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.     

Heterothermy in large mammals: inevitable or implemented?

Advances in biologging techniques over the past 20 years have allowed for the remote and continuous measurement of body temperatures in free‐living mammals. While there is an abundance of literature on heterothermy in small mammals, fewer studies have investigated the daily variability of body core temperature in larger mammals. Here we review measures of heterothermy and the factors that influence heterothermy in large mammals in their natural habitats, focussing on large mammalian herbivores. The mean 24 h body core temperatures for 17 species of large mammalian herbivores (>10 kg) decreased by ～1.3°C for each 10‐fold increase in body mass, a relationship that remained significant following phylogenetic correction. The degree of heterothermy, as measured by the 24 h amplitude of body core temperature rhythm, was independent of body mass and appeared to be driven primarily by energy and water limitations. When faced with the competing demands of osmoregulation, energy acquisition and water or energy use for thermoregulation, large mammalian herbivores appear to relax the precision of thermoregulation thereby conserving body water and energy. Such relaxation may entail a cost in that an animal moves closer to its thermal limits for performance. Maintaining homeostasis requires trade‐offs between regulated systems, and homeothermy apparently is not accorded the highest priority; large mammals are able to maintain optimal homeothermy only if they are well nourished, hydrated, and not compromised energetically. We propose that the amplitude of the 24 h rhythm of body core temperature provides a useful index of any compromise experienced by a free‐living large mammal and may predict the performance and fitness of an animal.     

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Many tropical mammals are vulnerable to heat because their water budget limits the use of evaporative cooling for heat compensation. Further increasing temperatures and aridity might consequently exceed their thermoregulatory capacities. Here, we describe two novel modes of torpor, a response usually associated with cold or resource bottlenecks, as efficient mechanisms to counter heat. We conducted a field study on the Malagasy bat Macronycteris commersoni resting in foliage during the hot season, unprotected from environmental extremes. On warm days, the bats alternated between remarkably short micro-torpor bouts and normal resting metabolism within a few minutes. On hot days, the bats extended their torpor bouts over the hottest time of the day while tolerating body temperatures up to 42.9°C. Adaptive hyperthermia combined with lowered metabolic heat production from torpor allows higher heat storage from the environment, negates the need for evaporative cooling and thus increases heat tolerance. However, it is a high-risk response as the torpid bats cannot defend body temperature if ambient temperature increases above a critical/lethal threshold. Torpor coupled with hyperthermia and micro-torpor bouts broaden our understanding of the basic principles of thermal physiology and demonstrate how mammals can perform near their upper thermal limits in an increasingly warmer world.     

Evidence from Tarentola mauritanica (Gekkota: Phyllodactylidae) helps validate thermography as a tool to infer internal body temperatures of lizards

Infrared (IR) thermal imaging has become an increasingly popular tool to measure body temperature of animals. The high-resolution data it provides with short lag and minimum disturbance makes it an appealing tool when studying reptile thermal ecology. However, due to the common phenomenon of regional heterothermy and surface-to-core temperature gradients, it is essential to select the appropriate body part to measure and provide calibrations to accurately infer internal body temperatures. This work follows from a previous study on lacertid lizards to assess the reliability of thermography-measured body temperatures, from several body locations, as a proxy for internal body temperature in lizards. This study focuses on the Moorish gecko, Tarentola mauritanica, due to its distant phylogenetic relationship and its different ecology and morphology from the previously tested species. A total of 60 adult geckos of both sexes and of a range of sizes were tested in thermal gradients and subjected to a sequence of randomly assorted treatments of heating and cooling. The temperatures of the animals were periodically measured with a thermal camera at six different body parts and, immediately after, the cloacal temperature was then measured with a thermocouple probe. Body parts’ temperatures, obtained thermographically, were regressed against cloacal temperature using OLS regression and the pairwise correlations were tested using Spearman coefficients. Relationships among all body parts and between all body parts and the cloaca were strong in all cases (R² > 0.87, Spearman Correlation > 0.95). The observed pattern was very similar to those previously obtained from lacertid lizards. Ultimately, the eye proved to provide the best overall proxy for internal temperature, when accounting for both the slope and intercept of the regression. Hence, this study provides further support for the establishment of the eye as the standard location to infer internal body temperatures of lizards through thermography.     

Body mass affects short-term heterothermy in Neotropical bats

Recent work in Australia and Africa has shown that heterothermy is widespread among phylogenetically diverse tropical and subtropical mammalian taxa. However, data on the use of heterothermy by Neotropical mammals are relatively scant, and those studies that exist focus on insect-eating bats. We investigated the capacity of fruit-eating Neotropical bats to use heterothermy when exposed to acute cold temperatures, and compared this to previous data focused on insect-eating bats sampled from the same region and time of year. We measured rectal temperatures prior to acute cold exposure (1 hr at an air temperature of 6, 7, or 10°C), and again after exposure. Our data show considerable variation in the thermoregulatory patterns of Neotropical bats, and generally, our results show that smaller bats cool quicker and to a greater extent than larger bats. Our results highlight the importance of energy conservation even in environments in which resources are relatively abundant.     

Effects of reproductive condition,roost microclimate,and weather patterns on summer torpor use by a vespertilionid bat

A growing number of mammal species are recognized as heterothermic, capable of maintaining a high‐core body temperature or entering a state of metabolic suppression known as torpor. Small mammals can achieve large energetic savings when torpid, but they are also subject to ecological costs. Studying torpor use in an ecological and physiological context can help elucidate relative costs and benefits of torpor to different groups within a population. We measured skin temperatures of 46 adult Rafinesque's big‐eared bats (Corynorhinus rafinesquii) to evaluate thermoregulatory strategies of a heterothermic small mammal during the reproductive season. We compared daily average and minimum skin temperatures as well as the frequency, duration, and depth of torpor bouts of sex and reproductive classes of bats inhabiting day‐roosts with different thermal characteristics. We evaluated roosts with microclimates colder (caves) and warmer (buildings) than ambient air temperatures, as well as roosts with intermediate conditions (trees and rock crevices). Using Akaike's information criterion (AIC), we found that different statistical models best predicted various characteristics of torpor bouts. While the type of day‐roost best predicted the average number of torpor bouts that bats used each day, current weather variables best predicted daily average and minimum skin temperatures of bats, and reproductive condition best predicted average torpor bout depth and the average amount of time spent torpid each day by bats. Finding that different models best explain varying aspects of heterothermy illustrates the importance of torpor to both reproductive and nonreproductive small mammals and emphasizes the multifaceted nature of heterothermy and the need to collect data on numerous heterothermic response variables within an ecophysiological context.     

Can heterothermy facilitate the colonization of new habitats?

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Body size phenology in a regional bee fauna: a temporal extension of Bergmann's rule

Bergmann's rule originally described a positive relationship between body size and latitude in warm‐blooded animals. Larger animals, with a smaller surface/volume ratio, are better enabled to conserve heat in cooler climates (thermoregulatory hypothesis). Studies on endothermic vertebrates have provided support for Bergmann's rule, whereas studies on ectotherms have yielded conflicting results. If the thermoregulatory hypothesis is correct, negative relationships between body size and temperature should occur in temporal in addition to geographical gradients. To explore this possibility, we analysed seasonal activity patterns in a bee fauna comprising 245 species. In agreement with our hypothesis of a different relationship for large (endothermic) and small (ectothermic) species, we found that species larger than 27.81 mg (dry weight) followed Bergmann's rule, whereas species below this threshold did not. Our results represent a temporal extension of Bergmann's rule and indicate that body size and thermal physiology play an important role in structuring community phenology.     

Heterothermy,body size,and locomotion as ecological predictors of migration in mammals

1. Migration is ubiquitous among animals and has evolved repeatedly and independently. Comparative studies of the evolutionary origins of migration in birds are widespread, but are lacking in mammals. Mammalian species have greater variation in functional traits that may be relevant for migration. Interspecific variation in migration behaviour is often attributed to mode of locomotion (i.e. running, swimming, and flying) and body size, but traits associated with the evolutionary precursor hypothesis, including geographic distribution, habitat, and diet, could also be important predictors of migration in mammals. Furthermore, mammals vary in thermoregulatory strategies and include many heterothermic species, providing an alternative strategy to avoid seasonal resource depletion.
2. We tested the evolutionary precursor hypothesis for the evolution of migration in mammals and tested predictions linking migration to locomotion, body size, geographic distribution, habitat, diet, and thermoregulation. We compiled a dataset of 722 species from 27 mammalian orders and conducted a series of analyses using phylogenetically informed models.
3. Swimming and flying mammals were more likely to migrate than running mammals, and larger species were more likely to migrate than smaller ones. However, heterothermy was common among small running mammals that were unlikely to migrate. High-latitude swimming and flying mammals were more likely to migrate than high-latitude running mammals (where heterothermy was common), and most migratory running mammals were herbivorous. Running mammals and frugivorous bats with high thermoregulatory scope (greater capacity for heterothermy) were less likely to migrate, while insectivorous bats with high thermoregulatory scope were more likely to migrate.
4. Our results indicate a broad range of factors that influence migration, depending on locomotion, body size, and thermoregulation. Our analysis of migration in mammals provided insight into some of the general rules of migration, and we highlight opportunities for future investigations of exceptions to these rules, ultimately leading to a comprehensive understanding of the evolution of migration.