White-Nose Syndrome in Bats by Chris Wisniewski

The Past, Present and Future of White-Nose
Syndrome in Bats
Abstract
White-nose syndrome (WNS) is an invasive fungal disease that has killed millions of bats since it was
recently discovered in New York. The fungus colonizes and deteriorates the tissues of hibernating bats
leading to degradation of water balance, frequent arousals from torpor, accelerated fat store depletion and
eventually death. Considering the exceedingly high mortality rate (~ 90%) and rapid spread, which as of
spring 2015 WNS has been confirmed in twenty-six states and five Canadian provinces, its projected that
once common bat species will soon become extinct from affected North American regions unless new
breakthroughs in research and intervening conservation efforts occur. These insectivorous bats play a
crucial role in pest control. It has been suggested if WNS continues to devastate these keystone species,
the agricultural industry will suffer great losses.
Christopher D. Wisniewski
Southern Connecticut State University
Department of Biology
Spring 2015
Table of Contents
The Past, Present and Future of White-Nose Syndrome in Bats
Introduction....pp. 2-3
Pseudogymnoascus destructans....................................pp. 3-4
Pd introduction to North America.pp. 4-5
Pd transmission..pp. 5-8
Pd incubation.....p. 8
WNS detection...pp. 8-10
Pd infection....pp. 10-11
Potential recovery from WNS...pp. 11-12
Physiological disturbances associated with WNS....pp. 12-13
Behavioral disturbances associated with WNS.pp. 13-15
Population devastation...pp. 15-17
Looking forward....pp. 17-20
Why bats are important..p. 20
Ecological importance of bats...pp. 20-21
Economic importance of batspp. 21-22
Bats as model speciesp. 22
Conservation..pp. 22-26
In closing...p. 26
Acknowledgements...p. 27
References.pp. 28-33
Introduction
White nose syndrome (WNS), an emerging mycosis, has been responsible for killing
millions of bats in the United States and Canada since it was discovered at Howe Caverns in
upstate New York in 2006 (Blehert et al. 2009). The psychrophilic fungus which causes WNS,
Pseudogymnoascus destructans (Pd) (Blehert et al. 2009; Gargas et al. 2009; Lorch et al. 2011;
Warnecke et al. 2012; Minnis & Lindner, 2013), develops on bats as a filamentous white growth
on wings, muzzles and ears. While fungal conidia growth around the muzzle of bats is one of the
most conspicuous signs of WNS, bat wing membranes are often the most afflicted regions by Pd
SCSU Biology
due to this region containing the largest surface area of exposed skin (Meteyer et al. 2009; Cryan
et al. 2010). Pd spores colonize these superficial tissues and begin to deteriorate the epidermis
and dermis (Meteyer et al. 2009; Cryan et al. 2010). This destruction allows for further
expansion of the fungal colony into healthy, superficial and deep tissue leading to a plethora of
physiological and behavioral disruptions which ultimately cause mortality (Cryan et al. 2010;
Turner, Reeder & Coleman, 2011; Verant et al. 2014).
Since the initial documentation in 2006, its estimated that WNS has killed between 5.7 6.7 million bats in hibernacula across twenty-six states and five Canadian provinces (US Fish &
Wildlife Service, 2012; 2014). In addition to the twenty-six states with confirmed WNS, two
additional states have reported the presence of Pd in hibernacula without being able to confirm
the disease in bats (US Fish & Wildlife Service, 2014). Seven species of insectivorous bats are
currently afflicted by WNS: big brown bat (Eptesicus fuscus), eastern small-footed bat (Myotis
leibii), gray bat (M. grisescens), Indiana bat (M. sodalis), little brown bat (M. lucifugus),
northern long-eared bat (M. septentrionalis), and tricolored bat (Perimyotis subflavus) (US Fish
& Wildlife Service, 2014). Of this group M. sodalis, M. grisescens and M. septentrionalis are
listed under the Endangered Species Act, while M. lucifugus has been proposed for listing on
endangered lists in some states (e.g. CT). Furthermore, five additional species have been
detected carrying Pd, but have yet to be diagnostically confirmed with WNS: eastern red bat
(Lasiurus borealis), southeastern bat (M. austroriparius), silver-haired bat (Lasionycteris
noctivagans), Rafinesques big-eared bat (Corynorhinus rafinesquii) and Virginia big-eared bat
(C. townsendii virginianus), of which C. townsendii virginianus is listed under the Endangered
Species Act (US Fish & Wildlife Service, 2014).
The highest concentrations of WNS cases remain in New England and throughout regions
surrounding the Appalachian Mountains, but increasing concentrations of WNS are being
reported from the Midwest. Pd grows optimally in cold temperatures. Growth is slow, and
unfortunately most WNS infected hibernacula are found in climates which seasonally fall within
the optimal growth range of Pd, allowing prime conditions for Pd to thrive (Blehert et al. 2009).
Mortality rates can average 90% (Frick et al. 2010; Turner, Reeder and Coleman, 2011; Langwig
et al. 2012), but some regions are reporting a ~100% mortality rate (US Fish and Wildlife
SCSU Biology
Service, 2014). These high mortality rates over repeated hibernation cycles have led to massive
population declines of once common native bat species.
The devastation of North American bat species by WNS is unprecedented. This is the
largest wildlife epidemic ever recorded and it poses a threat of regional extinction to multiple bat
species in the coming years (Frick et al. 2010; Langwig et al. 2012). This review aims to bring
together available data on WNS in North America into one convenient report in hopes to
generate new directions for habitat/species management practices as well as aid conservation
strategies and future research. As I advocate the dire need for conservation and continued
research efforts, I hope to increase awareness, educate others, and encourage more individuals to
become involved to help bring our local bat species back from the brink of extinction, thus
preserving our natural history.
Pseudogymnoascus destructans
The causative agent of white-nose syndrome (WNS), Pseudogymnoascus destructans
(Pd; formerly classified Geomyces), is a psychrophilic fungus found to grow between 0-20C
(Blehert et al. 2009; Gargas et al. 2009; Lorch et al. 2011; Warnecke et al. 2012; Verant et al.
2012; Minnis & Lindner, 2013). While Pd grows optimally between 12.5-15.8C, it has been
found Pd cannot grow at temperatures as low as -10C or as high as 25C, with 19-19.8C being
the approximate upper growth/temperature limit (Blehert et al. 2009; Chaturvedi et al. 2010;
Verant et al. 2012). Pd reproduces asexually and is characterized by the presence of colonizing
fungal hyphae with distinctive asymmetrically curved conidia (Blehert et al. 2009; Gargas et al.
2009). Gross identification of Pd on bats is possible due to the presence of white filamentous
growth appearing on wings, muzzles and ears (Blehert et al. 2009; Gargas et al. 2009) or as a
filmy substance on wings (Meteyer et al. 2009). Perhaps the most indicative/characteristic sign
of the disease on bats in the field is the presence of white conidia growth on the muzzle, which
also contributed to the creation of the white-nose designation of the disease (Blehert et al.
2009; Cryan et al. 2010).
Pd introduction to North America
SCSU Biology
As of spring 2015, WNS has been confirmed in hibernacula across twenty-six states and
five Canadian provinces (US Fish & Wildlife Service, 2014). In addition, Pd is also currently
present in two additional states where the disease has yet to be confirmed in bats. How did Pd
and WNS come to be in North America? Via experimentation, North American bat species were
shown to be equally susceptible to strains of Pd from both North America and Europe. This
allowed Warnecke et al. (2012) to support the novel pathogen hypothesis in which it is believed
that Pd was accidentally introduced from Europe where Pd and WNS are present, but without the
associated mass mortality present in North American bat species. The introduction of Pd on
nave populations of North American bats is believed to be the driving force behind the
subsequent mass mortality (Warnecke et al. 2012). In fact, Pd remained overlooked on the bats
of Europe until the recent explosion of WNS in North America nine years ago (Warnecke et al.
2012). Warnecke et al. (2012) suggest that bats with Pd in Europe display more well-adapted
physiological and behavioral responses compared to the disorderly responses of North American
species; this accounts for the absence of mass mortality of bats in Europe compared to North
America. This work also supports Wibbelt et al. (2010) who mention that: 1.) Pd may have been
present and coevolved with European bats leading to an immunological or behavioral resistance
or tolerance to form in regards to the fungus, or that 2.) Microbial flora present on bats or in
hibernacula in Europe may have coevolved with Pd leading to its nonpathogenic role. Both
suggestions could explain why there is such a contrast in mortality cases between the two
continents. It would be interesting to determine the effects of the North American strain of Pd on
European bat species. Further testing could potentially fill gaps about the differences in
pathogenicity between the two continents and help to support an explanation as to why European
bats are capable of living with the fungus. Furthermore, I hypothesize the culturing of the skin
microbiome of European bats may provide useful data in regards to potential naturally occurring
microbes which may possess antifungal properties similar to the North American bats in the Hoyt
et al. (2015) study which is discussed later. This could explain the lack of mortality in European
bats and provide droves of useful data which could have large implications for North American
bats, given sufficient testing.
The novel pathogen hypothesis was further supported by Lorch et al. (2013) who were
able to disprove the hypothesis that a less virulent strain of Pd was always present in North
SCSU Biology
America, until a mutation and subsequent increasing pathogenicity emerged leading to the
current WNS outbreak. Lorch et al. (2013) screened collected sediment samples from
hibernacula both inside and outside of WNS affected regions and isolated DNA from these
samples. Of the 295 sediment samples screened, 17 were positive for Pd, all of which came
from within WNS affected regions; no Pd was discovered in samples from non-affected regions
(Lorch et al. 2013). These findings provide evidence against an endemic strain of Pd being
present in North America prior to the WNS outbreak and instead support the novel pathogen
hypothesis suggesting Pd was accidently introduced from Europe to North America.
Pd transmission
Although possible modes of transmission for WNS are still being investigated, some have
been well supported. WNS can be transmitted among bats via direct contact between individuals
or via direct contact between bats and hibernacula/environment (Lorch et al. 2011; Lorch et al.
2013; Hoyt et al. 2014; Bernard et al. 2015). Some early indications for bat to bat transmission
of WNS comes from documentation of infection at multiple sites in Pennsylvania, which were
initially shielded from humans and population management before WNS was detected, still, the
resulting infection was hypothesized to have been introduced by infected bats (Turner, Reeder &
Coleman, 2011). Similarly, Lorch et al. (2011) housed naturally infected bats together with
healthy bats and found that 89% of the healthy individuals developed characteristic WNS lesions
by the 102 day mark of the experiment. This data is rather important as it shows tightly clustered
groups have a near 90% chance of transferring and developing WNS between individuals. Most
species afflicted by WNS tend to form tightly clustered groups in natural hibernacula settings,
behavior which further increases the spread of WNS.
Lorch et al. (2011) also tested how well WNS conidia could be spread through the air.
Researchers separated two groups of bats, one infected and one healthy, in mesh cages which
were placed 1.3 cm apart. No direct contact among infected and non-infected individuals
occurred, and at the 102 day mark, none of the healthy individuals showed evidence of being
infected with WNS. They suggest the conidia of Pd may not be able to disperse through air at
high enough concentrations to infect otherwise healthy individuals.
SCSU Biology
Pd can also be transmitted via direct contact between bats and hibernacula/environment.
It is understood that Pd has the ability to survive in hibernacula in the absence of bats serving as
a reservoir for new infections. Lorch et al. (2013) detected live Pd in 7 out of 14 hibernacula
sites during the late summer when bat population densities were low. In this same study,
sediment samples from the sites were tested and live Pd was found in sites where bats had not
been present from a few months, to up to two years, indicating long term persistence of the
fungus is possible given suitable hibernacula conditions. Hoyt et al. (2014) also showed Pd can
persist in environments in the absence of a host. They isolated Pd from bats, and stored pure
isolates in an incubator at 5C and 30-40% relative humidity for 5-6 years. After this time, Pd
from six of the nine original isolates grew on new media, confirming enough viable conidia
remained over this extended period of time. This demonstrates that even after long term
laboratory storage Pd can grow in the absence of a host, suggesting that environments
contaminated with Pd conidia can continually infect bats. Additionally, its suggested that the
presence of other microbes, inducing competition, and humidity may affect Pd survival in
natural conditions (Hoyt et al. 2014). Recent data also supports that Pd spread can be expedited
via contact between bats and hibernacula. Bernard et al. (2015) found C. rafinesquii, L. borealis
and L. noctivagans tested positive for Pd. While these species have not been confirmed
diagnostically for WNS, they have been shown to carry the fungus, potentially spreading it
among hibernacula and other individuals. This is rather unsettling as Boyles, Dunbar &
Whitaker Jr. (2006) and Dunbar, Whitaker Jr. & Robbins (2007) have shown these species to
remain active during winter months and maintain fat stores; traits which potentially allow these
species to further spread Pd over a larger geographic range during winter months compared to
other torpid individuals.
Recently, five mechanisms driving seasonality transmission of Pd were proposed. The
mechanisms, proposed by Langwig et al. (2015A) are: 1.) Sociality, which can increase or
decrease infectious contact rates. 2.) Seasonal birth pulses, which can increase transmission
through new, susceptible individuals introduced to populations. 3.) Seasonal changes in habitat
use, which could influence the transmission and persistence of Pd. 4.) Climatic change,
potentially influencing the persistence of Pd. 5.) Seasonal difference in host immune function,
which could determine the pathogenicity of Pd on certain species. Of the six species involved in
SCSU Biology
the experiment all showed consistent concentrations of Pd which varied with the seasons.
Langwig et al. (2015A) found no support for the hypothesis that birth pulses drive seasonality.
They found the prevalence of Pd dropped during the summer months when births occurred. It
was also found that seasonal changes in habitat use showed low transmission and infection
intensity until prolonged torpor was employed by bats, meaning another factor had to have been
driving seasonality (Langwig et al. 2015A). Langwig et al. (2015A) found that hibernation was
the dominant factor driving transmission and pathogenicity. Prolonged torpor brought about
close to 100% of individuals becoming infected. Contact rates during this time are unknown, but
they could influence transmission. It is understood that the body temperature of bats during this
time, also within the range required by Pd to thrive, is what allows for such an explosion of
pathogen growth and transmission (Langwig et al. 2015A). The influence of Pd on hibernating
bats during this time is maximized; as when infection peaks, populations are usually at their
lowest concentrations which brings about the most drastic implications of WNS. Overall, the
seasonal timing (winter hibernation) of transmission and pathogenicity allow for the most
damage to be dealt to bat species, while at the same time, seasonal timing affects Pd spread due
to the periods of low mobility demonstrated by the hibernating bat hosts (Langwig et al. 2015A).
The researchers hypothesized that if transmission rates were comparable in autumn as they are
during winter, that Pd spread and infectiousness would be much higher than we currently witness
(Langwig et al. 2015A).
It should also be noted that Pd can be transmitted via humans who come in contact with
either bats or hibernacula. Pd conidia can be transported on equipment and clothes, increasing
the likelihood of Pd spread and thus WNS occurrence (Turner, Reeder & Coleman, 2011; Hoyt et
al. 2014). In fact, this form of transmission is conducive with the novel pathogen hypothesis and
is believed to be how Pd and WNS were introduced to North America. Hoyt et al. (2014)
suggested that Pd may be able to survive outside of hibernacula (on equipment, clothes, etc.) if
such materials are stored in cool dry places.
Pd incubation
Lorch et al. (2011) were able to quantify the incubation period of Pd in bats, how much
time passed until WNS became characteristically present and how long until mass mortality of
SCSU Biology
populations took place. Through experimental infection with Pd, and subsequent histological
examination they found that inoculated bats developed diagnostic lesions for WNS 83 days after
being treated and all were positive for WNS when the trial was terminated at the 102 day mark.
Large scale mortality among infected bats was not witnessed, but this was due to the short term
of their experiment. The study was able to support data on the development of WNS in wild
bats. In wild populations, WNS lesions are initially detected in late September prior to the onset
of long term hibernation. Mass mortality can begin in late January and peak in March (Lorch et
al. 2011). This demonstrates that mortality from WNS doesnt begin until approximately 120
days from when bats begin long term, winter hibernation in which cold temperatures necessary
for Pd to thrive occur, also mortality peaks at about 180 days; this accounts for why mass
mortality wasnt observed in their experiment which was terminated at the 102 day mark before
the disease could progress further to induce mortality.
WNS detection
White fungal growth found on the muzzles, wings and ears of bats are characteristic signs
of WNS (Blehert et al. 2009; Gargas et al. 2009). These gross fungal lesions can be indicative of
WNS; however they dont always lead to a diagnosis. Gross lesions can be damaged or lost
when bats are prepared and transported from hibernacula to laboratory settings, making further
examination imperative for confirmation of the disease (Meteyer et al. 2009).
Histopathologic examination is considered the most effective way to confirm WNS in an
infected organism (Meteyer et al. 2009). Alterations in skin of infected bats can include patches
of rough skin, loss of sheen on glabrous skin, irregular pigmentation and tears in wing
membranes (Meteyer et al. 2009). Through microscopy, detection of Pd hyphae and conidia on
infected tissue is possible. The surface area of tissue needs to be maximized, which can be
accomplished by fixing longitudinal sections of tissue in 10% neutral buffered formalin and
embedding trimmed surfaces to maintain the position of fungus in regards to dermal structures
(Meteyer et al. 2009). Meteyer et al. (2009) found staining useful in detecting the fungus;
periodic acid-Schiff stain was shown to be the most effective at detecting non-pigmented fungal
hyphae and conidia. Cup-like epidermal erosions found via microscopy of wing membranes
are characteristic of WNS and are often filled with hyphae (Meteyer et al. 2009). The fungus can
SCSU Biology
be found continuing to invade underlying connective tissue and can encompass the full thickness
of the wing membrane. In regards to the muzzle, hyphae invade hair follicles, sebaceous glands,
apocrine glands and connective tissue (Meteyer et al. 2009). Meteyer et al. (2009) also note bats
with damaged wings collected from outside hibernacula showed severe inflammation in
accordance with the fungal infection. Suppurative dermatitis with folliculitis, edema, infiltrates
of macrophages, and serocellular inflammatory crusts with hyphae were also noted histological
changes found by Meteyer et al. (2009). The necrosis and impairment of wing membranes can
be very problematic to bats and will be discussed in coming sections.
Histologic examination, a very effective diagnostic tool, often requires euthanasia in
order to acquire enough suitable tissue for testing. When considering the soaring mortality rates
associated with WNS, a non-lethal diagnostic tool would be most advantageous for field and
laboratory research. Recently, Turner et al. (2014) have been successful in detecting WNS in
bats via the use of long-wavelength UV light (360-385 nm), a method which does not require
euthanasia. They found that WNS infected individuals displayed a unique orange/yellow
fluorescence when under this UV light. Turner et al. (2014) have hypothesized that the lesions of
cupping erosion found on wing membranes is what is indeed fluorescing under UV light,
which they have supported. Turner et al. (2014) supported their findings via histopathologic
examination which confirmed, in accordance with their UV method of identification, infected
versus non-infected individuals. With exceedingly high WNS mortality rates this new diagnostic
tool should show one of its greatest virtues in future analyses, not requiring euthanasia for valid
diagnosis of WNS.
Polymerase chain reaction (PCR) also offers a fast and reliable way to detect Pd. The
PCR technique allows for rapid detection of Pd DNA from using a small amount of bat skin
usually collected via wing punch. Previous approaches using PCR based techniques to detect
Pd, while being beneficial, have had limitations (Lorch et al. 2010; Chaturvedi et al. 2011).
However, recent approaches are proving to be more promising. A specific and sensitive realtime TaqMan PCR test detects DNA from Pd by targeting a multicopy IGS region of rRNA gene
(Muller et al. 2013). This PCR technique has shown to be more sensitive than its predecessors at
detecting Pd and should continue to be an effective diagnostic tool.
SCSU Biology
The culture technique used to detect Pd is probably the least efficient diagnostic tool of
those mentioned thus far, but its not without its benefits. This technique requires taking an
infected tissue sample, growing the microbial elements of the sample on media and then
identifying the given organisms and their morphology under microscope in order to determine if
Pd is present (Lorch et al. 2010). The culture method has been shown to have a diagnostic
sensitivity of 54%, compared to PCR, histologic and UV diagnostic sensitivities which range 90100% (Lorch et al. 2010; Muller et al. 2013; Turner et al. 2014). The low sensitivity of the
culture method is likely due to competition between other microbes present in the sample and Pd
on the medium.
The histologic identification method remains the most commonly used for identifying
WNS in bats, but PCR methods have shown their worth and can be just as effective. The newest
method of identification via ultraviolet fluorescence also appears to be viable and should prove
valuable in the coming years to researchers, especially field biologists, as the application of longwave UV fluorescence is readily straightforward when using a field portable fluorescent light
(Turner et al. 2014). The culture method, used in accordance with any of these other methods
should also be beneficial; however it should not be relied upon as the sole identification method.
Pd infection
Pd conidia colonize muzzles, ears and wing membranes of hibernating bats. The Pd
infection initially invades the epidermis of the ears and wings, of which are most afflicted due to
the large surface area of skin (Meteyer et al. 2009; Cryan et al. 2010). Inflammation can be
absent in infected tissues, although this is most likely due to the suppression of immune
responses associated with hibernation (Meteyer et al. 2009; 2011). As the infection progresses,
Pd appears as hyphae filled, cup-like lesions within the epidermis, which continue to invade and
degrade sebaceous and apocrine glands, hair follicles, connective tissue, lymphatic vessels and
muscle fibers in infected areas (Meteyer et al. 2009; Cryan et al. 2010). Infarction has been
observed in wing membranes and although Pd is not vasculotropic it appears to have an effect on
blood flow to certain regions of the wings (Cryan et al. 2010). Reichard and Kunz (2009)
identified five types of wing damage on bats with WNS, including; splotching, flaking, necrosis,
holes and membrane loss. Damaged wings from WNS are far more prevalent and more varied
SCSU Biology
10
than wing damage associated with normal environmental occurrences (Reichard & Kunz,
2009). Such damage can affect flight abilities and physiological mechanisms necessary for
survival. This destruction not only allows for further expansion of the fungal colony into healthy
tissue, but leads to a plethora of physiological and behavioral disruptions (Cryan et al. 2010;
Verant et al. 2014; Turner, Reeder & Coleman, 2011). The ultimate mechanisms leading to
mortality from WNS remain debated; however, degradation of bodily tissues from Pd remains an
underlying, causative agent of such mechanisms.
Potential recovery from WNS
Bats have been found to recover from WNS, given the right conditions. Meteyer et al.
(2011) collected 30 infected bats from the wild and provided them with supportive care in
captivity for 70 days. The supportive care included an initial .75 mL dose of lactated Ringers
solution (given subcutaneously), a steady diet of mealworms per night and housing temperature
ranging from approximately 18-24C. 26 of the 30 individuals survived the treatment, and of
those, all but one showed recovery of wing membranes (Meteyer et al. 2011). In addition to
membrane recovery, PCR tests and microscopic examination of tissue samples showed no
presence of Pd. An acidic vinegar solution, which was hypothesized might aid in healing, was
also applied to bats during the 70 day period, but treated bats showed no additional benefit in
recovery compared to non-vinegar treated bats. It is probable that the supportive care and
namely the increased temperature allowed for WNS recovery. As mentioned previously,
suppression of the immune system during hibernation allows for an absent or delayed
inflammatory response, giving an advantage to Pd against an otherwise defenseless bat (Meteyer
et al. 2009; 2011). Meteyer et al. (2011) showed that the increased captive temperature and thus
increased body temperature of bats was detrimental to the growth of Pd, which cannot thrive at
such temperatures. In addition, Meteyer et al. (2011) found that some bats showed an increased
neutrophilic response after homeothermic resurgence following hibernation. This neutrophilic
response should be beneficial to bats recovering from WNS during the emergence from
hibernation, but it can also play a role in compromising flight before full recovery is obtained,
making recovery of wild bats from WNS dependent on a multitude of factors and even then
recovery is not guaranteed.
SCSU Biology
11
Recovery of bats from WNS is possible in the wild; however it is rarer than perhaps the
most infamous trait associated with WNS afflicted bats, mass mortality. The hypothesized
ultimate mechanisms leading to mortality from WNS include disruptions of vital physiologic
functions necessary for maintaining homeostasis; e.g. thermoregulation, water balance,
metabolic regulation, maintaining fat stores, etc. (Verant et al. 2014). These disruptions are also
thought to alter behaviors in bats with WNS; e.g. frequent arousals from torpor, daytime flying,
uncoordinated flight, etc. (Verant et al. 2014).
Physiological disruptions associated with WNS
Verant et al. (2014) used collected works (Meteyer et al. 2009; Cryan et al. 2010; 2013;
Reeder et al. 2012; Warnecke et al, 2012; 2013), as well as their own data to generate a multistage progression model, which provides an all-inclusive view regarding the progression of
WNS, from infection to death.
This model supports the hypothesis suggesting infection with Pd and development of
WNS increases energy/fat store usage thus leaving inadequate energy stores needed for winter
survival. Verant et al. (2014) showed that under similar conditions, bats with WNS used twice as
much energy compared to their non-infected counterparts. Furthermore, the increased energy
usage didnt correlate with increased arousals from torpor, suggesting that bats have an elevated
metabolism long before late stage behavioral alterations are noticed.
The model proposes that initial wing membrane colonization by Pd leads to the invasion
and degradation of the epidermis. During the epidermal invasion by Pd, the metabolic rate of the
bat increases as does CO2 levels in the blood. This increased CO2 leads to acidemia and
hyperkalemia, both of which lead to chronic respiratory acidosis and the depletion of fat
reserves. Further degradation of the epidermis occurs and Verant et al. (2014) suggest that as
pCO2 increases, hyperventilation is induced leading to arousals from torpor to remove excess
CO2 and regulate blood pH. These arousals then lead to dehydration and further depletion of fat
stores. As the Pd invasion progresses deeper, reaching connective tissue, additional water and
electrolyte loss occurs. Dehydration is then intensified leading to additional arousals from
torpor. This all creates a positive feedback loop enveloping arousal, water loss, electrolyte loss
SCSU Biology
12
and energy use. This feedback loop continues until all compensatory mechanisms and energy/fat
reserves are drained, leading to death, however, if compensatory mechanisms and energy/fat
reserves remain until the spring emergence from hibernation then its possible for the Pd
infection to recede and for the bat to possibly recover.
This model is the first of its kind and includes testable hypotheses which should provide a
basis for future research and should provide crucial knowledge of disease progression that will
aid conservation practices in the fight against WNS.
Behavioral disturbances associated with WNS
WNS is also known to bring about behavioral disturbances in hibernating bats. The most
debated behavioral disturbance in bats due to WNS is arousal from torpor. Torpor (a form of
dormancy, similar to hibernation, but occurring over much shorter periods in which body
temperature and metabolic rates are reduced) can last from periods of days to weeks in bats
(Geiser, 2004; Reeder et al. 2012). During normal torpor, brief arousals may occur and last in
intervals of one to two hours (Geiser, 2004). Arousals generally demand a great energetic cost
and bats with WNS have been found to have three to four times as many arousals than their noninfected conspecifics (Warnecke et al. 2012), resulting in an even higher energetic cost in
infected compared to healthy individuals. For example, M. lucifugus requires enough sustainable
fat reserves to survive ~ 190 days (Thomas, Dorais & Bergeron, 1990). Warnecke et al. (2012)
estimate that each arousal from torpor decreases a bats ability to hibernate by approximately nine
days; extrapolate this number with three times as many arousals in an infected individual and its
understandable as to why so many bats are observed with prematurely depleted energy/fat
reserves. Recently, Verant et al. (2014) found that greater energy use of bats with WNS is not
associated with an increase of arousals from torpor like previously thought, but instead bats with
WNS have an elevated metabolism from the onset of infection. They mention that initially,
hyperventilation stimulates arousals to allow for the removal of excess CO2 to regulate blood pH.
Additional arousals also occur in response to water and electrolyte loss in hopes of replenishing
such resources (Verant et al. 2014).
SCSU Biology
13
Furthermore, Turner et al. (2015) provide evidence that synchronization of arousals

reflects disturbances of torpid bats by infected conspecifics. They discuss that hibernating bats
are highly susceptible to disturbance, making arousal more likely if actively infected bats
continue to come in contact with torpid individuals. As hibernation and infection progresses this
increased contact brought about a cascade effect of increasing arousals over time (Turner et al.
2015). Nonetheless, the high energetic demands of frequent arousals from torpor remain and are
still instrumental in the depletion of hibernating resources and subsequent mortality.
WNS is associated with other abnormal behaviors in hibernating bats as well. While
winter flying, specifically daytime winter flying, in healthy bats is not considered abnormal
(Hendricks & Hendricks, 2010), bats suspected of potentially having WNS have been observed
partaking in excessive flying (Cryan et al. 2010), unusual daytime flying, uncoordinated flying
including collisions into nearby trees, buildings, etc. (Turner, Reeder and Coleman, 2011) and an
overall premature emergence from winter hibernation (Cryan et al. 2010). These bats have also
been observed flying near water deposits, possibly in an attempt to drink to restore water loss, as
well as eating snow to increase their water intake (Cryan et al. 2010). In laboratory observations
bats with WNS have been observed partaking in increased grooming behavior possibly due to
irritation from Pd infection (Brownlee-Bouboulis & Reeder, 2013). Brownlee-Bouboulis &
Reeder (2013) noted bats with WNS spent more time active which resulted in decreased resting
and restorative behaviors. As a result of increased grooming and overall activity it was
mentioned that the ingestion of Pd spores among infected bats occurs and that the survivability
of Pd through the bats digestive system and further spread through guano is possible (BrownleeBouboulis & Reeder, 2013). While Brownlee-Bouboulis & Reeder (2013) noticed more
grooming and activity in WNS infected bats, Wilcox et al. (2014) noted no increase in grooming,
activity or water intake in bats in their experiment.
In addition to these behaviors, bats with WNS have been observed engaging in altered
roosting behaviors, such as roosting towards the entrances of hibernacula or roosting individually
(McAlpine et al. 2011; Langwig et al. 2012; Wilcox et al. 2014). Wilcox et al. (2014) provide
support for reduced rates of clustering in bats with WNS as they observed infected bats form
more clusters of fewer bats during their experiment. Langwig et al. (2012) and Wilcox et al.
SCSU Biology
14
(2014) mention this reduced clustering being a tenet of sickness behavior in which it is more
advantageous for individuals in infected hibernacula to remain isolated from one another to
reduce the spread and other unfavorable side effects of the given disease. This led Turner et al.
(2014) to identify that reduced clustering and isolation could be an adaptive response by bats
with WNS to reduce the spread of Pd. The behavioral study of bats in laboratory and wild
settings is often difficult; although some observations and experiments have been completed
more data and examination into the behavioral disturbances of bats with WNS is needed to
clarify competing results and establish well-supported explanations. It would be interesting to
observe if any additional altered or adaptive behaviors are occurring in bat populations in states
near the epicenter of the WNS outbreak. Bats of this region have shown persistence in response
to WNS before (Reichard et al. 2014), and as this region has been affected by WNS the longest,
altered or adaptive behaviors may be more likely to occur here and thus have a greater
probability of being witnessed by researchers compared to a region which has only recently
become infected.
Population devastation
To date WNS has been responsible for the death of upwards of seven million bats. The
sophistication, complexity and mystery of WNS has led to the unprecedented mortality thats
now threatening multiple species of bats with regional extinction. Annual declines of 30- 99% of
bats at infected hibernacula showcase the impact WNS is having on these afflicted populations
(Frick et al. 2010). Frick et al. (2010) simulated one-hundred years of post-WNS population
dynamics to assess what the future of these North American insectivores may look like. PreWNS population growth of M. lucifugus was estimated using a population matrix model with
data from 1993-2008 (Frick et al. 2010). The geometric mean growth rates of M. lucifugus from
winter count surveys from the previous three decades was also calculated, Population growth
gathered from the population matrix model was positive, showing stable population growth
during pre-WNS years. Long-term growth rates show 86% of hibernacula displayed stable or
increasing populations as well (Frick et al. 2010).
Using a stochastic population model with data from infected and susceptible populations
Frick et al. (2010) performed one thousand simulations of one hundred years of growth
SCSU Biology
15
dependent on five scenarios from an initial population of 6.5 million bats. As such, they expect a
99% chance of regional extinction of M. lucifugus by the year 2026; annual declines would need
to be less than 5% per year for a noticeable reduction in the chance of extinction occurring over
one hundred years. Its important to note that these predictions were derived for the previously
most abundant bat species in North America, M. lucifugus. If the most plentiful bat species in
North America is expected to be regionally extinct in WNS affected areas by 2026 its most
likely that pre-WNS endangered bat species like M. sodalis and M. grisescens or newly listed
endangered bat species M. septentrionalis will also become extinct. There is evidence of
interannual survival of M. lucifugus in New England states as some colonies seem to persist
(Reichard et al. 2014). However, as the once common little brown bat is proposed for listing on
the endangered species list in Connecticut, its doubtful if populations will ever recover to preWNS levels.
Population forecasting has also been researched by Langwig et al. (2012). They
estimated population growth rates of six bat species both before and after the outbreak of WNS
based on data from 120 regional populations. After incorporating changes in roosting behavior,
environmental variation and population densities into their mathematical models, Langwig et al.
(2012) found that prior to WNS all of their tested species showed increasing population growth.
However, in years following WNS discovery, population growth rates for four species showed
significant decline (M. lucifugus, M. sodalis, M. septentrionalis & P. subflavus), while the
remaining two species showed neither growth nor decline (E. fuscus & M. leibii) (Langwig et al.
2012). Overall, all growth rates were much lower post-WNS discovery than in pre-WNS years,
and ~27% of the examined bat populations (32 of 120) became extinct (Langwig et al. 2012).
Based on their results and continued modeling M. septentrionalis, M. sodalis and M. lucifugus
are predicted to go extinct.
Alves, Terribile & Brito (2014) have also conducted modeling to examine the potential
increasing spread of WNS as well as its continued effect on bat populations. They used
ecological niche modeling (ENM) to predict potentially new geographic regions which may
become afflicted by WNS. This data would be of great use to such regions as it would allow
them to take the necessary precautions and implement strategies to effectively deal with the
SCSU Biology
16
fungus and protect their local bat populations. The ENM took into account variations of
temperature, precipitation, elevation and land classes when modeling potential regions Pd could
infect and survive in. The generated map of potential spread displayed the current distribution of
Pd (Alves, Terribile & Brito, 2014). The map also showed regions susceptible to Pd which
presently are unaffected, including, coastal regions of the Northeastern U.S., the Mississippi
basin region and the Rocky Mountain region (Alves, Terribile & Brito, 2014). Alves, Terribile &
Brito (2014) hypothesize WNS will spread to these regions and urge that preliminary steps be
taken to reduce potential impacts of the disease. The modeling of this experiment also
demonstrated a pessimistic scenario in which nine species of North American bats could
potentially lose between 25% - 96% of their entire population as a result of WNS (Alves,
Terribile & Brito, 2014). The species include; M leibii, M. grisescens, C. rafinesquii, M.
austroriparius, M. sodalis, N. humeralis, P. subflavus, M. septentrionalis and E. fuscus.
Thankfully, some of these species have yet to be confirmed diagnostically for WNS, yet this
modeling still shows the ever present risk of population decline associated with WNS.
Surprisingly, M. lucifugus just missed being included in this listing as they received a ~23%
population decline score.
Looking forward
There is some hope for bats in the fight against WNS. Recently, Frank et al. (2014) have
found E. fuscus to show resistance to WNS at multiple sites in New York. Initially, Frank et al.
(2014) observed all E. fuscus to have torpor bouts which fell within the normal range of seven to
twenty-five days. Then it was found E. fuscus didnt deplete their fat reserves prior to the end of
hibernation as other affected species like M. lucifugus have at the same given sites. This
research group also examined the twenty-six big brown bats via long-wave UV light in which
they showed no signs of Pd infection (Frank et al. 2014). Overall, the number of big brown bats
at the given site increased over time by 43%, while the number of hibernating little brown bats
decreased by 99.6% (Frank et al. 2014). These field studies show E. fuscus not only subsisting
in Pd infected hibernacula, but actually flourishing as shown by the 43% population growth rate.
Previous records of decreasing numbers of E. fuscus in Northeast hibernacula are accounted to
other ecological factors rather than WNS.
SCSU Biology
17
Research from Hoyt et al. (2015) also shows promise. They assessed if bacteria from the
bats skin microbiome can inhibit Pd growth. Hoyt et al. (2015) demonstrated that these naturally
occurring bacteria can: 1.) Reduce initial colonization by Pd on bats, and can 2.) Displace Pd
already present on bats. The isolated bacteria, pseudomonas spp., are known to have antifungal
qualities and are most closely related to Pseudomonas fluorescens (Rainey & Travisano, 1998;
Hoyt et al. 2015). The strongest isolates produced in this study were cultured from E. fuscus,
which has previously displayed a lesser extent of mortality (Frank et al. 2014) in response to
WNS compared to other species. Hoyt et al. (2015) stress additional research is needed to
determine the abilities and limitations of these bacteria, also, that these pseudomonas strains
should be tested against a species known for high mortality from WNS (i.e. M. lucifugus) to
determine any potential functional significance.
The work of Johnson et al. (2015), investigating antibody-mediated immune response to
Pd in bats, is also important. In both captive and field studies, bat species from North America
and Europe were sampled. Blood samples collected from all species were heavily analyzed
which led to multiple findings. Johnson et al. (2015) found 90% of M. lucifugus sampled from
WNS negative hibernacula tested positive for anti-Pd antibodies and found M. lucifugus injected
with Pd to have greater anti-Pd antibody titers compared to control individuals. Johnson et al.
(2015) also found varying levels of seroprevalence and titers among multiple North American
species (dependent on the season) as well as differences in anti-Pd antibody levels among North
American and European species. Most notably, it was found that European bat species have
much lower antibody titers compared to North American species (Johnson et al. 2015). This data
provides evidence that an antibody immune response is not a mechanism of survival among
European bats; evidence further supported by the finding that M. lucifugus displays the highest
titers among species from both continents, yet still has one of the highest mortality rates from
WNS (Johnson et al. 2015). Bat populations in states where Pd has been present for a greater
period of time also showed greater seroprevalence and titers compared to populations in states
where Pd has only recently been found; suggesting that the bats with greater seroprevalence and
titer have already survived exposure to Pd and that behavioral or physiological traits may have
aided their ability to do so (Johnson et al. 2015). This work helped to further investigate survival
SCSU Biology
18
among bat populations in the presence of Pd and also provides evidence that immunizing bats
may provide protection from Pd (Johnson et al. 2015).
Recently published data from Lorch et al. (2015) should also be noted. They discuss how
nonlethal fungal infections may have gone undetected in bats before the outbreak of WNS. In
2011 in Wisconsin, hibernating bats with gross white fungal infections similar to those of Pd and
WNS were reported (Lorch et al. 2015). Initial histopathologic examination of the bats returned
negative for Pd and after a myriad of screening techniques including molecular and UV
examination, Lorch et al. (2015) found that newly characterized Trichophyton redellii (Tr) was
responsible for this colonization of hibernating bats. Tr is suspected to be native to North
America as it exhibits great genetic variation. Tr is believed to have been overlooked by
researchers until the recent WNS outbreak which increased awareness of fungal infections in
hibernating bats. Gross signs of Tr may be confused with those of Pd, but upon closer inspection
Tr can be differentiated from Pd. Microscopy of Tr reveals radially symmetric obovate to
pyriform microconidia that attach laterally to the sides or ends of hyphae and are sessile (Lorch
et al. 2015). Pd has been characteristically known for cup-like erosion of epidermal and
dermal layers (Meteyer et al. 2009), but Tr doesnt penetrate beyond the epidermis and does not
elicit the multitude of physiological or behavioral disturbances from its bat hosts as Pd and WNS
have (Lorch et al. 2015). Tr and Pd do share similar characteristics which Lorch et al. (2015)
mention could provide useful insight in future WNS work; they show similar characteristics such
as, both are slow growing psychrophiles capable of infecting bats and both are believed to have
soil residing ancestors. Through their work Lorch et al. (2015) propose Tr does not appear to
pose a threat to hibernating bat populations and they hope further study may explain mechanisms
as to how bats coincide with fungal infections and why Pd is associated with mass mortality.
Why bats are important
Bats play a crucial role in ecosystems across the world and are known to be essential
predators, seed dispersers, pollinators and nutrient distributors (Kunz et al. 2011). Bats also play
vital economic roles in relation to pest control, guano mining, medicine, education and research
(Kunz et al. 2011; Boyles et al. 2011; Kasso & Balakrishnan, 2013). Its projected that
ecological and economical losses will rise substantially if the continued population loss of bats
SCSU Biology
19
due to WNS is not combated in the coming years. If WNS continues to devastate these keystone
species, affected regions will suffer immense losses.
Researchers and other professionals have become aware of how detrimental WNS is.
However, some governing bodies and related policy makers, as well as most of the general
public, arent as privy. Bat advocacy will highlight the importance of this group of animals from
economic, ecological and natural history perspectives, motivate research and perhaps raise vital
funding thus aide new, innovative conservation practices. Considering the repercussions of a
loss of bats on this scale, it is wise to advocate in government, professional and public venues so
people will know what WNS is and what affects it will have, not only on our bat populations, but
in many aspects of peoples lives if its spread and subsequent mortality persist.
Ecological importance of bats
Agricultural pests of the arthropod variety have been known to upset farmlands all across
North America. The repercussions caused by such arthropods can destroy entire fields of crops
and leave farmers without food or income to support their families. Usually, pesticides are used
to combat such pests, but pesticides have unwanted effects, such as the contamination of foods,
human and non-human organisms and ecosystems (Aktar, Sengupta & Chowdhury, 2009). In
some cases contamination can cause death or other serious physiological complications in human
and non-human organisms, making pesticide use controversial and potentially hazardous to those
exposed (Aktar, Sengupta & Chowdhury, 2009). In addition to these unwanted effects, it has
been estimated that over 400 species of crop-pest insects have developed resistance to commonly
used pesticides, creating an even greater challenge in the realm of pest control (Kunz et al. 2011).
Enter the insectivorous bat. The bats plagued by WNS in North America are all
temperate, insectivorous species. They opportunistically feed on a variety of insects from
different environments including forests, grasslands, farmlands, etc. (Kunz et al. 2011). During
winter hibernation consumption slows, but activity and feeding still occur and are more common
in bats which hibernate in thermally unstable microhabitats (Dunbar, Whitaker, Jr. & Robbins,
2007). For context as to how many insects bats can eat, Kurta et al. (1989) mentions that during
the peak of lactation the little brown bat (M. lucifugus) needs to consume 9.9 g (>100% of its
SCSU Biology
20
body mass) of insects per night to account for energy expenditures and Whitaker (1995)
determined that a colony of 150 big brown bats (E. fuscus) in the Midwest can annually consume
approximately 1.3 million crop-pest insects. These numbers support what many people have
known for centuries, that insectivorous bats are a natural form of pest control.
Anthony and Kunz (1977) and Kurta et al. (1989) found that the little brown bat can
consume between 4 g 8 g of insects on an average night. The little brown bat is also one of the
most, if not the most affected bat in regards to WNS. As of 2010, Boyles & Willis extrapolated
this 4 g 8 g per night consumption rate during the active season to the estimated 500,000 bats
that died from WNS and estimated that between 330 and 660 metric tons of insects were no
longer being consumed in WNS regions. Now multiply that number by the estimated seven
million bats that have died as of spring 2015; between 4,620 and 9,240 metric tons of insects are
no longer being consumed in WNS regions. Imagine the increased use of pesticides in affected
regions to combat these insects. A job bats were performing naturally pre-WNS with no
unwanted side effects will now, in the post-WNS world, rely upon chemicals which have the
chance to devastate entire ecosystems if used improperly. The realization of the impacts WNS is
having on our natural world is enough to leave one speechless.
Economic importance of bats
After acknowledging the work of Anthony & Kunz (1977), Kurta et al. (1989), Whitaker
(1995) and Boyles & Willis (2010) its easy to understand the impacting role bats play in regards
to insect suppression. Economic estimates of the role bats play in pest control are still not fully
understood, however some published work has estimated the potential economic losses the
agricultural industry will suffer from the mass mortality of bats with WNS. Boyles et al. (2011)
estimate the value of bats to the agricultural industry to be approximately $22.9 billion per year.
This estimate was derived with the reduced costs of pesticide applications in mind, but it does
not include certain factors like predation of insects in forest ecosystems, or the secondary effects
of predation on insects (reducing the potential for pesticide resistant insects to thrive) (Boyles et
al. 2011). Imagine if WNS moves into the bread basket region of the United States. WNS has
been confirmed in the Midwest already and further spread could be detrimental to the
agricultural industry not to mention the bat species of the region. The $22.9 billion/year
SCSU Biology
21
estimated by Boyles et al. (2011) could easily be doubled over the span of a year if WNS were to
move into this region.
Bats as model species
Although its sometimes difficult to quantify the impact of bats to academia and research,
these flying mammals surely have an extraordinary value which needs to be recognized.
Numerous fields have experienced advances from the study of bats. One of the largest
contributions from the study of insectivorous bat species, some of which are now plagued by
WNS, to the educational and research worlds has been the study of bat echolocation and
locomotion (Kunz et al. 2011). The study of such functions has provided advances in fields
related to sonar systems, biomedical ultrasound, wireless communication and BATMAVS (batlike motorized aerial vehicles) (Kunz et al. 2011). People enjoy vilifying bats. If people were to
understand the influence bats, especially the insectivorous bats plagued by WNS, have on our
natural world, culture, education and technological advancements they would surely join the
countless researchers and wildlife enthusiasts who are desperately trying to understand and
combat WNS.
Conservation
As has been discussed, WNS is obliterating our insectivorous bat populations (Frick et al.
2010; Langwig et al. 2012; Verant et al. 2014). Researchers, organizations and enthusiasts have
been working non-stop to decrease spread of WNS. The U.S. Fish and Wildlife Service has
instituted a national plan to better manage WNS (U.S. Fish and Wildlife Service, 2011;
www.whitenosesyndrome.org/sites/default/files/white-nose_syndrome_national_plan_may_2011.pdf ).
The goal of this national plan is to form a coordinated response among federal and state agencies
in response to WNS. Some of the major components of the plan include surveillance,
management, research, communication, education and funding all of which will be instituted
locally, regionally and nationally. Individual states have also implemented their own plans to not
only gain a better understanding of WNS, but to also decrease its spread and provide much
needed conservation for afflicted bat species. In addition, conservation organizations are doing
SCSU Biology
22
their part too. Bat Conservation International assists in allocating funds and other resources to
help in studying and finding solutions to WNS.
A real world application to cure bats of WNS that can span twenty-six states has yet to
be perfected. Still, in the nine years since the discovery of WNS in North America, the scientific
community has learned much about the disease and produced copious amounts of data bringing
us ever closer to a viable solution. However, resources are still needed. The vigilance and
resolve of the professionals researching WNS needs to be instituted in the general public. One of
the hopes I have is to bring the WNS discussion to the forefront and create a sense of urgency
among the public. With more public involvement not only will more conservation efforts occur
and more funding be raised, but policy-makers hearing from their advocating constituents will
hopefully do more to allocate resources to vital research already in progress.
Discussions among the scientific community about the response to wildlife diseases are
in progress. Langwig et al. (2015B) have developed conservation responses, broken into four
stages, based on the pathogen invasion process. The first stage of the pathogen invasion process
is pre-arrival. Langwig et al. (2015B) stress that the first goal in this stage should be to
determine the threat posed by a given disease to the particular region(s); then precautions should
be taken and interventions implemented to reduce the probability of disease introduction.
Understanding potential pathways of introduction and implementing a rapid, proactive response
are vital in this stage. If necessary, biosecurity should be implemented to quarantine/restrict
access to areas at high risk for infection before a large scale outbreak occurs (i.e. cave & mine
closures in response to WNS) (Langwig et al. 2015B). Establishing communication and
spreading awareness are also crucial. It is of the upmost importance to have the public aware
and involved. Real-time reporting of potential cases is possible with public involvement and can
allow for a rapid response by agencies and researchers to assess potential issues.
Next is the invasion front stage in which a disease has arrived in a given region. The goal
of this stage should be to prevent pathogen establishment and minimize damage to affected
ecosystems (Langwig et al. 2015B). If the infected area is relatively small, eradication of the
disease may be possible, yet challenging. Reducing the further spread of the disease is
paramount and should be implemented whenever possible.
SCSU Biology
23
Invasion front is followed by the epidemic stage in which pathogen establishment has
occurred within a region. The main goal of this stage should focus on reducing impacts from the
disease on local populations and environments (Langwig et al. 2015B). Ways of reducing
impacts include, but are not limited to, vaccinations, treatment with chemical or biological
agents, habitat manipulation and augmenting demographic rates (reducing natural predation, etc.)
(Langwig et al. 2015B). Host resistance or tolerance may be facilitated from implementing the
above measures and could prove worthy once spread among the given population and potentially
passed onto subsequent generations; in the case of WNS, the work of Frank et al. (2014) and
Hoyt et al. (2015) shows great potential in this area of study.
The last stage is known as the established stage in which a given disease has created a
stronghold over a greater area and is currently afflicting local populations. In this stage the
protection and restoration of local populations is of the upmost importance, both of which should
be implemented in any reasonable way (Langwig et al. 2015B). Furthermore, four additional
actions are of great importance among all of the aforementioned stages. The actions include: 1.)
Risk assessment among management actions, in which those in management positions
understand potential risk, try to avoid unnecessary risk, and weigh potential risk against inaction.
2.) Develop a plan of action, in which responses can be enacted as soon as possible. 3.) Public
engagement, in which an increase of involvement from the public can help inhibit disease spread
as well as raise funds which could be of great use to research activities and other projects. 4.)
Management needs to be willing to be adaptive, vigilant and forthcoming with information and
strategies; these traits will promote current and future works through open communication
(Langwig et al. 2015B).
Our struggle with WNS is currently in the latter stages of the pathogen invasion process.
I urge, as many before have, a dire need for a responsible and proactive approach to extinguish
WNS. Waiting and dealing with the aftermath of WNS will not work, for then it will be too late,
and we will have lost. Its important for individuals to take steps now to reduce instances of
WNS and to save our local bats. Agencies, researchers, organizations and other professionals
have been taking steps to confront WNS. I propose additional support from the non-scientific
community is drastically needed. One major step these individuals can achieve is to report
SCSU Biology
24
unusual bat behavior in affected regions. Abnormal, daytime flying from December to March
when bats should be hibernating can be indicative of WNS and should be reported to state
environmental agencies immediately (Cryan et al. 2010). By reporting such incidences,
communication is kept open as to new potential WNS occurrences and agencies can direct a
more rapid, real-time response.
Individuals also want to avoid potentially spreading Pd. As discussed earlier, evidence
supports that Pd and WNS were introduced from Europe, most likely inadvertently via humans
(Warnecke et al. 2012; Lorch et al. 2013). Pd has also been found to survive in hibernacula, on
clothes and equipment given the right environmental conditions making it absolutely necessary
that cavers and others do their best to avoid contact with Pd (Turner, Reeder & Coleman, 2011;
Lorch et al. 2013; Hoyt et al. 2014). An individual can avoid contact with the fungus by sporting
protective outerwear when visiting hibernacula, decontaminating after visiting and if possible,
avoid infected hibernacula all together. A national WNS decontamination protocol was
developed by multiple agencies which should prove useful to field researchers and other wildlife
enthusiasts and can be found on WhiteNoseSyndrome.Org (U.S. Fish and Wildlife Service, 2012;
www.whitenosesyndrome.org/sites/default/files/resource/national_wns_revise_final_6.25.12.pdf ).
With the ever increasing manifestations of infected hibernacula, artificial roosting

locations would be most advantageous for bats fighting for survival in WNS regions. I
recommend individuals post bat houses if applicable. A bat house provides a sustainable and
clean location for bats to roost and live. Information on posting bat houses can be found at
BatCon.Org (Tuttle, Kiser & Kiser, 2013; www.batcon.org/pdfs/BHBuildersHdbk13_Online.pdf). In
addition to smaller bat houses, abandoned buildings or barns also work well as artificial roosts
and if ones situations allows, the presence of bats in such outbuildings should be welcomed. Bat
houses have recently come to the campus of Southern Connecticut State University in New
Haven, CT to promote long-term research and most importantly aid bat conservation in one of
the first states where WNS was discovered. Its recognized these local conservation efforts are
small compared to the large scale nature of WNS, but if dozens of individuals were to become
involved across multiple states the likelihood of persistence by some bat colonies would
increase.
SCSU Biology
25
Possibly the biggest step individuals can take in the fight against WNS is to educate
others and help increase awareness. Its vital for everyone who reads this review to go out of
their way to discuss WNS with someone who was previously unaware. Think of the resources
and assistance which could come to fruition if more members of the general public knew of
WNS and the forecasted outcomes of the disease.
In closing
WNS is a vile disease. As Ive discussed the past, present and future of WNS in bats its
easy to see how troublesome WNS is on so many fronts; yet, some hope has been seen in recent
publications which aspire to answer the question thats plagued researchers from the start, the
question of wondering how to fix this calamity. The scientific community is so far from where
we were in 2006, our knowledge of WNS has increased exponentially, but many unanswered
questions remain and much work is left to be done. This review has covered works from nine
years of WNS research and brought together many testable hypotheses. I hope this compilation
brings a new viewpoint to data which may have been previously overlooked and upon
reinvestigation, could now lead to new research, conservation and species management
opportunities. The pursuance of scientific work throughout the remainder of this decade could
very well provide us with an answer of how to remedy WNS, bring our bats back from the brink
of extinction, and preserve our natural history. Certainly, the scientific community embraces the
challenge and looks forward to the opportunity.
Acknowledgements
Many thanks to those who have helped support this research throughout all of its phases. Your assistances
and enthusiasms are deeply appreciated.
Dr. Miranda Dunbar

Biology Department, Southern Connecticut State University
Student Government Association, Southern Connecticut State University
David & Susan Wisniewski
SCSU Biology
26
References
Aktar, M. W., Sengupta, D., & Chowdhury, A. (2009). Impact of pesticides use in agriculture: their
benefits and hazards. Interdisciplinary Toxicology, 2(1), 1-12. http://dx.doi.org/10.2478/v10102-0090001-7
Alves, D. M., Terribile, L. C., & Brito, D. (2014). The Potential Impact of White-Nose Syndrome on
the Conservation Status of North American Bats. PLoS ONE, 9(9).
http://dx.doi.org/10.1371/journal.pone.0107395
Anthony, E. L.P., & Kunz, T. H. (1977). Feeding strategies of the little brown bat, myotis lucifugus, in
southern new hampshire. Ecology, 58(4), 775-786.
Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L., & McCracken, G. F. (2015). Molecular
Detection of the Causative Agent of White-nose Syndrome on Rafinesque's Big-eared Bats
(Corynorhinus rafinesquii) and Two Species of Migratory Bats in the Southeastern USA. Journal of
Wildlife Diseases, 51(2), 519-522. http://dx.doi.org/10.7589/2014-08-202
SCSU Biology
27
Blehert, D. S., Hicks, A. C., Behr, M., Meteyer, C. U., Berlowski-Zier, B. M., Buckles, E. L., . . .
Stone, W. B. (2009). Bat White-Nose Syndrome: An Emerging Fungal Pathogen? Science, 323(5911),
227. http://dx.doi.org/10.1126/science.1163874
Boyles, J. G., Cryan, P. M., McCracken, G. F., & Kunz, T. H. (2011). Economic Importance of Bats in
Agriculture. Science, 332(6025), 41-42. http://dx.doi.org/10.1126/science.1201366
Boyles, J. G., Dunbar, M. B., & Whitaker, J. O., Jr. (2006). Activity following arousal in winter in
North American vespertilionid bats. Mammal Review, 36(4), 267-280.
http://dx.doi.org/10.1111/j.1365-2907.2006.00095.x
Boyles, J. G., & Willis, C. K.R. (2010). Could localized warm areas inside cold caves reduce mortality
of hibernating bats affected by white-nose syndrome? Read More:
http://www.esajournals.org/doi/abs/10.1890/080187. Frontiers in Ecology and the Environment, 8(2),
92-98. http://dx.doi.org/10.1890/080187
Brownlee-Bouboulis, S. A., & Reeder, D. M. (2013). White-nose syndrome-affected little brown
myotis (Myotis lucifugus) increase grooming and other active behaviors during arousals from
hibernation. Journal of Wildlife Diseases, 49(4), 850-859. http://dx.doi.org/10.7589/2012-10-242
Chaturvedi, S., Rudd, R. J., Davis, A., Victor, T. R., Li, X., Appler, K. A., . . . Chaturvedi, V. (2011).
Rapid Real-Time PCR Assay for Culture and Tissue Identification of Geomyces destructans: the
Etiologic Agent of Bat Geomycosis (White Nose Syndrome). Mycopathologia, 172(4), 247-256.
http://dx.doi.org/10.1007/s11046-011-9435-5
Chaturvedi, V., Springer, D. J., Behr, M. J., Ramani, R., Li, X., Peck, M. K., . . . Chaturvedi, S. (2010).
Morphological and Molecular Characterizations of Psychrophilic Fungus Geomyces destructans from
New York Bats with White Nose Syndrome (WNS). PLoS ONE, 5(5).
http://dx.doi.org/10.1371/journal.pone.0010783
Cryan, P. M., Meteyer, C. U., Blehert, D. S., Lorch, J. M., Reeder, D. M., Turner, G. G., . . . Castle, K.
T. (2013). Electrolyte depletion in white-nose syndrome bats. Journal of Wildlife Diseases, 49(2), 398402. http://dx.doi.org/10.7589/2012-04-121
Cryan, P. M., Meteyer, C. U., Boyles, J. G., & Blehert, D. S. (2010). Wing pathology of white-nose
syndrome in bats suggests life-threatening disruption of physiology. BMC Biology, 8(135).
http://dx.doi.org/10.1186/1741-7007-8-135
Dunbar, M. B., Whitaker, J. O., Jr., & Robbins, L. W. (2007). Winter feeding by bats in Missouri. Acta
Chiropterologica, 9(1), 305-310. http://dx.doi.org/10.3161/17335329(2007)9[305:WFBBIM]2.0.CO;2
Frank, C. L., Michalski, A., McDonough, A. A., Rahimian, M., Rudd, R. J., & Herzog, C. (2014). The
Resistance of a North American Bat Species (Eptesicus fuscus) to White-Nose Syndrome (WNS).
PLoS ONE, 9(12). http://dx.doi.org/10.1371/journal.pone.0113958
Frick, W. F., Pollack, J. F., Hicks, A. C., Langwig, K. E., Reynolds, D. S., Turner, G. G., . . . Kunz, T.
H. (2010). An Emerging Disease Causes Regional Population Collapse of a Common North American
Bat Species. Science, 329(679), 679-682. http://dx.doi.org/10.1126/science.1188594
SCSU Biology
28
Gargas, A., Trest, M. T., Christensen, M., Volk, T. J., & Blehert, D. S. (2009). Geomyces destructans
sp. nov. associated with bat white-nose syndrome. Mycotaxon, 108, 147-154.
http://dx.doi.org/10.5248/108.147
Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor.
The Annual Review of Physiology, 66, 239-274.
http://dx.doi.org/10.1146/annurev.physiol.66.032102.115105
Hendricks, P., & Hendricks, L. M. (2010). Water Acquisition During Daylight by Free-Ranging
Myotis Bats. Northwestern Naturalist, 91(3), 336-338. http://dx.doi.org/10.1898/NWN10-12.1
Hoyt, J. R., Cheng, T. L., Langwig, K. E., Hee, M. M., Frick, W. F., & Kilpatrick, A. M. (2015).
Bacteria Isolated from Bats Inhibit the Growth of Pseudogymnoascus destructans, the Causative Agent
of White-Nose Syndrome. PLoS ONE, 10(4). http://dx.doi.org/10.1371/journal.pone.0121329
Hoyt, J. R., Langwig, K. E., Okoniewski, J., Frick, W. F., Stone, W. B., & Kilpatrick, A. M. (2014).
Long-Term Persistence of Pseudogymnoascus destructans, the Causative Agent of White-Nose
Syndrome, in the Absence of Bats. EcoHealth. http://dx.doi.org/10.1007/s10393-014-0981-4
Johnson, J.S., Reeder, D.M., Lilley, T.M., Czirjak, G.A., Voigt, C.C., McMichael III, J.W., Field,
K.A. (2015). Antibodies to Pseudogymnoascus destructans are not sufficient for protection against
white-nose syndrome. Ecology and Evolution. http://dx.doi.org/10.1002/ece3.1502
Kasso, M., & Balakrishnan, M. (2013). Ecological and Economic Importance of Bats (Order
Chiroptera). ISRN Biodiversity. http://dx.doi.org/10.1155/2013/187415
Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., & Fleming, T. (2011). Ecosystem services
provided by bats. Annals of the New York Academy of Science, 1223, 1-38.
http://dx.doi.org/10.1111/j.1749-6632.2011.06004.x
Kurta, A., Bell, G. P., Nagy, K. A., & Kunz, T. H. (1989). Energetics of pregnancy and lactation in
free-ranging little brown bats (myotis lucifugus). Physiological Zoology, 62(3), 804-818.
Langwig, K. E., Frick, W. F., Bried, J. T., Hicks, A. C., Kunz, T. H., & Kilpatrick, A. M. (2012).
Sociality, density-dependence and microclimates determine the persistence of populations suffering
from a novel fungal disease, white-nose syndrome. Ecology Letters, 15, 1050-1057.
http://dx.doi.org/10.1111/j.1461-0248.2012.01829.x
Langwig, K. E., Frick, W. F., Reynolds, R., Parise, K. L., Drees, K. P., Hoyt, J. R., . . . Kilpatrick, A.
M. (2015A). Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose
syndrome. Royal Society Proceedings B, 282(1799). http://dx.doi.org/10.1098/rspb.2014.2335
Langwig, K. E., Voyles, J., Wilber, M. Q., Frick, W. F., Murray, K. A., Bolker, B. M., . . . Kilpatrick,
A. M. (2015B). Context-dependent conservation responses to emerging wildlife diseases. Frontiers in
Ecology and the Environment, 13(4), 195-202. http://dx.doi.org/10.1890/140241
Lorch, J. M., Gargas, A., Meteyer, C. U., Berlowski-Zier, B. M., Green, D. E., Shearn-Bochsler,
V., . . . Blehert, D. S. (2010). Rapid Polymerase Chain Reaction Diagnosis of White-Nose Syndrome
in Bats. Journal of Veterinary Diagnostic Investigation, 22(2), 224-230.
http://dx.doi.org/10.1177/104063871002200208
SCSU Biology
29
Lorch, J. M., Meteyer, C. U., Behr, M. J., Boyles, J. G., Cryan, P. M., Hicks, A. C., . . . Blehert, D. S.
(2011). Experimental infection of bats with Geomyces destructans causes white-nose syndrome.
Nature, 480(7377), 376-378. http://dx.doi.org/10.1038/nature10590
Lorch, J. M., Minnis, A. M., Meteyer, C. U., Redell, J. A., White, J. P., Kaarakka, H. M., . . . Blehert,
D. S. (2015). The fungus Trichophyton redellii sp. nov. causes skin infections that resemble whitenose syndrome of hibernating bats. Journal of Wildlife Diseases, 51(1), 36-47.
http://dx.doi.org/10.7589/2014-05-134
Lorch, J. M., Muller, L. K., Russell, R. E., O'Connor, M., Lindner, D. L., & Blehert, D. S. (2013).
Distribution and Environmental Persistence of the Causative Agent of White-Nose Syndrome,
Geomyces destructans, in Bat Hibernacula of the Eastern United States. Applied and Environmental
Microbiology, 79(4), 1293-1301. http://dx.doi.org/10.1128/AEM.02939-12
McAlpine, D. F., Vanderwolf, K. J., Forbes, G. J., & Malloch, D. (2011). Consumption of Bats
(Myotis spp.) by Raccoons (Procyon lotor) During an Outbreak of White-Nose Syndrome in New
Brunswick, Canada: Implications for Estimates of Bat Mortality. The Canadian Field-Naturalist,
125(3), 257-260.
Meteyer, C. U., Buckles, E. L., Blehert, D. S., Hicks, A. C., Green, D. E., Shearn-Bochsler, V., . . .
Behr, M. J. (2009). Histopathologic Criteria to Confirm White-nose Syndrome in Bats. Journal of
Veterinary Diagnostic Investigation, 21(4), 411-414. http://dx.doi.org/10.1177/104063870902100401
Meteyer, C. U., Valent, M., Kashmer, J., Buckles, E. L., Lorch, J. M., Blehert, D. S., . . . Ballmann, A.
E. (2011). Recovery of little brown myotis (Myotis lucifugus) from natural infection with Geomyces
destructans, white-nose syndrome. Journal of Wildlife Diseases, 47(3), 618-626.
Minnis, A. M., & Lindner, D. L. (2013). Phylogenetic evaluation of Geomyces and allies reveals no
close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North
America. Fungal Biology, 117(9), 638-649. http://dx.doi.org/10.1016/j.funbio.2013.07.001
Muller, L. K., Lorch, J. M., Lindner, D. L., O'Connor, M., Gargas, A., & Blehert, D. S. (2013). Bat
white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic
spacer region of Geomyces destructans. Mycologia, 105(2), 253-259. http://dx.doi.org/10.3852/12-242
National White-Nose Syndrome Decontamination Protocol. (2012, June).Digital copy can be retrieved
from: https://www.whitenosesyndrome.org/sites/default/files/resource/national_wns_revise_final_6.25
.12.pdf
Rainey, P. B., & Travisano, M. (1998). Adaptive radiation in a heterogeneous environment. Nature,
394, 69-72. http://dx.doi.org/10.1038/27900
Reeder, D. M., Frank, C. L., Turner, G. G., Meteyer, C. U., Kurta, A., Britzke, E. R., . . . Blehert, D. S.
(2012). Frequent Arousal from Hibernation Linked to Severity of Infection and Mortality in Bats with
White-Nose Syndrome. PLoS ONE, 7(6). http://dx.doi.org/10.1371/journal.pone.0038920
Reichard, J. D., Fuller, N. W., Bennett, A. B., Darling, S. R., Moore, M. S., Langwig, K. E., . . .
Reynolds, D. S. (2014). Interannual Survival of Myotis lucifugus (Chiroptera: Vespertilionidae) near
SCSU Biology
30
the Epicenter of White-Nose Syndrome. Northeastern Naturalist, 21(4), N56-N59.

http://dx.doi.org/10.1656/045.021.0410
Reichard, J. D., & Kunz, T. H. (2009). White-nose syndrome inflicts lasting injuries to the wings of
little brown myotis (Myotis lucifugus). Acta Chiropterologica, 11(2), 457-464.
http://dx.doi.org/10.3161/150811009X485684
Thomas, D. W., Dorais, M., & Bergeron, J.-M. (1990). Winter Energy Budgets and Cost of Arousals
for Hibernating Little Brown Bats, Myotis lucifugus. Journal of Mammalogy, 71(3), 475-479.
Turner, G. G., Meteyer, C. U., Barton, H., Gumbs, J. F., Reeder, D. M., Overton, B., . . . Blehert, D. S.
(2014). Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions
indicative of white-nose syndrome. Journal of Wildlife Diseases, 50(3).
http://dx.doi.org/10.7589/2014-03-058
Turner, G. G., Reeder, D. M., & Coleman, J. T.H. (2011). A five-year assessment of mortality and
geographic spread of white-nose syndrome in North American bats and a look to the future. Bat
Research News, 52(2), 13-27.
Turner, J. M., Warnecke, L., Wilcox, A., Baloun, D., Bollinger, T. K., Misra, V., & Willis, C. K.R.
(2015). Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose
syndrome. Physiology & Behavior, 140, 71-78. http://dx.doi.org/10.1016/j.physbeh.2014.12.013
Tuttle, M. D., Kiser, M., & Kiser, S. (2013). The bat house builder's book. Bat Conservation
International. Digital copy can be retrieved
from: www.batcon.org/pdfs/BHBuildersHdbk13_Online.pdf
U.S. Fish and Wildlife Service. (2011, May). A National Plan for Assisting States, Federal Agencies,
and Tribes in Managing White-Nose Syndrome in Bats. Digital copy can be retrieved
from: https://www.whitenosesyndrome.org/sites/default/files/whitenose_syndrome_national_plan_may_2011.pdf
U.S. Fish and Wildlife Service. (2012, January 17). North American bat death toll exceeds 5.5 million
from white-nose syndrome.
U.S. Fish and Wildlife Service. (2014, August). White-nose syndrome: The devastating disease of
hibernating bats in North America.
Verant, M. L., Boyles, J. G., Waldrep, W., Jr., Wibbelt, G., & Blehert, D. S. (2012). TemperatureDependent Growth of Geomyces destructans, the Fungus That Causes Bat White-Nose Syndrome.
PLoS ONE, 7(9). http://dx.doi.org/10.1371/journal.pone.0046280
Verant, M. L., Meteyer, C. U., Speakman, J. R., Cryan, P. M., Lorch, J. M., & Blehert, D. S. (2014).
White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC
Physiology, 14(10). http://dx.doi.org/10.1186/s12899-014-0010-4
Warnecke, L., Turner, J. M., Bollinger, T. K., Lorch, J. M., Misra, V., Cryan, P. M., . . . Willis, C. K.R.
(2012). Inoculation of bats with European Geomyces destructans supports the novel pathogen
hypothesis for the origin of white-nose syndrome. Proceedings of the National Academy of Sciences
of the United States, 109(18), 6999-7003. http://dx.doi.org/10.1073/pnas.1200374109
SCSU Biology
31
Warnecke, L., Turner, J. M., Bollinger, T. K., Misra, V., Cryan, P. M., Blehert, D. S., . . . Willis, C.
K.R. (2013). Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing
damage to mortality. Royal Society Biology Letters, 9(4). http://dx.doi.org/10.1098/rsbl.2013.0177
Whitaker, J. O., Jr. (1995). Food of the Big Brown Bat Eptesicus fuscus from Maternity Colonies in
Indiana and Illinois. American Midland Naturalist, 134(2), 346-360.
Wibbelt, G., Kurth, A., Hellmann, D., Weishaar, M., Barlow, A., Veith, M., . . . Blehert, D. S. (2010).
White-Nose Syndrome Fungus (Geomyces destructans) in Bats, Europe. Emerging Infecitous
Diseases, 16(8), 1237-1242. http://dx.doi.org/10.3201/eid1608.100002
Wilcox, A., Warnecke, L., Turner, J. M., McGuire, L. P., Jameson, J. W., Misra, V., . . . Willis, C. K.R.
(2014). Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that
causes white-nose syndrome. Animal Behaviour, 88, 157-164.
http://dx.doi.org/10.1016/j.anbehav.2013.11.026
SCSU Biology
32

White-Nose Syndrome in Bats by Chris Wisniewski

Hochgeladen von

Dokumentinformationen

Originaltitel

Copyright

Verfügbare Formate

Dieses Dokument teilen

Dokument teilen oder einbetten

Freigabeoptionen

Stufen Sie dieses Dokument als nützlich ein?

Sind diese Inhalte unangemessen?

Copyright:

Verfügbare Formate

White-Nose Syndrome in Bats by Chris Wisniewski

Hochgeladen von

Copyright:

Verfügbare Formate

The Past, Present and Future of White-Nose

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

Furthermore, Turner et al. (2015) provide evidence that synchronization of arousals

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

With the ever increasing manifestations of infected hibernacula, artificial roosting

The Past, Present and Future of White-Nose Syndrome in Bats

Dr. Miranda Dunbar

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

The Past, Present and Future of White-Nose Syndrome in Bats

the Epicenter of White-Nose Syndrome. Northeastern Naturalist, 21(4), N56-N59.

The Past, Present and Future of White-Nose Syndrome in Bats

Das könnte Ihnen auch gefallen