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Title:
Impacts of White-Nose Syndrome Observed During Long-Term Monitoring of a Midwestern Bat Community
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Journal of Fish and Wildlife Management
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Pettit, Joseph L.
O'Keefe, Joy M.
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Bats ( lcsh )
Endangered species ( lcsh )
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White-nose syndrome (WNS) is an emerging fungal disease suspected to have infected Indiana caves in the winter of 2010–2011. This disease places energetic strains on cave-hibernating bats by forcing them to wake and use energy reserves. It has caused >5.5 million bat deaths across eastern North America, and may be the driving force for extinction of certain bat species. White-nose syndrome infection can be identified in hibernacula, but it may be difficult to determine whether bats in a particular area are affected if no known hibernacula exist. Thus, our aim was to use long-term monitoring data to examine changes in a summer population away from hibernacula that may be attributable to WNS effects during winter. We used capture data from a long-term bat-monitoring project in central Indiana with data from 10 repeatedly netted sites consistent across all reproductive periods. We modeled capture data by WNS exposure probability to assess changes in relative abundance of common species and reproductive classes as WNS exposure probability increases. We base exposure probability on a cokriging spatial model that interpolated WNS infection from hibernaculum survey data. The little brown bat Myotis lucifugus, the Indiana bat M. sodalis, and the tri-colored bat Perimyotis subflavus suffered 12.5–79.6% declines; whereas, the big brown bat Eptesicus fuscus, the eastern red bat Lasiurus borealis, and the evening bat Nycticeius humeralis showed 11.5–50.5% increases. We caught more nonreproductive adult females and postlactating females when WNS exposure probabilities were high, suggesting that WNS is influencing reproductive success of affected species. We conclude that, in Indiana, WNS is causing species-specific declines and may have caused the local extinction of M. lucifugus. Furthermore, WNS-affected species appear to be losing pups or forgoing pregnancy. Ongoing long-term monitoring studies, especially those focusing on reproductive success, are needed to measure the ultimate impacts of WNS.

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ArticlesImpactsofWhite-NoseSyndromeObservedDuringLongTermMonitoringofaMidwesternBatCommunityJosephL.Pettit*andJoyM.O’KeefeJ.L.PettitDepartmentofEarthandEnvironmentalSystems,IndianaStateUniversity,600ChestnutStreet,TerreHaute,Indiana 47809J.M.O’KeefeCenterforBatResearch,Outreach,andConservation,IndianaStateUniversity,600ChestnutStreet,TerreHaute, Indiana47809 AbstractWhite-nosesyndrome(WNS)isanemergingfungaldiseasesuspectedtohaveinfectedIndianacavesinthewinterof 2010–2011.Thisdiseaseplacesenergeticstrainsoncave-hibernatingbatsbyforcingthemtowakeanduseenergy reserves.Ithascaused 5.5millionbatdeathsacrosseasternNorthAmerica,andmaybethedrivingforcefor extinctionofcertainbatspecies.White-nosesyndromeinfectioncanbeidentifiedinhibernacula,butitmaybedifficult todeterminewhetherbatsinaparticularareaareaffectedifnoknownhibernaculaexist.Thus,ouraimwastouse long-termmonitoringdatatoexaminechangesinasummerpopulationawayfromhibernaculathatmaybe attributabletoWNSeffectsduringwinter.Weusedcapturedatafromalong-termbat-monitoringprojectincentral Indianawithdatafrom10repeatedlynettedsitesconsistentacrossallreproductiveperiods.Wemodeledcapturedata byWNSexposureprobabilitytoassesschangesinrelativeabundanceofcommonspeciesandreproductiveclassesas WNSexposureprobabilityincreases.WebaseexposureprobabilityonacokrigingspatialmodelthatinterpolatedWNS infectionfromhibernaculumsurveydata.Thelittlebrownbat Myotislucifugus, theIndianabat M.sodalis, andthetricoloredbat Perimyotissubflavus suffered12.5–79.6%declines;whereas,thebigbrownbat Eptesicusfuscus, theeastern redbat Lasiurusborealis, andtheeveningbat Nycticeiushumeralis showed11.5–50.5%increases.Wecaughtmore nonreproductiveadultfemalesandpostlactatingfemaleswhenWNSexposureprobabilitieswerehigh,suggesting thatWNSisinfluencingreproductivesuccessofaffectedspecies.Weconcludethat,inIndiana,WNSiscausingspeciesspecificdeclinesandmayhavecausedthelocalextinctionof M.lucifugus .Furthermore,WNS-affectedspeciesappear tobelosingpupsorforgoingpregnancy.Ongoinglong-termmonitoringstudies,especiallythosefocusingon reproductivesuccess,areneededtomeasuretheultimateimpactsofWNS. Keywords:bats;capturerates;disease;endangeredspecies; Eptesicusfuscus; mist-nettingsurveys;speciesdeclines Received:October7,2016;Accepted:January11,2017;PublishedOnlineEarly:January2017;Published:June2017 Citation:PettitJL,O’KeefeJM,2017.Impactofwhite-nosesyndromeobservedduringlong-termmonitoringofa midwesternbatcommunity. JournalofFishandWildlifeManagement 8(1):69–78;e1944-687X.doi:10.3996/102016JFWM-077 Copyright:Allmaterialappearinginthe JournalofFishandWildlifeManagement isinthepublicdomainandmaybe reproducedorcopiedwithoutpermissionunlessspecificallynotedwiththecopyrightsymbol & .Citationofthe source,asgivenabove,isrequested. Thefindingsandconclusionsinthisarticlearethoseoftheauthor(s)anddonotnecessarilyrepresenttheviewsofthe U.S.FishandWildlifeService. *Correspondingauthor:Joseph.Pettit@usu.edu IntroductionWhite-nosesyndrome(WNS),afungaldiseasecaused by Pseudogymnoascusdestructans, hasresultedin significantdeclinesofhibernatingbatsineasternNorth America.White-nosesyndromehasspreadsteadilyfrom itsorigininNewYork,whereitwasdiscoveredin2006 (Blehertetal.2009),souththroughtheAppalachian JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|69

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Mountains,andintosouthernandMidwesternstates (seemapsinTurneretal.2011andCryanetal.2013).The fungusinfectstheexposedskinofcave-hibernatingbats; infectionislinkedtothedepletionoffatstoresandoften leadstodeathofthebathost(Cryanetal.2013).Bats’ immuneresponsesaresuppressedduringhibernation (Boumaetal.2010)and,thus,recoveryfromWNS typicallydoesnotbeginuntilspringemergencefrom hibernationwhentheimmuneresponsereturnsto normallevels(Meteyeretal.2011)andinsectpreyare readilyavailabletoresupplylostfatstores.However, becauseWNScauseswingdamageinadditiontofat storedepletion,spring-emergingbatsmayfaceenergy depletionsoveranextendedperiod(ReichardandKunz 2009).Batsthatsurvivethewintermaystillsuccumbto theeffectsofWNSinspringormayhavelowerfecundity whencomparedwithpre-WNS. JonassonandWillis(2011)makethecasethatbecause femalebatsenterhibernationwithlargerfatstoresand consumethemmoreslowlythandomalebats,theymay bemorelikelytosurvivehibernationinaWNS-infected hibernaculum(caveorminewherebatshibernateduring thewintermonths).However,survivaldoesnotensure successfulreproduction.Infact,anyharmtobody conditionislikelytohaveimplicationsforreproductive success.Evenindirectfactorssuchasexcessprecipitation (Grindaletal.1992)orlatitude(Kunzetal.1998)have beenshowntoinfluencetheproportionofreproductive bats.White-nosesyndromehasbeenshowntodirectly influencebodyconditionand,thus,islikelytohavea significantimpactonreproduction;Fricketal.(2010) suggestedthisconnectionwhentheyfounddecreased reproductiveratesforlittlebrownbats Myotislucifugus within4yofWNSbeingdetectedinhibernaculainthe northeasternUnitedStates.Francletal.(2012)found reductionsinencounterratesforreproductivefemales andjuvenilesduringcapturesurveysinWestVirginia immediatelyaftertheonsetofWNS.Declinesin recruitmentpaintanevengrimmerpictureforWNSaffectedbatspeciesand,thus,itmaybeprudentto studytheeffectsofWNSonreproduction. TheeffectsofWNSaremostvisibleinhibernacula, whicharegenerallyrestrictedtokarstareas,specifically cavesormines,butitisnotalwaysfeasibletouse hibernaculasurveystodetermineWNSstatus.Annualor biannualcavesurveyshavealloweddetectionofthe diseaseinhibernatingbatpopulations;thesesurveys showedthatWNSarrivedinIndianacavesasearlyasthe winterof2010–2011.However,inareaswithnoknown hibernationsites,itisdifficulttodeterminewhetherbat populationshavebeenaffectedbyWNS.Thisisthecase formanysummermaternitysites.Currently,thereisno simpleandcost-effectivewaytodetectthefunguson batsduringsummer.Surveysofmaternityareasoffera lessdirectassessmentofWNSinfluenceinaparticular area,butaredesirableinthatinformationonabundance andreproductioncanbegained.Previousresearch duringthesummerhasshownthatWNSisdetectable throughchangesincaptureratesduringmist-net surveys(Francletal.2012;Moosmanetal.2013)andin batactivityviaacousticmonitoring(Brooks2011;Dzalet al.2011).Inthisstudy,weaimedtorecordthearrivaland impactofWNStoapartofcentralIndianawherethere arenoknownwinterhibernacula.Weuseddatafrom long-termmonitoringof10repeatedlynettedsites,with 8yofpre-WNSdatatakenconsistentlyacrossall reproductiveperiods(pregnancy,lactation,andpostlactation),to1)discernwhichspeciesweredeclining coincidentwiththearrivalofWNStoIndiana,and2) determinewhetherreproductivefrequenciesortiming wereaffectedbyWNSpresence.StudyAreaOurstudyareawaslocatedalongaripariancorridor southwestoftheIndianapolisInternationalAirportin HendricksCounty,Indiana.TheIndianapolisAirport Authorityowns1,045haofnaturalareasadjacentto theEastForkofWhiteLickCreek,where10permanent nettingsiteswereestablishedalongthecreekin1997. Onenetsiteconsistsofafixedlocationforwhichsimilar netarrangementswereusedonsuccessivevisits.Two majorsitechangeshappenedin2003:onesitewas moved460mupstreambecauseofatreefall,and highwayconstructionforcedtheremovalofanothersite; subsequently,areplacementnetsitewasestablished nearothersites ~ 2.5kmupstream. Thesevenmostcommonspeciesofbatscaughtinthis studyareawere Myotislucifugus (littlebrownbat) ,M. septentrionalis (northernlong-earedbat) ,M.sodalis (Indianabat) ,Perimyotissubflavus (tri-coloredbat) Eptesicusfuscus (bigbrownbat) ,Lasiurusborealis (eastern redbat) and Nycticeiushumeralis (eveningbat;Whitaker etal.2004).Thefirstfourspecieshavebeenheavily affectedbyWNSinnortheasternNorthAmerica(Blehert etal.2009;Cryanetal.2010;Langwigetal.2012).Less common,butalsocapturedinthisarea,were Lasiurus cinereus (hoarybat)and Lasionycterisnoctivagans (silverhairedbat).MethodsWemist-nettedeachofthe10sitesforbats1night/ 30-dperiod,2002–2014,(3nights/y)foranaverageof4.5 h/night,startingatdusk,from15Mayto15August.We definedonenightofnettingataparticularsiteasone sitevisit.Wetimedsitevisitstoevenlyrepresentall reproductiveperiods.Duringeachvisitwedeployeda combinationof1–3single-,double-,ortriple-highnets 6–18mwide.Netsweredesignedforcapturingbats, withafineweight(75/2denier),38-mmpolyestermesh, andreducedbags(Avinet,Dryden,NY).Foramore detaileddescriptionofthesiteandmethods,see Whitakeretal.(2004).WefollowedAmericanSocietyof Mammalogists’guidelinesforuseofwildmammalsin research(Sikesetal.2011;IndianaStateUniversity InstitutionalAnimalCareandUseCommitteeprotocols forJ.O.WhitakerandJ.M.O’Keefe)and,beginningin 2011,WNSprotocolsasspecifiedbytheU.S.Fishand WildlifeService(2012).Werecordedspecies,reproductivecondition,sex,age,andbodyconditionforeachbat, usingdegreeofossificationoffingerjointstoassessageLong-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|70

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(juvenileoradult).Weattacheduniquelynumbered aluminumforearmbands(Porzana,Ltd.,EastSussex, England,UK)beforereleasingbatsatthecapturesite.We conductedfieldworkunderfederalpermitsheldbyJ.M. O’Keefe(TE206872),J.O.Whitaker(TE839763),andB.L. Walters(TE106220),aswellasStateofIndianapermitsby theseindividualsandleadtechnicians. Analysis WeexaminedeffectsofWNSpresenceinIndianaon1) frequencyofcapturebyspeciesand2)frequencyand timingofreproductivestatesor  condition  (i.e.,pregnancy,lactation,postlactation,andnonreproductive).Only20 batsbandedatthisstudyareahavebeenobservedat Midwesthibernacula;allbandrecoverieswerewithin Indiana(TableS1);but,withsofewrecoveries,welack robustinformationonwhenallbatsinthisareawerefirst exposedtoWNS.Therefore,weapproximatedexposure probabilitiesusingcokriging,anextrapolationtoolin ArcGISGeostatisticalAnalyst(v.10.1,Redlands,CA).Cokriginguses 2spatialdatasourcestoestimatevaluesof exposureforpixelswhereexposuredataarelackingor unmeasurable.CokrigingmodelswerebasedonIndiana bathibernaculapopulationdatacuratedbyAndrewKing (U.S.FishandWildlifeService,dataaccessed3January 2014;seealsoThogmartinetal.2012).Thesedataincluded currentandhistoricalsurveysofIndianabatpopulationsize andtheinfectionyearfor506hibernaculain136counties across25U.S.states(189hibernaculawereinfectedinthe UnitedStatesatthetimeofdataaccess).Weusedyearly hibernaculuminfectionstatus(WNSconfirmedornot observed)andthe10-ymaximumIndianabatpopulation ofamonitoredcountytopredictprobabilityofWNS exposureforallspeciesofcave-hibernatingbats.Weused populationdatafortheIndianabatasaproxyfortotal populationsizeofhibernaculabecausetotalpopulation dataofallspecieswerenotavailableforallhibernacula. Cokrigingmodelsoutputacontinuouspredictionsurface givingprobabilityofinfectionofhypotheticalhibernacula. Thismethodissubjecttohighererrorrateswheredata representationislow(e.g.,lowcavedensityorareaswhere Indianabathibernaculaarenotpresent;seeFigureS1). Fromtheoutputmap,weinferredahighprobabilityof WNSpresencewherecokrigingprobabilitieswere 50%. Whilethiscokrigingmodelattemptstopredicthibernaculuminfection,itwasasimplemethodforapproximating theprobabilityofexposureonthesummerlandscape. Usingamixedmodelingapproachtoaccommodate forzero-inflation,weanalyzedcapturesofadultfemale batspersitevisitwiththepsclpackageinR(Zeileisetal. 2008;Jackman2015).Totestforchangesinspecies abundance,weassessedtheeffectsofWNSexposure probability(outputfromthecokriginganalysis),species, andtheinteractionbetweenWNSexposureandspecies oncapturerates.Totestforchangesinreproduction,we assessedcaptureratesbyWNSexposure,reproductive condition,andareproductiveconditionbyWNS exposureinteraction.Otherfactorsofinterestwere monthofcapturetocontrolforanyseasonaldifferences inspeciesabundance,neteffort(netarea 3 hournetting) toaccountfordifferencesinnetsetupbetweensite visits,andnetsitetocontrolforspeciesabundance differencesbetweensites.Welog-transformedneteffort tonormalizethedata.Wetestedeachvariablefor normality,homogeneity,andindependence.Although wedidrecapturesomeindividualsinthisdataset,we treatedallcapturesasnewbatsforthisanalysis. Wetested14zero-inflatedmodels,ofwhich12useda negativebinomialdistributionandtwousedaPoisson distribution(TableS2).Weusedzero-inflatedmodels becausethereweremanysitevisitswherewecaughtno batsornotallbatspecies.Thezero-inflatedmodelwasa two-parthierarchicalmodel;partonewasalogisticmodel thatestimatedtheprobabilityofobtainingastructural zero(batsarenotpresentatthetimeofsamplingand thus,arenotdetected)andparttwowasageneralized linear  count  modeldeterminingtheimpactoffactors oncapturefrequencies.Webuiltaglobalzero-inflated mixedmodelthatincludedallfactorsmentionedabovein boththelogisticandcountmodels.Tochoosethe appropriatemodeldistribution(Poissonversusnegative binomial),wecomparedmodelsusinglikelihoodratio tests.Wethenrefinedtheglobalmodelbyplottingeach factorbythemodelresiduals,andcheckingforoverdispersiontoensureallimportantfactorswerepresent. Wefurtherrefinedmodelstoeliminatefactorsthatwe deemednonsignificant,asdeterminedbylikelihoodratio tests(Zuuretal.2009).Tocreatethefinal,refinedmodel, wesequentiallydroppednonsignificantfactorsfromthe globalmodel,untilallremainingfactorssignificantly contributedtomodelperformance. SimilartothemethodsofFrancletal.(2012),weused locallyweightedregression(loess.sdinthemsirpackage Scrucca2011)inR(RCoreTeam2014)toassesschanges inthetimingofreproductiveconditionacrossWNStime periods.Locallyweightedregressionoffersaflexible methodoffittingalinetothedata,butrequireslarge samplesizes;thus,weassessedchangesintimingof reproductionforthemostcommonlycapturedspecies,thebigbrownbat.Wewerealsointerestedinthetiming ofreproductionin Myotis speciesthatarehighlyaffected byWNSandhavesimilarlife-historytiming(Fentonand Barclay1980;Thomson1982;CaceresandBarclay2000). Toaccountforsmallsamplesizesforeach Myotis species, wepooledthesesamplesandperformedlocallyweightedregressionanalysesonthepooleddataset.We considereddifferencesbetweenthelinesmeaningful where95%confidenceintervalsdidnotoverlap.We usedaconservativeLoessspanof0.75forallreproductiontimingmodels.Forinterpretation,wedefineda reproductiveperiodastimeswhen 50%ofadultfemale capturesexhibitedaparticularreproductivecondition (e.g.,pregnant,lactating,postlactation,ornonreproductive).Finally,todiscernshiftsincapturefrequenciesof juvenilebatsandrecapturedbats,wechosetoanalyze twoadditionaldatasets,oneofjuvenilecapturesandone ofrecapturedbats.Thezero-inflatedmodelsandtheLong-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|71

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samplesizeofthefullcapturedatasetdidnotallowfor modelscomplexenoughtotestforsignificantshiftsinin capturesofthesedemographicsand,thus,weanalyzed themseparatelyusingdescriptivestatistics.ResultsWesurveyedtheEastForkofWhiteLickCreekon380 sitevisitsfrom2002to2014,capturing2,511bats(Table S3).Silver-hairedandhoarybatswerecapturedirregularly( n 5and n 7,respectively)and,thus,we excludedthemfromfurtheranalyses.Werefinedthe datasetforouranalysistouseonlycapturerecordsof adultfemalebatsforthesevenmostcommonspecies caughtatourstudyarea(1,376bats). Cokrigingmodelsbasedonhibernaculainfectiondata showedtheprobabilityofWNSexposureinHendricks Countybegantoincreaseinsummer2011,andbats summeringtherewereprobablyexposedtoWNSby 2012(TablesS1andS4).ThismodelshowedWNS spreadingfromtheoriginalinfectionsiteinNewYork, souththroughtheAppalachians,andthenwest(Figure 1).By2013,probabilityofWNSexposurewas0.5–1.0for batpopulationsinallstateseastofIndiana,except Florida.Basedonthesedistinctprobabilities,we delineatedtwoexposuretimeperiodsatourstudysite: thepre-WNSperiodasallyearswithprobabilities approachingzero(1998–2010);andtheWNSperiod (2011–2014),whichcanbeseparatedintoinitial-WNS (theyearwithaprobability 0and 0.5[2011]),and late-WNSperiod(yearswith 0.5probabilityofWNS presence[2012–2014]). Ourmixed-modelinganalysisshowedthatimpact fromWNSwasdetectableinlong-termsummercapture data.Thefinalmodelfromthemixed-modelanalysis containedalogisticzero-inflationcomponent(TableS35) andanegativebinomialcountcomponent(TableS6), bothcontainingthesamefactors.Modelrefinementdid notproduceasignificantlybettermodelbyremoving nonsignificantornear-significantfactors.Therefore,our modelscontainedthefollowingfactors:WNSexposure probability,species,reproductivestatus,month,lognet effort,netsite,andinteractionsbetweenWNSexposure andspeciesandbetweenWNSexposureandreproductivestatus.Species,reproductivestatus,month,andsite variablesweresignificantwithinthelogisticmodel, providingsupportthatthesevariableswereinfluentialin determiningtheprobabilityofstructuralzerosinthe data(batswerenotpresentand,thus,notobserved). Structuralzerosweremostcommonforeveningbats, nonreproductivefemales,earlyspringcaptures,andat Figure1. Probabilityofwhite-nosesyndrome(WNS)infectionfortheeasternUnitedStatesfrom2008to2013;surfacewascreated byinterpolatinginfectiondataforIndianabat Myotissodalis hibernaculawithcokrigingmodels.Theblackstarrepresentsthecentral Indianalong-termmonitoringsitewherewemeasuredWNSimpactsinsummer.White-nosesyndromedatafromCanadawerenot includedinthisanalysis.Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|72

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oneparticularnetsite.Monthwasasignificantfactorin thecountmodelbecausecaptureratesvariedovertime withinaparticularyear.Wecapturedbatsathigherrates inJulyandAugustandlowerratesinMay.Inthecount model,WNSexposureprobabilityalonewasnota statisticallysignificantpredictorvariable,buttheWNS exposure 3 speciesinteractionwassignificantforIndiana batsandlittlebrownbats(Figure2);thus,WNSexposure probabilitywasmaintainedinthefinalfittedmodel.We capturedsignificantlyfewerlittlebrownbatsandIndiana batsastheWNSexposureprobabilityincreased. Empiricaldatasummariesshowcapturespernight droppedforlittlebrownbatsfrom0.19( 6 0.5SD, n 271)priorto2011to0.09( 6 0.3SD, n 119)from2011 to2014;therewerenolittlebrowncapturesduringthe summerof2014.Indianabatcapturespernightdropped from0.32( 6 0.8SD, n 271)to0.15( 6 0.5SD, n 119) overthesameinterval. Captureratesvariedwithreproductiveconditionin thecountmodel;lactatingfemalesweremostcommon (1.39 6 2.5SDbats/night2002–2014, n 380)and nonreproductiveadultswereleastcommon(0.14 6 0.5 bats/night2002–2014, n 380).Inthecountmodel,the WNSexposure 3 reproductiveconditioninteraction showedasignificantincreaseinthenumberof postlactatingadultfemalesasWNSexposureprobability increased(Figure3andTableS46).Capturesof nonreproductivefemalesalsoincreasednotablywith WNSexposurebuttheWNSexposure 3 reproductive conditioninteractionparameterwasnotsignificantin Figure2. Loess-smoothedlineoffittedvaluesorganizedbyspeciesfromazero-inflatedmixed-modelanalysisofbatcapturesata long-termmonitoringsiteincentralIndiana(2002–2014).Anasteriskdenotesasignificantchangeinthecountportionofthemodel duringthewhite-nosesyndrome(WNS)period.Loessspan 0.5.VerticaldashedlinerepresentsthefirstyearofWNSobservationin Indiana.Bigbrownbat Eptesicusfuscus (EPFU),easternredbat Lasiurusborealis (LABO),littlebrownbat Myotislucifugus (MYLU), northernlong-earedbat M.septentrionalis (MYSE),Indianabat M.sodalis (MYSO),eveningbat Nycticeiushumeralis (NYHU),tricoloredbat Perimyotissubflavus (PESU).Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|73

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thecountportionofthezero-inflationmodel.Itwas significantinthelogisticportion,indicatingthat structuralzerosweremorecommonatlowexposure probabilities(i.e.,nonreproductivebatswerenotpresent atlowinfectionprobabilitiesandcouldnotbedetected). Priorto2011,onlythreenonreproductiveadultfemales wereobserved,comparedwiththe51observedfrom 2011to2014. White-nosesyndromeincreasedtheincidenceof nonreproductiveadultfemales,butWNSdidnot significantlyinfluencetimingforreproductivelyactive bats.Mostnonreproductivebigbrownbatswere caughtaftertheparturitiondateduringthetimewe wouldexpecttocatchlactatingfemales(Figure4),but nonreproductive Myotis specieswerecaughtduring theentiresummer.Thebigbrownbatlactationperiod (when 50%ofadultfemalecaptureswerelactating) was15dshorterduringtheWNSperiodthanitwas pre-WNS(Figure4),andthe Myotis lactationperiodwas 12dshorter(Figure5).However,becausethe confidenceintervalsoverlappedacrossWNSperiods, wedeterminedthatthisshorteningofthelactation periodwasnotsignificantforeitherbigbrownbatsor Myotis bats. Juvenilecapturesandrecapturesofallbatsincreased afterWNSaffectedIndianacaves.Wecaught407 juvenilebatsofallspeciesduringthe261pre-WNS periodsitevisitsand271juvenilesduringthe119WNS periodsitevisits.However,whenonly Myotis species juvenileswereconsidered,wecaught42juvenilespreWNSversus11duringWNS.Werecaptured98batsofall speciesduringthe261pre-WNSperiodsitevisitsand 100duringthe119WNSperiodsitevisits.OfthepreWNSrecaptures,62%werebigbrownbats,12%were Indianabats,8%weretri-coloredbats,and7%were northernlong-earedbats.Littlebrownbats,evening bats,andeasternredbatsmadeuptheremaining11% inorderofabundance.DuringtheWNSperiod,70%of recaptureswerebigbrownbats,18%wereevening bats,andtheremaining12%wereeasternredbats, Indianabats,northernlong-earedbats,tri-coloredbats, andlittlebrownbats.DiscussionByexaminingcapturedatafromalong-termstudyina WNS-affectedareaandextrapolatingdatafromWNSaffectedhibernaculatotheeasternUnitedStates,we havedemonstratedthatWNSeffectscanbedetectedin Figure3. Loess-smoothedlineoffittedvaluesforsevenpooledbatspeciesorganizedbyreproductiveconditionfromazeroinflatedmixed-modelanalysisofbatcapturesatalong-termmonitoringsiteincentralIndiana(2002–2014).Loessspan 0.5. Verticaldashedlinerepresentsthefirstyearofwhite-nosesyndromeobservationinIndiana.Lactating(L),nonreproductive(NR), pregnant(P),andpostlactating(PL). Figure4. Loess-smoothedlinesshowingtheproportionofbig brownbat Eptesicusfuscus capturesthatare (a) pregnant, (b) lactating,or (c) nonreproductivebydayofyear;dataarefroma long-termstudyincentralIndiana(2002–2014).Solidlines representthepre-white-nosesyndrome(WNS)fittedvaluesand dashedlinesrepresenttheWNSperiodfittedvalues;thinlines are95%confidenceintervals.Loessspan 0.75.Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|74

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summerpopulations,possiblypredictably,inareasaway fromhibernacula.Thecokrigingmodelmadepredictions matchingchangesincaptureratesandchangesin species-specificreproductiveconditionthatweobserved atourcentralIndianasite.Changesweremoreapparent for Myotis species,withlittlebrownbatssufferingthe greatestimpact.BigbrownbatsdidnotshowWNSinduceddeclines,nordideasternredbatsorevening bats,twospeciesnotknowntobeaffectedbyWNS.At highWNSexposureprobabilities,weobservedmore nonreproductiveandpostlactatingadultfemalesthan expectedbasedonpre-WNScapturesandnoticedshifts intimingandproportionofcertainreproductiveclasses forWNS-affectedspecies.However,oursmallsamplesize duringtheWNSperioddidnotallowfordetectionof statisticallysignificantchangesinreproductivetiming. ThecokrigingmodelsuggestsatimelineofWNS impactsinthestudyareathatmirrorsthespreadofthe infectiontoIndianacavesinJanuary2011.The probabilityofWNSinfectionwaslowduring2011and thenincreaseddramaticallyin2012.Basedonourdata showingbatsthatsummerinHendricksCountyare hibernatinginWNS-infectedcaves(TableS1)andthe closeproximityofinfectedcaves,weknowthe probabilityofWNSexposureofHendricksCountybats was0.95in2013andpresumablyisrising.Thesedata alsosupporttheideathatbatscouldbeavectorfor moving Pseudogymnoascusdestructans tooursummer studyarea,addingvaliditytotheapplicationofthe cokrigingmodelonthesummerlandscape(MillerButterworthetal.2014;Meyeretal.2016). Datafromthisstudyandpreviousstudiesusing capturesurveys(Francletal.2012),populationmodeling (Fricketal.2010;Moosmanetal.2013),andacoustic surveys(Brooks2011;Dzaletal.2011)havedemonstrateddeclinesin Myotis speciesduringthematernityperiod afterregionaldetectionofWNS.Thisepidemicdisease hashadthegreatestimpactonpopulationsoflittle brownbats(e.g.,73%declinesinthenortheast,Fricket al.2010;78%declinesinNewYork,Dzaletal.2011).We observeda79.6%declineinlittlebrowncapturesfrom pre-WNStotheWNSperiod(Table1),and2014wasthe onlyyearthatwedidnotcapturelittlebrownbats duringthis13-ystudy.DeclinesinIndianabatcaptures weregreaterinthisstudy(59.6%decline)thanthe10.8% declinesfromastudyinWestVirginia(Francletal.2012). Itshouldbenoted,however,thatIndianabatswere caughtingreaterproportioninthisstudycomparedwith theFrancletal.(2012)study(6.8%ofcapturesversus 0.3%respectively).ThefactthatIndianabatsweremore commoninourstudyareacouldexplainsomeofthe differenceindeclinesobservedbetweenstudies.We observedaslightincreaseincapturesofnorthernlongearedbatsthatcontrastedwithfindingsinotherregions (e.g.,77%declineinWestVirginia,Francletal.2012;or 95%declinesinthesameareafoundbyReynoldsetal. Figure5. Loess-smoothedlinesshowingtheproportionof capturesthatwere (a) pregnant, (b) lactating,or (c) nonreproductive Myotis species(littlebrownbats,northernlong-eared bats,andIndianabats)bydayofyear;dataarefromalongtermstudyincentralIndiana(2002–2014).Solidlinesrepresent thepre-white-nosesyndrome(WNS)fittedvaluesanddashed linesrepresenttheWNSperiodfittedvalues;thinlinesare95% confidenceintervals.Loessspan 0.75. Table1. Meannumberofbatscapturedatalong-termmonitoringsiteincentralIndianaduringthreetimeperiodscenteredaround theyearwhite-nosesyndrome(WNS)wasfirstdetectedinIndiana(January2011).Capturesarestandardized(std.)byneteffortand percentratechangeisreportedforeachspecies.Negativechangesarebolded.Pre-WNSmeanstd. captures/year 2002–2010 Initial-WNSmeanstd. captures/year 2011 WNSmeanstd. captures/year 2012–2014 Percentratechange (WNS–Pre)/Pre 3 100 Eptesicusfuscus ,bigbrownbat90.481.5134.411.5 Lasiurusborealis ,easternredbat15.717.931.550.5 Myotislucifugus ,littlebrownbat10.58.62.9 79.6 Myotisseptentrionalis ,northernlong-earedbat6.97.09.42.1 Myotissodalis ,Indianabat16.78.19.0 59.6 Nycticeiushumeralis ,eveningbat8.67.816.746.5 Perimyotissubflavus ,tri-coloredbat16.120.018.8 12.5 Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|75

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2016),thoughtheincreaseweobservedwasdriven mostlybyanincreaseincapturesduring2012. InIndianahibernacula,theIndianaDepartmentof NaturalResources(2015)hasobserveddeclinesforlittle brownbats,Indianabats,tri-coloredbats,andbigbrown bats(90%,27%,71%,and51%,respectively).Aswe observedinthisstudy,twoofIndianaÂ’smostcommon cavedwellershavedeclinedsignificantlysince Pseudogymnoascusdestructans wasfirstdetectedinIndiana caves;thelittlebrownbatdeclinedfrom7,603batsin 2009to794batsin2015andtheIndianabatdeclined from166,891batsin2009to121,582batsin2015 (IndianaDepartmentofNaturalResources2015).Althoughthenumbersoftri-coloredbatsandbigbrown batshavedroppedsignificantlyinIndianacaves,wedid notdetectsignificantdeclinesforthesespeciesinthis study.Thisdiscrepancycouldbeduetomethodological differencesandthewinteringecologyofthesebats.Big brownbatscanhibernateinman-madestructuresin additiontocavesandmines(WhitakerandGummer 2000)and,thus,mayhaveanaturalrefugefromWNS. Tri-coloredbatsaretypicallynotobservedinlarge numbersduringcavesurveysbecausetheyusuallyroost singlyindeepportionsofthecave(FujitaandKunz 1984). WedidnotdetectanegativeeffectofWNSoncapture ratesforeveningbats,easternredbats,orbigbrownbats. Otherstudieshavealsoshownthebigbrownbatand easternredbatcaptureratesandacousticactivity increasingafterWNSinfection(Brooks2011;Francletal. 2012),despitethefactthat Pseudogymnoascusdestructans hadbeenfoundpresentinskinswabsofthesespecies (Bernardetal.2015).Oursisthefirststudytoshowchanges incaptureratesforeveningbatsafterWNSinfection.Big brownbatsamassgreateramountsoffatpriorto hibernationand,thus,maybeabletobettersurvive WNS-inducedresourcedepletionduringhibernation(Frank etal.2014).BothFrancletal.(2012)andFordetal.(2011) hypothesizedthatcaptureratesmightbeincreasingfor somespeciesbecauseofadecreaseincompetitionas populationsofotherbatspeciesdecline.Wesurmisethat duringtheWNSperiodwemayhavebeenmorelikelyto capturebigbrownbatsinmistnetsbecauseoffewerWNSaffectedbatsusingtheairspacearoundmistnets.We detectedan11.5%increaseincaptureratesforbigbrown bats,buttheobservedreductioninreproductivefemales suggestsWNScouldstillaffectpopulationsizesbyaltering fecundityforaffectedbats. OurdatashowthatWNSisaffectingthesuccessful completionofthereproductivecycleforlittlebrown bats,northernlong-earedbats,Indianabats,andbig brownbats.Weobservedanincreaseincapturesof nonreproductiveandpostlactatingadultfemalesathigh WNSexposureprobabilities.Theincreasedencounter ratefornonreproductiveadultfemalesofthesespecies indicatesthatevenbatsthatsurvivehibernationina WNS-infectedcavemaylosetoomuchenergyto successfullyproduceviableoffspring.Adultfemalelittle brownbatsenterhibernationwithgreaterfatreserves andconsumethemmoreslowlythantheirmale counterparts(JonassonandWillis2011).Thissavesmore energyforspringreproduction,whichshouldincrease thereproductivesuccessoffemalebats.However, femalesconservesaidfatstoresthroughgreateruseof torpor,abehaviorthatisinterruptedbyWNS-induced arousals(Reederetal.2012).Therefore,femalesmay emergefromhibernationwithinsufficientenergyto supportfetaldevelopment.Analternativehypothesisis thatsomebatsarelosingpupsratherthanforegoing pregnancy;itfollowsthatWNS-inducedresourcedepletioncouldbedecreasingreproductivesuccessina numberofways.Thefactthat19ofthe20nonreproductiveadultfemalebigbrownbatswerecaughtafter theparturitiondatesuggeststhatbigbrownbatsinour studyareawerelosingpupsafterbecomingpregnantin spring.Also,ourdatasuggestthatrecruitmentof Myotis speciesjuvenilesisdecliningandsimilarresultswere foundbyFrancletal.(2012).Werecommendthatfuture studiesmonitortherelativeproportionofnonreproductiveadultsandjuvenilerecruitmentinastudypopulationasindicatorsofWNSimpactsandencouragestudies thatobservefemalesduringpregnancytoreveal mechanismsresponsibleforpuploss.ManagementImplicationsInourlong-termstudyarea,WNS-affectedspecies representabroadecologicalnichethatmaybeseverely affectedaspopulationsdecline(Jachowskietal.2014). ThoughwedemonstratedanimpactofWNS4yafterit reachedIndianacaves,thereisnoguaranteethatthefull effectofWNStothebatsofIndianahasbeenrealized. DeclinesincaptureratesforIndianabatsandlittlebrown batsweresignificant,andweexpectthatasWNS progressestheimpactonpopulationsoftri-coloredbats andnorthernlong-earedbatswillbemoreapparent. Also,becauseWNSisimpactingthereproductivecycleof affectedbats,furtherresearchisneededtodetect changesinrecruitment,especiallyforhighlyaffected species.ThisWNSstudy,unparalleledinthelengthofthe studyterm,providesanexampleofhowwemayuse summercapturenumberstoanalyzetheimpactofa diseasethatinfectsbatsduringthehibernationperiod.SupplementaryMaterialPleasenote:TheJournalofFishandWildlifeManagementisnotresponsibleforthecontentorfunctionality ofanysupplementalmaterial.Queriesshouldbedirected tothecorrespondingauthorforthearticle. TableS1. RecordsofIndianabatsobservedinIndiana cavesduringhibernationsurveysin2011and2013.Bats wereoriginallybandedatalong-termmonitoringsitein centralIndianabetween2002and2012.Thewhite-nose infectionyear,distance,anddirectionislistedforeach cave.Cavesaregroupedbyproximitytoourstudyarea andrepresenttwomajorhibernaculaconcentrationsin Indiana. FoundatDOI:http://dx.doi.org/10.3996/102016JFWM-077.S1(DOCX21.0KB).Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.OÂ’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|76

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TableS2. Listoffactorsanddistributionsforzeroinflatedmixedmodelsusedtopredictbatcapturesata long-termmonitoringsiteincentralIndiana(2002–2014). Themostsupportedmodel,asshownbylikelihoodratio tests,isthefullmodelwithanegativebinomial distribution,Model4.FoundatDOI:http://dx.doi.org/ 10.3996/102016-JFWM-077.S2(DOCX27.4KB). TableS3. Datacontaininginformationonbat capturesfrom2002to2014organizedbysitevisitfora long-termmonitoringstudyincentralIndiana.Foundat DOI:http://dx.doi.org/10.5061/10.3996/102016-JFWM077.S3(CSV1.2MB). TableS4. Predictedprobabilityofwhite-nosesyndrome(WNS)exposureforalong-termbatmonitoring siteincentralIndianaandnumberofWNS-infected cavesinIndianabyyear(2008–2013).Annualvaluesfor thecentralIndianasitewereextractedfromcokriging spatialmodelsdevelopedusingpopulationdatafrom Indianabat Myotissodalis hibernacula.FoundatDOI: http://dx.doi.org/10.3996/102016-JFWM-077.S4(DOCX 18.8KB). TableS5. Parameterestimates,standarderrors, z values,and P -valuesformodelparametersinthelogistic portionofthefinalzero-inflatedmodelpredictingbat capturesatalong-termmonitoringsiteincentralIndiana (2002–2014).FoundatDOI:http://dx.doi.org/10.3996/ 102016-JFWM-077.S5(DOCX34.5KB). TableS6. Parameterestimates,standarderrors, z values,and P -valuesformodelparametersinthecount portionofthefinalzero-inflatedmodelpredictingbat capturesatalong-termmonitoringsiteincentralIndiana (2002–2014).FoundatDOI:http://dx.doi.org/10.3996/ 102016-JFWM-077.S6(DOCX35.2KB). FigureS1. Standarderrorestimatefora2013 cokrigingspatialmodelpredictingwhite-nosesyndrome (WNS)exposureprobabilityacrossacontinuouslandscapeineasternNorthAmerica.Thestandarderror estimateforourlong-termmonitoringsiteincentral Indianawas0.06,suggestingthatpredictedvaluesfor WNSpresence(seeFigure1)wereaccurate.Foundat DOI:http://dx.doi.org/10.3996/102016-JFWM-077.S7(PPT 462KB).AcknowledgmentsDatacollectionwasfundedbytheIndianapolisAirport Authority.J.Pettitwassupportedbyagrantfromthe IndianaDepartmentofNaturalResourcesandassistantshipsfromIndianaStateUniversity.Wethankmanyfield techniciansandgraduatestudentsfordatacollectionand B.Walters,D.Sparks,andN.Gikasfordatamanagement to2012.Wegreatlyappreciatehelpfulcomments providedbytheAssociateEditorandreviewers. Anyuseoftrade,firm,orproductnamesisfor descriptivepurposesonlyanddoesnotimplyendorsementbytheU.S.Government.ReferencesBernardRF,FosterJT,WilcoxEV,PraiseKL,McCracken GF.2015.Moleculardetectionofthecausativeagent ofwhite-nosesyndromeonRafinesque’sbig-earedbat ( Corynorhinusrafinesquii )andtwospeciesofmigratory batsinthesoutheasternUSA.JournalofWildlife Diseases51:519–522. BlehertSD,HicksAC,BehrM,MeteyerCU,Berlowski-Zier BS,BucklesEL,ColemanJTH,DarlingSR,GargasA, NiverR,OkoniewskiJC,RuddRJ,StoneWB.2009.Bat white-nosesyndrome:anemergingfungalpathogen? Science323:227. BoumaHR,CareyHV,KroeseFGM.2010.Hibernation:the immunesystematrest?JournalofLeucocyteBiology 88:619–624. BrooksRT.2011.Declinesinsummerbatactivityin centralNewEngland4yearsfollowingtheinitial detectionofwhite-nosesyndrome.BiodiversityConservation20:2537–2541. CaceresMC,BarclayRMR.2000. Myotisseptentrionalis TheMammalianSpecies634:1–4. CryanPM,MeteyerCU,BoylesJG,BlehertDS.2010.Wing pathologyofwhite-nosesyndromeinbatssuggests life-threateningdisruptionofphysiology.BMCBiology 8:135. CryanPM,MeteyerCU,BoylesJG,BlehertDS.2013. White-nosesyndromeinbats:illuminatingthedarkness.BMCBiology11:47. DzalY,McGuireLP,VeselkaN,FentonMB.2011.Going, going,gone:theimpactofwhite-nosesyndromeon thesummeractivityoftheLittleBrownBat( Myotis lucifugus ).BiologyLetters7:392–394. FentonMB,BarclayRMR.1980. Myotislucifugus .The MammalianSpecies142:1–2. FordWM,BritzkeER,DobonyCA,RodrigueJL,Johnson JB.2011.Patternsofacousticalactivityofbatspriorto andfollowingwhite-nosesyndromeoccurrence. JournalofFishandWildlifeManagement2:125–134. FranclKE,FordWM,SparksDW,BrackVJr.2012.Capture andreproductivetrendsinsummerbatcommunities inWestVirginia:assessingtheimpactofwhite-nose syndrome.JournalofFishandWildlifeManagement 3:33–42. FrankCL,MichalskiA,McDonoughAA,RahimianM,Rudd RJ,HerzogC.2014.TheresistanceofaNorthAmerican batspecies( Eptesicusfuscus )towhite-nosesyndrome (WNS).PLoSONE9:e113958. FrickWF,PollockJF,HicksAC.2010.Anemergingdisease causesregionalpopulationcollapseofacommon NorthAmericanbatspecies.Science329:679–682. FujitaMS,KunzTH.1984. Pipistrellussubflavus .MammalianSpecies228:1–6.Long-termMonitoringtoAssessWhite-NoseSyndromeImpactJ.L.PettitandJ.M.O’Keefe JournalofFishandWildlifeManagement|www.fwspubs.orgJune2017|Volume8|Issue1|77

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