Environmental transmission of Pseudogymnoascus destructans to hibernating little brown bats

Pathogens with persistent environmental stages can have devastating effects on wildlife communities. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in bat populations of North America. In 2009, during the early stages of the WNS investigation and before molecular techniques had been developed to readily detect P. destructans in environmental samples, we initiated this study to assess whether P. destructans can persist in the hibernaculum environment in the absence of its conclusive bat host and cause infections in naive bats. We transferred little brown bats (Myotis lucifugus) from an unaffected winter colony in northwest Wisconsin to two P. destructans contaminated hibernacula in Vermont where native bats had been excluded. Infection with P. destructans was apparent on some bats within 8 weeks following the introduction of unexposed bats to these environments, and mortality from WNS was confirmed by histopathology at both sites 14 weeks following introduction. These results indicate that environmental exposure to P. destructans is sufficient to cause the infection and mortality associated with WNS in naive bats, which increases the probability of winter colony extirpation and complicates conservation efforts.

The presence of Pseudogymnoascus destructans, a fungal pathogen of bats, correlates with changes in microbial metacommunity structure

Metacommunity theory provides a framework for how community patterns arise from processes across scales, which is relevant for understanding patterns in host-associated microbial assemblages. Microbial metacommunities may have important roles in host health through interactions with pathogens; however, it is unclear how pathogens affect host microbial metacommunities. Here, we studied relationships between a fungal pathogen and a host-associated microbial metacommunity. We hypothesized that a fungal pathogen of bats, Pseudogymnoascus destructans, correlates with a shift in metacommunity structure and changes in relationships between community composition, and factors shaping these assemblages, such as ecoregion. We sampled bat cutaneous microbial assemblages in the presence/absence of P. destructans and analyzed microbial metacommunity composition and relationships with structuring variables. Absence of P. destructans correlated with a metacommunity characterized by a common core microbial group that was lacking in disease positive bats. Additionally, P. destructans presence correlated with a change in the relationship between community structure and ecoregion. Our results suggest that the fungal pathogen intensifies local processes influencing a microbial metacommunity and highlights the importance of cutaneous microbial assemblages in host–pathogen interactions.

Hepatic lipid signatures of little brown bats (Myotis lucifugus) and big brown bats (Eptesicus fuscus) at early stages of white-nose syndrome

White-nose syndrome (WNS) is an emergent wildlife fungal disease of cave-dwelling, hibernating bats that has led to unprecedented mortalities throughout North America. A primary factor in WNS-associated bat mortality includes increased arousals from torpor and premature fat depletion during winter months. Details of species and sex-specific changes in lipid metabolism during WNS are poorly understood and may play an important role in the pathophysiology of the disease. Given the likely role of fat metabolism in WNS and the fact that the liver plays a crucial role in fatty acid distribution and lipid storage, we assessed hepatic lipid signatures of little brown bats (Myotis lucifugus) and big brown bats (Eptesicus fuscus) at an early stage of infection with the etiological agent, Pseudogymnoascus destructans (Pd). Differences in lipid profiles were detected at the species and sex level in the sham-inoculated treatment, most strikingly in higher hepatic triacylglyceride (TG) levels in E. fuscus females compared to males. Interestingly, several dominant TGs (storage lipids) decreased dramatically after Pd infection in both female M. lucifugus and E. fuscus. Increases in hepatic glycerophospholipid (structural lipid) levels were only observed in M. lucifugus, including two phosphatidylcholines (PC [32:1], PC [42:6]) and one phosphatidylglycerol (PG [34:1]). These results suggest that even at early stages of WNS, changes in hepatic lipid mobilization may occur and be species and sex specific. As pre-hibernation lipid reserves may aid in bat persistence and survival during WNS, these early perturbations to lipid metabolism could have important implications for management responses that aid in pre-hibernation fat storage.

Ten-year projection of white-nose syndrome disease dynamics at the southern leading-edge of infection in North America

Predicting the emergence and spread of infectious diseases is critical for the effective conservation of biodiversity. White-nose syndrome (WNS), an emerging infectious disease of bats, has resulted in high mortality in eastern North America. Because the fungal causative agent Pseudogymnoascus destructans is constrained by temperature and humidity, spread dynamics may vary by geography. Environmental conditions in the southern part of the continent are different than the northeast, where disease dynamics are typically studied, making it difficult to predict how the disease will manifest. Herein, we modelled WNS pathogen spread in Texas based on cave densities and average dispersal distances of hosts, projecting these results out to 10 years. We parameterized a predictive model of WNS epidemiology and its effects on bat populations with observed cave environmental data. Our model suggests that bat populations in northern Texas will be more affected by WNS mortality than southern Texas. As such, we recommend prioritizing the preservation of large overwintering colonies of bats in north Texas through management actions. Our model illustrates that infectious disease spread and infectious disease severity can become uncoupled over a gradient of environmental variation and highlight the importance of understanding host, pathogen and environmental conditions across a breadth of environments.

Projecting the compound effects of climate change and white-nose syndrome on North American bat species

Climate change and disease are threats to biodiversity that may compound and interact with one another in ways that are difficult to predict. White-nose syndrome (WNS), caused by a cold-loving fungus (Pseudogymnoascus destructans), has had devastating impacts on North American hibernating bats, and impact severity has been linked to hibernaculum microclimate conditions. As WNS spreads across the continent and climate conditions change, anticipating these stressors’ combined impacts may improve conservation outcomes for bats. We build on the recent development of winter species distribution models for five North American bat species, which used a hybrid correlative-mechanistic approach to integrate spatially explicit winter survivorship estimates from a bioenergetic model of hibernation physiology. We apply this bioenergetic model given the presence of P. destructans , including parameters capturing its climate-dependent growth as well as its climate-dependent effects on host physiology, under both current climate conditions and scenarios of future climate change. We then update species distribution models with the resulting survivorship estimates to predict changes in winter hibernacula suitability under future conditions. Exposure to P. destructans is generally projected to decrease bats’ winter occurrence probability, but in many areas, changes in climate are projected to lessen the detrimental impacts of WNS. This rescue effect is not predicted for all species or geographies and may arrive too late to benefit many hibernacula. However, our findings offer hope that proactive conservation strategies to minimize other sources of mortality could allow bat populations exposed to P. destructans to persist long enough for conditions to improve.

Characteristics of caves used by wintering bats in a subtropical environment

Many cave-roosting bats are declining in number throughout their range because of multiple threats, including disease, disturbance by humans, and habitat loss. Successful conservation of cave-roosting bats requires an understanding of the roles of microclimate, cave structure, and the surrounding landscape on the distribution and abundance of bats, and in particular, the use of winter cave roosts. Cave bats have been well-studied in temperate climates, but we know little about these bats in subtropical climates. From 2015-2017 we conducted 399 winter surveys of 162 caves in Florida to evaluate factors affecting presence and abundance of bats at cave roosts. We also determined whether temperatures at these cave roosts were suitable for Pseudogymnoascus destructans, the fungus that causes white-nose syndrome. Across all 3 years, we detected three species of bats: tri-colored bats Perimyotis subflavus in 126 (77.8%) caves, southeastern myotis Myotis austroriparius in 51 (31.5%) caves, and a single Rafinesque's big-eared bat Corynorhinus rafinesquii. We analyzed presence of both tri-colored bats and southeastern myotis in caves using mixed-effects models with a binomial distribution and the number of tri-colored bats using generalized linear mixed-effects models with a Poisson error distribution. Tri-colored bat presence was significantly and positively influenced by a cooler cave surface temperature, larger cave entrance size, as well as a single entrance, and the presence of solution holes. Tri-colored bat abundance increased in longer, cooler caves that had solution holes, a single entrance, free of obstructions, and had no signs of flooding. Southeastern myotis presence was positively associated with longer, domed caves. To be most effective, conservation efforts in subtropical climates should focus on caves with the identified characteristics. More than 90% of caves surveyed each year had a cave interior surface temperature below the upper critical growth limit for P. destructans (19.8 °C), indicating that most Florida caves are suitable for growth of P. destructans. Therefore, regular monitoring of winter bat populations in subtropical caves may be important for detecting P. destructans or white-nose syndrome.