To assess the vulnerability of birds and mammals to climate change recent studies have used the upper critical limit of thermoneutrality (TUC) as an indicator of thermal tolerance. But, the association between TUC and thermal tolerance is not straightforward and most studies describe TUC based solely on a deviation in metabolism from basal levels, without also considering the onset of evaporative cooling. It was argued recently that certain torpor-using bat species who survived prolonged exposure to high ambient temperatures (i.e. high thermal tolerance) experienced during extreme heat events did so by entering torpor and using facultative heterothermy to thermoconform and save on body water. Assuming that TUC is indicative of thermal tolerance, we expect TUC in torpor-using species to be higher than that of species which are obligate homeotherms, albeit that this distinction is based on confirmation of torpor use at low temperatures. To test this prediction, we performed a phylogenetically informed comparison of bat species known to use torpor (n = 48) and homeothermic (n = 16) bat species using published thermoregulatory datasets to compare the lower critical limit of thermoneutrality (TLC) and TUC in relation to body temperature. The influence of diet, biogeographical region, body mass and basal metabolic rate (BMR) was also considered. Body mass had a positive relationship with BMR, an inverse relationship with TLC and no relationship with TUC. Normothermic body temperature scaled positively with BMR, TLC and TUC. There was no relationship between diet or region and BMR, but both influenced thermal limits. Torpor-using bats had lower body mass and body temperatures than homeothermic bats, but there was no difference in BMR, TLC and TUC between them. Exceptional examples of physiological flexibility were observed in 34 torpor-using species and eight homeothermic species, which included 15 species of bats maintaining BMR-level metabolism at ambient temperatures as high as 40 °C (and corresponding body temperatures ∼39.2 °C). However, we argue that TUC based on metabolism alone is not an appropriate indicator of thermal tolerance as it disregards differences in the ability of animals to tolerate higher levels of hyperthermia, importance of hydration status and capacity for evaporative cooling. Also, the variability in TUC based on diet challenges the idea of evolutionary conservatism and warrants further consideration.

Torpor is an adaptive strategy allowing heterothermic animals to cope with energy limitations. In birds and mammals, intrinsic and extrinsic factors, such as body mass and ambient temperature, are the main variables influencing torpor use. Speakman and Thomas (2003) proposed a theoretical model of the relationship between the metabolic rate during torpor and the ambient temperature. Nevertheless, no empirical attempts have been made to assess the model predictions under different climates. Using open-flow respirometry, we evaluated the ambient temperature at which bats entered torpor and when torpid metabolic rate reached its minimum, the reduction in metabolic rate below basal values, and minimum torpid metabolic rate in 11 bat species of the family Vespertilionidae with different body mass from warm and cold climates. We included data on the minimum torpid metabolic rate of five species we retrieved from the literature. We tested the effects using mixed-effect phylogenetic models. All models showed a significant interaction between body mass and climate. Smaller bats went into torpor and reached minimum torpid metabolic rates at warmer temperatures, showed a higher reduction in the metabolic rate below basal values, and presented lower torpid metabolic rates than larger ones. The slopes of the models were different for bats from different climates. These results are likely explained by differences in body mass and the metabolic rate of bats, which may favor larger bats expressing torpor in colder sites and smaller bats in the warmer ones. Further studies to assess torpor use in bats of different climates are proposed.

Achieving a reversible decrease of metabolism and other physiological processes in the whole organism, as occurs in animals that experience torpor or hibernation, could contribute to increased survival after serious injury. Using a Bayesian network tool with transcriptomic data and chemical structure similarity assessments, we predicted that the Alzheimer\'s disease drug donepezil (DNP) could be a promising candidate for a small molecule drug that might induce a torpor-like state. This was confirmed in a screening study with Xenopus laevis tadpoles, a nonhibernator whole animal model. To improve the therapeutic performance of the drug and minimize its toxicity, we encapsulated DNP in a nanoemulsion formulated with low-toxicity materials. This formulation is composed of emulsified droplets <200 nm in diameter that contain 1.250 mM DNP, representing ≥95% encapsulation efficiency. The DNP nanoemulsion induced comparable torpor-like effects to those produced by the free drug in tadpoles, as indicated by reduced swimming motion, cardiac beating frequency, and oxygen consumption, but with an improved biodistribution. Use of the nanoemulsion resulted in a more controlled increase of DNP concentration in the whole organism compared to free DNP, and to a higher concentration in the brain, which reduced DNP toxicity and enabled induction of a longer torpor-like state that was fully reversible. These studies also demonstrate the potential use of Xenopus tadpoles as a high-throughput in vivo screen to assess the efficacy, biodistribution, and toxicity of drug-loaded nanocarriers.

The dwarf lemurs (Cheirogaleus spp.) of Madagascar are the only obligate hibernators among primates. Despite century-old field accounts of seasonal lethargy, and more recent evidence of hibernation in the western fat-tailed dwarf lemur (Cheirogaleus medius), inducing hibernation in captivity remained elusive for decades. This included the Duke Lemur Center (DLC), which maintains fat-tailed dwarf lemurs and has produced sporadic research on reproduction and metabolism. With cumulative knowledge from the field, a newly robust colony, and better infrastructure, we recently induced hibernation in DLC dwarf lemurs. We describe two follow-up experiments in subsequent years. First, we show that dwarf lemurs under stable cold conditions (13°C) with available food continued to eat daily, expressed shallower and shorter torpor bouts, and had a modified gut microbiome compared to peers without food. Second, we demonstrate that dwarf lemurs under fluctuating temperatures (12-30°C) can passively rewarm daily, which was associated with altered patterns of fat depletion and reduced oxidative stress. Despite the limitations of working with endangered primates, we highlight the promise of studying hibernation in captive dwarf lemurs. Follow-up studies on genomics and epigenetics, metabolism, and endocrinology could have relevance across multidisciplinary fields, from biomedicine to evolutionary biology, and conservation.

Fine-scale variation in microclimates between habitats may impact energy consumption for the organisms that inhabit them. This may be particularly important for sedentary species or those unable to change habitats for long periods, such as hibernators. Low ambient temperatures were traditionally thought key to microclimatic selection for hibernation locations, but recent research suggests that other factors may contribute or exceed ambient temperature in importance. We aimed to characterise microclimates at hibernacula of wild hibernating hazel dormice Muscardinus avellanarius, and test how these microclimates differ to those at locations without hibernacula using a microclimatic modelling approach. Dormice hibernated in areas with warmer soil temperatures and lower variability in humidity and relative shortwave radiation. These results add to the growing body of evidence that low ambient temperatures may not be the primary driver of hibernation microclimate selection, although temperature is still likely to play an important role. We also found that ambient temperatures measured at the microclimatic level were substantially buffered compared to point samples taken at the nearest weather station (∼1.6 km away), highlighting the importance of considering microclimates in wildlife conservation in the face of future environmental change.

Although Mexico holds the southernmost hibernating bats in North America, information on winter behavior and hibernacula microclimate use of temperate Mexican bats is limited. We studied hibernating bats at high altitudes (>1,000 m a.s.l.) in northern and central Mexico during 5 consecutive winters. Our aims were to document and describe the hibernacula, winter behavior (such as abundance and roost pattern), and microclimates (estimated as adjacent substrate temperature) of cave-hibernating bats in Mexico. We found 78 hibernacula and 6,089 torpid bats of 10 vespertilionid species, increasing by over 50% the number of cave-hibernating bat species and quadrupling the number of hibernacula for Mexico. Hibernacula were at altitudes between 1,049 and 3,633 m a.s.l., located in 3 mountain ranges, mainly in oak and conifer forests. Myotis velifer was the most common species, followed by Corynorhinus townsendii and C. mexicanus. We recorded the adjacent substrate temperatures from 9 species totaling 1,106 torpid bats and found differences in microclimate use among the 3 most common species. In general, abundance of torpid bats in our region of study was similar to those in the western United States, with aggregations of tens to a few hundred individuals per cave, and was lower than in the eastern United States where a cave may hold thousands of individuals. Knowledge of bat hibernation is crucial for developing conservation and management strategies on current conditions while accommodating environmental changes and other threats such as emerging diseases.
Aunque México tiene los murciélagos hibernantes más sureños en Norteamérica, la información sobre el comportamiento invernal y el uso de microclimas en los refugios de hibernación de los murciélagos templados mexicanos es limitada. Estudiamos a los murciélagos hibernantes en altitudes altas (>1000 msnm) en el norte y centro de México durante cinco inviernos consecutivos. Nuestros objetivos fueron documentar y describir las cuevas de hibernación, el comportamiento invernal (como la abundancia y patrón de percha), y el uso de microclimas (estimado como la temperatura del sustrato adyacente), de los murciélagos que hibernan en cuevas en México. Encontramos 78 cuevas de hibernación con 6089 murciélagos en torpor de 10 especies de vespertiliónidos, incrementando en más del 50% el número de especies de murciélagos que hibernan en cuevas y cuadriplicando el número de cuevas de hibernación para México. Las cuevas de hibernación estuvieron en elevaciones entre 1049 y 3633 msnm, localizadas en tres cadenas montañosas, principalmente en bosques de encinos y coníferas. Myotis velifer fue la especie más común, seguida por Corynorhinus townsendii y C. mexicanus. Reportamos las temperaturas del sustrato adyacente de 1106 murciélagos en torpor de nueve especies y encontramos diferencias en el uso de microclimas entre las tres especies más comunes. Aquí proveemos información relevante para especies de murciélagos templados en la ocurrencia más sureña de hibernación de murciélagos en Norteamérica. En general, la abundancia de murciélagos en torpor que encontramos fue similar a las del oeste de Estados Unidos, con agregaciones de decenas y algunos cientos de individuos por cueva; y fue menor que las del este de Estados Unidos, donde las cuevas pueden albergar miles de murciélagos. El conocimiento de la hibernación de murciélagos es crucial para el desarrollo de estrategias de conservación y manejo adecuadas en la actualidad y mientras se adaptan a los cambios ambientales y a otras amenazas tales como las enfermedades emergentes.

Seasonal variation in animal activity influences fitness and the intensity of ecological interactions (e.g., competition, predation), yet aspects of global change in the Anthropocene may catalyze shifts in seasonal activity. Invasive plants are components of global change and can modify animal daily activity, but their influence on animal seasonal activity is less understood. We examined how invasive woody shrubs (Autumn olive [Elaeagnus umbellata] and Amur honeysuckle [Lonicera maackii]) affect seasonal activity of three common small-mammal species by coupling experimental shrub removal with autumnal camera trapping for two consecutive years at six paired forest sites (total 12 plots). Eastern chipmunks (Tamias striatus) foraged more, and foraging was observed at least 20 days longer, in shrub-invaded forests. White-footed mice (Peromyscus leucopus) foraged more in invaded than cleared plots in one study year, but P. leucopus autumn activity timing did not differ between shrub-removal treatments. Fox squirrel (Sciurus niger) activity displayed year-specific responses to shrub removal suggesting intraannual cues (e.g., temperature) structure S. niger autumnal activity. Our work highlights how plant invasions can have species-specific effects on seasonal animal activity, may modify the timing of physiological processes (e.g., torpor), and could generate variation in animal-mediated interactions such as seed dispersal or granivory.

Torpor is widespread among bats presumably because most species are small, and torpor greatly reduces their high mass-specific resting energy expenditure, especially in the cold. Torpor has not been recorded in any bat species larger than 50 g, yet in theory could be beneficial even in the world\'s largest bats (flying-foxes; Pteropus spp.) that are exposed to adverse environmental conditions causing energy bottlenecks. We used temperature telemetry to measure body temperature in wild-living adult male grey-headed flying-foxes (P. poliocephalus; 799 g) during winter in southern Australia. We found that all individuals used torpor while day-roosting, with minimum body temperature reaching 27°C. Torpor was recorded following a period of cool, wet and windy weather, and on a day with the coldest maximum air temperature, suggesting it is an adaptation to reduce energy expenditure during periods of increased thermoregulatory costs and depleted body energy stores. A capacity for torpor among flying-foxes has implications for understanding their distribution, behavioural ecology and life history. Furthermore, our discovery increases the body mass of bats known to use torpor by more than tenfold and extends the documented use of this energy-saving strategy under wild conditions to all bat superfamilies, with implications for the evolutionary maintenance of torpor among bats and other mammals.

Understanding how animals meet their daily energy requirements is critical in our rapidly changing world. Small organisms with high metabolic rates can conserve stored energy when food availability is low or increase energy intake when energetic requirements are high, but how they balance this in the wild remains largely unknown. Using miniaturized heart rate transmitters, we continuously quantified energy expenditure, torpor use and foraging behaviour of free-ranging male bats (Nyctalus noctula) in spring and summer. In spring, bats used torpor extensively, characterized by lowered heart rates and consequently low energy expenditures. In contrast, in summer, bats consistently avoided torpor, even though they could have used this low-energy mode. As a consequence, daytime heart rates in summer were three times as high compared with the heart rates in spring. Daily energy use increased by 42% during summer, despite lower thermogenesis costs at higher ambient temperatures. Likely, as a consequence, bats nearly doubled their foraging duration. Overall, our results indicate that summer torpor avoidance, beneficial for sperm production and self-maintenance, comes with a high energetic cost. The ability to identify and monitor such vulnerable energetic life-history stages is particularly important to predict how species will deal with increasing temperatures and changes in their resource landscapes.

Ultradian rhythms of metabolism, body temperature and activity are attenuated or disappear completely during torpor in Djungarian hamsters, for all three ultradian periodicities (URsmall, URmedium and URlarge). URsmall and URmedium disappear during entrance into torpor, whereas URlarge disappear later or continue with a low amplitude. This suggests a tight functional link between torpor and the expression of ultradian rhythms, i.e. torpor is achieved by suppression of metabolic rate as well as silencing of ultradian rhythms. Spontaneous torpor is often initiated after an ultradian burst of activity and metabolic rate, beginning with a period of motionless rest and accompanied by a decrease of metabolic rate and body temperature. To extend previous findings on the potential role of the adrenergic system on torpor induction we analysed the influence of the ß3-adrenergic agonist Mirabegron on torpor in Djungarian hamsters, as compared to the influence of the ß-adrenergic antagonist Propranolol. Hamsters were implanted with 10 day release pellets of Mirabegron (0.06 mg day-1) or Propranolol (0.3 mg day-1). Mirabegron transiently supressed and accelerated ultradian rhythms but had no effect on torpor behaviour. Propranolol did not affect torpor behaviour nor the expression of ultradian rhythms with the dosage applied during this study.