Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development

Most mammals and birds are altricial, small and naked at birth/hatching. They attain endothermic thermoregulation at a fraction of their adult size at a vulnerable stage with high heat loss when many could profit from using torpor for energy conservation. Nevertheless, detailed data on the interrela...

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Main Authors: Fritz Geiser, Jing Wen, Gansukh Sukhchuluun, Qing-Sheng Chi, De-Hua Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2019.00469/full
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author Fritz Geiser
Fritz Geiser
Jing Wen
Gansukh Sukhchuluun
Gansukh Sukhchuluun
Qing-Sheng Chi
De-Hua Wang
De-Hua Wang
author_facet Fritz Geiser
Fritz Geiser
Jing Wen
Gansukh Sukhchuluun
Gansukh Sukhchuluun
Qing-Sheng Chi
De-Hua Wang
De-Hua Wang
author_sort Fritz Geiser
collection DOAJ
description Most mammals and birds are altricial, small and naked at birth/hatching. They attain endothermic thermoregulation at a fraction of their adult size at a vulnerable stage with high heat loss when many could profit from using torpor for energy conservation. Nevertheless, detailed data on the interrelations between torpor expression and development of endothermic thermoregulation are currently restricted to <0.1% of extant endotherms. We investigated at what age and body mass (BM) desert hamsters (Phodopus roborovskii), wild-caught in Inner Mongolia and born in autumn/early winter when environmental temperatures in the wild begin to decrease, are able to defend their body temperature (Tb) at an ambient temperature (Ta) of ∼21°C and how soon thereafter they could express torpor. Measurements of surface temperatures via infrared thermometer and thermal camera show that although neonate hamsters (BM 0.9 ± 0.1 g) cooled rapidly to near Ta, already on day 15 (BM 5.5 ± 0.2 g) they could defend a high and constant Tb. As soon as day 16 (BM 5.8 ± 0.2 g), when their maximum activity metabolism (measured as oxygen consumption) approached maxima measured in vertebrates, animals were able to enter torpor for several hours with a reduction of metabolism by >90%, followed by endothermic arousal. Over the next weeks, torpor depth and duration decreased together with a reduction in resting metabolic rate at Ta 30–32°C. Our data show that development of endothermy and torpor expression in this altricial hamster is extremely fast. The results suggest that precocious torpor by juvenile hamsters in autumn and winter is an important survival tool in their vast and harsh Asian desert habitats, but likely also for many other small mammals and birds worldwide.
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spelling doaj.art-f4727fb868d94cc6a9d8fcab65bdcb772022-12-21T21:47:14ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-04-011010.3389/fphys.2019.00469437468Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During DevelopmentFritz Geiser0Fritz Geiser1Jing Wen2Gansukh Sukhchuluun3Gansukh Sukhchuluun4Qing-Sheng Chi5De-Hua Wang6De-Hua Wang7State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaCentre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, AustraliaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaMammalian Ecology Laboratory, Institute of General and Experimental Biology, Mongolian Academy of Sciences, Ulaanbaatar, MongoliaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaUniversity of the Chinese Academy of Sciences, Beijing, ChinaMost mammals and birds are altricial, small and naked at birth/hatching. They attain endothermic thermoregulation at a fraction of their adult size at a vulnerable stage with high heat loss when many could profit from using torpor for energy conservation. Nevertheless, detailed data on the interrelations between torpor expression and development of endothermic thermoregulation are currently restricted to <0.1% of extant endotherms. We investigated at what age and body mass (BM) desert hamsters (Phodopus roborovskii), wild-caught in Inner Mongolia and born in autumn/early winter when environmental temperatures in the wild begin to decrease, are able to defend their body temperature (Tb) at an ambient temperature (Ta) of ∼21°C and how soon thereafter they could express torpor. Measurements of surface temperatures via infrared thermometer and thermal camera show that although neonate hamsters (BM 0.9 ± 0.1 g) cooled rapidly to near Ta, already on day 15 (BM 5.5 ± 0.2 g) they could defend a high and constant Tb. As soon as day 16 (BM 5.8 ± 0.2 g), when their maximum activity metabolism (measured as oxygen consumption) approached maxima measured in vertebrates, animals were able to enter torpor for several hours with a reduction of metabolism by >90%, followed by endothermic arousal. Over the next weeks, torpor depth and duration decreased together with a reduction in resting metabolic rate at Ta 30–32°C. Our data show that development of endothermy and torpor expression in this altricial hamster is extremely fast. The results suggest that precocious torpor by juvenile hamsters in autumn and winter is an important survival tool in their vast and harsh Asian desert habitats, but likely also for many other small mammals and birds worldwide.https://www.frontiersin.org/article/10.3389/fphys.2019.00469/fullAsiadesert hamsters (Phodopus roborovskii)heterothermyaltricialbody temperaturemetabolic rate
spellingShingle Fritz Geiser
Fritz Geiser
Jing Wen
Gansukh Sukhchuluun
Gansukh Sukhchuluun
Qing-Sheng Chi
De-Hua Wang
De-Hua Wang
Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
Frontiers in Physiology
Asia
desert hamsters (Phodopus roborovskii)
heterothermy
altricial
body temperature
metabolic rate
title Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
title_full Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
title_fullStr Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
title_full_unstemmed Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
title_short Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development
title_sort precocious torpor in an altricial mammal and the functional implications of heterothermy during development
topic Asia
desert hamsters (Phodopus roborovskii)
heterothermy
altricial
body temperature
metabolic rate
url https://www.frontiersin.org/article/10.3389/fphys.2019.00469/full
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