White-nose syndrome (WNS) is an emerging disease affecting hibernating bats in eastern North America that causes mass mortality and precipitous population declines in winter hibernacula. First discovered in 2006 in New York State, WNS is spreading rapidly across eastern North America and currently affects seven species. Mortality associated with WNS is causing a regional population collapse and is predicted to lead to regional extinction of the little brown myotis (Myotis lucifugus), previously one of the most common bat species in North America. Novel diseases can have serious impacts on naïve wildlife populations, which in turn can have substantial impacts on ecosystem integrity.

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.

AimWe investigated the effects of disease on the local abundances and distributions of species at continental scales by examining the impacts of white-nose syndrome, an infectious disease of hibernating bats, which has recently emerged in North America.

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.

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.

White-nose syndrome (WNS) is a fungal disease in bats and one of the most devastating infectious disease outbreaks in wild mammals to emerge over the past century 1-15. WNS was first detected in 2007 by biologists who discovered an abnormal mortality event at a cave in Albany County, New York (NY), USA, while conducting routine bat population monitoring surveys 16. Bats that were still alive were covered in a white fungus, which was most noticeable on their muzzles, ears and wings, thus leading to the disease being named WNS 17,18. Following this discovery, inspection of nearby hibernation sites (hibernacula) led to similar findings and further examination of photos collected from previous winter surveys revealed that bats at another nearby site had visible signs of infection with the fungus in the winter of 2005-2006. Thus, the earliest evidence of this disease in North America is on 16 February 2006 in Howes Cave, NY 17. Histological examination of dead and dying bats later identified the likely causative agent as Geomyces destructans 19 , a novel fungus that was unknown to science before its discovery in North America 17. Based on DNA sequence data from other Geomyces spp. and related fungi, G. destructans was reclassified as Pseudogymnoascus destructans 16,17,20 in 2013. P. destructans is a multi-host psychrophilic ascomycete 20 in the order Onygenales, which contains many other pathogenic and environmentally resilient fungi. Molecular evidence suggests that P. destructans has evolved with Eurasian bat communities, with which it has coexisted for millenia 21,22 , to become a specialist pathogen that relies primarily on living bat tissue for growth and replication 22-24. The investment in parasitic traits has led to physiological and ecological trade-offs 22-26 , which make P. destructans both reliant on but also well adapted to infecting the epidermal tissue of hibernating bats during the winter 26,27. While bat communities across Eurasia experience greatly reduced WNS disease severity with no evidence of mass mortality 28,29 , naive host communities in North America experienced unprecedented population declines 1-15 on first exposure to this virulent pathogen 26,27. Routine monitoring and retrospective photo documentation of bat populations enabled biologists to estimate the timing of P. destructans' introduction to North America with some certainty, making this disease emergence unique among other wildlife diseases. Early detection enabled the spread of P. destructans across North America to be tracked and the impacts of the pathogen on hosts to be accurately assessed. Building on this information, the first decade of WNS research has led to considerable advances in the understanding of the closely tied interactions between P. destructans and its hosts compared with other emerging wildlife diseases over similar timescales 30,31. In this Review, we describe the origins, distribution, seasonal life history, pathogenesis, and the impacts and persistence of bats with P. destructans across the globe. Finally, we...

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’.