Kate E. Langwig

An emerging disease causes regional population collapse of a common North American bat species.

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. Like the passenger pigeon, millions of little brown bats face the possibility of rapid extinction, this time from disease. 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.

Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome.

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.

Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome

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.

Context-dependent conservation responses to emerging wildlife diseases

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.

Bacteria Isolated from Bats Inhibit the Growth of Pseudogymnoascus destructans, the Causative Agent of White-Nose Syndrome

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 non-inhibitory 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.

Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies

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.

Little Brown Myotis Persist Despite Exposure to White-Nose Syndrome

Abstract 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 synd...

Invasion dynamics of white-nose syndrome fungus, midwestern United States, 2012–2014

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.

Moving Beyond Too Little, Too Late: Managing Emerging Infectious Diseases in Wild Populations Requires International Policy and Partnerships

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.

Resistance in persisting bat populations after white-nose syndrome invasion

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’.