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  1. Abstract

    Pathogens with persistent environmental stages can have devastating effects on wildlife communities. White-nose syndrome (WNS), caused by the fungusPseudogymnoascus 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 detectP. destructansin environmental samples, we initiated this study to assess whetherP. destructanscan 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 twoP. destructanscontaminated hibernacula in Vermont where native bats had been excluded.Infection withP. destructanswas 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 toP. destructansis 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.

     
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  2. 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.

     
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  3. Abstract

    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 pathogenPseudogymnoascus destructans. Within‐site transmission ofP. destructansprimarily 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 spreadP.destructanswhen they are highly infectious, but have reduced mobility. In communities whereP. destructanswas 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.

     
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  4. Abstract

    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.

     
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  5. Summary

    White‐nose syndrome, a disease that is caused by the psychrophilic fungusPseudogymnoascus destructans, has threatened several North America bat species with extinction. Recent studies have shown that East Asian bats are infected withP. destructansbut show greatly reduced infections. While several factors have been found to contribute to these reduced infections, the role of specific microbes in limitingP. destructansgrowth remains unexplored. We isolated three bacterial strains with the ability to inhibitP. destructans, namely,Pseudomonas yamanorumGZD14026,Pseudomonas brenneriXRD11711 andPseudomonas fragiGZD14479, from bats in China.Pseudomonas yamanorum, with the highest inhibition score, was selected to extract antifungal active substance. Combining mass spectrometry (MS) and nuclear magnetic resonance (NMR) spectroscopy analyses, we identified the active compound inhibitingP. destructansas phenazine‐1‐carboxylic acid (PCA), and the minimal inhibitory concentration (MIC) was 50.12 μg ml−1. Whole genome sequencing also revealed the existence of PCA biosynthesis gene clusters. Gas chromatography‐mass spectrometry (GC‐MS) analysis identified volatile organic compounds. The results indicated that 10 ppm octanoic acid, 100 ppm 3‐tert‐butyl‐4‐hydroxyanisole (isoprenol) and 100 ppm 3‐methyl‐3‐buten‐1‐ol (BHA) inhibited the growth ofP. destructans. These results support that bacteria may play a role in limiting the growth ofP. destructanson bats.

     
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  6. Free, publicly-accessible full text available December 31, 2024
  7. Yang, Junyuan (Ed.)
    The ongoing COVID-19 pandemic has killed at least 1.1 million people in the United States and over 6.7 million globally. Accurately estimating the age-specific infection fatality rate (IFR) of SARS-CoV-2 for different populations is crucial for assessing and understanding the impact of COVID-19 and for appropriately allocating vaccines and treatments to at-risk groups. We estimated age-specific IFRs of wild-type SARS-CoV-2 using published seroprevalence, case, and death data from New York City (NYC) from March to May 2020, using a Bayesian framework that accounted for delays between key epidemiological events. IFRs increased 3-4-fold with every 20 years of age, from 0.06% in individuals between 18–45 years old to 4.7% in individuals over 75. We then compared IFRs in NYC to several city- and country-wide estimates including England, Switzerland (Geneva), Sweden (Stockholm), Belgium, Mexico, and Brazil, as well as a global estimate. IFRs in NYC were higher for individuals younger than 65 years old than most other populations, but similar for older individuals. IFRs for age groups less than 65 decreased with income and increased with income inequality measured using the Gini index. These results demonstrate that the age-specific fatality of COVID-19 differs among developed countries and raises questions about factors underlying these differences, including underlying health conditions and healthcare access. 
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    Free, publicly-accessible full text available May 17, 2024
  8. Ansari, Ali R. (Ed.)
    Null models provide a critical baseline for the evaluation of predictive disease models. Many studies consider only the grand mean null model (i.e. R 2 ) when evaluating the predictive ability of a model, which is insufficient to convey the predictive power of a model. We evaluated ten null models for human cases of West Nile virus (WNV), a zoonotic mosquito-borne disease introduced to the United States in 1999. The Negative Binomial, Historical (i.e. using previous cases to predict future cases) and Always Absent null models were the strongest overall, and the majority of null models significantly outperformed the grand mean. The length of the training timeseries increased the performance of most null models in US counties where WNV cases were frequent, but improvements were similar for most null models, so relative scores remained unchanged. We argue that a combination of null models is needed to evaluate the forecasting performance of predictive models for infectious diseases and the grand mean is the lowest bar. 
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    Free, publicly-accessible full text available May 5, 2024
  9. 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. 
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  10. 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. 
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