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Title:
High annual survival in infected wildlife populations may veil a persistent extinction risk from disease
Series Title:
Ecosphere
Creator:
Maslo, Brooke
Stringham, Oliver C.
Bevan, Amanda J.
Brumbaugh, Amanda
Sanders, Chris
Hall, MacKenzie
Fefferman, Nina H.
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Ecological Society of America
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Myotis sodalis ( lcsh )
White-nose syndrome ( lcsh )
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serial ( sobekcm )

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Host response to emerging pathogens is variable, causing uncertainty about population‐level impacts and challenging effective disease management. White‐nose syndrome (WNS) has caused catastrophic declines in some bat species, while others appear less impacted. Developing predictive models based on observed survival patterns can generate testable hypotheses about mechanisms driving population dynamics and contribute to the development of targeted approaches to disease management. We conducted a mark–recapture study of federally endangered Indiana bats (Myotis sodalis) during 2011–2016. Annual survival decreased from 0.78 (95% CI: 0.59, 0.89) and 0.79 (95% CI: 0.70, 0.86) for females and males, respectively, in 2011 to 0.74 (95% CI: 0.33, 0.94) and 0.75 (95% CI: 0.53, 0.89) for females and males, respectively, in 2015. We then modeled two explanatory mechanisms potentially driving the observed patterns: (1) phased exposure to disease through the spatial spread of the pathogen within the hibernaculum; and (2) cumulative mortality risk from iterative yearly WNS infection. Under a phased exposure scenario, models suggest that infected individuals have an average survival probability of 0.68, and disease prevalence is predicted to reach 100% within 9 yr of disease emergence. Under the cumulative mortality risk hypothesis, survival probability of individuals decreases with each infection cycle. In either case, infected populations are predicted to stabilize at a negative growth rate. Results suggest that Indiana bats tolerate a pathogen load prior to onset of infection, leading to a less pronounced population decline than for other susceptible species. However, the long‐term risk of WNS to Indiana bats may be more severe than current population trends suggest. To inform current conservation management, we performed a vital rate sensitivity analysis, which suggested that modest increases in survival (4–5%) through targeted intervention may return declining populations to stability (λ = 1.0). Demographic modeling approaches coupled with continued population monitoring can highlight important differences in disease response, and ultimately extinction risk, in host species allowing conservation practitioners to tailor intervention actions so that they will be most effective.
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Volume 8, Issue 12

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Highannualsurvivalininfectedwildlifepopulationsmayveil apersistentextinctionriskfromdiseaseBROOKEMASLO,1,2,OLIVERC.STRINGHAM,1AMANDAJ.BEVAN,1AMANDABRUMBAUGH,3CHRISSANDERS,3MACKENZIEHALL,4ANDNINAH.FEFFERMAN51DepartmentofEcology,EvolutionandNaturalResources,Rutgers,TheStateUniversityofNewJersey,14CollegeFarmRoad, NewBrunswick,NewJersey08901USA2RutgersCooperativeExtension,NewJerseyAgriculturalExperimentStation,Rutgers,TheStateUniversityofNewJersey, 88LipmanDrive,NewBrunswick,NewJersey08901USA3SandersEnvironmental,Inc.,322BorealisWay,Bellefonte,Pennsylvania16823USA4EndangeredandNongameSpeciesProgram,NJDivisionofFishandWildlife,1VanSyckelsRoad,Clinton,NewJersey08809USA5Ecology&EvolutionaryBiology,TheUniversityofTennessee,1416CircleDrive,Knoxville,Tennessee37996USA Citation: Maslo,B.,O.C.Stringham,A.J.Bevan,A.Brumbaugh,C.Sanders,M.Hall,andN.H.Fefferman.2017.High annualsurvivalininfectedwildlifepopulationsmayveilapersistentextinctionriskfromdisease.Ecosphere8(12): e02001.10.1002/ecs2.2001Abstract.Hostresponsetoemergingpathogensisvariable,causinguncertaintyaboutpopulation-level impactsandchallengingeffectivediseasemanagement.White-nosesyndrome(WNS)hascausedcatastrophicdeclinesinsomebatspecies,whileothersappearlessimpacted.Developingpredictivemodels basedonobservedsurvivalpatternscangeneratetestablehypothesesaboutmechanismsdrivingpopulationdynamicsandcontributetothedevelopmentoftargetedapproachestodiseasemanagement.Weconductedamark – recapturestudyoffederallyendangeredIndianabats( Myotissodalis )during2011 – 2016. Annualsurvivaldecreasedfrom0.78(95%CI:0.59,0.89)and0.79(95%CI:0.70,0.86)forfemalesand males,respectively,in2011to0.74(95%CI:0.33,0.94)and0.75(95%CI:0.53,0.89)forfemalesandmales, respectively,in2015.Wethenmodeledtwoexplanatorymechanismspotentiallydrivingtheobservedpatterns:(1)phasedexposuretodiseasethroughthespatialspreadofthepathogenwithinthehibernaculum; and(2)cumulativemortalityriskfromiterativeyearlyWNSinfection.Underaphasedexposurescenario, modelssuggestthatinfectedindividualshaveanaveragesurvivalprobabilityof0.68,anddiseaseprevalenceispredictedtoreach100%within9yrofdiseaseemergence.Underthecumulativemortalityrisk hypothesis,survivalprobabilityofindividualsdecreaseswitheachinfectioncycle.Ineithercase,infected populationsarepredictedtostabilizeatanegativegrowthrate.ResultssuggestthatIndianabatstoleratea pathogenloadpriortoonsetofinfection,leadingtoalesspronouncedpopulationdeclinethanforother susceptiblespecies.However,thelong-termriskofWNStoIndianabatsmaybemoreseverethancurrent populationtrendssuggest.Toinformcurrentconservationmanagement,weperformedavitalratesensitivityanalysis,whichsuggestedthatmodestincreasesinsurvival(4 – 5%)throughtargetedintervention mayreturndecliningpopulationstostability( k = 1.0).Demographicmodelingapproachescoupledwith continuedpopulationmonitoringcanhighlightimportantdifferencesindiseaseresponse,andultimately extinctionrisk,inhostspeciesallowingconservationpractitionerstotailorinterventionactionssothatthey willbemosteffective.Keywords: epidemiology;mark – recapture; Myotissodalis; populationviabilityanalysis; Pseudogymnoascusdestructans; white-nosesyndrome;wildlifedisease. Received 6July2017;revised21September2017;accepted29September2017.CorrespondingEditor:DebraP.C.Peters. Copyright: 2017Masloetal.ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttribution License,whichpermitsuse,distributionandreproductioninanymedium,providedtheoriginalworkisproperlycited. E-mail: brooke.maslo@rutgers.edu www.esajournals.org1December2017Volume8(12)Articlee02001

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INTRODUCTIONFungalpathogensarebecomingincreasingly prevalentasemergingdiseaseagentsandare responsibleforseveralcurrentmajorepizootics (Fisheretal.2012).Notableexamplesinclude Pseudogymnoascusdestructans (white-nosesyndrome[WNS])inbats(Gargasetal.2009), Batrachochytriumdendrobatitis (chytridiomycosis)in frogs(Kilpatricketal.2010), Batrachochytriumsalamandrivorans (chytridiomycosis)insalamanders (Marteletal.2013),and Ophidiomycesophiodiicola (snakefungaldisease)insnakes(Lorchetal. 2015).Hostsusceptibilitytoemergingdiseasesis variable,withsomespeciesdecliningby > 90% andotherspersistingwithendemicinfection (Daszaketal.2003,Langwigetal.2017). Driversofpost-infectionpopulationdynamics likelyincludeacombinationofhostphysiological,genetic,andbehavioralfactors.Forsome species,evolutionaryprocesses(Woodworth etal.2005),compensatoryeffects(Muthsetal. 2011),orchangesinsociality(Langwigetal. 2012)caneitherreducetherateofpopulation declineorpromotepopulationpersistenceinthe presenceofthepathogen.Importantly,however, relativelymoderatepopulationdeclinesmayveil apersistentextinctionrisk.Hostcharacteristics promotingdiseaseresistanceortolerancemaybe negatedbyinter-hostinteractionsthatamplify pathogenprevalenceortransmission(Mideo etal.2008,Ellisetal.2017).Alternatively,populationsovercomingtheacutemortalityassociatedwiththeepidemicphaseofpathogen invasionmayexperiencemoresubtle,chronic negativeimpactsthatmaintainpronouncedvulnerabilitytoextinction. Particularlyformulti-hostpathogens,understandinghoweachspeciesrespondstoan emergingdiseasebecomescriticaltosuccessful intervention.Conservationmanagersoftenface limitedtimeandresourcesandthusmustprioritizespecies,populations,andsiteswhereinterventionwillhavethegreatestimpact(Arponen2012). Uncertaintyinspecies-levelimpactspreventssuch targeteddiseasemanagementplanning,diminishingthepotentialbene tsofconservationactions (Possinghametal.2001)andincreasingtheriskof unintendedoutcomes(i.e.,exacerbatingdeclines; Masloetal.2017).Combiningpopulationmonitoringwithpredictivemodelsaimedatgenerating testablehypothesestoexplainobserveddynamics, theninvestigatingthosehypothesesempirically, canguideconservationeffortsthroughanadaptivemanagementframeworkandultimately increasethepotentialforsuccess. White-nosesyndrome,causedbythefungal pathogen Pseudogymnoascusdestructans (Gargas etal.2009),isadiseaseofhibernatingbatsthat hasrecentlyemergedinNorthAmerica(Warneckeetal.2012).AlthoughWNShasbeenconrmedinmultiplebatspecies(Blehertetal. 2009),thereexistsconsiderablevariabilityin infectionintensityandimpactonhostpopulation dynamics(Fricketal.2015,2017).Asanexample,initialdeclinesoflittlebrownbats( Myotis lucifugus )averaged73%,leadingtopredictions ofregionalextirpationinlessthantwodecades (Fricketal.2010 a ).Incontrast,thecloselyrelated Indianabat Myotissodalis hasexperiencedmuch lessseverepopulation-levelimpactsacrossmost ofitsinfectedrange(Fricketal.2015).Countsof multiplehibernatingcolonieshaveestimatedan ~ 6%reductioninaveragegrowthrateforWNSinfectedpopulations(Langwigetal.2012).These data,coupledwithrecentevidenceofreduced pathogenloadsoninfectedindividuals(Frick etal.2017),suggeststhatIndianabatsmaybe bufferedagainstextirpationfromWNS. Here,wepresentthesex-speci candtemporal trendsinIndianabatsurvivalgeneratedfrom ve yearsofmark – recapturedatafromaWNS-infected hibernaculum.Basedontheseempiricalestimates, wegeneratetwohypothesestopotentiallyexplain themechanismsdrivingobservedsurvivalpatterns:(1)spatialspreadof P.destructans withina hibernaculumresultinginaphasedexposureof Indianabatstoaninfectivedose(i.e.,leadingto disease);and(2)Indianabatsexperiencingcumulativemortalityriskfromrepeatedexposuretothe pathogen.Usingmathematicalmodelingapproaches,wepredictthefuturedynamicsofIndiana batpopulationsundereachscenario.METHODSMark – recapturemethodsWeconducted eldworkfrom2011to2016at thewesternshaftoftheMt.HopeMinecomplex locatedonprivatelyownedlandinRockaway, NewJersey,USA.Thisgated41-mverticalshaftis theroostsiteofthelargestknownhibernating www.esajournals.org2December2017Volume8(12)Articlee02001MASLOETAL.

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colonyofIndianabatsinNewJerseyandwasconrmedasaWNS-infectedsitein2011usingUV uorescence(Turneretal.2014,Fricketal.2017). Ineachprojectyear,wecapturedIndianabatsduringthefallswarm(August – October)overthree separatethree-nightsamplingevents.Wecaptured batsusingtwoharptraps(ModelG7;BatConservationandManagement,Carlisle,Pennsylvania, USA)andthree38-mmmesh,2.6-mmistnets (Avinet,Freeville,NewYork,USA)placedat6,9, and12mheights.Wepositionedtheharptrapsat thegatesurroundingtheshaftopening,andwe stationedonemistnetadjacenttotheshaftopening.Wedeployedtwomistnetswithin200m fromtheshaftopening,oneonanearbyabandonedminingroadandoneattheentrancetoan exposedrockgorge.Webandedcapturedindividualswithunique2.9-mm(in2011)or2.4-mm (2012 – 2016)lippedalloybands(Porzana,Icklesham,UK)andrecordedtheirage(young-of-theyearoradult, > 1yr;Brunet-RossiniandWilkinson 2009)andsex.Bandingactivitieswereconducted underannuallyissuedNJDivisionofFishand WildlifeScienti cCollectingPermitsandgenerally followedboththeUnitedStatesFishandWildlife ServiceRange-wideIndianaBatSummerSurvey Guidelines,aswellasthemethodsofKunzand Parsons(2009).All eldpersonnelfollowed nationalWhite-NoseSyndromeDecontamination Protocolsduringallvisits.SurvivalestimationWeusedthestandardCormack-Jolly-Seber modeltoestimateannualapparentsurvival, S andrecaptureprobability, p (Lebretonetal.1992). Wegenerated19aprioricandidatemodelscontainingcombinationsofconstant,yearly,time trend,andsex-speci ceffectsonannualsurvival andrecaptureprobabilities(AppendixS1: TableS1).Becausethesamplesizeprecluded meaningfulage-speci cinferencestobedrawn, weexcludedage-relateddatafromallanalyses. Totestmodel t,weusedaparametricbootstrappingprocedurewith500simulationsofourglobal model,whichincludedfullytime-dependentand sex-speci csurvivalandrecapture.Weranked candidatemodelsby D QAICC,whichrepresents therelativelikelihoodofthemodel,giventhedata (JohnsonandOmland2004).Toreducemodel selectionbiasanduncertainty,wecalculatedestimatesbyaveragingparameterswithinallmodels returninga D QAICC< 2(BurnhamandAnderson 2002,Burnhametal.2011).Modelingpopulationdynamicsunderaphased exposureto P.destructansStudieshaveshownthatprevalenceof P.destructans onIndianabatswithinahibernaculumnears100%withinthreeyearsofitsarrivalto asite(Fricketal.2017),butindividualshave moderate P.destructans loadsrelativetospecies thatexperiencedmassiveinitialdeclines(Hoyt etal.2016).Wehypothesizedthatthespatial spreadof P.destructans withinahibernaculum couldresultinaphasedexposureofIndianabats toaninfectivedose( P.destructans loadcausing diagnosticsigns)ofWNS.Weproposetodifferentiatebetweenaninoculumthatresultsinapositive P.destructans laboratorytestandan “ infective dose ” suf cienttoleadtoactivepathologyinthe hostbat.Inthiscase,survivalprobabilities derivedfrommark – recaptureoperationswould re ectthepopulationaverage.However,thepopulationconsistsofbothinfectedanduninfected individualsthataresurvivingattwodifferent rates.Tocalculatethe “ true ” survivalprobability ofinfectedindividuals,wedisaggregatedthe Indianabatpopulationintotwodiscretecompartments(uninfectedandinfected),whereindividualsfromtheuninfectedcompartmentcancontract WNSandjointheinfectedcompartmentwhere theyremainuntildeath.Wemodeledthepopulationgrowthofbothcompartmentsusingthefollowingsetofexponentialgrowthequations: Ut 1 kuUt at(1) It 1 kiIt at(2) where Itand Utrefertothenumbersofbatsin theinfectedanduninfectedcompartments, respectively, k isthecompartment-speci c growthrate(speci edbythesuperscripts i and u ), atisthenumberofbatsnewlyinfectedby transmissioninyear t ,andthesubscript t denotestimeinyears. Tosimulatepopulationgrowth,wecalculated kuasthedominanteigenvaluefortheuninfected compartmentusingthefollowingtwo-stage Lefkovitchmatrix(MorrisandDoak2002): kum Sj Bj mjSa Ba maSjSa m (3) www.esajournals.org3December2017Volume8(12)Articlee02001MASLOETAL.

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where m istheeigenvectorassociatedwiththe uniquelargestpositiveeigenvalue; S represents survivalofuninfectedIndianabats; B represents theproportionofuninfectedfemalesbreeding; m isfecundity;andthesubscriptsjandaindicate valuesforjuvenile(i.e., rst-year)oradultbats, respectively.Becausetheestimatedsurvival probabilityfor2011generatedfromthemark – recaptureanalysiswasconsistentwithliterature describingIndianabatdynamicsjustpriortothe emergenceofWNS(Thogmartinetal.2012),we usedthisvaluetoparameterizeadultsurvivalin thematrix( Sa).Weset rst-yearbatsurvivalasa constantproportion(0.47)ofadultsurvival (Fricketal.2010 a ,Masloetal.2015),andwe heldfecundityconstantat m = 1,asIndianabats typicallyproduceasinglepupperyear(Barclay andHarder2003).Weassignedbreedingproportionvaluesfor rst-yearbatsandadultsas Bj= 0.38and Ba= 0.85,respectively,basedon estimatesreportedinthecloselyrelatedlittle brownbatbecausenocurrentempirically deriveddataforIndianabatsexist(Reichardand Kunz2009,Fricketal.2010 b ,Masloetal.2015). Wecalculatedthegrowthrateoftheinfected compartment, ki,byusingtheexponential growthequationsubdividedintothetwocompartmentsandweightedbytheproportionof infectedindividualsinagivenyear, pt: Kw t 1 pt ku ptki(4) where Kw trepresentsthegrowthrateoftheentire populationinanygivenyear, t ,calculatedby populatingtheabovematrixwiththeempirically derivedsurvivalprobabilitiesfor2012.Initially, weassumedthat5 – 15%ofthepopulation becameinfectedbythesecondyear. Tocalculate It,we rstdeterminedtheproportionofindividualswhoareintheinfectedcompartmentduringagivenyear, pt,bysolvingfor ptkiinEq.4.Wethencalculatedthenumberof infectedbatsinaspeci edyear: It ptNtwhere Ntistheprojectedtotalpopulationsizeat time t givenexponentialgrowthwith Kw t,andan initialpopulationsizeof409(USFWS2017).We thensolveforthenumberuninfectedbatsthat becomeinfectedduringaspeci edyear, at, accordingtoanassumedTypeIfunctional responsecurve(i.e.,linear): at j It p (5) where j and p aretheslopeandinterceptofa linearregressionestimatingtherelationshipbetweenthenumberofuninfectedbatsthatbecame infected( at)andthetotalnumberofbats( It).A TypeIfunctionalresponseissimilartohow transmissionismodeledinabasicsusceptibleinfected-recoveredepidemiologicalmodeland assumesthatthecontactratebetweenindividualsineithercompartmentisproportionaltopopulationdensity(McCallumetal.2001). Todeterminethelong-termdynamicsofthe population,weprojectedtheinitialpopulation 20yrintothefutureusingEqs.1and2and tracking U I ,and N. Weaddedstochasticeffects byrunning1000iterationsofthemodel,drawing fromnormaldistributionswithastandarddeviationof0.1ofeachmean kuand ki.Becausethe Indianabatpopulationislow,therearelikelyno density-dependenteffects;weignoredpotential Alleeeffectsbecausenodataareavailableforbat populationsreducedbyWNS.ModelingcumulativemortalityrisktoIndiana batsfromiterativeWNSinfectionGrowthof P.destructans istemperaturedependent(Verantetal.2012),andinfectedbatssurvivingthehibernationperiodcanclearfungal loadsduringthesummerseason.Batsarethen reinfectedupontheirreturntohibernationsites, whichserveasenvironmentalreservoirs(Lorch etal.2013).WehypothesizedthatIndianabats couldbeexperiencingsystemicphysiological degradationfromWNSsuchthatsurvivalprobabilitydecreaseswitheachrepeatedexposureto P.destructans. Wethuscalculatedtheimpactof eachaccumulationofyearsofdiseaseexposure asamixedratesproblem.Weassumedthatin theabsenceofthepathogenallvitalrateswere constant,andweusedthemeanobserved2011 survivalprobabilitygeneratedfromthemark – recaptureanalysisastheuninfectedbaseline.We thenassumedthattheobservedannualdecrease insurvivalwastheimpactsolelyofdiseaseintroductionintothepopulation(Thogmartinetal. 2012).Using2012asthe rstyearunderdisease in uence,weassumedthatalladultssurviving inthepopulationwerelivingwiththeburdenof oneyearofdiseaseexposure.In2013, rstt-year batsbornin2012wouldthenbeexposedto www.esajournals.org4December2017Volume8(12)Articlee02001MASLOETAL.

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WNSforasingleyear,butallothersurviving adultsnowcarriedtheburdenoftwoyearsof exposure.In2014, rst-yearbatsexperienceda singleyearofexposure,2-yr-oldbatshadtwo yearsofexposure,andalloldersurvivingadults existedwiththeburdenofthreeyearsofexposure.BaseduponlongevityrecordsforIndiana bats(ParadisoandGreenhall1967,Humphrey andCope1977),weusedamaximumlife expectancyof11yr.Therefore,interactionof post-exposuredemographywasstableonlyafter 10yrofdiseasepresenceinthepopulation.At thistime,therewouldnolongerbemultipleage classesexperiencingthesamenumberofyearsof exposure;rather,numberofyearsofexposurewouldsimplybedeterminedbyanindividual ’ sage. Basedupontheseassumptions,wecalculated thesurvivalpenaltyIndianabatsincurwitheach cumulativeWNSinfectioncycle.Wede ne skas theaveragesurvivalprobabilityforeachage k adultclassintheyearspriortoWNSemergence (asestimatedbythemark – recaptureanalysis). Wethende ne s kasthemodi edsurvivalin eachageclass k ,basedonthedurationofexposureineachyear t (inthiscase,from2012to 2015).Becauseweknowtheaverageannualsurvivalprobabilityoverallageclassesduringthese years, St,fromthemark – recapturedata,wecan solveforthepenaltyassociatedwitheachaccumulationofyearsofexposure, et,foreachyear accordingtotheequation St Pks kxkk where xkistheproportionofindividualsinage class k ,and s k skpt 2011if t 2011 k skekif t 2011 [ k (6) Becausetheobservationalwindowincludes onlyfouryearsofdatafollowingWNSintroduction,wehypothesizedtwopotentialfunctional formsfortheshapeoftheexposurepenaltylastingmorethanfouryearsinduration:linearand logarithmicprogression.Tode nethese,we employedastandardcurve ttingalgorithmfor linearandlogarithmicfunctions(minimizing sumofsquareddifferences)onthefourpenalties: e1, ... ,e4.Wethenusedthosetwo tfunctionsto projecttheprogressionofthepenaltyforyears5 through11.Usingthepenaltymodi erstothe survivalprobabilities(i.e.,the s kforeachsubsequentyear),wethenprojectedthepopulation overthe rst10yrfollowingWNSemergence usingstandardLesliematrixcalculationsand calculatedtheexpectedpopulationgrowthrate atstability(i.e.,theassociateddominanteigenvalueforthematrixusingthe s kfor k > 11).VitalratesensitivityanalysisTodeterminehowbesttorapidlyincrease populationsizeofaninfectedIndianabatcolony inashorttimeframe,weusedavitalratesensitivityanalysis(VRSA).Thisapproachismore advantageousthantraditionalsensitivityanalyses(e.g.,MorrisandDoak2002)becausethe stableagedistributionassumptioncanberelaxed (FeffermanandReed2006),whichisbene cial whenpopulationsareundergoingrapiddeclines (e.g.,FeffermanandReed2006,Reedetal.2009). Further,vitalratesensitivityanalysesfocuson maximizingpopulationsizeoverashorttimeframe,whichcanbecriticalforconservation action(Fieldetal.2007).Tobeconservative,we populatedtheVRSAmatrixwiththelowestsurvivalestimategeneratedfromourdata. BasedonthestatusofongoingresearchprojectsonWNSmanagement,publishedliterature onpotentialmanagementactions(Cornelison etal.2014,WilcoxandWillis2016,Masloetal. 2017),andtheresultsofoursurvivalanalysis,we developedthreemanagementstrategiesfor returninginfectedIndianabatcoloniestostable populationgrowth( k = 1):(1)increasingadult annualsurvival;(2)increasingadultandjuvenile annualsurvival;and(3)increasingadultand juvenilereproduction.Foreachstrategy,wecalculatedthe10-yrcumulativegrowthrate( k10) and nalpopulationsizeofthecolonyresulting fromagivenpercentageincreaseintherelevant vitalrate(s).Weprojectedtheinfectedpopulation vectorthroughthematrixandbeganvitalrate perturbationsinyear2ofWNSinfection.To accountforuncertainty,weran10,000iterations oftheVRSAprojectionsforeachpopulation structureinaMonteCarlosimulation,incorporatingstochasticity(asabove)bydrawingadult andjuvenilesurvivalfrombetadistributions wherethestandarddeviationwassetto0.1. www.esajournals.org5December2017Volume8(12)Articlee02001MASLOETAL.

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RESULTSSurvivalofIndianabatsFrom2011to2016,wecaptured670Indiana bats(617males,53females);ofthese,328individualswererecapturedinsubsequentyears.The goodness-ofttestreturnedavariancein ation factorof ^ c = 1.26forourglobalmodel,indicating modestoverdispersioninourdata;thus,we adjustedoursmallsamplecorrectedquasiAkaike ’ sInformationCriterion(QAICC)bythis value(BurnhamandAnderson2002).Model resultsshowedstrongsupportforalinear decreasingtrendinsurvivalsincearrivalofWNS (Table1).Ofthe19candidatemodelstested,68% oftheAkaikeweightswerecapturedinthetop twomodels,whichreturneda D QAICc< 2. Model-averagedsurvivaldecreasedfrom0.78 (95%CI:0.59,0.89)and0.79(95%CI:0.70,0.86) forfemalesandmales,respectively,in2011to0.74 (95%CI:0.33,0.94)and0.75(95%CI:0.53,0.89) forfemalesandmales,respectively,in2015 (Fig.1).Theanalysissuggestednosigni cantdifferencesinsurvivalbetweenthesexes,whichboth decreasedatarateof ~ 1%peryear(Fig.1). Recaptureratesdidvarysigni cantlybetweenthe sexes,rangingfrom0.04(95%CI:0.00,0.30)to 0.06(95%CI:0.01,0.39)forfemalesand0.22(95% CI:0.16,0.28)and0.51(95%CI:0.43,0.59)for males,likelybecausebandingoperationsoccurred duringthefallswarm(Fenton1969,Cope1976).Withinhibernaculumspatialspreadof P.destructansTheuninfectedIndianabatcompartment growthratewaspositive,at k = 1.05.Wecalculatedsurvivalofinfectedindividualsas0.68 (95%CI:0.58,0.71).Modelresultsindicatean infectivedoseof P.destructans spreadswithinthe populationatarateof ~ 12.5%annually(Fig.2). WhilepopulationsizeofIndianabatsinitially appearstobeincreasingintheyearofdisease emergence,theproportionofinfectedbatsgraduallyincreasesto100%withinnineyears.Inthis model,whentheproportionofinfectedbats become > 36%,theoverallgrowthrateofthepopulationbecomesnegativeandeventuallystabilizesat k = 0.91(9%annualdecline)whenthe proportionofinfectedbatsis100%.CumulativemortalityriskofiterativeWNS infectionBasedontheempiricaldatageneratedthrough themark – recaptureanalysis,theexposurepenaltyincreasesfrom0.987inthe rstyearofinfectionto0.845after11yrunderalinearprogression (Table2),increasinginseverityby ~ 1.4%with eachWNSinfectioncycle.After11yr,thepopulationstabilizesatasurvivalprobabilityof s k= 0.71 andagrowthrateof k = 0.993(Fig.3).Undera logarithmicprogression,survivalstabilizesat s k= 0.73resultingfromanexposurepenaltythat graduallylessensinmagnitudewitheachWNS infectioncycle(Table2).Populationgrowthrate stabilizesat k = 0.9991(Fig.3). Table1.Topeightaprioricandidatemodelsusedfor estimatingsurvivalandrecaptureprobabilitiesfor Indianabats( Myotissodalist ; N = 670)atMt.Hope Mine,Rockaway,NewJersey,USA.ModelQAICcD QAICcw S (time), p (year,sex)1797.060.000.36 S (time,sex), p (year,sex)1797.280.210.32 S (constant,sex), p (year)1799.312.250.12 S (constant), p (year,sex)1799.352.290.11 S (constant,sex), p (year,sex)1801.003.940.05 S (time,sex), p (year)1802.625.560.02 S (year), p (year,sex)1804.567.500.01 S (year,sex), p (year,sex)1807.5410.50.00 Notes: Toptwomodelsinboldface( D QAICc)wereused formodel-averagedsurvivalparameterestimation.QAICc, quasi-Akaike ’ sInformationCriterioncorrectedforsmallsamplesize; D QAICc,differencebetweentheQAICcvalue betweeneachmodelandthetopmodel; w ,quasi-Akaike weight; S ,survival; p ,recaptureprobability;time,lineartime trend;year,yearlyvariation. Fig.1.Model-averagedsurvivalestimatesand95% con denceintervalsforfemaleandmaleIndianabats ( Myotissodalis )capturedatMt.HopeMine,Rockaway, NewJersey,USA,from2011to2016. www.esajournals.org6December2017Volume8(12)Articlee02001MASLOETAL.

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VitalratesensitivityanalysisOverall,increasingadultandjuvenilesurvival (ManagementStrategy2)hasthegreatestcumulativeimpactonpopulationgrowthofinfected Indianabatcolonies(Tables3 – 5).A4%increase inthesevitalratesreturnsaninfectedpopulation tostablegrowth( k10= 1)in10yr.Outcomesof increasingadultsurvival(ManagementStrategy 1)areonlymarginallylower,withpopulation growthreaching k10= 1aftera5%increasein annualsurvival.Incontrast,bothadultandjuvenilereproductionmustbeincreased(ManagementStrategy3)by28%toachievestability.DISCUSSIONOurworkprovidesthe rstempirically derivedsurvivalestimatesforIndianabatsafter thearrivalofWNS.Estimatesareconsistentwith observationsthattheIndianabatpopulationwas experiencingaverageannualgrowthof1.4%in thetwodecadespriortodiseaseemergence (Thogmartinetal.2012).Whilesomehibernating colonieshavedecreasedby > 80%afterWNS (Thogmartinetal.2012),therehavebeenlimited observationsofmassivemortalityevents.Indeed, populationdeclinesforIndianabatshavebeen markedlylessseverethanforothersusceptible species(Fricketal.2015).Ourresultssupport theseobservationsandshowthatannualsurvivalremainshighevenwhen Pseudogymnoascus destructans hasbeendocumentedatasite. Underaphasedexposurescenario,Indiana batsmaybeescapingsigni cantpopulation-level impactsthroughaslowedtransmissionrate,as modelresultsindicateittakesnineyearsforthe entirepopulationtobecomeinfected.Prevalence of P.destructans onsubstratessmalldistances Fig.2.PredictedpopulationdynamicsforIndiana bats( Myotissodalis )experiencingaphasedexposureto aninfectivedoseof Pseudogymnoascusdestructans resultingfromincreasingspatialspreadofthepathogenwithinthehibernaculum.Solidblueandredlines indicatethechangeinthenumberofuninfectedand infectedbats,respectively,overtheyearsforwhich empiricaldataonsurvivalexist(2011 – 2015).Dotted linesillustratepopulationprojectionsalongwith95% con denceintervals. Table2.Predictedsurvival, s i,ofIndianabats( Myotissodalis )andpenalty, et, incurredwitheachyearofinfection underacumulativeriskofiterativeexposureto Pseudogymnoascusdestructans hypothesis.SurvivalLinearLogarithmicExposurepenaltyLinearLogarithmic s00.780.78 s 10.770.77 e10.9870.987 s 20.760.76 e20.9740.974 s 30.750.75 e30.9600.960 s 40.740.74 e40.9440.944 s 50.730.74 e50.9310.942 s 60.730.74 e60.9160.936 s 70.720.73 e70.9020.932 s 80.720.73 e80.8880.928 s 90.710.73 e90.8730.924 s 100.710.73 e100.8590.921 s 110.710.73 e110.8450.918 Note: Estimatesarereportedforbothlinearandlogarithmicdecayfunctions. www.esajournals.org7December2017Volume8(12)Articlee02001MASLOETAL.

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fromroostingbatsislessthanunderroosting bats(Langwigetal.2015),suggestingthatat leastduringtheearlyyearsofdiseasepresence transmissionisprimarilybat-to-bat(e.g.,Indiana batsoccupyingahibernaculumwithinfectedlittlebrownbatsmaynotbeimmediatelyexposed unlessroostinginthesamecluster).Whilesimilarintimescale,thepossibilityofincreasing cumulativeimpactsfromongoingexposure yieldsadifferenttrajectoryforpopulation decline.Underthisscenario,itisnotuntilthe durationofpathogenpresenceinthepopulation approachesthelifeexpectancyofthehoststhat thefullnegativeimpactofdiseaseexposurewill beobservableintheage-speci cvitalratesofall agesand,therefore,fortheentirepopulation. Ineithercase,thegenerallyhighsurvivalestimatesderivedfromthemark – recapturedata indicatethatIndianabatshaveahighertolerance of P.destructans relativetootheraffectedspecies. Ourresultsareconsistentwithotherstudies examiningWNSimpacts,whichfoundIndiana Fig.3.PredictedpopulationdynamicsforIndiana bats( Myotissodalis )experiencingacumulativemortalityriskassociatedwithrepeatedexposureto Pseudogymnoascusdestructans .Thesolidlinedepictsthe populationtrajectoryunderalinearprogression;the dottedlineillustratesthepopulationtrajectoryundera logarithmicprogression. Table3.Outcomesofincreasingsurvivalofinfected adultIndianabats(ManagementStrategy1),aspredictedbyvitalratesensitivityanalysis(VRSA).Percentageincrease SaD N † k10‡ 00.68 380.95 10.69 310.96 20.70 230.97 30.71 150.98 40.72 9.50.99 50.7321.00 60.74151.01 70.75221.02 80.76361.03 90.77501.04 100.78601.05 110.79701.06 120.80881.07 130.811031.08 140.821081.09 150.831301.09 160.841391.10 170.851671.10 180.861721.11 190.871931.12 200.882091.13 † D N valuesrepresentthechangeinpopulationsizefrom (year0)to(year10)oftheVRSA. ‡ k10representsthecumulativeannualgrowthrate derivedfromtheVRSA. Table4.Outcomesofincreasingsurvivalofinfected adultandjuvenileIndianabats(ManagementStrategy2),aspredictedbyvitalratesensitivityanalysis (VRSA).Percentageincrease SaSjD N † k10‡ 00.680.32 380.95 10.690.33 310.97 20.700.34 230.97 30.710.35 120.99 40.720.3611.00 50.730.37161.01 60.740.38231.02 70.750.39401.03 80.760.40531.04 90.770.41681.05 100.780.42831.06 110.790.431061.07 120.800.441271.08 130.810.451501.10 140.820.461701.10 150.830.471911.11 160.840.482151.12 170.850.492451.13 180.860.502691.14 190.870.513041.15 200.880.523301.16 † D N valuesrepresentthechangeinpopulationsizefrom (year0)to(year10)oftheVRSA. ‡ k10representsthecumulativeannualgrowthrate derivedfromtheVRSA. www.esajournals.org8December2017Volume8(12)Articlee02001MASLOETAL.

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batssustain P.destructans loadssimilartoless affectedspeciesbothinitsinvasiverangeaswell asitsendemicrangewhereWNScauseslittle mortality(Puechmailleetal.2011,Hoytetal. 2016,Fricketal.2017).Reducedmortalitymay bedrivenbyphysiologicalmechanisms(i.e., interactionswiththecutaneousmicrobiome, increasedfatreserves),epidemiology(delayedor decreasedtransmissionratesleadingtolower infectionintensity),orsuboptimalhabitatsuitabilityfor P.destructans whereIndianabatsroost. Giventhatsomehibernatingcolonieshave declineddramatically(Thogmartinetal.2012),it isnotlikelythatthespeciespossessesaninherent geneticresistance. Despitehighsurvivalrates,however,we foundstrongevidenceforadecliningtrendin thisvitalrateovertimesincediseaseemergence, andbothpopulationmodelsstabilizeatnegative growth.Therefore,theapparenttoleranceof P.destructans byIndianabatsmaynotbeindicativeofreducedlong-termextinctionrisk.Subtle cumulativecosts,aggregatingovertime,may insidiouslycompromisepopulationpersistence inwaysthattakeadecadeormoretoreachtheir fullimpact(duetobaselinehostlifeexpectancy). Infact,thethreattoIndianabatpopulationviabilitymaybeassevereasthatofbatspeciesthat haveexperiencedhighpopulation-levelimpacts overthe10yrthatWNShasbeenpresentin NorthAmerica(e.g.,littlebrownbats).Inareas where P.destructans rstestablishedinNorth America,somepopulationsoflittlebrownbats andthehighlyimpactedtricoloredbat( Perimyotissub avus )arepersisting(Fricketal.2017). Studieshaveshownthatlittlebrownbatsurvival reboundsandexhibitsgradualimprovement eachyearfollowingtheinitialmassmortality event,suggestingthatresistancetoWNSinfectionmayexistinsomepopulations(Masloetal. 2015).Forthisspecies,WNSmayhaveimposed astrongselectivepressuresuchthatasurviving phenotypeisbecominglyincreasinglyrepresentedinthesepopulationsandreturningthem topositivegrowth(MasloandFefferman2015). TheselectiveforcesactingonIndianabats appeartobeconsiderablyweaker,asevidenced bythegradualpopulationdeclineandthelackof signi cantmortalityinmostsites.Therefore, evolutionaryprocessesareunlikelytorescue populationsfromextirpationevenifresistant genotypesarepresent. Lesspronouncedpopulation-levelimpacts, however,likelyrenderproposedconservation actionsmorefeasible.Asshownwithlittle brownbats(Masloetal.2015,2017),actively improvingreproductionhaslittleimpactonpopulationrecoveryrelativetoincreasingsurvival; therefore,captivebreedingprogramsarenot likelycost-effective.Slightincreasesinadultand Table5.Outcomesofincreasinginfectedadultand juvenileIndianabatreproduction(Management Strategy3),aspredictedbyvitalratesensitivity analysis(VRSA).Increase(%) BaBjD N † k10‡ 00.580.12 380.95 10.590.13 370.96 20.600.14 350.96 30.610.15 340.96 40.620.16 320.96 50.630.17 320.96 60.640.18 310.96 70.650.19 300.97 80.660.20 290.97 90.670.21 280.97 100.680.22 270.97 110.690.23 260.97 120.700.24 250.97 130.710.25 220.98 140.720.26 200.98 150.730.27 170.98 160.740.28 150.98 170.750.29 140.99 180.760.30 120.99 190.770.31 110.99 200.780.32 100.99 210.790.33 90.99 220.800.34 80.99 230.810.35 60.99 240.820.36 41.00 250.830.37 11.00 260.840.3801.00 270.850.3921.00 280.860.4041.00 290.870.4161.01 300.880.4281.01 310.890.4391.01 320.900.44111.01 330.910.45131.01 340.920.46151.01 350.930.47171.02 † D N valuesrepresentthechangeinpopulationsizefrom (year0)to(year10)oftheVRSA. ‡ k10representsthecumulativeannualgrowthrate derivedfromtheVRSA. www.esajournals.org9December2017Volume8(12)Articlee02001MASLOETAL.

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juvenilesurvivalcouldhelpIndianabatpopulationstopersistovertheshortterm.Currently, severalalternativesforchemicalandbiological controlof P.destructans haveshownpromising inhibitorypropertiesinthelaboratory(Cornelisonetal.2014,Hoytetal.2015,Raudabaugh andMiller2015,Padhietal.2016);however, thesestrategiesfaceconsiderablechallenges beforethetreatmentofinfectedpopulationscan besuccessful.Treatmentef cacyinthewildis notyetknown,andeconomicandlogisticalconstraintssigni cantlyreducethepercentofthe infectedpopulationthatfeasiblycanbetreated. Habitatmodi cationapproaches(i.e.,heated roostboxes;WilcoxandWillis2016)maypositivelyimpactbothvitalratesbydirectlyimprovingsurvival(throughreducedenergycosts)and indirectlyimprovingreproduction(birthsearlier inthesummer).ForspecieslikeIndianabats decliningatslowertimescales,targetedinterventionevenwithmodestresultsmayreturn infectedpopulationstostationarydynamics. Theoppositesurvivalpatternsexhibitedby Indianabatsandthecloselyrelatedlittlebrown bats(Masloetal.2015)reinforcethatvariation existsintheimpactsemergingpathogenshave onhostspecies.Slightdifferencesinphysiology orbehaviormayresultinmarkedlydifferent responses,leadingtonoticeablevariationin demographyearlyinthediseasechronology. Modestdeclinesmayleadtoafalsesenseof assurancethatapopulationcanpersist.Inthe caseofmulti-hostpathogens,aone-sizets-all diseasestrategyislikelyineffectiveinreaching conservationgoals.Demographicmodeling approachescoupledwithcontinuedpopulation monitoringcanhighlightimportantdifferences indiseaseresponse,andultimatelyextinction risk,inhostspecies,allowingconservationpractitionerstotailorinterventionactionssothatthey willbemosteffective.ACKNOWLEDGMENTSWethankmultiple eldtechnicianswhoassistedin thecollectionofmark – recapturedataatMt.Hope Mine,aswellasJ.Chenger,B.Hines,andC.Herzogfor fruitfuldiscussionsontheobserveddynamicsof IndianabatpopulationsacrosstheWNS-infectedrange. TheUnitedStatesFishandWildlifeServiceWhitenoseSyndromeResearchSmallGrantsProgram, administeredthroughtheWildlifeManagementInstitute,providedfundingforthiswork(Awardnumber 69-2B29-12-176).LITERATURECITEDArponen,A.2012.Prioritizingspeciesforconservation planning.BiodiversityandConservation21:875 – 893. Barclay,R.M.,andL.D.Harder.2003.Lifehistoriesof bats:lifeintheslowlane.Pages209 – 253 in T.H. KunzandM.B.Fenton,editors.Batecology. UniversityofChicagoPress,Chicago,Illinois, USA. Blehert,D.S.,A.C.Hicks,M.Behr,C.U.Meteyer,B. M.Berlowski-Zier,E.L.Buckles,J.T.Coleman,S. R.Darling,A.Gargas,andR.Niver.2009.Bat white-nosesyndrome:Anemergingfungalpathogen?Science323:227. Brunet-Rossini,A.K.,andG.S.Wilkinson.2009.Methodsforageestimationandthestudyofsenescence inbats.Pages315 – 325 in T.H.KunzandS.Parsons,editors.Ecologicalandbehavioralmethods forthestudyofbats.TheJohnsHopkinsUniversity Press,Baltimore,Maryland,USA. Burnham,K.P.,andD.R.Anderson.2002.Model selectionandmultimodelinference:apractical information-theoreticapproach.Springer,New York,NewYork,USA. Burnham,K.P.,D.R.Anderson,andK.P.Huyvaert. 2011.AICmodelselectionandmultimodelinferenceinbehavioralecology:somebackground, observations,andcomparisons.BehavioralEcologyandSociobiology65:23 – 35. Cope,J.1976.Populationecologyofthelittlebrown bat, Myotislucifugus inIndianaandNorth-central Kentucky.AmericanSocietyofMammalogistsSpecialPublication4:81. Cornelison,C.T.,K.T.Gabriel,C.Barlament,andS.A. CrowJr.2014.Inhibitionof Pseudogymnoascus destructans growthfromconidiaandmycelial extensionbybacteriallyproducedvolatileorganic compounds.Mycopathologia177:1 – 10. Daszak,P.,A.A.Cunningham,andA.D.Hyatt.2003. Infectiousdiseaseandamphibianpopulationdeclines.DiversityandDistributions9:141 – 150. Ellis,V.A.,M.C.Medeiros,M.D.Collins,E.H.Sari, E.D.Coffey,R.C.Dickerson,C.Lugarini,J.A. Stratford,D.R.Henry,andL.Merrill.2017.Prevalenceofavianhaemosporidianparasitesis positivelyrelatedtotheabundanceofhostspecies atmultiplesiteswithinaregion.ParasitologyResearch116:73 – 80. Fefferman,N.H.,andJ.M.Reed.2006.Avitalrate sensitivityanalysisfornonstableagedistributions www.esajournals.org10December2017Volume8(12)Articlee02001MASLOETAL.

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