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.
Disease can play an important role in structuring species communities because the effects of disease vary among hosts; some species are driven toward 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 in bats, has decimated some species while sympatric and closely related species have experienced little effect. We analyzed 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. In contrast, fungal loads varied over three 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 more higher fungal loads and higher 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 behavioral 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.
1. 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. 2. 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. 3. 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. 4. 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 m
Predicting species' fates following the introduction of a novel pathogen is a significant and growing problem in conservation. Comparing disease dynamics between introduced and endemic regions can offer insight into which naive hosts will persist or go extinct, with disease acting as a filter on host communities. We examined four hypothesized mechanisms for host–pathogen persistence by comparing host infection patterns and environmental reservoirs for Pseudogymnoascus destructans (the causative agent of white-nose syndrome) in Asia, an endemic region, and North America, where the pathogen has recently invaded. Although colony sizes of bats and hibernacula temperatures were very similar, both infection prevalence and fungal loads were much lower on bats and in the environment in Asia than North America. These results indicate that transmission intensity and pathogen growth are lower in Asia, likely due to higher host resistance to pathogen growth in this endemic region, and not due to host tolerance, lower transmission due to smaller populations, or lower environmentally driven pathogen growth rate. Disease filtering also appears to be favouring initially resistant species in North America. More broadly, determining the mechanisms allowing species persistence in endemic regions can help identify species at greater risk of extinction in introduced regions, and determine the consequences for disease dynamics and host–pathogen coevolution.
1. 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. 2. We illustrate how Integral Projection Models (IPMs) provide a novel modelling 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. 3. 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 modelling the temperature-dependent epizootic dynamics of amphibian chytrid fungus in Mountain yellow-legged frogs (Rana muscosa). 4. The host–parasite IPM can be applied to other diseases such as facial tumour 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 modelling wildlife disease.
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. destructansgrowth 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.
K. E. Langwig, J. Voyles, M. Q. Wilber, W. F. Frick, K. Murray, B.M. Bolker, J.P. Collins, J. R. Hoyt, W. Willis, C, T. L. Cheng, M. Fisher, D. Lindner, H. I. McCallum, R. Puschendorf, E.B. Rosenblum, M. Toothman, C. J. Briggs, and A. M. Kilpatrick. 2015. “Context dependent conservation responses to wildlife disease.” Frontiers in Ecology and the Environment.Abstract
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.
W. F. Frick, S. J. Puechmaille, J. R. Hoyt, B. A. Nickel, K. E. Langwig, J. T. Foster, K. E. Barlow, T. Bartonička, D. Feller, A. Haarsma, C. Herzog, I. Horacek, J. van der Kooij, B. Mulkens, B. Petrov, R. Reynolds, L. Rodrigues, C. W. Stihler, G. G. Turner, and A. M. Kilpatrick. 2015. “Disease alters macroecological patterns of North American bats.” Global Ecology and Biogeography, 24, Pp. 741-749.Abstract
We 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.
North America and Europe.
We used four decades of population counts from 1108 populations to compare the local abundances of bats in North America before and after the emergence of white-nose syndrome to the situation in Europe, where the disease is endemic. We also examined the probability of local extinction for six species of hibernating bats in eastern North America and assessed the influence of winter colony size prior to the emergence of white-nose syndrome on the risk of local extinction.
White-nose syndrome has caused a 10-fold decrease in the abundance of bats at hibernacula in North America, eliminating large differences in species abundance patterns that existed between Europe and North America prior to disease emergence. White-nose syndrome has also caused extensive local extinctions (up to 69% of sites in a single species). For five out of six species, the risk of local extinction was lower in larger winter populations, as expected from theory, but for the most affected species, the northern long-eared bat (Myotis septentrionalis), extinction risk was constant across winter colony sizes, demonstrating that disease can sometimes eliminate numerical rarity as the dominant driver of extinction risk by driving both small and large populations extinct.
Species interactions, including disease, play an underappreciated role in macroecological patterns and influence broad patterns of species abundance, occurrence and extinction.
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.
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.
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 5°C 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.
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 threats EIDs pose to wildlife (Sleeman 2013). While it is true that developing new analytical models, diagnostic assays and molecular tools will significantly avance outr abilities to respond to disease threats, we also propose that addressing difficult problems in EIDs will require considerable shofts in international health policy and infrastructure. While there are currently international organizations responsbile for rapidly initiating and coordinating preventative measures to control infectious diseases in human, livestock, and arable systems, there are few comparable instiutions that have the authority to implement transnational responses to EIDs in wildlife. This absence of well-developed infastructure hampers the rapid responses necessary to mitigate international spread of EIDs.
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.
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.
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.