White-nose syndrome in bats by Chris Wisniewski

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    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 wasrecently discovered in New York. The fungus colonies and deteriorates the tissues of hibernating bats

    leading to degradation of water balance! fre"uent arousals from tor#or! accelerated fat store de#letion and

    eventually death. $onsidering the e%ceedingly high mortality rate (& ') and ra#id s#read! which as of 

    s#ring *+, WNS has been confirmed in twenty-si% states and five $anadian #rovinces! its #roected that

    once common bat s#ecies will soon become e%tinct from affected North /merican regions unless new

     breakthroughs in research and intervening conservation efforts occur. These insectivorous bats #lay a

    crucial role in #est control. 0t has been suggested if WNS continues to devastate these keystone s#ecies!

    the agricultural industry will suffer great losses.

    Christopher D. Wisnies!i

    Southern Connecticut State "ni#ersity

    Department of Bio$o%y

    Sprin% &'()

    Tab$e of Contents

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    The 1ast! 1resent and 2uture of White-Nose Syndrome in 3ats   1

    0ntroduction4444444444444444....##. *-5

     Pseudogymnoascus destructans.................................... ##. 5-6

     Pd introduction to North /merica44444444.##. 6-,

     Pd  transmission444444444444444..##. ,-7

     Pd  incubation44444444444444...4..#. 7

    WNS detection444444444444444...##. 7-+

     Pd infection4444444444444444....##. +-++

    1otential recovery from WNS444444444...##. ++-+*

    1hysiological disturbances associated with WNS4....##. +*-+5

    3ehavioral disturbances associated with WNS444.##. +5-+,

    1o#ulation devastation444444444444...##. +,-+8

    9ooking forward44444444444444....##. +8-*

    Why bats are im#ortant44444444444.4.#. *

    :cological im#ortance of bats444444444...##. *-*+

    :conomic im#ortance of bats4444444444##. *+-**

    3ats as model s#ecies4444444444444#. **

    $onservation444444444444444.4.##. **-*;

    0n closing44444444444444444...#. *;

    /cknowledgements4444444444444...#. *8

    owe $averns in

    u#state New York in *; (3lehert et al. *'). The #sychro#hilic fungus which causes WNS!

     Pseudogymnoascus destructans ( Pd ) (3lehert et al. *'? @argas et al. *'? 9orch et al. *++?

    Warnecke et al. *+*? Ainnis B 9indner! *+5)! develo#s on bats as a filamentous white growth

    on wings! mules and ears. While fungal conidia growth around the mule of bats is one of the

    most cons#icuous signs of WNS! bat wing membranes are often the most afflicted regions by Pd  

    S$S= 3iology

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    The 1ast! 1resent and 2uture of White-Nose Syndrome in 3ats   2

    due to this region containing the largest surface area of e%#osed skin (Aeteyer et al. *'? $ryan

    et al. *+).  Pd  s#ores colonie these su#erficial tissues and begin to deteriorate the e#idermis

    and dermis (Aeteyer et al. *'? $ryan et al. *+). This destruction allows for further

    e%#ansion of the fungal colony into healthy! su#erficial and dee# tissue leading to a #lethora of

     #hysiological and behavioral disru#tions which ultimately cause mortality ($ryan et al. *+?

    Turner!

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    Service! *+6). These high mortality rates over re#eated hibernation cycles have led to massive

     #o#ulation declines of once common native bat s#ecies.

    The devastation of North /merican bat s#ecies by WNS is un#recedented. This is thelargest wildlife e#idemic ever recorded and it #oses a threat of regional e%tinction to multi#le bat

    s#ecies in the coming years (2rick et al. *+? 9angwig et al. *+*). This review aims to bring

    together available data on WNS in North /merica into one convenient re#ort in ho#es to

    generate new directions for habitatFs#ecies management #ractices as well as aid conservation

    strategies and future research. /s 0 advocate the dire need for conservation and continued

    research efforts! 0 ho#e to increase awareness! educate others! and encourage more individuals to

     become involved to hel# bring our local bat s#ecies back from the brink of e%tinction! thus

     #reserving our natural history.

     Pseudogymnoascus destructans

    The causative agent of white-nose syndrome (WNS)! Pseudogymnoascus destructans

    ( Pd ? formerly classified Geomyces)! is a #sychro#hilic fungus found to grow between G-*G$

    (3lehert et al. *'? @argas et al. *'? 9orch et al. *++? Warnecke et al. *+*? Cerant et al.

    *+*? Ainnis B 9indner! *+5). While Pd  grows o#timally between +*.,G-+,.7G$! it has been

    found Pd  cannot grow at tem#eratures as low as -+G$ or as high as *,G$! with +'G-+'.7G$ being

    the a##ro%imate u##er growthFtem#erature limit (3lehert et al. *'? $haturvedi et al. *+?

    Cerant et al. *+*).  Pd re#roduces ase%ually and is characteried by the #resence of coloniing

    fungal hy#hae with distinctive asymmetrically curved conidia (3lehert et al. *'? @argas et al.

    *'). @ross identification of Pd  on bats is #ossible due to the #resence of white filamentous

    growth a##earing on wings! mules and ears (3lehert et al. *'? @argas et al. *') or as a

    filmy substance on wings (Aeteyer et al. *'). 1erha#s the most indicativeFcharacteristic sign

    of the disease on bats in the field is the #resence of white conidia growth on the mule! which

    also contributed to the creation of the Hwhite-noseI designation of the disease (3lehert et al.

    *'? $ryan et al. *+).

     Pd  introduction to North America

    S$S= 3iology

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    /s of s#ring *+,! WNS has been confirmed in hibernacula across twenty-si% states and

    five $anadian #rovinces (=S 2ish B Wildlife Service! *+6). 0n addition! Pd is also currently

     #resent in two additional states where the disease has yet to be confirmed in bats. >ow did Pd

    and WNS come to be in North /mericaJ Cia e%#erimentation! North /merican bat s#ecies were

    shown to be e"ually susce#tible to strains of Pd from both North /merica and :uro#e. This

    allowed Warnecke et al. (*+*) to su##ort the novel #athogen hy#othesis in which it is believed

    that Pd  was accidentally introduced from :uro#e where Pd and WNS are #resent! but without the

    associated mass mortality #resent in North /merican bat s#ecies. The introduction of Pd on

    naKve #o#ulations of North /merican bats is believed to be the driving force behind the

    subse"uent mass mortality (Warnecke et al. *+*). 0n fact! Pd remained overlooked on the bats

    of :uro#e until the recent e%#losion of WNS in North /merica nine years ago (Warnecke et al.*+*). Warnecke et al. (*+*) suggest that bats with Pd  in :uro#e dis#lay more well-ada#ted

     #hysiological and behavioral res#onses com#ared to the disorderly res#onses of North /merican

    s#ecies? this accounts for the absence of mass mortality of bats in :uro#e com#ared to North

    /merica. This work also su##orts Wibbelt et al. (*+) who mention thatD +.) Pd  may have been

     #resent and coevolved with :uro#ean bats leading to an immunological or behavioral resistance

    or tolerance to form in regards to the fungus! or that *.) Aicrobial flora #resent on bats or in

    hibernacula in :uro#e may have coevolved with Pd  leading to its non#athogenic role. 3oth

    suggestions could e%#lain why there is such a contrast in mortality cases between the two

    continents. 0t would be interesting to determine the effects of the North /merican strain of Pd  on

    :uro#ean bat s#ecies. 2urther testing could #otentially fill ga#s about the differences in

     #athogenicity between the two continents and hel# to su##ort an e%#lanation as to why :uro#ean

     bats are ca#able of living with the fungus. 2urthermore! 0 hy#othesie the culturing of the skin

    microbiome of :uro#ean bats may #rovide useful data in regards to #otential naturally occurring

    microbes which may #ossess antifungal #ro#erties similar to the North /merican bats in the >oyt

    et al. (*+,) study which is discussed later. This could e%#lain the lack of mortality in :uro#ean

     bats and #rovide droves of useful data which could have large im#lications for North /merican

     bats! given sufficient testing.

    The novel #athogen hy#othesis was further su##orted by 9orch et al. (*+5) who were

    able to dis#rove the hy#othesis that a less virulent strain of Pd  was always #resent in North

    S$S= 3iology

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    /merica! until a mutation and subse"uent increasing #athogenicity emerged leading to the

    current WNS outbreak. 9orch et al. (*+5) screened collected sediment sam#les from

    hibernacula both inside and outside of WNS affected regions and isolated LN/ from these

    sam#les. Ef the *', sediment sam#les screened! +8 were #ositive for Pd ! all of which came

    from within WNS affected regions? no Pd  was discovered in sam#les from non-affected regions

    (9orch et al. *+5). These findings #rovide evidence against an endemic strain of Pd  being

     #resent in North /merica #rior to the WNS outbreak and instead su##ort the novel #athogen

    hy#othesis suggesting Pd  was accidently introduced from :uro#e to North /merica.

     Pd transmission 

    /lthough #ossible modes of transmission for WNS are still being investigated! some have been well su##orted. WNS can be transmitted among bats via direct contact between individuals

    or via direct contact between bats and hibernaculaFenvironment (9orch et al. *++? 9orch et al.

    *+5? >oyt et al. *+6? 3ernard et al. *+,). Some early indications for bat to bat transmission

    of WNS comes from documentation of infection at multi#le sites in 1ennsylvania! which were

    initially shielded from humans and #o#ulation management before WNS was detected! still! the

    resulting infection was hy#othesied to have been introduced by infected bats (Turner!

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     Pd can also be transmitted via direct contact between bats and hibernaculaFenvironment.

    0t is understood that Pd has the ability to survive in hibernacula in the absence of bats serving as

    a reservoir for new infections. 9orch et al. (*+5) detected live Pd  in 8 out of +6 hibernacula

    sites during the late summer when bat #o#ulation densities were low. 0n this same study!

    sediment sam#les from the sites were tested and live Pd was found in sites where bats had not

     been #resent from a few months! to u# to two years! indicating long term #ersistence of the

    fungus is #ossible given suitable hibernacula conditions. >oyt et al. (*+6) also showed Pd  can

     #ersist in environments in the absence of a host. They isolated Pd  from bats! and stored #ure

    isolates in an incubator at ,G$ and 5-6 relative humidity for ,-; years. /fter this time! Pd  

    from si% of the nine original isolates grew on new media! confirming enough viable conidia

    remained over this e%tended #eriod of time. This demonstrates that even after long termlaboratory storage Pd  can grow in the absence of a host! suggesting that environments

    contaminated with Pd  conidia can continually infect bats. /dditionally! its suggested that the

     #resence of other microbes! inducing com#etition! and humidity may affect Pd  survival in

    natural conditions (>oyt et al. *+6).

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    the e%#eriment all showed consistent concentrations of Pd  which varied with the seasons.

    9angwig et al. (*+,/) found no su##ort for the hy#othesis that birth #ulses drive seasonality.

    They found the #revalence of Pd dro##ed during the summer months when births occurred. 0t

    was also found that seasonal changes in habitat use showed low transmission and infection

    intensity until #rolonged tor#or was em#loyed by bats! meaning another factor had to have been

    driving seasonality (9angwig et al. *+,/). 9angwig et al. (*+,/) found that hibernation was

    the dominant factor driving transmission and #athogenicity. 1rolonged tor#or brought about

    close to + of individuals becoming infected. $ontact rates during this time are unknown! but

    they could influence transmission. 0t is understood that the body tem#erature of bats during this

    time! also within the range re"uired by Pd to thrive! is what allows for such an e%#losion of

     #athogen growth and transmission (9angwig et al. *+,/). The influence of Pd on hibernating bats during this time is ma%imied? as when infection #eaks! #o#ulations are usually at their

    lowest concentrations which brings about the most drastic im#lications of WNS. Everall! the

    seasonal timing (winter hibernation) of transmission and #athogenicity allow for the most

    damage to be dealt to bat s#ecies! while at the same time! seasonal timing affects  Pd  s#read due

    to the #eriods of low mobility demonstrated by the hibernating bat hosts (9angwig et al. *+,/).

    The researchers hy#othesied that if transmission rates were com#arable in autumn as they are

    during winter! that Pd s#read and infectiousness would be much higher than we currently witness

    (9angwig et al. *+,/).

    0t should also be noted that Pd  can be transmitted via humans who come in contact with

    either bats or hibernacula.  Pd conidia can be trans#orted on e"ui#ment and clothes! increasing

    the likelihood of Pd s#read and thus WNS occurrence (Turner! oyt et

    al. *+6). 0n fact! this form of transmission is conducive with the novel #athogen hy#othesis and

    is believed to be how Pd and WNS were introduced to North /merica. >oyt et al. (*+6)

    suggested that Pd  may be able to survive outside of hibernacula (on e"ui#ment! clothes! etc.) if

    such materials are stored in cool dry #laces.

     Pd  incubation

    9orch et al. (*++) were able to "uantify the incubation #eriod of Pd  in bats! how much

    time #assed until WNS became characteristically #resent and how long until mass mortality of

    S$S= 3iology

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     #o#ulations took #lace. Through e%#erimental infection with Pd, and subse"uent histological

    e%amination they found that inoculated bats develo#ed diagnostic lesions for WNS 75 days after

     being treated and all were #ositive for WNS when the trial was terminated at the +* day mark.

    9arge scale mortality among infected bats was not witnessed! but this was due to the short term

    of their e%#eriment.  The study was able to su##ort data on the develo#ment of WNS in wild

     bats. 0n wild #o#ulations! WNS lesions are initially detected in late Se#tember #rior to the onset

    of long term hibernation. Aass mortality can begin in late Manuary and #eak in Aarch (9orch et

    al. *++). This demonstrates that mortality from WNS doesnt begin until a##ro%imately +*

    days from when bats begin long term! winter hibernation in which cold tem#eratures necessary

    for Pd  to thrive occur! also mortality #eaks at about +7 days? this accounts for why mass

    mortality wasnt observed in their e%#eriment which was terminated at the +* day mark beforethe disease could #rogress further to induce mortality.

    WNS detection

    White fungal growth found on the mules! wings and ears of bats are characteristic signs

    of WNS (3lehert et al. *'? @argas et al. *'). These gross fungal lesions can be indicative of 

    WNS? however they dont always lead to a diagnosis. @ross lesions can be damaged or lost

    when bats are #re#ared and trans#orted from hibernacula to laboratory settings! making further

    e%amination im#erative for confirmation of the disease (Aeteyer et al. *').

    >isto#athologic e%amination is considered the most effective way to confirm WNS in an

    infected organism (Aeteyer et al. *'). /lterations in skin of infected bats can include #atches

    of rough skin! loss of sheen on glabrous skin! irregular #igmentation and tears in wing

    membranes (Aeteyer et al. *'). Through microsco#y! detection of Pd hy#hae and conidia on

    infected tissue is #ossible. The surface area of tissue needs to be ma%imied! which can be

    accom#lished by fi%ing longitudinal sections of tissue in + neutral buffered formalin and

    embedding trimmed surfaces to maintain the #osition of fungus in regards to dermal structures

    (Aeteyer et al. *'). Aeteyer et al. (*') found staining useful in detecting the fungus?

     #eriodic acid-Schiff stain was shown to be the most effective at detecting non-#igmented fungal

    hy#hae and conidia. H$u#-likeI e#idermal erosions found via microsco#y of wing membranes

    are characteristic of WNS and are often filled with hy#hae (Aeteyer et al. *'). The fungus can

    S$S= 3iology

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     be found continuing to invade underlying connective tissue and can encom#ass the full thickness

    of the wing membrane. 0n regards to the mule! hy#hae invade hair follicles! sebaceous glands!

    a#ocrine glands and connective tissue (Aeteyer et al. *'). Aeteyer et al. (*') also note bats

    with damaged wings collected from outside hibernacula showed severe inflammation in

    accordance with the fungal infection. Su##urative dermatitis with folliculitis! edema! infiltrates

    of macro#hages! and serocellular inflammatory crusts with hy#hae were also noted histological

    changes found by Aeteyer et al. (*'). The necrosis and im#airment of wing membranes can

     be very #roblematic to bats and will be discussed in coming sections.

    >istologic e%amination! a very effective diagnostic tool! often re"uires euthanasia in

    order to ac"uire 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.

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    The culture techni"ue used to detect Pd  is #robably the least efficient diagnostic tool of

    those mentioned thus far! but its not without its benefits. This techni"ue re"uires taking an

    infected tissue sam#le! growing the microbial elements of the sam#le on media and then

    identifying the given organisms and their mor#hology under microsco#e in order to determine if

     Pd  is #resent (9orch et al. *+). The culture method has been shown to have a diagnostic

    sensitivity of ,6! com#ared to 1$

    absent in infected tissues! although this is most likely due to the su##ression of immune

    res#onses associated with hibernation (Aeteyer et al. *'? *++). /s the infection #rogresses!

     Pd  a##ears as hy#hae filled! cu#-like lesions within the e#idermis! which continue to invade and

    degrade sebaceous and a#ocrine glands! hair follicles! connective tissue! lym#hatic vessels and

    muscle fibers in infected areas (Aeteyer et al. *'? $ryan et al. *+). 0nfarction has been

    observed in wing membranes and although Pd is not vasculotro#ic it a##ears to have an effect on

     blood flow to certain regions of the wings ($ryan et al. *+).

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    than wing damage associated with HnormalI environmental occurrences (

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    . These arousals then lead to dehydration and further de#letion of fat

    stores. /s the Pd  invasion #rogresses dee#er! reaching connective tissue! additional water and

    electrolyte loss occurs. Lehydration is then intensified leading to additional arousals from

    tor#or. This all creates a #ositive feedback loo# envelo#ing arousal! water loss! electrolyte loss

    S$S= 3iology

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    and energy use. This feedback loo# continues until all com#ensatory mechanisms and energyFfat

    reserves are drained! leading to death! however! if com#ensatory mechanisms and energyFfat

    reserves remain until the s#ring emergence from hibernation then its #ossible for the Pd  

    infection to recede and for the bat to #ossibly recover.

    This model is the first of its kind and includes testable hy#otheses which should #rovide a

     basis for future research and should #rovide crucial knowledge of disease #rogression that will

    aid conservation #ractices in the fight against WNS.

    Beha#iora$ disturbances associated ith 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 tor#or. Tor#or (a form of

    dormancy! similar to hibernation! but occurring over much shorter #eriods in which body

    tem#erature and metabolic rates are reduced) can last from #eriods of days to weeks in bats

    (@eiser! *6?

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      2urthermore! Turner et al. (*+,) #rovide evidence that synchroniation of arousals

    reflects disturbances of tor#id bats by infected cons#ecifics. They discuss that hibernating bats

    are highly susce#tible to disturbance! making arousal more likely if actively infected bats

    continue to come in contact with tor#id individuals. /s hibernation and infection #rogresses this

    increased contact brought about a Hcascade effectI of increasing arousals over time (Turner et al.

    *+,). Nonetheless! the high energetic demands of fre"uent arousals from tor#or remain and are

    still instrumental in the de#letion of hibernating resources and subse"uent mortality.

    WNS is associated with other abnormal behaviors in hibernating bats as well. While

    winter flying! s#ecifically daytime winter flying! in healthy bats is not considered abnormal

    (>endricks B >endricks! *+)! bats sus#ected of #otentially having WNS have been observed

     #artaking in e%cessive flying ($ryan et al. *+)! unusual daytime flying! uncoordinated flying

    including collisions into nearby trees! buildings! etc. (Turner!

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    (*+6) mention this reduced clustering being a tenet of Hsickness behaviorI in which it is more

    advantageous for individuals in infected hibernacula to remain isolated from one another to

    reduce the s#read and other unfavorable side effects of the given disease. This led Turner et al.

    (*+6) to identify that reduced clustering and isolation could be an ada#tive res#onse by bats

    with WNS to reduce the s#read of Pd . The behavioral study of bats in laboratory and wild

    settings is often difficult? although some observations and e%#eriments have been com#leted

    more data and e%amination into the behavioral disturbances of bats with WNS is needed to

    clarify com#eting results and establish well-su##orted e%#lanations. 0t would be interesting to

    observe if any additional altered or ada#tive behaviors are occurring in bat #o#ulations in states

    near the e#icenter of the WNS outbreak. 3ats of this region have shown #ersistence in res#onse

    to WNS before (

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    de#endent on five scenarios from an initial #o#ulation of ;., million bats. /s such! they e%#ect a

    '' chance of regional e%tinction of M. lucifugus by the year **;? annual declines would need

    to be less than , #er year for a noticeable reduction in the chance of e%tinction occurring over

    one hundred years. 0ts im#ortant to note that these #redictions were derived for the #reviously

    most abundant bat s#ecies in North /merica! M. lucifugus. 0f the most #lentiful bat s#ecies in

     North /merica is e%#ected to be regionally e%tinct in WNS affected areas by **; its most

    likely that #re-WNS endangered bat s#ecies like M. sodalis and M. grisescens or newly listed

    endangered bat s#ecies M. septentrionalis will also become e%tinct. There is evidence of

    interannual survival of M. lucifugus in New :ngland states as some colonies seem to #ersist

    (owever! as the once common little brown bat is #ro#osed for listing on

    the endangered s#ecies list in $onnecticut! its doubtful if #o#ulations will ever recover to #re-WNS levels.

    1o#ulation forecasting has also been researched by 9angwig et al. (*+*). They

    estimated #o#ulation growth rates of si% bat s#ecies both before and after the outbreak of WNS

     based on data from +* regional #o#ulations. /fter incor#orating changes in roosting behavior!

    environmental variation and #o#ulation densities into their mathematical models! 9angwig et al.

    (*+*) found that #rior to WNS all of their tested s#ecies showed increasing #o#ulation growth.

    >owever! in years following WNS discovery! #o#ulation growth rates for four s#ecies showed

    significant decline ( M. lucifugus, M. sodalis, M. septentrionalis B P. subflavus)! while the

    remaining two s#ecies showed neither growth nor decline ( E. fuscus B M. leibii) (9angwig et al.

    *+*). Everall! all growth rates were much lower #ost-WNS discovery than in #re-WNS years!

    and &*8 of the e%amined bat #o#ulations (5* of +*) became e%tinct (9angwig et al. *+*).

    3ased on their results and continued modeling M. septentrionalis, M. sodalis and M. lucifugus

    are #redicted to go e%tinct.

    /lves! Terribile B 3rito (*+6) have also conducted modeling to e%amine the #otential

    increasing s#read of WNS as well as its continued effect on bat #o#ulations. They used

    ecological niche modeling (:NA) to #redict #otentially new geogra#hic 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 #recautions and im#lement strategies to effectively deal with the

    S$S= 3iology

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    fungus and #rotect their local bat #o#ulations. The :NA took into account variations of

    tem#erature! #reci#itation! elevation and land classes when modeling #otential regions Pd  could

    infect and survive in. The generated ma# of #otential s#read dis#layed the current distribution of 

     Pd  (/lves! Terribile B 3rito! *+6). The ma# also showed regions susce#tible to Pd  which

     #resently are unaffected! including! coastal regions of the Northeastern =.S.! the Aississi##i

     basin region and the

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    oyt et al. (*+,) also shows #romise. They assessed if bacteria from the

     bats skin microbiome can inhibit Pd  growth. >oyt et al. (*+,) demonstrated that these naturally

    occurring bacteria canD +.)

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    among bat #o#ulations in the #resence of Pd  and also #rovides evidence that immuniing bats

    may #rovide #rotection from Pd  (Mohnson et al. *+,).

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    due to WNS is not combated in the coming years. 0f WNS continues to devastate these keystone

    s#ecies! affected regions will suffer immense losses.

    owever! some governing bodies and related #olicy makers! as well as most of the general

     #ublic! arent as #rivy. 3at advocacy will highlight the im#ortance of this grou# of animals from

    economic! ecological and natural history #ers#ectives! motivate research and #erha#s raise vital

    funding thus aide new! innovative conservation #ractices. $onsidering the re#ercussions of a

    loss of bats on this scale! it is wise to advocate in government! #rofessional and #ublic venues so

     #eo#le will know what WNS is and what affects it will have! not only on our bat #o#ulations! but

    in many as#ects of #eo#les lives if its s#read and subse"uent mortality #ersist.

    co$o%ica$ importance of bats

    /gricultural #ests of the arthro#od variety have been known to u#set farmlands all across

     North /merica. The re#ercussions caused by such arthro#ods can destroy entire fields of cro#s

    and leave farmers without food or income to su##ort their families. =sually! #esticides are used

    to combat such #ests! but #esticides have unwanted effects! such as the contamination of foods!

    human and non-human organisms and ecosystems (/ktar! Sengu#ta B $howdhury! *'). 0n

    some cases contamination can cause death or other serious #hysiological com#lications in human

    and non-human organisms! making #esticide use controversial and #otentially haardous to those

    e%#osed (/ktar! Sengu#ta B $howdhury! *'). 0n addition to these unwanted effects! it has

     been estimated that over 6 s#ecies of cro#-#est insects have develo#ed resistance to commonly

    used #esticides! creating an even greater challenge in the realm of #est control (un et al. *++).

    :nter the insectivorous bat. The bats #lagued by WNS in North /merica are all

    tem#erate! insectivorous s#ecies. They o##ortunistically feed on a variety of insects from

    different environments including forests! grasslands! farmlands! etc. (un et al. *++). Luring

    winter hibernation consum#tion slows! but activity and feeding still occur and are more common

    in bats which hibernate in thermally unstable microhabitats (Lunbar! Whitaker! Mr. B

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     body mass) of insects #er night to account for energy e%#enditures and Whitaker (+'',)

    determined that a colony of +, big brown bats ( E. fuscus) in the Aidwest can annually consume

    a##ro%imately +.5 million cro#-#est insects. These numbers su##ort what many #eo#le have

    known for centuries! that insectivorous bats are a natural form of #est control.

    /nthony and un (+'88) and urta et al. (+'7') found that the little brown bat can

    consume between 6 g P 7 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. /s of *+! 3oyles B Willis e%tra#olated

    this 6 g P 7 g #er night consum#tion rate during the active season to the estimated ,! bats

    that died from WNS and estimated that between 55 and ;; metric tons of insects were no

    longer being consumed in WNS regions. Now multi#ly that number by the estimated seven

    million bats that have died as of s#ring *+,? between 6!;* and '!*6 metric tons of insects are

    no longer being consumed in WNS regions. 0magine the increased use of #esticides in affected

    regions to combat these insects. / ob bats were #erforming naturally #re-WNS with no

    unwanted side effects will now! in the #ost-WNS world! rely u#on chemicals which have the

    chance to devastate entire ecosystems if used im#ro#erly. The realiation of the im#acts WNS is

    having on our natural world is enough to leave one s#eechless.

    conomic importance of bats

    /fter acknowledging the work of /nthony B un (+'88)! urta et al. (+'7')! Whitaker

    (+'',) and 3oyles B Willis (*+) its easy to understand the im#acting role bats #lay in regards

    to insect su##ression. :conomic estimates of the role bats #lay in #est control are still not fully

    understood! however some #ublished work has estimated the #otential economic losses the

    agricultural industry will suffer from the mass mortality of bats with WNS. 3oyles et al. (*++)

    estimate the value of bats to the agricultural industry to be a##ro%imately Q**.' billion #er year.

    This estimate was derived with the reduced costs of #esticide a##lications in mind! but it does

    not include certain factors like #redation of insects in forest ecosystems! or the secondary effects

    of #redation on insects (reducing the #otential for #esticide resistant insects to thrive) (3oyles et

    al. *++). 0magine if WNS moves into the Hbread basketI region of the =nited States. WNS has

     been confirmed in the Aidwest already and further s#read could be detrimental to the

    agricultural industry not to mention the bat s#ecies of the region. The Q**.' billionFyear

    S$S= 3iology

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    estimated by 3oyles et al. (*++) could easily be doubled over the s#an of a year if WNS were to

    move into this region.

    Bats as mode$ species

    /lthough its sometimes difficult to "uantify the im#act of bats to academia and research!

    these flying mammals surely have an e%traordinary value which needs to be recognied.

     Numerous fields have e%#erienced advances from the study of bats. Ene of the largest

    contributions from the study of insectivorous bat s#ecies! some of which are now #lagued by

    WNS! to the educational and research worlds has been the study of bat echolocation and

    locomotion (un et al. *++). The study of such functions has #rovided advances in fields

    related to sonar systems! biomedical ultrasound! wireless communication and 3/TA/CS (bat-like motoried aerial vehicles) (un et al. *++). 1eo#le enoy vilifying bats. 0f #eo#le were to

    understand the influence bats! es#ecially the insectivorous bats #lagued by WNS! have on our

    natural world! culture! education and technological advancements they would surely oin the

    countless researchers and wildlife enthusiasts who are des#erately trying to understand and

    combat WNS.

    Conser#ation

    /s has been discussed! WNS is obliterating our insectivorous bat #o#ulations (2rick et al.

    *+? 9angwig et al. *+*? Cerant et al. *+6).

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    their #art too. 3at $onservation 0nternational assists in allocating funds and other resources to

    hel# in studying and finding solutions to WNS.

    / real world a##lication to HcureI bats of WNS that can s#an twenty-si% states has yet to be #erfected. Still! in the nine years since the discovery of WNS in North /merica! the scientific

    community has learned much about the disease and #roduced co#ious amounts of data bringing

    us ever closer to a viable solution. >owever! resources are still needed. The vigilance and

    resolve of the #rofessionals researching WNS needs to be instituted in the general #ublic. Ene of 

    the ho#es 0 have is to bring the WNS discussion to the forefront and create a sense of urgency

    among the #ublic. With more #ublic involvement not only will more conservation efforts occur

    and more funding be raised! but #olicy-makers hearing from their advocating constituents will

    ho#efully do more to allocate resources to vital research already in #rogress.

    Liscussions among the scientific community about the res#onse to wildlife diseases are

    in #rogress. 9angwig et al. (*+,3) have develo#ed conservation res#onses! broken into four

    stages! based on the #athogen invasion #rocess. The first stage of the #athogen invasion #rocess

    is #re-arrival. 9angwig et al. (*+,3) stress that the first goal in this stage should be to

    determine the threat #osed by a given disease to the #articular region(s)? then #recautions should

     be taken and interventions im#lemented to reduce the #robability of disease introduction.

    =nderstanding #otential #athways of introduction and im#lementing a ra#id! #roactive res#onse

    are vital in this stage. 0f necessary! biosecurity should be im#lemented to "uarantineFrestrict

    access to areas at high risk for infection before a large scale outbreak occurs (i.e. cave B mine

    closures in res#onse to WNS) (9angwig et al. *+,3). :stablishing communication and

    s#reading awareness are also crucial. 0t is of the u#most im#ortance to have the #ublic aware

    and involved.

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    0nvasion front is followed by the e#idemic stage in which #athogen establishment has

    occurred within a region. The main goal of this stage should focus on reducing im#acts from the

    disease on local #o#ulations and environments (9angwig et al. *+,3). Ways of reducing

    im#acts include! but are not limited to! vaccinations! treatment with chemical or biological

    agents! habitat mani#ulation and augmenting demogra#hic rates (reducing natural #redation! etc.)

    (9angwig et al. *+,3). >ost resistance or tolerance may be facilitated from im#lementing the

    above measures and could #rove worthy once s#read among the given #o#ulation and #otentially

     #assed onto subse"uent generations? in the case of WNS! the work of 2rank et al. (*+6) and

    >oyt et al. (*+,) shows great #otential 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 #o#ulations. 0n this stage the

     #rotection and restoration of local #o#ulations is of the u#most im#ortance! both of which should

     be im#lemented in any reasonable way (9angwig et al. *+,3). 2urthermore! four additional

    actions are of great im#ortance among all of the aforementioned stages. The actions includeD +.)

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    unusual bat behavior in affected regions. /bnormal! daytime flying from Lecember to Aarch

    when bats should be hibernating can be indicative of WNS and should be re#orted to state

    environmental agencies immediately ($ryan et al. *+). 3y re#orting such incidences!

    communication is ke#t o#en as to new #otential WNS occurrences and agencies can direct a

    more ra#id! real-time res#onse.

    0ndividuals also want to avoid #otentially s#reading Pd . /s discussed earlier! evidence

    su##orts that Pd and WNS were introduced from :uro#e! most likely inadvertently via humans

    (Warnecke et al. *+*? 9orch et al. *+5).  Pd has also been found to survive in hibernacula! on

    clothes and e"ui#ment given the right environmental conditions making it absolutely necessary

    that cavers and others do their best to avoid contact with  Pd (Turner! oyt et al. *+6). /n individual can avoid contact with the fungus by s#orting

     #rotective outerwear when visiting hibernacula! decontaminating after visiting and if #ossible!

    avoid infected hibernacula all together. / national WNS decontamination #rotocol was

    develo#ed by multi#le agencies which should #rove useful to field researchers and other wildlife

    enthusiasts and can be found on WhiteNoseSyndrome.Erg (=.S. 2ish and Wildlife Service! *+*?

    www.whitenosesyndrome.orgFsitesFdefaultFfilesFresourceFnationalRwnsRreviseRfinalR;.*,.+*.#df ).

    With the ever increasing manifestations of infected hibernacula! artificial roosting

    locations would be most advantageous for bats fighting for survival in WNS regions. 0

    recommend individuals #ost bat houses if a##licable. / bat house #rovides a sustainable and

    clean location for bats to roost and live. 0nformation on #osting bat houses can be found at

    3at$on.Erg (Tuttle! iser B iser! *+5? www.batcon.orgF#dfsF3>3uilders>dbk+5REnline.#df ). 0n

    addition to smaller bat houses! abandoned buildings or barns also work well as artificial roosts

    and if ones situations allows! the #resence of bats in such outbuildings should be welcomed. 3at

    houses have recently come to the cam#us of Southern $onnecticut State =niversity in New

    >aven! $T to #romote long-term research and most im#ortantly aid bat conservation in one of

    the first states where WNS was discovered. 0ts recognied these local conservation efforts are

    small com#ared to the large scale nature of WNS! but if doens of individuals were to become

    involved across multi#le states the likelihood of #ersistence by some bat colonies would

    increase.

    S$S= 3iology

    http://www.whitenosesyndrome.org/sites/default/files/resource/national_wns_revise_final_6.25.12.pdfhttp://www.batcon.org/pdfs/BHBuildersHdbk13_Online.pdfhttp://www.whitenosesyndrome.org/sites/default/files/resource/national_wns_revise_final_6.25.12.pdfhttp://www.batcon.org/pdfs/BHBuildersHdbk13_Online.pdf

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    1ossibly the biggest ste# individuals can take in the fight against WNS is to educate

    others and hel# increase awareness. 0ts vital for everyone who reads this review to go out of

    their way to discuss WNS with someone who was #reviously unaware. Think of the resources

    and assistance which could come to fruition if more members of the general #ublic knew of

    WNS and the forecasted outcomes of the disease.

    *n c$osin%

    WNS is a vile disease. /s 0ve discussed the #ast! #resent and future of WNS in bats its

    easy to see how troublesome WNS is on so many fronts? yet! some ho#e has been seen in recent

     #ublications which as#ire to answer the "uestion thats #lagued researchers from the start! the

    "uestion of wondering how to fi% this calamity. The scientific community is so far from wherewe were in *;! our knowledge of WNS has increased e%#onentially! but many unanswered

    "uestions 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 hy#otheses. 0 ho#e this com#ilation

     brings a new view#oint to data which may have been #reviously overlooked and u#on

    reinvestigation! could now lead to new research! conservation and s#ecies management

    o##ortunities. The #ursuance of scientific work throughout the remainder of this decade could

    very well #rovide us with an answer of how to remedy WNS! bring our bats back from the brink

    of e%tinction! and #reserve our natural history. $ertainly! the scientific community embraces the

    challenge and looks forward to the o##ortunity.

    Ac!no$ed%ements

    Aany thanks to those who have hel#ed su##ort this research throughout all of its #hases. Your assistances

    and enthusiasms are dee#ly a##reciated.

    Lr. Airanda Lunbar 

    3iology Le#artment! Southern $onnecticut State =niversity Student @overnment /ssociation! Southern $onnecticut State =niversity

    Lavid B Susan Wisniewski

    S$S= 3iology

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    eferences

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     benefits and haards. "nterdisciplinary !o#icology! $(+)! +-+*. htt#DFFd%.doi.orgF+.*687Fv++*-'-

    +-8 /lves! L. A.! Terribile! 9. $.! B 3rito! L. (*+6). The 1otential 0m#act of White-Nose Syndrome on

    the $onservation Status of North /merican 3ats. PLo% &E ! '(').

    htt#DFFd%.doi.orgF+.+58+Fournal.#one.+85', /nthony! :. 9.1.! B un! T. >. (+'88). 2eeding strategies of the little brown bat! myotis lucifugus! in

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    htt#DFFd%.doi.orgF+.++6;Fannurev.#hysiol.;;.5*+*.++,+, >endricks! 1.! B >endricks! 9. A. (*+). Water /c"uisition Luring Laylight by 2ree-oyt! M. ee! A. A.! 2rick! W. 2.! B il#atrick! /. A. (*+,).

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    the :#icenter of White-Nose Syndrome. ortheastern aturalist ! $-(6)! N,;-N,'.

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    htt#DFFd%.doi.orgF+.5+;+F+,7++'U67,;76 Thomas! L. W.! Lorais! A.! B 3ergeron! M.-A. (+''). Winter :nergy 3udgets and $ost of /rousals

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     iseases! -0 (7)! +*58-+*6*. htt#DFFd%.doi.orgF+.5*+Feid+;7.+* Wilco%! /.! Warnecke! 9.! Turner! M. A.! Ac@uire! 9. 1.! Mameson! M. W.! Aisra! C.! . . . Willis! $. .