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Migration is a widespread and highly variable trait among animals. Population-level patterns arise from individual-level decisions, including physiological and energetic constraints. Many aspects of migration are influenced by behaviors and strategies employed during periods of stopover, where migrants may encounter variable or unpredictable conditions. Thermoregulation can be a major cost for homeotherms which largely encounter ambient temperatures below the lower critical temperature during migration, especially during the rest phase of the daily cycle. In this review we describe the empirical evidence, theoretical models, and potential implications of bats and birds that use heterothermy to reduce thermoregulatory costs during migration. Torpor-assisted migration is a strategy described for migrating temperate insectivorous bats, whereby torpor can be used during periods of inactivity to drastically reduce thermoregulatory costs and increase net refueling rate, leading to shorter stopover duration, reduced fuel load requirement, and potential consequences for broad-scale movement patterns and survival. Hummingbirds can adopt a similar strategy, but most birds are not capable of torpor. However, there is an increasing recognition of the use of more shallow heterothermic strategies by diverse bird species during migration, with similarly important implications for migration energetics. A growing body of published literature and preliminary data from ongoing research indicate that heterothermic migration strategies in birds may be more common than traditionally appreciated. We further take a broad evolutionary perspective to consider heterothermy as an alternative to migration in some species, or as a conceptual link to consider alternatives to seasonal resource limitations. There is a growing body of evidence related to heterothermic migration strategies in bats and birds, but many important questions related to the broader implications of this strategy remain., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

AbstractHibernation requires balancing energy and water demands over several months. Many studies have noted the importance of fat for hibernation energy budgets, but protein catabolism in hibernation has received less attention, and whole-animal changes in lean mass have not previously been considered. We used quantitative magnetic resonance body composition analysis to measure deposition of fat and lean mass of cave myotis ( Myotis velifer ) during the prehibernation period and decreases in fat and lean mass of Townsend's big-eared bats ( Corynorhinus townsendii ) during hibernation. For cave myotis, lean mass represented 25% and 38% (female and male, respectively) of prehibernation mass gain. In hibernating Townsend's big-eared bats, lean mass decrease was similar for females and males. We used values for Townsend's big-eared bats to explore the functional implications of lean mass change for water and energy budgets. Lean mass accounted for a substantial proportion of mass change during hibernation (female: 18%, male: 35%), and although not accounting for a large proportion of the energy budget (female: 3%, male: 7%), lean mass catabolism represented an important contribution to water production (female: 14%, male: 29%). Although most mammals cannot rely on protein catabolism for metabolic water production because of the water cost of excreting urea, we propose a variation of the protein-for-water strategy whereby hibernators could temporally compartmentalize the benefits of protein catabolism to periods of torpor and the water cost to periodic arousals when free drinking water is typically available. Combined, our analyses demonstrate the importance of considering changes in lean mass during hibernation.

Disease results from interactions among the host, pathogen, and environment. Inoculation trials can quantify interactions among these players and explain aspects of disease ecology to inform management in variable and dynamic natural environments. White-nose Syndrome, a disease caused by the fungal pathogen, Pseudogymnoascus destructans (Pd), has caused severe population declines of several bat species in North America. We conducted the first experimental infection trial on the tri-colored bat, Perimyotis subflavus, to test the effect of temperature and humidity on disease severity. We also tested the effects of temperature and humidity on fungal growth and persistence on substrates. Unexpectedly, only 37% (35/95) of bats experimentally inoculated with Pd at the start of the experiment showed any infection response or disease symptoms after 83 days of captive hibernation. There was no evidence that temperature or humidity influenced infection response. Temperature had a strong effect on fungal growth on media plates, but the influence of humidity was more variable and uncertain. Designing laboratory studies to maximize research outcomes would be beneficial given the high costs of such efforts and potential for unexpected outcomes. Understanding the influence of microclimates on host-pathogen interactions remains an important consideration for managing wildlife diseases, particularly in variable environments., (© 2022. The Author(s).)

Species with broad geographic ranges may experience varied environmental conditions throughout their range leading to local adaptation. Variation among populations reflects potential adaptability or plasticity, with implications for populations impacted by disease, climate change, and other anthropogenic influences. However, behavior may counteract divergent selection among populations. We studied intraspecific variation in hibernation physiology of Myotis lucifugus (little brown myotis) and Corynorhinus townsendii (Townsend's big-eared bat), two species of bats with large geographic ranges. We studied M. lucifugus at three hibernacula which spanned a latitudinal gradient of 1500 km, and C. townsendii from 6 hibernacula spread across 1200 km latitude and 1200 km longitude. We found no difference in torpid metabolic rate among populations of either species, nor was there a difference in the effect of ambient temperature among sites. Evaporative water loss was similar among populations of both species, with the exception of one C. townsendii pairwise site difference and one M. lucifugus site that differed from the others. We suggest the general lack of geographic variation is a consequence of behavioral microhabitat selection. As volant animals, bats can travel relatively long distances in search of preferred microclimates for hibernation. Despite dramatic macroclimate differences among populations, hibernating bats are able to find preferred microclimate conditions within their range, resulting in similar selection pressures among populations spread across wide geographic ranges., (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Hibernation is widespread among mammals in a variety of environmental contexts. However, few experimental studies consider interspecific comparisons, which may provide insight into general patterns of hibernation strategies. We studied 13 species of free-living bats, including populations spread over thousands of kilometers and diverse habitats. We measured torpid metabolic rate (TMR) and evaporative water loss (two key parameters for understanding hibernation energetics) across a range of temperatures. There was no difference in minimum TMR among species (i.e., all species achieved similarly low torpid metabolic rate) but the temperature associated with minimum TMR varied among species. The minimum defended temperature (temperature below which TMR increased) varied from 8 °C to < 2 °C among species. Conversely, evaporative water loss varied among species, with species clustered in two groups representing high and low evaporative water loss. Notably, species that have suffered population declines due to white-nose syndrome fall in the high evaporative water loss group and less affected species in the low evaporative water loss group. Documenting general patterns of physiological diversity, and associated ecological implications, contributes to broader understanding of biodiversity, and may help predict which species are at greater risk of environmental and anthropogenic stressors., (© 2021. The Author(s).)

White-nose syndrome (WNS) has decimated hibernating bat populations across eastern and central North America for over a decade. Disease severity is driven by the interaction between bat characteristics, the cold-loving fungal agent, and the hibernation environment. While we further improve hibernation energetics models, we have yet to examine how spatial heterogeneity in host traits is linked to survival in this disease system. Here, we develop predictive spatial models of body mass for the little brown myotis ( Myotis lucifugus ) and reassess previous definitions of the duration of hibernation of this species. Using data from published literature, public databases, local experts, and our own fieldwork, we fit a series of generalized linear models with hypothesized abiotic drivers to create distribution-wide predictions of prehibernation body fat and hibernation duration. Our results provide improved estimations of hibernation duration and identify a scaling relationship between body mass and body fat; this relationship allows for the first continuous estimates of prehibernation body mass and fat across the species' distribution. We used these results to inform a hibernation energetic model to create spatially varying fat use estimates for M. lucifugus . These results predict WNS mortality of M. lucifugus populations in western North America may be comparable to the substantial die-off observed in eastern and central populations., Competing Interests: The authors claim no conflict of interest., (© 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Energy conservation has long been a focal point in hibernation research. A long-standing assumption is that ambient temperature (Ta) largely defines the rate of energy expenditure because of well-known relationships between Ta, metabolic rate and frequency of arousal from torpor. Body condition and humidity also affect energy expenditure but are usually considered secondary factors. We held tricolored bats (Perimyotis subflavus) in captivity under multiple environmental conditions to directly compare the importance of Ta, fat mass and humidity for hibernation energy expenditure. Fat mass was the best predictor of female mass loss, followed by Ta and humidity. However, males had less fat and adopted a more energetically conservative hibernation strategy. Our results demonstrate that understanding the evolution of behavior, physiology and ecology of hibernation requires disentangling the relative contributions of multiple drivers of hibernation energetics, and that Ta is not always the most important factor driving energy expenditure., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Multidisciplinary approaches to conservation and wildlife management are often effective in addressing complex, multi-factor problems. Emerging fields such as conservation physiology and conservation behaviour can provide innovative solutions and management strategies for target species and systems. Sensory ecology combines the study of 'how animals acquire' and process sensory stimuli from their environments, and the ecological and evolutionary significance of 'how animals respond' to this information. We review the benefits that sensory ecology can bring to wildlife conservation and management by discussing case studies across major taxa and sensory modalities. Conservation practices informed by a sensory ecology approach include the amelioration of sensory traps, control of invasive species, reduction of human-wildlife conflicts and relocation and establishment of new populations of endangered species. We illustrate that sensory ecology can facilitate the understanding of mechanistic ecological and physiological explanations underlying particular conservation issues and also can help develop innovative solutions to ameliorate conservation problems., (© The Author(s) 2021. Published by Oxford University Press and the Society for Experimental Biology.)

Processes associated with recovery of survivors are understudied components of wildlife infectious diseases. White-nose syndrome (WNS) in bats provides an opportunity to study recovery of disease survivors, understand implications of recovery for individual energetics, and assess the role of survivors in pathogen transmission. We documented temporal patterns of recovery from WNS in little brown bats ( Myotis lucifugus ) following hibernation to test the hypotheses that: (1) recovery of wing structure from WNS matches a rapid time scale (i.e. approximately 30 days) suggested by data from free-ranging bats; (2) torpor expression plays a role in recovery; (3) wing physiological function returns to normal alongside structural recovery; and (4) pathogen loads decline quickly during recovery. We collected naturally infected bats at the end of hibernation, brought them into captivity, and quantified recovery over 40 days by monitoring body mass, wing damage, thermoregulation, histopathology of wing biopsies, skin surface lipids and fungal load. Most metrics returned to normal within 30 days, although wing damage was still detectable at the end of the study. Torpor expression declined overall throughout the study, but bats expressed relatively shallow torpor bouts - with a plateau in minimum skin temperature - during intensive healing between approximately days 8 and 15. Pathogen loads were nearly undetectable after the first week of the study, but some bats were still detectably infected at day 40. Our results suggest that healing bats face a severe energetic imbalance during early recovery from direct costs of healing and reduced foraging efficiency. Management of WNS should not rely solely on actions during winter, but should also aim to support energy balance of recovering bats during spring and summer., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2020. Published by The Company of Biologists Ltd.)

Hibernation consists of extended durations of torpor interrupted by periodic arousals. The 'dehydration hypothesis' proposes that hibernating mammals arouse to replenish water lost through evaporation during torpor. Arousals are energetically expensive, and increased arousal frequency can alter survival throughout hibernation. Yet we lack a means to assess the effect of evaporative water loss (EWL), determined by animal physiology and hibernation microclimate, on torpor bout duration and subsequent survival. White-nose syndrome (WNS), a devastating disease impacting hibernating bats, causes increased frequency of arousals during hibernation and EWL has been hypothesized to contribute to this increased arousal frequency. WNS is caused by a fungus, which grows well in humid hibernaculum environments and damages wing tissue important for water conservation. Here, we integrated the effect of EWL on torpor expression in a hibernation energetics model, including the effects of fungal infection, to determine the link between EWL and survival. We collected field data for Myotis lucifugus, a species that experiences high mortality from WNS, to gather parameters for the model. In saturating conditions, we predicted healthy bats experience minimal mortality. Infected bats, however, suffer high fungal growth in highly saturated environments, leading to exhaustion of fat stores before spring. Our results suggest that host adaptation to humid environments leads to increased arousal frequency from infection, which drives mortality across hibernaculum conditions. Our modified hibernation model provides a tool to assess the interplay between host physiology, hibernaculum microclimate, and diseases such as WNS on winter survival., Competing Interests: The authors have declared that no competing interests exist.

As organisms face variation in energetic challenges and physiological demands, they often respond with reversible changes in behavior, physiology, and morphology, described as phenotypic flexibility. From the magnitude of phenotypic change, we can infer the energetic challenges of different life stages. We studied phenotypic flexibility in a population of reproductive and pre-migratory female insectivorous bats (Tadarida brasiliensis). While female reproductive demands are well described in insectivorous bats, there are questions regarding the demands of migration. Our objective was to measure phenotypic flexibility to assess the cost of autumn migration compared to reproduction in an insectivorous bat. We measured plasma triglycerides to quantify foraging rate, and body composition (body mass and individual organ mass) of T. brasiliensis throughout the summer season (from arrival in spring through pre-migration/migration departure in autumn) according to the female reproductive cycle. We found phenotypic changes during pre-migration/migration similar to periods of high-energy demand during reproduction (e.g., late pregnancy and lactation). Most notably, bats weighed as much during peak pregnancy, as they did during migration, and the rapid mass gain from post-lactation through the migratory period was due to a combination of hyperphagia and hypertrophy of digestive organs. Our results indicate that energetic demands incurred during migration are similar to those during reproduction and emphasize the energetic challenges of migration.

As small, flying, mammalian endotherms, insectivorous bats are adapted to operate at high levels of energy expenditure. In response to seasonally variable challenges, we predicted that bats should balance energy budgets by flexibly adjusting aspects of their physiology or behavior in ways that elevate metabolic capacity. We examined variation in energy storage and pathways for oxidative metabolism in Brazilian free-tailed bats ( Tadarida brasiliensis ) related to estimated costs associated with reproduction and migration. We collected pectoral muscle and liver from female T. brasiliensis at six time points during the summer and fall and measured changes in the activity of four enzymes involved with lipid metabolism. Body mass varied substantially with life-cycle stage, suggesting that rapid accumulation and use of fat stores occurs in response to current and anticipated energy demands. Catabolic enzyme activity (carnitine palmitoyl transferase [CPT], 3-hydroxyacyl-CoA dehydrogenase [HOAD], and citrate synthase [CS]) in the muscle was increased during lactation compared with early pregnancy but exhibited no change before fall migration. While there was no temporal change in lipid biosynthetic capacity in the liver, fatty acid synthase activity was negatively correlated with body mass. Variation in body mass and enzyme activity in T. brasiliensis during the summer suggests that stored energy is mobilized and lipid oxidative capacity is increased during periods of increased demand and that lipid biosynthetic capacity is increased with depletion of fat stores. These results suggest that bats are able to flexibly adjust metabolic capacity based on energy requirement to maintain energy balance despite high levels of expenditure.

Plasma metabolite concentrations can be used to understand nutritional status and foraging behavior across ecological contexts including prehibernation fattening, migration refueling, and variation in foraging habitat quality. Generally, high plasma concentrations of the ketone β-hydroxybutyrate, a product of fat catabolism, indicate fasting, while triglycerides indicate recent feeding and fat accumulation. In recent studies of insectivorous bats, triglyceride concentration increased after feeding as expected, but β-hydroxybutyrate also unexpectedly increased rather than decreased. An aerial-hawking foraging strategy is energetically demanding, and thus it has been hypothesized that foraging by insectivorous bats requires catabolism of stored fat. We tested this hypothesis by quantifying plasma β-hydroxybutyrate and triglyceride concentration following feeding in little brown bats ( Myotis lucifugus ) that were temporarily housed in individual cages to prevent flight. We provided a fixed amount of food and collected blood samples at different intervals after feeding to produce variation in plasma metabolite concentrations. Plasma triglyceride concentration responded as predicted, but similar to previous studies and contrary to our prediction, when flight was eliminated plasma β-hydroxybutyrate concentration responded similarly to triglyceride. Thus, it is unlikely that the unexpected plasma β-hydroxybutyrate patterns observed in previous studies were related to flight. The mechanism underlying this unexpected pattern remains unknown, but the response has been consistent in all studies to date. Thus, plasma metabolite analysis provides an effective tool for studies of nutritional status, although more work is needed to understand why insectivorous bats respond differently than other taxa.

Many species use stored energy to hibernate through periods of resource limitation. Hibernation, a physiological state characterized by depressed metabolism and body temperature, is critical to winter survival and reproduction, and therefore has been extensively quantified and modeled. Hibernation consists of alternating phases of extended periods of torpor (low body temperature, low metabolic rate), and energetically costly periodic arousals to normal body temperature. Arousals consist of multiple phases: warming, euthermia, and cooling. Warming and euthermic costs are regularly included in energetic models, but although cooling to torpid body temperature is an important phase of the torpor-arousal cycle, it is often overlooked in energetic models. When included, cooling cost is assumed to be 67% of warming cost, an assumption originally derived from a single study that measured cooling cost in ground squirrels. Since this study, the same proportional value has been assumed across a variety of hibernating species. However, no additional values have been derived. We derived a model of cooling cost from first principles and validated the model with empirical energetic measurements. We compared the assumed 67% proportional cooling cost with our model-predicted cooling cost for 53 hibernating mammals. Our results indicate that using 67% of warming cost only adequately represents cooling cost in ground squirrel-sized mammals. In smaller species, this value overestimates cooling cost and in larger species, the value underestimates cooling cost. Our model allows for the generalization of energetic costs for multiple species using species-specific physiological and morphometric parameters, and for predictions over variable environmental conditions., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Fungi are increasingly recognised as harmful pathogens of wildlife. White-nose syndrome (WNS) is a fungal disease that has killed millions of hibernating bats in North America. High mortality has driven research to identify management strategies for the disease. Increased energy expenditure and fat depletion, as well as fluid loss, hypotonic dehydration and electrolyte depletion appear to be key aspects of WNS pathophysiology. Bats with WNS spend energy too quickly and also lose fluids containing water and electrolytes from lesions on exposed skin surfaces. During periodic arousals, bats often drink water but, in most of the WNS-affected area, food is not available during winter and, therefore, they cannot maintain energy balance or replace lost electrolytes. Therefore, providing a liquid caloric/electrolyte/nutrient supplement could be useful for treating WNS. We studied captive, hibernating little brown bats ( Myotis lucifugus ) to test whether providing supplemental energy and electrolytes (a 1:1 dilution of unflavoured Pedialyte) to hibernating bats could reduce severity of WNS symptoms and increase survival. Infected bats in the Pedialyte-supplemented group generally avoided the Pedialyte and preferentially drank plain water. We did not observe any differences in survival, arousal frequency or blood chemistry, but bats in the Pedialyte-supplemented group had higher fungal load and more UV fluorescence than the control group that was only provided with water. Supplemental electrolytes would be an attractive management strategy because of their low cost and logistic feasibility but our results suggest this approach would be ineffective. However, it could be useful to conduct preference experiments with multiple dilutions and/or flavours of electrolyte solution. Although they did not prefer Pedialyte in our experiment, bats in the hand readily drink it and electrolyte supplementation remains an important tool for rehabilitation of captive bats recovering from WNS and other causes of dehydration.

Linked article : https://doi.org/10.1002/ece3.4034.

It is well established that hypothalamic neurons producing the peptide corticotropin-releasing factor (CRF) play a key role in stress adaptation, including reduction of food intake when a threat or stressor is present. We have previously reported on the presence of an intrinsic CRF signaling system within the optic tectum (OT), a brain area that plays a key role in visually guided prey capture/predator avoidance decisions. To better understand the potential role of tectal CRF neurons in regulating adaptive behavior and energy balance during stress we examined evidence for modulation of tectal CRF neuronal activity after stressor exposure and food deprivation in the African clawed frog Xenopus laevis. We tested two predictions, 1) that exposure to categorically distinct stressors (ether vapors and shaking) will reduce food intake and modulate the activity of tectal CRF cells, and 2) that food deprivation will modulate the activity of tectal CRF cells. Exposure to ether increased tectal content of CRF and CRF transcript, but lowed CRFR1 transcript abundance. Two weeks of food deprivation reduced total fat stores in frogs and decreased tectal content of CRF content while having no effect on CRF and CRFR1 transcript abundance. Our data are consistent with a role for tectal CRF neurons in modulating food intake in response to certain stressors., (Copyright © 2017. Published by Elsevier Inc.)

Hibernating animals use torpor [reduced body temperature (T b ) and metabolic rate] to reduce energy expenditure during winter. Periodic arousals to normal T b are energetically expensive, so hibernators trade off arousal benefits against energetic costs. This is especially important for bats with white-nose syndrome (WNS), a fungal disease causing increased arousal frequency. Little brown bats (Myotis lucifugus) with WNS show upregulation of endogenous pyrogens and sickness behaviour. Therefore, we hypothesized that WNS should cause a fever response characterized by elevated T b . Hibernators could also accrue some benefits of arousals with minimal T b increase, thus avoiding full arousal costs. We compared skin temperature (T sk ) of captive Myotis lucifugus inoculated with the WNS-causing fungus to T sk of sham-inoculated controls. Infected bats re-warmed to higher T sk during arousals which is consistent with a fever response. Torpid T sk did not differ. During what we term "cold arousals", bats exhibited movement following T sk increases of only 2.2 ± 0.3 °C, compared to >20 °C increases during normal arousals. Cold arousals occurred in both infected and control bats, suggesting they are not a pathophysiological consequence of WNS. Fever responses are energetically costly and could exacerbate energy limitation and premature fat depletion for bats with WNS. Cold arousals could represent an energy-saving mechanism for both healthy and WNS-affected bats when complete arousals are unnecessary or too costly. A few cold arousals were observed mid-hibernation, typically in response to disturbances. Cold arousals may, therefore, represent a voluntary restriction of arousal temperature instead of loss of thermoregulatory control.

Fungal diseases of wildlife typically manifest as superficial skin infections but can have devastating consequences for host physiology and survival. White-nose syndrome (WNS) is a fungal skin disease that has killed millions of hibernating bats in North America since 2007. Infection with the fungus Pseudogymnoascus destructans causes bats to rewarm too often during hibernation, but the cause of increased arousal rates remains unknown. On the basis of data from studies of captive and free-living bats, two mechanistic models have been proposed to explain disease processes in WNS. Key predictions of both models are that WNS-affected bats will show 1 ) higher metabolic rates during torpor (TMR) and 2 ) higher rates of evaporative water loss (EWL). We collected bats from a WNS-negative hibernaculum, inoculated one group with P. destructans , and sham-inoculated a second group as controls. After 4 mo of hibernation, TMR and EWL were measured using respirometry. Both predictions were supported, and our data suggest that infected bats were more affected by variation in ambient humidity than controls. Furthermore, disease severity, as indicated by the area of the wing with UV fluorescence, was positively correlated with EWL, but not TMR. Our results provide the first direct evidence that heightened energy expenditure during torpor and higher EWL independently contribute to WNS pathophysiology, with implications for the design of potential treatments for the disease., (Copyright © 2017 the American Physiological Society.)

Mitigation of emerging infectious diseases that threaten global biodiversity requires an understanding of critical host and pathogen responses to infection. For multihost pathogens where pathogen virulence or host susceptibility is variable, host-pathogen interactions in tolerant species may identify potential avenues for adaptive evolution in recently exposed, susceptible hosts. For example, the fungus Pseudogymnoascus destructans causes white-nose syndrome (WNS) in hibernating bats and is responsible for catastrophic declines in some species in North America, where it was recently introduced. Bats in Europe and Asia, where the pathogen is endemic, are only mildly affected. Different environmental conditions among Nearctic and Palearctic hibernacula have been proposed as an explanation for variable disease outcomes, but this hypothesis has not been experimentally tested. We report the first controlled, experimental investigation of response to P. destructans in a tolerant, European species of bat (the greater mouse-eared bat, Myotis myotis ). We compared body condition, disease outcomes and gene expression in control (sham-exposed) and exposed M. myotis that hibernated under controlled environmental conditions following treatment. Tolerant M. myotis experienced extremely limited fungal growth and did not exhibit symptoms of WNS. However, we detected no differential expression of genes associated with immune response in exposed bats, indicating that immune response does not drive tolerance of P. destructans in late hibernation. Variable responses to P. destructans among bat species cannot be attributed solely to environmental or ecological factors. Instead, our results implicate coevolution with the pathogen, and highlight the dynamic nature of the "white-nose syndrome transcriptome." Interspecific variation in response to exposure by the host (and possibly pathogen) emphasizes the importance of context in studies of the bat-WNS system, and robust characterization of genetic responses to exposure in various hosts and the pathogen should precede any attempts to use particular bat species as generalizable "model hosts."

Widespread animals at the extremes of the species' distribution experience ecological constraints different than individuals in the core of the distribution. For example, small endotherms at very high latitudes face short summers with cool temperatures and a lack of true darkness. In particular, insectivorous bats at high latitudes may experience constraints because of their unique life history traits, and may have different energy requirements than bats at lower latitudes. To evaluate the extent of these differences, we estimated an energy budget and refueling rates for reproductively active female little brown bats (Myotis lucifugus) roosting in buildings in eastern Alaska (~63°N). Physiological parameters (torpor use and metabolic rates) and daily energy expenditures (25.7±5.3kJd(-1)) were similar to, or slightly lower than, conspecifics at lower latitudes. Northern little brown bats foraged for less time than southerly conspecifics, but measurements of plasma β-hydroxybutyrate concentrations suggest that northern bats refuel at a rate considerably higher than those to the south. It appears that high refueling rates (and therefore foraging intensity) involve a dietary shift to orb-weaver spiders, which are abundant and likely offer higher energetic benefit than the small, flying insects consumed by individuals in other parts of the distribution. Environmental factors may limit species' distributions, but our results provide an example of a population at the limit of their geographic range that has compensated for environmental challenges by adopting unique behavioral strategies while the underlying physiology (including daily energy expenditure) remains similar to populations at the core of the species' range., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Torpor is an adaptation that allows many endotherms to save energy by abandoning the energetic cost of maintaining elevated body temperatures. Although torpor reduces energy consumption, the metabolic heat production required to arouse from torpor is energetically expensive and can impact the overall cost of torpor. The rate at which rewarming occurs can impact the cost of arousal, therefore, factors influencing rewarming rates of heterothermic endotherms could have influenced the evolution of rewarming rates and overall energetic costs of arousal from torpor. Bats are a useful taxon for studies of ecological and behavioral correlates of rewarming rate because of the widespread expression of heterothermy and ecological diversity across the >1200 known species. We used a comparative analysis of 45 bat species to test the hypothesis that ecological, behavioral, and physiological factors affect rewarming rates. We used basal metabolic rate (BMR) as an index of thermogenic capacity, and local climate (i.e., latitude of geographic range), roost stability and maximum colony size as ecological and behavioral predictors of rewarming rate. After controlling for phylogeny, high BMR was associated with rapid rewarming while species that live at higher absolute latitudes and in less thermally stable roosts also rewarmed most rapidly. These patterns suggests that some bat species rely on passive rewarming and social thermoregulation to reduce costs of rewarming, while others might rely on thermogenic capacity to maintain rapid rewarming rates in order to reduce energetic costs of arousal. Our results highlight species-specific traits associated with maintaining positive energy balance in a wide range of climates, while also providing insight into possible mechanisms underlying the evolution of heterothermy in endotherms., (Copyright © 2016 Elsevier Inc. All rights reserved.)

White-nose syndrome is caused by the fungus Pseudogymnoascus destructans and has killed millions of hibernating bats in North America but the pathophysiology of the disease remains poorly understood. Our objectives were to (1) assess non-destructive diagnostic methods for P. destructans infection compared to histopathology, the current gold-standard, and (2) to evaluate potential metrics of disease severity. We used data from three captive inoculation experiments involving 181 little brown bats (Myotis lucifugus) to compare histopathology, quantitative PCR (qPCR), and ultraviolet fluorescence as diagnostic methods of P. destructans infection. To assess disease severity, we considered two histology metrics (wing area with fungal hyphae, area of dermal necrosis), P. destructans fungal load (qPCR), ultraviolet fluorescence, and blood chemistry (hematocrit, sodium, glucose, pCO2, and bicarbonate). Quantitative PCR was most effective for early detection of P. destructans, while all three methods were comparable in severe infections. Correlations among hyphae and necrosis scores, qPCR, ultraviolet fluorescence, blood chemistry, and hibernation duration indicate a multi-stage pattern of disease. Disruptions of homeostasis occurred rapidly in late hibernation. Our results provide valuable information about the use of non-destructive techniques for monitoring, and provide novel insight into the pathophysiology of white-nose syndrome, with implications for developing and implementing potential mitigation strategies.

While transposable elements (TE) have long been suspected of involvement in species diversification, identifying specific roles has been difficult. We recently found evidence of TE-derived regulatory RNAs in a species-rich family of bats. The TE-derived small RNAs are temporally associated with the burst of species diversification, suggesting that they may have been involved in the processes that led to the diversification. In this commentary, we expand on the ideas that were briefly touched upon in that manuscript. Specifically, we suggest avenues of research that may help to identify the roles that TEs may play in perturbing regulatory pathways. Such research endeavors may serve to inform evolutionary biologists of the ways that TEs have influenced the genomic and taxonomic diversity around us.

Pseudogymnoascus destructans is an ascomycetous fungus responsible for the disease dubbed white-nose syndrome (WNS) and massive mortalities of cave-dwelling bats. The fungus infects bat epidermal tissue, causing damage to integumentary cells and pilosebaceous units. Differences in epidermal lipid composition caused by P. destructans infection could have drastic consequences for a variety of physiological functions, including innate immune efficiency and water retention. While bat surface lipid and stratum corneum lipid composition have been described, the differences in epidermal lipid content between healthy tissue and P. destructans-infected tissue have not been documented. In this study, we analyzed the effect of wing damage from P. destructans infection on the epidermal polar lipid composition (glycerophospholipids [GPs] and sphingomyelin) of little brown bats (Myotis lucifugus). We hypothesized that infection would lead to lower levels of total lipid or higher oxidized lipid product proportions. Polar lipids from three damaged and three healthy wing samples were profiled by electrospray ionization tandem mass spectrometry. We found lower total broad lipid levels in damaged tissue, specifically ether-linked phospholipids, lysophospholipids, phosphatidylcholine, and phosphatidylethanolamine. Thirteen individual GP species from four broad GP classes were present in higher amounts in healthy tissue. Six unsaturated GP species were absent in damaged tissue. Our results confirm that P. destructans infection leads to altered lipid profiles. Clinical signs of WNS may include lower lipid levels and lower proportions of unsaturated lipids due to cellular and glandular damage.

Bats and birds must balance time and energy budgets during migration. Migrating bats face similar physiological challenges to birds, but nocturnality creates special challenges for bats, such as a conflict between travelling and refueling, which many birds avoid by feeding in daylight and flying at night. As endothermic animals, bats and birds alike must expend substantial amounts of energy to maintain high body temperatures. For migratory birds refueling at stopovers, remaining euthermic during inactive periods reduces the net refuelling rate, thereby prolonging stopover duration and delaying subsequent movement. We hypothesized that bats could mitigate similar ambient-temperature dependent costs by using a torpor-assisted migration strategy. We studied silver-haired bats Lasionycteris noctivagans during autumn migration using a combination of respirometry and temperature-sensitive radiotelemetry to estimate energy costs incurred under ambient temperature conditions, and the energy that bats saved by using torpor during daytime roosting periods. All bats, regardless of sex, age, or body condition used torpor at stopover and saved up to 91% of the energy they would have expended to remain euthermic. Furthermore, bats modulated use of torpor depending on ambient temperature. By adjusting the time spent torpid, bats achieved a rate of energy expenditure independent of the ambient temperature encountered at stopover. By lowering body temperature during inactive periods, fuel stores are spared, reducing the need for refuelling. Optimal migration models consider trade-offs between time and energy. Heterothermy provides a physiological strategy that allows bats to conserve energy without paying a time penalty as they migrate. Although uncommon, some avian lineages are known to use heterothermy, and current theoretical models of migration may not be appropriate for these groups. We propose that thermoregulatory strategies should be an important consideration of future migration studies of both bats and birds.

Pilosebaceous units found in the mammalian integument are composed of a hair follicle, the proximal portion of the hair shaft, a sebaceous gland, and the erector pili muscle. Pilosebaceous units release protective oils, or sebum, by holocrine secretion onto skin and hair through rupturing of sebocytes. Sebum is composed largely of polar and neutral lipids including glycerolipids, free fatty acids, sterols, wax esters, sterol esters, and squalene. In addition to these lipid classes, there is a small proportion of ionic/anionic glycerophospholipids (GPs). Composition of GPs on hair is rarely addressed despite their broad biological activities as signaling molecules and membrane stability. Furthermore, knowledge on GP composition in bats is lacking. Bat GP composition is important to document due to GP roles ranging from decreasing drag during migration to interaction with the integumentary microbiome. In this study, we analyzed GP molecular composition with liquid chromatography electrospray ionization tandem mass spectrometry and compared GP content to previous literature. A total of 152 GPs were detected. Broad GP classes identified include lysophosphatidylcholine, phosphatidylcholine (PC), lysophosphatidylethanolamine, phosphatidylethanolamine, phosphatidylinositol, phosphatidylserine, phosphatidic acid, and phosphatidylglycerol, with PC being the most abundant class. The acyl components were consistent with fatty acid methyl esters and triacylglyceride moieties found in Eastern red bat sebum. Glycerophospholipid proportions of the hair surface were different from a previous study on bat lung surfactants. This study determined the broad class and molecular species of bat sebum GPs that may be used in future ecological studies in vespertilionid bats.

Animal personality or temperament refers to individual differences in behaviour that are repeatable over time and across contexts. Personality has been linked to life-history traits, energetic traits and fitness, with implications for the evolution of behaviour. Personality has been quantified for a range of taxa (e.g., fish, songbirds, small mammals) but, so far, there has been little work on personality in bats, despite their diversity and potential as a model taxon for comparative studies. We used a novel environment test to quantify personality in little brown bats (Myotis lucifugus) and assess the short-term repeatability of a range of behaviours. We tested the hypothesis that development influences values of personality traits and predicted that trait values associated with activity would increase between newly volant, pre-weaning young-of-the-year (YOY) and more mature, self-sufficient YOY. We identified personality dimensions that were consistent with past studies of other taxa and found that these traits were repeatable over a 24-hour period. Consistent with our prediction, older YOY captured at a fall swarming site prior to hibernation had higher activity scores than younger YOY bats captured at a maternity colony, suggesting that personality traits vary as development progresses in YOY bats. Thus, we found evidence of short-term consistency of personality within individuals but with the potential for temporal flexibility of traits, depending on age.

Altitudinal migrations are common in all major vertebrate and some invertebrate lineages. Such migrations have important implications for the basic and applied ecology of animals making these movements. The idea that bats make altitudinal migrations has been suggested for nearly a century. However, studies documenting the existence and causes of altitudinal bat migrations are scarce, and are frequently published in the 'grey' literature. For the first time, we comprehensively review the evidence supporting the existence of altitudinal bat migrations worldwide, describe basic patterns of migration in temperate and tropical regions, and articulate and propose tests of hypotheses potentially explaining these migrations. We compiled a list of 50 studies indicative of altitudinal bat migration in 61 species (five families) from 21 countries (four continents). The temporal and spatial patterns of these migrations grouped biogeographically. Temperate bats generally exhibit sex-biased migrations with females inhabiting lower elevations than males during reproductive periods. Although there is less information on tropical bat migration, few studies report sex-biased migration. We compiled hypotheses proposed in the bat and (more extensive) avian literature to provide a list of hypotheses potentially explaining altitudinal bat migrations. These hypotheses rely upon temporal availability of (and competition for) food resources, spatial distribution of geomorphological features suitable for hibernation, sex-related differences in the use of torpor, mating opportunities, and climatic factors that impose direct physiological challenges to survival or that restrict the ability to forage. A more thorough description of the migration patterns of most species will be required to distinguish effectively among these hypotheses. We identify research avenues that would broaden our understanding of bat migration patterns and provide critical information required for effective conservation., (© 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society.)

The high energy density of fat, and limited capacity for carbohydrate storage suggest that migrating bats should fuel endurance flights with fat, as observed in migrating birds. Yet, cursorial mammals are unable to support high intensity exercise with fat stores. We hypothesized that migratory bats and birds have converged on similar physiological mechanisms to fuel endurance flight with fat. We predicted bats would seasonally upregulate fatty acid transport and oxidation pathways when migration demands were high. We studied seasonal variation in mitochondrial oxidative enzyme activities and fatty acid transport protein expression in the flight muscle of hoary bats (Lasiurus cinereus). Carnitine palmitoyl transferase, 3-hydroxyacyl-CoA dehydrogenase and citrate synthase activity increased during migration. There were no changes in expression of fatty acid translocase or plasma membrane fatty acid binding protein. Heart-type fatty acid binding protein expression increased 5-fold in migrating females, but did not vary seasonally in males. An aerial insectivore lifestyle, and the coincidence of migration and pregnancy may explain differences in transporter expression compared to previously studied birds. Overall, our results are consistent with seasonal upregulation of lipid metabolism and aerobic capacity, and confirm that migration poses distinct physiological challenges for bats., (Copyright © 2013 Elsevier Inc. All rights reserved.)

Many species of bats migrate long distances, but the physiological challenges of migration are poorly understood. We tested the hypothesis that migration is physiologically demanding for bats by examining migration-related phenotypic flexibility. Both bats and birds are endothermic, flying vertebrates; therefore, we predicted that migration would result in similar physiological trade-offs. We compared hoary bats (Lasiurus cinereus) during spring migration and summer non-migratory periods, comparing our results with previous observations of birds. Migrating bats had reduced digestive organs, enlarged exercise organs, and fat stores had higher proportions of polyunsaturated fatty acids (PUFAs). These results are consistent with previous studies of migrating birds; however, we also found sex differences not typically associated with bird migration. Migrating female hoary bats increased the relative size of fat stores by reducing lean body components, while males maintained the same relative amount of fat in both seasons. The ratio of n-6 to n-3 PUFA in flight muscle membrane increased in migrating males and decreased in migrating females, consistent with males using torpor more frequently than females during spring migration. Enlarged exercise organs, reduced digestive organs and changes in adipose tissue composition reflect the elevated energetic demands of migration. Sex-specific patterns of fat storage and muscle membrane composition likely reflect challenges faced by females that migrate while pregnant. Our results provide some of the first insights into the physiological demands of bat migration and highlight key differences between bats and birds.

1. Some bat species make long-distance latitudinal migrations between summer and winter grounds, but because of their elusive nature, few aspects of their biology are well understood. The need for migratory stopover sites to rest and refuel, such as used by birds, has been repeatedly suggested, but not previously tested empirically in bats. 2. We studied migrating silver-haired bats (Lasionycteris noctivagans) at Long Point, ON, Canada. We used digital radio-transmitters to track 30 bats using an array of five towers that effectively covered the entire region (c. 20 × 40 km). We measured stopover duration and departure direction, and documented movement patterns, foraging activity and roost sites. We measured body composition on arrival using quantitative magnetic resonance and simulated long-distance migration using observed body composition to predict migration range and rate. 3. Migration occurred in two waves (late August and mid-September). Most bats stayed 1-2 days, although two remained >2 weeks. One third of the bats foraged while at the site, many foraging opportunistically on nights when rain precluded continued migration. Bats roosted in a variety of tree species and manmade structures in natural and developed areas. Half of the bats departed across Lake Erie (minimum crossing distance c. 38 km) while half departed along the shoreline. 4. Simulations predicted a migration rate of c. 250-275 km per day and suggest that all but one of the bats in our study carried sufficient fuel stores to reach the putative wintering area (estimated distance 1500 km) without further refuelling. 5. Our results suggest that migrating bats stopover for sanctuary or short-term rest as opposed to extended rest and refuelling as in many songbirds. Daily torpor could reduce energy costs when not in flight, minimizing the need for extended stopovers and allowing bats to potentially complete their migration at a fraction of the time and energy cost of similar sized birds., (© 2011 The Authors. Journal of Animal Ecology © 2011 British Ecological Society.)

Background: Annual movements of tri-colored bats (Perimyotis subflavus) are poorly understood. While this species has been considered a regional migrant, some evidence suggests that it may undertake annual latitudinal migrations, similar to other long distance North American migratory bat species., Methodology/principal Findings: We investigated migration in P. subflavus by conducting stable hydrogen isotope analyses of 184 museum specimen fur samples and comparing these results (δD(fur)) to published interpolated δD values of collection site growing season precipitation (δD(precip)). Results suggest that the male molt period occurred between June 23 and October 16 and 33% of males collected during the presumed non-molt period were south of their location of fur growth. For the same time period, 16% of females were south of their location of fur growth and in general, had not travelled as far as migratory males. There were strong correlations between δD(fur) from the presumed molt period and both growing season δD(precip) (males--r(2) = 0.86; p<0.01; females--r(2) = 0.75; p < 0.01), and latitude of collection (males--r(2) = 0.85; p<0.01; females--r(2) = 0.73; p<0.01). Most migrants were collected at the northern (>40 °N; males and females) and southern (<35 °N; males only) extents of the species' range., Conclusions/significance: These results indicate a different pattern of migration for this species than previously documented, suggesting that some P. subflavus engage in annual latitudinal migrations and that migratory tendency varies with latitude and between sexes. We suggest that this species' hibernation ecology makes it particularly susceptible to long winters, making migration from the northern extent of the species' range to more southern hibernacula preferable for some individuals. Fur δD values for some of the northern individuals may indicate an increase in the currently accepted northern range of this species. Sex-biased differences in migration may be the result of differences in reproductive pressures.

Since its discovery in the winter of 2005-2006, white-nose syndrome (WNS) has killed over one million little brown bats (Myotis lucifugus) in the American northeast. Although many studies have reported die-offs of bats at winter hibernacula, it is important to understand how bat mortality linked to WNS at winter hibernacula affects bat activity levels in their summer ranges. In the summer (May-August) of 2007, 2008 and 2009, we recorded echolocation calls to determine bat activity at sites along the Hudson River, NY (within approx. 100 km of where WNS was first reported). We documented a 78 per cent decline in the summer activity of M. lucifugus, coinciding with the arrival and spread of WNS. We suggest that mortality of M. lucifugus in winter hibernacula is reflected by reduced levels of activity in the summer and that WNS affects the entire bat population of an area, and not only individual hibernacula.

Migratory bird species have smaller brains than non-migratory species. The behavioural flexibility/migratory precursor hypothesis suggests that sedentary birds have larger brains to allow the behavioural flexibility required in a seasonally variable habitat. The energy trade-off hypothesis proposes that brains are heavy, energetically expensive and therefore, incompatible with migration. Here, we compared relative brain, neocortex and hippocampus volume between migratory and sedentary bats at the species-level and using phylogenetically independent contrasts. We found that migratory bats had relatively smaller brains and neocortices than sedentary species. Our results support the energy trade-off hypothesis because bats do not exhibit the same degree of flexibility in diet selection as sedentary birds. Our results also suggest that bat brain size differences are subtler than those found in birds, perhaps owing to bats' shorter migration distances. Conversely, we found no difference in relative hippocampus volume between migratory and sedentary species, underscoring our limited understanding of the role of the hippocampus in bats.

Many species of birds and bats undertake seasonal migrations between breeding and over-wintering sites. En-route, migrants alternate periods of flight with time spent at stopover--the time and space where individuals rest and refuel for subsequent flights. We assessed the spatial scale of movements made by migrants during stopover by using an array of automated telemetry receivers with multiple antennae to track the daily location of individuals over a geographic area ~20 × 40 km. We tracked the movements of 322 individuals of seven migratory vertebrate species (5 passerines, 1 owl and 1 bat) during spring and fall migratory stopover on and adjacent to a large lake peninsula. Our results show that many individuals leaving their capture site relocate within the same landscape at some point during stopover, moving as much as 30 km distant from their site of initial capture. We show that many apparent nocturnal departures from stopover sites are not a resumption of migration in the strictest sense, but are instead relocations that represent continued stopover at a broader spatial scale.

Insectivorous bats regularly experience dramatic and sometimes rapid changes in nutrient stores, yet our ability to study these changes has been limited by available techniques. Plasma metabolite analysis has proven effective for studying individual rates of mass change in birds but has not been validated for other taxa. We tested the effectiveness of plasma metabolite analysis by conducting a study with captive big brown bats (Eptesicus fuscus) and little brown bats (Myotis lucifugus) in the field. In the lab, we varied food availability to induce various rates of mass change. As predicted, individual rate of mass change was positively correlated with plasma triglyceride concentration, but there was no relationship with plasma beta-hydroxybutyrate concentration, whereas such a relationship has been found in birds. In the field, we collected blood samples from postlactating females as they emerged in the evening (fasted) and when they returned from feeding in the morning. Plasma triglyceride concentration was greater in fed bats than fasted bats, and the increase was less when rain limited foraging. Contrary to predictions, beta-hydroxybutyrate concentration was also greater in fed bats than fasted bats. Analysis of plasma triglyceride concentration provides a technique for assessing individual feeding state and rate of mass change of bats and will facilitate further study of bat nutritional ecology and energetics.