Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites


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Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites
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PLOS ONE
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Schaik, Jaap van
Janssen, René
Bosch, Thijs
Haarsma, Anne-Jifke
Dekker, Jasja J. A.
Kranstauber, Bart
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PLOS
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Bats -- Hibernation ( lcsh )
Swarming (Zoology) ( lcsh )
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serial ( sobekcm )

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During autumn in the temperate zone of both the new and old world, bats of many species assemble at underground sites in a behaviour known as swarming. Autumn swarming behaviour is thought to primarily serve as a promiscuous mating system, but may also be related to the localization and assessment of hibernacula. Bats subsequently make use of the same underground sites during winter hibernation, however it is currently unknown if the assemblages that make use of a site are comparable across swarming and hibernation seasons. Our purpose was to characterize the bat assemblages found at five underground sites during both the swarming and the hibernation season and compare the assemblages found during the two seasons both across sites and within species. We found that the relative abundance of individual species per site, as well as the relative proportion of a species that makes use of each site, were both significantly correlated between the swarming and hibernation seasons. These results suggest that swarming may indeed play a role in the localization of suitable hibernation sites. Additionally, these findings have important conservation implications, as this correlation can be used to improve monitoring of underground sites and predict the importance of certain sites for rare and cryptic bat species.

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RESEARCHARTICLEBatsSwarmWhereTheyHibernate: CompositionalSimilaritybetweenAutumn SwarmingandWinterHibernation AssemblagesatFiveUndergroundSitesJaapvanSchaik1* ,RenéJanssen2,ThijsBosch3,Anne-JifkeHaarsma4,JasjaJ. A.Dekker5 ¤,BartKranstauber6,71 DepartmentofBehaviouralEcologyandEvolutionaryGenetics,MaxPlanckInstituteforOrnithology, Eberhard-Gwinner-Strasse,82319,Seewiesen,Germany, 2 BionetNatuuronderzoek,Valderstraat39, 6171EL,Stein,TheNetherlands, 3 AdHocZoogdieronderzoek,OudeVelperweg34,6824HE,Arnhem,The Netherlands, 4 AnimalEcology&Ecophysiologygroup,InstituteforWaterandWetlandResearch,Radboud UniversityNijmegen,P.O.Box9010,6500GL,Nijmegen,TheNetherlands, 5 DutchMammalSociety,P.O. Box6531,6503GA,Nijmegen,TheNetherlands, 6 DepartmentofMigrationandImmuno-ecology,Max PlanckInstituteforOrnithology,AmObstberg1,78315,Radolfzell,Germany, 7 UniversityofKonstanz, DepartmentofBiology,Konstanz,Germany ¤ Currentaddress:JasjaDekkerDierecologie,Enkhuizenstraat26,6843,WZ,Arnhem,TheNetherlands * JaapvanSchaik@gmail.comAbstractDuringautumninthetemperatezoneofboththenewandoldworld,batsofmanyspecies assembleatundergroundsitesinabehaviourknownasswarming.Autumnswarming behaviouristhoughttoprimarilyserveasapromiscuousmatingsystem,butmayalsobe relatedtothelocalizationandassessmentofhibernacula.Batssubsequentlymakeuseof thesameundergroundsitesduringwinterhibernation,howeveritiscurrentlyunknownifthe assemblagesthatmakeuseofasitearecomparableacrossswarmingandhibernationseasons.Ourpurposewastocharacterizethebatassemblagesfoundatfiveunderground sitesduringboththeswarmingandthehibernationseasonandcomparetheassemblages foundduringthetwoseasonsbothacrosssitesandwithinspecies.Wefoundthattherelativeabundanceofindividualspeciespersite,aswellastherelativeproportionofaspecies thatmakesuseofeachsite,werebothsignificantlycorrelatedbetweentheswarmingand hibernationseasons.Theseresultssuggestthatswarmingmayindeedplayaroleinthe localizationofsuitablehibernationsites.Additionally,thesefindingshaveimportantconservationimplications,asthiscorrelationcanbeusedtoimprovemonitoringofunderground sitesandpredicttheimportanceofcertainsitesforrareandcrypticbatspecies.IntroductionBetweenAugustandOctobermanytemperate-zonebatspeciesinboththenewandoldworld gatheratundergroundsitesinabehaviourknownasswarming[ 1 ].Theassembledbatsdisplay PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 1/12 a11111 OPENACCESS Citation: vanSchaikJ,JanssenR,BoschT, HaarsmaA-J,DekkerJJA,KranstauberB(2015) BatsSwarmWhereTheyHibernate:Compositional SimilaritybetweenAutumnSwarmingandWinter HibernationAssemblagesatFiveUndergroundSites. PLoSONE10(7):e0130850.doi:10.1371/journal. pone.0130850 Editor: BrockFenton,UniversityofWesternOntario, CANADA Received: March17,2015 Accepted: May25,2015 Published: July8,2015 Copyright: ©2015vanSchaiketal.Thisisanopen accessarticledistributedunderthetermsofthe CreativeCommonsAttributionLicense ,whichpermits unrestricteduse,distribution,andreproductioninany medium,providedtheoriginalauthorandsourceare credited. DataAvailabilityStatement: Allrelevantdata regardingswarmingcapturesarewithinthepaper. WintercountdataareownedbytheDutchMammal Societyandduetoethicalrestrictionsareavailable uponrequestfromMauriceLaHaye,e-mail: info@zoogdiervereniging.nl ,mail:Postbus6531, 6503GA,Nijmegen. Funding: Thisprojectwasfundedbyagrantfrom theprovinceofLimburg(LandschapinUitvoering). BionetNatuuronderzoekandAdHoc Zoogdieronderzoekprovidedsupportintheformof

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intenseflightactivity,circlinginandaroundtheentranceofthesitethroughoutthenight,but predominantlydonotroostthereduringtheday[ 2 ].Swarmingactivityislargelylimitedto speciesthatmakeuseofundergroundsitesseasonally,hibernatingthereinwinterbutroosting elsewhereinsummer[ 3 ].Manybehaviouralandgeneticstudieshaveshownthatswarming actsasapromiscuousmatingbehaviour,facilitatinggeneflowbetweenotherwiseisolatedsummercolonies(eg.[ 4 , 5 , 6 ]).Inaddition,itsoccurrenceatundergroundsiteshasoftenledtothe suggestionthatswarmingalsoplaysanimportantroleintheassessmentofthesuitabilityofa hibernaculum[ 1 , 7 , 8 ]and/orthesocialtransferofinformationregardingitslocation[ 9 ]. Withintheswarmingseasonthereisconsiderablevariationinthetimingofswarmingactivityamongspecies,aswellaslocalvariationintimingbasedonaltitude[ 10 , 11 ]andlatitude [ 12 , 13 ].However,thegeneralpatternissimilarforallspecies.Theassemblageofbatsis stronglymale-biased,withobservedsexratiosofaround4:1[ 11 , 12 , 14 ],andmalebatsroost closertothesitethanfemales[ 15 ].Geneticanalysishasshownthatfemalesfrommultiplecoloniesmakeuseofaswarmingsite,boththroughouttheswarmingseasonandonindividual nights[eg.4].In Myotisnattereri ,ithasbeenshownthatfemalesfromasinglecolonyattend multipleswarmingsites,withmostindividualsswarmingatthenearestsite[ 14 ].Ringingstudiessuggestthatindividualsofbothsexesdisplaygeneralsitefidelitywithinandacrossyears, beingrecapturedmostoftenatthesamesite[ 16 ].Similarly,individualsradio-trackedat swarmingsiteswereneverfoundtovisitothersites[ 14 , 17 ],althoughringedindividualshave beenfoundatothersites[eg.1].Approximatelyonetotwomonthsafterthepeakswarming activityofaspecies,individualsreturntoundergroundsitestohibernate[ 3 ]. Whetherbatshave(species-specific)preferencesforparticularundergroundsiteshasbeen investigatedbothduringswarmingandhibernationseasons.Glover&Altringham[ 13 ]showed thatswarmingintensitywashighestatundergroundsiteswith1)extensivechamberdevelopment,2)withouthydrologicalactivity,and3)withasheltered,horizontallyorientedentrance. RandallandBroders[ 18 ]alsofoundchamberlengthanddevelopmenttobeimportant,while alsosuggestingthatstreamlengthinthesurroundingareapositivelyinfluencesswarming behaviour.ContrarytoGloverandAltringham[ 13 ],RandallandBrodersalsofoundthatshelteredentrancesnegativelyinfluencedswarming,althoughallsitesintheirstudywereconsideredhighlysheltered(21of25weremorethan75%sheltered).Finally,Johnsonetal.[ 19 ] foundthatswarmingbatspreferredsiteswithasingleisolatedentrance,whilealsosuggesting thatalargercaveentrancesizewasimportantforseveralspecies. Duringhibernation,batshavesimilarlybeenshowntohavepreferencesforcertainsitesand microclimates[ 20 , 21 ].Particularly,areaswithadequateandstablehumiditywhichreduce evaporativewaterlossappeartobecritical[ 22 , 23 ].Additionally,broadgenusandspecies-specificpreferencesfortemperaturehavebeenreported[ 24 ].However,speciesareoftenfound hibernatingatawiderangeoftemperatures,andtemperaturepreferencesmayalsobesexand agespecific[ 25 ],varythroughouttheseason[ 26 –28 ],orvarydependingontheamountoffat reservespossessedbyindividuals[ 29 ].Moreover,severalmonitoringeffortshavereportedthat batsfrequentlymovewithinandbetweensitesthroughoutthewinter[ 21 , 30 ],especiallyfollowingextremeweatherchanges,suggestingtheymaybeflexibleinrelocatingtomoreoptimal conditions/locations[ 31 , 32 ]. Severalstudieshavemadeinferencesastowhetherindividualsobservedatasiteduringthe swarmingseasonarealsofoundthereduringhibernation(eg.whetherpreferencesforparticularswarmingandhibernationsitesarelinked).Fenton[ 1 ]suggestedthatbatstendedtohibernatewheretheyhadbeencaughtduringtheswarmingseason.Likewise,Rivers etal .[ 14 ] suggestedthatatleastaproportionofindividualsremainatasitetohibernateandproposed thatcharacterizingtheswarmingassemblagemaybeasuitablealternativeforwintersurveys, especiallyinthecaseofcrevice-dwellingbatssuchas M . nattereri .Morerecently,Randalland CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 2/12 salariesforauthorsRJandTBrespectively,butdid nothaveanyadditionalroleinthestudydesign,data collectionandanalysis,decisiontopublish,or preparationofthemanuscript.Thespecificrolesof theseauthorsarearticulatedinthe ‘ author contributions ’ section. CompetingInterests: Theauthorshavedeclared thatnocompetinginterestsexist.

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Broders[ 18 ]explicitlymadetheassumptionthatsitesusedduringswarmingwerelikelytoalso behibernacula.Conversely,inseveralstudiesnoclearrelationhasbeenfoundbetweenswarmingandhibernationassemblagessuggestingthatbatsdonotexclusivelyhibernatewherethey swarm[ 2 , 7 ],whereasothersfoundgenerallycomparableassemblagesbutfarfewerbatsduring thehibernationseasonsuggestingthatmostbatsdonotusethesamesiteinwinter[ 33 ]. Finally,severalstudiesinvestigatingwhichsitecharacteristicsareimportanttoswarmingbats haveconcludedthattheirobservationsareinsufficienttodrawclearinferencesconcerningthe useofthesesitesashibernacula[ 13 , 19 ]. Herewecharacterizetheautumnswarmingactivityatsixknownhibernacula,andsubsequentlycomparetheswarmingandhibernatingassemblagesatfiveofthesesitesforwhich hibernationsurveydatawasavailable.Todoso,wefirstconfirmedthatthenumberofbats,per species,wasdistributednon-uniformlyacrosstheinvestigatedsitesduringbothseasons.We predictedthatthedistributionofbatsamongsitesshouldbenon-uniformasaresultofspecies-specificsitepreferences[eg.13,18,20,27]duringbothswarmingandhibernationseasons. Next,weassessedwhethertherewasastatisticalcorrelationbetweentheobservedswarming andhibernationassemblagesintwodifferentways.Persite,wecomparedthecompositionof theswarmingandhibernationassemblagesbycomparingtherelativeabundanceofthedifferentbatspeciesbetweenseasons.Additionally,perspecies,wecomparedtherelativeproportion ofanindividualbatspeciesencounteredateachsiteduringtheswarmingandhibernationseasons.Basedonpreviousresearch[ 1 , 14 , 18 ],wehypothesizedthatthepreferencesforparticular sitesduringbothswarmingandhibernationseasonsarelinked,andthusweexpectedacompositionalsimilarityintheswarmingandhibernationassemblages,bothpersiteandperspecies.MaterialsandMethods StudysiteThestudywascarriedoutatsixofthe136disusedlimestoneminesavailabletobatsinthe Zuid-LimburgregionoftheNetherlands( Table1 ).Thesemines,togetherwithsimilarmines inBelgium,arethemainpotentiallysuitableundergroundsitesinthearea,andaretherefore highlyimportantforregionalbatpopulations.Giventhatthesiteswesurveyedaredisused mines,withfarfewerlargecracksandcrevicesthanmostother(natural)undergroundsites, hibernationsurveydatafortheseminesiscomparativelyaccurate.Nevertheless,countslikely remainanunderestimateofthetruenumberofbatshibernatingatthesesites[ 34 ].Themaximumpairwisedistancebetweensiteswaslessthan10km(1.9 – 8.4km; Table1 ),wellwithinthe migratorydistanceofallbatspeciesinvestigated[ 16 ].Thereforeweexpecttheselectedsitesto havelargelyoverlappingcatchmentareas,andthuswearguethatanyobserveddifferencesin batassemblagearenotpurelytheresultofdifferencesinthelocalbatcommunitiesneareach site.Siteswereselectedbasedonpreviouscapturedatainanattempttogetarepresentative sampleofallspeciespresentinthearea.SwarmingcapturesBatswerecaughtusingmist-netsattheentrancetoeachmineusingastandardizednetconfigurationforeachmine.Eachsitewassampledeleventimes,onceeverysevendays,throughout theswarmingseason(fromAugust2,2008toOctober12,2008).Intheeventofheavyrain, samplingwascarriedoutonthefollowingday.Foreachindividualbat,forearmlength,body mass,sex,reproductivestatus,andage(adult/juvenile;basedonossificationoftheepiphyseal joints[ 35 ])wererecorded.Batsweretemporarilymarkedonthetoenailsusingnon-toxicnail polishtoexcluderecapturedindividuals.Batcaptureswerecarriedoutunderlicensefromthe DutchministryofEconomicaffairs,(permitFF/75A/2003/150),andwithpermissionofallsite CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 3/12

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owners(Staatsbosbeheer;LimburgsLandschap).Allbatswerereleasedwithinonehour,atthe pointofcapture.WinterhibernationsurveysWinterhibernationcountswerecarriedoutbyvolunteersatfiveofthesixsites(Oudbergis inaccessible)andsurveydatawereobtainedfromtheDutchMammalSocietydatabase.Each hibernaculumwassurveyedonasingledaybyteamswithmorethan10yearsofsurveying experience.Specieswereidentifiedinsitu,andbatswerenothandled.Ceilingsofminesarelow enoughforreliablevisualinspection,insomecasesaidedbybinoculars.Thespecies M . mystacinus and M . brandtii werecombined,astheycannotbereliablydistinguishedinwinterwithoutdisturbance.Incaseswhereindividualscouldnotbeidentifiedtheywereclassifiedas “ indet. ” andnotincludedinthisanalysis(2 – 12batspersite).Surveydatawereavailable between1994 – 2009;sincecountsforeachsitewerecomparablebetweenyears,weperformed theanalysisusingthecountdatafromthemostrecentwinterseasonavailablepersite(2008 forRiesenberg-Noord,2009forallothersites).StatisticalanalysisTemporalpatternswithintheswarmingseasonwereexploredvisuallybyplottingtheabundanceofeachbatspeciesperweekrelativetothetotalnumberofbatscaughtinthatweek usingR3.1.2(38). Totestforadisproportionatedistributionofthenumberofbatsperspeciesacrossthesampledsites,weperformedaPearson'sChi-squaredtestinR3.1.2[ 37 ]withineachseason(cumulativeswarmingseasonandwinterhibernationsurvey). Forthecomparisonsbetweenswarmingandwinterassemblages,allspeciesforwhichthere werelessthan10winterrecordswereomitted( Myotisbechsteinii , Plecotusauritus , Eptesicus serotinus ).Tocomparetheswarmingandhibernationdatasets,wecomparedtwotypesofrelativeabundancesratherthanactualcountdata.Thisallowedustocompensateforvariationin speciesphenologyduringtheswarmingseasonandtocomparedatasetsofswarmingandwintercounts,whichcannotbecomparedintermsofabsolutequantities.First,persite,wecalculatedtherelativeabundanceofeachbatspeciesforboththecumulativeswarmingseasonand Table1.Descriptivecharacteristicsoftheundergroundsiteswesampled. LocationEntranceInnercharacteristicsSpecies SiteCoordinatesAltNSize(m2)OrientationShelterAreaChamberHydrSH Barakkengroeve50.865,5.7919914.6HorizontalSheltered33.1YesDry107 Koelenbosch-groeve50.852,5.7759018.9HorizontalSheltered7.6YesDry105 Riesenberg-Noord50.798,5.74510525.6HorizontalSheltered4.5NoDry117 GroevedeSchark50.828,5.67885324.6HorizontalExposed3.6YesDry106 Schenkgroeve50.873,5.76665251.6HorizontalSheltered5.9NoDry87 Oudberggroeve50.825,5.6657510.09HorizontalSheltered8NoDry9Abbreviations:latitudeandlongitudeindecimaldegrees(Coordinates);altitudeatthesiteentranceinmeters(Alt);thenumberofentrances(N); thetotal entrancesize(Size);theorientationoftheentrance(Orientation);degreeofshelteraroundtheentrance(Shelter);thesurfaceareaoftheminein ha (Area);degreeofchamberdevelopment(Chamber);hydrologicalactivityinthemine(Hydr.);andthenumberofspeciesobservedduringswarming (Swarm),andhibernationsurveys(Hiber).Allsubjectiveminecharacteristics(Orientation,Shelter,Chamberdevelopment,Hydrology)werechar acterized asdescribedinGloverandAltringham[ 13 ].RemainingmeasurementswereobtainedfromtheStudiegroepOnderaardseKalksteengroeven[ 36 ],and updatedbasedonthedatasetofAJH. doi:10.1371/journal.pone.0130850.t001 CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 4/12

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thewinterhibernationsurvey.Second,perspecies,wecalculatedtherelativeproportionofa speciesthatwasencounteredateachsite,againforboththecumulativeswarmingseasonand thewinterhibernationsurvey.Inbothcases,thecompositionalsimilaritybetweentheswarmingandhibernationseasonswasmeasuredusingapermutationalanalysisofvarianceusing Bray-Curtisdistancematrices(calculatedusingtheadonisfunctionofRpackage ‘ vegan ’ version2.2 – 1[ 38 ]).Forbothtests,100permutationswereusedduetothelimitednumberofpossiblepermutationsgiventhesizeofthedataset.Results SwarmingcapturesAtotalof1351uniqueindividualsof13specieswerecaughtduringthisstudy.Fortwospecies ( Nyctalusnoctula , Plecotusaustriacus )onlyoneindividualwascaught,andthereforethesespecieswerenotincludedinfurtheranalysis.Innineoftheremainingelevenspeciesthesexratio wasmalebiased(67to87%; Table2 ),whereastwospecies( Myotismyotis , Pipistrelluspipistrellus )showedaslightfemalebias(43and45%malesrespectively).Thetimingofpeakswarming activityvariedbetweenspecies( Fig1 )with Pipistrelluspipistrellus , Eptesicusserotinus ,and Myotisbrandtii peakingearliest(earlyAugust), Myotisdasycneme , Myotisdaubentonii , Myotis mystacinus and Myotisbechsteinii peakingbetweenlateAugustandearlySeptember,and Myotisemarginatus and Myotisnattereri showingthelatestpeak(endofSeptember).Twospecies, Plecotusauritus and Myotismyotis ,didnotshowapeakandwerefoundatlowlevelsthroughoutthesamplingperiod.HibernationcountsDuringhibernationcounts(January2009;2008forRiesenberg-Noord),1797batsofeightspeciesandonespeciescomplexwererecorded. Myotisbechsteinii wasnotfoundatanyofthe sites,andboth Eptesicusserotinus and Plecotusauritus werefoundinlownumbers(1and9 respectively).Forallsites,thenumberofspeciesfoundduringtheswarmingseasonwashigher thanobservedduringhibernationcounts( Table1 ).DistributionacrosssitesThedistributionofbats,perspecies,acrosstheinvestigatedsiteswassignificantlydifferent fromauniformdistributionduringboththeswarming( 2test,p < 0.001)andhibernationseason( 2test,p < 0.001). Forthesixspeciesandthe Myotismystacinus/brandtii complex,forwhichdatainbothseasonsweresufficient,thepersiterelativeabundanceofaspeciesduringtheswarmingseason wassignificantlycorrelatedwiththerelativeabundanceofthatspeciesatthatsiteduringhibernation(F4,5=11.67;p=0.02; Fig2a ).Similarly,perspecies,therewasaclearcorrelation betweentherelativeproportionofaspeciesfoundateachsiteduringtheswarmingseasonand therelativeproportionofthatspeciesfoundatthesamesiteduringhibernation(F6,7=7.78; p=0.01; Fig2b ).DiscussionTheoveralldistributionofbatsacrosstheunder groundsitesinvestigatedinthisstudywas notuniforminbothseasons.Asthetypicalmigrationdistanceoftheobservedspeciesfar exceedsthespatialproximityofthesites,andalargenumberofbatsvisitthesesites(andthe othersaroundthem),thislargedeviationfromauniformdistributionacrosssitescannot onlybeexplainedbyconfoundingfactorssuchaslandscapecharacteristics,orthe CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 5/12

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distributionofmaternitycoloniesinthearea.Instead,inaccordancewithpreviousstudies, wearguethatspeciespreferentiallyvisitsp ecificsitesduringbothseasons.Indeed,wefind thatthesesitepreferencesappeartobelinkedastherelativeabundanceofbatspeciesatindividualsiteswasstronglycorrelatedbetweensw armingandhibernationseasons.Similarly, therelativeproportionofindividualbatspeci esfoundateachofthefiveinvestigatedsites wascorrelatedbetweentheswarmingandhibernationseasons.Theconcordancebetween thesetwoanalysessuggeststhattherearenosign ificantsite-orspecies-specificdifferencesin eithersamplingaccuracyorbehaviour.Takent ogether,theseresultsindicatethatundergroundsitesmaybeactivelyselectedbybatspecies,eitheronthebasisoftheirsuitabilityas swarmingsites(eg.arenacharacteristics)orhi bernationsites(eg.microclimate),oracombinationofboth. Giventhatwedonothaveindividualizeddata,wecannotdetermineifthesecorrelationsare theresultofindividualbatsmakinguseofthesiteduringbothseasons,orwhethertheabsolute numberofbatsusingasiteineachseasoniscomparable.Infact,severalringingandmonitoringstudiessuggestthisisnotalwaysthecase[ 14 , 16 ].Nevertheless,severalimportantconclusionscanbedrawnbasedonourobservations.Species-specificobservationsWefoundamalebias( > 66%)inallbuttwospecies( Pipistrelluspipistrellus , Myotismyotis ), andadditionallydidnotfindapeakinswarmingactivityfor M . myotis .Intriguingly,thesetwo speciesareamongthoseknowntohaveothermatingstrategies( P . pipistrellus :songflightand maleterritories[ 39 ]; M . myotis :temporaryharems[ 40 ]),suggestingthattheirbehaviourat swarmingsitesmaynotbeentirelyanalogoustothatoftheremainingspecies. Severalspecieswereomittedfromtheanalysesduetoinsufficient( < 10)winterrecords ( Eptesicusserotinus , Plecotusauritus and Myotisbechsteinii ),orincludedbutonlyfoundata singlesiteinwinter( Pipistrelluspipistrellus ).Nevertheless,thesespecieswerepresentinlarger numbersduringtheswarmingseason.Both E . serotinus and P . pipistrellus areconsideredto hibernatemostlyincoldcrevices[ 41 ],andmayhavethereforebeenunderestimatedinwinter duetotheirroostingecology.Regarding P . auritus ,wedidnotcapturemorethan16 Table2.Numberofindividualscapturedperspeciesandsiteduringtheautumnswarmingsurvey. Species% Male Barakkengroeve Koelenbosch groeve RiesenbergNoord Groevede Schark Schenkgroeve Oudberggroeve Total Eptesicusserotinus 8712123135045 Myotisbechsteinii 83011005153 Myotisbrandtii 86324103435 Myotisdasycneme 716121409142 Myotisdaubentonii 761028056255968390 Myotisemarginatus 8227643035725206 Myotismyotis 45100508023 Myotismystacinus 733227041367 Myotisnattereri 678830222712018305 Pipistrellus pipistrellus 4326437743117 Plecotusauritus 8113481316256 Tableincludestheobservedsexratioforeachspecies(%male).Asingleindividualof Nyctalusnoctula (Riesenberg-Noord),and Plecotusaustriacus (GroevedeSchark)werealsocaptured(notshown). doi:10.1371/journal.pone.0130850.t002 CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 6/12

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individualsatanygivensiteanddidnotfindaclearactivitypeakduringtheswarmingseason asfoundinotherstudies[ 15 ],suggestingthatthesitesselectedinthisstudymaysimplynotbe veryimportantforthisspecies.Lastly, M . bechsteinii onlyoccurredinlargenumbersatasingle siteduringtheswarmingseason(Oudberg).However,asthissiteisinaccessibleinwinter,it wasomittedfromthecomparisonbetweenswarmingandhibernationassemblages.Thus, althoughthesefourspecieswereomittedfromthecomparison,webelievethattheobserved correlationsmayindeedholdforthesespeciesaswell. Fig1.Weeklyrelativeabundanceofeachspeciesthroughouttheswarmingseason. Sampleswere pooledacrossallsampledswarmingsitesperweektocompensateforweathereffects.Speciesaresorted basedonthetimingofpeakswarmingactivity(fromearliest: Pipistrelluspipistrellus tolatest: Myotis nattereri ).Noclearpeakinswarmingactivitywasobservedfor Myotismyotis and Plecotusauritus . doi:10.1371/journal.pone.0130850.g001 CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 7/12

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Fig2.Comparisonoftherelativeabundanceofbatspeciesduringswarmingandhibernationseasonsmeasured(A)persite,and(B)perspecies. Forbothcomparisonsthecumulativeswarmingseason(S)iscomparedtothehibernationsurvey(H). doi:10.1371/journal.pone.0130850.g002 CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 8/12

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FunctionofswarmingTheobservedcorrelationbetweenswarmingandhibernationassemblageslendscredibilityto thetheorythatswarmingbehaviourmayplayaroleintheinspectionof,orsocialinformation transferregarding,thesuitabilityofanundergroundsiteasahibernaculuminadditiontoits roleinthematingsystemofthesebatspecies. Bycomparingswarmingbehaviourinbatstothelargerangeofmatingsystemsseenin anothermammalianclade,ungulates,ageneralscenariothatcombinesbothfunctionscanbe generated.Asinseveralungulatesystems[ 42 ],malebatsofthespeciesinvestigatedinthis studyaregenerallyunabletodirectlydefendfemalesorfemaleranges,andthereforemust resorttoassemblingatlocationscommontomanyfemalegroups(inbats:hibernacula).Inthe eventthatfemalebatscometotheundergroundsitesto(re-)inspecttheirsuitabilityasahibernaculum,theassembledmalescouldformverysmallterritoriesintheseareassimilartothe clusteredmatingterritoriesseeninpuku( Kobusvardoni ;[ 42 ]).If,however,thefemalescome totheundergroundsitessolelyforthepurposeofmating,theassemblywouldresembleaclassiclek(inwhichthefemalesreceivenobenefitfromvisitingthesiteotherthanmating;see [ 43 ]),asseeninungulatessuchasfallowdeer( Damadamadama [ 44 ])andUgandakob ( Kobuskobthomasi [ 45 ]).Inthecaseofaclassiclek,thecorrelationbetweenswarmingand hibernationassemblagescanstillbeexplained,asinthisscenariomalesmustselectadisplay habitatknownto,andregularlyfrequentedby,largenumbersoffemales.Sincethemalesof mostswarmingspeciesaresolitaryorliveinsmallmalegroupsthroughoutthesummer[ 46 ] andinsomecasesevengeographicallyisolatedfromfemalehomeranges( M . daubentonii :[ 47 , 48 ]; M . dasycneme :[ 49 ]),theundergroundsitesusedcommunallybybothsexesduringhibernationwouldbetheonlysuchlocation. Giventhatlargenumbersofjuvenilebatsarealsocaughtatswarmingsites,theuseof swarmingbehaviourasaclassiclekappearsunlikely,astheseindividualsaregenerallynotyet sexuallymature.Incombinationwiththeobservedcompositionalsimilaritybetweenswarming andhibernationassemblages,wethereforesuggestthatmalebatsofthesespeciesareforming clusteredmatingterritoriesathibernaculaduringtheautumnswarmingseason.However,furtherstudiesinvestigatingthebehaviourofjuvenileindividualsaswellasindividualizedstudies onthevisitationpatternsofadultindividualswillberequiredtofurtherelucidatethefunction ofswarmingbehaviourinbats.ConservationapplicationsandimplicationsOurfindingssupportprevioussuggestionsthattheswarmingassemblagemaybeaninformativeproxyforrelativepopulationsizeandimportanceofanundergroundsiteduringhibernation[ 14 ].However,itisimportanttotakeintoaccountthatsamplingmusttakeplace throughouttheentireswarmingseasontosampleallspecies,andthatinferencesregardingthe relativeimportanceofasiteascomparedtoothersintheareawillrequiresimilarlydetailed informationforsurroundingsites.Nevertheless,whendesignedcorrectly,suchapproachescan aidgreatlyintheidentificationandprotectionofimportantundergroundsites,especiallywhen appliedtospecies-specificresearchobjectives.Forexample,severalspeciessuchas M . nattereri and M . bechsteinii oftenhibernateindeepcrevicesandkarstformations[ 50 ].Bysurveying potentialhibernaculaduringtheswarmingseasonitmaybepossibletoidentifythemost importantundergroundsitesforsuchelusivespecies.Notably,thiscorrelationcanalsobeused topredicttheimportanceofundergroundsitesthataretoodangerousortoodifficulttoaccess inwinter(eg.theOudberginthisstudy).Similarly,forspeciesthatareindistinguishablein winter(eg. M . mystacinus / M . brandtii / M . alcathoe ),swarmingsurveyscanprovideanindicationastotherelativecontributionsofeachofthecrypticspecies.Finally,recentadvancesin CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 9/12

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remotemonitoringtechnologies(eg.camera-traplogging[ 50 ]),mayfurthersimplifyand enhancetheconservationapplicationsofthesefindings,astheywillallowsuchstudiestobe carriedoutwithoutinvasivemist-nettingand/orhibernationsurveys. Thesefindingsalsohaveseveralnotableimplicationsforconservation.Thenon-uniform distributionofspeciesacrosssitesemphasizesthatindividualundergroundsitesmaydiffer greatlyintermsoftheirimportancetothelocalbatcommunity.Therefore,thedisturbance/ lossofasinglesitewithinanareamayaffectthelocalspeciesdifferently,andevencomparativelysmallswarmingsitesmaybecriticalintermsoftheirconservationvalueforspecificspecies.Inaddition,iftheobservednon-uniformityacrosssitesisaconsequenceofpreferencesfor particularsite/entrance/microclimaticcharacteristics,anyalterationofthesesitesmayresultin significantpopulationdeclinesorchangesintheobservedspeciesassemblage.Similarly,the compositionalsimilaritybetweenswarmingandhibernationassemblageshighlighttheimportanceofprotectingimportanthibernaculathroughouttheyear,asanydisturbanceineither seasonwilllikelyalsoaffecttheuseofthesiteintheotherseason.AcknowledgmentsWewouldliketothankJanHovenkamp,PaulVoskampforadviceandlogisticalsupport,and volunteersthathelpedduringthefieldwork.WewouldalsoliketothankHansWeinreich,Jos Cobben,BernardGrol,BenVerboom,WillemVergoossen,MauriceLaHayeandthevolunteersofTelgroepNHGL,TelgroepLOGEandTelgroepUtrecht,formakingtheirhibernation countdataavailableforthisstudy.WethankDaanDekeukeleire,LeonieBaier,MarkBrigham andtwoanonymousreviewersforprovidingusefulcommentsonearlierversionsofthismanuscript.JvSandBKweresupportedbytheInternationalMaxPlanckResearchSchoolforOrganismalBiology.AuthorContributionsConceivedanddesignedtheexperiments:JvSRJBK.Performedtheexperiments:JvSRJTB AJHJJADBK.Analyzedthedata:JvSRJJJADBK.Wrotethepaper:JvS.References1. FentonMB.Summeractivityof Myotislucifugus (Chiroptera:Vespertilionidae)athibernaculainOntario andQuebec.CanadianJournalofZoology.1969;47:597 – 602. 2. ParsonsKN,JonesG,Davidson-WattsI,GreenawayF.SwarmingofbatsatundergroundsitesinBritain — implicationsforconservation.BiologicalConservation.2003;111(1):63 – 70.PMID: ISI:000181368800006 . 3. HoracekI,ZimaJ.Net-RevealedCaveVisitationandCave-DwellinginEuropeanBats.FoliaZoologica. 1978;27(2):135 – 48.PMID: ISI:A1978FM95200005 . 4. KerthG,KieferA,TrappmannC,WeishaarM.Highgenediversityatswarmingsitessuggesthotspots forgeneflowintheendangeredBechstein'sbat.ConservationGenetics.2003;4(4):491 – 9.PMID: ISI:000184171500007 . 5. RiversNM,ButlinRK,AltringhamJD.GeneticpopulationstructureofNatterer'sbatsexplainedbymatingatswarmingsitesandphilopatry.MolecularEcology.2005;14(14):4299 – 312.doi: 10.1111/j.1365294X.2005.02748.x PMID: WOS:000233286300008 . 6. FurmankiewiczJ,AltringhamJ.Geneticstructureinaswarmingbrownlong-earedbat(Plecotusauritus)population:evidenceformatingatswarmingsites.ConservationGenetics.2007;8(4):913 – 23.doi: 10.1007/s10592-006-9246-2 PMID: WOS:000248300300014 . 7. HallJS,BrennerFJ.SummernettingofbatsatacaveinPennsylvania.JournalofMammalogy.1968; 49(4):779 – &.PMID: WOS:A1968C232400031 . 8. VeithM,BeerN,KieferA,JohannesenJ,SeitzA.Theroleofswarmingsitesformaintaininggeneflow inthebrownlong-earedbat(Plecotusauritus).Heredity.2004;93(4):342 – 9.doi: 10.1038/sj.hdy. 6800509 PMID: WOS:000224092300004 . CompositionalSimilarityinBatSwarmingandHibernationAssemblages PLOSONE|DOI:10.1371/journal.pone.0130850July8,2015 10/12

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