Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory

The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in...

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Published in:Journal of Experimental Biology
Main Authors: Simons, Mirre J. P., Reimert, Inonge, van der Vinne, Vincent, Hambly, Catherine, Vaanholt, Lobke M., Speakman, John R., Gerkema, Menno P.
Format: Article in Journal/Newspaper
Language:English
Published: 2011
Subjects:
Online Access:https://hdl.handle.net/11370/55f18a51-cd26-4ef0-8bf3-afa311b23e69
https://research.rug.nl/en/publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69
https://doi.org/10.1242/jeb.044230
https://pure.rug.nl/ws/files/6755778/2011JExpBiolSimons.pdf
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spelling ftunigroningenpu:oai:pure.rug.nl:publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69 2024-06-23T07:52:13+00:00 Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory Simons, Mirre J. P. Reimert, Inonge van der Vinne, Vincent Hambly, Catherine Vaanholt, Lobke M. Speakman, John R. Gerkema, Menno P. 2011-01 application/pdf https://hdl.handle.net/11370/55f18a51-cd26-4ef0-8bf3-afa311b23e69 https://research.rug.nl/en/publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69 https://doi.org/10.1242/jeb.044230 https://pure.rug.nl/ws/files/6755778/2011JExpBiolSimons.pdf eng eng https://research.rug.nl/en/publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69 info:eu-repo/semantics/openAccess Simons , M J P , Reimert , I , van der Vinne , V , Hambly , C , Vaanholt , L M , Speakman , J R & Gerkema , M P 2011 , ' Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis) : a test of the heat dissipation limit theory ' , Journal of Experimental Biology , vol. 214 , no. 1 , pp. 38-49 . https://doi.org/10.1242/jeb.044230 heat dissipation litter size enlargement sustained energy intake fur removal ambient temperature lactation pup mortality SUSTAINED ENERGY-INTAKE DOUBLY-LABELED WATER MOUSE MUS-MUSCULUS METABOLIC-RATE LABORATORY MICE MILK-PRODUCTION FOOD-INTAKE FIELD-VOLE BODY-MASS LASIOPODOMYS-BRANDTII article 2011 ftunigroningenpu https://doi.org/10.1242/jeb.044230 2024-06-03T16:23:25Z The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in livestock has increased litter size or productivity in these animals. To test the wider validity of the heat dissipation limit theory, we studied common voles (Microtus arvalis), which have small litter sizes by comparison with mice and rats, and regular addition of wild-caught individuals of this species to our laboratory colony ensures a natural genetic background. A crossover design of ambient temperatures (21 and 30 degrees C) during pregnancy and lactation was used. High ambient temperature during lactation decreased milk production, slowing pup growth. The effect on pup growth was amplified when ambient temperature was also high during pregnancy. Shaving fur off dams at 30 degrees C resulted in faster growth of pups; however, no significant increase in food intake and or milk production was detected. With increasing litter size (natural and enlarged), asymptotic food intake during lactation levelled off in the largest litters at both 21 and 30 degrees C. Interestingly, the effects of lactation temperature on pup growth where also observed at smaller litter sizes. This suggests that vole dams trade-off costs associated with hyperthermia during lactation with the yield from investment in pup growth. Moreover, pup survival was higher at 30 degrees C, despite lower growth, probably owing to thermoregulatory benefits. It remains to be seen how the balance is established between the negative effect of high ambient temperature on maternal milk production and pup growth (and/or future reproduction of the dam) and the positive effect of high temperatures on pup survival. This balance ultimately determines the effect of different ambient temperatures on reproductive success. Article in Journal/Newspaper Common vole Microtus arvalis University of Groningen research database Journal of Experimental Biology 214 1 38 49
institution Open Polar
collection University of Groningen research database
op_collection_id ftunigroningenpu
language English
topic heat dissipation
litter size enlargement
sustained energy intake
fur removal
ambient temperature
lactation
pup mortality
SUSTAINED ENERGY-INTAKE
DOUBLY-LABELED WATER
MOUSE MUS-MUSCULUS
METABOLIC-RATE
LABORATORY MICE
MILK-PRODUCTION
FOOD-INTAKE
FIELD-VOLE
BODY-MASS
LASIOPODOMYS-BRANDTII
spellingShingle heat dissipation
litter size enlargement
sustained energy intake
fur removal
ambient temperature
lactation
pup mortality
SUSTAINED ENERGY-INTAKE
DOUBLY-LABELED WATER
MOUSE MUS-MUSCULUS
METABOLIC-RATE
LABORATORY MICE
MILK-PRODUCTION
FOOD-INTAKE
FIELD-VOLE
BODY-MASS
LASIOPODOMYS-BRANDTII
Simons, Mirre J. P.
Reimert, Inonge
van der Vinne, Vincent
Hambly, Catherine
Vaanholt, Lobke M.
Speakman, John R.
Gerkema, Menno P.
Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
topic_facet heat dissipation
litter size enlargement
sustained energy intake
fur removal
ambient temperature
lactation
pup mortality
SUSTAINED ENERGY-INTAKE
DOUBLY-LABELED WATER
MOUSE MUS-MUSCULUS
METABOLIC-RATE
LABORATORY MICE
MILK-PRODUCTION
FOOD-INTAKE
FIELD-VOLE
BODY-MASS
LASIOPODOMYS-BRANDTII
description The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in livestock has increased litter size or productivity in these animals. To test the wider validity of the heat dissipation limit theory, we studied common voles (Microtus arvalis), which have small litter sizes by comparison with mice and rats, and regular addition of wild-caught individuals of this species to our laboratory colony ensures a natural genetic background. A crossover design of ambient temperatures (21 and 30 degrees C) during pregnancy and lactation was used. High ambient temperature during lactation decreased milk production, slowing pup growth. The effect on pup growth was amplified when ambient temperature was also high during pregnancy. Shaving fur off dams at 30 degrees C resulted in faster growth of pups; however, no significant increase in food intake and or milk production was detected. With increasing litter size (natural and enlarged), asymptotic food intake during lactation levelled off in the largest litters at both 21 and 30 degrees C. Interestingly, the effects of lactation temperature on pup growth where also observed at smaller litter sizes. This suggests that vole dams trade-off costs associated with hyperthermia during lactation with the yield from investment in pup growth. Moreover, pup survival was higher at 30 degrees C, despite lower growth, probably owing to thermoregulatory benefits. It remains to be seen how the balance is established between the negative effect of high ambient temperature on maternal milk production and pup growth (and/or future reproduction of the dam) and the positive effect of high temperatures on pup survival. This balance ultimately determines the effect of different ambient temperatures on reproductive success.
format Article in Journal/Newspaper
author Simons, Mirre J. P.
Reimert, Inonge
van der Vinne, Vincent
Hambly, Catherine
Vaanholt, Lobke M.
Speakman, John R.
Gerkema, Menno P.
author_facet Simons, Mirre J. P.
Reimert, Inonge
van der Vinne, Vincent
Hambly, Catherine
Vaanholt, Lobke M.
Speakman, John R.
Gerkema, Menno P.
author_sort Simons, Mirre J. P.
title Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
title_short Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
title_full Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
title_fullStr Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
title_full_unstemmed Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis):a test of the heat dissipation limit theory
title_sort ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (microtus arvalis):a test of the heat dissipation limit theory
publishDate 2011
url https://hdl.handle.net/11370/55f18a51-cd26-4ef0-8bf3-afa311b23e69
https://research.rug.nl/en/publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69
https://doi.org/10.1242/jeb.044230
https://pure.rug.nl/ws/files/6755778/2011JExpBiolSimons.pdf
genre Common vole
Microtus arvalis
genre_facet Common vole
Microtus arvalis
op_source Simons , M J P , Reimert , I , van der Vinne , V , Hambly , C , Vaanholt , L M , Speakman , J R & Gerkema , M P 2011 , ' Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis) : a test of the heat dissipation limit theory ' , Journal of Experimental Biology , vol. 214 , no. 1 , pp. 38-49 . https://doi.org/10.1242/jeb.044230
op_relation https://research.rug.nl/en/publications/55f18a51-cd26-4ef0-8bf3-afa311b23e69
op_rights info:eu-repo/semantics/openAccess
op_doi https://doi.org/10.1242/jeb.044230
container_title Journal of Experimental Biology
container_volume 214
container_issue 1
container_start_page 38
op_container_end_page 49
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