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Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat (Myotis lucifugus) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans, which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting populations than in declining populations where the fungus has recently invaded. Fitted models indicate that this is most consistent with a reduction in the growth rate of the pathogen when fungal loads become high. The data are inconsistent with the evolution of tolerance or an overall reduced pathogen growth rate that might be caused by environmental factors. The existence of resistance in some persisting populations of little brown bats offers a glimmer of hope that a precipitously declining species will persist in the face of this deadly pathogen. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

Reduced food availability is implicated in declines in avian aerial insectivores, but the effect of nutritional stress on mammalian aerial insectivores is unclear. Unlike birds, insectivorous bats provision their young through lactation, which might protect nursing juveniles when prey availability is low but could increase the energetic burden on lactating females. We analyzed a 15-year capture–mark–recapture data set from 5312 individual little brown myotis (Myotis lucifugus) captured at 11 maternity colonies in northwestern Canada, to test the hypothesis that nutritional stress is impacting these mammalian aerial insectivores. We used long-bone (forearm [FA]) length as a proxy for relative access to nutrition during development, and body mass as a proxy for access to nutrition prior to capture. Average FA length and body mass both decreased significantly over the study period in adult females and juveniles, suggesting decreased access to nutrition. Effect sizes were very small, similar to those reported for declining body size in avian aerial insectivores. Declines in juvenile body mass were only observed in individuals captured in late summer when they were foraging independently, supporting our hypothesis that lactation provides some protection to nursing young during periods of nutritional stress. Potential drivers of the decline in bat size include one or both of (1) declining insect (prey) abundance, and (2) declining prey availability. Echolocating insectivorous bats cannot forage effectively during rainfall, which is increasing in our study area. The body mass of captured adult females and juveniles in our study was lower, on average, after periods of high rainfall, and higher after warmer-than-average periods. Finally, survival models revealed a positive association between FA length and survival, suggesting a fitness consequence to declines in body size. Our study area has not yet been impacted by bat white-nose syndrome (WNS), but research elsewhere has suggested that fatter bats are more likely to survive infection. We found evidence for WNS-independent shifts in the body size of little brown myotis, which can inform studies investigating population responses to WNS. More broadly, the cumulative effects of multiple stressors (e.g., disease, nutritional stress, climate change, and other pressures) on mammalian aerial insectivores require urgent attention.

Abstract The role of the skin microbiome in resistance and susceptibility of wildlife to fungal pathogens has been examined from a taxonomic perspective but skin microbial function, in the context of fungal infection, has yet to be studied. Our objective was to understand effects of a bat fungal pathogen site infection status and course of invasion on skin microbial function. We sampled seven hibernating colonies of Myotis lucifugus covering three-time points over the course of Pseudogymnoascus destructans (Pd) invasion and white nose syndrome (pre-invasion, epidemic, and established). Our results support three new hypotheses about Pd and skin functional microbiome: (1) there is an important effect of Pd invasion stage, especially at the epidemic stage; (2) disruption by the fungus at the epidemic stage could decrease anti-fungal functions with potential negative effects on the microbiome and bat health; (3) the collection site might have a larger influence on microbiomes at the pre-invasion stage rather than at epidemic and established stages. Future studies with larger sample sizes and using meta-omics approaches will help confirm these hypotheses, and determine the influence of the microbiome on wildlife survival to fungal disease.

The use of quantitative real-time PCR (qPCR) to monitor pathogens is common; however, quantitative frameworks that consider the observation process, dynamics in pathogen presence, and pathogen load are lacking. This can be problematic in the early stages of disease progression, where low level detections may be treated as ‘inconclusive’ and excluded from analyses. Alternatively, a framework that accounts for imperfect detection would provide more robust inferences. To better estimate pathogen dynamics, we developed a hierarchical multi-scale dynamic occupancy hurdle model (MS-DOHM). The model used data gathered during sampling for Pseudogymnoascus destructans (Pd) , the causative agent of white-nose syndrome, a fungal disease that has cause severe declines in several species of hibernating bats in North America. The model allowed us to estimate initial occupancy, colonization, persistence and prevalence of Pd at bat hibernacula. Additionally, utilizing the relationship between cycle threshold and pathogen load, we estimated pathogen detectability and modeled expected colony and bat pathogen loads. To assess the ability of MS-DOHM to estimate pathogen dynamics, we compared MS-DOHM’s results to those of a dynamic occupancy model and naïve detection/non-detection. MS-DOHM’s estimates of site-level pathogen presence were up to 11.9% higher than estimates from the dynamic occupancy model and 35.7% higher than naïve occupancy. Including prevalence and load in our modeling framework resulted in estimates of pathogen arrival that were two to three years earlier compared to the dynamic occupancy and naïve detection/non-detection, respectively. Compared to naïve values, MS-DOHM predicted greater pathogen loads on colonies; however, we found no difference between model estimates and naïve values of prevalence. While the model predicted no declines in site-level prevalence, there were instances where pathogen load decreased in colonies that had been Pd positive for longer periods of time. Our findings demonstrate that accounting for pathogen load and prevalence at multiple scales changes our understanding of Pd dynamics, potentially allowing earlier conservation intervention. Additionally, we found that accounting for pathogen load and prevalence within hibernacula and among individuals resulted in a better fitting model with greater predictive ability.

The St. Lawrence River in Eastern Ontario, Canada, has been a designated an area of concern due to past industrial contamination of sediment in some areas and transport of mercury from tributaries. Previous research using bats as sentinel species identified elevated concentrations of total mercury (THg) in fur of local bats and species-specific variation between little brown bats (Myotis lucifugus) and big brown bats (Eptesicus fuscus). Here, we investigated the mercury exposure pathways for these two species by testing the hypothesis that diet variation, particularly the reliance on aquatic over terrestrial insects, is a determinant of local bat mercury concentrations. We analyzed THg concentration and stable isotope ratios of δ15N and δ13C in fur of little and big brown bats, and in aquatic and terrestrial insects. Big brown bats, especially males, accumulated significantly higher THg concentrations in their fur compared to little brown bats. However, this difference was not related to diet because big brown bats consumed terrestrial insects, which were lower in mercury than aquatic insects, the primary prey for little brown bats. We also evaluated whether fur THg concentrations translate into molecular changes in tissues linked to (methyl)mercury toxicity by quantifying tissue changes in global DNA methylation and mitochondrial DNA abundance. No significant changes in DNA molecular markers were observed in relation to fur THg concentration, suggesting mercury exposure to local bats did not impact molecular level changes at the DNA level. Higher mercury in bats was not associated with local aquatic contamination or genotoxicity in this study area.

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.

During late summer and early autumn, temperate bats migrate from their summering sites to swarming sites, where mating likely occurs. However, the extent to which individuals of a single summering site migrate to the same swarming site, and vice versa, is not known. We examined the migratory connectivity between summering and swarming sites in two temperate, North American, bat species, the little brown bat (Myotis lucifugus) and the northern long-eared bat (Myotis septentrionalis). Using mitochondrial and microsatellite DNA markers, we examined population structuring within and among summering and swarming sites. Both species exhibited moderate degrees of mitochondrial DNA differentiation (little brown bat: F.sub.ST(SWARMING) = 0.093, F.sub.ST(SWARMING) = 0.052; northern long-eared bat: F.sub.ST(SWARMING) = 0.117, F.sub.ST(SWARMING) = 0.043) and little microsatellite DNA differentiation among summering and among swarming sites. Haplotype diversity was significantly higher at swarming sites than summering sites, supporting the idea that swarming sites are comprised of individuals from various summering sites. Further, pairwise analyses suggest that swarming sites are not necessarily comprised of only individuals from the most proximal summering colonies.

Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), believed to have originated from a bat species, can infect a wide range of non-human hosts. Bats are known to harbor hundreds of coronaviruses capable of spillover into human populations. Recent studies have shown a significant variation in the susceptibility among bat species to SARS-CoV-2 infection. We show that little brown bats (LBB) express angiotensin-converting enzyme 2 receptor and the transmembrane serine protease 2, which are accessible to and support SARS-CoV-2 binding. All-atom molecular dynamics (MD) simulations revealed that LBB ACE2 formed strong electrostatic interactions with the RBD similar to human and cat ACE2 proteins. In summary, LBBs, a widely distributed North American bat species, could be at risk of SARS-CoV-2 infection and potentially serve as a natural reservoir. Finally, our framework, combining in vitro and in silico methods, is a useful tool to assess the SARS-CoV-2 susceptibility of bats and other animal species.

Management of wildlife populations impacted by novel threats is often challenged by a lack of data on temporal changes in demographic response. Populations may suffer rapid declines from the introduction of new stressors, but how demography changes over time is critical to determining long-term outcomes for populations. White-nose syndrome (WNS), an infectious disease of hibernating bats, has caused massive and rapid population declines in several hibernating species of bats in North America since the disease was first observed on the continent in 2006. Estimating annual survival rates and demographic trends among remnant colonies of hibernating bats that experienced mass mortality from WNS is needed to determine long-term population viability of species impacted by this disease. Using mark-recapture data on infected little brown bats ( Myotis lucifugus ), we estimated the first apparent annual survival rates for four years following WNS detection at a site. We found strong support for an increasing trend in annual survival, which improved from 0.68 (95% CI = 0.44-0.85) to 0.75 (95% CI = 0.51-0.89) for males and 0.65 (95% CI = 0.44-0.81) to 0.70 (95% CI = 0.50-0.84) for females. These results suggest that stabilization at remnant colonies after mass mortality from WNS may be due to improved survival and not from immigration from other areas. Despite ameliorating survival, our stochastic matrix projection model predicts continued declines for little brown bat populations (λ = 0.95), raising concern for the regional persistence of this species. We conducted a vital rate sensitivity analysis and determined that adult and juvenile survival, as opposed to fecundity, are the demographic parameters most important to target to maximize recovery potential of little brown bat populations in areas impacted by WNS.

Threats to North American bat species necessitate the quantification of bat habitat. To characterize bat habitat, we recorded bat echolocation calls from state forests in Indiana, USA. We identified calls using automated classification software and constructed detection histories for 3 species of conservation concern: Indiana bat (Myotis sodalis), little brown bat (Myotis lucifugus), and northern long-eared bat (Myotis septentrionalis). We analyzed these data using single- and multi-species occupancy approaches to estimate occurrence and detection probabilities at the genus level (Myotis) and for each species separately. We constructed models using a suite of habitat covariates (e.g., forest cover, edge, streams, hibernacula, public roads) and determined the effect of these features on occupancy for each species (or group). We validated all models using training and independent data. Occupancy of all species was affected by the proportion of forest in surrounding areas. For most models, bat occupancy was greatest in areas with a lower proportion of forest within 1 km. Occupancy was also often greatest in recently harvested or intact, mature second-growth stands as opposed to stands 10–30 years following harvest. The spatial configuration of water and roads also affected species occupancy. Our methods allowed us to assess the factors that affect occupancy for the genus and individual species, thus allowing for the identification of features useful in classifying important habitat at both taxonomic levels. The results of this study can aid land managers in identifying habitat that may be used by foraging bats and in planning future timber harvests in managed forests.