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      Long-term survival, temperature, and torpor patterns

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      1 , 2 ,
      Scientific Reports
      Nature Publishing Group UK
      Ecology, Evolution, Physiology, Zoology

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          Abstract

          Mammalian and avian torpor is highly effective in reducing energy expenditure. However, the extent of energy savings achieved and thus long-term survival appear to differ between species capable of multiday hibernation and species restricted to daily heterothermy, which could, however, be due to thermal effects. We tested how long-term survival on stored body fat (i.e. time to lean body mass), crucial for overcoming adverse periods, is related to the pattern of torpor expressed under different ambient temperatures (T a: 7 °C typical of hibernation, 15 and 22 °C typical of daily torpor) in the small marsupial hibernator the pygmy-possum ( Cercartetus nanus). Possums expressed torpor at all T as and survived without food for 310 days on average at T a 7 °C, 195 days at T a 15 °C, and 127 days at T a 22 °C. At T a 7 and 15 °C, torpor bout duration (TBD) increased from < 1–3 to ~ 5–16 days over 2 months, whereas at T a 22 °C, TBD remained at < 1 to ~ 2 days. At all T as daily energy use was substantially lower and TBD and survival times of possums much longer (3–12 months) than in daily heterotherms (~ 10 days). Such pronounced differences in torpor patterns and survival times even under similar thermal conditions provide strong support for the concept that torpor in hibernators and daily heterotherms are physiologically distinct and have evolved for different ecological purposes.

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            Daily torpor and hibernation in birds and mammals.

            Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
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              Hibernation in black bears: independence of metabolic suppression from body temperature.

              Black bears hibernate for 5 to 7 months a year and, during this time, do not eat, drink, urinate, or defecate. We measured metabolic rate and body temperature in hibernating black bears and found that they suppress metabolism to 25% of basal rates while regulating body temperature from 30° to 36°C, in multiday cycles. Heart rates were reduced from 55 to as few as 9 beats per minute, with profound sinus arrhythmia. After returning to normal body temperature and emerging from dens, bears maintained a reduced metabolic rate for up to 3 weeks. The pronounced reduction and delayed recovery of metabolic rate in hibernating bears suggest that the majority of metabolic suppression during hibernation is independent of lowered body temperature.
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                Author and article information

                Contributors
                Thomas.Ruf@vetmeduni.ac.at
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                24 April 2023
                24 April 2023
                2023
                : 13
                : 6673
                Affiliations
                [1 ]GRID grid.1020.3, ISNI 0000 0004 1936 7371, Centre for Behavioural and Physiological Ecology, Zoology, , University of New England, ; Armidale, 2351 Australia
                [2 ]GRID grid.6583.8, ISNI 0000 0000 9686 6466, Department of Interdisciplinary Life Sciences, Research Institute of Wildlife Ecology, , University of Veterinary Medicine, ; Savoyenstrasse 1, 1160 Vienna, Austria
                Article
                33646
                10.1038/s41598-023-33646-6
                10126141
                37095170
                79a189cd-2022-4b97-aa1a-fa7c792fb580
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 20 January 2023
                : 17 April 2023
                Funding
                Funded by: Australian Research Council
                Funded by: University of Veterinary Medicine Vienna
                Categories
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                © The Author(s) 2023

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                ecology,evolution,physiology,zoology
                Uncategorized
                ecology, evolution, physiology, zoology

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