Ten-year projection of white-nose syndrome disease dynamics at the southern leading-edge of infection in North America

AbstractPredicting the emergence and spread of infectious diseases is critical for effective conservation of biodiversity. White-nose syndrome (WNS), an emerging infectious disease of bats, has resulted in high mortality in eastern North America. Because the fungal causative agent Pseudogymnoascus destructans is constrained by temperature and humidity, spread dynamics may vary greatly by geography. Environmental conditions in the southern part of the continent, where disease dynamics are typically studied, making it difficult to predict how the disease will manifest. Herein, we modeled the spread of WNS in Texas based on available cave densities and average dispersal distances of species occupying these sites, and projected these results out to 10 years. We parameterized a predictive model of WNS epidemiology and its effects on hibernatory bat populations with observed environmental data from bat hibernation sites in Texas. Our model suggests that bat populations in northern Texas will be more affected by WNS mortality than southern Texas. As such, we recommend prioritizing the preservation of large overwintering colonies of bats in north Texas through management actions. Our model further illustrates that infectious disease spread and infectious disease severity can become uncoupled over a gradient of environmental variation. Finally, our results highlight the importance of understanding host, pathogen and environmental conditions in various settings to elucidate what may happen across a breadth of environments.

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Ten-year projection of white-nose syndrome disease dynamics at the southern leading-edge of infection in North America

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.0719 ◽

2021 ◽

Vol 288 (1952) ◽

pp. 20210719

Author(s):

Melissa B. Meierhofer ◽

Thomas M. Lilley ◽

Lasse Ruokolainen ◽

Joseph S. Johnson ◽

Steven R. Parratt ◽

...

Keyword(s):

Infectious Disease ◽

North America ◽

Environmental Conditions ◽

Leading Edge ◽

Environmental Data ◽

Disease Spread ◽

Disease Dynamics ◽

Pseudogymnoascus Destructans ◽

White Nose Syndrome ◽

Management Actions

Predicting the emergence and spread of infectious diseases is critical for the effective conservation of biodiversity. White-nose syndrome (WNS), an emerging infectious disease of bats, has resulted in high mortality in eastern North America. Because the fungal causative agent Pseudogymnoascus destructans is constrained by temperature and humidity, spread dynamics may vary by geography. Environmental conditions in the southern part of the continent are different than the northeast, where disease dynamics are typically studied, making it difficult to predict how the disease will manifest. Herein, we modelled WNS pathogen spread in Texas based on cave densities and average dispersal distances of hosts, projecting these results out to 10 years. We parameterized a predictive model of WNS epidemiology and its effects on bat populations with observed cave environmental data. Our model suggests that bat populations in northern Texas will be more affected by WNS mortality than southern Texas. As such, we recommend prioritizing the preservation of large overwintering colonies of bats in north Texas through management actions. Our model illustrates that infectious disease spread and infectious disease severity can become uncoupled over a gradient of environmental variation and highlight the importance of understanding host, pathogen and environmental conditions across a breadth of environments.

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Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2861 ◽

2016 ◽

Vol 283 (1826) ◽

pp. 20152861 ◽

Cited By ~ 22

Author(s):

Joseph R. Hoyt ◽

Kate E. Langwig ◽

Keping Sun ◽

Guanjun Lu ◽

Katy L. Parise ◽

...

Keyword(s):

North America ◽

Infection Prevalence ◽

Disease Dynamics ◽

Pseudogymnoascus Destructans ◽

Endemic Region ◽

White Nose Syndrome ◽

Resistant Species ◽

Host Pathogen ◽

Lower Transmission ◽

Host Infection

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.

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Experimental Infection ofTadarida brasiliensiswithPseudogymnoascus destructans, the Fungus That Causes White-Nose Syndrome

mSphere ◽

10.1128/msphere.00250-18 ◽

2018 ◽

Vol 3 (4) ◽

Author(s):

Michelle L. Verant ◽

Carol U. Meteyer ◽

Benjamin Stading ◽

David S. Blehert

Keyword(s):

Animal Model ◽

Experimental Animal ◽

Experimental Infection ◽

Abundant Species ◽

Experimental Animal Model ◽

Pseudogymnoascus Destructans ◽

Tadarida Brasiliensis ◽

Content Type ◽

White Nose Syndrome ◽

Management Actions

ABSTRACTWhite-nose syndrome (WNS) is causing significant declines in populations of North American hibernating bats, and recent western and southern expansions of the disease have placed additional species at risk. Understanding differences in species susceptibility and identifying management actions to reduce mortality of bats from WNS are top research priorities. However, the use of wild-caught susceptible bats, such asMyotis lucifugus, as model species for WNS research is problematic and places additional pressure on remnant populations. We investigated the feasibility of usingTadarida brasiliensis, a highly abundant species of bat that tolerates captivity, as the basis for an experimental animal model for WNS. Using methods previously established to confirm the etiology of WNS inM. lucifugus, we experimentally infected 11T. brasiliensisbats withPseudogymnoascus destructansin the laboratory under conditions that induced hibernation. We detectedP. destructanson all 11 experimentally infected bats, 7 of which exhibited localized proliferation of hyphae within the epidermis, dermis, and subcutaneous tissue, similar to invasive cutaneous ascomycosis observed inM. lucifugusbats with WNS. However, the distribution of lesions across wing membranes ofT. brasiliensisbats was limited, and only one discrete “cupping erosion,” diagnostic for WNS, was identified. Thus, the rarity of lesions definitive for WNS suggests thatT. brasiliensisdoes not likely represent an appropriate model for studying the pathophysiology of this disease. Nonetheless, the results of this study prompt questions concerning the potential for free-ranging, migratoryT. brasiliensisbats to become infected withP. destructansand move the fungal pathogen between roost sites used by species susceptible to WNS.IMPORTANCEWhite-nose syndrome (WNS) is a fungal disease that is causing severe declines of bat populations in North America. Identifying ways to reduce the impacts of this disease is a priority but is inhibited by the lack of an experimental animal model that does not require the use of wild-caught bat species already impacted by WNS. We tested whetherTadarida brasiliensis, one of the most abundant species of bats in the Americas, could serve as a suitable animal model for WNS research. WhileT. brasiliensisbats were susceptible to experimental infection with the fungus under conditions that induced hibernation, the species exhibited limited pathology diagnostic for WNS. These results indicate thatT. brasiliensisis not likely a suitable experimental model for WNS research. However, the recovery of viable WNS-causing fungus from experimentally infected bats indicates a potential for this species to contribute to the spread of the pathogen where it coexists with other species of bats affected by WNS.

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Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland

Open Life Sciences ◽

10.2478/s11535-013-0280-z ◽

2014 ◽

Vol 9 (4) ◽

pp. 437-443 ◽

Cited By ~ 1

Author(s):

Konrad Sachanowicz ◽

Arkadiusz Stępień ◽

Mateusz Ciechanowski

Keyword(s):

North America ◽

Mass Mortality ◽

Parasitic Fungus ◽

Pseudogymnoascus Destructans ◽

Southern Poland ◽

White Nose Syndrome ◽

Two Samples ◽

Myotis Myotis ◽

Myotis Daubentonii ◽

Fungal Dna

AbstractPseudogymnoascus destructans (Pd), a parasitic fungus (being responsible for a disease known as white-nose syndrome, WNS) that caused mass mortality of cave-dwelling, hibernating bats in North America, appears to be native of Europe, where it also occurs on wintering bats, but no similar outbreaks of WNS have been recorded. Herein, we provide the first account on prevalence and phenology of P. destructans in Poland. Bats were counted once per month, from October or January to May (2010-2013), in an abandoned ore mine in southern Poland. Presence of P. destructans in two samples was confirmed by sequencing of isolated fungal DNA. Observations of phenotypically identical mycosis on bats hibernating at this site in March 2006 are likely to be the first known records of P. destructans from Poland. All Pd-suspected individuals were Myotis myotis with an exception of one Myotis daubentonii. The first Pd-suspected bats were noted in mid-February, but their number was the highest in March, what overlapped with maximum numbers of hibernating M. myotis. The prevalence in March was 7%–27% of M. myotis individuals. No mass mortality of bats was observed in the mine, with only three dead individuals found in the hibernaculum which hosted up to 130 bats, representing 6–7 species.

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Phylogenetics of a Fungal Invasion: Origins and Widespread Dispersal of White-Nose Syndrome

mBio ◽

10.1128/mbio.01941-17 ◽

2017 ◽

Vol 8 (6) ◽

Cited By ~ 27

Author(s):

Kevin P. Drees ◽

Jeffrey M. Lorch ◽

Sebastien J. Puechmaille ◽

Katy L. Parise ◽

Gudrun Wibbelt ◽

...

Keyword(s):

Genetic Diversity ◽

North America ◽

North American ◽

Fungal Pathogen ◽

Phylogenetic Study ◽

Pseudogymnoascus Destructans ◽

Long Distance ◽

Recent Introduction ◽

White Nose Syndrome ◽

The North

ABSTRACT Globalization has facilitated the worldwide movement and introduction of pathogens, but epizoological reconstructions of these invasions are often hindered by limited sampling and insufficient genetic resolution among isolates. Pseudogymnoascus destructans , a fungal pathogen causing the epizootic of white-nose syndrome in North American bats, has exhibited few genetic polymorphisms in previous studies, presenting challenges for both epizoological tracking of the spread of this fungus and for determining its evolutionary history. We used single nucleotide polymorphisms (SNPs) from whole-genome sequencing and microsatellites to construct high-resolution phylogenies of P. destructans . Shallow genetic diversity and the lack of geographic structuring among North American isolates support a recent introduction followed by expansion via clonal reproduction across the epizootic zone. Moreover, the genetic relationships of isolates within North America suggest widespread mixing and long-distance movement of the fungus. Genetic diversity among isolates of P. destructans from Europe was substantially higher than in those from North America. However, genetic distance between the North American isolates and any given European isolate was similar to the distance between the individual European isolates. In contrast, the isolates we examined from Asia were highly divergent from both European and North American isolates. Although the definitive source for introduction of the North American population has not been conclusively identified, our data support the origin of the North American invasion by P. destructans from Europe rather than Asia. IMPORTANCE This phylogenetic study of the bat white-nose syndrome agent, P. destructans , uses genomics to elucidate evolutionary relationships among populations of the fungal pathogen to understand the epizoology of this biological invasion. We analyze hypervariable and abundant genetic characters (microsatellites and genomic SNPs, respectively) to reveal previously uncharacterized diversity among populations of the pathogen from North America and Eurasia. We present new evidence supporting recent introduction of the fungus to North America from a diverse Eurasian population, with limited increase in genetic variation in North America since that introduction.

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Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis ( Myotis lucifugus )

Royal Society Open Science ◽

10.1098/rsos.140470 ◽

2015 ◽

Vol 2 (2) ◽

pp. 140470 ◽

Cited By ~ 19

Author(s):

Laura E. Grieneisen ◽

Sarah A. Brownlee-Bouboulis ◽

Joseph S. Johnson ◽

DeeAnn M. Reeder

Keyword(s):

Infectious Disease ◽

Myotis Lucifugus ◽

Eastern North America ◽

The Novel ◽

Pseudogymnoascus Destructans ◽

Term Survival ◽

White Nose Syndrome ◽

Myotis Myotis ◽

The Impact

White-nose syndrome (WNS), an emerging infectious disease caused by the novel fungus Pseudogymnoascus destructans , has devastated North American bat populations since its discovery in 2006. The little brown myotis, Myotis lucifugus , has been especially affected. The goal of this 2-year captive study was to determine the impact of hibernacula temperature and sex on WNS survivorship in little brown myotis that displayed visible fungal infection when collected from affected hibernacula. In study 1, we found that WNS-affected male bats had increased survival over females and that bats housed at a colder temperature survived longer than those housed at warmer temperatures. In study 2, we found that WNS-affected bats housed at a colder temperature fared worse than unaffected bats. Our results demonstrate that WNS mortality varies among individuals, and that colder hibernacula are more favourable for survival. They also suggest that female bats may be more negatively affected by WNS than male bats, which has important implications for the long-term survival of the little brown myotis in eastern North America.

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Fungus Causing White-Nose Syndrome in Bats Accumulates Genetic Variability in North America with No Sign of Recombination

mSphere ◽

10.1128/mspheredirect.00271-17 ◽

2017 ◽

Vol 2 (4) ◽

Cited By ~ 17

Author(s):

Jigar Trivedi ◽

Josianne Lachapelle ◽

Karen J. Vanderwolf ◽

Vikram Misra ◽

Craig K. R. Willis ◽

...

Keyword(s):

North America ◽

North American ◽

Disease Ecology ◽

Spontaneous Mutation ◽

North American Population ◽

Pseudogymnoascus Destructans ◽

Clonal Population ◽

White Nose Syndrome ◽

The North ◽

Single Clone

ABSTRACT Emerging fungal diseases of wildlife are on the rise worldwide, and the white-nose syndrome (WNS) epidemic in North American bats is a catastrophic example. The causal agent of WNS is a single clone of the fungus Pseudogymnoascus destructans. Early evolutionary change in this clonal population has major implications for disease ecology and conservation. Accumulation of variation in the fungus through mutation, and shuffling of variation through recombination, could affect the virulence and transmissibility of the fungus and the durability of what appears to be resistance arising in some bat populations. Our genome-wide analysis shows that the clonal population of P. destructans has expanded in size from a single genotype, has begun to accumulate variation through mutation, and presents no evidence as yet of genetic exchange among individuals. IMPORTANCE Since its discovery in 2006, the emerging infectious disease known as white-nose syndrome has killed millions of bats in North America, making it one of the most devastating wildlife epidemics in recorded history. We demonstrate that there has been as yet only spontaneous mutation across the North American population of P. destructans, and we find no indication of recombination. Thus, selective forces, which might otherwise impact pathogenic virulence, have so far had essentially no genetic variation on which to act. Our study confirmed the time of origin for the first and, thus far, only introduction of P. destructans to North America. This system provides an unprecedented opportunity to follow the evolution of a host-pathogen interaction unfolding in real time.

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Caver Knowledge and Biosecurity Attitudes Towards White-Nose Syndrome and Implications for Global Spread

EcoHealth ◽

10.1007/s10393-020-01510-y ◽

2021 ◽

Author(s):

S. Salleh ◽

K. Cox-Witton ◽

Y. Salleh ◽

Jasmin Hufschmid

Keyword(s):

Risk Assessment ◽

North America ◽

Pseudogymnoascus Destructans ◽

White Nose Syndrome ◽

Qualitative Survey ◽

The World ◽

Global Spread ◽

Willingness To Help ◽

Sydney Australia

AbstractWhite-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused catastrophic declines of bat populations in North America. Risk assessment indicates that cavers could pose a risk for the spread of the fungus, however, information on cavers’ knowledge of WNS and their caving and biosecurity habits is lacking. An anonymous qualitative survey was completed by delegates (n = 134) from 23 countries at an international speleological conference in Sydney, Australia. Cavers indicated that they visit caves frequently (80.6% at least bimonthly), including outside of their own country, but 20.3% of respondents did not know about WNS prior to the conference. Some respondents were incorrect, or unsure, about whether they had visited caves in countries where P. destructans occurs (26.5%) or whether their own country was free of the fungus (7.8%). Although 65.9% of respondents were aware of current decontamination protocols, only 23.9% and 31.2% (when in Australian or overseas caves, respectively) fully adhered to them. Overall, cavers showed strong willingness to help prevent further spread of this disease, but further efforts at education and targeted biosecurity activities may be urgently needed to prevent the spread of P. destructans to Australia and to other unaffected regions of the world.

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Temporal Changes in Body Mass and Body Condition of Cave-Hibernating Bats During Staging and Swarming

Journal of Fish and Wildlife Management ◽

10.3996/042015-jfwm-033 ◽

2015 ◽

Vol 6 (2) ◽

pp. 360-370 ◽

Cited By ~ 6

Author(s):

Michael J. Lacki ◽

Luke E. Dodd ◽

Rickard S. Toomey ◽

Steven C. Thomas ◽

Zachary L. Couch ◽

...

Keyword(s):

Body Mass Index ◽

Body Mass ◽

Body Condition ◽

Leading Edge ◽

Myotis Lucifugus ◽

Pseudogymnoascus Destructans ◽

White Nose Syndrome ◽

Close Proximity ◽

Fungal Distribution ◽

Little Brown Bats

Abstract The rapid colonization of the Pseudogymnoascus destructans fungus across cave systems in eastern North America and the associated bat mortalities (white-nose syndrome; WNS), necessitates studies of cave-hibernating bats that remain unaffected by, or in close proximity to, the leading edge of the fungal distribution to provide baseline predisturbance data from which to assess changes due to fungal effects. Studies of the physiological ecology of cave-hibernating bats during the spring staging and autumn swarming seasons are few, and an understanding of patterns in body condition of bats associated with entry into and emergence from hibernation is incomplete. We sampled bats at the entrance to a cave in Mammoth Cave National Park, Kentucky, during swarming and staging, prior to (2011 and 2012), concurrent with (2013), and following (2014) the arrival of the WNS fungus. We evaluated seasonal and annual changes in body mass and body condition of bats entering and leaving the cave. We captured 1,232 bats of eight species. Sex ratios of all species were male-biased. Capture success was substantially reduced in 2014, following the second winter after arrival of the WNS fungus. Significant temporal variation in body mass and body mass index was observed for little brown bats Myotis lucifugus, northern long-eared bats M. septentrionalis, and tri-colored bats Perimyotis subflavus, but not Indiana bats M. sodalis. Little brown bats and northern long-eared bats demonstrated significant increases in mean body mass index in 2014; this pattern likely reflected a relatively better body condition in bats that survived exposure to the WNS fungus. Most species demonstrated highest body mass and body mass index values in late swarming compared with other sampling periods, with tri-colored bats showing the greatest percent increase in body mass (42.5%) and body mass index (42.9%) prior to entering hibernation. These data indicate significant intraspecific variation in body condition of cave-hibernating bat species, both among years and between the seasons of autumn swarming and spring staging. We suggest this variation is likely to have implications for the relative vulnerability of species to WNS infection across the distribution of the Pseudogymnoascus fungus.

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White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America

Scientific Reports ◽

10.1038/srep19829 ◽

2016 ◽

Vol 6 (1) ◽

Cited By ~ 57

Author(s):

Jan Zukal ◽

Hana Bandouchova ◽

Jiri Brichta ◽

Adela Cmokova ◽

Kamil S. Jaron ◽

...

Keyword(s):

North America ◽

Fungal Infection ◽

Source Region ◽

West Siberian Plain ◽

Pseudogymnoascus Destructans ◽

The West ◽

Host Pathogen Interaction ◽

White Nose Syndrome ◽

Fungal Load ◽

The Difference

Abstract A striking feature of white-nose syndrome, a fungal infection of hibernating bats, is the difference in infection outcome between North America and Europe. Here we show high WNS prevalence both in Europe and on the West Siberian Plain in Asia. Palearctic bat communities tolerate similar fungal loads of Pseudogymnoascus destructans infection as their Nearctic counterparts and histopathology indicates equal focal skin tissue invasiveness pathognomonic for WNS lesions. Fungal load positively correlates with disease intensity and it reaches highest values at intermediate latitudes. Prevalence and fungal load dynamics in Palearctic bats remained persistent and high between 2012 and 2014. Dominant haplotypes of five genes are widespread in North America, Europe and Asia, expanding the source region of white-nose syndrome to non-European hibernacula. Our data provides evidence for both endemicity and tolerance to this persistent virulent fungus in the Palearctic, suggesting that host-pathogen interaction equilibrium has been established.

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