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      Thermal physiology and activity in relation to reproductive status and sex in a free-ranging semelparous marsupial

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          Abstract

          In a changing climate, southern hemisphere mammals are predicted to face rising temperatures and aridity, resulting in food and water shortages, which may further challenge already constrained energetic demands. Especially semelparous mammals may be threatened because survival of the entire population depends on the success of a single breeding event. One of these species, the yellow-footed antechinus, Antechinus flavipes, a small, heterothermic marsupial mammal, commences reproduction during winter, when insect prey is limited and energetic constraints are high. We examined the inter-relations between thermal and foraging biology of free-ranging A. flavipes and examined whether they use torpor for energy conservation, despite the fact that reproduction and torpor are considered to be incompatible for many mammals. Females used torpor during the reproductive season, but patterns changed with reproductive status. Prior to breeding, females used frequent (86% of days), deep and long torpor that was more pronounced than any other reproductive group, including pre-mating males (64% of days). Pregnant females continued to use torpor, albeit torpor was less frequent (28% of days) and significantly shorter and shallower than before breeding. Parturient and lactating females did not express torpor. During the mating period, males reduced torpor use (24% of days). Pre-reproductive females and pre-mating males were the least active and may use torpor to minimize predator exposure and enhance fat deposition in anticipation of the energetic demands associated with impending mating, gestation and lactation. Reproductive females were most active and likely foraged and fed to promote growth and development of young. Our data show that A. flavipes are balancing energetic demands during the reproductive season by modifying torpor and activity patterns. As the timing of reproduction is fixed for this genus, it is probable that climate change will render these behavioural and physiological adaptations as inadequate and threaten this and other semelparous species.

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          Hibernation and daily torpor minimize mammalian extinctions.

          Small mammals appear to be less vulnerable to extinction than large species, but the underlying reasons are poorly understood. Here, we provide evidence that almost all (93.5%) of 61 recently extinct mammal species were homeothermic, maintaining a constant high body temperature and thus energy expenditure, which demands a high intake of food, long foraging times, and thus exposure to predators. In contrast, only 6.5% of extinct mammals were likely heterothermic and employed multi-day torpor (hibernation) or daily torpor, even though torpor is widespread within more than half of all mammalian orders. Torpor is characterized by substantial reductions of body temperature and energy expenditure and enhances survival during adverse conditions by minimizing food and water requirements, and consequently reduces foraging requirements and exposure to predators. Moreover, because life span is generally longer in heterothermic mammals than in related homeotherms, heterotherms can employ a 'sit-and-wait' strategy to withstand adverse periods and then repopulate when circumstances improve. Thus, torpor is a crucial but hitherto unappreciated attribute of small mammals for avoiding extinction. Many opportunistic heterothermic species, because of their plastic energetic requirements, may also stand a better chance of future survival than homeothermic species in the face of greater climatic extremes and changes in environmental conditions caused by global warming.
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            Deep, prolonged torpor by pregnant, free-ranging bats.

            Many mammals save energy during food shortage or harsh weather using controlled reductions in body temperature and metabolism called torpor. However, torpor slows offspring growth, and reproductive individuals are thought to avoid using it because of reduced fitness resulting from delayed offspring development. We tested this hypothesis by investigating torpor during reproduction in hoary bats (Lasiurus cinereus, Vespertilionidae) in southern Canada. We recorded deep, prolonged torpor bouts, which meet the definition for hibernation, by pregnant females. Prolonged torpor occurred during spring storms. When conditions improved females aroused and gave birth within several days. Our observations imply a fitness advantage of torpor in addition to energy conservation because reduced foetal growth rate could delay parturition until conditions are more favourable for lactation and neonatal survival.
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              Influence of torpor on milk protein composition and secretion in lactating bats.

              In the pipistrelle bat (Pipistrellus pipistrellus), the metabolic load of lactation is not met to any significant extent by increased food intake or mobilization of body reserves, and aerial foraging accounts for most of the animal's energy expenditure even during lactation. Energy conservation must, therefore, play a critical role in maintaining lactation. The principal mechanism for energy conservation appears to be the bat's ability to enter torpor, but this may itself interrupt milk synthesis and secretion unless the pipistrelle mammary gland is adapted to counteract its effect. The effect of torpor on mammary tissue function was studied in mammary tissue explant cultures prepared in weeks 1-3 of lactation, when milk water yield was 0.20, 0.88, and 0.30 mL/d respectively. Protein synthesis measured by incorporation of radiolabeled amino acids was 44% lower (P < 0.001) in bat tissue explants cultured at ambient temperature (22 degrees C) compared with 37 degrees C. The reduction was similar to that observed in mouse mammary tissue (57%) and was unaffected by stage of lactation. Analysis of explant protein after [35S]methionine labelling showed the majority of proteins synthesised in culture to be milk proteins; it also demonstrated that the decrease in protein synthesis at ambient temperature was a general phenomenon: synthesis of both secretory and intracellular mammary proteins was reduced at the lower culture temperature. The results suggest that bat mammary tissue has no mechanism to counteract the effect of reduced body temperature and that periods of lactational torpor are likely to cause a pronounced diurnal variation in the rate of milk secretion.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2019
                11 November 2019
                11 November 2019
                : 7
                : 1
                : coz073
                Affiliations
                [1 ] Centre for Behavioural and Physiological Ecology , Zoology, University of New England, Armidale, NSW 2351, Australia
                [2 ] Department of Biology , Norwegian University of Science and Technology, Trondheim 7491, Norway
                Author notes
                Corresponding author: Department of Biology, Norwegian University of Science and Technology, Trondheim, 7491, Norway. Email: clare.stawski@ 123456ntnu.no
                Author information
                http://orcid.org/0000-0003-1714-0301
                Article
                coz073
                10.1093/conphys/coz073
                6846706
                b47169f6-ae63-4664-8db5-38853205911f
                © The Author(s) 2019. Published by Oxford University Press and the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 December 2018
                : 26 June 2019
                : 21 August 2019
                Page count
                Pages: 10
                Funding
                Funded by: University of New England 10.13039/501100001772
                Funded by: Australian Research Council 10.13039/501100000923
                Funded by: Discovery Early Career Researcher Award
                Categories
                Research Article

                body temperature,lactation,mammal,pregnancy,torpor
                body temperature, lactation, mammal, pregnancy, torpor

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