Patterns of Cave Biodiversity and Endemism in the Appalachians and Interior Plateau of Tennessee, USA


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Patterns of Cave Biodiversity and Endemism in the Appalachians and Interior Plateau of Tennessee, USA

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Patterns of Cave Biodiversity and Endemism in the Appalachians and Interior Plateau of Tennessee, USA
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PLOS One
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Niemiller, Matthew L.
Zigler, Kirk S.
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Biodiversity ( local )
Endemism ( local )
Tennessee ( local )
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Using species distribution data, we developed a georeferenced database of troglobionts (cave-obligate species) in Tennessee to examine spatial patterns of species richness and endemism, including >2000 records for 200 described species. Forty aquatic troglobionts (stygobionts) and 160 terrestrial troglobionts are known from caves in Tennessee, the latter having the greatest diversity of any state in the United States. Endemism was high, with 25% of terrestrial troglobionts (40 species) and 20% of stygobionts (eight species) known from just a single cave and nearly two-thirds of all troglobionts (130 species) known from five or fewer caves. Species richness and endemism were greatest in the Interior Plateau (IP) and Southwestern Appalachians (SWA) ecoregions, which were twice as diverse as the Ridge and Valley (RV). Troglobiont species assemblages were most similar between the IP and SWA, which shared 59 species, whereas the RV cave fauna was largely distinct. We identified a hotspot of cave biodiversity with a center along the escarpment of the Cumberland Plateau in south-central Tennessee defined by both species richness and endemism that is contiguous with a previously defined hotspot in northeastern Alabama. Nearly half (91 species) of Tennessee’s troglobiont diversity occurs in this region where several cave systems contain ten or more troglobionts, including one with 23 species. In addition, we identified distinct troglobiont communities across the state. These communities corresponded to hydrological boundaries and likely reflect past or current connectivity between subterranean habitats within and barriers between hydrological basins. Although diverse, Tennessee’s subterranean fauna remains poorly studied and many additional species await discovery and description. We identified several undersampled regions and outlined conservation and management priorities to improve our knowledge and aid in protection of the subterranean biodiversity in Tennessee.
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PLOS One, Vol. 8, no. 5 (2013-05-22).

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PatternsofCaveBiodiversityandEndemisminthe AppalachiansandInteriorPlateauofTennessee,USAMatthewL.Niemiller1,KirkS.Zigler2*1 DepartmentofEcologyandEvolutionaryBiology,YaleUniversity,NewHaven,Connecticut,UnitedStatesofAmerica, 2 DepartmentofBiology,UniversityoftheSouth, Sewanee,Tennessee,UnitedStatesofAmericaAbstractUsingspeciesdistributiondata,wedevelopedageoreferenceddatabaseoftroglobionts(cave-obligatespecies)in Tennesseetoexaminespatialpatternsofspeciesrichnessandendemism,including . 2000recordsfor200described species.Fortyaquatictroglobionts(stygobionts)and160terrestrialtroglobiontsareknownfromcavesinTennessee,the latterhavingthegreatestdiversityofanystateintheUnitedStates.Endemismwashigh,with25%ofterrestrialtroglobionts (40species)and20%ofstygobionts(eightspecies)knownfromjustasinglecaveandnearlytwo-thirdsofalltroglobionts (130species)knownfromfiveorfewercaves.SpeciesrichnessandendemismweregreatestintheInteriorPlateau(IP)and SouthwesternAppalachians(SWA)ecoregions,whichweretwiceasdiverseastheRidgeandValley(RV).Troglobiontspecies assemblagesweremostsimilarbetweentheIPandSWA,whichshared59species,whereastheRVcavefaunawaslargely distinct.WeidentifiedahotspotofcavebiodiversitywithacenteralongtheescarpmentoftheCumberlandPlateauin south-centralTennesseedefinedbybothspeciesrichnessandendemismthatiscontiguouswithapreviouslydefined hotspotinnortheasternAlabama.Nearlyhalf(91species)ofTennessee’stroglobiontdiversityoccursinthisregionwhere severalcavesystemscontaintenormoretroglobionts,includingonewith23species.Inaddition,weidentifieddistinct troglobiontcommunitiesacrossthestate.Thesecommunitiescorrespondedtohydrologicalboundariesandlikelyreflect pastorcurrentconnectivitybetweensubterraneanhabitatswithinandbarriersbetweenhydrologicalbasins.Although diverse,Tennessee’ssubterraneanfaunaremainspoorlystudiedandmanyadditionalspeciesawaitdiscoveryand description.Weidentifiedseveralundersampledregionsandoutlinedconservationandmanagementprioritiestoimprove ourknowledgeandaidinprotectionofthesubterraneanbiodiversityinTennessee.Citation: NiemillerML,ZiglerKS(2013)PatternsofCaveBiodiversityandEndemismintheAppalachiansandInteriorPlateauofTennessee,USA.PLoSONE8(5): e64177.doi:10.1371/journal.pone.0064177 Editor: VincentLaudet,EcoleNormaleSupe ´ rieuredeLyon,France Received December6,2012; Accepted April13,2013; Published May22,2013 Copyright: 2013Niemiller,Zigler.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermits unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited. Funding: ThisworkwassupportedbytheTennesseeWildlifeResourcesAgency(contractnos.ED-06-02149-99andED-08-023417-00toMLN),AmericanMuseum ofNaturalHistory(MLN),CaveResearchFoundation(MLN),NationalSpeleologicalSociety(MLN),theYaleInstituteforBiosphericStudies(MLN),a ndtheUniversity oftheSouth(KSZ).Thefundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparationofthemanuscript. CompetingInterests: Theauthorshavedeclaredthatnocompetinginterestsexist. *E-mail:kzigler@sewanee.eduIntroductionCavesandsimilarhabitatsareamongthemostunforgiving environmentsontheplanet.Nonetheless,ataxonomicallydiverse faunahasbeendocumentedfromsubterraneanhabitats.For example,morethan1,138cave-restrictedspeciesandsubspecies from112familiesand239generahavebeendescribedinthe UnitedStatesalone[1].Nearlyallofthesecave-obligatespecies (troglobionts)havedevelopedconspicuousregressiveandconstructivetraitsuniquelyassociatedwithlifeinperpetualdarkness andgenerallylimitedfoodresources,suchaslossandreductionof eyesandpigmentation,elongationofappendages,increased longevity,andenhancementofnonvisualsensorymodalities[2]. Subterraneanbiodiversityhasbeendocumentedformanytaxa intheUnitedStates[1,3–8],aswellasforsmallerspatialscales, includingthecompilationofseveralstateandregionalfaunallists [9–16].Ofthemorethan50,000cavesreportedintheUnited States,nearly20%occurinTennessee.Twoofthemostcave-rich karstregionsinthenation,theInteriorLowPlateauandthe Appalachians,covermuchofTennessee[1,8],andTennesseelies justtothenorthofthehypothesizedmid-latitudebiodiversityridge interrestrialcavefaunainNorthAmerica[17].Considerable biospeleologicalresearchhasbeenconductedformorethana centuryinthestate[18–22];andreferenceslistedinTextS1and thenumberofcave-restrictedspeciesdescribedfromTennessee hassteadilyincreasedduringthistime.Peck[6]compiledagenuslevelsummaryofobligatesubterraneanfaunaintheUnitedStates thatincluded33generaofterrestrialtroglobiontsand8generaof stygobiontsinTennessee.Themostrecentspecieslistfor TennesseeisprimarilyderivedfromCulveretal.’s[8]studyand includes126terrestrialtroglobiontsand44stygobionts,ranking second(at170species)behindTexas(201species)forthemost obligatesubterraneanspeciesintheUnitedStates[1]. SinceCulveretal.’s[8]study,therehasbeenanincreasein cave-relatedresearch(seereferencesinTextS1)thathas dramaticallyimprovedourknowledgeofthediversityand distributionoftheobligatesubterraneanfaunainTennessee, includingbiologicalinventoriesandsurveys[23–28],taxonomic revisionsanddescriptionsofnewspecies[29–35],andphylogeographicstudies[36–42].Despitethelargenumberofstudieson cave-obligatespecies,spatialpatternsofspeciesrichnessand endemismhavenotbeenexaminedatalocalscaleinthestate. Moreover,mostcavesinTennesseeareprivatelyownedand affordedlittleprotection.Lessthan8%oflandisprotectedin PLOSONE|www.plosone.org1May2013|Volume8|Issue5|e64177

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Tennessee(ProtectedAreasDatabaseoftheUnitedStates, availableonlineathttp://gapanalysis.usgs.gov/padus)andmuch ofthisprotectedareaiscomprisedoflandholdingsthatdonot includecave-richecoregions.Consequently,thereisaneedto documentlocalandregionalcentersofsubterraneanbiodiversity toassistinsettingconservationprioritiesandguidingmanagement decisionsfortroglobiontsinTennessee. Asafirststeptowardprioritizingareasforconservationand futureresearch,wecompiledallavailabledistributionaldatafor troglobiontstocreateageoreferenceddatabaseofobligate subterraneanbiotainTennessee.Usingthisdatabase,we(1) identifiedandmappedareasofspeciesrichnessandendemismfor troglobitesandstygobitesatalocalscaleinTennessee;(2) examinedthetaxonomiccompositionoflocalandregionalspecies assemblages;(3)definedcavebiogeographicregionsbasedon similarityofcavecommunities;and(4)evaluatedgapsinour knowledgeofTennesseeÂ’scavebiodiversity.Inaddition,we examinepotentialprocessesunderlyingobservedpatternsof biodiversityandendemismaswellastheimplicationsofthese patternsforconservationandmanagementofcavefaunas. Figure1.EcoregionsandcavedistributioninTennessee. (a)EcoregionsofTennessee[following79].TheeightLevelIIIecoregionsarelabeled andLevelIVsubdivisionsoftheseecoregionsareindividuallycoloredwithcolorthemes(e.g.,oranges,blues,andgreens)correspondingtotheLev el IIIecoregions.(b)Distributionof9517georeferencedcavesand(c)661caveswithatleastonetroglobiontrecordedinTennesseeoverlaidonto ecoregions.CaveandkarstregionsoccurinsixLevelIIIecoregionswiththegreatestdensityofcavesintheInteriorPlateau,Southwestern Appalachians,andRidgeandValley.Themajorityofcavesoccurinexposedgeologicalstrataalongescarpmentsmarkingthetransitionbetween ecoregions.Countyboundariesarealsohighlighted. doi:10.1371/journal.pone.0064177.g001 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org2May2013|Volume8|Issue5|e64177

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MaterialsandMethods EthicsStatementBiologicalsurveysthatgenerateddatanotincludedinother publishedstudieswereconductedinaccordancewithprotocols approvedbytheInstitutionalAnimalCareandUseCommitteeat theUniversityofTennessee-Knoxville(protocolno.1589–0507) andYaleUniversity(protocolno.2012–10681),andunder authorizationoftheTennesseeWildlifeResourcesAgency(permit nos.1585and1605)andtheTennesseeDepartmentof EnvironmentandConservation(permitno.2011-005).Efforts weremadetominimizethenumberofspecimenscollectedfor properidentificationandtominimizehabitatdisturbanceduring biologicalsurveys.StudyAreaTwomajorkarstbiogeographicregions,theInteriorPlateau andtheAppalachians,occurinTennessee[1,8].Morethan9500 caveshavebeenreportedfromthestate,withthegreatestdensity occurringalongthewesternmarginoftheCumberlandPlateau (Fig.1).CaveshavebeenreportedfromsixoftheeightLevelIII ecoregionsrecognizedinTennessee.Theseecoregionsare generallyorientatednorth-southacrossthestatefromwesttoeast (Fig.1).Cavesandkarstaremostextensivelydevelopedinthe InteriorPlateau(IP),SouthwesternAppalachians(SWA),and RidgeandValley(RV)ecoregionsinthecentralandeasternpart ofthestate(Table1). TheIPinTennesseeisdividedintofiveLevelIVecoregions, eachwithsignificantareasofcavesandkarst:WesternPennyroyal Karst,WesternHighlandRim,EasternHighlandRim,Outer NashvilleBasin,andInnerNashvilleBasin(Table1).The HighlandRimencirclestheoval-shapedNashvilleBasinandis 150–180mhigherinelevation.MuchoftheIPinTennesseeis underlainbysolublecarbonatestrataandexhibitsmoderatelyto well-developedkarsttopography[43].Threemajorkarstterranes occurintheIPofTennessee,includingtheHighlandRimKarst, NashvilleBasinKarst,andCumberlandPlateauKarst,thelastof whichalsoincludesthePlateauEscarpmentecoregionoftheSWA [44,45].TheHighlandRimKarstandCumberlandPlateauKarst aredevelopedinEarlytoMiddleMississippian-agestrata,whereas theNashvilleBasinKarstisdevelopedinEarlytoMiddle Ordovician-agelimestones.MostcavesdevelopedintheIPoccur inexposedstrataalongescarpments,markingtheboundaries betweenecoregions. TotheeastoftheIPistheSWA(Fig.1a),whichissubdivided intothreeLevelIVecoregions:thePlateauEscarpment,the CumberlandPlateau,andtheSequatchieValley(Table1).The majortopographicfeatureoftheSWAistheCumberlandPlateau, anelevatedupland(550–610mabovesealevel(ASL))boundedto theeastbytheRVecoregionandtothewestbytheEastern HighlandRimoftheIP(275–350mASL).TheCumberland PlateauiscappedbythePennsylvanian-agedsandstoneoverlaying Mississippian-agedlimestones.Thishydrogeologicalsettingis optimalforcavedevelopment[46,47].Almost180millionyears ofdifferentialloweringbetweenCumberlandPlateauandEastern HighlandRimhascreatedahighly-dissected,eastward-retreating escarpmentalongthewesternmarginoftheCumberlandPlateau [47].CavedensityinTennesseepeaksalongthePlateau Escarpmentecoregion(Table1,Fig.1),withtheoldestcave passagesdatedto5.7Mya[47].Cavedevelopmentalsois prominentwithinandalongthemarginsoftheSequatchieValley, whichisanopen,rollingvalleyaveraging6.4kmwideand extending240kmfromCumberlandCountyinTennesseeinto northwestAlabama.Thisecoregionisassociatedwithananticline whereerosionhasformedadeepvalleynearly300mlowerin elevationthanthesurroundingCumberlandPlateau. TheRVconsistsofaseriesofmainlyparallelridgesandvalleys thatgenerallyrunfromsouthwesttonortheastbetweentheSWA andCentralAppalachianstothewestandtheBlueRidge Mountainstotheeast.Ordovician-agelimestonesanddolomites characterizethisecoregion,withelevationsranging210–610m ASLandlocalreliefupto210m.Rocklayersinthisecoregion havebeensignificantlyfaultedandfoldedduetopasttectonic eventsassociatedwiththeupliftoftheAppalachianMountains. Table1. Caves,cavedensity,andcaveswithtroglobiontrecords(‘‘sampledcaves’’)byecoregioninTennessee.EcoregionArea(km2)No.ofcavescaves/100km2No.ofsampledcavesPct.ofsampledcaves SoutheasternPlains13,318140.1428.6% InteriorPlateau40,72428347.02789.8% WesternHighlandRim15,2364242.8296.8% WesternPennyroyalKarstPlain2,13723010.82410.4% InnerNashvilleBasin4,3243688.5297.9% OuterNashvilleBasin11,4687876.98510.8% EasternHighlandRim7,5581,02513.611110.8% SouthwesternAppalachians12,497501140.12895.8% CumberlandPlateau8,2351071.365.6% PlateauEscarpment3,6074791132.82605.4% SequatchieValley65111317.42320.4% CentralAppalachians2,302180.8211.1% RidgeandValley19,60014697.5755.1% BlueRidgeMountains6,3791712.7137.6% Total94,820951710.06616.9% ThesixLevelIIIecoregionsthatcontaincavesareshowninbold.AlsoshownareLevelIVecoregionsubdivisionsoftheInteriorPlateauandtheSouthw estern Appalachians. doi:10.1371/journal.pone.0064177.t001 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org3May2013|Volume8|Issue5|e64177

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DatabaseCompilationWecreatedadatabaseofdistributionalrecordsforallformally describedspeciesrestrictedtocavesandotherassociated subterraneanhabitats(e.g.,phreaticwaters)inTennessee.Our databasealsoincludedrecordsfortaxaconsideredundescribed andnewtoscienceintheliteratureorviapersonalcommunication withtaxonomicexperts.WefollowedthedefinitionofSket[48] with‘troglobiont’referringtoanyspeciesstrictlyboundto Table2. Taxonomicdiversityofcave-obligatespeciesinTennessee,includingnumberofgenera,numberofdescribedspecies, numberofsingle-caveendemics,numberofsingle20 6 20kmcellendemics,andnumberofoccurrencerecords.TaxonNo.genera No.ofdescribed species No.ofsingle-cave endemics No.ofsingle-cell endemicsNo.ofrecords Annelida Clitellata Branchiobdellida12222 Lumbriculida11111 Platyhelminthes Turbellaria Tricladida130030 Mollusca Gastropoda Basommatophora110010 Stylommatophora230021 Arthropoda Arachnida Acari11003 Araneae61433201 Opiliones110018 Pseudoscorpiones618910101 Diplopoda Callipodida120055 Chordeumatida229211178 Julida11008 Polydesmida12117 Malacostraca Amphipoda31233115 Decapoda2500267 Isopoda31123223 Maxillopoda Cyclopoida230012 Ostracoda Podocopida220014 Hexapoda Collembola41000118 Diplura130061 Insecta Coleoptera10722529336 Diptera1100118 Chordata Actinopterygii Percopsiformes1100109 Amphibia Caudata120049 Total5520048632057 Thislistdoesnotincludeundescribedspeciesorrecordsthatwerenotidentifiedtothespecieslevel. doi:10.1371/journal.pone.0064177.t002 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org4May2013|Volume8|Issue5|e64177

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subterraneanhabitats.Inpractice,specieswereconsidered troglobiontsiftheyhadfewornorecordsfromsurfacehabitats, weredescribedascaveobligatesbypreviousauthors,orexhibited troglomorphicfeatures,suchasthereductionorlossofeyes,little tonopigmentation,andelongationofappendages[2].Troglobiontswerefurtherclassifiedbasedonhabitat,asterrestrial troglobiontsthatoccurinterrestrialsubterraneanhabitatsandas stygobiontsthatoccurinaquaticsubterraneanhabitats. Weexcludedspeciesconsideredaseutroglophiles,subtroglophiles,andtrogloxenes(following[48])thatwerenotobligately associatedwithsubterraneanhabitats.Suchspecieswereidentified onthebasisofhavingseveralrecordsfromsurfacehabitatsor havingbeenclassifiedastroglophiles,trogloxenes,oraccidentals bypreviousauthors.Weexcludednon-troglobiontsfromthe currentstudybecause(1)manyspeciesoccasionallyentercaves andtheirdegreeofcaveassociationisoftendifficulttodetermine, (2)cavestudiesandsurveysreportnon-troglobiontstovarying degrees,and(3)troglobiontsareacoherentecologicalgroupingof speciesthatarerestrictedtosubterraneanhabitatsandusually exhibitdistinctmorphologicalfeaturesaidingintheirecological classificationcomparedtonon-troglobionts.InformationonnontroglobiontcavebiodiversityinTennesseecanbefoundinseveral papers[10,20,24,26,39,49,50]. Distributionalrecordswerecompiledfromseveralsources, includingrelevantscientificliterature,existingbiodiversitydatabases,andpersonalrecords.Literaturerecordswereassembled frompeer-reviewedjournals,books,thesesanddissertations, governmentreports,andcavingorganizationnewsletters.This includedkeywordsearchesofISIWebofScienceandGoogle Scholarandexaminingindetailallreferencescitedintheresulting articles.AfulllistofreferencesisprovidedinTextS1.Wealso obtainedrecordsfrombiodiversitydatabasesmaintainedbythe TennesseeNaturalHeritageInventoryProgram(TNHP),the TennesseeChapterofTheNatureConservancy(TNC),andthe TennesseeCaveSurvey(TCS).Thedatabasealsowassupplementedwithreliableunpublisheddistributionalrecordsmaintainedbyseveraltaxonomicspecialists,aswellasnewrecords resultingfromourownbiospeleologicalsurveys.Biologicalsurveys consistedprimarilyofvisualencountersurveysofterrestrialand aquaticcavehabitatsaswellastrappingforterrestrialinvertebrates(i.e.,baitedpitfalltraps)andaquaticinvertebrates(i.e., baitedfunneltraps). Figure2.Averagetaxonomicdistinctness( D+)forcavesofTennessee:(a)alltroglobionts,(b)terrestrialtroglobiontsonly,and(c) stygobiontsonly. Eachpointrepresentsacave.Ecoregionsarecolor-coded.Thesolidlineisthesimulatedmeanvalueandthefunnelcurveshows the95%confidentlimitsofexpectedvalues. doi:10.1371/journal.pone.0064177.g002 Table3. Mean 6 SDoftaxonomicdistinctness( D+)andspeciesrichness(Sobs)ofsubterraneanbiodiversityinTennesseeperLevel IIIecoregionforalltroglobionts,terrestrialtroglobionts,andstygobionts.InteriorPlateau Southwestern AppalachiansRidge&ValleyInter-ecoregiondifferences Significantpairwise comparisons Taxonomicdistinctness All83.9 6 10.483.0 6 8.179.2 6 11.1H=10.84,df=2,P , 0.01RVvs.IP Terrestrial troglobionts 77.9 6 12.678.5 6 9.079.1 6 7.0H=2.50,df=2,P . 0.05none Stygobionts85.5 6 13.585.5 6 13.073.7 6 17.8H=8.93,df=2,P , 0.05RVvs.IP,RVvs.SWA Speciesrichness All2.9 6 3.03.3 6 3.42.3 6 1.6H=0.31,df=2,P . 0.05none Terrestrial troglobionts 1.8 6 2.42.0 6 2.91.2 6 1.3H=1.35,df=2,P . 0.05none Stygobionts1.1 6 1.11.3 6 1.21.1 6 1.0H=6.02,df=2,P . 0.05none doi:10.1371/journal.pone.0064177.t003 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org5May2013|Volume8|Issue5|e64177

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Alldistributionalrecordsfromcaveswereincorporatedintoan ArcGIS(v.10)databasealongwithspatialinformation(geographic coordinates,ecoregion,county,etc.).Weattemptedtogeoreferenceeachdistributionrecordusingadatabaseofcavesin TennesseemaintainedbyTCS.Some9705caveshavebeen recordedinTennessee,with9517cavesthathavebeenreliably georeferencedandincludedinourstudy(Fig.1).TheTCS requirescavestohaveahorizontallengthof50 9 ,atotalvertical extentof40 9 ,ora30 9 pittobeincludedintheirdatabase.In addition,wecross-referencedourbiologicaldatabasewiththe databasesmaintainedbyTNHP,TNC,TCS,andaU.S.cave biodiversitydatabasecompiledbyCulveretal.[8],whichis availableonlineathttp://www.karstwaters.org.Forseveral reasons,somerecordswereexcluded,includingtaxonomic revisionleadingtosynonymyofspecies,recordsthatwere questionableorrevisedintheliterature,typographicerrors, duplicaterecords,erroneouslocalityinformation,andimproper classificationastroglobiontsintheliteraturebasedonthecriteria mentionedpreviously. Troglobiontdistributionalrecordsinthedatabasewere translatedintoapresence-absencematrix,inwhicheachcave localityrepresentedarowinthematrixandeachcolumn representedasinglespecies.Thismatrixwasusedinanalysesof taxonomicdiversityandspeciesrichness.Thelistoftroglobionts Figure3.Spatialpatternsofspeciesrichnessin20 6 20kmgridcellsdistributedacrossTennessee,including(a)196cave-obligate specieswithmappableoccurrencerecords,(b)terrestrialtroglobiontsonly,and(c)stygobiontsonly. doi:10.1371/journal.pone.0064177.g003 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org6May2013|Volume8|Issue5|e64177

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andthepresence-absencematrixareavailableinTableS1and DatasetS1,respectively.Toprotectsensitivecavehabitatsand species,aswellascopyrighteddataoftheTCS,cavelocationsare notincluded.Pleasecontacttheauthorsorappropriateorganizations(i.e.,TNHP,TNC,andTCS)fordatarequests.SpatialPatternsofBiodiversityWeexaminedspatialpatternsofsubterraneanbiodiversityby generatingagrid-baseddistributionmapofspeciesrichnessand endemisminArcGIS.Wemappeddistributionalpatternsby overlayingagridof20 6 20kmcells(400km2)ontoabasemapof Tennessee.Atotalof321gridcellscoveredtheentirestate,with 215ofthesecellscontainingoneormorecaves.Eachgeoreferencedrecordinthedatabasewasthenassignedtoacellofthis grid.Distributionmapsofspeciesrichnessandendemismwere producedbycountingthenumberofspeciesandendemics(see below)presentinthe321cellsofthegridcoverage.Someprevious studiesexaminedcavebiodiversityatthecountylevel(e.g.,[8]). Tofacilitatecomparisontothesestudies,wealsomappedspecies richnessandsingle-siteendemismatthecountylevel.SamplingEffortandGapAnalysesDeterminingtowhatextentspeciesrichnesswithinagiven 20 6 20kmgridcellreflectstruediversityorsamplingeffortis difficultfromourdatasetalone,aswedidnotincludedistributionaldataofnon-troglobioticfauna.Therefore,weemployed approachesatseveralscales–acrossthestate,byLevelIIIand LevelIVecoregions,andby20 6 20kmcell–toidentifyand evaluatepotentialgaps.First,weusedSpearman’sRank Correlationtesttodetermineifacorrelationbetweenthetotal numberofcavesandthenumberofsampledcaveswithatleast onetroglobiontinagridcellexisted.Cellsthatlackedcaveswere excluded.Astrongcorrelationovertheentirestudyregionwould suggestthattherewasnotasignificantbiasingeographicextentof samplingeffort.Second,wenotedthepercentageofcaveswith troglobiontrecords(‘‘sampledcaves’’)acrossecoregionstoidentify ecoregionsthathadbeensampledatahigherorlowerrate.Third, weusedtwomethodstoidentify‘undersampled’cells.Wefirst identifiedcellswiththegreatestnegativestandardizedresiduals fromthebest-fitlinerelatingcaves/cellandsampledcaves/cell. Wealsousedathresholdapproachtoidentifyallcellswhere , 3% ofcaveshadbeensampledtoidentifycellsthathadbeensampled atamuchlowerratethanthe6.9%ofcavesstatewidethathad beensampled.Cellswithfewerthan10caveswereexcludedfrom thethresholdanalysis.Fortheseandallotheranalyses,allcaves werecountedequally;wedidnotconsidercavelengthordepth.TaxonomicDistinctnessTaxonomicdistinctnesswascalculatedusingthemetricaverage taxonomicdistinctness( D+),whichisthemeanofdistances throughaclassificationtreeforallpairsofspeciesinasample[51]. Higher D+valuesimplyamoretaxonomicallydiversespecies assemblage,whereaslowervaluesimplylowertaxonomicdiversity.Thismetricwascalculatedforeachcaveasasampleusingthe vegan packagev2.0.4[52]inRv2.15.1[53].Becauseaphylogenyis notavailableforallsubterraneanorganisms,theLinnean hierarchicallevels(i.e.,phylum,class,order,family,genus,species) weretranslatedintoaninputclassificationtreefollowingthe IntegratedTaxonomicInformationSystem(ITIS)taxonomically structuredspeciesdatabase[54]. D+wasscaledtoamaximum100 forthemosttaxonomicallyunrelatedspecies.Thismetricwas calculatedforalltroglobionts,terrestrialtroglobionts,and stygobiontsoverallandforeachecoregion.Wetestedfor differencesin D+betweenthethreemainecoregions(IP,SWA, Table4. Sampledcaves,troglobionts(Obs.),single-caveendemics(End.),andestimatedspeciesrichnessbyecoregionin Tennessee.OverallTerrestrialTroglobiontsStygobionts EcoregionCavesObs.End.ChaoJK1BSObs.ChaoJK1BSObs.ChaoJK1BS SoutheasternPlains4305 6 45 6 14 6 111 6 02 6 11 6 023 6 13 6 12 6 0 InteriorPlateau27811619179 6 27158 6 8134 6 598155 6 26135 6 8114 6 41824 6 823 6 220 6 1 WesternHighlandRim2929341 6 942 6 535 6 32234 6 1033 6 427 6 278 6 29 6 18 6 1 WesternPennyroyalKarstPlain2415015 6 117 6 117 6 21111 6 113 6 113 6 248 6 04 6 08 6 0 InnerNashvilleBasin2916025 6 1022 6 418 6 21023 6 1715 6 312 6 267 6 17 6 17 6 1 OuterNashvilleBasin85531178 6 1474 6 662 6 34361 6 1260 6 551 6 31018 6 1214 6 212 6 1 EasternHighlandRim111665118 6 3191 6 776 6 45282 6 1971 6 660 6 41414 6 020 6 316 6 1 SouthwesternAppalachians28910215134 6 15133 6 8116 6 579107 6 15105 6 791 6 42327 6 528 6 225 6 1 CumberlandPlateau617059 6 3928 6 922 6 51652 6 3326 6 820 6 411 6 02 6 11 6 0 PlateauEscarpment2609813126 6 13129 6 8112 6 57597 6 12100 6 786 6 42329 6 529 6 226 6 2 SequatchieValley2329243 6 1041 6 735 6 42033 6 1130 6 524 6 2911 6 312 6 310 6 2 CentralAppalachians2414 6 06 6 25 6 133 6 05 6 14 6 111 6 02 6 11 6 0 RidgeandValley755010120 6 4079 6 762 6 337103 6 4460 6 646 6 31322 6 1019 6 215 6 1 BlueRidgeMountains139214 6 712 6 210 6 156 6 16 6 15 6 144 6 06 6 15 6 1 Total66119647286 6 30262 6 10225 6 5158239 6 30215 6 9183 6 53848 6 848 6 342 6 2 ThesixLevelIIIecoregionsthatcontaincavesarehighlightedinbold.AlsoshownareLevelIVecoregions(subregionsorLevelIIIecoregions)ofthe InteriorPlateauand SouthwesternAppalachians.Observedtroglobiontspeciesrichnessdonotsumbecausesomespeciesarepresentinmorethanoneecoregion.Wealsoest imated extrapolatedspeciesrichnessfromsampledcavesusingthreenon-parametricincidence-basedestimators,includingChao2(Chao),first-orderja ck-knife(JK1),and bootstraprichnessestimator(BS).Fourtroglobionts(includingonesingle-caveendemic)arenotincludedherebecausetheirrecordscouldnotber eliably georeferenced. doi:10.1371/journal.pone.0064177.t004 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org7May2013|Volume8|Issue5|e64177

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andRV)usingaKruskal-Wallisranksumtestafterexaminationof normalityplots.Apost-hocmultiplecomparisontestwasusedto determinewhichpairwisecomparisonsweredifferentusingthe pgirmess packagev1.5.4inR.ObservedandEstimatedSpeciesRichnessSpeciesaccumulationcurveswereconstructedinthe vegan packagebyrandomlysubsamplingcaveswithoutreplacement [55].Wealsoestimatedextrapolatedspeciesrichnessfromthe observedsamples(caves)usingthreenon-parametricincidencebasedestimators,Chao2[56,57],first-orderjack-knife[58],and bootstraprichnessestimator[59].Wechosetoemployavarietyof richnessestimatorsbecausenosingleestimatorhasbeenshownto bebestsuitedacrossallsituationsandtaxa[60].Species accumulationcurveswereconstructedforalltroglobionts, terrestrialtroglobionts,andstygobiontsoverallandforeach ecoregion.Wealsotestedfordifferencesinobservedspecies richnessamongecoregionsusingaKruskal-Wallisranksumtest.EndemismWeexaminedpatternsofendemismattwoscales.First,we consideredthenumberofspeciesthatoccuratonlyasinglecave (i.e.,single-siteendemics).Wealsoconsideredthenumberof speciespresentinonlyonegridcellofthesamplinggridasa measureoflocalendemism(i.e.,single-cellendemics).Wetested foracorrelationbetweenendemismandspeciesrichnessforboth sitesandgridcellsusingSpearman’sRankCorrelationtest.Cells thatlackedcaveswereexcluded.SubterraneanCommunityCompositionWeusedmultivariateanalysestoidentifycavesthathadsimilar troglobiontcommunitiesandtoidentifybiogeographicbreaksin troglobiontcommunities.WeusedtheMultivariateStatistical Packagev3.1[61]toconductPrincipalComponentsAnalysis (PCA)andDetrendedCorrespondenceAnalysis(DCA)ona presence/absencematrixoftroglobionts,generatingascatterplot whereeachcavewasrepresentedbyasinglepoint.Weincluded caveswitheightormoreknowntroglobionts(N=58from16 counties),afterexcludingthreecaves(TCB9inClaiborneCounty, TMN26inMarionCountyandTBD1inBledsoeCounty)that preliminaryanalysesidentifiedasextremeoutliers.TCB9wasthe onlycaveintheRVwitheightormoretroglobionts,andTMN26 andTBD1weretheonlycavesontheeasternescarpmentofthe CumberlandPlateauwitheightormoretroglobionts.Tointerpret theclusteringweobservedinthePCAandDCA,welookedfor correspondencebetweenthoseclustersandfourregionalboundaries:counties,ecoregions,20km 6 20kmcells,andU.S.GeologicalSurvey-definedsubbasins(HUC8).Results DatabaseOverviewandSamplingEffortWecompiled2287recordsofdescribedtroglobiontsfrom Tennessee,ofwhich96%(1976records)couldbegeoreferenced. Another18recordswerefromeightlocalitiesthatwerenotinthe cavedatabasebecausetheselocalitiesfailedtomeettheminimize lengthordepthrequirementstobeconsideredacavebytheTCS. Sixty-threerecordscouldnotbeconfidentlyassignedtoaknown Table5. Tennesseecavesandcavesystemswiththegreatestnumberofcave-obligatespecies.CaveCountyEcoregionTCSNo.No.ofspeciesNo.oftypes CrystalCaveGrundyIP–EasternHighlandRimTGD10232 BigMouthCaveGrundySWA–PlateauEscarpmentTGD2160 DryCaveFranklinSWA–PlateauEscarpmentTFR9162 TomPackCaveFranklinSWA–PlateauEscarpmentTFR87140 LittleSlipperySlitCaveOvertonIP–EasternHighlandRimTOV427140 TrussellCaveGrundyIP–EasternHighlandRimTGD26141 CumberlandCavernsWarrenSWA–PlateauEscarpmentTWR7146 McElroyCaveVanBurenSWA–PlateauEscarpmentTVB10132 HerringCaveRutherfordIP–InnerNashvilleBasinTRU8131 KeithCaveFranklinSWA–PlateauEscarpmentTFR14130 SwampRiverCaveVanBurenIP–EasternHighlandRimTVB657130 SkullCaveGrundyIP–EasternHighlandRimTGD24130 BunkumCavePickettIP–EasternHighlandRimTPI2123 CaneyHollowCaveFranklinIP–OuterNashvilleBasinTFR2121 GrapevineCaveFranklinSWA–CumberlandPlateauTFR423120 WalkerSpringCaveFranklinIP–EasternHighlandRimTFR28120 CavesystemCountyEcoregionTCSNo.No.ofspeciesNo.oftypes Crystal/WonderCaveSystemGrundyIP–EasternHighlandRimTGD10,TGD30246 BigMouth/BigRoomCaveSystemGrundySWA–PlateauEscarpmentTGD2,TGD3,TGD20200 RumblingFallsCaveSystemVanBurenIP–EasternHighlandRimTVB657,TVB588,TVB515, TVB352 170 Undescribedspeciesarenotincluded.TheuniqueTennesseeCaveSurveynumber(TCSNo.)foreachcave,ecoregion(LevelIIIandLevelIV),speciesric hness(No.of species),andthenumberofspeciesforwhicheachcave/cavesystemisthetypelocality(No.oftypes)arealsonoted. doi:10.1371/journal.pone.0064177.t005 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org8May2013|Volume8|Issue5|e64177

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caveinthedatabase.Ourworkingdatasetincluded1976records from661caves(Fig.1c),representing196species.Wealso compiled147recordsfortaxareportedas‘‘new’’or‘‘undescribed’’speciesand83recordsthatcouldnotbereliably identifiedtothespecieslevel.Ofthese230records,98%could beconfidentlyassignedtoacaveintheTCScavedatabase. However,theserecords,aswellasthosethatcouldnotbe georeferenced,wereexcludedfromsubsequentanalyses. Just6.9%ofallcavesinTennesseehaverecordsoftroglobionts. MostsampledcaveswereconcentratedinthePlateauEscarpment oftheSWAandintheIP(Table1).Thecumulativenumberof describedtroglobiontshasincreasedwithtime(Fig.S1).Since 1950,thenumberofspecieshasincreasedby270%from54 speciesto200speciesatpresent.However,therateofnewspecies reportedfromTennesseehasslowedsince1980despitean increaseinthenumberofstudiesandpublications.TaxonomicDiversityThecompileddatabasecontainedrecordsfor55generaand 200describedspecies(includingthreesubspecies),whichincluded fourphyla,tenclasses,and22ordersofinvertebratesaswellas twoclassesandordersofvertebrates(Table2).Terrestrial troglobiontsaccountedfor80%(160species)ofalltroglobionts, whereasstygobiontsaccountedfor20%(40species).Coleoptera (beetles;tengeneraand72species),chordeumatidmillipedes(two generaand29species),andpseudoscorpions(sixgeneraand18 species)werethemostdiverseterrestrialorders,comprising74.4% ofallterrestrialtroglobionts.Amphipods(threegeneraand12 species)andisopods(twogeneraandtenspecies)werethemost diverseaquaticgroups. Mostcaveshad D+valueshigherthanthesimulatedmean butwithin95%confidencelimits(Fig.2a).Ninecaves(fourin theIPandfiveintheSWA)hadhigherthanexpected D+for alltroglobionts,whereasnocavesintheRVhadhigheror lowerthanexpected D+.Asinglecave(TWR10intheIP)had lowerthanexpected D+.Threecaveshadhigherthanexpected D+foralltroglobiontsandoneothercaveintheIPhadhigher thanexpected D+forterrestrialtroglobionts(Fig.2b)butnot stygobionts(Fig.2c).Fourcaveshadlowerthanexpected D+for terrestrialtroglobionts,butnotforstygobionts.Averagetaxonomicdistinctnessoftroglobiontsvariedamongecoregions,with thehighestvaluesintheIPandSWA(Table3).However, differenceswereonlysignificantbetweentheIPandRV.All ecoregionshadsimilarvaluesof D+whenconsideringterrestrial troglobiontsonly,whereastheIPandSWAhadsimilarvalues of D+forstygobionts,whichwerebothsignificantlyhigherthan theRV(Table3).SpeciesRichnessSpeciesrichnesswasgreatestalongtheescarpmentsofthe CumberlandPlateaumarkingthetransitionfromtheSWAinto theIP(Fig.3a),particularlythesouthernsectionwheregreatest richnessoccurredinnortheasternFranklin,southwesternGrundy, andnorthwesternMarioncounties(Fig.S2).Incontrast, troglobiontspeciesrichnesswasgreatestinthenorthernRVin ClaiborneandHancockcounties.Speciesrichnessdifferedamong thethreemajorcave-containingecoregions,withgreatestspecies richnessintheIPandSWAandlowestspeciesrichnessintheRV (Table4).AmongLevelIVecoregions,greatestspeciesrichness wasobservedinthePlateauEscarpmentoftheSWA(98species) followedbytheadjacentEasternHighlandRim(66species)and OuterNashvilleBasin(53species)oftheIPtothewest(Table4; Fig.S3).Observedterrestrialtroglobiontrichnessfollowedan identicalpatternwithoveralltroglobiontrichness,withgreatest speciesrichnessobservedintheIPandSWA,specificallywithin thePlateauEscarpmentecoregion(79species)oftheSWA (Table4,Fig.3b).Observedstygobiontrichnessalsowasgreatest intheIPandSWA,withgreatestspeciesrichnessinthePlateau Escarpment(Table4,Fig.3c). Troglobiontspeciesrichnessaveraged3.0 6 3.0speciesper sampledcave.Thirty-ninecavescontainedtenormoretroglobionts,includingthreecaveswith15ormorespeciesandonecave with23species(Table5).Allofthesecaveswerelocatedineither theIPorSWA.Over47%(313)ofcaveswererepresentedbya singledocumentedspecies.Terrestrialtroglobiontspeciesrichness averaged1.8 6 2.5speciespercave.Twelvecavescontainedtenor moreterrestrialtroglobiontspecieswithamaximumof19species inasinglecaveintheIP.Stygobiontspeciesrichnessaveraged Figure4.Speciesaccumulationcurvesfor(a)alltroglobionts, (b)terrestrialtroglobionts,and(c)stygobiontsinthethree majorcave-bearingecoregionsinTennessee. Theshadedarea aroundeachlinerepresentsthe95%confidenceinterval. doi:10.1371/journal.pone.0064177.g004 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org9May2013|Volume8|Issue5|e64177

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1.2 6 1.1speciespercave.Sixcavescontainedfiveormorespecies withamaximumofeightspeciesatasinglecaveintheSWA. Therewasastrongassociationbetweenterrestrialtroglobiont speciesrichnessandstygobiontspeciesrichness( r= 0.79, P , 0.001).Observedspeciesrichnessforalltroglobionts,terrestrial troglobionts,andstygobiontsdidnotdifferamongmajor ecoregions(Table3). Observedspeciesrichnesswashighlycorrelatedwithsampling effort(numberofcaveswithrecordsinagridcell; r =0.95, P , 0.001),withnearlyidenticalcorrelationcoefficientswhen consideringjustterrestrialtroglobionts( r =0.88,P , 0.001)andjust stygobionts( r =0.89,P , 0.001),respectively.Speciesaccumulation curvesdidnotapproachanasymptoteforalltroglobionts(Fig.4a) ineachmajorecoregion,butthiswasdrivenprimarilyby terrestrialtroglobionts(Fig.4b),asstygobiontsdidapproachan asymptote(Fig.4c).Thissuggeststhatthecurrentlevelofsampling capturedtotalspeciesrichnesswellforaquaticcavetaxabutnot forterrestrialspecies.Thethreerichnessestimatesshowedthatthe observedspeciesrichnessofalltroglobiontsrepresentedatleast 69%ofestimatedspeciesrichness,withobservedterrestrial troglobiontrichnessandobservedstygobiontrichnessrepresenting atleast66%and79%oftotalestimatedrichness,respectively (Table4).EndemismMosttroglobiontshavesmallgeographicrangesinTennessee. 31.5%(63species)oftroglobiontswereknownfromasingle 20 6 20kmcell,with24%(48species)knownfromjustasinglesite (Fig.5).Fortysingle-siteendemicswereterrestrialtroglobionts, including25speciesofbeetles(orderColeoptera)andninespecies ofpseudoscorpions(orderPseudoscorpiones)(Table2).Almost two-thirds(130species)ofalltroglobiontsinTennesseeareknown fromfiveorfewercaves,including111terrestrialtroglobionts (69%ofallterrestrialtroglobionts)and19stygobionts(48%ofall stygobionts)(Fig.6).Only22troglobionts(14terrestrialtroglobiontsandeightstygobionts)areknownfrom20ormorecaves andjustfivespecies(theisopod Caecidoteabicrenata ,thecrayfish Orconectesaustralis ,thespider Phanettasubterranea ,thefly Spelobia tenebrarum ,andthecavefish Typhlichthyssubterraneus )havebeen reportedfrom100 + caves.Sixcaveswerehometomorethanone single-siteendemic:TMN26inMarionCountyhadthreesinglesiteendemicspecies,whereasTCB9(ClaiborneCounty),TMU1 (MauryCounty),TCY13(ClayCounty),TWR7(WarrenCounty) andTRH2(RheaCounty)eachhadtwosingle-siteendemic species. Single-cell( r =0.31, P , 0.001)andsingle-siteendemicity ( r =0.23, P , 0.001)wereweaklycorrelatedwiththenumberof cavespergridcell.Thenumberofsingle-cellendemics( r =0.55, P , 0.001)andsingle-siteendemics( r =0.48, P , 0.001)werealso positivelycorrelatedwithspeciesrichnesspergridcell.GapAnalysisThenumberofcavessampledwascorrelatedwiththetotal numberofcavespergridcellacrossTennessee( r =0.67, P , 0.001).Thissuggestsareasonablyevenlevelofsampling acrossthestate.Thepercentageofsampledcavesranged5.1– 28.6%withinLevelIIIecoregionsthatcontainedcaves,and 5.1–9.8%amongthethreemajorcaveecoregions(Table1). WithinLevelIVecoregionsoftheIPandSWA,thepercentage ofsampledcavesranged5.4–10.8%withtheexceptionofthe SequatchieValley,where20.4%ofcaveshavebeensampled (Table1). Onasmallerscale,weidentifiedgridcellsthatwere undersampledbytwodifferentmethods–usingresidualsand usingathreshold.Bothmethodsidentifiedsimilargroupsof cells(74%overlapbetweenthetwoapproaches),butthe thresholdmethodincludedcellswithfewercavesandomitted somecellswithhundredsofcavesthathadbeensampledat . 3%.Wepreferredthethresholdmethodasitemphasizedcells thathadnotbeensampledatall,evenwhenthecellcontained relativelyfewcaves.Thethresholdmethodidentified16cells thatcontainmorethan25documentedcaveswhere , 3%had beensampled.Thesecellswereconcentratedinnortheast TennesseeintheRVbutalsoscatteredacrosstheIP(Fig.7). Weidentified29gridcellsthatcontain10–25documented cavesandhavenothadasinglecavesampled.Thesecellswere alsoconcentratedinthenortheastRV,withotherundersampled cellsscatteredacrossthesouthernRVandIP(Fig.7).TroglobiontCommunitiesPCAandDCAidentifiedsimilarregionalstructurein troglobiontcommunitiesacrosscentralTennessee.Thisstructure largelycorrespondedtoUSGSHUC8watershedsubbasins(Fig.8a (PCA),DCAnotshown).Weidentifiedfivetroglobiontcommunitiescomposedofcavesfromonetothreeadjacentsubbasins. Fifty-fiveof58cavesclusteredwithcavesfromtheirrespective subbasinoradjacentsubbasins,andtherewasalmostnooverlapin thePCAbetweenthefivetroglobiontcommunities(Fig.8a).The twocavesfromtheUpperElksubbasinthatclusteredwithcaves fromtheTennesseeRiver-GuntersvilleLakesubbasinarelocated ontheeasternsideoftheUpperElksubbasin,lessthan3kmfrom Figure5.Spatialpatternsofendemismin20 6 20kmgridcellsdistributedacrossTennessee:numberofsingle-celltroglobionts. doi:10.1371/journal.pone.0064177.g005 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org10May2013|Volume8|Issue5|e64177

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thedrainagedividewiththeTennesseeRiver-GuntersvilleLake subbasin(Fig.8b). ThemostextremeoutlierinthisanalysiswasTCB9in ClaiborneCountyinthePowellRiversubbasin,theonlycavein theRidgeandValleyecoregionwitheightormoreknown troglobionts(Fig.8b).OftheninetroglobiontsknownfromTCB9, sevenwerenotsharedwithanyothercaveintheanalysis.Thetwo sharedspecieswerethespider Phanettasubterranea ,whichiswidely Figure6.HistogramofcaverecordsinTennesseefor(a)terrestrialtroglobiontsand(b)stygobionts. Mostspeciesofterrestrial troglobiontsandstygobiontshavebeenreportedfromfiveorfewercaves. doi:10.1371/journal.pone.0064177.g006 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org11May2013|Volume8|Issue5|e64177

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distributedacrossthestate,andtheamphipod Crangonyxantennatus , whichisalsofoundintwocavesontheeasternescarpmentofthe CumberlandPlateau:TMN26intheMiddleTennesseeRiver– ChickamaugasubbasinandTBD1atthenortheastcornerofthe SequatchieRiversubbasin(Fig.8b).Thesetwocaveswerealsothe nextgreatestoutliersintheanalysis.Discussion SpatialPatternsofSpeciesRichnessandEndemism withinTennesseeTennesseepossessesaremarkablediversityofcave-obligate organisms,matchedbyonlyTexaswithrespecttooverall speciesrichness,whilehavingmoreterrestrialtroglobiontsthan anyotherstateintheUnitedStates[1].Twomajorkarst regions,theAppalachiansandtheInteriorLowPlateau,occur inTennessee[62,63].Thesekarstregionsextendacrossmultiple statesandcontainmorecavesandtroglobiontsthananyother caveregionsinthecountry[1,63].TheAppalachianscave regioninTennesseeisrepresentedbytheRidgeandValley ecoregion,whereastheInteriorLowPlateaucaveregionis representedbytwoecoregions,theInteriorPlateauand SouthwesternAppalachians.Eachoftheseecoregionssupports asignificanttroglobiontcommunity.Althoughthelistofknown caveobligatespeciesinTennesseeisnotcomplete,several significantpatternshaveemergedfromourstudy. First,speciesrichnessisnotevenlydistributedamongthemajor caveregionsinthestate(e.g.,theIP,SWAandRV).Instead,itis clusteredwithhighestrichnessinthesouthernsectionofthe CumberlandPlateau(intheIPandSWA),withamaximumof36 terrestrialtroglobiontsandeightstygobiontsinasingle20 6 20km gridcell.AlthoughspeciesrichnesswasequivalentbetweentheIP andSWA,speciesrichnessintheRVwaslessthanhalfthat observedintheothertwoecoregions.Thisdisparityissomewhat surprisinggiventhatspeciesrichnessiscomparablebetweenthe InteriorLowPlateau,whichincludestheIPandSVA,andthe Appalachianscaveregion,whichincludestheRV[1,62,63].This isbestexplainedbydecreasedavailabilityofcaveandkarsthabitat intheRVcomparedtoIPandSWAinTennessee,giventhat speciesrichnessisstronglyassociatedwiththenumberofcaves observed(aproxyforavailablehabitat;[7],thisstudy).Thereare 1469documentedcavesintheRVversus5011and2834cavesin theIPandSWA,respectively(Table1).Cavedensity(andspecies richness)dramaticallydeclinesinthesouthernRVofTennessee wherethicknessandextentofexposedcarbonaterocksare reduced(Figs.1and3). Onlyasmallfraction(7.5%,15species)oftroglobiontsinthe stateissharedbetweentheIP,SWA,andRV.Ofthe troglobiontsthatoccurinallthreeecoregions,mosthavebroad distributionscomprisingmultiplestates,suchasthepseudoscorpion Hesperochernesmirabilis andthecavespider Phanettasubterranea [64].Beyondthesefifteenspecies,theIPandSWAshared another44species,whereastheRVsharedjustthreeadditional specieswitheithertheIPorSWA.Overall,theIPandSWA sharemanytroglobionts,whereastheRVfaunaislargely distinctfromboth. Inadditiontothemajordifferencesintroglobiontdiversity betweenecoregions,weidentifiedhydrologicalbasinsasanother importantinfluenceoncavebiodiversityinTennessee.Troglobiontcommunitiesmorecloselyreflecthydrologicalboundaries thanecoregionboundaries;indeed,mosttroglobiontcommunities includedcavesfromtheSWAandtheadjacentIP(Fig.8b).This overlaphelpsexplainthelargenumberofspeciessharedbetween theSWAandIP.Thispatternisconsistentwithabiogeographic breakincavecommunitiespreviouslyobservedbetweenhydrologicalbasinsinsouth-centralTennessee[27].Additional samplingisrequiredtodeterminehowtroglobiontcommunities varyacrosstheRV. MostsubterraneandiversityinTennesseecavesisfound regionallyratherthanlocallywithinindividualcaves.Mostcaves containbutasmallfractionoftheregionaldiversitywithina 20 6 20kmgridcell.Thislowalpha-versushighbeta-diversity appearstobetheruleratherthantheexceptioninsubterranean assemblages[2,65–67].Lowlevelsofconnectivityamongcaves andreducedopportunitiesfororabilitiestodispersemayresultin substantiallylowerlocaldiversitythanregionaldiversity[65]. Anotherspatialpatternthatemergedisthatthereisageneral declineinspeciesrichnessfromsouthtonorthintheeasternIP andSWA,particularlyalongthewesternescarpmentofthe CumberlandPlateau(Fig.3a),eventhoughcavedensitiesare highertothenorth(Fig.1b).Thispatternhasbeendocumented previouslyintheInteriorLowPlateaucaveregionbyCulveretal. [17],whoidentifiedamidlatituderidgebetween33 u and35 u Nin NorthAmericawhereterrestrialsubterraneanbiodiversitypeaks. Theprimaryhotspotofspeciesrichness(andendemism;seebelow) inTennesseeliesjusttothenorthofthishypothesizedridge,with severalgroupsreachingtheirhighestdiversityinthisarea,suchas amphipods,millipedes,andcollembolans.Incontrast,thediversity gradientdeclinesnorthtosouthintheRV,butcorrespondswith thegradientincavedensityinthisecoregion. Endemism,likespeciesrichness,isnothomogenousnorisit concentratedinperipheralorisolatedcaveregions.Rather Figure7.Spatialpatternsofsamplinggapsin20 6 20kmgridcellsdistributedacrossTennessee. Allcellswherelessthan3%ofcaves havetroglobiontrecordsarehighlighted. doi:10.1371/journal.pone.0064177.g007 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org12May2013|Volume8|Issue5|e64177

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endemismishigherinTennesseewithinareasthatalsohave higherspeciesrichness.Inparticular,endemismwasconcentratedinthesouthernsectionoftheCumberlandPlateau, where25%(12species)ofsingle-siteendemicsarefoundinjust Figure8.ZoogeographicregionsfortroglobiontsofTennessee. (a)PrincipalComponentsAnalysisfor58caveswitheightormoreknown troglobionts.PCAAxes1and2correspondtotheXandYaxes,respectively.EachpointonthePCArepresentsasinglecave,andcaveswithsimilar proximitybetweenpointsindicatesimilaritybetweenthetroglobiontcommunitiesofthosecaves.Eachcaveiscoloredtoreflectitslocationinone of theU.S.GeologicalSurvey-defined(HUC8)watershedsubbasins.Fiveclustersrepresentinggeographicallycontiguousgroupingsofcavesarecirc led andlabeled.(b)Locationsofcavescolor-codedbytheirclustersonthePCA.Alsoincludedarethreecaves(oneeachfromthePowell,Sequatchie,and MiddleTennessee–Chickamaugasubbasins)thatwereexcludedfromthePCAanalysisasextremeoutliersandthathadhighlydistincttroglobiont communities.WatershedboundariesareoverlainonecoregionscoloredasinFigure1. doi:10.1371/journal.pone.0064177.g008 SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org13May2013|Volume8|Issue5|e64177

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six20 6 20kmgridcellsinFranklin,Grundy,andMarion counties(Fig.5).Thisregioniscontiguouswithanareaofhigh endemismidentifiedpreviouslyinadjacentnortheasternAlabama[68].Interestingly,endemismisnothighestinregions withthegreatestpotentialforisolation.TheRVecoregionis moredissectedandlesscontiguous(i.e.,greaterpotentialfor isolation)thanthesubregionsoftheIPandPlateauEscarpment oftheSWA,yetthenumberofsingle-caveendemicspeciesin theRVisconsiderablylower(Table4). Mostcave-obligatespeciesareknownfromjustafewlocalities andfewspecieshavebeenreportedacrosslargerareasgivingthe impressionthatendemismishigh.Whilelevelsofendemismmay beoverestimatedduetoincompletesamplingorinvalidtaxonomy, highendemisminsubterraneanfaunaisacommonpattern.Most terrestrialandaquaticspecieshavesmallgeographicranges,with justasmallfractionhavinglargedistributions[64].Ofthose specieswithpresumablylargedistributions,molecularstudieshave shownthatseveralareactuallycomprisedofmorphologically crypticlineageswithsignificantlysmallerranges[69–71],includingthelonecavefishspeciesfoundinTennessee[40]. Typhlichthys subterraneus isthefourthmostabundantcave-obligatespeciesin Tennesseeintermsofnumberoflocalities.However,recent molecularworkindicatesthatthisspeciesisactuallycomprisedof severalcrypticlineages(sevenlineagespresentinTennessee)with smallergeographicrangesthatarelargelyisolatedbecauseof hydrologicalbarriers[40].Lessthan10%ofTennessee’s troglobiontshavebeensubjectsofmolecularorphylogeographic studies.Consequently,thereisahighlikelihoodthatadditional crypticbiodiversitywillbediscoveredinthefuture.ProcessesUnderlyingPatternsofBiodiversityand EndemismDifferencesinspatialpatternsofbiodiversityandendemism amongsubterraneancommunitiessuggestthattheyaregoverned bydifferentfactors,includinghabitatavailability,opportunityfor dispersal,historicalfactors,andsurfaceproductivity.Thesefactors arenotmutuallyexclusiveandmultiplefactorslikelycontributeto presentpatternsofbiodiversityandendemism.Additional distributionaldataandstudyareneededtounravelthe contributionsofhypothesizedunderlyingprocessesthathave resultedinthesepatternsofdiversityandendemisminsubterraneancommunitiesoftheInteriorLowPlateauandAppalachians. However,Tennessee’sremarkablesubterraneandiversitymaybe largelyexplainedby(1)thelargeamountofexposedkarstandcave developmentbutalsoavariedtopographyandgeology,(2)a geographiclocationatthejunctionofthetwokarstregionsin NorthAmericawiththegreatesttroglobiontdiversity,and(3)its proximitytotheproposedmid-latitudebiodiversityridgefor terrestrialcavefauna,ahypothesizedregionoflong-termhigh productivityandfavorableclimate[17].Below,wespeculateon theimportanceoftheseprocessesthatunderlietheobserved spatialpatternsofsubterraneanbiodiversityinthestate. Thegreatertheamountofavailablehabitat,thegreater likelihoodofsupportinghigherspeciesrichness,asthereis greaterpotentialtosupportlargerpopulationsandforlower extinctionrates[17,64].Largerareasofkarst,liketheInterior LowPlateau,areexpectedtosupportgreaternumbersof speciesduetomorecavesandgreaterhabitatdiversity[8]. Speciesrichnessishighestalongthewesternescarpmentofthe CumberlandPlateauintheInteriorLowPlateau,which coincideswiththeregionofgreatestcavedensity.Previous studieshavealsoshownthatthenumberofcavesisagood predictorofregionalspeciesrichness[17,63,64].Inthe Appalachianscaveregion,bothcavedensityandspecies richnessarelower.Increasedcavedensitymayalsoprovide moreopportunitiesforcolonizationofsubterraneanhabitats [17]. Differencesincaveconnectivityandopportunitiesfordispersal alsolikelyinfluencepatternsofsubterraneanbiodiversity.Assumingcavedensityispositivelycorrelatedwithcaveconnectivity, areasofhighcavedensitypresumablyhavehigherconnectivity betweencaves,whichoffergreateropportunitiesfordispersal. Dispersalmaydecreaseextinctionratesanddifferencesinspecies compositionamonglocalitiesorregions[72].Ouridentificationof fivetroglobiontcommunitiesintheSWAandIPofcentral Tennesseeisconsistentwiththishypothesis,asgeographically proximatecaveshadmoresimilartroglobiontcommunities.These communitiescorrespondedtohydrologicalboundariesandlikely reflectincreasedpastorcurrentconnectivitybetweensubterraneanhabitatswithinandbarriersbetweendrainages,givenmost cavesintheIPandSWAaresolutionalcavesformedfrom dissolutionoflimestonesanddolomitesbycarbonicaciddissolved inrainwaterandgroundwater.Thegreaterconnectivityand dispersalbetweentheIPandSWAmayexplainthelargenumber ofsharedspeciesbetweentheseregions.Incontrast,less connectivitymaypromotedifferencesinspeciescompositionand endemism.Thefaultedandfoldedcave-bearingrocklayersofthe RVaremoredissectedandmuchlesscontiguousthanthe horizontalstrataoftheInteriorLowPlateau(IPandSWA),which offergreaterprobabilityofisolation.Whilefewspeciesareshared betweentheAppalachiansandInteriorLowPlateaucaveregions inTennessee,endemismisactuallylowerintheAppalachians ([68],thisstudy).Variationincaveconnectivityandopportunities fordispersalisaplausiblehypothesistoexplaindifferencesin speciescompositionbutitcannotaloneexplaindifferencesin endemismamongregions.However,mosttroglobiontsin Tennesseeareknownfromasmallnumberofcavesandhave smallgeographicdistributions,sounquestionablycaveconnectivityanddispersalplaysignificantrolesinshapingspatialpatternsof diversityandendemisminsubterraneanfaunas. Differencesinregionalspeciesdiversityandendemismarealso likelyinfluencedbypastandcurrentenvironmentalfactors,such asclimaticshiftsduringthePleistoceneandvariationinsurface productivityamongregions.InNorthAmerica,thecaveregion (southernsectionoftheInteriorLowPlateau)withgreatest biodiversityisassociatedwithhighprecipitationandtemperature relativetomostothercaveregions[17].Becausealmostall availablefoodincavesystemsresultsfromsurfaceproductivity,it hasbeensuggestedthatthishotspotofterrestrialcavebiodiversity, whichthesouthernTennesseeborderliesjusttothenorthof, couldcorrespondtolong-termlevelsofhighsurfaceproductivity, particularlyoverrecentgeologicaltimesinthePleistocene[17]. Onaverage,cavesinthisregionlikelyhavemoreenergyavailable tosupportlargerpopulations,morespecies,andmorediverse communities.Indeed,almostallcaveswiththemosttaxonomically diversecommunitiesoccurinthisregion.Southernsectionsofthe InteriorLowPlateauinTennesseemaynothaveexperienced significantdecreasesinsurfaceproductivitycomparedtoareas furthernorthandintheAppalachianscaveregion,which experiencedcoolertemperaturesandfacedmoredramaticdry episodesduringthePleistocene.Suchrapidclimaticshiftslikely causedmanyspecies,particularlyterrestrialspecies,tobe extirpatedortogoextinctintheseregions.HotspotsofSubterraneanBiodiversityAsoriginallydefined[73,74],hotspotsofbiodiversityarelarge regionsofsignificantspeciesrichnessandendemismthatarealso underthreatataglobalscale.However,hotspotsarealsoSubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org14May2013|Volume8|Issue5|e64177

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delineatedatregionalandlocalscalestoassistinsetting conservationpriorities.Previousstudiesofsubterraneanbiodiversityhaveidentifiedregionalhotspotsbasedonspeciesrichness, endemismorrarity[7,68,75–78].Weidentifiedahotspotof subterraneanbiodiversitywithacenteralongtheescarpmentof theCumberlandPlateauinnortheasternFranklin,southwestern Grundy,andwesternMarioncountiesdefinedbybothspecies richnessandendemism.Centersofbothterrestrialandaquatic troglobiontdiversityandendemismoccurwithinthishotspot.This hotspotextendsnorthwardalongthewesternescarpmentofthe plateauintoVanBurenCountyandiscontiguoustothesouth withahotspotpreviouslyidentifiedfromJacksonCounty, Alabama[8,17].Thishotspot,comprisinglessthan5%of Tennessee’stotalarea,hostsnearly50%(91of200species)of Tennessee’ssubterraneanbiodiversity,including71terrestrial troglobiontsand20stygobionts. Althoughsubterraneandiversityisgreateratregionalversus localscales,conservationeffortsforsubterraneanfaunaoftenstart withtheprotectionofindividualcaves.CulverandSket[65]were thefirsttoidentifyhotspotsofsubterraneanbiodiversityatthe levelofindividualcaves.Theydocumented18cavesandtwokarst wellsthatcontain20ormorespeciesoftroglobionts,butthislist hassinceincreasedto36sites[2].Ofthese,justsixsitesoccurin NorthAmerica,includingSheltaCaveinMadisonCo.,Alabama (24species),andtheMammothCavesysteminEdmonsonCo., Kentucky(41species).Here,weaddCrystalCaveinGrundy CountytoCulverandPipan’s[2]listofbiologicallydiversecaves. CrystalCavesupports23troglobionts,morethananyothercave inthestate.However,severaladditionalcavesinFranklin, Grundy,andMarioncountiesmayreachorsurpass20species withadditionalsamplingeffort(Table5).KnowledgeGapsandImplicationsforConservationand ManagementTheidentificationandprotectionofpriorityareasarecommon goalsinmanagingandconservingbiodiversity.However,our knowledgeofsubterraneanbiodiversityisinconsistentandoften deficientinmanyareas.Withfewexceptions,caveecosystemsand habitatsarepoorlysampledwhencomparedwithsurface ecosystems.Forinstance,lessthan7%ofcavesinTennessee havebeensampled.Themajorityofspeciesareknownfromjusta fewoccurrences(Fig.6).However,samplingincavesandother subterraneanhabitatsisdifficultandoftendirectedatspecifictaxa (e.g.,formolecularstudies).Consequently,spatialcoverageand samplingeffortareundeniablyvariableamonggroupsanditis extremelydifficulttodeterminewhetheragivenspeciesisactually rareorpresumedrarityistheconsequenceofinadequate sampling.Regardless,weidentifiedseveralgridcellsthatare undersampledrelativetotherestofthestate,particularlyinthe northernRVofnortheastTennessee(Fig.7). Moreover,cavebiologicalinventoriesareoftenplaguedby uncertaintaxonomyorspeciesdetermination.Weexcluded147 occurrencerecordsfortheseveryreasons,includingrecordsto 60speciesreportedasneworundescribedandawaiting descriptionintheliterature.Thislistincludesupto19 potentiallynewspeciesofbeetles,11collembolans,eight diplurans,andsevenamphipods.Speciesrarefactioncurvesof expectedspeciesrichnessalsosuggestthatsubstantialdiversity remainstobesampledfromeachmajorecoregion(Fig.4; Table4),particularlyforterrestrialspecies.Theevidence stronglysuggeststhatmanyadditionalspeciesawaitdiscovery fromsubterraneanhabitatsinTennessee. Tothisend,weoutlinesixconservationandmanagement prioritiesrelatedtosubterraneanfaunaintheInteriorLow PlateauandAppalachianscaveregionsofTennessee:(1) Improvethespatialcoveragebysamplingcavesinareas identifiedasundersampled,inparticulartheRidgeandValley ecoregionofnortheastTennessee.(2)Improvethesampling effortfordiversetaxonomicgroups,particularly Pseudanophthalmus beetles, Litocampa diplurans,and Stygobromus amphipods, wheremostspeciesareknownfromjustafewcavesand numerousundescribedspecieshavebeenreported.(3)Conduct molecularworkonwidespreadspecies(e.g.,theisopod Caecidotea bicrenata ,thespider Phanettasubterranea andthefly Spelobia tenebrarum )todeterminewhetherthesetaxacontaincryptic lineagesanddiversity.(4)Workwithtaxonomicspecialiststo describethe60taxareportedasneworundescribedinthe literature.(5)Increasethegeographicextentofthedatabaseto includecaveregionsinadjacentstatesinordertoimproveour knowledgeongeographicdistributionsofindividualspeciesas wellasestimatesofspeciesrichnessandendemismatvarying spatialscales.(6)Conductconservationassessmentswhendata warrantontroglobiontsofTennessee.Just10ofthe200species reportedinTennesseehavehadInternationalUnionforthe ConservationofNature(IUCN)RedListassessmentsconducted (TableS1).Despiterecentprogress,significantworkremainsto clarifytheecologyandevolutionofTennessee’scaveecosystems.SupportingInformationFigureS1Cumulativenumberofnewspeciesof troglobiontsreportedfromTennesseesince1840. The dashedlineshowsthenumberofspeciesdescribedbydecade. (TIF)FigureS2Spatialpatternsofspeciesrichnessand endemisminTennesseecounties. (a)CountiesofTennessee, (b)troglobiontspercounty,and(c)single-siteendemicspercounty. (TIF)FigureS3Speciesaccumulationcurvesforthemajor cave-bearingLevelIVecoregions(subregionsofLevelIII ecoregionsinTennessee,including(a)WesternHighlandRim,(b)WesternPennyroyalKarst,(c)Outer NashvilleBasin,(d)InnerNashvilleBasin,(e)Eastern HighlandRim,and(f)PlateauEscarpment. Species accumulationcurvesareshownforalltroglobionts(gray), terrestrialtroglobionts(red),andstygobionts(blue).Theshaded areaaroundeachlinerepresentsthe95%confidenceinterval. (TIF)TableS1Listofdescribedtroglobionts,including160terrestrial troglobiontsand40stygobionts,documentedfromTennessee cavesandassociatedhabitats. (DOCX)DatasetS1CSVdatafileofpresence-absencematrixof cavesandspeciesusedinstatisticalanalyses. The workingdatasetincluded1976recordsrepresenting661caves and196troglobionts. (CSV)TextS1BibliographyofTennesseecaveobligatespecies. (DOC)AcknowledgmentsWethanktheTennesseeCaveSurvey(GeraldMoni),TennesseeChapter oftheNatureConservancy(CoryHolliday),TennesseeNaturalHeritage Program(RogerMcCoyandDavidWithers),andseveraltaxonomic SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org15May2013|Volume8|Issue5|e64177

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specialistsforprovidingdata,particularlyJulianLewis.Wealsothank ChrisVandeVenforassistancewithArcGIS.AuthorContributionsConceivedanddesignedtheexperiments:MLNKSZ.Performedthe experiments:MLNKSZ.Analyzedthedata:MLNKSZ.Contributed reagents/materials/analysistools:MLNKSZ.Wrotethepaper:MLZ KSZ.References1.HobbsHHIII(2012)DiversitypatternsintheUnitedStates.In:WhiteWB, CulverDC,editors.Encyclopediaofcaves,2ndedition.Amsterdam:Academic Press.251–264. 2.CulverDC,PipanT(2009)Thebiologyofcavesandothersubterranean habitats.Oxford:OxfordUniversityPress.256p. 3.PackardAS(1888)ThecavefaunaofNorthAmerica,withremarksonthe anatomyofthebrainandtheoriginoftheblindspecies.MemNatlAcadSci4: 1–156. 4.NicholasBG(1960)ChecklistofmacroscopictroglobiticorganismsoftheUnited States.AmMidlNat64:123–160. 5.BarrTC,CulverD,KaneT(1995)BiospeleologyintheUnitedStates.In: JuberthieC,DecuV,editors.Encyclopediabiospeologica.Moulis,France: SocietedeBiospeologi.403–416. 6.PeckSB(1998)AsummaryofdiversityanddistributionoftheobligatecaveinhabitingfaunasoftheUnitedStatesandCanada.JCaveKarstStud60:18– 26. 7.CulverDC,HobbsHHIII,ChristmanMC,MasterLL(1999)Distributionmap ofcavesandcaveanimalsintheUnitedStates.JCaveKarstStud61:139–140. 8.CulverDC,MasterLL,ChristmanMC,HobbsHHIII(2000)Obligatecave faunaofthe48contiguousUnitedStates.ConservBiol14:386–401. 9.HolsingerJR,PeckSB(1971)TheinvertebratecavefaunaofGeorgia.BullNatl SpeleolSoc33:23–44. 10.HolsingerJR,CulverDC(1988)TheinvertebratecavefaunaofVirginiaanda partofeasternTennessee:zoogeographyandecology.Brimleyana14:1–162. 11.PeckSB(1989)ThecavefaunaofAlabama:partI.Theterrestrialinvertebrates (excludinginsects).BullNatlSpeleolSoc51:11–33. 12.PeckSB(1995)ThecavefaunaofAlabama:partII.Theinsects.BullNatl SpeleolSoc40:39–63. 13.CulverDC,HobbsHHIII,MylroieJE(1999)Alabama:asubterranean biodiversityhotspot.JAlaAcadSci70:97–104. 14.ElliottWR(2007)ZoogeographyandbiodiversityofMissouricavesandkarst. 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Cullowhee,NorthCarolina:WesternCarolinaUniversity.83p. 50.ReevesWK(2000)InvertebratecavernicolesoftheGreatSmokyMountains NationalPark,USA.JElishaMitchellSciSoc116:334–343. 51.ClarkeKR,WarwickRM(1998)Ataxonomicdistinctnessindexandits statisticalproperties.JApplEcol35:523–531. 52.OksanenJ,BlanchetGF,KindtR,LegendreP,O’HaraRB,etal.(2011)vegan: CommunityEcologyPackage.Rpackageversion2.0–4.Available:http://cran. r-project.org/,http://vegan.r-forge.r-project.org/.Accessed2012Apr15. 53.RDevelopmentalCoreTeam(2012)R:Alanguageandenvironmentfor statisticalcomputing.Vienna,Austria:RFoundationforStatisticalComputing. Available:http://www.r-project.org/.Accessed2012Apr15. 54.BisbyFA,RoskovYR,OrrellTM,NicolsonD,PaglinawanLE,etal.(2011) Species2000&ITISCatalogueofLife:2011AnnualChecklist.Available: http://www.catalogueoflife.org/annual-checklist/2011/.Accessed2012Apr 15.SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org16May2013|Volume8|Issue5|e64177

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55.GotelliNJ,ColwellRK(2001)Quantifyingbiodiversity:Proceduresandpitfalls inthemeasurementandcomparisonofspeciesrichness.EcolLett4:379–391. 56.ChaoA(1984)Nonparametricestimationofthenumberofclassesina population.ScandJStat11:265–270. 57.ChaoA(1987).Estimatingthepopulationsizeforcapture-recapturedatawith unequalcatchability.Biometrics43:783–791. 58.BurnhamKP,OvertonWS(1978)Estimationofthesizeofaclosedpopulation whencaptureprobabilitiesvaryamonganimals.Biometrika65:625–633. 59.SmithEP,vanBelleG(1984).Nonparametricestimationofspeciesrichness. Biometrics40:119–129. 60.WaltherBA,MooreJL(2005)Theconceptsofbias,precisionandaccuracy,and theiruseintestingtheperformanceofspeciesrichnessestimators,witha literaturereviewofestimatorperformance.Ecography28:815–829. 61.KovachWL(2007)MVSP–AMultivariateStatisticalPackageforWindows, ver.3.1.Pentraeth,Wales:KovachComputingServices. 62.CulverDC,HobbsHHIII(2002)PatternsofspeciesrichnessintheFlorida stygobiticfauna.In:MartinJB,WicksCM,SasowskyID,editors.Hydrogeology andbiologyofpost-Paleozoiccarbonateaquifers.SpecialPublication7. Charlestown,WestVirginia:KarstWatersInstitute.60–63. 63.CulverDC,ChristmanMC,ElliottWR,HobbsHHIII,ReddellJR(2003)The NorthAmericanobligatecavefauna:Regionalpatterns.BiodiversityConserv 12:441–448. 64.ChristmanMC,CulverDC(2001)Therelationshipbetweencavebiodiversity andavailablehabitat.JBiogeogr28:367–380. 65.CulverDC,SketB(2000)Hotspotsofsubterraneanbiodiversityincavesand wells.JCaveKarstStud62:11–17. 66.CardosoP(2012)Diversityandcommunityassemblypatternsofepigeanvs. troglobiontspidersintheIberianPeninsula.IntJSpeleol41:83–94. 67.DeharvengL,BedosA(2012)Diversitypatternsinthetropics.In:WhiteWB, CulverDC,editors.Encyclopediaofcaves,2ndedition.Amsterdam:Academic Press.238–250. 68.ChristmanMC,CulverDC,MaddenM,WhiteD(2005)Patternsofendemism oftheeasternNorthAmericancavefauna.JBiogeogr32:1441–1452. 69.FinstonT,JohnsonM,HumphreysW,EberhardSM,HalseSA(2007)Cryptic speciationintwowidespreadsubterraneanamphipodgenerareflectshistorical drainagepatternsinanancientlandscape.MolEcol16:355–365. 70.TronteljP,DouadyCJ,FiserC,GibertJ,GorickiS,etal.(2009)Amolecular testforcrypticdiversityingroundwater:howlargearetherangesofmacrostygobionts?FreshwaterBiol54:727–744. 71.JuanC,EmersonBC(2010)Evolutionunderground:sheddinglightonthe diversificationofsubterraneaninsects.JBiol9:17. 72.MalardF,MoutinC,CamachoAI,FerreiraD,MichelG,etal.(2009)Diversity patternsofstygobioticcrustaceansacrossmultiplespatialscalesinEurope. FreshwaterBiol54:756–776. 73.MyersN(1988)Threatenedbiotas:Hotspotsintropicalforests.The Environmentalist8:1–20. 74.MyersN,MittermeierRA,MittermeierCG,daFonescaGAB,KentJ(2000) Biodiversityhotspotsforconservationpriorities.Nature403:853–858. 75.CastellariniF,Dole-OliverMJ,MalardF,GibertJ(2007)Modelingthe distributionsofstygobiontsintheJuraMountains(easternFrance):Implications fortheprotectionofgroundwaters.DiversityDistrib13:213–224. 76.FerreiraD,MalardF,Dole-OliverMJ,GibertJ(2007)Obligategroundwater faunaofFrance:speciesrichnesspatternsandconservationimplications. BiodiversityConserv16:567–596. 77.DeharvengL,StochF,GibertJ,BedosA,GalassiD,etal.(2009)Groundwater biodiversityinEurope.FreshwaterBiol54:709–726. 78.MichelG,MalardF,DeharvengL,diLorenzoT,SketB,etal.(2009)Reserve selectionforconservinggroundwaterbiodiversity.FreshwaterBiol54:861–876. 79.OmernikJM(1987)EcoregionsoftheconterminousUnitedStates(map supplement).AnnAssocAmGeogr77:118–125.SubterraneanBiodiversityofTennessee PLOSONE|www.plosone.org17May2013|Volume8|Issue5|e64177


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Cras efficitur magna et sapien varius, luctus ullamcorper dolor convallis. Orci varius natoque penatibus et magnis dis parturient montes, nascetur ridiculus mus. Fusce sit amet justo ut erat laoreet congue sed a ante.

CHICAGO

Phasellus ornare in augue eu imperdiet. Donec malesuada sapien ante, at vehicula orci tempor molestie. Proin vitae urna elit. Pellentesque vitae nisi et diam euismod malesuada aliquet non erat.

WIKIPEDIA

Nunc fringilla dolor ut dictum placerat. Proin ac neque rutrum, consectetur ligula id, laoreet ligula. Nulla lorem massa, consectetur vitae consequat in, lobortis at dolor. Nunc sed leo odio.