Bibliography

Balaszs, D. (1977). The geographical distribution of karst areas.Proceedings of the Seventh International Congress of Speleology,Sheffield, 1, 13�15.

Bonacci, O. (2004). Poljes. In J. Gunn (Ed.), Encyclopedia of caves andkarst science (pp. 599�600). New York: Fitzroy Dearborn.

Euliss, N. H., LaBaugh, J. L., Fredrickson, L. H., Mushet, D. M.,Laubhan, M. K., Swanson, G. A., et al. (2004). The wetland contin-uum: A conceptual framework for interpreting biological studies.Wetlands, 24, 448�458.

Gaberscik, A. (Ed.), (2003). In A. Gaberscik (Ed.), Jezero, ki izginjaLjubljana: Monografija o Cerkniskem jezeru. Drustvo EkologovSlovenije.

Gunn, J. (2006). Turlough and tiankengs: Distinctive doline forms.Speleogenesis and Evolution of Karst Aquifers, 4, 1�4.

Leibowitz, S. G. (2003). Isolated wetlands and their function: An eco-logical perspective. Wetlands, 23, 517�531.

Mitsch, W. J., & Gosselink, J. G. (2007). Wetlands (4th ed.). New York:Wiley.

Mulec, J., Mihevc, A., & Pipan, T. (2005). Intermittent lakes in thePivka basin. Acta Carsologica, 34, 543�565.

Petric, M. (2010). Characterization, exploitation, and protection of theMalenscica karst spring, Slovenia. In N. Kresic & Z. Stevanovic(Eds.), Groundwater hydrology of springs (pp. 428�441).Amsterdam: Elsevier.

Petric, M., & Kogovsek, J. (2005). Hydrogeological characteristics of thearea of intermittent karst lakes of Pivka. Acta Carsologica, 34, 599�618.

Pipan, T. (2005). Fauna of the Pivka Intermittent Lakes. ActaCarsologica, 34, 650�659.

Sheehy Skeffinton, M., Moran, J., O’Connor, A., Regan, E., Coxon,C. E., Scot, N. E., et al. (2006). Turloughs—Ireland’s unique wet-land habitat. Biological Conservation, 133, 265�290.

Sheehy Skeffinton, M., & Gormally, M. (2007). Turoughs: a mosaic ofbiodiversity and management systems unique to Ireland. ActaCarsologica, 36, 217�222.

Stumberger, B. (2010). A classification of karst poljes in the Dinaridesand their significance for waterbird conservation. In D. Denac,M. Schneider-Jacoby & B. Stumberger (Eds.), Adriatic flyway �clasoing the gap in bird conservation (pp. 151�154). Radofzell,Germany: Euronatur.

Vessels, N., & Jack, J. D. (2001). Effects of fish on zooplankton com-munity structure in Chaney Lake, a temporary karst wetland inWarren County, Kentucky. Journal of the Kentucky Academy ofScience, 62, 52�59.

Wiggins, G. B., MacKay, R. J., & Smith, I. M. (1980). Evolutionaryand ecological strategies of animals in annual temporary pools.Archieves de Hydrobiologie Supplement, 2, 97�206.

WHITE-NOSE SYNDROME: A FUNGALDISEASE OF NORTH AMERICAN

HIBERNATING BATSMarianne S. Moore and Thomas H. Kunz

Boston University

INTRODUCTION

White-nose syndrome (WNS) is an epizootic currentlyaffecting several species of hibernating bats in North

America. The most devastating wildlife disease inrecorded history, WNS is causing unprecedented mor-tality and threatening regional extinction in at least onepreviously common bat species (Frick et al., 2010). Thesyndrome is named for a white, filamentous growth offungal hyphae and conidia (spores) on the nose, ears,wings, and tail membranes of affected bats (Blehertet al., 2009; Fig. 1). The first evidence of this fungalgrowth on hibernating bats was photographed on 16February 2006 at Howes Cave, located approximately50 km west of Albany, New York (Blehert et al., 2009).In the four years since it was first observed, the putativefungal pathogen, Geomyces destructans (Gd), associatedwith WNS, has spread rapidly from its epicenter,southward to North Carolina, westward to Missouriand Oklahoma, and northward to Canada. As of April2011, Gd has been reported from bats in 17 states(Connecticut, Delaware, Indiana, Maryland, Massachusetts,Missouri, New Hampshire, New Jersey, New York, NorthCarolina, Ohio, Oklahoma, Pennsylvania, Tennessee,Vermont, Virginia, and West Virginia) and three Canadianprovinces (New Brunswick, Ontario, and Quebec),although confirmed infections based on histopathologyhave not been determined for bats from Missouri andOklahoma (United State Fish & Wildlife Service, 2011).

In contrast to stable or increasing pre-WNS batpopulations, declines of hibernating bats in the north-eastern United States, ranging from 30�99% annuallyand averaging 73%, have been documented (Fricket al., 2010). Assuming that current rates of mortalitycontinue, the once common little brown myotis (Myotislucifugus) is expected to be extinct in the northeasternUnited States by the year 2026 (Frick et al., 2010), andat least five other hibernating bat species (M. septentrio-nalis, M. sodalis, M. leibii, Eptesicus fuscus, andPerimyotis subflavus) in this region are at risk (Blehert

FIGURE 1 Hibernating little brown myotis (Myotis lucifugus)infected with a putative fungal pathogen, Geomyces destructans, asso-ciated with white-nose syndrome. Photo by A.C. Hicks, New YorkDepartment of Environmental Conservation. Used with permission.

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et al., 2009; Turner and Reeder, 2009; Courtin et al.,2010; K.E. Langwig, pers. comm). Based on morpho-logical and molecular (polymerase chain reaction,PCR) criteria, Gd was recently reported from threeother hibernating bat species in North America (M. gri-sescens [listed as federally endangered], M. austroripar-ius, and M. velifer) although infections have not beenconfirmed in M. grisescens from Missouri or M. veliferfrom Oklahoma based on histopathology. Two feder-ally endangered subspecies of Townsendi’s long-earedbat, Corynorhinus townsendii (C. t. virginianus and C. t.ingens), are within the geographic range of hibernatingbats affected by Gd, but to date there is no evidencethat this fungus has spread to these two species.

No introduced pathogen has caused such a precipi-tous decline in any mammal species in recorded his-tory. Low reproductive rates and long life span of bats(Kunz and Fenton, 2003) will make their recoveryextremely slow unless the syndrome can somehow becontrolled. The recent decline of bat populations in thenortheastern United States caused by WNS is likely tohave adverse economic consequences on the ecology ofboth natural and human-derived agroecosystems.

BAT MORTALITY AND THEPUTATIVE PATHOGEN

Beginning in late winter 2007/2008, wildlife biologistsbegan to document unusual physical conditions, beha-viors, and mortality in bats hibernating in caves andabandoned mines in New York State. Subsequently, post-mortem histopathological examinations revealed a dis-tinct cutaneous fungal infection where hyphae invadedthe epidermis, hair follicles, sebaceous and sweat glands,and breached the basement membrane of hibernatingbats (Blehert et al., 2009). Examination of these bats withcutaneous fungal infections revealed a previously unde-scribed fungus with an asymmetrically curved conidia(Blehert et al., 2009). Laboratory studies later documentedthat this fungus is psychrophilic (i.e., cold loving) andgrows optimally between 5 and 10�C, well within the sea-sonal temperature range of most hibernacula (2�14�C)(Blehert et al., 2009). Phylogenetic analysis has placedthese isolates within the inoperculate ascomycetes (orderHelotiales) and near the anamorphic genus Geomyces (tel-eomorph Pseudogymnoascus). The closest relative of thefungal isolates from bats was identified as the ubiqui-tous G. pannorum, a keratinophylic species of which asubspecies, G. pannorum var. pannorum, has been iden-tified in superficial skin and fingernail infections inhumans. The combination of a unique morphologyand genetic composition (specifically at the identicalinternal transcribed spacer region and small subunitribosomal RNA gene) distinguishes the bat isolate

from other members of Geomyces. This discovery led tothe recognition of a new species within the genus, andsubsequently the fungus associated with WNS wasaptly named Geomyces destructans. To date, it is notentirely clear whether Gd is the causative agent ofWNS, but it appears that this fungus alters the physiol-ogy of hibernating bats (Boyles and Willis, 2009) andthus may have a direct pathogenic role (Meteyer et al.,2009; Cryan et al., 2010). Aside from the histopatholog-ical evidence that Gd causes severe cutaneous lesions(Meteyer et al., 2009), secretory proteases involvedin tissue digestion have been identified from Gd sup-porting the etiologic role of the fungus in WNS(Chaturvedi et al., 2010). Additionally, genotyping offive genetic markers using Gd isolates collected frombats within a 200-km survey distance from its epicen-ter provide preliminary evidence that a single strainwas introduced into New York and a clonal popula-tion is infecting all bats within the affected region(Chaturvedi et al., 2010).

DIAGNOSTICS

Histopathology is currently the gold standard ofdiagnostic tools used to confirm WNS, which with spe-cialized training and appropriate staining and visuali-zation of tissues, allows the identification of Gd andassociated cutaneous lesions (Meteyer et al., 2009).Culture, isolation and morphological examination canalso be used to identify presence of the fungus fromtissue or swab samples (Blehert et al., 2009; Gargaset al., 2009; Chaturvedi et al., 2010); however, a numberof researchers have noted low rates of isolation (e.g.,54%) (Lorch et al., 2010) despite an abundance of avail-able Gd-affected tissue, a complication that may be dueto competition from other microorganisms colonizingbat skin (Chaturvedi et al., 2010; Lorch et al., 2010).PCR amplification and sequencing of genetic materialis a promising, economical, and rapid alternative thatcan also be used to identify the presence of Gd on skin,hair, and other tissue samples (Chaturvedi et al., 2010;Lorch et al., 2010), and trials using this method onthe skin of bats inoculated with various concentrationsof Gd showed 96% diagnostic sensitivity and 100%diagnostic specificity (Lorch et al., 2010). However,although this technique can be used to less invasivelyscreen individual bats for the presence of Gd, small tis-sue samples usually collected for DNA extraction andPCR amplification may not provide accurate resultsbecause the fungus is not equally distributed across alltissue surfaces (Lorch et al., 2010). Additionally, theuse of PCR amplification and culture/isolation/exami-nation methods only allow for confirmed presence ofthe fungus, which may occur in the absence of

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cutaneous lesions, and do not provide the ability todetermine the extent of Gd invasion into cutaneous tis-sues as compared with histopathological examination.

BAT SPECIES AFFECTED BY WNS

To date, six hibernating cave-roosting bat species haveexperienced varied rates of mortality associated withWNS, including the little brown myotis (Myotis lucifu-gus), northern long-eared myotis (M. septentrionalis), thefederally listed endangered Indiana myotis (M. sodalis),the small-footed myotis (M. leibii), the tricolored bat(Perimyotis subflavus), and the big brown bat (Eptesicusfuscus) (Blehert et al., 2009; Courtin et al., 2010; A.C. Hicksand K.E. Langwig, pers. comm.). More recently, Gd, thefungus associated with WNS, has also been identifiedmorphologically and genetically (using PCR) from thesoutheastern myotis (Myotis austroriparius), the federallylisted endangered gray myotis (M. grisescens), and cavebat (M. velifer), although to date no other symptoms asso-ciated with WNS, including mass mortality, have beenobserved in these three species.

CHARACTERISTICS OF WNS

Fungal Infections and Tissue Damage

The primary characteristic of WNS is the presenceof cutaneous lesions from Gd, where the invasion offungal hyphae causes cup-like epidermal erosions,ulcers, and degradation of regional connective tissue(Meteyer et al., 2009; Fig. 2). Invasion by Gd leads tothe replacement of cutaneous glands, blood, and lym-phatic vessels and muscle as the fungus digests tissuesand also causes a reduction in tone, tensile strength,and elasticity of wing membranes (Cryan et al., 2010).Additionally, tissue damage and necrosis, apparentlydue to oxygen depletion (i.e., infarcted tissue), hasbeen observed in regions of wing membrane distantfrom the area of fungal invasion (Cryan et al., 2010).Given the importance of bat wings in many physiolog-ical processes, these observations suggest that a mas-sive homeostatic imbalance caused by the destructionof wing tissue may be a possible proximate cause ofdeath in hibernating bats (Cryan et al., 2010).

Depleted Fat Reserves

WNS is also manifested in hibernating bats by anapparent premature mobilization of fat reserves(Blehert et al., 2009; Meteyer et al., 2009; Courtin et al.,2010; J.D. Reichard, pers. comm.) suggesting thatstarvation due to depleted fat reserves may also be a

proximate cause of death in bats affected by WNS.Depletion in energy reserves may be due to the poten-tial homeostatic imbalance noted above or an initialdearth of fat reserves in bats as they enter hibernationpossibly due to a lack of fatty acids in the diet becauseof changes in insect abundance. It is also possible thatdepleted fat reserves are the result of acceleratedenergy consumption if bats are arousing from torpormore frequently to groom the fungus from their skin,or to mount immune responses. Arousing from torporand maintaining euthermic body temperatures at typi-cal hibernaculum temperatures are energetically expen-sive activities (Boyles and Willis, 2009). If normaltorpor-arousal patterns are disrupted during the devel-opment of WNS, increases in metabolic rates could eas-ily require more fat reserves than bats typically store inpreparation for hibernation and result in the observeddepletion of these reserves and death by starvation.

Atypical Winter Behavior

In addition to wing damage, depleted fat reserves,and fungal infections, bats affected by WNS mayalso exhibit atypical behavior including flying outsidehibernacula in midwinter (A.C. Hicks, pers. comm.)and the inability to arouse from torpor when disturbedby human activity (A.C. Hicks, J.G. Boyles, andJ.D. Reichard, pers. comm.). In fact, infrared thermalimaging of clusters of hibernating little brown myotisshows that many torpid bats affected by WNS do notelevate their body temperatures upon anthropogenic

FIGURE 2 Histological section of a wing membrane collected from ahibernating little brown myotis (Myotis lucifugus) affected by white-nosesyndrome immediately following euthanasia. Exuberant growth ofGeomyces destructans and conidia (spores) are present on the skin surface(arrow) as well as penetrating wing membrane (arrowheads) withoutassociated inflammation. PAS stain. Bar5 15 µm. Photo by C.U. Meteyer,U.S. Geological Survey; Meteyer et al., 2009. Used with permission.

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disturbance (J.D. Reichard, unpubl. data; J.G. Boyles,unpubl. data).

Atypical behavior of hibernating bats infected withGd also appears to manifest increased frequencies ofarousal from torpor (D.M. Reeder, pers. comm.).Because elevating body temperature (Tb) from nearambient to B37�C and sustaining this elevation of Tb

during arousals is extremely energetically costly(Boyles and Willis, 2009), this behavioral change islikely to incur extreme costs in the form of fat depletion. Itis possible that increased frequencies of arousal from

torpor are due to irritation caused by the cutaneous fungalinfection, or to elevate immune responses in an attempt toresist fungal invasion. It is also possible that the depletionof fat reserves prompts bats to arouse from torpor to feed,which is supported by the observations of bats emergingfrom hibernacula in midwinter potentially in an attemptto forage (Blehert et al., 2009; A.C. Hicks, pers. comm.; J.D.Reichard, pers. comm.).

Changes in Immune Response duringHibernation

As true hibernators, bat species affected by WNSmay experience levels of immunocompetence con-strained by prolonged periods of deep torpor, giventhat research on other hibernating mammals suggeststhat deep torpor depresses numerous mechanismsassociated with immunity (Bouma et al., 2010). Becauseof attempted resistance against fungal invasion, theimmune function in hibernating bats affected withWNS may be altered, with some aspects apparentlyelevated and others reduced in comparison to unaf-fected bats (M.S. Moore, unpubl. data; R. Jacob andD.M. Reeder, unpubl. data). Based on histopathologicalexamination, the little brown myotis does not appearto mount a morphologically detectable inflammatoryresponse to Gd (Meteyer et al., 2009); however, theextent to which WNS-affected bats attempt to resistinvasion by Gd through other immunologicalresponses remains unknown.

Wing Damage

Bats that survive hibernation while being affectedby WNS may return to maternity colonies with ulcer-ated, necrotic, and scarred wing membranes (Reichardand Kunz, 2009; N.W. Fuller, pers. comm.). In fact,severe wing damage was observed in the majority oflittle brown myotis roosting in two New Hampshirematernity colonies during the summer of 2008 (Fig. 3).Damage to wings caused by wounds or infections canimpair the ability of wings to perform their functionsand may result in reduced foraging success andincreased vulnerability to predation. However, theresults from a recent study indicate that complete heal-ing from WNS-associated damage can occur in someindividuals during summer months (N.W. Fuller, pers.comm.). If bats with damaged wings experiencereduced foraging success during the active season, fur-ther reductions may occur in the relative body condi-tion of bats arriving at maternity colonies in an alreadycompromised state. This reduction in body conditionmay also result in an inability to properly care foryoung, avoid predation, and enter the following

FIGURE 3 Wings of little brown myotis (Myotis lucifugus) unaf-fected by and affected by white-nose syndrome captured in earlyspring from a maternity colony. (A) Undamaged wing (wing-damageindex 0); (B) wing showing moderate scarring and spotting (wing-damage index 11); (C) wing showing severe scarring and necrosis(wing-damage index 3). Wing-damage index after Reichard and Kunz,2009. Photo by N.W. Fuller, Boston University. Used with permission.

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hibernation period with sufficient fat reserves. In fact,reduced body condition and lower recapture rateshave been observed in relation to WNS-induced wingdamage (Reichard and Kunz, 2009). In addition to themassive mortality that has been observed duringhibernation, this physiological challenge incurred dur-ing the active season also has presumably contributedto the approximately 73% decline in summer activityof little brown myotis within regions affected by WNS(Dzal et al., 2011; Brooks, 2011).

FUNGALTRANSMISSION

The pattern of expansion away from its epicenter, theknown behavioral patterns of bats throughout the year,and the fact that some gated caves and mines have hadno human visitors for several years prior to becomingaffected, support the hypothesis that bat-to-bat contact isthe primary mode of transmission. However, the possi-bility of anthropogenic transmission was acknowledgedwhen researchers first became aware that the majority ofnewly affected sites in 2008 had been visited by humans,either as biologists or recreational users (Turner andReeder, 2009). However, in 2009, bats infected with Gdappeared in areas distant from other affected sites, sug-gesting that human transmission of the fungus was apossibility. These infected sites have high recreationaluse and small hibernating populations or may havebeen visited by people with gear used at other affectedsites. Thus, it appears that while bat-to-bat transmissionfacilitates the movement of Gd into new sites adjacent ornear to affected hibernacula, anthropogenic transmissionmay accelerate the spread and introduce the fungus intorelatively distant sites and areas.

A EUROPEAN CONNECTION?

As early as the 1980s, repeated observations of whitefungal growth on the muzzles of hibernating bats werereported in Europe; however, no unusual mortalityevents have been documented in association with thesereports (Martınkova et al., 2010; Wibbelt et al., 2010).Since the advent of WNS in North America and theidentification of the associated fungus, Gd, in nine spe-cies of bats in Europe, sampled in Germany,Switzerland, Hungary, the Czech Republic, Slovakia,and France (Martınkova et al., 2010; Puechmaille et al.,2010; Wibbelt et al., 2010), no mass mortality has beenassociated with these isolations. Some researchers havepostulated that the fungus may be native to Europe orat least that it predates its presence in North America(Martınkova et al., 2010; Wibbelt et al., 2010).Alternatively, it is also possible that the fungus had its

origin in North America and was recently introducedto Europe. However, because considerable genetic vari-ability was observed in Gd isolates from the CzechRepublic and Slovakia (Martınkova et al., 2010), in con-trast to the identical clones found in New York(Chaturvedi et al., 2010), these results suggest that thefungus had its origin in Europe. One hypothesis is thatGd caused mass mortality in European bats long beforehuman observations were recorded and that theyevolved resistance while being exposed to this fungus.Different hibernation strategies may also affect the sus-ceptibility of various species to the syndrome. As sug-gested by Wibbelt et al. (2010), competition between Gdand other microbial flora colonizing bat skin or roostsurfaces and soils in hibernacula in Europe may havecontributed to the evolution of a nonpathogenic formin Europe, while a lack of similar competition in NorthAmerica may have led the evolution of a pathogenicvariant of Gd that affects hibernating bats.

CURRENTAND FUTURE RESEARCH

A multicontinent research effort has been mobilizedto study the effects of WNS on North American andEuropean bats, and includes researchers from numer-ous academic, governmental and nonprofit institu-tions. One of the primary areas of focus is indetermining if the fungus is the cause of mortality oris a secondary symptom. Controlling the spread andmitigating the effects of WNS are also high priorityareas of research. As an example, based on modelingefforts, Boyles and Willis (2009) suggested that local-ized “thermal refugia,” or warm areas inside hibernac-ula, could reduce heat loss and energy expenditureduring periodic arousals, possibly providing a stop-gap measure to employ while other control measuresare being developed. However, this unconventionalpractice would require that bats somehow could detectand travel to refugia and that these practices wouldnot alter conditions within the rest of hibernaculawhere refugia are installed. Culling has also been sug-gested as a possible means to reduce transmission(Arnold Air Force Base, 2009), although Hallam andMcCracken (2011) modeled the effects of culling ontransmission cycles and concluded that this mitigationpractice will have little effect on the spread of the syn-drome. Some groups are also conducting trials to testthe ability of fungicides to eradicate Gd from contami-nated gear and the efficacy of compounds to treataffected bats (H. Barton, pers. comm.; D.M. Reeder,pers. comm.; A.H. Robbins, pers. comm.).

Additional studies initiated shortly after the emer-gence of the syndrome include investigations into pat-terns of arousal and torpor, thermoregulatory changes,

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variation in metabolic rates, behavioral changes,determination of variation in body condition and typesof fat throughout the hibernation period, immunologi-cal correlates, and examination of the bacterial flora ofdigestive systems in WNS-affected bats (Turner andReeder, 2009). The possible role of environmental con-taminants has been investigated to a degree, showinghigh levels of persistent organic pollutants (Kannanet al., 2010), lead, and arsenic (Courtin et al., 2010) inWNS-affected bats. However, high levels of organicpollutants were also found in bats hibernating in unaf-fected hibernacula (Kannan et al., 2010), making theinterpretation of these results ambiguous. Primersdeveloped for the detection of Gd on bat tissueshave been tested on environmental samples to betterunderstand the geographic distribution of this newlydescribed fungus, although high levels of cross-reactionwith other species of fungi have prevented this methodfrom being used to successfully identify Gd in samplesother than those directly collected from bat tissue(Lorch et al., 2010). Modeling efforts have compareddemographics in the affected little brown myotis topredict the risk of extinction as a result of mortalitycaused by WNS (Frick et al., 2010), and demographicmodels are being developed to help explain the dif-ferential rates of mortality among affected species(K.E. Langwig, pers. comm.; A.P. Wilder, pers. comm.).

More recently, researchers have begun to investigateadditional components important to the developmentof WNS. Quantitative PCR methods are being devel-oped to determine fungal load on affected bats.Investigations are being conducted into the pathogene-sis, microbial ecology and phylogeography of the fun-gus, including sequencing the genome of Gd (J.T.Foster, pers. comm.). Population genetic structure andgene flow in the little brown myotis is being evaluatedto help predict the further spread of the syndrome(C.M. Miller-Buttersworth, pers. comm.; A.P. Wilder,pers. comm.). Studies are also under way to comparethe North American and European strains of the fun-gus and differences in susceptibility between NorthAmerican and European species.

CAVE CLOSURES ANDDECONTAMINATION PROTOCOLS

Because of the likelihood that human visitations facili-tate the transmission of Gd to unaffected sites, a numberof states have closed caves on state-owned property andthe U.S. Fish and Wildlife Service (USFWS) recommendsthat all cavers observe cave closures, advisories, anddecontamination protocols. Decontamination proceduresand a list of current cave closures can be found at www.fws.gov/WhiteNoseSyndrome/cavers.html. For the most

current list of WNS-affected and adjacent states, visitwww.fws.gov/WhiteNoseSyndrome/. Most importantly,bats should not be handled by people unless authorizedto do so. If live or dead bats are encountered in cavesand mines with the appearance of WNS, contact thenearest state wildlife agency, USFWS EcologicalServices Field Office, or email WhiteNoseBats@fws.gov.State office listings can be found at www.fws.gov/offices/statelinks.html. USFWS office listings can befound at: www.fws.gov/offices/.

Acknowledgments

We wish to thank H.A. Barton, J.G. Boyles, N.W. Fuller, A.C. Hicks, R.Jacob, K.E. Langwig, D.M. Reeder, J.D. Reichard, A.H. Robbins, andA.P. Wilder for sharing unpublished information referenced in thischapter. We are grateful to the American Society of Mammalogists,Bat Conservation International, the Eppley Foundation for Research,National Science Foundation, Morris Animal Foundation, NationalSpeleological Society, U.S. Fish and Wildlife Service, and the WoodtigerFund for supporting our research on WNS.

See Also the Following Article

Bats

Bibliography

Arnold Air Force Base (2009). White nose syndrome cooperative monitor-ing and response plan for Tennessee 2009. Tullahoma, TN: ArnoldAir Force Base.

Blehert, D. S., Hicks, A. C., Behr, M., Meteyer, C. U., Berlowski-Zier,B. M., Buckles, E. L., et al. (2009). Bat white-nose syndrome: Anemerging fungal pathogen? Science, 323(5911), 227.

Bouma, H. R., Carey, H. V., & Kroese, F. G. M. (2010). Hibernation: Theimmune system at rest? Journal of Leukocyte Biology, 88, 619�624.

Boyles, J. G., & Willis, C. K. R. (2009). Could localized warm areas insidecold caves reduce mortality of hibernating bats affected by white-nose syndrome? Frontiers of Ecology and the Environment, 8, 92�98.

Brooks, R. T. (2011). Declines in summer bat activity in central NewEngland 4 years following the initial detection of white-nose syn-drome. Biodiversity and Conservation, 20(1), 2537�2541.doi:10.1007/s10531-011-9996-0.

Chaturvedi, V., Springer, D. J., Behr, M. J., Ramani, R., Li, X., Peck,M. K., et al. (2010). Morphological and molecular characteriza-tions of psychrophilic fungus Geomyces destructans from NewYork bats with white nose syndrome (WNS). PLoS ONE, 5(5),e10783. doi:10.1371/journal.pone.0010783.

Courtin, F., Stone, W. B., Risatti, G., Gilbert, K., & Van Kruiningen,H. J. (2010). Pathogenic findings and liver elements in hibernatingbats with white-nose syndrome. Veterinary Pathology, 47, 214�219.

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.

Dzal, Y., McGuire, L. P., Veselka, N., & Fenton, M. B. (2011). Going,going, gone: The impact of white-nose syndrome on the summeractivity of the little brown bat (Myotis lucifugus). Biology Letters, 7(3), 392�394. doi:10.1098/rsbl.2010.0859.

Frick, W. F., Pollock, J. F., Hicks, A. C., Langwig, K. E., Reynolds,D. S., Turner, G. G., et al. (2010). An emerging disease causes

909WHITE-NOSE SYNDROME: A FUNGAL DISEASE OF NORTH AMERICAN HIBERNATING BATS

ENCYCLOPEDIA OF CAVES

regional population collapse of a common North American batspecies. Science, 329(5992), 679�682.

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.

Hallam, T. G., & McCracken, G. F. (2011). Management of the pan-zootic white-nose syndrome through culling of bats. ConservationBiology, 25, 189�194.

Kannan, K., Yun, S. H., Rudd, R. J., & Behr, M. J. (2010). High con-centrations of persistent organic pollutants including PCBs, DDT,PBDEs and PFOS in little brown bats with white-nose syndromein New York, U.S.A. Chemosphere, 80, 613�618.

Kunz, T. H., & Fenton, M. B. (2003). Bat ecology. Chicago, IL:University of Chicago Press.

Lorch, J. M., Gargas, A., Meteyer, C. U., Berlowski-Zier, B. M.,Green, D. E., Shearn-Bochsler, V., et al. (2010). Rapid polymerasechain reaction diagnosis of white-nose syndrome in bats. Journalof Veterinary Diagnostic Investigations, 22, 224�230.

Martınkova, N., Backor, P., Bartonicka, T., Blazkova, P., Cerveny, J.,Falteisek, L., et al. (2010). Increasing incidence of Geomycesdestructans fungus in bats from the Czech Republic and Slovakia.PLoS ONE, 5(11), e13853. doi:10.1098/rsbl.2010.0859.

Meteyer, C. U., Buckles, E. L., Blehert, D. S., Hicks, A. C.,Green, D. E., Shearn-Bochsler, V., et al. (2009). Histopathologiccriteria to confirm white-nose syndrome in bats. Journal ofVeterinary Diagnostic Investigations, 21, 411�414.

Puechmaille, S. J., Verdeyroux, P., Fuller, H., Gouilh, M. A.,Bekaert, M., & Teeling, E. C. (2010). White-nose syndrome fun-gus (Geomyces destructans) in bats, France. Emerging InfectiousDiseases, 16, 290�293.

Reichard, J. D., & Kunz, T. H. (2009). White-nose syndrome inflictslasting injuries to the wings of little brown myotis (Myotis lucifu-gus). Acta Chiroptera, 11, 457�464.

Turner, G. G., & Reeder, D. M. (2009). Update of white-nose syn-drome in bats, September 2009. Bat Research News, 50, 47�53.

United States Fish & Wildlife Service (USFWS). (2011). White-nosesyndrome: Something is killing our bats. www.fws.gov/white-nosesyndrome/. Accessed 02.11.11.

Wibbelt, G., Kurth, A., Hellmann, D., Weishaar, M., Barlow, A., Veith,M., et al. (2010). White-nose syndrome fungus (Geomyces destruc-tans) in bats, Europe. Emerging Infectious Diseases, 16, 1237�1242.

WORMSElzbieta Dumnicka

Institute of Nature Conservation, Polish Academy of Sciences

GENERAL CHARACTERISTICS

Several types (phyla) of small invertebrates are usuallyincluded under the common term worms: flatworms(Turbellaria), roundworms (Nematoda), ribbon worms(Nemertea), and annelids (Annelida). Sometimes thewormlike Onychophora are also included. The shapeof worms is rather simple: flat, filiform, or tube-like.The body is usually small: from half a millimeter to2�3 cm, exceptionally more. Nevertheless true“giants” can be found among worms—some reachinglengths in the meters. The majority of worm species do

not show morphological changes connected with lifein the cave environment, because they are usuallyunpigmented and blind. Only in flatworms, leeches,and a few ribbon worms, which are normally occu-lated and pigmented, do these changes occur. Thebody coloration is determined principally by the con-tents of the digestive tube and by blood pigments (asin annelids). Features characteristic of typical cavefauna other than morphological ones have beenobserved, including aperiodicity of breeding and pro-longation of all stages of the life cycle (Dumnicka,1984).

The majority of worms living in caves are the samespecies that live in the soil or in marine or freshwaterenvironments. Nevertheless, in all phyla there are alsospecies found exclusively in various kinds of under-ground habitats (including caves), and they are classifiedas troglobionts (terrestrial forms) or stygobionts (aquaticforms). The distribution of particular stygobiotic speciesis often wider than that of species found only in cavessince stygobionts can live in various types of under-ground waters (e.g., interstitial waters, hyporheic watersof rivers, etc.; (Botosaneanu, 1986). They can even migratefrom the drainage area of one river to the other—due toso-called stream capture (or stream piracy)—via an under-ground connection between streams from different rivercatchments. Stygobionts also live in regions withoutcaves; in such a situation they inhabit fissures and smallspaces between the grains of sediments filled with water.Their presence in underground waters of such areas isnoticed during studies made in wells or springs, wherethey have been caught after being washed out fromunderground waters following heavy rains.

HISTORY OF STUDIES

Though studies on cave worms started many yearsago (e.g., Jeannel, 1926; Hyman, 1937), there is still alot that is unknown. World data on the distribution,biology, and ecology of various taxonomic groupswere summarized in Encyclopaedia Biospeologica(Juberthie and Decu, 1994, 1998) and Stygofauna Mundi(Botosaneanu, 1986) (for water fauna). From theUnited States, Culver et al. (2000) listed 927 species liv-ing obligatory in caves, but Nematoda were omittedfrom this list, whereas other worms were representedby only a small number of species: Tricladida, 24 spe-cies; Oligochaeta, 5 species; and Branchiobdellida, 7species. From that time a few new stygobiotic wormswere described in this region but more studies of thisgroup are needed. Since the publication of those books,many new species or even higher taxa have beendescribed from other regions, especially Europe. Forexample, 66 stygobiotic oligochaete species were cited

910 W

Encyclopedia of Caves. © 2012 Elsevier Inc. All rights reserved.