ day(-1); P=0.021) and litter growth rate (shaved: 9.4±0.7 g 4 days(-1), unshaved: 7.7±0.7 g 4 days(-1); P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3%) than in unshaved ones (78.5±0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.

AB - Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day(-1), unshaved: 14.4±0.2 g day(-1); P<0.0001), average daily metabolic rate (shaved: 109±2 kJ day(-1), unshaved: 97±2 kJ day(-1); P<0.0001) and metabolisable energy intake (shaved: 215±4 kJ day(-1), unshaved: 185±4 kJ day(-1); P<0.0001), as well as the milk energy output (shaved: 104±4 kJ day(-1); unshaved: 93±4 kJ day(-1); P=0.021) and litter growth rate (shaved: 9.4±0.7 g 4 days(-1), unshaved: 7.7±0.7 g 4 days(-1); P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3%) than in unshaved ones (78.5±0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.

KW - artificial selection

KW - doubly labelled water

KW - food consumption

KW - maternal investment

KW - milk energy output

KW - thermal conductance

U2 - 10.1242/jeb.134437

DO - 10.1242/jeb.134437

M3 - Article

VL - 219

SP - 805

EP - 815

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 6

ER -