Infection with Pseudogymnoascus destructans in bats (white-nose syndrome)
- Host Animals
- Hosts/Species Affected
- Distribution Table
- List of Symptoms/Signs
- Disease Course
- Impact: Economic
- Impact: Environmental
- Impact: Social
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Infection with Pseudogymnoascus destructans in bats
Preferred Common Name
- white-nose syndrome
International Common Names
- English: bat white-nose syndrome; Geomyces destructans infection; Pseudogymnoascus destructans infection
OverviewTop of page
White-nose syndrome (WNS) is an emerging disease of North American bats that has caused unprecedented population declines. It is caused by the psychrophilic (cold-loving) fungus Pseudogymnoascus destructans, which is believed to have been introduced to North America from Europe or Asia (where it is present but does not cause significant mortality), although the full extent of its native range is unknown. The route of introduction is also unknown. In North America, hibernating bats become infected with P. destructans when body temperature decreases during winter torpor into the range permissive for growth of this fungus. Infected bats may develop visible fungal growth on the nose or wings, awaken more frequently from torpor, and experience a cascade of physiologic changes that result in weight loss, dehydration, electrolyte imbalances, and death. P. destructans persists in the environments of underground bat hibernation sites (hibernacula) and is believed to spread primarily by natural movements of infected bats. The first evidence of WNS in North America is from a photograph of a hibernating bat taken during winter of 2005-2006 in a hibernaculum near Albany, New York. P. destructans subsequently spread rapidly from the northeastern United States throughout much of the eastern portions of the United States and Canada, and most recently (as of May 2017) was detected in Washington State. It has killed millions of bats, threatening some species with regional extirpation and putting at risk the valuable environmental services that bats provide by eating harmful insects.
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Barbastella barbastellus||Wild host|
|Eptesicus fuscus||Wild host|
|Eptesicus nilssonii||Wild host|
|Miniopterus schreibersii||Wild host|
|Myotis austroriparius||Wild host|
|Myotis bechsteinii||Wild host|
|Myotis brandtii||Wild host|
|Myotis dasycneme||Wild host|
|Myotis daubentonii||Wild host|
|Myotis emarginatus||Wild host|
|Myotis grisescens||Wild host|
|Myotis leibii||Wild host|
|Myotis lucifugus||Wild host|
|Myotis myotis||Wild host|
|Myotis nattereri||Wild host|
|Myotis petax||Wild host|
|Myotis septentrionalis||Wild host|
|Myotis sodalis||Wild host|
|Myotis velifer||Wild host|
|Myotis volans||Wild host|
|Myotis yumanensis||Wild host|
|Perimyotis subflavus||Wild host|
|Plecotus auritus||Wild host|
|Rhinolophus euryale||Wild host|
|Rhinolophus hipposideros||Wild host|
Hosts/Species AffectedTop of page
White-nose syndrome (WNS) has been diagnosed in a diversity of bat species from North America, Europe, and Asia (Blehert et al., 2009; Turner et al., 2011; Pikula et al., 2012; Zukal et al., 2014; Hoyt et al., 2016; Zukal et al., 2016). In addition, P. destructans has been detected on a number of other bat species from these areas without documented signs of WNS (Martinkova et al., 2010; Wibbelt et al., 2010; Bernard et al., 2015; Hoyt et al., 2016). It is not known at this time why some North American species of bats experience more severe disease or higher mortality from WNS than others, nor what resistance mechanisms result in less severe disease in some species, although certain host traits and hibernation conditions are hypothesized to play a role (Flory et al., 2012; Hayman et al., 2016).
The Host Animals table lists species that, as of August 2018, were confirmed to demonstrate diagnostic evidence of white-nose syndrome associated with P. destructans infection. The fungus has been detected on a number of other bat species without histopathologic evidence of clinical disease; these species are not included in the table. An updated list of all bats that are either affected by white-nose syndrome or potentially carry the fungus is maintained at: https://www.whitenosesyndrome.org/about/bats-affected-wns.
Isolates of P. destructans from both North America and Europe have similar virulence in the North American little brown bat (Myotis lucifugus) (Warnecke et al., 2012). However, while skin infection with P. destructans has been detected in a number of European bat species, mass mortality attributable to infection has not been observed (Wibbelt et al., 2010; Puechmaille et al., 2011a; Puechmaille et al., 2011b; Pikula et al., 2012; Zukal et al., 2014).
DistributionTop of page
Pseudogymnoascus destructans has been detected on bats or in environments utilized by bats for hibernation in North America (United States and Canada), at least 18 European countries, and China. The native range of the fungus is unknown but is minimally presumed to include parts of Europe, where there is evidence of genetic diversification (Leopardi et al., 2015). The route of introduction to North America has not been determined. The disease has now been reported from 5 provinces in eastern Canada and 31 US states, mostly in the centre and east of the country; the fungus, but no clinical disease, has been found in a further two states. An interactive map of the spread and distribution of WNS in North America is available at: https://www.sciencebase.gov/gisviewer/wns/; the latest map of distribution, along with earlier versions, can be seen at https://www.whitenosesyndrome.org/resources/map.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
PathologyTop of page
Gross signs of infection by Pseudogymnoascus destructans can include white, powdery growth of fungal hyphae and conidia on the muzzle and a white, tacky, opaque film on the wings. However, visible fungal growth is not always seen (Meteyer et al., 2009). Changes to the skin of affected bats can be variable, including: patches of rough skin on the face, ears, forearms, wing membrane, and feet; pinpoint white foci that resemble comedones on the muzzle; loss of sheen on glabrous skin; and irregular pigmentation with areas of contraction or tears in the wing membrane (Meteyer et al., 2009). Bats may be in poor body condition with inadequate fat stores but do not demonstrate evidence of major organ failure or other consistent non-cutaneous pathologies (Courtin et al., 2010).
Direct cutaneous penetration and proliferation by hyphae of P. destructans causes characteristic epidermal erosions and ulcers (Meteyer et al., 2009). Unlike most transmissible dermatophytes, P. destructans invades the underlying connective tissue (Meteyer et al., 2009; Reichard and Kunz, 2009; Cryan et al., 2010). Cup-like epidermal erosions filled with fungal hyphae, or ulceration and fungal invasion of underlying connective tissue, are often observed on histopathology (Meteyer et al., 2009). Fungal hyphae in tissue sections are branching and septate with curved conidia on short aerial hyphae, although the latter structures are not always observed (Meteyer et al., 2009).
A notable observation on histopathology is the absence of inflammation in skin from hibernating bats, even when there is evidence for extensive invasion by P. destructans (Meteyer et al., 2009). Analysis of gene expression during infection reveals that infected hibernating bats initiate a partial immune response to fungal invasion, including activation of acute inflammation and wound healing pathways, but recruitment of white blood cells to affected sites for clearing infection is inadequate during torpor (Rapin et al., 2014; Field et al., 2015). Paradoxically, damage to the wing membranes is most notable in bats examined just after spring emergence from hibernation, which may be attributable to immune-mediated damage to invaded tissues on return to euthermia (Meteyer et al., 2012).
DiagnosisTop of page
Pseudogymnoascus destructans can be detected in environmental substrates from bat hibernation environments even when bats are absent. The fungus can additionally be detected on bats in the absence of clinical signs of disease. Thus the case definition for white-nose syndrome (WNS) distinguishes between detection of the pathogen by culture or molecular methods and confirmation of WNS through a combination of pathogen detection and observation of histologic signs of skin infection (USGS National Wildlife Health Center, 2015). Detection of P. destructans in the absence of histopathologic support or other field observations can only confirm that the fungus is present in a population or location.
P. destructans can be grown from a variety of sample types (e.g., soil, skin biopsies, and skin swabs), by culture on Sabouraud dextrose agar at 7°C (Gargas et al., 2009; Lorch et al., 2013a), or by polymerase chain reaction (PCR) targeting the intergenic spacer region of the rRNA gene complex (Muller et al., 2013). Confirmation of skin infection with fungal invasion characteristic of clinical WNS requires microscopic examination of skin cross-sections (Meteyer et al., 2009). When screening for presence of P. destructans, PCR is preferred over culture due to greater sensitivity (USGS National Wildlife Health Center, 2015).
Field signs that a hibernating bat population may be affected by WNS include: excessive or unexplained mortality at or near a hibernaculum; visible fungal growth on the muzzle or wings of live or freshly dead bats; abnormal daytime activity or movement towards hibernaculum openings; and moderate to severe wing damage in non-torpid bats in thin body condition (although the latter two signs are both nonspecific when observed in isolation) (USGS National Wildlife Health Center, 2015). In the field, ultraviolet light can also be used to screen hibernating bats for potential infection. Long-wave ultraviolet light elicits a distinct orange-yellow fluorescence when the fungus has invaded skin tissues (Turner et al., 2014). Observation of this characteristic fluorescence can be a valuable screening tool for guiding sample collection for laboratory testing (Turner et al., 2014). Field observations compatible with WNS, or detection of P. destructans by culture or molecular methods, can be paired with observation of UV fluorescence to support a diagnosis of suspected WNS.
List of Symptoms/SignsTop of page
|General Signs / Dehydration||Other:All Stages||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Other:All Stages||Sign|
|General Signs / Weight loss||Other:All Stages||Sign|
|Nervous Signs / Abnormal behavior, aggression, changing habits||Other:All Stages||Sign|
|Nervous Signs / Excessive or decreased sleeping||Other:All Stages||Sign|
|Skin / Integumentary Signs / Scarred skin||Other:All Stages||Sign|
|Skin / Integumentary Signs / Skin crusts, scabs||Other:All Stages||Sign|
|Skin / Integumentary Signs / Skin ulcer, erosion, excoriation||Other:All Stages||Diagnosis|
Disease CourseTop of page
Pathogenesis of white-nose syndrome (WNS) has emerged as a unique, multi-stage model whereby a skin infection progresses to causing abnormal behaviors and systemic illness due to physiological changes experienced by infected bats during winter torpor. Infection leading to disease is limited to hibernating bats whose body temperature is low enough to allow fungal growth and invasion (Cryan et al., 2010; Verant et al., 2012). Infected bats may develop visible fungal growth around the nose or on the wings as the fungus invades cutaneous tissues (although this sign is not always observed). This visible white growth on hibernating bats tends to be noticeable after midwinter, but phenology of hyphal and conidiophore growth above skin surfaces is not well characterized. Infected bats may also demonstrate abnormal hibernation behaviors, such as more frequent arousal from torpor, moving among roosting sites or congregating near hibernaculum entrances, and flying by day outside of hibernation sites (Castle and Cryan, 2010; Cryan et al., 2010; Frick et al., 2010; Blehert, 2012; Reeder et al., 2012;). Subsequently, infected bats experience a cascade of physiological changes that result in weight loss, dehydration, and electrolyte imbalances, potentially culminating in death (Willis et al., 2011; Cryan et al., 2013a; Verant et al., 2014).
Bats can recover from WNS in a captive setting following removal from torpor and provision of supportive care. Rehabilitation of individual animals, however, is a labour intensive process that is not broadly applicable to management of free-ranging bat populations (Fuller et al., 2011; Meteyer et al., 2011). Upon emergence from hibernation in spring, infected bats can naturally recover from WNS without human intervention, but individuals with extensive infections are less likely to survive the healing process (Dobony et al., 2011; Fuller et al., 2011). Following arousal from hibernation, the immune system response against Pseudogymnoascus destructans, which is not observed in torpid animals, can be so vigorous as to fatally impair the host (Meteyer et al., 2012).
EpidemiologyTop of page
White-nose syndrome (WNS) is primarily observed during winter months when bat skin temperatures are conducive to growth of Pseudogymnoascus destructans (Blehert, 2012; Verant et al., 2012; Langwig et al., 2015a). Infected bats are hypothesized to be a primary mechanism for moving the fungus among hibernation sites (Lorch et al., 2011; Lorch et al., 2013b; Hoyt et al., 2015b). Prevalence of P. destructans in bat populations peaks during late winter, but the fungus can be detected on bats at lower prevalence through early spring emergence; pathogen prevalence declines during summer months (Langwig et al., 2015a). The fungus can also persist outside the host for extended periods in substrates from hibernation sites, meaning that once infested, hibernacula serve as persistent reservoirs of the pathogen (Lorch et al., 2013b; Reynolds et al., 2015).
P. destructans can also likely be transferred among locations by humans on clothing, footwear, or equipment (Sleeman, 2011; Shelley et al., 2013; Ballmann et al., 2017). Restricting movement of these items from areas affected by WNS to unaffected areas and attention to decontamination is strongly advised as a precautionary principle for persons who visit potential bat hibernation habitats (e.g. recreational cavers, biologists, or miners). Guidance for decontaminating and restricting movement of equipment used in bat hibernation sites has been developed to reduce risks of anthropogenic contributions to the spread of WNS: https://www.whitenosesyndrome.org/resources/cavers.
Impact: EconomicTop of page
Millions of North American bats have died from white-nose syndrome (WNS), resulting in dramatic regional bat population declines (Frick et al., 2010; Frick et al., 2015; Reynolds et al., 2016). Insectivorous bats provide valuable pest control services. For example, bats eat insects that damage crops and forests, and that carry diseases. In the USA alone, insectivorous bats are estimated to save farmers over $3 billion annually in pest suppression services (Boyles et al., 2011). Recent experiments indicate that bat suppression of insect pests in corn (maize) fields could scale globally to one billion dollars in savings per year for that crop alone (Maine and Boyles, 2015). Many bat species in tropical and subtropical regions are also important pollinators and dispersers of seeds (Boyles et al., 2011; Kunz et al., 2011). Mortality due to WNS and other population stressors is expected to reduce the levels at which bat populations provide these valuable and irreplaceable ecosystem services.
Impact: EnvironmentalTop of page
White-nose syndrome affects all life stages of hibernating bats, and mortality at newly-affected hibernacula can be very high, resulting in substantial and rapid decreases in bat abundance (Frick et al., 2010). Millions of North American bats have died from WNS, and population declines for heavily impacted species could result in regional extirpation of some previously common species such as the little brown bat (Myotis lucifugus) and northern long-eared bat (M. septentrionalis) (Frick et al., 2010; Frick et al., 2015; Reynolds et al., 2016; Brooks, 2011; Thogmartin et al., 2013; Erickson et al., 2016).
Bat populations affected by WNS are expected to be slow to recover due to low annual fecundity, and some populations may struggle to achieve the numbers seen prior to emergence of this disease (Russell et al., 2015). Cumulative effects of other population stressors, such as mortality from wind-turbine collisions, could exacerbate disease impacts (Erickson et al., 2016). Long-term monitoring of bat populations will be vital for understanding recovery trajectories and guiding evidence-based management decisions (Russell et al., 2015).
Additionally, shifts in bat community composition and abundance have been documented in areas of the United States and Canada that have been affected by WNS (Francl et al., 2012; Frick et al., 2015). Although the implications of these declines and populations shifts are not fully understood, they are likely to exert ecological impacts (Brooks, 2011; Frick et al., 2015).
Large-scale impacts of WNS are confined to North America. Isolates of P. destructans from both North America and Europe have similar virulence in the North American little brown bat (Myotis lucifugus) (Warnecke et al., 2012). However, while skin infection with P. destructans has been detected in a number of European bat species, mass mortality attributable to infection has not been observed (Wibbelt et al., 2010; Puechmaille et al., 2011a; Puechmaille et al., 2011b; Pikula et al., 2012; Zukal et al., 2014).
Impact: SocialTop of page
Some bat species, such as the northern long-eared bat (M. septentrionalis), may consume large quantities of mosquitoes (Reiskind and Wund, 2009), and can therefore potentially benefit human health by reducing risks for transmission of vector-borne disease. Large-scale mortality due to WNS is expected to reduce these benefits.
Zoonoses and Food SafetyTop of page
Direct human health implications of Pseudogymnoascus destructans are unknown. However, there have been no reports to date of P. destructans infection occurring in human or animal species other than bats. Furthermore, human skin and core temperatures exceed the range permissive to growth of P. destructans.
Disease TreatmentTop of page
Captive experiments have demonstrated that individual animals removed from torpor can recover from infection through provision of appropriate supportive care (Meteyer et al., 2011). The fungus is also susceptible to a range of common antifungal medications that are used to treat other fungal infections through topical or systemic administration (Chaturvedi et al., 2011). However, appropriate dosing and tolerance of these medications is not established in bats. While treatment and rehabilitation of individual animals is possible (Meteyer et al., 2011) and could be deployed as a targeted intervention for critically endangered bat species that tolerate captivity, individualized disease treatment can make only small contributions to mitigating the impacts of white-nose syndrome on a population level.
Prevention and ControlTop of page
The U.S. Fish and Wildlife Service and the Canadian Wildlife Health Cooperative coordinate national and international partnerships to investigate and respond to white-nose syndrome (WNS) (U.S. Fish and Wildlife Service, 2011; Canadian Wildlife Health Cooperative, 2015). These interagency efforts have fostered considerable collaboration that led to rapid progress in monitoring and understanding the spread of WNS, characterizing Pseudogymnoascus destructans as a pathogen, developing effective diagnostic approaches, organizing multi-agency working groups to encourage collaboration, and developing federal-state surveillance partnerships to track pathogen spread (Voyles et al., 2015; Lankau and Moede Rogall, 2016).
Management of hibernacula, including restriction of human access to some sites, and development of procedures and requirements to disinfect caving equipment, was instituted in partnership with recreational caving communities to limit anthropogenic spread of P. destructans (Sleeman, 2011; Shelley et al., 2013; Ballmann et al., 2017). Preventing spread by natural movement of bats is not feasible given the mobility of free-ranging wildlife. Additionally, culling of infected individuals within a hibernaculum does not reduce morbidity and mortality from WNS because of the rapid spread of the fungus within dense populations and because of the role of environmental substrates as a persistent reservoir of P. destructans (Foley et al., 2011; Hallam and McCracken, 2011; Crozier and Schulte-Hostedde, 2014; Meyer et al., 2016).
Current research efforts to reduce bat population losses and support their recovery are increasingly focused on developing mitigation strategies to limit the expansion of WNS. Understanding of the pathobiology of P. destructans infection suggests avenues that could reduce prevalence or severity of clinical disease in hibernating bats. For example, a topic of active investigation is the potential to reduce burdens of P. destructans in hibernation environments to lessen morbidity and mortality of bats at a population level through application of biological- or chemical-control strategies (Cornelison et al., 2014a; Cornelison et al., 2014b; Frank et al., 2014; Hoyt et al., 2015a; Zhang et al., 2015; Boire et al., 2016; Cheng et al., 2016; Frank et al., 2016). Additionally, development of an oral vaccine that could be used to immunize bat populations against infection by P. destructans is underway; proof-of-concept testing of a candidate recombinant raccoonpox virus platform for oral immunization of bats was recently completed (Stading et al., 2016).
ReferencesTop of page
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OrganizationsTop of page
Canada: Canadian Wildlife Health Cooperative (CWHC), Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, S7N 5B4, http://www.cwhc-rcsf.ca/index.php
USA: Bureau of Land Management (BLM), 20 M Street SE, Washington, DC 20003, https://www.blm.gov/
USA: National Park Service (NPS), 1849 C Street NW, Washington, DC 20240, https://www.nps.gov/
USA: US Fish and Wildlife Service (USFWS), 300 Westgate Center Drive, Hadley, MA 01035, https://www.whitenosesyndrome.org/
USA: US Forest Service (USFS), 1400 Independence Ave. SW, Washington, DC 20250, https://www.fs.fed.us/
USA: US Geological Survey (USGS), USGS National Center, 12201 Sunrise Valley Drive, Reston, VA 20192, https://www.usgs.gov/
ContributorsTop of page
13/02/17: Original text by:
David Blehert, USGS National Wildlife Health Center, Madison, Wisconsin, USA
Emily Lankau, USGS National Wildlife Health Center, Madison, Wisconsin, USA
Use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US government.
Distribution MapsTop of page
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