[Show abstract][Hide abstract] ABSTRACT: White-nose syndrome (WNS) is an emerging infectious disease devastating hibernating North American bat populations that is caused by the psychrophilic fungus Geomyces destructans. Previous histopathological analysis demonstrated little evidence of inflammatory responses in infected bats, however few studies have compared other aspects of immune function between WNS-affected and unaffected bats. We collected bats from confirmed WNS-affected and unaffected sites during the winter of 2008-2009 and compared estimates of their circulating levels of total leukocytes, total immunoglobulins, cytokines and total antioxidants. Bats from affected and unaffected sites did not differ in their total circulating immunoglobulin levels, but significantly higher leukocyte counts were observed in bats from affected sites and particularly in affected bats with elevated body temperatures (above 20°C). Bats from WNS-affected sites exhibited significantly lower antioxidant activity and levels of interleukin-4 (IL-4), a cytokine that induces T cell differentiation. Within affected sites only, bats exhibiting visible fungal infections had significantly lower antioxidant activity and levels of IL-4 compared to bats without visible fungal infections. Overall, bats hibernating in WNS-affected sites showed immunological changes that may be evident of attempted defense against G. destructans. Observed changes, specifically elevated circulating leukocytes, may also be related to the documented changes in thermoregulatory behaviors of affected bats (i.e. increased frequencies in arousal from torpor). Alterations in immune function may reflect expensive energetic costs associated with these processes and intrinsic qualities of the immunocapability of hibernating bats to clear fungal infections. Additionally, lowered antioxidant activity indicates a possible imbalance in the pro- versus antioxidant system, may reflect oxidative tissue damage, and should be investigated as a contributor to WNS-associated morbidity and mortality.
PLoS ONE 01/2013; 8(3):e58976. · 3.73 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The Brazilian free-tailed bat (Tadarida brasiliensis) exhibits a highly vascularized, hairless thermal window (or "radiator") on the proximal ventral surfaces of extended wings and body. We identified this character using thermal infrared imaging and investigated the vasculature using barium sulfate enhanced microcomputed tomography (micro-CT). Micro-CT images revealed unique arrangements of arteries and veins in the region of the radiator positioned perpendicular to the axis of the body. Coupling micro-CT imaging with analysis of surface temperature profiles, we concluded that radiators aid in thermoregulation during flight in variable environments. This study represents the first application of contrast enhanced micro-CT to visualize vasculature of bats and thus exhibits a promising technique for further investigations of cardiovascular function and anatomy in bats.
The Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology 01/2012; 295(4):563-6. · 1.34 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The lipid matrix of the stratum corneum (SC), the outer layer of the epidermis of mammals and birds, constitutes the barrier to diffusion of water vapor through the skin. The lipids of the SC are structured in the intercellular spaces of the mammalian epidermis in ordered layers, called lamellae, which have been postulated to prevent water loss. Lipids in the mammalian SC are mainly cholesterol, free fatty acids and ceramides, the latter forming the structural support for the lamellae. However, knowledge on how the lipid composition of the SC alters cutaneous water loss (CWL) in mammals is rudimentary, and is largely derived from studies on laboratory animals and humans. We measured CWL of individuals of two species of syntopic bats, Tadarida brasiliensis and Myotis velifer. In the first study of its kind on wild mammals, we correlated CWL with the lipid composition of the SC, measured using thin layer chromatography and high performance liquid chromatography coupled with atmospheric pressure photoionization mass spectrometry. Surface-specific CWL was 20.6% higher in M. velifer than in T. brasiliensis, although differences were not significant. Compared with individuals of M. velifer, individuals of T. brasiliensis had more classes, and a higher proportion, of polar ceramides in the SC, a feature associated with lower CWL. Individuals of T. brasiliensis also had a class of non-polar ceramides that presumably spans the lamellae and gives more cohesiveness to the lipid matrix of the SC. We conclude that qualitative and quantitative modifications of the lipid composition of the SC contribute to regulate CWL of these two species of bats.
Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 11/2011; 161(2):208-15. · 2.20 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: White-nose syndrome (WNS) is having an unprecedented impact on hibernating bat populations in the eastern United States. While most studies have focused on widespread mortality observed at winter hibernacula, few have examined the consequences of wing damage that has been observed among those bats that survive hibernation. Given that WNS-related wing damage may lead to life-threatening changes in wing function, we tested the hypothesis that reduced abundance of free-ranging little brown myotis (Myotis lucifugus) with severe wing damage as the summer progresses is due to healing of wing tissue. Photographs of captured and recaptured adult females were examined for wing damage and healing rates were calculated for each category of wing damage index (WDI = 0-3). We found that free-ranging bats with severe wing damage were able to heal to a lower WDI score within 2 weeks. Bats with the most severe wing damage had faster healing rates than did individuals with less damage. We also found a significant relationship between body condition and WDI for adult females captured in the early weeks of the active season. Our results support the hypothesis that some bats can heal from severe wing damage during the active season, and thus may not experience increased mortality associated with reduced functions of wings. We urge researchers and wildlife managers to use caution when interpreting data on WDI to assess the impact of WNS on bat populations, especially during the later months of the active season.
[Show abstract][Hide abstract] ABSTRACT: White-nose syndrome (WNS) is the most devastating condition ever reported for hibernating bats, causing widespread mortality in the northeastern United States. The syndrome is characterized by cutaneous lesions caused by a recently identified psychrophilic and keratinophylic fungus (Geomyces destructans), depleted fat reserves, atypical behavior, and damage to wings; however, the proximate cause of mortality is still uncertain. To assess relative levels of immunocompetence in bats hibernating in WNS-affected sites compared with levels in unaffected bats, we describe blood plasma complement protein activity in hibernating little brown myotis (Myotis lucifugus) based on microbicidal competence assays using Escherichia coli, Staphylococcus aureus and Candida albicans. Blood plasma from bats collected during mid-hibernation at WNS-affected sites had higher bactericidal ability against E. coli and S. aureus, but lower fungicidal ability against C. albicans when compared with blood plasma from bats collected at unaffected sites. Within affected sites during mid-hibernation, we observed no difference in microbicidal ability between bats displaying obvious fungal infections compared to those without. Bactericidal ability against E. coli decreased significantly as hibernation progressed in bats collected from an affected site. Bactericidal ability against E. coli and fungicidal ability against C. albicans were positively correlated with body mass index (BMI) during late hibernation. We also compared complement activity against the three microbes within individuals and found that the ability of blood plasma from hibernating M. lucifugus to lyse microbial cells differed as follows: E. coli>S. aureus>C. albicans. Overall, bats affected by WNS experience both relatively elevated and reduced innate immune responses depending on the microbe tested, although the cause of observed immunological changes remains unknown. Additionally, considerable trade-offs may exist between energy conservation and immunological responses. Relationships between immune activity and torpor, including associated energy expenditure, are likely critical components in the development of WNS.
PLoS ONE 01/2011; 6(11):e27430. · 3.73 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Bat wings are important for thermoregulation, but their role in heat balance during flight is largely unknown. More than 80% of the energy consumed during flight generates heat as a by-product, and thus it is expected that bat wings should dissipate large amounts of heat to prevent hyperthermia. We measured rectal (T(r)) and surface (T(s)) temperatures of Brazilian free-tailed bats (Tadarida brasiliensis) as they emerged from and returned to their daytime roosts and calculated sensible heat transfer for different body regions (head, body, wings, and tail membrane). Bats' T(r) decreased from 36.8°C during emergence flights to 34.4°C during returns, and T(s) scaled positively with ambient temperature (T(a)). Total radiative heat loss from bats was significantly greater for a radiative sink to the night sky than for a sink with temperature equal to T(a). We found that free-ranging Brazilian free-tailed bats, on average, do not dissipate heat from their wings by convection but instead dissipate radiative heat (L) to the cloudless night sky during flight ([Formula: see text] W). However, within the range of T(a) measured in this study, T. brasiliensis experienced net heat loss between evening emergence and return flights. Regional hypothermia reduces heat loss from wings that are exposed to potentially high convective fluxes. Additional research is needed to establish the role of wings in evaporative cooling during flight in bats.
Physiological and Biochemical Zoology 10/2010; 83(6):885-97. · 2.46 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Billions of animals migrate each year. To successfully reach their destination, migrants must have evolved an appropriate genetic program and suitable developmental, morphological, physiological, biomechanical, behavioral, and life-history traits. Moreover, they must interact successfully with biotic and abiotic factors in their environment. Migration therefore provides an excellent model system in which to address several of the "grand challenges" in organismal biology. Previous research on migration, however, has often focused on a single aspect of the phenomenon, largely due to methodological, geographical, or financial constraints. Integrative migration biology asks 'big questions' such as how, when, where, and why animals migrate, which can be answered by examining the process from multiple ecological and evolutionary perspectives, incorporating multifaceted knowledge from various other scientific disciplines, and using new technologies and modeling approaches, all within the context of an annual cycle. Adopting an integrative research strategy will provide a better understanding of the interactions between biological levels of organization, of what role migrants play in disease transmission, and of how to conserve migrants and the habitats upon which they depend.
Integrative and Comparative Biology 09/2010; 50(3):261-79. · 3.02 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The Brazilian free-tailed bat (Tadarida brasiliensis) experiences challenging thermal conditions while roosting in hot caves, flying during warm daylight conditions, and foraging at cool high altitudes. Using thermal infrared cameras, we identified hot spots along the flanks of free-ranging Brazilian free-tailed bats, ventral to the extended wings. These hot spots are absent in syntopic cave myotis (Myotis velifer), a species that forages over relatively short distances, and does not engage in long-distance migration. We hypothesized that the hot spots, or "radiators," on Brazilian free-tailed bats may be adaptations for migration, particularly in this long-distance, high-flying species. We examined the vasculature of radiators on Brazilian free-tailed bats with transillumination to characterize the unique arrangements of arteries and veins that are positioned perpendicular to the body in the proximal region of the wing. We hypothesized that these radiators aid in maintaining heat balance by flushing the uninsulated thermal window with warm blood, thereby dissipating heat while bats are flying under warm conditions, but shunting blood away and conserving heat when they are flying in cooler air at high altitudes. We also examined fluid-preserved specimens representing 122 species from 15 of 18 chiropteran families and radiators appeared present only in species in the family Molossidae, including both sedentary and migratory species and subspecies. Thus, the radiator appears to be a unique trait that may facilitate energy balance and water balance during sustained dispersal, foraging, and long-distance migration.
Integrative and Comparative Biology 09/2010; 50(3):358-70. · 3.02 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: White-nose syndrome (WNS) is an emerging disease causing massive mortality of hibernating bats in the northeastern United States. At hibernacula, bats affected with WNS typically exhibit growth of a white psychrophylic fungus (Geomyces destructans) on the nose, wings and ears; many individuals seem to prematurely die of starvation owing to depleted fat reserves. Conspicuous scarring and necrosis of the wings on WNS-affected bats that survive hibernation may have lasting consequences for survival and reproductive success during the active season. We monitored two maternity colonies of little brown myotis, Myotis lucifugus, in Massachusetts and New Hampshire from 14 May to 8 August 2008 to assess body conditions after expected exposure to WNS over the previous winter. We developed a 4-point wing damage index (WDI = 0 to 3) to assess the incidence and severity of wing damage in the months following emergence from hibernation. Severe wing damage was observed up to 4 June and moderate damage was observed through 9 July. Light wing damage was observed on both adult and juvenile bats throughout the study period, but was not exclusively attributed to WNS. The most severe wing damage was associated with a lower body mass index which may reflect reduced foraging success. Overall, reproductive rate was 85.1% in 2008; slightly lower than reported in previous studies. The incidence, timing, and geographic range of wing damage observed on little brown myotis in 2008 correspond to the occurrence of WNS at hibernacula. Monitoring wing conditions of affected and healthy bats will be important tool for assessing the spread of this disease and for establishing baseline data for unaffected bats. The simple scale we propose should be useful for monitoring wing conditions in any bat species.
[Show abstract][Hide abstract] ABSTRACT: Using data collected with thermal imaging technology, we found a major reduction in population estimates of colony size in the Brazilian free-tailed bat (Tadarida brasiliensis) from 54 million, obtained in 1957 without this technology, to 4 million in 6 major cave colonies in the southwestern United States. The 1957 census was based on human visual observations of cave emergence flights that were subject to potentially high errors. The recent census was produced using an accurate, reproducible counting method and based on complete temporal records of colony emergences. Analysis of emergence flights from dusk through darkness also revealed patterns in group behavior that would be difficult to capture without thermal infrared technology. Flow patterns of bats during emergence flights exhibited characteristic single, double, or triple episodes, with the peak flow during the 1st episode. A consistent rhythmic pattern of flow episodes and pauses was revealed across colonies and was independent of emergence tempo.
Journal of Mammalogy - J MAMMAL. 01/2008; 89(1):18-24.