Growing up in a changing climate: how temperature affects the development of morphological, behavioral and physiological traits of a marsupial mammal

Climate change is likely to affect many mammalian phenotypes, yet little is known whether and how phenotypic plasticity is involved in responding to thermal challenges during mammalian development. We investigated the effect of continuous cold or warm exposure during development on morphological, behavioral, and functional variables of yellow-footed antechinus (Antechinus flavipes), a semelparous Australian marsupial mammal. Captive-bred young were exposed to two ambient temperatures (Ta), cold (17°C) or warm (25°C), once weaned. Treatments were reversed and metabolic rate (MR) measurements repeated after 2 months. We measured body mass weekly, activity continuously, and MRs over a range of Ta once they were adults. Growth rate was similar in both groups, but was faster in males. Antechinus in the warm group were initially more active than the cold group and decreased activity when exposed to cold, whereas the cold group increased activity when exposed to warm. Interestingly, females changed their night-time activity when Ta was changed, whereas males changed their daytime activity. MRs were originally lower in the warm group in comparison to the cold group for both sexes and increased slightly for females, but not for males, after being exposed to cold. After exposure to warm Ta, the MRs of the cold group decreased significantly over the entire Ta-range for both sexes. Our results reveal that temperatures experienced during development can influence behavioral and physiological traits in antechinus. Such phenotypic plasticity is vital for a species that within 1 year is dependent on a single breeding event and experiences a complete population turnover.publishedVersionCopyright © 2020 Stawski and Geiser. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms

Can hibernators sense and evade fires? Olfactory acuity and locomotor performance during deep torpor.

Increased habitat fragmentation, global warming and other human activities have caused a rise in the frequency of wildfires worldwide. To reduce the risks of uncontrollable fires, prescribed burns are generally conducted during the colder months of the year, a time when in many mammals torpor is expressed regularly. Torpor is crucial for energy conservation, but the low body temperatures (T b) are associated with a decreased responsiveness and torpid animals might therefore face an increased mortality risk during fires. We tested whether hibernators in deep torpor (a) can respond to the smell of smoke and (b) can climb to avoid fires at T bs below normothermic levels. Our data show that torpid eastern pygmy-possums (Cercartetus nanus) are able to detect smoke and also can climb. All males aroused from torpor when the smoke stimulus was presented at an ambient temperature (T a) of 15 °C (T b ∼18 °C), whereas females only raised their heads. The responses were less pronounced at T a 10 °C. The first coordinated movement of possums along a branch was observed at a mean T b of 15.6 °C, and animals were even able to climb their prehensile tail when they reached a mean T b of 24.4 °C. Our study shows that hibernators can sense smoke and move at low T b. However, our data also illustrate that at T b ≤13 °C, C. nanus show decreased responsiveness and locomotor performance and highlight that prescribed burns during winter should be avoided on very cold days to allow torpid animals enough time to respond

Hibernation: Endotherms

The main function of hibernation and daily torpor in heterothermic mammals and birds (i.e. species capable of expressing torpor) is to conserve energy and water and thus to survive during adverse environmental conditions or periods of food shortage no matter if they live in the arctic or the tropics. However, the reduced energy requirements also permit survival of bad weather during reproduction to prolong gestation into more favourable periods, conservation of nutrients for growth during development, and overall result in reduced foraging needs and thus exposure to predators, which appear major contributing reasons why heterotherms are often long lived and have lower extinction rates than strictly homeothermic species that cannot use torpor. Known heterothermic mammals and birds are diverse with about 2/3 of mammalian orders and 1/3 of avian orders containing heterothermic species, and their number continues to grow

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

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.publishedVersion© 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

A burning question: what are the risks and benefits of mammalian torpor during and after fires?

Although wildfires are increasing globally, available information on how mammals respond behaviourally and physiologically to fires is scant. Despite a large number of ecological studies, often examining animal diversity and abundance before and after fires, the reasons as to why some species perform better than others remain obscure. We examine how especially small mammals, which generally have high rates of energy expenditure and food requirements, deal with fires and post-fire conditions. We evaluate whether mammalian torpor, characterised by substantial reductions in body temperature, metabolic rate and water loss, plays a functional role in survival of mammals impacted by fires. Importantly, torpor permits small mammals to reduce their activity and foraging, and to survive on limited food. Torpid small mammals (marsupials and bats) can respond to smoke and arouse from torpor, which provides them with the possibility to evade direct exposure to fire, although their response is often slowed when ambient temperature is low. Post-fire conditions increase expression of torpor with a concomitant decrease in activity for free-ranging echidnas and small forest-dwelling marsupials, in response to reduced cover and reduced availability of terrestrial insects. Presence of charcoal and ash increases torpor use by captive small marsupials beyond food restriction alone, likely in anticipation of detrimental post-fire conditions. Interestingly, although volant bats use torpor on every day after fires, they respond by decreasing torpor duration, and increasing activity, perhaps because of the decrease in clutter and increase in foraging opportunities due to an increase in aerial insects. Our summary shows that torpor is an important tool for post-fire survival and, although the physiological and behavioural responses of small mammals to fire are complex, they seem to reflect energetic requirements and mode of foraging. We make recommendations on the conditions during management burns that are least likely to impact heterothermic mammals.publishedVersion© The Author(s) 2018. 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

Heterothermy in a Small Passerine : Eastern Yellow Robins Use Nocturnal Torpor in Winter

Torpor is a controlled reduction of metabolism and body temperature, and its appropriate use allows small birds to adapt to and survive challenging conditions. However, despite its great energy conservation potential, torpor use by passerine birds is understudied although they are small and comprise over half of extant bird species. Here, we first determined whether a free-living, small ~20 g Australian passerine, the eastern yellow robin (Eopsaltria australis), expresses torpor by measuring skin temperature (Ts) as a proxy for body temperature. Second, we tested if skin temperature fluctuated in relation to ambient temperature (Ta). We found that the Ts of eastern yellow robins fluctuated during winter by 9.1 ± 3.9°C on average (average minimum Ts 30.1 ± 2.3°C), providing the first evidence of torpor expression in this species. Daily minimum Ts decreased with Ta, reducing the estimated metabolic rate by as much as 32%. We hope that our results will encourage further studies to expand our knowledge on the use of torpor in wild passerines. The implications of such studies are important because species with highly flexible energy requirements may have an advantage over strict homeotherms during the current increasing frequency of extreme and unpredictable weather events, driven by changing climate

Seasonal Control of Mammalian Energy Balance : Recent advances in the understanding of daily torpor and hibernation

Funding This work was supported in part by BBSRC grant (BB/M001504/1) to PB, DFG Emmy-Noether HE6383 to AH, German Center for Diabetes Research (DZD) to MJ.Peer reviewedPostprin

Thermal biology and roost selection of free-ranging male little forest bats, Vespadelus vulturnus, during winter

Insectivorous bats are particularly susceptible to heat loss due to their relatively large surface area to volume ratio. Therefore, to maintain a high normothermic body temperature, bats require large amounts of energy for thermoregulation. This can be energetically challenging for small bats during cold periods as heat loss is augmented and insect prey is reduced. To conserve energy many bats enter a state of torpor characterized by a controlled reduction of metabolism and body temperature in combination with selecting roosts based upon thermal properties. Our study aimed to quantify torpor patterns and roost preferences of free-ranging little forest bats (Vespadelus vulturnus) during winter to identify physiological and behavioral mechanisms used by this species for survival of the cold season. All bats captured were male (body mass 4.9 ± 0.7 g, n = 6) and used torpor on every day monitored, with bouts lasting up to 187.58 h (mean = 35.5 ± 36.7 h, n = 6, total number of samples [N] = 61). Torpor bout duration was signifcantly correlated with daily minimum and maximum ambient temperature, mean skin temperature, insect mass, and body mass of individuals and the multiday torpor bouts recorded in the cold qualify as hibernation. The lowest skin temperature recorded was 5.2°C, which corresponded to the lowest ambient temperature measurement of −5.8°C. Most bats chose tall, large, live Eucalyptus trees for roosting and to leave their roost for foraging on warmer days. Many individuals often switched roosts (every 3–5 days) and movements increased as spring approached (every 1–2 days). Our data suggest that V. vulturnus are capable of using the environmental temperature to gauge potential foraging opportunities and as a cue to reenter torpor when conditions are unsuitable. Importantly, frequent use of torpor and appropriate roost selection form key roles in the winter survival of these tiny bats

Geographical variation in the standard physiology of brushtail possums (Trichosurus): implications for conservation translocations

Identifying spatial patterns in the variation of physiological traits that occur within and between species is a fundamental goal of comparative physiology. There has been a focus on identifying and explaining this variation at broad taxonomic scales, but more recently attention has shifted to examining patterns of intra-specific physiological variation. Here we examine geographic variation in the physiology of brushtail possums (Trichosurus), widely distributed Australian marsupials, and discuss how pertinent intra-specific variation may be to conservation physiology. We found significant geographical patterns in metabolism, body temperature, evaporative water loss and relative water economy. These patterns suggest that possums from warmer, drier habitats have more frugal energy and water use and increased capacity for heat loss at high ambient temperatures. Our results are consistent with environmental correlates for broad-scale macro-physiological studies, and most intra-generic and intra-specific studies of marsupials and other mammals. Most translocations of brushtail possums occur into Australia\u27s arid zone, where the distribution and abundance of possums and other native mammals have declined since European settlement, leading to reintroduction programmes aiming to re-establish functional mammal communities. We suggest that the sub-species T. vulpecula hypoleucus from Western Australia would be the most physiologically appropriate for translocation to these arid habitats, having physiological traits most favourable for the extreme Ta, low and variable water availability and low productivity that characterize arid environments. Our findings demonstrate that geographically widespread populations can differ physiologically, and as a consequence some populations are more suitable for translocation to particular habitats than others. Consideration of these differences will likely improve the success and welfare outcomes of translocation, reintroduction and management programmes