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Body mass and hibernation microclimate may predict bat susceptibility to white?nose syndrome

ABSTRACT: Abstract In multihost disease systems, differences in mortality between species may reflect variation in host physiology, morphology, and behavior. In systems where the pathogen can persist in the environment, microclimate conditions, and the adaptation of the host to these conditions, may also impact mortality. White?nose syndrome (WNS) is an emerging disease of hibernating bats caused by an environmentally persistent fungus, Pseudogymnoascus destructans. We assessed the effects of body mass, torpid metabolic rate, evaporative water loss, and hibernaculum temperature and water vapor deficit on predicted overwinter survival of bats infected by P. destructans. We used a hibernation energetics model in an individual?based model framework to predict the probability of survival of nine bat species at eight sampling sites across North America. The model predicts time until fat exhaustion as a function of species?specific host characteristics, hibernaculum microclimate, and fungal growth. We fit a linear model to determine relationships with each variable and predicted survival and semipartial correlation coefficients to determine the major drivers in variation in bat survival. We found host body mass and hibernaculum water vapor deficit explained over half of the variation in survival with WNS across species. As previous work on the interplay between host and pathogen physiology and the environment has focused on species with narrow microclimate preferences, our view on this relationship is limited. Our results highlight some key predictors of interspecific survival among western bat species and provide a framework to assess impacts of WNS as the fungus continues to spread into western North America. White?nose syndrome is an emerging disease of hibernating bats caused by an environmentally persistent fungus, Pseudogymnoascus destructans. We used a hibernation energetics model in an individual?based model framework to predict the probability of survival of nine bat species at eight sampling sites across North America. These results indicate that heavier bats that roost in drier conditions, which are unsuitable for the fungus that causes white?nose syndrome, are less susceptible to the disease. Our results highlight some key predictors of interspecific survival among western bat species and provide a framework to assess impacts of white?nose syndrome as the fungus continues to spread into western North America.

SUBMITTER: Haase C

PROVIDER: S-EPMC7790633 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Project description:The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus, Eptesicus fuscus, and Perimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen, Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans was present. Key bacterial families-including those potentially involved in pathogen defense-significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence of P. destructans for any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome in M. lucifugus but not for other bat species impacted by the disease.IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes of Myotis lucifugus and Perimyotis subflavus indicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd.

Project description:White-nose syndrome (WNS) is an emerging fungal disease of bats caused by Pseudogymnoascus destructans. Since it was first detected near Albany, NY, in 2006, the fungus has spread across eastern North America, killing unprecedented numbers of hibernating bats. The devastating impacts of WNS on Nearctic bat species are attributed to the likely introduction of P. destructans from Eurasia to naive host populations in eastern North America. Since 2006, the disease has spread in a gradual wavelike pattern consistent with introduction of the pathogen at a single location. Here, we describe the first detection of P. destructans in western North America in a little brown bat (Myotis lucifugus) from near Seattle, WA, far from the previously recognized geographic distribution of the fungus. Whole-genome sequencing and phylogenetic analyses indicated that the isolate of P. destructans from Washington grouped with other isolates of a presumed clonal lineage from the eastern United States. Thus, the occurrence of P. destructans in Washington does not likely represent a novel introduction of the fungus from Eurasia, and the lack of intensive surveillance in the western United States makes it difficult to interpret whether the occurrence of P. destructans in the Pacific Northwest is disjunct from that in eastern North America. Although there is uncertainty surrounding the impacts of WNS in the Pacific Northwest, the presence of the pathogen in western North America could have major consequences for bat conservation. IMPORTANCE White-nose syndrome (WNS) represents one of the most consequential wildlife diseases of modern times. Since it was first documented in New York in 2006, the disease has killed millions of bats and threatens several formerly abundant species with extirpation or extinction. The spread of WNS in eastern North America has been relatively gradual, inducing optimism that disease mitigation strategies could be established in time to conserve bats susceptible to WNS in western North America. The recent detection of the fungus that causes WNS in the Pacific Northwest, far from its previous known distribution, increases the urgency for understanding the long-term impacts of this disease and for developing strategies to conserve imperiled bat species.

Project description:Recent studies have revealed that western populations of little brown bats (Myotis lucifugus) in North America exhibit different hibernation behavior than their eastern counterparts. Understanding these differences is essential for assessing the risk white-nose syndrome (WNS) poses to western bat populations. We used acoustic monitoring and radiotelemetry to study the overwintering behavior of little brown bats near Juneau, Alaska during 2011-2014. Our objectives were to identify the structures they use for hibernation, measure the microclimates within those structures, and determine the timing of immergence and emergence and the length of the hibernation season. We radiotracked 10 little brown bats to underground hibernacula dispersed along two ridge systems. All hibernacula were ≤ 24.2 km from where the bats were captured. Eight bats hibernated in the "Milieu Souterrain Superficiel" (MSS), a network of air-filled underground voids between the rock fragments found in scree (talus) deposits. Two bats hibernated in holes in the soil beneath the root system of a tree or stump (rootball). At least two hibernacula in the MSS were reused in subsequent years. Average MSS and rootball temperatures were warmer and more stable than ambient temperature and were well below the optimal growth range of the fungus that causes WNS. Temperatures in the MSS dropped below freezing, but MSS temperatures increased with depth, indicating bats could avoid subfreezing temperatures by moving deeper into the MSS. Relative humidity (RH) approached 100% in the MSS and under rootballs and was more stable than ambient RH, which also was high, but dropped substantially during periods of extreme cold. Acoustic monitoring revealed that bats hibernated by late October and began emerging by the second week of April; estimates of minimum length of the hibernation season ranged from 156 to 190 days. The cold temperatures, dispersed nature of the hibernacula, and close proximity of hibernacula to summering areas may slow the spread and reduce the impacts of WNS on local populations of little brown bats.

Project description:White-nose syndrome (WNS), a fungal disease that has caused catastrophic population declines of bats in eastern North America, is rapidly spreading across the continent and now threatens previously unexposed bat species in western North America. The causal agent of WNS, the fungus Pseudogymnoascus destructans, can infect many species of hibernating bats, but susceptibility to WNS varies by host species. We previously reported that certain traits of the skin microbiome, particularly yeast diversity and abundance, of bat species in eastern North America are strongly associated with resistance to WNS. Using these traits, we developed models to predict WNS susceptibility of 13 species of western North American bats. Based on models derived from yeast species diversity, only one bat species, Myotis velifer, was predicted to be WNS resistant (i.e., may develop the disease, but with low mortality rates). We also screened yeasts found on western bats for P. destructans-antagonistic properties by spore germination and growth inhibition/competition assays and found the ability of yeasts to inhibit P. destructans in vitro to be strain specific. Similar to results of inhibition assays performed with yeasts isolated from bats in eastern North America, few yeasts isolated from bats in western North America inhibited P. destructans in vitro. Continued monitoring of western bat populations will serve to validate the accuracy of the mycobiome analysis in predicting WNS susceptibility, document population and susceptibility trends, and identify additional predictors to assess the vulnerability of naive bat populations to WNS. IMPORTANCE White-nose syndrome is one of the most devastating wildlife diseases ever documented. Some bat species are resistant to or tolerant of the disease, and we previously reported that certain traits of the skin mycobiome of bat species in eastern North America are strongly associated with resistance to WNS. Predicting which western bat species will be most susceptible to WNS would be of great value for establishing conservation priorities. Based on models derived from yeast species diversity, only one bat species was predicted to be WNS resistant. High susceptibility to WNS would pose a significant conservation threat to bats in western North America.

Project description:Prior to the introduction of white-nose syndrome (WNS) to North America, temperate bats were thought to remain within hibernacula throughout most of the winter. However, recent research has shown that bats in the southeastern United States emerge regularly from hibernation and are active on the landscape, regardless of their WNS status. The relationship between winter activity and susceptibility to WNS has yet to be explored but warrants attention, as it may enable managers to implement targeted management for WNS-affected species. We investigated this relationship by implanting 1346 passive integrated transponder (PIT) tags in four species that vary in their susceptibility to WNS. Based on PIT-tag detections, three species entered hibernation from late October to early November. Bats were active at hibernacula entrances on days when midpoint temperatures ranged from -1.94 to 22.78°C (mean midpoint temperature = 8.70 ± 0.33°C). Eastern small-footed bats (Myotis leibii), a species with low susceptibility to WNS, were active throughout winter, with a significant decrease in activity in mid-hibernation (December 16 to February 15). Tricolored bats (Perimyotis subflavus), a species that is highly susceptible to WNS, exhibited an increase in activity beginning in mid-hibernation and extending through late hibernation (February 16 to March 31). Indiana bats (M. sodalis), a species determined to have a medium-high susceptibility to WNS, remained on the landscape into early hibernation (November 1 to December 15), after which we did not record any again until the latter portion of mid-hibernation. Finally, gray bats (M. grisescens), another species with low susceptibility to WNS, maintained low but regular levels of activity throughout winter. Given these results, we determined that emergence activity from hibernacula during winter is highly variable among bat species and our data will assist wildlife managers to make informed decisions regarding the timing of implementation of species-specific conservation actions.

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Body mass and hibernation microclimate may predict bat susceptibility to white?nose syndrome

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