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Anthropogenically driven environmental change has imposed substantial threats on biodiversity, including the emergence of infectious diseases that have resulted in declines of wildlife globally. In response to pathogen invasion, maintaining diversity within host populations across heterogenous environments is essential to facilitating species persistence. White-nose syndrome is an emerging fungal pathogen that has caused mass mortalities of hibernating bats across North America. However, in the northeast, peripheral island populations of the endangered northern myotis (Myotis septentrionalis) appear to be persisting despite infection while mainland populations in the core of the species range have experienced sharp declines. Thus, this study investigated host and environmental factors that may contribute to divergent population responses. We compared patterns of pathogen exposure and infection intensity between populations and documented the environmental conditions and host activity patterns that may promote survival despite disease invasion. For island populations, we found lower prevalence and less severe infections, possibly due to a shorter hibernation duration compared to the mainland, which may reduce the time for disease progression. The coastal region of the northern myotis range may serve as habitat refugia that enables this species to persist despite pathogen exposure; however, conservation efforts could be critical to supporting species survival in the long term. 

Plasmodium parasites infect thousands of species and provide an exceptional system for studying host- pathogen dynamics, especially for multi-host pathogens. However, understanding these interactions requires an accurate assay of infection. Assessing Plasmodium infections using microscopy on blood smears often misses infections with low parasitemias (the fractions of cells infected), and biases in malaria prevalence estimates will differ among hosts that differ in mean parasitemias. We examined Plasmodium relictum infection and parasitemia using both microscopy of blood smears and quantitative polymerase chain reaction (qPCR) on 299 samples from multiple bird species in Hawai’i and fit models to predict parasitemias from qPCR cycle threshold (Ct) values. We used these models to quantify the extent to which microscopy underestimated infection prevalence and to more accurately estimate infection pat- terns for each species for a large historical study done by microscopy. We found that most qPCR-positive wild-caught birds in Hawaii had low parasitemias (Ct scores 35), which were rarely detected by microscopy. The fraction of infections missed by microscopy differed substantially among eight species due to differences in species’ parasitemia levels. Infection prevalence was likely 4–5-fold higher than previous microscopy estimates for three introduced species, including Zosterops japonicus, Hawaii’s most abundant forest bird, which had low average parasitemias. In contrast, prevalence was likely only 1.5–2.3-fold higher than previous estimates for Himatione sanguinea and Chlorodrepanis virens, two native species with high average parasitemias. Our results indicate that relative patterns of infection among species differ substantially from those observed in previous microscopy studies, and that differences depend on variation in parasitemias among species. Although microscopy of blood smears is useful for estimating the frequency of different Plasmodium stages and host attributes, more sensitive quantitative methods, including qPCR, are needed to accurately estimate and compare infection prevalence among host species. 

ABSTRACT 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 internal transcribed spacer amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructanswas 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 white-nose syndrome inM. lucifugusbut 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 ofMyotis lucifugusandPerimyotis subflavusindicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd. 

Abstract Environmental pathogen reservoirs exist for many globally important diseases and can fuel epidemics, influence pathogen evolution, and increase the threat of host extinction. Species composition can be an important factor that shapes reservoir dynamics and ultimately determines the outcome of a disease outbreak. However, disease‐induced mortality can change species communities, indicating that species responsible for environmental reservoir maintenance may change over time. Here we examine the reservoir dynamics ofPseudogymnoascus destructans, the fungal pathogen that causes white‐nose syndrome in bats. We quantified changes in pathogen shedding, infection prevalence and intensity, host abundance, and the subsequent propagule pressure imposed by each species over time. We find that highly shedding species are important during pathogen invasion, but contribute less over time to environmental contamination as they also suffer the greatest declines. Less infected species remain more abundant, resulting in equivalent or higher propagule pressure. More broadly, we demonstrate that high infection intensity and subsequent mortality during disease progression can reduce the contributions of high‐shedding species to long‐term pathogen maintenance. 

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. 

Abstract Disease results from interactions among the host, pathogen, and environment. Inoculation trials can quantify interactions among these players and explain aspects of disease ecology to inform management in variable and dynamic natural environments. White-nose Syndrome, a disease caused by the fungal pathogen, Pseudogymnoascus destructans ( Pd ), has caused severe population declines of several bat species in North America. We conducted the first experimental infection trial on the tri-colored bat, Perimyotis subflavus , to test the effect of temperature and humidity on disease severity. We also tested the effects of temperature and humidity on fungal growth and persistence on substrates. Unexpectedly, only 37% (35/95) of bats experimentally inoculated with Pd at the start of the experiment showed any infection response or disease symptoms after 83 days of captive hibernation. There was no evidence that temperature or humidity influenced infection response. Temperature had a strong effect on fungal growth on media plates, but the influence of humidity was more variable and uncertain. Designing laboratory studies to maximize research outcomes would be beneficial given the high costs of such efforts and potential for unexpected outcomes. Understanding the influence of microclimates on host–pathogen interactions remains an important consideration for managing wildlife diseases, particularly in variable environments. 

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 behaviour. 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. 

Abstract The age of an animal, determined by time (chronological age) as well as genetic and environmental factors (biological age), influences the likelihood of mortality and reproduction and thus the animal’s contribution to population growth. For many long-lived species, such as bats, a lack of external and morphological indicators has made determining age a challenge, leading researchers to examine genetic markers of age for application to demographic studies. One widely studied biomarker of age is telomere length, which has been related both to chronological and biological age across taxa, but only recently has begun to be studied in bats. We assessed telomere length from the DNA of known-age and minimum known-age individuals of two bat species using a quantitative PCR assay. We determined that telomere length was quadratically related to chronological age in big brown bats (Eptesicus fuscus), although it had little predictive power for accurate age determination of unknown-age individuals. The relationship was different in little brown bats (Myotis lucifugus), where telomere length instead was correlated with biological age, apparently due to infection and wing damage associated with white-nose syndrome. Furthermore, we showed that wing biopsies currently are a better tissue source for studying telomere length in bats than guano and buccal swabs; the results from the latter group were more variable and potentially influenced by storage time. Refinement of collection and assessment methods for different non-lethally collected tissues will be important for longitudinal sampling to better understand telomere dynamics in these long-lived species. Although further work is needed to develop a biomarker capable of determining chronological age in bats, our results suggest that biological age, as reflected in telomere length, may be influenced by extrinsic stressors such as disease. 

Abstract Emerging infectious diseases have caused population declines and biodiversity loss. The ability of pathogens to survive in the environment, independent of their host, can exacerbate disease impacts and increase the likelihood of species extinction. Control of pathogens with environmental stages remains a significant challenge for conservation and effective management strategies are urgently needed.We examined the effectiveness of managing environmental exposure to reduce the impacts of an emerging infectious disease of bats, white‐nose syndrome (WNS). We used a chemical disinfectant, chlorine dioxide (ClO₂), to experimentally reducePseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We combined laboratory experiments with 3 years of field trials at four abandoned mines to determine whether ClO₂could effectively removeP. destructansfrom the environment, reduce host infection and limit population impacts.ClO₂was effective at killingP. destructansin vitro across multiple concentrations. In field settings, higher concentrations of ClO₂treatment were needed to sufficiently reduce viableP. destructansconidia in the environment.The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was also higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus).Synthesis and applications. Our results highlight that targeted management of sources for environmental transmission can be an effective control strategy for wildlife disease. We found that successfully reducing pathogen in the environment decreased disease severity and increased survival, but required higher treatment exposure than was effective in laboratory experiments, and the effects varied among species. More broadly, our findings have implications for other emerging wildlife diseases with free‐living pathogen stages by highlighting how the degree of environmental contamination can have cascading impacts on hosts, presenting an opportunity for intervention.