Search

Understanding host persistence with emerging pathogens is essential for conserving populations. Hosts may initially survive pathogen invasions through pre-adaptive mechanisms. However, whether pre-adaptive traits are directionally selected to increase in frequency depends on the heritability and environmental dependence of the trait and the costs of trait maintenance. Body condition is likely an important pre-adaptive mechanism aiding in host survival, although can be seasonally variable in wildlife hosts. We used data collected over 7 years on bat body mass, infection and survival to determine the role of host body condition during the invasion and establishment of the emerging disease, white-nose syndrome. We found that when the pathogen first invaded, bats with higher body mass were more likely to survive, but this effect dissipated following the initial epizootic. We also found that heavier bats lost more weight overwinter, but fat loss depended on infection severity. Lastly, we found mixed support that bat mass increased in the population after pathogen arrival; high annual plasticity in individual bat masses may have reduced the potential for directional selection. Overall, our results suggest that some factors that contribute to host survival during pathogen invasion may diminish over time and are potentially replaced by other host adaptations.

Emerging infectious diseases have resulted in severe population declines across diverse taxa. In some instances, despite attributes associated with high extinction risk, disease emergence and host declines are followed by host stabilisation for unknown reasons. While host, pathogen, and the environment are recognised as important factors that interact to determine host–pathogen coexistence, they are often considered independently. Here, we use a translocation experiment to disentangle the role of host traits and environmental conditions in driving the persistence of remnant bat populations a decade after they declined 70–99% due to white-nose syndrome and subsequently stabilised. While survival was significantly higher than during the initial epidemic within all sites, protection from severe disease only existed within a narrow environmental space, suggesting host traits conducive to surviving disease are highly environmentally dependent. Ultimately, population persistence following pathogen invasion is the product of host–pathogen interactions that vary across a patchwork of environments. Published version

The spillover of SARS-CoV-2 into humans has caused one of the most devastating pandemics in recorded history. Human-animal interactions have led to transmission events of SARS-CoV-2 from humans to wild and captive animals. However, many questions remain about how extensive SARS-CoV-2 exposure is in wildlife, the factors that influence wildlife transmission risk, and whether sylvatic cycles can generate novel variants with increased infectivity and virulence. We sampled 22 different wildlife species in Virginia, U.S.A. We detected widespread exposure to SARS-CoV-2 across six wildlife species. Using quantitative reverse transcription polymerase chain reaction, we detected SARS-CoV-2 RNA in the Virginia opossum and had equivocal detections in six additional species. Furthermore, we used whole genome sequencing to confirm the presence of SARS-CoV-2 and compare mutations present to known circulating strains. Species that exhibit peridomestic tendencies had high seroprevalence, ranging between 62%-71%, and sites with high human presence had three times higher seroprevalence than low human-use areas across all species combined. SARS-CoV-2 genomic data from an opossum and molecular modeling exposed one previously uncharacterized change to an amino acid residue in the Spike receptor binding domain (RBD), which predicts improved binding between the Spike protein and human angiotensin-converting enzyme (ACE2) compared to the dominant variant circulating at the time of collection. Overall, our results highlight widespread exposure to SARS-CoV-2 in wildlife and suggest that areas with high human activity may serve as important points of contact for cross-species transmission. Furthermore, this work highlights the potential role of wildlife as reservoirs for SARS-CoV-2.Significance StatementThe emergence of SARS-CoV-2 has resulted in unprecedented consequences for humans across the globe. Transmission of SARS-CoV-2 among species has the potential to generate new and more virulent variants, posing a threat to both public health and animal populations. However, the ability of SARS-CoV-2 to infect wildlife other than white tailed deer and mustelids in nature remains unknown. We examined exposure to SARS-CoV-2 in 22 wildlife species, which are commonly found across the Eastern U.S. We found widespread SARS-CoV-2 exposure in six common wildlife species, which was elevated in areas with high human activity. Our results highlight the capacity of SARS-CoV-2 to spread through wildlife communities.

Environmental pathogen reservoirs exist for many globally important diseases and can fuel disease outbreaks, affect pathogen evolution, and increase the threat of host extinction. Differences in pathogen shedding among hosts can create mosaics of infection risk across landscapes by increasing pathogen contamination in high use areas. However, how the environmental reservoir establishes in multi-host communities and the importance of factors like host-specific infection and abundance in environmental contamination and transmission remain important outstanding questions. Here we examine how Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats, invades and establishes in the environment. We quantified dynamic changes in pathogen shedding, infection intensities, host abundance, and the subsequent propagule pressure imposed by each species within the community. We find that the initial establishment of the pathogen reservoir is driven by different species within the community than those that are responsible for maintaining the reservoir over time. Our results also show that highly shedding species do not always contribute the most to pathogen reservoirs. More broadly, we demonstrate how individual host shedding rates scale to influence landscape-level pathogen contamination.Open Research statementData will be made available through the Dryad Digital Repository before publication or upon reviewer request.

Demographic factors are fundamental in shaping infectious disease dynamics. Aspects of populations that create structure, like age and sex, can affect patterns of transmission, infection intensity and population outcomes. However, studies rarely link these processes from individual to population-scale effects. Moreover, the mechanisms underlying demographic differences in disease are frequently unclear. Here, we explore sex-biased infections for a multi-host fungal disease of bats, white-nose syndrome, and link disease-associated mortality between sexes, the distortion of sex ratios, and the potential mechanisms underlying sex differences in infection. We collected data on host traits, infection intensity, and survival of five bat species at 42 sites across seven years. We found females were more infected than males for all five species. Females also had lower apparent survival over winter and accounted for a smaller proportion of populations over time. Notably, female-biased infections were evident by early hibernation and likely driven by sex-based differences in autumn mating behavior. Male bats were more active during autumn which likely reduced replication of the cool-growing fungus. Higher disease impacts in female bats may have cascading effects on bat populations beyond the hibernation season by limiting recruitment and increasing the risk of Allee effects.

The recent introduction of Pseudogymnoascus destructans (the fungal pathogen that causes white-nose syndrome in bats) from Eurasia to North America has resulted in the collapse of North American bat populations and restructured species communities. The long evolutionary history between P. destructans and bats in Eurasia makes understanding host life history essential to uncovering the ecology of P. destructans. In this Review, we combine information on pathogen and host biology to understand the patterns of P. destructans spread, seasonal transmission ecology, the pathogenesis of white-nose syndrome and the cross-scale impact from individual hosts to ecosystems. Collectively, this research highlights how early pathogen detection and quantification of host impacts has accelerated the understanding of this newly emerging infectious disease.

Habitat alteration can influence suitability, creating ecological traps where habitat preference and fitness are mismatched. Despite their importance, ecological traps are notoriously difficult to identify and their impact on host–pathogen dynamics remains largely unexplored. Here we assess individual bat survival and habitat preferences in the midwestern United States before, during, and after the invasion of the fungal pathogen that causes white-nose syndrome. Despite strong selection pressures, most hosts continued to select habitats where disease severity was highest and survival was lowest, causing continued population declines. However, some individuals used refugia where survival was higher. Over time, a higher proportion of the total population used refugia than before pathogen arrival. Our results demonstrate that host preferences for habitats with high disease-induced mortality can create ecological traps that threaten populations, even in the presence of accessible refugia., Temperature-dependent host–pathogen interactions may lead species to shift their thermal preferences under pathogen pressure. However, here the authors show that bats have not altered their microclimate preferences due to temperature-mediated mortality from white-nose syndrome, finding instead a sustained preference for warmer sites with high mortality.

Provisioning of wildlife, such as backyard bird feeding, can alter animal behavior and ecology in diverse ways. For species that are highly dependent on supplemental resources, it is critical to understand how variation in the degree of provisioning, as occurs naturally across backyards, alters wildlife behavior and ecology in ways potentially relevant to disease spread. We experimentally manipulated feeder density at suburban sites and tracked local abundance, foraging behaviors, body mass, and movement in House Finches (Haemorhous mexicanus (P.L. Statius Müller, 1776)), the primary host of a pathogen commonly spread at feeders. Sites with high feeder density harbored higher local House Finch abundance, and birds at these sites had longer feeding bouts and total time on feeders relative to sites with low feeder density. House Finches at high-density feeder sites had lower residual body mass despite greater apparent feeder access. Finally, birds first recorded at low-density feeder sites were more likely to move to neighboring high-density feeder sites than vice versa. Because local abundance and time spent on feeders have both been linked with disease risk in this species, the effects of heterogeneity in bird feeder density on these traits may have important consequences for disease dynamics in this system and more broadly.

West Nile virus (WNV) was first identified in North America almost 20 yr ago. In that time, WNV has crossed the continent and established enzootic transmission cycles, resulting in intermittent outbreaks of human disease that have largely been linked with climatic variables and waning avian seroprevalence. During the transcontinental dissemination of WNV, the original genotype has been displaced by two principal extant genotypes which contain an envelope mutation that has been associated with enhanced vector competence by Culex pipiens L. (Diptera: Culicidae) and Culex tarsalis Coquillett vectors. Analyses of retrospective avian host competence data generated using the founding NY99 genotype strain have demonstrated a steady reduction in viremias of house sparrows over time. Reciprocally, the current genotype strains WN02 and SW03 have demonstrated an inverse correlation between house sparrow viremia magnitude and the time since isolation. These data collectively indicate that WNV has evolved for increased avian viremia while house sparrows have evolved resistance to the virus such that the relative host competence has remained constant. Intrahost analyses of WNV evolution demonstrate that selection pressures are avian species-specific and purifying selection is greater in individual birds compared with individual mosquitoes, suggesting that the avian adaptive and/or innate immune response may impose a selection pressure on WNV. Phylogenomic, experimental evolutionary systems, and models that link viral evolution with climate, host, and vector competence studies will be needed to identify the relative effect of different selective and stochastic mechanisms on viral phenotypes and the capacity of newly evolved WNV genotypes for transmission in continuously changing landscapes.

Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of a probiotic bacterium, Pseudomonas fluorescens, to reduce impacts of WNS in two simultaneous experiments with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the cage experiment there was no difference in survival between control and P. fluorescens-treated bats. However, body mass, not infection intensity, predicted mortality, suggesting that within-cage disturbance influenced the cage experiment. In the free-flying experiment, where bats were able to avoid conspecific disturbance, infection intensity predicted the date of emergence from the mine. In this experiment treatment with P. fluorescens increased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by approximately 32 days. These results suggest that treatment of bats with P. fluorescens may substantially reduce WNS mortality, and, if used in combination with other interventions, could stop population declines.

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.

Emerging infectious diseases can have devastating effects on host communities, causing population collapse and species extinctions. The timing of novel pathogen arrival into naïve species communities can have consequential effects that shape the trajectory of epidemics through populations. Pathogen introductions are often presumed to occur when hosts are highly mobile. However, spread patterns can be influenced by a multitude of other factors including host body condition and infectiousness.White‐nose syndrome (WNS) is a seasonal emerging infectious disease of bats, which is caused by the fungal pathogen Pseudogymnoascus destructans. Within‐site transmission of P. destructans primarily occurs over winter; however, the influence of bat mobility and infectiousness on the seasonal timing of pathogen spread to new populations is unknown. We combined data on host population dynamics and pathogen transmission from 22 bat communities to investigate the timing of pathogen arrival and the consequences of varying pathogen arrival times on disease impacts.We found that midwinter arrival of the fungus predominated spread patterns, suggesting that bats were most likely to spread P. destructans when they are highly infectious, but have reduced mobility. In communities where P. destructans was detected in early winter, one species suffered higher fungal burdens and experienced more severe declines than at sites where the pathogen was detected later in the winter, suggesting that the timing of pathogen introduction had consequential effects for some bat communities. We also found evidence of source–sink population dynamics over winter, suggesting some movement among sites occurs during hibernation, even though bats at northern latitudes were thought to be fairly immobile during this period. Winter emergence behaviour symptomatic of white‐nose syndrome may further exacerbate these winter bat movements to uninfected areas.Our results suggest that low infectiousness during host migration may have reduced the rate of expansion of this deadly pathogen, and that elevated infectiousness during winter plays a key role in seasonal transmission. Furthermore, our results highlight the importance of both accurate estimation of the timing of pathogen spread and the consequences of varying arrival times to prevent and mitigate the effects of infectious diseases., This paper examines when a virulent fungal disease of bat, white‐nose syndrome, spreads to new locations. The authors find that the fungus spreads to more new locations during the winter even though bats are mostly sedentary during this time.

The recent introduction of Pseudogymnoascus destructans (the fungal pathogen that causes white-nose syndrome in bats) from Eurasia to North America has resulted in the collapse of North American bat populations and restructured species communities. The long evolutionary history between P. destructans and bats in Eurasia makes understanding host life history essential to uncovering the ecology of P. destructans. In this Review, we combine information on pathogen and host biology to understand the patterns of P. destructans spread, seasonal transmission ecology, the pathogenesis of white-nose syndrome and the cross-scale impact from individual hosts to ecosystems. Collectively, this research highlights how early pathogen detection and quantification of host impacts has accelerated the understanding of this newly emerging infectious disease.

Population monitoring and research are essential for conserving wildlife, but these activities may directly impact the populations under study. These activities are often restricted to minimize disturbance, and impacts must be weighed against knowledge gained. However, few studies have quantified the effects of research or census-related visitation frequency on populations, and low visitation rates have been hypothesized to have little effect. Hibernating bats have been hypothesized to be especially sensitive to visitation because they have limited energetic stores to survive winter, and disturbance may partly deplete these stores. We examined the effect of site visitation frequency on population growth rates of three species of hibernating bats, little brown bats (Myotis lucifugus), Indiana bats (Myotis sodalis) and tri-colored bats (Perimyotis subflavus), both before and after detection of the disease white-nose syndrome. We found no evidence that more frequent visits decreased population growth rates for any of these species. Estimated coefficients were either the opposite sign as hypothesized (population growth rates increased with visitation frequency) or were very small (difference in population growth rates 0.067% [SE 2.5%]-1.8% [SE 9.8%]) relative to spatial and temporal variation (5.9-32%). In contrast, white-nose syndrome impacts on population growth rates were easily detected and well-characterized statistically (effect sizes 4.4-8.0; severe population declines occurred in the second and third years after pathogen detection) indicating that we had sufficient power to detect effects. These results indicate that visitation frequency (forM. sodalis:annual vs. semi-annual counts; forM. lucifugusandP. subflavus:1-3 three research visits per year) had undetectable impacts on bat population growth rates both with and without the additional stress of an emerging infectious disease. Knowledge gained from censuses and research may outweigh disturbance due to human visitation if it can be used to understand and conserve the species. National Science FoundationNational Science Foundation (NSF) [DEB-1115895, DEB-1336290, DEB 1911853]; US FWSUS Fish & Wildlife Service National Science Foundation, Grant/Award Numbers: DEB-1115895, DEB-1336290, DEB 1911853; US FWS Public domain – authored by a U.S. government employee

Understanding host interactions that lead to pathogen transmission is fundamental to the prediction and control of epidemics1-5. Although the majority of transmissions often occurs within social groups6-9, the contribution of connections that bridge groups and species to pathogen dynamics is poorly understood10-12. These cryptic connections-which are often indirect or infrequent-provide transmission routes between otherwise disconnected individuals and may have a key role in large-scale outbreaks that span multiple populations or species. Here we quantify the importance of cryptic connections in disease dynamics by simultaneously characterizing social networks and tracing transmission dynamics of surrogate-pathogen epidemics through eight communities of bats. We then compared these data to the invasion of the fungal pathogen that causes white-nose syndrome, a recently emerged disease that is devastating North American bat populations13-15. We found that cryptic connections increased links between individuals and between species by an order of magnitude. Individuals were connected, on average, to less than two per cent of the population through direct contact and to only six per cent through shared groups. However, tracing surrogate-pathogen dynamics showed that each individual was connected to nearly fifteen per cent of the population, and revealed widespread transmission between solitarily roosting individuals as well as extensive contacts among species. Connections estimated from surrogate-pathogen epidemics, which include cryptic connections, explained three times as much variation in the transmission of the fungus that causes white-nose syndrome as did connections based on shared groups. These findings show how cryptic connections facilitate the community-wide spread of pathogens and can lead to explosive epidemics.

Significance Infectious diseases can have devastating effects on populations, and the ability of a pathogen to persist in the environment can amplify these impacts. Understanding how environmental pathogen reservoirs influence the number of individuals that become infected and suffer mortality is essential for disease control and prevention. We integrated disease data with population surveys to examine the influence of the environmental reservoir on disease impacts for a devastating fungal disease of bats, white-nose syndrome. We find that the extent of pathogen present in the environment predicts how many hosts become infected and suffer mortality during disease outbreaks. These results provide a target for managing contamination levels in the environment to reduce population impacts., Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.

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, andPerimyotis 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 ITS amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructansis present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas 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 ofP. destructansfor 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 WNS inM. lucifugus, but not for other bat species impacted by white-nose syndrome.

Disease dynamics during pathogen invasion and establishment determine the impacts of disease on host populations and determine the mechanisms of host persistence. Temporal progression of prevalence and infection intensity illustrate whether tolerance, resistance, reduced transmission, or demographic compensation allow initially declining populations to persist. We measured infection dynamics of the fungal pathogen Pseudogymnoascus destructans that causes white-nose syndrome in bats by estimating pathogen prevalence and load in seven bat species at 167 hibernacula over a decade as the pathogen invaded, became established, and some host populations stabilized. Fungal loads increased rapidly and prevalence rose to nearly 100% at most sites within 2 yr of invasion in six of seven species. Prevalence and loads did not decline over time despite huge reductions in colony sizes, likely due to an extensive environmental reservoir. However, there was substantial variation in fungal load among sites with persisting colonies, suggesting that both tolerance and resistance developed at different sites in the same species. In contrast, one species disappeared from hibernacula within 3 yr of pathogen invasion. Variable host responses to pathogen invasion require different management strategies to prevent disease-induced extinction and to facilitate evolution of tolerance or resistance in persisting populations.

Summary The management of infectious diseases is an important conservation concern for a growing number of wildlife species. However, effective disease control in wildlife is challenging because feasible management options are often lacking. White-nose syndrome (WNS) is an infectious disease of hibernating bats that currently threatens several North American species with extinction. Currently, no effective treatments exist for WNS. We conducted a laboratory experiment to test the efficacy of probiotic treatment with Pseudomonas fluorescens, a bacterium that naturally occurs on bats, to reduce disease severity and improve survival of little brown bats Myotis lucifugus exposed to Pseudogymnoascus destructans, the fungal pathogen that causes WNS. We found that application of the probiotic bacteria at the time of fungal infection reduced several measures of disease severity and increased survival, whereas bacterial treatment prior to pathogen exposure had no effect on survival and worsened disease severity. Synthesis and applications. Our results suggest that probiotic treatment with Ps. fluorescens has potential for white-nose syndrome disease management, but the timing of application is critical and should coincide with natural exposure of bats to P. destructans. These results add to the growing knowledge of how natural host microbiota can be implemented as a biocontrol treatment to influence disease outcomes.

Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungusPseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of two treatments, a probiotic bacterium,Pseudomonas fluorescens, and a chemical, chitosan, to reduce impacts of WNS in two simultaneous experiments conducted with caged and free-flyingMyotis lucifugusbats at a mine in Wisconsin, USA. In the free-flying experiment, treatment withP. fluorescensincreased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by 30 days. Apparent overwinter survival for free-flying chitosan-treated bats was 18.0%, which did not differ significantly from control bats. In the cage experiment, chitosan-treated bats had significantly higher survival until release on March 8 (53%) than control andP. fluorescens-treated bats (both 27%). However, these differences were likely due to within-cage disturbance and not reduced WNS impacts, because chitosan-treated bats actually had significantly higher UV-fluorescence (a measure of disease severity), and body mass, not infection intensity, predicted mortality. Further, few of the bats released from the cage experiment were detected emerging from the mine, indicating that the survival estimates at the time of release did not carryover to overwinter survival. These results suggest that treatment of bats may reduce WNS mortality, but additional measures are needed to prevent declines.

Understanding the causes of vaccine failure is important for predicting disease dynamics in vaccinated populations and planning disease interventions. Pathogen exposure dose and heterogeneity in host susceptibility have both been implicated as important factors that may reduce overall vaccine efficacy and cause vaccine failure. Here, we explore the effect of pathogen dose and heterogeneity in host susceptibility in reducing efficacy of vaccines. Using simulation-based methods, we find that increases in pathogen exposure dose decrease vaccine efficacy, but this effect is modified by heterogeneity in host susceptibility. In populations where the mode of vaccine action is highly polarized, vaccine efficacy decreases more slowly with exposure dose than in populations with less variable protection. We compared these theoretical results to empirical estimates from a systematic literature review of vaccines tested over multiple exposure doses. We found that few studies (nine of 5,389) tested vaccine protection against infection over multiple pathogen challenge doses, with seven studies demonstrating a decrease in vaccine efficacy with increasing exposure dose. Our research demonstrates that pathogen dose has potential to be an important determinant of vaccine failure, although the limited empirical data highlight a need for additional studies to test theoretical predictions on the plausibility of reduced host susceptibility and high pathogen dose as mechanisms responsible for reduced vaccine efficacy in high transmission settings. Funding was provided by the NIH EEID grant R01GM113233. MGMG was funded by Fundação para a Ciência e a Tecnologia (IF/01346/2014) and is a member of the Human Infection Challenge Network for Vaccine Development (HIC-Vac), which is funded by the GCRF Networks in Vaccines Research and Development, which was co-funded by the MRC and BBSRC.

White-nose syndrome has devastated bat populations in eastern North America. In Midwestern United States, prevalence increased quickly in the first year of invasion (2012–13) but with low population declines. In the second year (2013–14), environmental contamination led to earlier infection and high population declines. Interventions must be implemented before or soon after fungal invasion to prevent population collapse.

Emerging infectious diseases pose an important threat to wildlife. While established protocols exist for combating outbreaks of human and agricultural pathogens, appropriate management actions before, during, and after the invasion of wildlife pathogens have not been developed. We describe stage-specific goals and management actions that minimize disease impacts on wildlife, and the research required to implement them. Before pathogen arrival, reducing the probability of introduction through quarantine and trade restrictions is key because prevention is more cost effective than subsequent responses. On the invasion front, the main goals are limiting pathogen spread and preventing establishment. In locations experiencing an epidemic, management should focus on reducing transmission and disease, and promoting the development of resistance or tolerance. Finally, if pathogen and host populations reach a stable stage, then recovery of host populations in the face of new threats is paramount. Successful management of wildlife disease requires risk-taking, rapid implementation, and an adaptive approach. "Funding was provided by the US National Science Foundation (grants EF-0914866, DGE-0741448, DEB-1115069, DEB-1336290) and the National Institutes of Health (grant 1R010AI090159)." https://esajournals.onlinelibrary.wiley.com/doi/abs/10.1890/140241

Heterogeneity in host susceptibility is a key determinant of infectious disease dynamics but is rarely accounted for in assessment of disease control measures. Understanding how susceptibility is distributed in populations, and how control measures change this distribution, is integral to predicting the course of epidemics with and without interventions. Using multiple experimental and modeling approaches, we show that rainbow trout have relatively homogeneous susceptibility to infection with infectious hematopoietic necrosis virus and that vaccination increases heterogeneity in susceptibility in a nearly all-or-nothing fashion. In a simple transmission model with an R0 of 2, the highly heterogeneous vaccine protection would cause a 35 percentage-point reduction in outbreak size over an intervention inducing homogenous protection at the same mean level. More broadly, these findings provide validation of methodology that can help to reduce biases in predictions of vaccine impact in natural settings and provide insight into how vaccination shapes population susceptibility., IMPORTANCE Differences among individuals influence transmission and spread of infectious diseases as well as the effectiveness of control measures. Control measures, such as vaccines, may provide leaky protection, protecting all hosts to an identical degree, or all-or-nothing protection, protecting some hosts completely while leaving others completely unprotected. This distinction can have a dramatic influence on disease dynamics, yet this distribution of protection is frequently unaccounted for in epidemiological models and estimates of vaccine efficacy. Here, we apply new methodology to experimentally examine host heterogeneity in susceptibility and mode of vaccine action as distinct components influencing disease outcome. Through multiple experiments and new modeling approaches, we show that the distribution of vaccine effects can be robustly estimated. These results offer new experimental and inferential methodology that can improve predictions of vaccine effectiveness and have broad applicability to human, wildlife, and ecosystem health.

Reduced populations of Myotis lucifugus (Little Brown Myotis) devastated by white-nose syndrome (WNS) persist in eastern North America. Between 2009 and 2013, we recaptured 113 marked individuals that survived between 1 and 6 winters in New England since the arrival of WNS. We also observed signs of reproductive success in 57 recaptured bats.

Emerging infectious diseases (EIDs) are on the rise due to multiple factors, including human facilitated movement of pathogens, broad-scale landscape changes, and perturbations to ecological systems (Jones et al. 2008; Fisher et al. 2012). Epidemics in wildlife are problematic because they can lead to pathogen spillover to new host organisms, erode biodiversity and threaten ecosystems that sustain human societies (Fisher et al. 2012; Kilpatrick 2011). There have been recent calls for large-scale research approaches to combat the threats EIDs pose to wildlife (Sleeman 2013). While it is true that developing new analytical models, diagnostic assays and molecular tools will significantly advance our abilities to respond to disease threats, we also propose that addressing difficult problems in EIDs will require considerable shifts in international health policy and infrastructure. While there are currently international organizations responsible for rapidly initiating and coordinating preventative measures to control infectious diseases in human, livestock, and arable systems, there are few comparable institutions that have the authority to implement transnational responses to EIDs in wildlife. This absence of well-developed infrastructure hampers the rapid responses necessary to mitigate international spread of EIDs.

Wildlife diseases have been implicated in the declines and extinctions of several species. The ability of a pathogen to persist outside its host, existing as an ''environmental reservoir'', can exacerbate the impact of a disease and increase the likelihood of host extinction. Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats, has been found in cave soil during the summer when hibernating bats had likely been absent for several months. However, whether the pathogen can persist over multiple years in the absence of bats is unknown, and long-term persistence of the pathogen can influence whether hibernacula where bats have been locally extirpated due to disease can be subsequently recolonized. Here, we show that P. destructans is capable of long-term persistence in the laboratory in the absence of bats. We cultured P. destructans from dried agar plates that had been kept at 5C and low humidity conditions (30-40% RH) for more than 5 years. This suggests that P. destructans can persist in the absence of bats for long periods which may prevent the recolonization of hibernation, sites where bat populations were extirpated. This increases the extinction risk of bats affected by this disease.

Host parasite models are typically constructed under either a microparasite or macroparasite paradigm. However, this has long been recognized as a false dichotomy because many infectious disease agents, including most fungal pathogens, have attributes of both microparasites and macroparasites. We illustrate how Integral Projection Models (IPM)s provide a novel, elegant modeling framework to represent both types of pathogens. We build a simple host-parasite IPM that tracks both the number of susceptible and infected hosts and the distribution of parasite burdens in infected hosts. The vital rate functions necessary to build IPMs for disease dynamics share many commonalities with classic micro and macroparasite models and we discuss how these functions can be parameterized to build a host-parasite IPM. We illustrate the utility of this IPM approach by modeling the temperature-dependent epizootic dynamics of amphibian chytrid fungus in Mountain yellow-legged frogs (Rana muscosa). The host-parasite IPM can be applied to other diseases such as facial tumor disease in Tasmanian devils and white-nose syndrome in bats. Moreover, the host-parasite IPM can be easily extended to capture more complex disease dynamics and provides an exciting new frontier in modeling wildlife disease.

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’.

We monitored a maternity colony of little brown myotis Myotis lucifugus on Fort Drum Military Installation in northern New York in 2009 and 2010 for impacts associated with white-nose syndrome. Declines in colony numbers presumed to be caused by white-nose syndrome were initially discovered in the spring 2009. Although colony numbers have continued to decline, we determined that a minimum of 12 individual banded female little brown myotis survived over multiple years despite exposure to white-nose syndrome. Our results also provide evidence that 14 of 20 recaptured female little brown myotis were able to heal from wing damage and infection associated with white-nose syndrome within a given year, and seven of eight recaptures from within both 2009 and 2010 showed evidence of reproduction.

White-nose syndrome (WNS) is a disease responsible for unprecedented mortality in hibernating bats. First observed in a New York cave in 2006, mortality associated with WNS rapidly appeared in hibernacula across the northeastern United States. We used yearly presence–absence data on WNS-related mortality among hibernating bat colonies in the Northeast to determine factors influencing its spread. We evaluated hazard models to test hypotheses about the association between the timing of mortality and colony-level covariates, such as distance from the first WNS-affected site, colony size, species diversity, species composition and type of hibernaculum (cave or mine). Distance to origin and colony size had the greatest effects on WNS hazard over the range of observations; the type of hibernaculum and species composition had weaker effects. The distance effect showed a temporal decrease in magnitude, consistent with the pattern of an expanding epizootic. Large, cave-dwelling bat colonies with high proportions of Myotis lucifugus or other species that seek humid microclimates tended to experience early mortality. Our results suggest that the timing of mortality from WNS is largely dependent on colony location, and large colonies tend to be first in an area to experience high mortality associated with WNS.

Inland pine barrens offer the rarest type of shrubland habitat in the northeastern United States and may contribute disproportionately to the regional diversity and conservation of shrubland birds. Testing local habitat specialization and estimating survey effort is needed to inform management of pine barrens for this rapidly declining avian group. We evaluated shrubland bird habitat associations in a heavily urbanized pine barrens of the northeastern United States, and used occupancy-detection sampling and analysis to estimate the number of sample points and surveys for point-based monitoring of shrubland birds in pine barrens. Although forest area was significantly greater than shrubland area, 8 of 11 reliably modeled species showed evidence of association for shrubland, and are thus potentially useful as indicators of pine barrens shrubland quality and management to avert succession. From the analysis of survey effort, we suggest two design options for point-based monitoring of shrubland birds in pine barrens: (1) include enough points to cover at least ∼3% of the study area and survey each point ≥5 times preferably during 05:00–08:00 hr, or (2) reduce the point sample, to no less than about 2% of study area, and increase the survey replication to ≥10 surveys. Three surveys, as suggested by shrubland bird experts for anthropogenic early-successional habitats (e.g., utility corridors) and by others as a general rule, may require too many sample points to feasibly monitor shrubland birds in pine barrens.

In Fig. 3d this Letter, the R2 value should have been ‘0.19’ instead of ‘0.66’; this has been corrected online.

Threats to and from Bats Bats appear to be able to host an assortment of alarming pathogens, which, if they do not extirpate the bats, have implications for human health (see the Perspective by Daszak ). For example, exposure to bats is the main source of human rabies in the Americas. But rabies is not generally transmitted among people; humans are a dead end for the virus. Streicker et al. (p. 676 , see the cover) show that rabies virus lineages tend to be specific for bat lineages. It seems that although rabies viruses have the potential for rapid evolution, this property alone is not enough to overcome genetic barriers, which inhibit the onward transmission of rabies virus into a new species. White-nose syndrome, an exotic fungal infection of bats, has, over the past 3 years, spread from upstate New York to West Virginia, killing on average 70% of the animals in a hibernating colony. The infection makes bats restless over winter when they should be dormant, which makes them exhaust their fat reserves, resulting in the death of over a million bats. Frick et al. (p. 679 ) have analyzed population data collected on bats in the northeastern United States for the past 30 years and show that, mainly owing to white-nose syndrome, the once abundant little brown bat is heading for regional extinction in the next 16 years or so. This scale of loss of an insectivorous mammal is expected to have repercussions for ecosystem integrity and for the economic costs of agricultural pest control.

To the Editor: Emerging infectious diseases have caused catastrophic declines in wildlife populations, and the introductions of many pathogen have been linked to increases in global trade and travel (1). Mapping the distribution of pathogens is necessary to identify species and populations at risk and identify sources of pathogen spillover and introduction. Once pathogen distributions are known, management actions can be taken to reduce the risk for future global spread (2). Bats with symptoms of white-nose syndrome (WNS) were first detected in the United States in 2006, and the disease has subsequently caused precipitous declines in temperate bat populations across eastern North America (3,4). Pseudogymnoascus destructans, the causative agent of WNS, is a cold-growing fungus that infects bats’ skin during hibernation, leading to more frequent arousals from torpor and death (3). P. destructans is widespread throughout Europe (5), but, to our knowledge, its presence in Asia has not been documented. We sampled bats and hibernacula surfaces (cave walls and ceilings) across northeastern China during 2 visits (June–July 2014 and March 2015) using a previously described swab-sampling technique (6). Bats were captured inside caves and at their entrances. DNA was extracted from samples by using a modified QIAGEN DNeasy blood and tissue kit (QIAGEN, Valencia, CA, USA) and tested in duplicate for the presence of P. destructans with a quantitative real-time PCR (qPCR) (6,7). In the summer of 2014 and winter of 2015, we collected 385 samples from hibernacula surfaces at 12 sites in 3 provinces and 1 municipality (Figure, panel A) and 215 samples from 9 species of bats at 10 sites (summer: Rhinolophus ferrumequinum, Rhinolophus pusillus, Myotis adversus, Myotis macrodactylus, Myotis pilosus, Myotis chinensis, Murina usseriensis; winter: R. ferrumequinum, Murina leucogaster, Myotis petax). During the summer, P. destructans was widely distributed across the study region with positive samples (determined on the basis of qPCR results) obtained from cave surfaces at 9 of 12 sites and from bats at 2 of the 9 sites where bats were sampled (Figure, panel A). Figure A) Distribution of Pseudogymnoascus destructans in cave environments during summer at 9 sites in northeastern China. Pie charts show the prevalence (red indicates fraction of positive samples) of P. destructans, and the size of pie graphs indicates the ... Prevalence of P. destructans was low during summer in the environment (mean prevalence across sites 0.06 ± 0.03) and in bats. Bats of 3 species tested positive for P. destructans in the summer: M. macrodactylus (1/10), M. chinensis (1/1), and M. ussuriensis (1/1). P. destructans was not detected in bats of 4 other species, of which >20 individual animals of each species were sampled (R. ferrumequinum, R. pusillus, M. pilosus, and M. adversus). The low prevalence of P. destructans in bats and on hibernacula surfaces in China during the summer was similar to comparable results from studies in North America (6). In winter, prevalence at the 2 sites we revisited was much higher; 75% of 85 samples from 3 species tested positive, including samples from 16/17 M. petax bats. We also detected P. destructans in bats from 2 additional species (R. ferrumequinum [11/19 bats] and M. leucogaster [11/16 bats]). In addition, during March 2015, we observed visual evidence of P. destructans in bats (M. petax; Figure, panel C) and obtained 2 fungal cultures from swab specimens taken from these bats. To isolate P. destructans from these samples, we plated swab specimens from visibly infected bats on Sabouraud dextrose agar at 10°C. We identified potential P. destructans isolates on the basis of morphologic characteristics. DNA was then extracted from 2 suspected fungal cultures and tested for P. destructans by qPCR, as previously described. To further confirm the presence of P. destructans, we prepared the fungal isolates for Sanger sequencing (Technical Appendix). The 600-nt amplification products from these 2 isolates were sequenced and found to be 100% identical to the P. destructans rRNA gene region targeted for amplification. In addition, using BLAST (http://www.ncbi.nlm.nih.gov/blast.cgi), we found that sequences were a 100% match with isolates from Europe (GenBank accession no. {"type":"entrez-nucleotide","attrs":{"text":"GQ489024","term_id":"284944064","term_text":"GQ489024"}}GQ489024) and North America (GenBank accession no. {"type":"entrez-nucleotide","attrs":{"text":"EU884924","term_id":"211905147","term_text":"EU884924"}}EU884924). This result confirms that the same species of fungus occurs on all 3 continents. We also obtained wing biopsy punches from these bats and found lesions characteristic of WNS by histopathologic examination (Figure, panel B; Technical Appendix). The occurrence of P. destructans at most sites sampled indicates that this pathogen is widespread in eastern Asia (Figure, panel A). The presence of P. destructans in bats from 6 species in China and on bats in 13 species in Europe (8) confirms the generalist nature of this fungus and suggests that it may occur throughout Eurasia (Figure, panel D). Decontamination and restrictions on the use of equipment that has been used in caves in Asia would help reduce the probability of introducing P. destructans to uninfected bat populations (e.g., western North America, New Zealand, southern Australia, and temperate areas of South America). These measures would also reduce the risk of introducing new strains of P. destructans to regions where bats are already infected (e.g., eastern North America and Europe). These measures are necessary to prevent the devastating effects this pathogen has had on bats in North America and would help maintain the ecosystem services that bats provide (9,10). Technical Appendix: The Technical Appendix describes the DNA sequencing of fungal isolates to confirm the presence of Pseudogymnoascus destructans and histologic examination of bat fungal lesions. Click here to view.(238K, pdf)

Emerging infectious diseases are a key threat to wildlife. Several fungal skin pathogens have recently emerged and caused widespread mortality in several vertebrate groups, including amphibians, bats, rattlesnakes and humans. White-nose syndrome, caused by the fungal skin pathogen Pseudogymnoascus destructans, threatens several hibernating bat species with extinction and there are few effective treatment strategies. The skin microbiome is increasingly understood to play a large role in determining disease outcome. We isolated bacteria from the skin of four bat species, and co-cultured these isolates with P. destructans to identify bacteria that might inhibit or kill P. destructans.We then conducted two reciprocal challenge experiments in vitro with six bacterial isolates (all in the genus Pseudomonas) to quantify the effect of these bacteria on the growth of P. destructans. All six Pseudomonas isolates significantly inhibited growth of P. destructans compared to noninhibitory control bacteria, and two isolates performed significantly better than others in suppressing P. destructans growth for at least 35 days. In both challenge experiments, the extent of suppression of P. destructans growth was dependent on the initial concentration of P. destructans and the initial concentration of the bacterial isolate. These results show that bacteria found naturally occurring on bats can inhibit the growth of P. destructans in vitro and should be studied further as a possible probiotic to protect bats from white-nose syndrome. In addition, the presence of these bacteria may influence disease outcomes among individuals, populations, and species. United States Fish and Wildlife Service: F12AP01081 National Science Foundation: DEB-1115895 Bat Conservation International Student Scholarship

Disease can play an important role in structuring species communities because the effects of disease vary among hosts; some species are driven towards extinction, while others suffer relatively little impact. Why disease impacts vary among host species remains poorly understood for most multi-host pathogens, and factors allowing less-susceptible species to persist could be useful in conserving highly affected species. White-nose syndrome (WNS), an emerging fungal disease of bats, has decimated some species while sympatric and closely related species have experienced little effect. We analysed data on infection prevalence, fungal loads and environmental factors to determine how variation in infection among sympatric host species influenced the severity of WNS population impacts. Intense transmission resulted in almost uniformly high prevalence in all species. By contrast, fungal loads varied over 3 orders of magnitude among species, and explained 98% of the variation among species in disease impacts. Fungal loads increased with hibernating roosting temperatures, with bats roosting at warmer temperatures having higher fungal loads and suffering greater WNS impacts. We also found evidence of a threshold fungal load, above which the probability of mortality may increase sharply, and this threshold was similar for multiple species. This study demonstrates how differences in behavioural traits among species—in this case microclimate preferences—that may have been previously adaptive can be deleterious after the introduction of a new pathogen. Management to reduce pathogen loads rather than exposure may be an effective way of reducing disease impact and preventing species extinctions. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

Disease has caused striking declines in wildlife and threatens numerous species with extinction. Theory suggests that the ecology and density-dependence of transmission dynamics can determine the probability of disease-caused extinction, but few empirical studies have simultaneously examined multiple factors influencing disease impact. We show, in hibernating bats infected with Geomyces destructans, that impacts of disease on solitary species were lower in smaller populations, whereas in socially gregarious species declines were equally severe in populations spanning four orders of magnitude. However, as these gregarious species declined, we observed decreases in social group size that reduced the likelihood of extinction. In addition, disease impacts in these species increased with humidity and temperature such that the coldest and driest roosts provided initial refuge from disease. These results expand our theoretical framework and provide an empirical basis for determining which host species are likely to be driven extinct while management action is still possible.

Seasonal patterns in pathogen transmission can influence the impact of disease on populations and the speed of spatial spread. Increases in host contact rates or births drive seasonal epidemics in some systems, but other factors may occasionally override these influences. White-nose syndrome, caused by the emerging fungal pathogen Pseudogymnoascus destructans , is spreading across North America and threatens several bat species with extinction. We examined patterns and drivers of seasonal transmission of P. destructans by measuring infection prevalence and pathogen loads in six bat species at 30 sites across the eastern United States. Bats became transiently infected in autumn, and transmission spiked in early winter when bats began hibernating. Nearly all bats in six species became infected by late winter when infection intensity peaked. In summer, despite high contact rates and a birth pulse, most bats cleared infections and prevalence dropped to zero. These data suggest the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation. Our study is the first, to the best of our knowledge, to describe the seasonality of transmission in this emerging wildlife disease. The timing of infection and fungal growth resulted in maximal population impacts, but only moderate rates of spatial spread.