Citation
Journal of cave and karst studies

Material Information

Title:
Journal of cave and karst studies
Series Title:
Journal of Cave & Karst Studies
Alternate Title:
Continues NSS bulletin (OCLC: 2087737)
Creator:
National Speleological Society
Publisher:
National Speleological Society
Publication Date:
Language:
English

Subjects

Subjects / Keywords:
Geology ( local )
Genre:
serial ( sobekcm )
Location:
United States

Notes

General Note:
65th Anniversary Special Issue
Restriction:
Open Access - Permission by Publisher
Original Version:
Vol. 69, no. 1 (2007)

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Source Institution:
University of South Florida Library
Holding Location:
University of South Florida
Rights Management:
All applicable rights reserved by the source institution and holding location.
Resource Identifier:
K26-02046 ( USFLDC DOI )
k26.2046 ( USFLDC Handle )
6752 ( karstportal - original NodeID )
0146-9517 ( ISSN )

USFLDC Membership

Aggregations:
Karst Information Portal

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Serial

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Cover and Table of Contents ( .pdf )

Sixty Five and Still Going Strong / Malcolm S. Field ( .pdf )

Cave Geology and Speleogenesis Over the Past 65 Years: Role of the National Speleological Society in Advancing the Science / Arthur N Palmer ( .pdf )

A Brief History of Karst Hydrogeology: Contributions of the NSS / William B. White ( .pdf )

Cave Archaeology and the NSS: 1941-2006 / George Crothers, P. Willey, and Patty Jo Watson ( .pdf )

Cave Mineralogy and the NSS: Past, Present, Future / Carol A. Hill and Paolo Forti ( .pdf )

The Importance of Cave Exploration to Scientific Research / Patricia Kambesis ( .pdf )

Development of the Carbonate Island Karst Model / Joan R. Mylroie and John E. Mylroie ( .pdf )

Cave Sediments and Paleoclimate / William B. White ( .pdf )

Ground-Water Residence Times in Unconfined Carbonate Aquifers / Stephen R. H. Worthington ( .pdf )

Pseudokarst in the 21st Century / William R. Halliday ( .pdf )

The Biology and Ecology of North American Cave Crickets / Kathleen H. Lavoie, Kurt L. Helf, and Thomas L Poulson ( .pdf )

Zoogeography and Biodiversity of Missouri Caves and Karst / William R. Elliott ( .pdf )

Geomicrobiology in Cave Environments: Past, Current, and Future Perspectives / Hazel A. Barton and Diana E. Northrup ( .pdf )

Subterranean Biogeography: What Have We Learned From Molecular Techniques? / Megan L. Porter ( .pdf )

Observations on the Biodiversity of Sulfidic Karst Habitats / Annette Summers Engel ( .pdf )

Risks to Cavers and Cave Workers From Exposures to Low-Level Ionizing α Radiation from 222Rn Decay in Caves Malcolm S. Field ( .pdf )

The Reflection of Karst in the online Mirror: A Survey Within Scientific Databases, 1960-2005 / Lee J Florea, Beth Fratesi, and Todd Chavez ( .pdf )


Full Text

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PSEUDOKARSTINTHE21 ST CENTURY W ILLIAM R.H ALLIDAY HawaiiSpeleologicalSurvey,6530CornwallCourt,Nashville,TN37205,w rhbna@bellsouth.net A BSTRACT : Karstisaspecifictypeofterrain(orlandscapes)withcharacteristicsu itesof well-knownsurfaceandsubsurfacedissolutionalfeatures.Thelatterre sultfrom integratedsubsurfacedrainage.Avarietyofnondissolutionalprocesse sformsterrains analogoustocertaintypesofkarst;thesearetermedpseudokarst.Before 1906,these generallywerebelievedtobekarstsomehowformedinpoorlysolublerocks .Theyshare aconsiderablerangeoffeatures,resourcesandvalueswithkarst,common ly(butnot invariably)includingcaves,andthetwoarelinkedacrossawidespectrum ofprocesses andfeatures(e.g.,betweendissolutionalandpipingcaves).Unlikekars t,integrated subsurfacedrainagemaynotbepresent.Isolatedcavesdefineneitherkar stnor pseudokarst.Multiprocessterrainsandlandscapesarenotuncommon.Bas edlargely onconclusionsofaworkingsessionofthe1997InternationalCongressofS peleology, eighttypesofpseudokarstareidentified,withnotablydifferentimplic ationsfor extraterrestrialhabitats:rheogenicpseudokarst,glacierpseudokars t,badlandsand pipingpseudokarst,permafrostpseudokarst,taluspseudokarst,crevic epseudokarst, compactionpseudokarstandconsequentpseudokarst.Someappeartoexist onMars. Speleologistsexpertintheirdifferentiationshouldserveasconsultan tstoplanetary geologists. I NTRODUCTION The65 th anniversaryoftheNationalSpeleological Societyalsoisthe65 th Anniversaryoftheuseoftheterm pseudokastinthetitleofascientificarticle(Floridia,1941). Now,studiesofpseudokarstandpseudokarsticcaves constitutesarapidlyexpandingsubdivisionofspeleology. NumerousarticlesinpublicationsoftheNationalSpeleologicalSocietyconcernpseudokarstanditscavesinlava, inandunderglaciers,inseacoasts,inbadlandsand landslidetopography,crevicecavesandterrainsinavariety ofrocks,andevenmultiprocesscaves.Inpart,thistrend hasresultedfromemphasisonpseudokarstinplanetary geology,butmanyarefascinatingintheirownright.The InternationalUnionofSpeleologynowhasafull-fledged CommissionforPseudokarstaswellasanotherCommissiononVolcanicCaves,andathirdwhichmaintains thatseeminglypseudokarsticglacierfeaturesactuallyare karstic,notpseudokarstic. H ISTORY Landformsnowgenerallyrecognizedaspseudokarstic werewrittenaboutinChinaperhaps2,300yearsago(Liu etal.,citedbyPeweetal.,1995)andatItaly’sMountEtna onlyalittlelater(Carus,T.,citedinBanti,1993).Amapof Iceland’sSurtshellirsystemwaspublishedin1759(Halliday,2004).Duringtheearly20 th Centurytheterm originatedindependentlyinseveralEuropeanlanguages, forseveraltypesoffeaturesandwidelyvaryingterrains. TheGermangeologistvonKnebel(1906)appearstohave beenthefirsttouseitinprint,identifyingcreviceterrainin Icelandwhichengulfsariveraspseudokarstic.Manyof theseearlywriterswerefarfromcentersoflearningand werenotacademics.Commonlytheiraccountswerein obscurepublications.Manywereinlanguageswhichwere notwidelyread.Locallyinventedterminologiestendedto bafflereaders,especiallythosewhichattemptedtoapply karsticconceptstophenomenawhichonlylookedkarstic. Beginningaround1927,Russianscientistspioneered thestudyofkarst-likefeaturesinpermafrostandinpoorly solublerocks.In1931and1935F.P,Savarenskijwrote aboutkarst-likephenomenainloessandclayeysediments, termingthemloesskarstandclaykarst(Savarenskij,1931, 1935[citedbyAlexanderKlimchouk,writtencomm.]).In 1947,N.A.Gvozdetskiyrecommendedqualifieduseofthe termpseudokarst,correctlypointingoutthatitsprocesses arereal,notpseudo.Abreakoutoccurredinmid-century whencentralEuropeanspeleologistsbeganpublishing English-languagesummaries,thenentirepapersinEnglish (e.g.,Kukla,1950;Kunsky,1957).Vulcanospeleology developedseparately,withinitiallydiscreteItalianand Americanrootswhichmergedasaresultofinternational symposiabeginninginthe1970s.Initialmomentumin glaciospeleologyalsohadaseparatebeginning,entirely European.InJuly1886Forelmappedanewlydiscovered 250-metercaveintheArollaGlacierat1:5000,and describedanddiscusseditayearlater(Forel,1887).In 1892,aglacialoutburstfromtheTete-RousseGlacier killedsome150Swissvillagers.TheDirectoroftheMont BlancObservatoryinvestigatedandfoundaglaciercave 175mlongleadingtoadrainedglaciallake(Anon.,1892; Vallotetal.,1892).In1895Siegerfollowedwithalengthy articleentitled KarstformerderGletscher .Itsummarizes severalearlierreportsofglaciercavesinvariouspartsof theworld(Sieger,1895).Threeyearslater,proceedingsof W.R.Halliday–Pseudokarstinthe21 st century. JournalofCaveandKarstStudies, v.69,no.1,p.103–113. JournalofCaveandKarstStudies, April2007 N 103

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asymposiumonglacialhydrologywerepublishedin SpeluncaNo.16. D EFINITION Aworkingsessionofthe1997InternationalCongress ofSpeleologyconcludedthat‘‘pseudokarstsarelandscapes withmorphologiesresemblingkarst,and/ormayhave apredominanceofsubsurfacedrainagethroughconduittypevoids,butlacktheelementoflong-termevolutionby solutionandphysicalerosion’’(KempeandHalliday, 1997).Notclearlycoveredbythisdefinition,however,are somelandscapesarisingintaluswithanactivestreamflow (e.g.,Colorado’sLostCreekCaveSystem,discussed below).Anolder,simplerdefinitionnowseemsmore desirable:karst-likemorphologyprimarilyproducedby aprocessotherthandissolution. T YPESOF P SEUDOKARST Onaglobalbasis,the1997workingsessionspecifically identified: 1)rheogenicpseudokarst(pseudokarstonlavaflows) 2)glacierpseudokarst 3)badlandandpipingpseudokarst(includingloess) 4)permafrostpseudokarst 5)taluspseudokarst(includingboulderfieldsandroofed streamcourses) Timelimitationsprecludedconsiderationoftwoother importanttypes,andathirdisidentifiedhereforthefirst time: 6)crevicepseudokarst(includinglittoralpseudokarst) 7)compactionpseudokarst 8)consequentpseudokarst Otherpseudokarstictypesexist(e.g.,towerpseudokarst,asdiscussedbyWray[1997]). R HEOGENIC P SEUDOKARST Rheogenicpseudokarstincludesthoseportionsoflava flowswhichareshapedbythepresenceofopenlavatubes (Fig.1).Itscavesandpitsincludelavatubecaves,hollow tumuli,hollowlavarises,hollowflowlobesandtongues, openverticalvolcanicconduits,treeandanimalmold caves,hollowhornitos,andaveryfewhollowdikes. Spaciousnessandnear-levelfloorsofnumerousterrestrial lavatubecavessuggestthattheymaybeamajor extraterrestrialresource(Halliday,1966).TheCommission onVolcanicCavesoftheInternationalUnionofSpeleologyhastakenaproactiveapproachtoidentificationand documentationofrheogeniccavesandpitsthroughoutthe world,andaglobalfileofmapsoflavatubecavesis fundedbyNASAandmaintainedatArizonaState University. Inthelasthalf-century,studiesoflavatubecaveshave revealedthattheyareresourcesscarcelysecondto dissolutioncaves,withmanyfeaturesincommon.Some containagreaterrangeofmineralsthandokarsticcaves andsomecontainbiotaasspecializedasthoseofkarstic cavesandmesocaverns.Whilesignificantdifferencesexist intheirhydrogeologicmechanisms,lavatubecavespose virtuallythesamediseasehazardsasdissolutioncaves.A fewcontaincaveart,habitations,fossillocalitiesandother culturalfeatures.Othersarenotablerecreationalsites includingshowcaves. Figure1.Rheogenicpseudokarst.Obliqueaerialphotoofpartiallycolla psedlavatubecave,ElMalpaisNationalMonument, NewMexico.ComparewithFigure7showingrectilinearcrevicepseudokars t. P SEUDOKARSTINTHE 21 ST CENTURY 104 N JournalofCaveandKarstStudies, April2007

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ThelongestknownlavatubecaveisHawaiiÂ’sKazumuraCavewhichhasaslopelengthof65.6km.Never morethan20mbelowthesurface,ithasaverticalextent of1,100m.Itsfloorplanbasicallyissinuous,withlocal braiding.Itisespeciallynotablefordrainedplungepools upto 20mwide.Thedeepestknownopenvertical volcanicconduitisIcelandÂ’sThrinukagigur,204mdeep. HawaiiÂ’sNaOnepitcratercontainsasmalleropenvertical volcanicconduitwhichbeginsonaledgenearthebottom ofthepitcrater.Theircombineddepthis268m.Divers havedescended122minthewater-filledverticalconduitof HawaiiÂ’sKauhakoCenter,withthebottombeyondreach oftheirlights. Othervolcanicislandswithespeciallynotablerheogenic pseudokarstandcavesincludeIceland,Honshu(Japan), JejuIsland(Korea),AzoresArchipelago,CanaryIslands, ComoroArchipelago,GalapagosArchipelago,Samoaand RapaNui(EasterIsland).Majorcontinentalsitesinclude Italy(Mt.Etna),KenyaandAustralia.Otherlocations includeSyria,Jordan,SaudiArabia,Rwanda,Chile, ArgentinaandTanzaniawhereauniquecarbonatite rheogenicpseudokarstexistsinthecraterofOlDoinyo Lenggaivolcano.IntheconterminousUnitedStates, notablerheogenicpseudokarstispresentinmostofthe stateswestoftheGreatPlains(MontanaandWyomingare exceptions;asingleopenverticalvolcanicconduitrecently wasidentifieldinNevada,andtodate,examplesofthis typeofpseudokarstinColoradoareminor). G LACIER P SEUDOKARST Glaciospeleologyisthestudyofcavesandstreams withinandbeneathglaciersandfirn(Fig.2).Fountainand Wilder(1998)haveprovidedanexcellentoverviewalbeit withminimalreferencetocaves.Currentstudiesare especiallyactiveinIceland,Greenland(especiallyof moulins),Svalbard(Spitzbergen),Siberiaandsouthern SouthAmerica.SuchstudieshavelaggedinAntarctica wheretheworldÂ’slargestglaciercaveeitherunderliesthe RossIceShelforistheintraglacialcavecontainingLake Vostok.GeothermalcavesonMountErebusarereceiving increasingstudy.U.S.GeologicSurveygeologist,Israel Russell,wasthefatherofAmericanglaciospeleology.He producedseveralnotablereportsonthe4,000km 2 (1,500mi 2 )MalaspinaGlacierinAlaska(e.g.,Russell, 1893)withspecialreferencetotheircavesandhydrogeology.AlonghiatusfollowedRussellÂ’swork,butadditional glacierpseudokarstwasfoundinAlaskaandelsewherein thenorthwesternUnitedStatesandinthepartofBritish Figure2.Glacierpseudokarst.MultipleentrancestotheParadiseIceCav esystemca.1970. W.R.Halliday JournalofCaveandKarstStudies, April2007 N 105

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ColumbiaborderingtheAlaskanpanhandle.Asidefrom thesmall,anomalouslow-elevationBigFourIceCaves (WashingtonState),themostaccessiblewason4,392meter MountRainier.Itswell-knownParadiseIceCaves originallywereinaterminallobeofitsParadiseGlacier. By1908attractivepicturesofthesecavesadornedlocal guidebooks.Also,geothermalcaveswereidentifiedin cratersofseveralnorthwesternvolcanoes.Thelargestwere atopMountRainier.OnOregon’sMountHood,gas emissionsinsuchacavearelethalatleastintermittently (Anonymous,undated,reprinted,1994a).Geothermal cavesofMountBakerwerefoundandstudiedmuchlater. Inthe1940s,theParadiseIceCavesatthesnoutofthe ParadiseGlacierdisappearedastheirlobeshriveledand vanished.Afewyearslater,similarcaveswerefoundinthe nearbyStevensGlacier.Throughthe1950sand1960sthey graduallyenlargedandthenameParadiseIceCaveswas transferredtothem.AlsoonMountRainier,anoutburst floodfromapreviouslyunknowncaveintheKautz Glaciercausedconsiderabledamage,butdecadespassed beforethefloodandthenew-foundcavewerecorrelated. MuchthesamehappenedonOregon’sMountHoodin 1921(Anonymous,undated,reprinted1994b). Theyear1968markedthebeginningofashortgolden eraofAmericanglaciospeleologycenteredintheAlaskaBritishColumbiaicefields(e.g.,MacKenzieandPeterson, 1968)andonthenewParadiseIceCaves(e.g.,Andersonet al.,1994).Inthelatter,Andersonandco-workersfound andmappedatotalofalmost25kmofephemeral passages.Thesepassagesappeared,enlargedintospacious rooms,collapsedanddisappearedasthisglacierlobealso shriveled,expanded,shrivelledagainandfinallydisappeared.Maximumlengthatanygiventimewas13.25km (Andersonetal.,1994).Icespeleothemsandglareiceand firninclusionsintheglacierwereespeciallynotable features.Partofthesystemreappearedbrieflyinfirnin themid-1990s. In1970,climbers,caversandgeologistsbecameinterestedingeothermalablationcavesinthesummitcraters ofMountRainier.EugeneKiverandco-workersmapped 1.8kmofpassagesintheeastcraterand305minthe smallerwestcrater.Itcontainedasmalllakeatanaltitude of4,329m.Evaluatingmudflowhazards,Lokey(1973) spent42consecutivedaysinthesecratersandtheircaves. Studiesofsimilar,comparativelyaccessiblecavesinthe craterofMountBakerwereunderwaywhenMountSt. Helenseruptedin1980.Theimpactoftheeruption refocusedallnorthwesternspeleologicalactivity,andno furtherworkhasbeendoneintheMountBakergeothermalcaves. B ADLANDSAND P IPING P SEUDOKARST Pipingisthehorizontal,gradedorverticalgrain-bygrainremovalofparticlesbychannelizedground-water flowinagranularmaterialandinsomepoorlysoluble rocks(Fig.3).ParkerandHiggins(1990)andDunne (1990,p.1–28)presentdifferentmind-setsanddifferent vocabulariesinthesamevolume.Itlongwasrecognized primarilyasacauseofseriousengineeringproblems.In recentyears,extensivepipingcaveshavebecomerecognizedasimportantindividualfeatures.Pipingwasfirst recognizedinloessandloess-likesiltinChina,butnatural cavesarenotcharacteristicofloesstopography. Thepureformofpipingisthepseudokarstextremeof aspeleogeneticspectrumwith100%karsticdissolutionat theother.Betweentheseextremesisanintermediate interfaceinimpurecarbonatesandevaporiterocksand limysandstonesandotherpoorlysolublerocks.Pipingalso participatesindevelopmentoflargemultiprocesscavesin sometropicalquartzitesandindevelopmentofcompaction pseudokarst(seebelow). Somebadlandstopographyisriddledwithpipes,piping caves,funnel-shapedsinks,dryvalleysandotherfeatures ofcentripetalsubsurfacedrainagecommonlyobservedon karsticterrains.Locallytheseformspecificlandscapes. Manyoftheirindividualfeaturesareshort-lived;somelast onlyfromonestormtothenext.Theoveralllandscape, however,tendstopersistthroughlongperiodsofscarp Figure3.GigglersCaves,Kenya,apipingcaveinhard granulartuff. P SEUDOKARSTINTHE 21 ST CENTURY 106 N JournalofCaveandKarstStudies, April2007

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retreat.BadlandsNationalPark(SouthDakota)isthe Americantypelocality,andPetrifiedForestNationalPark alsocontainsnotableexamples.InOregonÂ’sJohnDay Country,345-meterOfficersCave(Fig.4)wasdescribedas anisolatedgeologicalcuriosityin1964(Parker,1964).A fewyearslater,TexasandCaliforniaspeleologistsbegan describingincreasinglylarge,complexpipingcavesin avarietyofpoorlyconsolidateddrylands.Beginningwith AnvilPointsClaystoneCavein2001,Davisunleashed aseemingfloodofreportsonexamplesindrylandsin westernColorado(e.g.,Davis,2001).Pipesalsoare commoninboglands,withslutchcavesupto50mlong reportedinEngland.ThelongestrecordedAmerican pipingcaveis804mChristmasCanyonCave,formedin athinlayerofunconsolidatedvolcanicashbetween asurficialbasaltlayerandamudflowdeposit.Itserves asaseasonalresurgenceformuchoftheCaveBasaltlava flowonthesouthsideofMountSt.Helens,Washington (Halliday,2004). Inmoreconsolidatedrocks,pipingformscomplex cavesinsandstonesinMinnesotaandArkansas,and participatesinformationofothersinhardgranulartuff andinpartiallysolublelakebeddepositsinKenya.The latterincludeKitumCave,formerlybelievedtohavebeen excavatedbyelephantsseekingsalt.Perhapsthelongest pipingcaveonrecordis8kmBohemiaCaveinNew Zealand,saidtohavebeenformedlargelybyground-water erosioninphyllitesunderlyingmarble. P ERMAFROST P SEUDOKARST Roughly10%oftheearthÂ’ssurfaceisunderlainby permafrost.Inareaswhereitiscoveredbytundraortaiga, acombinationofthawingandpipingproducescurvilinear thawponds,steep-walleddepressions,funnel-shapedpits, ponors,dryvalleys,smallcavesandotherkarst-like features.Thesearelargelyofinterestasengineering problems,butRussianandsomeothergeologistshave discussedthemspecificallyasimportantpseudokarst features.Somewhatsimilarfeaturesarepresentwhere residualsoilofmeltingglacierstakestheplaceoftundraor taiga.InEurope,thetermthermokarsthasbeenappliedto permafrostpseudokarst,butthereisnothingdissolutional intheprocesseswhichformanyofit.MarjorieSweeting isamongthosewhohavedecriedthisunfortunateterm, pointingoutitsconfusingsimilaritytothermalkarst. T ALUS P SEUDOKARST Taluscavesarereceivingincreasingattentioninthe worldspeleologicliterature,buttaluspseudokarstisrarely mentioned.Nevertheless,talusaccumulationsoccasionally formimportantlandscapesandAmericanspeleologists tendtounderestimatetheoccurrenceandsignificanceof taluscavesperse(Fig.5).InsomepartsofEurope,they arethelargestandcommonesttypeofcave.Sjoberg (1989a)foundthat15%ofSwedishtaluscaveshavehigh scientificand/orrecreationalvalues;SwedenÂ’sBodagrottornahasmorethan2,500mofpassage.Intemperate Figure4.SmallroominOfficerÂ’sCave,Oregon,apipingcaveinapyroclast iclandslide.Inmoreconsolidatedrockwithless frequentrockfall,pipingcavesmayprovideextraterrestrialshelter. W.R.Halliday JournalofCaveandKarstStudies, April2007 N 107

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climatessuchcavesmayserveasimportantglacieresor provideothermicroclimatesfavorabletospecializedlife forms.Inaridregions,someminimizeevaporationof runningorpondedwater.Especiallyingraniteand anorthosite,someprovidedelightfulrecreationalcaving. Afewhavebeendevelopedasshowcaves.InSouthern Californiaandprobablyelsewhere,sometaluscavesserved ashumanhabitationswellintothe20 th Century. IntheUnitedStates,taluscavesexistalmostexclusively inoneoftwosettings:hillsideorcliff-bottomrockpile fieldswhichformtaluspseudokarst,andsteep-walled streamgullies.Sjoberg(1989b)alsodescribedneotectonic bouldercavesinSweden.Someoftheseareendproducts ofrochesmoutonnees,smoothedandroundedbyglacial erosion,thenfracturedbytectonicactivityafterdeglaciation.Thiscombinationofprocesseshaspreservedthe overallcontouroftherochemoutonnee,andproduced alocalizedtaluspseudokarst. Rockpileandrockslidetaluscavescharacteristicallyare slopefailurefeaturesfoundespeciallyinboulderfieldsat thebasesofcliffs,onslopesorinnarrowstreamgorges,or, rarely,innarrowgrabens.Avarietyofprocessesis involved:blockglide,grusificationofgranite,andothers. Somerepresentastageofdisintegrationofcrevicecaves affectedbydifferingratesofdownslopemovement.In CaliforniaandinpartsofthenortheasternUnitedStates, thosepartiallyfillingnarrow,steep-walledgranitegorges arelocallytermed,purgatorycaves.Someoftheseare activemultiprocesscaves,withactivevadosesolution, grusification,pipingandscouringoftalusandbedrock alike.ThealpineLostCreeksystemofColoradohas formedadistinctivenarrowdendriticpseudokarst5km long,withlargepseudokarsticwindows,flat-stacked bouldersandridgesofpartiallygrusifiedgraniteupto 60mhigh.Here,LostCreekrepeatedlydisappearsinto swalletcaves,reappearingtoflowacrossflat-bottomed sinkholes(Hose,1996).Enormousquantitiesofgranitic sanddebrishavebeenclearedfromcavesandsinkholesin thisunusualsystem.Smallerexampleshavebeendescribed inEurope. MalinandEdgett(2000)havereportedseveralMartian featuresresemblingcertainterrestrialtaluspseudokarst. Someareimmediatelydownslopefrompresumedoutbursts ofwater.ThesearepotentialMartianglaciers.Othersmay serveassmallhabitationsites. C REVICE P SEUDOKARST Thefirstidentificationofaterrainaspseudokarst describedacrevicepseudokarstinIceland(vonKnebel, 1906).Wherekarstandkarsticcavesarereadily accessible,however,allbutthemostspectacularcrevice cavesandcrevicepseudokarst(e.g.,FingalÂ’sCave,Island ofStaffa,Scotland)arecommonlyignored.Consequently theyaremuchmorecommonthanisgenerallyrecognized.Theyoccurinbothlittoralandinlandterrains;the formerincludeslittoralzonesofnow-dryinlandPleistocenelakes.Littoralexamplesareformedbyhydraulic wedgingbywavesandotherformsofmarineerosion. Thesemayformfracturesextendinghundredsofmeters inland,readilytraceableonthesurface(Fig.6).Especiallywheresinkholesdevelopalongsuchfractures,small butinterestingpseudokarsticlandscapesmaybeidentified.ExamplesincludetheislandofStaffa,Scotland,the BallybunioncoastalareaofIreland,sectionsofthe OregoncoastincludingtheDevilÂ’sPunchbowlandthe areaofSunsetCliffs,SanDiegoCounty,California. Becauseoftheiroriginandgeometry,fewsuchcavesare inhabitable. Inlandcrevicecavesvarygreatlyinsize.Afewhave extraordinaryparameters,suchasDevilÂ’sHoleinthesmall NevadasectionofDeathValleyNationalPark.Thesmall near-surfacesectionofthisfeatureiscomplexandkarstic, butmostofitconsistsofasinglespaciouscrevicein Figure5.TaluspseudokarstatPottstown,Pennsylvania. Becausethegeneralpublicismoreinterestedintaluscaves thanarespeleologists,oldpostcardsareausefulresourcein identifyingthem. P SEUDOKARSTINTHE 21 ST CENTURY 108 N JournalofCaveandKarstStudies, April2007

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limestoneoccupiedbywarmgroundwaterapparently muchmorethan100mdeep(theNationalParkService prohibitscavedivinghere).Itapparentlyformedasaresult ofstructuraltensionintheGreatBasinanditswaterispart ofamajorregionalaquifer(Riggsetal.,2000). Smallerinlandcrevicecavesvaryfromisolatedcracks incliffstonarrowrectilinearnetworksonslopes.Many ofthelatterareanintermediatestageofbreakupof competentrockmassesduetomassmovementorgravityslidingenhancedbylocalsubsurfacedrainage.Wherethe movementisnotuniformacrossthelengthofsuchacrevice, bedrockblocksslideandrotateatdifferentspeedsandin differentdirections,convertingpartorallofcrevicecaves intooneormoretaluscaves.Basaltandgranitecommonly developcurvilinearcrevicecavesratherthanrectilinear forms.Somedeepcavesintropicalquartzitearecrevice caves,butothersaremultiprocesscavesextensivelymodified bypiping.CreviceterrainsinArizonaappeartobeofone oftwotypes.SomeinnorthernArizonaarebelievedtobe theproductofsubsidencecausedbydeeplyburiedkarst. Othersinareasofespeciallydeepalluviumappeartobethe resultofexcessivedrawdownofgroundwater(Harrisand Allison,2006).Tectonicandsolutionalcavesoccuralongthe former. MostoftheislandofHawaiilackssurfacedrainageas aresultofcrevicepseudokarstformedasaresultof fracturesinbrittlebasaltssecondarytovariousvolcanic andseismicevents.Mostofthesecrevicesareconcealedby vegetationorbyvolcanicash,orbysubsequentlavaflows. ButtheGreatCrackinthesouthwestriftzoneofKilauea volcanoisakilometer-widezoneofenecheloncrevicesof variouswidthsanddepths,locallyopentothesurface (Figs.7and8).Animplausibleconceptofitsoriginisthat theweightofKilaueavolcanoistiltingthatpartofthe islandofHawaiiawayfromMaunaLoavolcano,andthat Kilaueavolcanoultimatelywillslideortoppleintothe PacificOcean.Moreplausibleisthepossibilitythatthisis aself-propagatingcrevice,enlargedandelongatedby injectionofpressurizedmagmaintoinitiallysmallfractures inthewallofHalemaumaucrater.Withinit,mapping teamshavereachedadepthof183m.Atseverallevels,one ormorelateralcoatingsorlavareveallateralflowoflava atdepth.TheGreatRiftofsouthcentralIdahoisanother verylargeinlandcreviceinabasaltflowfield(Fig.9).At leastoneeruptivefractureonMountEtna(Italy)extends downslopeintheformofalavatubecave(Giudiceand Scalia,1994). Unlessblockglidehasbeenactive,crevicecaves characteristicallytaperdownward.Localizedfloorsgenerallyareformedbywedgedbreakdownblocks.Thus extraterrestrialcrevicecavesareunlikelytobesuitable habitationsites. C OMPACTION P SEUDOKARST Compactioniscommoninlandslideandavalanche deposits.Thisfacilitatespiping(seeabove).Pseudokarst maybeformedbysuchcompaction,andisdiscussedhere forthefirsttime.Initially,drainageofsuchdepositstends tobeinternalandtheirsurfacesmaybepittedwithlarge andsmallpunchedoutorconicalcrater-likedepressions (Fig.10).Anotableexampleformedinunconsolidated materialatthenorthernbaseofMountSt.Helens (WashingtonState)onMay18,1980.Here,virtuallythe entirenorthernsideofthevolcanoavalanchedmoments Figure6.Littoralcrevicepseudokarst,islandofStaffa,Scotland.Ther ighthandopeningistheentrancetoFingalÂ’sCave. W.R.Halliday JournalofCaveandKarstStudies, April2007 N 109

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Figure7.Crevicepseudokarstina2kmsegmentoftheSouthwestRiftZoneof KilaueaVolcano,Hawaii.Individualpits alongtheGreatRiftareletteredfromnorthtosouth;PitHisnearthecente rofthephoto.Ithasbeenmappedtoadepthof 186m.Notethatsmallerenecheloncrevicesaremostlyhiddenbyvegetatio n. P SEUDOKARSTINTHE 21 ST CENTURY 110 N JournalofCaveandKarstStudies, April2007

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beforealateralash-clouderuptioncovereditsslumpwith severalmetersofslightlycohesivevolcanicsand.The avalanchelayercontainedlargeandsmallfragmentsof fracturedglaciereaswellasshatteredblocksofbedrock. Someweretransportedlaterallyforseveralkilometersin theiroriginaluprightposition.Allwasheated,butthe degreeofhydrothermalinjectionvaried.Almostatonce, meltingandcompactionbegantogeneratecrateriformand punched-outdepressionsvaryingwidelyinsize. Theoverlyingashclouddepositunderwentrapid erosion,withformation,enlargementandheadwarderosion ofnewgulliesfollowedbycoalescenceofcloseddepressions andpondformation.Duringthefirstfewmonths,vertical pipingwasprominentlocally.Asgulliesenlarged,deepened andpiratedtheirneighbors,parallelcrevicesformedinthe pyroclasticashcloudsand,elongatingup-slope.Somewere partiallyroofedbyblockslumping,andpipingdeveloped alongtheirbases.Moreextensiveroofingformedafew short-livedpyroclasticcaves. A1mlayerofquicksandatoponetemporarypond supportedtheweightofinvestigators,butdidnot withstandtheimpactoflargerockswhichsometimes brokelooseandrolleddownthesteepslopeoftheclosed depression.Theresultingorificerevealedmuddywaterin alowcavernroofedbythequicksandlayer. Overall,thispseudokarstevolvedrapidly.Witheach seasonalrain,thesurfaceofthepondsrosedisproportionatelyastheashclouddepositwashedintothem.Surface drainagedeveloped,andallbutthelargestdepressions disappearedwithin15years.After25yearstheareastill couldberecognizedaspseudokarstic. InsouthernNevadaandadjacentUtah,severalsmall cavesandpitshavebeenidentifiedinalluviumincluding AlluviumCave.Some,butnotall,aretheresultofpiping. C ONSEQUENT P SEUDOKARST Consequentpseudokarstiskarst-liketerrainsresulting fromactionofnaturalprocessesonshallowmines, undergroundquarriesandothersubsurfaceworksof man.AlthoughtheU.S.GeologicalSurveyhasstudied manysuchoccurrences,thetermandtheunifyingconcept weredevelopedlateinthe20 th CenturybyIstvanEszterhas ofHungary.Someoftheaffectedareascontainextensive cavernsformedbynaturalstoping,boundedonallsidesby talusorbyfracturesurfaces.Theirsurfacefeaturestendto berectilinear,andtheycommonlycauseseriousengineeringproblems.Undergrounddrainageisminimalorabsent. T HE F UTUREOF P SEUDOKARST Despite20 th Centuryprogressinthisrapidlyemerging field,documentationandstudyofpseudokarstinevitably haslaggedbehindthoseofkarst.Applicationofhardlearnedcalcareospeleologicalexplorationtechniquesto somevolcanicpseudokarst,however,hasshownthatmany long-establishedtechniquesareeasilymodifiedtomeetnew conditionsasneeded(e.g.,hyperthermal,hypothermal, hypoxic,andhypercarbiccaves). IfthisistobemanÂ’scenturyofbreakoutintospace, speleologistseverywhereneedtostayalerttothegreat volumeofrelevantdatanowpouringbackfromMarsand beyond,andtovolunteerourassistanceintheinterpretationofdataalreadyseentodemonstrateconfusinglyvaried terrains.Thisisanareaofprogressivelynarrowspecializationandwecannotexpectplanetarygeologists,oreven terrestrialgeologistslackinginexperiencewithvarious typesofterrestrialpseudokarst,torecognizeandproperly utilizetheirextraterrestrialanalogues.AlreadyonMars, whatappearstobeatypicalcrevicecavehasbeen identifiedasapotentiallyhabitablelavatube.Plansrelying heavilyonsuchmisidentificationsopenthewaytodisaster. Perhapsthefirststepshouldbebreakingdownthe languagebarrierwhichstillhindersdefinitivecommunicationbetweencentralEuropeanpseudokarstspecialistsand thoseoftherestoftheworld.Ifnecessary,traveltoaseries ofinternationalmeetingsonpseudokarstshouldbe subsidized.TheNationalSpeleologicalSocietyandthe Figure8.AshortsegmentoftheGreatRift,Idaho,seen fromalargeskylight.Theflatisanartificialpathway constructedtopermitvisitoraccess. W.R.Halliday JournalofCaveandKarstStudies, April2007 N 111

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Figure9.Landingcreatedbywedgingofrockfall,theGreatCrack,Hawaii. Terrestrialcavesofthistypeareunsuitablefor humanhabitation. Figure10.Subsidencepseudokarst.ThisconicaldepressionintheSpirit Lakepseudokarst(MountSt.Helens,Washington State)wasphotographedinanearlystageofitsevolution.Athinash-clou dtephradepositisstillpresentontheflatsformedon topofthelandslidedepositcontainingthesinkhole. P SEUDOKARSTINTHE 21 ST CENTURY 112 N JournalofCaveandKarstStudies, April2007

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InternationalUnionofSpeleologyshouldtaketheleadin suchendeavors.Thesurvivalofmaninspacemaydepend onit. A CKNOWLEDGEMENTS TheauthorwouldliketothankJanPaulvanderPasfor theobliquephotographthatappearsinFigure6andChris Okuboforthe1988NASAphotographthatappearsin Figure7. R EFERENCES Anonymous,1892,(untitled),Nature,v.46,no.1192,p.420. Anonymous,undated1994a(reprinted),Deadlyfurmarolesalways intriguing:BulletinoftheInternationalGlaciospeleologicalSurvey, v.6,p.30–31. Anonymous,undated,1994b(reprinted),PioneerswitnessedHood’s volcanicfire:BulletinoftheInternationalGlaciospeleologicalSurve y, v.6,p.31–32. Anderson,C.H.,Vining,M.R.,andNichols,C.M.,1994,Evolutionof theParadise/StevensGlacierIceCaves:BulletinoftheNational SpeleologicalSociety,v.56,no.2,p.70–81. Banti,M.,ed.,1993,ProceedingsoftheInternationalSymposiumonthe ProtohistoryofSpeleology,CittadiCaseello(Italy),Prhomes. Davis,D.,2001,AnvilPointsClaystoneCaveComplex:Anexceptionally large‘‘mudcave’’system:NationalSpeleologicalSocietyNews,v.59, no.11,p.331–334. Dunne,T.,1990,Hydrology,mechanicsandgeomorphologicalimplicationsoferosionbysubsurfaceflow, in Groundwatergeomorphology: Theroleofsurfacewaterinearth-surfaceprocessesandlandforms, Higgins,C.G.,andCoats,D.R.,eds.,GeologicalSocietyofAmerica SpecialPublication252. Floridia,G.,1941,Unparticolarefenomenopseudocarsicomanifestatod a alguneargile:BolletinodellaSocietaeiScienciaNaturaleed EconomichediPalermo,v.23,p.10–19. Forel,F.A.,1887,EtudesGlaciares:II,LagrottenaturaleduGlacier d’Arolla:ArchivesdesSciencesPhysiquesetNaturale(Geneva), TroisiemePeriode,tomexvii,no.5,p.469–504. Fountain,A.,andWilder,J.,1998,Waterflowthroughtemperateglaciers : ReviewsofGeophysics,v.36,no.3,p.294. Guidice,G.,andScalia,N.,1994,LafratturaeruttivadiProfundo-Nero: BolletinodellaAccademiaGioenidiScienzeNaturali,v.27,no.348, p.161–171. Halliday,W.R.,1966,Terrestrialpseudokarstandthelunartopography: BulletinoftheNationalSpeleologicalSociety,v.28,p.167–170. Halliday,W.R.,2004,Pseudokarst, in Encyclopediaofcavesandkarst science,Gunn,J.,ed.,London,G.B.,FitzroyDearborn(animprintof Taylor&FrancisBooks,Inc.),p.604–608. Harris,R.,andAllison,M.L.,2006,Hazardouscracksrunningthrough Arizona:Geotimes,p.24–27. Hose,L.,1996,TheLostParkReservoirProject,ParkCounty,Colorado, in Kolstad,R.,ed.,ThecavesandkarstofColorado:1996National SpeleologicalSocietyConventionGuidebook. Kempe,S.,andHalliday,W.R.,1997,Reportonthediscussionon pseudokarast, in Proceedingsofthe12 th InternationalCongressof Speleology,v.6,Basel,Switzerland,Speleoprojects. Kukla,J.,1950,PseudokrasovejeskyneuLotunoSokolovsku, CeskoslovenskyKras,v.3,p.274–278. Kunsky,J.,1957,TypesofpseudokarstphenomenainCzechoslovakia, CeskoslovenskyKras,v.10,no.3,p.111–125. Lee,F.T.,andAbel,J.F.,1983,Subsidencefromundergroundmining: Environmentalanalysisandplanningconsiderations,U.S.Geological SurveyCircular876. Lokey,W.M.,1973,Craterstudiesonasleepingvolcano:Explorers Journal,v.51,no.3,p.167–170. Malin,M.,andEdgett,K.,2000,Evidenceforrecentgroundwaterseepage andsurfacerunoffonMars:Science,v.288,p.2,330–2,335. McKenzie,G.D.,andPeterson,D.W.,1968,Observationsofaglacier caveinGlacierBayNationalMonument,Alaska:Bulletinofthe NationalSpeleologicalSociety,v.30,no.3,p.47–54. Parker,G.,1964,OfficersCave,apseudokarsticfeatureinalteredtuffa nd volcanicashintheJohnDayformationineasternOregon:Geological SocietyofAmericaBulletin,v.75,p.393–401. Parker,G.,andHiggins,C.,1990,Pipingandpseudokarstindrylands, in Higgins,C.G.,andCoates,D.R.,eds.,Groundwatergeomorphology: Theroleofsubsurfacewaterinearth-surfaceprocessesandlandforms: GeologicalSocietyofAmericaSpecialPaper252. Pewe,T.,Liu,T.,Slatt,R.M.,andLi,B.,1995,Originandcharacteristic s ofloess-likesiltinthesouthernQinghai-Xizang(Tibet)Province, China:U.S.GeologicalSurveyProfessionalPaper1549. Riggs,A.C.,Winograd,I.J.,Carr,W.J.,Kolesar,P.T.,andHoffman,R.J. 2000,Devil’sHole,atectoniccaveinsouthernNevadawith acontinuous0.5million-year-longpaleoclimaterecord, in Levich, R.A.,Linden,R.M.,Patterson,R.L.,andStuckless,J.S.,eds., HydrologicandgeologiccharacteristicsoftheYuccaMountainsite relevanttotheperformanceofapotentialrepository:Geological SocietyofAmericaFieldGuide2,p.387–392. Russell,I.C.,1893,MalaspinaGlacier:JournalofGeology,v.l,no.1, p.11–37. Sieger,R.,1895,Karstformerdergletscher:HellnersGeographische Zeitschrift,v.1,p.182–204. Sjoberg,R.,1989a,CavesasindicatorsofneoteconicsinSweden, in Proceedings,2 nd SymposiumonPseudokarst,Janovickynear Broumova,1985,Prague,CzechSpeleologicalSociety. Sjoberg,R.,1989b,AninventoryofcavesinthecountyofVesternorrland, northernSweden, in Proceedings,2 nd SymposiumPseudokarst, JanovickynearBroumova,1985,Prague,CzechSpeleologicalSociety. Vallot,M.J.,Delebecque,A.,andDuParc,L.,1892,Lacatastrophedu Saint-Gervais12Juillet1892:ArchivesdesSciencesPhysiqueset Naturales,Geneva,TroisiemePeriode,v.28,p.179–201. vonKnebel,W.,1906,HohlenkundemitBerucksichtigungderKarstphanomene,Braunschweig,Germany,DruckundVerlagvonFreidrich ViewegundSohn,p.183. Wray,R.A.L.,1997,Aglobalreviewofsolutionalweatheringformson quartzsandstones:EarthScienceReview,v.47,p.137–160. W.R.Halliday JournalofCaveandKarstStudies, April2007 N 113



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THEBIOLOGYANDECOLOGYOFNORTHAMERICAN CAVECRICKETS K ATHLEEN H.L AVOIE 1 ,K URT L.H ELF 2 AND T HOMAS L.P OULSON 3 Abstract Caveandcamelcricketsarewidelydistributedincavesthroughoutthewor ld, andinNorthAmericatheymakeupthebulkofthebiomassinmanycaves.Mostc aves donothavelargepopulationsofbats,sotheguano,eggs,andcarcassesoft hese cavernicolouscricketsaredependablesourcesoffixedenergyfortroglo bites(Mohrand Poulson,1966;Barr,1967;BarrandKuehne,1971;Richards,1971;Harris, 1973).The cricketsoftenareatruekeystonespecies,maintainingcricketguanocom munitiesand specializedeggpredators,aswellasprovidingmoredispersedenergyinp utsthatincrease overallecosystemdiversity.Theyareallcommonlyreferredtoascricket s,andareallin thesameOrder(Orthopterans)withgrasshoppers,crickets,andkatydids .Mostcave cricketsactuallyaregrasshoppers.CavecricketsinHawaiiaretruecric kets(Gryllids). Becausecavecricketsarerelativelylargeandabundant,theyhavereceiv edmorestudyas agroupthanmostothercavernicolousinvertebrates,buttherearestilla lotofthingswe don’tknowaboutcavecricketsandsomecontinuingmysteries. C LASSIFICATION A ND G ENETICS Earlyresearcherswerefascinatedbythebizarrelife formsfrequentlyencounteredincaves,andspentalotof effortlookingforconfirmationoftheirevolutionaryideas. Inhis1888 TheCaveFaunaofNorthAmerica ,Packardwas surprisedtofindthatcavecricketscollectedfromdeep insideacaveshowedthesameeyemorphologyasthose collectednearanentrance.Heinvokedacomplicated explanationofaccelerationandretardationtoexplain differencesinovipositorlengthinsteadofattributing differencestoarangeofsizesandagesincrickets. Cavernicolousmembersofthetribe Ceuthophilini are widelydistributedthroughouttheUnitedStatesandinto Mexico,whilecavernicolousmembersofthetribe Hadenoecini arerestrictedtotheAmericansoutheast.The taxonomicrelationsandgeographicaldistributionsofthe tribe Ceuthophilini havebeenreportedbyHubbell(1936) andtribe Hadenoecini byHubbellandNorton(1978).In Mayof2006,NorthernArizonaUniversityannouncedthe discoveryofanewgenusofcavecricketandtwonew speciesofcavernicolous Ceuthophilus .Thesenewcrickets werefoundaspartofasurveyof24cavesinthe GrandCanyon-ParashantNationalMonumentinArizona (www.onlinepressroom.net/nau/). Rhaphidiphoridsarewingless,withlongantennae. Theyhaverobusthindlegsforjumping,andaresometimes calledcamelcricketsbecausethebackishumpedupwith theheadbentdown.Bothmalesandfemaleshavetwocerci attheendoftheabdomenthatarerichinsensory receptors.Adultfemalecricketshaveanovipositor betweenthetwosensorycerci.Cavernicolouscrickets showarangeofadaptations(troglomorphy)tothecave environment.Somespecies,suchas Ceuthophilusstygius camelcricketsinKentucky,usethecaveonlyasarefuge duringtheday.Theyforageandlayeggsoutsideinthe forest.Theyoungcricketshatch,andmanyover-winter justinsidecaveentrances.Theyareclearlytrogloxenes. Hadenoecussubterraneus cavecricketsinMammothCave and Ceuthophilusconicaudus inCarlsbadCavernleavethe caveonlytofeed,andallotheraspectsoftheirlifecycle occurincaves,sotheyarehabitualtrogloxenesor troglophiles.Somespecies,suchas Caconemobiusvarius foundinthelavatubeKaumanaCaveinHawaii,feedand reproduceincaveswithouteverleaving,andaretrue troglobites. InCarlsbadCaverntherearethreedifferentspeciesof Ceuthophilus cricketsthatrepresentarangeoftroglomorphicadaptations(Fig.1).Theleastcave-adapted speciesistherobust C.carlsbadensis thatiscommonin areaswithbatguano.Themostcaveadaptedspecies, C. longipes ,livesinremoteareasofCarlsbadwherefoodis verylimited.Theintermediatespecies, C.conicaudus ,is widelydistributedinsmallercavesthroughoutthePark. Averyinterestinganddiversegroupoftruegryllid cricketsliveinlava-tubecavesoftheHawaiianarchipelago (Fig.2).Howarth(personalcommunication)statesthat therearemoredifferentkindsofcavecricketsinHawaii thaninallofcontinentalNorthAmerica.Thereareatleast two Caeconemobius speciesthatliveinKaumanaCaveon thebigislandofHawaiiandanotherspeciesinsmall interstitialspacesonthelavaflow.Boththecavecrickets andthelavaflowcricketarepresumablyevolvedfrom alarge,dark,eyedspeciesthatlivesinthewave-splashzone ofrockybeaches.Thelavaflowcricketretainsitseyesand showsaslightreductioninpigmentationandagreat 3 318MarlberryCircle,Jupiter,FL33458-2850tomandliz@bellsouth.net 2 DivisionofScienceandResourceManagement,MammothCaveNationalPark, MammothCave,KY422259kurt_helf@nps.gov 1 StateUniversityofNewYorkCollegeatPlattsburgh,101BroadSt.,Platts burgh, NY12901lavoiekh@plattsburgh.edu KathleenHLavoie,KurtLHelf,andThomasLPoulson–Thebiologyandecolog yofNorthAmericancavecrickets. JournalofCave andKarstStudies, v.69,no.1,p.114–134. 114 N JournalofCaveandKarstStudies, April2007

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reductioninsize.Thehighly-caveadaptedspeciesisvery small,blind,andhaslostnearlyallofitspigment.Whatis particularlynoteworthyisthatthisdivergencefrom acommonancestormusthavehappenedbetween700,000 and1,000,000yearsago,whichisthemaximumageofthe bigislandofHawaii(Howarth,1983,1987;Otte,1994). Thegeneticsofninespeciesofcavecricketsfromsitesin PennsylvaniathroughAlabamawereanalyzedbyCaccone andSbordoni(1987)andCacconeandPowell(1987).The resultsshowthatpopulationsofcavecricketsinareas wherethelimestoneiscontinuous,buthighlyfractured,are geneticallymorevariablethanpopulationsfromregions wherethelimestonedistributionismoredisjointed.This patternsuggeststhatcricketmovementbetweenpopulationsthroughsubsurfaceconduitsisimportantinmaintaininggeneticvariability.Alackofgeneticdifferentiation amongpopulationsofthetrogloxeniccamelcricket, Ceuthophilusgracilipes ,wasreportedbyCockleyetal. (1977)overa1,000km 2 (386mi 2 )areaintheeastern UnitedStates.Thisspeciesisfoundincavesandinthe forestunderlogsandloosebark.Theirfindingssuggest thattheforestpopulationsmayserveasageneticbridge amongcavepopulations. Genomesizeisanimportanttaxonomicfactorbecause itinfluencescellsizeandhowlongittakesacelltodivide. Genomesizeinorthopteransaverages8.2pg 6 0.5for haploidDNA.Thesmallestknownorthopterangenome sizeis1.55pgin H.subterraneus (Gregory,2001). L IFE H ISTORY Thelifehistoryof Hadenoecussubterraneus beginswhen afemalecricketinsertsherovipositorintosandysoil,and insertsaneggbelowthesurface.Theegg,aboutthesize andshapeofagrainoflongrice,staysburiedforabout Figure1.ComparisonofthethreeCarlsbad Ceuthophilus crickets,lefttoright, C.carlsbadensis,C.conicaudus ,and C.longipes .Adultmales. Figure2.Undescribedundergroundtreecricket( Thaumatogryllussp )fromcavesonMaui.Adultfemale. K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 115

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12weeksbeforethenymphhatches.Thenymphisnot completelydeveloped;ithasyolkwhereitsdigestivetract willbe,butthelongertheeggstaysinthesand,themore likelyitwillbeeatenbyaspecializedeggpredator,thesand beetle Neaphaenopstellkampfii .Onceithatches,thenymph worksitswayoutofthesoilandmovestothewallsand ceilingofthepassagewhereithaslesschanceofbeing eaten.Cricketsatthisstagecompletelylackpigment,and arecalledwhities. Manymeasuresofcricketsizehavebeenusedbyfield biologists,includingheadwidthandleglengths.For Hadenoecussubterraneus ,wehavereliablymeasuredthe lengthofthedrumstick(i.e.,thefemurofthehindmost pairoflegs,orHindFemurLength[HFL]).Whitieshave HFLofslightlylessthan5mm.Ascricketsmolttheygo throughmanystagesorinstars.Theyfirstbeginto developsecondarysexualcharacteristicsataround 10mmHFLandreachaganglyteen-agestageataround 15mmHFLandaregrayish-brownincolor.Theymake theirfinalmolttoadultsatHFLusuallygreaterthan 20mmHFL.Werarely(0.5–3.8%)findasexuallymature adultcavecricketwithaHFLlessthan20mm.Most adultshaveaHFLofaround23mm;wehavenever measureda Hadenoecus cavecricketlargerthan26mm HFL.Sexuallymatureadultcricketsaredarkerbrown thansub-adultsduetohardeningandtanning(sclerotization)oflegsandovipositors.Wehypothesizethatthe cricketstakeuptothreetofouryearstoreachadultsize thatisprobablyinfluencedbytheirsuccessinfinding food.Cricketsmayliveanotherthreetofouryears(or longer)asasexuallymatureadult.Oneofthebestlines ofevidencewehaveforthisextremelongevityisthe frequencyofobservedmoltingcrickets. C.stygius ,which livesforayear,routinelyhas2–6%ofthepopulation molting,comparedto H.subterraneus ,wheretherates are0.1–0.01%(basedononemoltingcricketof512 observed,oneof969,andoneof1,024ondifferent censusdates,andmanythousandsofcricketsobserved withnomolts). Reproductivestudiesoncavecricketshaveconcentratedonthepresenceandsizeofmaturegonads,egg-laying rates,andreproductivebehaviors.Seasonaldissectionsof cricketsforspermatophoresinmalesandovainfemales suggestthat H.subterraneus arecapableofreproductionin allmonthswiththepossibleexceptionofJuly.(Cyretal., 1991).Thesedatasupporttheobservedseasonalityin reproductionreportedbyHubbellandNorton(1978)and GriffithandPoulson(1993). Measurableovawerefoundin Ceuthophilusstygius only inAugust,September,andOctobersamples,indicating markedseasonalityinreproductioninthisannualspecies (Cyretal.,1991).Parasitismbyhairwormsmarkedly affectsnumberandsizeofovaformedin C.stygius (Studieretal.,1991).Sixnon-parasitised C.stygius contained25.5 6 4.2ova/femalewhilenineparasitized femalescollectedatthesametimecontainedanaverageof 2.2ova.Sevenparasitizedfemaleshadnoovaatall. NorthupandCrawford(1992)studiedtwoofthe Ceuthophilus speciesinthreepassagesinCarlsbadCavern. Someseasonalityinreproductionandfrequencyofadults of C.carlsbadensis wasnoted,butthepatternisnotas strongforthemorecave-adapted C.longipes.C.carlsbadensis females(n 745)contained0–60eggs,withamean of6.34( / 1.09)eggsperfemale. C.longipes (n 43)had arangeof0–4eggsperfemale,withanaverageof0.67eggs ( / 0.17).Seventy-twopercentofadultfemale C.carlsbadensis hadeggscomparedtoonly37%ofadult C.longipes. C.longipes producessignificantlyfewerandlargereggs,as expectedofamorecave-adaptedanimal.Patternsof distributionofimmatureandadolescentcricketswere highlyvariableinbothtimeandlocation.Theauthors suggestthatbothspeciesofcamelcricketsareableto reproducethroughouttheyear. Totalannualeggproductionby H.subterraneus was estimatedbyCyretal.(1991).Duringwinter,20–30eggs werelaidbyindividuallycagedfemalecricketsina2–3day periodofrapidegglaying,whileinearlysummer,therate was1–3eggslaideveryeightdays.Ifaverageeggslaidper yearisbasedonmaximumegg-layingratesforeachperiod ofobservation,thentheannualeggproductionis96to371 eggslaidperyearperfemale.Itisunlikelythatcrickets maintainmeasuredmaximumegg-layingoverextended timeperiods.Threepairsofcagedcavecrickets,collected in copulo ,however,laidanaverageof0.46eggs/dayover a154dayintervalfromMarchtoAugust,whichcorrespondstoanannualegg-layingrateof167eggs/year.The timespanstudiedwasnotthepeaktimeforeggproduction,andthe154dayintervalisalsolongerthanthe estimated12weeksneededforeggstohatch,sothisrate estimateisprobablylow.ComparedtootherOrthopterans,theestimatedrangeissomewhatlow.Inayear,the commonhousecricketlays728eggs,Germancockroaches lay218–267eggs,andAmericancockroacheslay200–1000 eggs(AltmanandDittmer1972). Individually-cagedadultfemale H.subterraneus showed seasonaldifferencesintheamountofegg-layingin MammothCave(Cyretal.,1991).Atadeepcavesitein Sophy’sAvenue,manymoreeggswerelaidintwoday intervalsfromOctobertoFebruary(4.3ova/day)thanin AprilandJuly(0.6ova/day).Egg-layingattheFrozen NiagaraEntrancesiteaveraged0.1–0.8ova/dayinspring throughfall.Theinfluenceofseasonalenvironmental conditionsisshowninthewinterdata,wherethegreatest numberofeggswerelaidinSophy’sAvenue,andnoeggs werelaidinFrozenNiagara.Atthatstudytimethe entrancedoortoFrozenNiagarawasdamaged,which allowedcold,dryairtoenterandextendapproximately 75mintothecavewherethefemaleswerecaged.Halfof thecagedfemalesdied,andnoneofthesurvivorslaidany eggsorevenmadeanyovipositorholes. T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 116 N JournalofCaveandKarstStudies, April2007

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P OPULATION S IZE Thesizeofindividual H.subterraneus, andtheside passagesandalcoveswecan’taccess,makecompletedirect populationcountsextremelydifficultandoflimited reliability.Andexceptinsmallcaves,exactlywhereisthe endofthecaveforpurposesofacensus?Onlyafew attemptsatpopulationstudieshavebeenmadeandonly forlargecavecrickets.Ingeneral,resultsaremore consistentinverysmallcaves,suchasLittleBeautyCave andWhiteCaveinMammothCaveNationalPark. Onetechniqueusedtoestimatetotalpopulationsizeis knownasmark-recapture.Allindividuals(markedand unmarked)arecountedandmarkedwithadifferentcolor ondays1and2andcountedagainonday3.Cricketscan bemarkedsuccessfullywithdotsofdifferentcoloredoffice correctionfluidorpaintontheirbacks,bygluingon numberedbeetags,orusingUVbrightpaint.Total numbersofmarkedandunmarkedcricketsoneachdayare usedtocalculateastatisticalestimateoftotalpopulation size.Attemptstodomark-recapturestudiesofcavecricket populationsareoftencomplicatedbythelargeturnoverof animalsfromaccessiblestagingareaswherewecanseeand markthem,toroostareasthatareinaccessibletohumans. Problemswithmark-recapturestudiesareacontinuing mystery. Amark-recapturestudybyHellman(1989)fromfallto winterfortheFrozenNiagaraEntranceofMammothCave estimatedthattherewere976.8( 6 209.4)adultcricketsin October1987,butonly70.6( 6 35.9)cricketsinFebruary 1988.Thedifferencesarenotduetoahugepopulation crash,butreflectthereducedmovementofcricketsinthe wintermonths.HobbsandLawyer(2002)marked769 adult Hadenoecuscumberlandicus cavecricketsfrom aparthenogenicpopulation(allfemales)inCoon-in-the CrackCaveinKentucky.Basedonthemark-recapture rate,theyestimatethetotaladultpopulationsizeinthis caveas5,508individuals. Duringalong-termbiomonitoringprojectatMammoth CaveNationalPark,Poulsonetal.(1998)foundsome interestingdifferencesamong H.subterraneus populations atninemonitoredentrances.Theycollectedcensusdataby dividingcricketsintofoursizeclasses,1–4,withsizeone beingthesmallestjuveniles,andsizefourbeingsexually matureadultsasestimatedbysizeanddegreeoftanningof ovipositorsandlegs.Insteadofexistingasonemetapopulationwithroughlyequalinteractionsamongsubpopulations,therearesourceandsinkpopulations.In asourcepopulationthereisagreaternumberofsmaller sizeclassesrelativetolargersizeclasses,whichsuggests apopulationthatisincreasing,althoughsmallcrickets neveroutnumberlargeadults.Asinkpopulationisgreatly skewedtothelargeradultandsub-adultsizeclasses,with lowlevelsoflocalreproduction.Thesinkpopulationsare maintainedbyimmigrationofcricketsfromsource populations.Thereweresourcepopulationsatthreeof nineentrances,andsinksattheremainingsix.Thereisno relationshipbetweentotalpopulationsizeandwhether anentranceisasourceorasink.Ingeneral,source populationsarelocatedinentrancesthathaveceiling pocketsthatprovidearefugeabovetheinfluxofsurfaceair andareclosetosuitablereproductiveareas.Mostofthe sourceentrancesarelocatedinsinkholesorinmature foreststhatoffergoodforagingopportunitiesandaprotectedmicroclimate.Bothtypesofpopulationsshouldbe protectedsinceemigrationofadultsfromasinkcan repopulateasourcepopulationshoulditbewipedout. I NTRACAVE D ISTRIBUTION Inmanycaves,cricketsaredifficulttofind,butinother cavesyoucaneasilyseehundredsofindividualsin arelativelysmallarea.Thesenumbersmaychange drasticallywithtimeofdayandseason.Cavecrickets gatheraroundentrancesasroostsandinstagingareas wheretheycanevaluatesurfaceconditionsbeforeleaving thecavetoforage.Theyarealsofoundinstabledeepcave areasawayfromhuman-sizedentrances,butcloseto cricket-sizedentrances. CathedralCave,asmallcaveinalimestonebluff overlookingtheGreenRiverinMammothCaveNational Park,wasthesiteforathreeyearstudyofthemigration patternsof H.subterraneus byBrotherNicholasandhis students(Nicholas,1962).Cricketsweretheonlyimportantsourceoffoodinputintothecave.Thesmallcavewas dividedinto123.1m(10ft)longtransects.Adifferent colorpaintwasassignedtoeachtransect,andalllarge cricketsineachtransectweremarked,atotalof3,750 individuals.Ninety-sevenpercentofmarkedindividuals werefoundintheiroriginal3.1m(10ft)quadranteachday (Nicholas,1962).Dailyobservationshowedthatabout1/3 ofthecricketsemergedeachnighttoforageunderoptimal environmentalconditions.Thisregularexitingof1/3ofthe populationisnotconsistentwithmorerecentmetabolic studies,asdiscussedbelow.Wealsoobservegreat reductionsinthenumbersofmarkedcricketsoverlonger periodsoftime. Neilsen(1989)tookadvantageoftheveryflatceilingin FloydCollinsCrystalCave,MammothCaveNational Park,forastudyof H.subterraneus distributionoversix days.Hemountedalightonatripodwithagridoverthe endtoprojectapatternofonemetersquaresontheceiling inthefirst28metersofthecave.Everysixhours,every otherdayforthreecensusdays,heandateammappedthe locationofeveryindividualcricket.Theyfoundthatthe distributionoftotalcricketswasveryuneven(Fig.3),with someareashavinglargenumbersofindividualsofallsizes, andotherareasconsistentlyhavingnone.Thedistribution isprobablyrelatedtolocalmicroclimatedifferenceswith lesswindfloworhighermoistureforthecrickets. Totalcountsofroosting H.subterraneus showacyclical patternwithrespecttodayandtimeofcollection.Highest K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 117

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populationcountsintheentirecensusareaareinthe eveningat1800hours(367individuals)whilethelowest countisintheearlymorningat0600hours(255 individuals).Emergenceofmorecricketsintothestudy areaduringthe1800hourcountisconsistentwithcrickets samplingentranceconditionsintheeveningtoseeif epigeanclimateisappropriateforforaging(Studieretal., 1986).Numbersalsofluctuatewithtimeascricketsretreat toandemergefromsitesthatareinaccessibletohumans. Cricketswereobservedatdistancesintothecavegreater thanthe28meterssampledinthisstudy.Wherethe cricketsgowhentheyleavetheaccessiblesitesisoneofthe mysteriesofthecave. Patchydistributionsoffemale Hadenoecuscumberlandicus cavecricketsinshelteredlocationswerereportedby HobbsandLawyer(2002).Yoderetal.(2002)reportthat aggregationbehaviorsinthesecavecricketsserveto protectthemfromdehydration.Increasingcricketgroup size(1,5,10,and20)causedlowerwaterlossratesincaged crickets.Theprotectivegroupeffectwaseliminatedwhen theyuseddryflowingair.Theyproposedthatthe protectionfromclusteringisfromincreasedlocalrelative humidity. Fewstudiesexaminetheintracavemovementand dispersalofcavecrickets.HobbsandLawyer(2002) marked2,378adultfemaleandjuvenile Hadenoecus cumberlandicus cavecricketsfromCoon-in-the-Crack CaveinKentucky.Basedontaggedindividuals,the majorityofcricketsmovedanaverageof10–15md 1 withameanof41m.DowningandHellman(1989)also examinedin-cavemovementof H.subterraneus from WhiteCave,MammothCaveNationalPark.Theyused differentcolorsoftypewritercorrectionfluidtomark adultcavecricketsneartheentrance(10–15mfromthe entrance)andthosefounddeeperinthecave(35–40m fromtheentrance).Thedistributionofthemarkedadult cricketswasmonitoreddailyforaweekby5mtransects fromtheentranceto50mintothecave.Within24hours therewasageneralmovementofcricketsfromthefrontof thecavetowardstherear,includingoneindividualthat moved25m.Cricketsmarkedfromdeeperinthecave tendedtomovearoundless.Onthemorningofday4, aftertheonewarmnightduringthestudyperiod,there wasmovementofcricketsfromthebacktothefrontofthe cave.Asimilarrhythmicmovementpatternwasobserved byCampbell(1976)with C.conicaudus inSpiderCavein NewMexico. S EASONAL D ISTRIBUTIONAND A BUNDANCE InsomecaveentrancesincentralKentucky, H. subterraneus co-existinverylargenumberswithmuch smallernumbersof C.stygius .Largenumbersofcrickets werecollectedintheirroostingcavesduringallfour seasonsfromWhiteCave,WalnutHillCave,theFrozen NiagaraEntrancetoMammothCave,andFloydCollins CrystalCave(Studier,etal.,1988).Cricketswerecollected byhand,sexedwhenlargeenough,andhindfemurlengths (HFL)measuredtothenearest0.1mm.Considerablecare wastakeninsearchingforandcollectingallsizesof cricketssincesmallercricketsareeasilyoverlookedbecause theyroostinsmallcrevicesandstayawayfromopen spaces. ThedistributionofcricketsbyHFLforallcavesstudied foreachseasonispresentedinFig.4. H.subterraneus ofall sizesarepresentinallseasons,andadults(HFL 19.9mm)makeupthegreatestfractionofeachpopulation inallseasons.Thereisnoapparentseasonaldifferencein distributionbysize,andnotraceablepeaksforthesmaller Figure3.Cavecricketdistributionsummedoverallcensus countsinFloydCollinsCrystalCave(Neilson1989). T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 118 N JournalofCaveandKarstStudies, April2007

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sizedcricketsthatwouldindicateaseasonalperiodof intensereproductionwithinthepopulations,despite reportedmarkedseasonaldifferencesinreproductiveeffort inthisspecies(Barr,1967;KaneandPoulson,1976; HubbellandNorton,1978).Differencescouldbebecause allsitessampledforthisstudyareentrancesitesincontrast todeepcavesitesasdiscussedlaterinthispaper. Thepopulationstructurefor H.subterraneus shownin Figure4whereadultspredominate,istypicalofalonglivedpopulation.Weknowfromrecoveryofmarked, numbered,individualsthatadultcavecricketscanliveas adultsatleast17to24months,considerablylongerthan the7to11monthsreportedbyHubbellandNorton (1978).Thepreponderanceoflarge,sexually-matureadults atalltimesoftheyearshowsthatcavecricketsare relativelylong-lived,perhapslivingforfouryearsormore. Datafor C.stygius arealsopresentedinFigure4as discreteboxes,wheretheverticallineisthemeanHFLof cricketsmeasured,andthewidthshows95%confidence intervals(Studieretal.,1988).Camelcricketsaretypically foundindiscretesizecategoriesineachseasonduetotheir yearlylifecycle. C.stygius showsabigjumpinsizefrom springtosummerwithaperiodofrapidgrowthand attainmentofsexualmaturity.Anewcohortofyoung appearsinthefalltojointhecohortofcurrentadults.By winter,mostlysmallcamelcricketsover-wintertobecome thenextseason’scohortofadultsastheyemergeinthe springtofeed. ThesamedatafromFigure4showsthattotalcrickets bygenderamongsub-adults(15.0–19.9mm;263females and231males)haveasexratiocloseto1:1.Adultcrickets bygender(713females:509males)haveasexratiothatis significantlydifferentinwhichfemalespredominate.Lack ofagenderbiasamongsub-adultsandthepreponderance offemalesamongadultcricketssuggestsadifferential mortalitywithgreaterdeathratesforadultmalecrickets. Malecricketsmustleavethesafetyofthecavetofeedmore frequentlyandtheystayoutlongerthanfemales,which probablyresultsinahighermortalityrateformales (Studier,etal.,1986).Alternatively,femalesmaysimply livelongerthanmales.Norton(personalcommunication) foundunpredictablevariationsinmale:femaleratiosof H. subterraneus ,sothisisanothermysteryofthecave. E NTRANCEVS .D EEP C AVE S ITES HubbellandNorton(1978)suggestthattheremaybe differencesbetweenentrancepopulationsofcavecrickets anddeepcavepopulations.Anentrancesiteisalocation thatcanbeusedbyhumanstoenterthecave.Adeepcave siteislocatedawayfromanentranceaccessibletohumans anddoesnotexperiencetheseasonalchangesintemperatureandhumidityatanentrancesite.BecauseofadomepitarrangementattheSophy’sAvenuesiteandatBubbly PitinGreatOnyxCave,densecoldwinterairflowsdirectly pasttheroostsitewithlittleeffectonroosttemperatureor relativehumidity.Inallcases,successfulreproduction requiresanareawithasuitablesand-claysubstrate. H. subterraneus cavecricketsareverynegativelyaffectedby airthatisnotwater-saturatedandbytemperature fluctuations(Studieretal.,1987b;StudierandLavoie, 1990). Ourlongtermbiomonitoringstudyshowsthatthe populationsfromthesetwoareascangradeintoone another.OurbestexamplecomesfromtheNewDiscovery entrance,wherealargepopulationofcricketsofallsizes, withadultspredominating,isfoundinthefirst20meters fromtheentrancereadytoexitthecaveandforage. Continuingintothecavefor100metersshowsaswitchto adeepcavesitewherethemainfunctionofthepopulation isreproductionandthereareonlyadultsandsmallyoung cricketspresent. Figure4.Seasonaldistributionbyhindfemurlength(HFL) of H.subterraneus (datapoints)and C.stygius (boxofmean, widthis95%confidenceinterval)fromfourentrancesin Kentucky(Studier,etal.1988). K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 119

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Seasonalaveragesofova(eggs)perfemale H.subterraneus arequiteconsistent,butdoshowsite-related differences.Cricketsinentranceareasshowconsistently lowlevelsofreproductionasevidencedbythenumberof eggsperfemalecricket(average6.7ova/female),while femalesfromadeepcavesiteshowstrongseasonal differencesinreproductionandegg-laying(average18.1 ovaperfemale)(Cyretal.,1991).HubbellandNorton (1978)reportaveragenumbersoflargeovaforfemalesin JulyandJanuaryattheentranceatGreatOnyxat2.1and 5.3,fromdeepinGreatOnyxat5.6and7.0,andfrom JanuaryinParkersCaveat3.6intheentranceand7.6 deeperinthecave. Anotherstrikingdifferenceisthesize-classdistribution between H.subterraneus inentrancesitesanddeepcave sites.Entrancesites(Fig.4)showamajorityofadultsand afairlyevenrepresentationofcricketsinothersizeclasses. Datacollectedfromtwodeepcavesitesareshownin Figure5(StudierandLavoie,unpublisheddata).Thereare manylargeadultsandmanysmalljuveniles,butthe intermediatesizeclassesarenearlyabsent.Adultsare skewedtoamalesexbias,andmalesandfemaleshave muchlessfoodintheircropsthaninentranceareas.The deepcavesitesserveasreproductiveandnurseryareas wherecricketsgotomateandlayeggs(Hubbelland Norton,1978;KaneandPoulson,1976).Theeggshatch andtheyoungcricketsgothroughseveralmoltsinthecave beforeleavingtoroostaroundentranceswheretheycan leavethecavetofeed.Youngcricketsinthedeepcave areasmayfeedmostlyonotherindividualsoftheirspecies (Levy,1976).Theactualnumberofmoltstoreachadult sizeisestimatedbyHubbellandNorton(1978)aseight. Theyreportedthatcagedhatchlingsstayedinthenonfeedingwhitestageforfiveweeks,moltedtofeedingsecond instarsfortenweeks,andtheywereunabletoraisethe cricketsbeyondthat. M ETABOLIC R ATESAND W ATER B ALANCES Lowmetabolicratesareassumedtobeatroglomorphic characteristic.Studiesofthemetabolismandwaterbalance of H.subterraneus and C.stygius weremadebycaging adultindividualsinthecaveandmeasuringweightlossas afunctionoftime(Studieretal.,1986,1987a,1987b;Viele andStudier,1990).Thesewerewild-caughtanimals,and weselectedforcricketsthatappearedtohavemorecrop contents.Dissectedcrops,carcasses,gonads,andcombined wasteswereanalyzedinthelabformoisturecontentand caloricvalue.Themetabolicratesfor H.subterraneus are one-halfthatofsurfaceinsectsofsimilarmass(Studieret al.,1986).TherelationshipbetweenbodymassandHFL differsbysexfor C.stygius andisthesameforbothsexes forcavecrickets.Thisrelationshiphasahighpredictive value( R 2 0.902)andallowsustomeasurethehindfemur lengthandweightofacricket,andbyextrapolation determineitscropcontentswithouthavingtosacrificethe cricket,usingtheequation: CELWmg 2 698HFL2 50 07HFL 274 1 1 Inthisstudy,wild-caughtfemalesstartedat101%oftheir crop-emptyliveweight.Theseadultfemale H.subterraneus lostweightataratethatwouldmakethemcrop-emptyin 11.5days.Adultmaleslostweightataslowerrate,but theyhadconsumedonly72%oftheirbodyweight,sothese malesshouldleavethecavetofeedatleastevery9.9days. H.subterraneus exitingWhiteCavehadnearlyemptycrops and65.2%ofexitingcricketsweremales(Studieretal., 1986).Helf(2003)reportsthatsomecricketscanconsume inexcessof200%oftheirbodyweightinfoodinasingle feeding.Mostfullwild-caughtcricketshad110–130%of theircrop-emptyliveweight(CELW)intheircrops.Higher startingcropcontentswouldextendtheseprojectionsof timebetweenfeedingsbyupto2–2.5timeswhichwouldbe themaximumtimetheycouldstayinthecavebefore leavingtofeedtoavoidusingupbodyenergyreserves. Adult C.stygius lostweightattworatesoverthefive daysofthestudy,whichweinterpretasarapidphasedue tocrop-emptying,followedbyaslowerrateofweightloss whenfatreservesarebeingutilized(Studieretal.,1986).If theyaretoavoidusingfatreserves,femalecamelcrickets mustforageatleastevery3.0daysandmalesevery 2.3days. C.stygius areabletoconsumeonly34%to39% (males vs. females)oftheirbodyweightinfood.Because camelcricketshaveverylittleflexibilityinhowoftenthey Figure5.Distributionof H.subterraneus byhindfemur length(HFL)attwodeepcavesitesinMammothCave NationalPark.(StudierandLavoieunpublisheddata.) T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 120 N JournalofCaveandKarstStudies, April2007

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mustfeedtomaintaintheirfatreserves,theymustbeable toleavethecavemorefrequentlyandendureawiderrange ofenvironmentalconditionsthancavecrickets. Cavecricketsarealsoverysensitivetomoisturelossby evaporationbecausetheiroutercuticleisthincomparedto camelcrickets(Fig.6).Thecuticleof H.subterraneus is approximatelyhalfasthickandappearstolackepicuticularwaxcomparedto C.stygius .Yoderetal.(2002) reportedthatextractablecuticularlipidsweresignificantly lowerfrom H.cumberlandicus comparedto C.stygius Themetabolismofthethreespeciesof Ceuthophilus cricketsfromCarlsbadCavernshowtheexpecteddifferenceswithdegreeoftroglomorphy(Northupetal.,1993). Basedonanin-caveweightlossstudy,calculatedmetabolic rates(calh 1 )were1.04for C.carlsbadensis and0.52for C. longipes .Thesemetabolicratesarehalfthosepredictedfor epigeanspeciesofsimilarsize.Thelong-termweightloss patternsarelinearforallthreespeciesoverthefivedaysof theweightlossstudy.Foragingintervalsareinferredfor femalesandmales,respectively,of5.1and4.4daysfor C. carlsbadensis ,4.6and5.7daysfor C.longipes ,and5.0and 4.2daysfor C.conicaudus .Again,thesewild-caught cricketshadfedatsomeunknownearliertime,andthe actualfeedingintervalsarecertainlylonger. R ESPONSESTO T EMPERATUREAND R ELATIVE H UMIDITY IncentralKentucky,cavecricketsmustforageforfood outsidethecave,butforagingisveryrestrictedbysurface temperatureandrelativehumidity(LejaandPoulson, 1990;StudierandLavoie,1990;Helf,2003).Outside temperaturesmustbeclosetocavetemperaturesof13 u C (55 u F)andrelativehumiditymustbeclosetosaturated. Tracingsfromanelectriceyecricketcounterareshownin Figure7fortwotimesoftheyearatMammothCave (Helf,2003).Insummer,apatternoftwopeaks(exitand entry)isseeneverynight.Inwinter,cricketsdonotleave thecavewhenthetemperaturedropsbelowabout5 u C. Largenumbersofcricketsleaveonlyonthewarmest nights.WeatherrecordsforMammothCaveNationalPark indicatethatonmostnightsthroughouttheyearforat leastashorttime,surfaceconditionsallowforaging.There areonlyafewweeksduringthehottestmonthsofsummer andthedepthofwinterthatarecompletelyoff-limitsto foraging.Fivedegreescelsiuswasthelowertemperature limitforsurfaceforaging.Attheselowtemperatures, H. subterraneus experiencehighevaporativewaterlossthat maybemadeupbyconsumptionofmoisterfoods. H.subterraneus rapidlylosewateranddieaboveeven themildtemperatureof20 u C(62 u F).At13 u C, H. subterraneus lostwater(0.35–0.53mg%h 1 )atamuch higherratethan C.stygius (0.08mg%h 1 ).At23 u Cwater losswasabout5to9timeshigherforbothspeciesof crickets,but H.subterraneus (1.49–1.52mg%h 1 )again greatlyexceedwaterlossfor C.stygius (0.27mg%h 1 ).In termsofQ10,aroughmeasureoftheeffectoftemperature onphysiology,theQ10at9.5 u C–15 u Cwasabout1.2, indicatingnoeffect,temperaturesfrom15 u C–20 u Cand 20 u C–25 u Cwere2.5–3.0,whichisatypicalphysiologic activityrange.At25 u C–30 u C,theQ10waslethal. Ectothermssuchasinvertebrates,fish,andreptiles, cannotmetabolicallyregulatetheirbodytemperatures,so bodytemperaturechangesinresponsetochangesin environmentaltemperature.Themetabolicrateinthese animalsisexpectedtoincreasewithincreasingtemperature.Theabsoluteincreaseinmetabolicrateismuch greaterin H.subterraneus thanin C.stygius (Studierand Lavoie,1990).Thefactthat H.subterraneus dievery quicklyandcouldnotevenbetestedattemperatures exceeding25 u Cindicatesthattheyhavemuchgreater thermalsensitivitythan C.stygius .Thesemarkedthermal sensitivitiesindicateadaptationtonearlyconstantambient cavetemperatureandresultingreatlyincreasedmetabolic demandsathighertemperatures.Asaresult,weexpect voluntaryepigeanforagingatambienttemperaturesmuch abovecaveconditionstobereduced. Because H.subterraneus foragesonthesurface throughouttheyear,itisexposedtohighlyvariable climaticconditionsrelativetothoseinthesubsurface environment.Helf(2003)examinedtheimpactofclimatic conditionson H.subterraneus exitpatternsinMammoth Figure6.Crosssectionofthecuticleofa) H.subterraneus andb) C.stygius takenat400 3 K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 121

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CaveNationalPark.Heanalyzeddatafrom1996to1998 onsurfacetemperature,precipitation,and H.subterraneus exitpatternsusinganelectroniceyeplacedatanarrow crackjustoutsideacaveentranceknowntobeheavilyused bycrickets.Overall,significantlygreaternumbersofcave cricketsexitedthecavenightlyinsummer(approximately 460 6 50/night)versuswinter(approximately190 6 25/ night).Inspring/summer,therewasasignificantpositive correlationbetweennumbersofcavecricketsexitingcaves andrainfall.Cavecricketbiologysupportsthisconclusion inthateveningswithsignificantrainfallwouldreducetheir evaporativewaterlossandincreasethevolatilityof odoriferousfoodpatches,thusincreasingcricketsuccess infindingfood. Evenmoreimportantistheeffectofcoldwintersand summerdroughtsoncricketsurvival.From1994–1997we Figure7.CountsofexitingcricketsatFrozenNiagaraEntrance,MammothC aveduringoptimalforagingtemperaturesin 1997andsuboptimalforagingtemperaturesin1998.SolidLinesreflectcr icketsexitingthroughacrack3maboveground level.Dottedlinesindicatetemperature(Helf2003). T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 122 N JournalofCaveandKarstStudies, April2007

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censused H.subterraneus populations2–6timesperyearin ninecaveentrancesinMammothCaveNationalPark (Poulsonetal.,1998).Theoverallnumbersofsizeclasses1 (smallest),2,3and4(largeadults)generallyincreasedinall cavesoverthefouryearswithmeannumberspercaveof 1,026,1,998,1,645,and2,670.Inthetwocaveswiththe largestpopulationstherewasasteadyincreaseof1,250, 2,180,2,895,and4,148bothforaweaksourcecave(Great Onyx)and1,980,2,133,2,597,and2,695forasinkcave (White).Theinitiallownumberswereprobablythe lingeringeffectofaseverelate1980sdroughtandsevere early1990swinters.From1994to1997theTaylorDrought Indexgenerallydecreasedasdidthenumberoflongwinter coldsnapsthatabsolutelyprecludeforagingbycrickets. Wealsoknowfromindirectevidenceofcricketguano communitiesthatdroughthashadanegativeeffecton cricketpopulationsintheintervalfromtheearly1970sto late1980s(Poulsonetal.,1995).Thepresumedmechanism isthatcricketspreferredmoistand/orrottingfruit,feces, micro-carrion,andmushroomsarelargelyunavailable duringdroughts.Inthiscontextitisnotsurprisingthatour bestsourcecaveshavemoist,protected,matureforests aroundtheirentrances. Thethreecloselyrelatedgryllidcricket Caconemobius speciesfromHawaiiareanappropriatecomparisonamong acave-adaptedspeciesanditstwocloselyrelatedsurface species.AhearnandHowarth(1983)studiedwaterbalance physiologyandmetabolicratesofthesespeciesand,as expected,foundthattheirabilitytoconservewateris stronglycorrelatedwiththeirenvironment. C.sandwichensis ,themarinerockzoneancestor,israrely,ifever,subjected toextremesintemperatureortorelativehumiditylessthan 98%. C.fori ,thelavaflowspecies,isexposedtoextremesin temperatureandrelativehumidityfromdailycycles,and mayalsohavetocontendwithgeothermalheat.Thecave species, C.varius ,livesinaconstanttemperatureenvironmentandisextremelysensitivetorelativehumiditybelow saturation.After12hoursinadryenvironmentneartheir normalambienttemperature(19 u C),thecavespecieslost significantlymorewater(14.7 6 0.7%ofbodymass)than dideithersurfacespecies, C.fori (8.8 6 0.7%)and C. sandwichensis (11.5 6 0.6%). D IETAND D IGESTION Whatdocricketseatinthewildisasimplequestion,yet isoneofourenduringmysteriesofcavecricketbiology. Theyactasscavengers,eatingwhateverissmellyenoughto gettheirattentionandsoftenoughtochew. H.subterraneus havebeenobservedeatingmushrooms,deadinsects, animaldroppings,berries,andflowers.Tayloretal.(2005) observedoneforaging C.secretus cavecricketwithalive hemipteraninitsmandibles.Cricketscomereadilyto awiderangeofbaits,includingrottenliver,limburger cheese,catfood,grapejelly,andpeanutbutter.Examinationofgutcontentsshowsmostlyunidentifiablemush, withanoccasionalrecognizableinsectpartorpieceofmoss (Levy,1976).Cricketsseemtoeatamuchmorevarieddiet insummerthaninwinter.Theyarealsocannibalisticand willeatanycricketthatisinjured,buttheywillnoteatthe cropoftheinjuredcricket.Cropsmaybeasourceofinjury ordeath,andcricketsmayavoideatingthemtopreventthe cricketequivalentoffoodpoisoning(Janzen1977). Astudyofcaged H.subterraneus feddifferenttypesof foodsoneatatime(Lavoieetal.,1998,Helf2003)shows thatcricketsdonoteatpartiallydecomposedleaflitter, moss,lichen,orliveearthworms.Cricketsgained5–35%of theircrop-emptyliveweight(CELW)onoverripefruit, deerfecalpellets,orfreshmushrooms.Cricketsgained70– 120%ofCELWfromeatingrottingmushrooms.Offering cricketsartificialbaitsofcatfoodorwetcerealcaused themtoreallytank-up,eating100–250%oftheirCELW. Wehavedoneextensivesearchesforcricketfoodsinthe wild,andwehavealotlesssuccessatitthanthecricketsdo withtheirwell-developedsenseofsmell.Thenaturalcrop contentsarelowinsodiumrelativetopotassium,andlow intotalcalories,whichsuggeststhatthecricketsdonot commonlyfindsuchhigh-qualityfoodsascarrionordead insectsinthewild(Studier,1996). Organismsthatconsumeplantdetritus,decayingfruit, rottingwood,andherbivoredungingestavarietyof bacteria,protozoaandfungialongwiththeirfood(Martin andKukor,1986).Ifingestedmicrobessurviveand proliferateinthedigestivetractorexcreteenzymesthat remainactiveinthegut,theningestedmicrobescan augmentorextendthedigestiveandmetaboliccapabilities oftheorganismthatconsumesandharborsthem(Martin andKukor,1986,KaufmanandKlug,1991).Thecropof H.subterraneus isaverythin-walledstructurethatlies betweentheesophagusandhindgut(Fig.8).These cricketsfrequentlyeattothepointofphysicaldistortion byconsumingverylargeamountsoffoodinasingle foragingbout.Thecropmayactasastorageand fermentationchamberwhereanassemblageofmicrobes pre-digeststhefood.SomeOrthopterans,includingcrickets,grasshoppersandcockroaches,dependonboth residentandingestedmicrobestoaidindigestion, fermentation,andproductionofsecondarymetabolites, includingpotentialtoxins. H.subterraneus maybepartiallyrestrictedtoanarrow temperaturerangetokeeptheircropmicrobes,including bacteriaandyeast,undercontrol.AsreportedbyStudier andLavoie(1990),cavecricketsdieinafewhoursifheldat temperaturesaboveroomtemperature(23 u C).Someof thesecrickets,aswellasanoccasionalfield-collected specimen,hadcropsvisiblydistendedwithgas,occasionallytothepointofrupture.Wethinkthatcricketswere killedbyunregulatedgrowthofcropmicrobesthat produceexcessivegaseousortoxicmetabolitesatelevated temperatures. Mostmicrobesisolatedat20 u Cfromcavecricketcrops orhindgutsgrewbestaboveambientcavetemperaturesof K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 123

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13.5 u Cwithonlyoneisolateshowingoptimumgrowthat caveambienttemperature(Phillpotts,1989).Thepatternof growthatdifferenttemperaturesislargelyduetothe activityofenzymesatdifferenttemperatures.Enzyme activitygenerallyincreasesuptothetemperatureoptimum, andcropenzymeactivitywasoptimumat23 u C.One limitationoncavecricketforagingistheneedtoslowdown themetabolicactivitiesofcropmicrobesthatarelargely responsibleforfooddigestion.Whencavecricketswerefed dietsrichineithercarbohydratesorproteinandcompared tothenaturaldiet,theactivitiesofspecificenzymes respondedrapidlytothedifferentdiets,aswouldbe expectedifmicrobeswereproducingthedigestiveenzymes (White,1989;Coller,unpublisheddata). Whateverthereasonorreasonsfortheextremethermal sensitivityobservedin H.subterraneus ,evenamodest increaseincaveambientconditionscouldhaveprofound negativeeffectsoncavecrickets.Sincecavesmaintainthe averageannualtemperatureoftheareawheretheyare located,globalwarmingwouldresultinincreasedcave temperatures.Evenamodestincreaseof2–6 u Coverthe next50years(Schneider,1989)wouldgreatlyincrease metabolicdemandsandevaporativewaterloss,which wouldforcemorefrequentforagingboutsandexposureto surfaceconditionsandpredators.Thesechangeswould probablyresultinextinctionofcavecricketsandthe concomitantlossofthemajorsourceoffixedcarbon energyinputsintocavesincentralKentuckyandmany otherareasaroundtheworld(Poulson,1991). F ORAGING Mostcavecricketsmustleavethecavetoforagefor food.Theyhavetoconsidermanyfactorsindecidingwhen toleavethecave.Theywillleaveonlywhenitisdarkand conditionsonthesurfaceareclosetocaveconditionsof15 u Cand100%humidity,whichareobviouslyinfluencedby season.Howfullthecricketisanditsriskofbeingeaten areotherfactorstheyhavetoconsider.Adultcricketshave theadvantageofhavinggreaterfatreservesthanjuveniles, sotheycanaffordtowaitlongerforbetterforaging conditionsthansmallercrickets. Campbell(1976)usedadirectionalelectriceyecounterto showthatdecreasinglightintensitywasthetriggerfor C. conicaudus toemergefromSpiderCave.Totalnumbers emergingwereinfluencedbytemperature,relativehumidity, andmoonlightintensity.Numberscouldchangedrastically inashorttime.FromJuly3–4,110cricketsemerged comparedtoJuly7–8when1,195cricketsemerged.Inlab studies,hungrycricketsweremoreactive.Thehighest emergenceoccurredonnightswithlowtemperatures,high relativehumidity,andlowlightintensity. Levy(1976)observedthat H.subterraneus useodorto differentiateamongfoodchoices.Smallcricketsareless fussyaboutwhattheyeatthanmediumorlargecrickets. Smallcricketsfedonthefirstfooditemtheyencountered, comparedtolargercricketswithlongerlegsandantennae thatcansensefoodfromagreaterdistanceaway,andget topickandchooseamongthedifferentfeedingopportunities.Shedescribed H.subterraneus asscavengersonstilts. Odorishighlycorrelatedwithcaloricvalue;smellyfoods tendtohavemorecalories,butLevycouldnotdetermine whethercricketsshowedarealpreferenceforhigher caloriesorjustsmell. DeLong(1989)didadeceptivelysimplecaloricdensity preferencestudyinthecavebyoffering H.subterraneus abuffetofthreefoodchoices.Heusedtwoextremes;pure peanutbutter,whichhasastrongsmellandishighinfat andcalories(5.9Kcalg 1 ),andpurecornstarch,which hasnoodorandisapurecarbohydratewithmuchlower caloricvalue(4.1Kcalg 1 ).Athirdbaitchoicewasa 50:50mixturethatreducedavailablecalories(downto 5.0Kcalg 1 ),butkeptthestrongodorassociatedwith peanutbutter.Thebaitbuffetwasofferedforonehour underseparatelivetraps(aplasticringcappedwith screeningandproppedupwithastick),trapsweresetby remotelyyankingastringattachedtothestick,and capturedcricketswerecounted,sexed,andhadtheir HFLmeasured(Table1). ConsistentwithLevy’sscavengeronstiltsmodel(Levy, 1976),non-sexablesmallcrickets(HFL 10mm)were evenlydistributedamongthebaits,whilelargeadult(HFL 20mm)andmedium(HFL10–19mm)cricketswere preferentiallyfoundinthehighercaloriebaits.Thesesizerelateddifferencessuggestthatsmallcricketsdonotforage fortheoptimumcaloricpay-off,butstoptofeedatthefirst availablefoodstuff.Theseresultsalsoshowthatmedium andlargecricketsdoselectforhighercaloriefoodstuffs basedonodor,butarenotabletoselectthehighestcalorie food.Databygenderformediumandlargecricketsshow nearlyequalnumbersofmalesandfemalesattractedtothe 100%and50%PBbaits. Figure8. Hadenoecus cavecricketcropwallshavechitinous structuresforgrindingandmixingfood,andlargenumbers ofresidentbacteria. T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 124 N JournalofCaveandKarstStudies, April2007

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Understandingtheextentofthedistanceawayfroman entrancethatcavecricketsforageisanimportant considerationincavemanagement.Ifthecricketsarethe baseofthefoodinputintothecave,effortshavetobe madetoensurethattheyhavesuitablehabitatforforaging. Tayloretal.(2005)usedUVbrightpainttomarkabout 2000 C.secretus outofabout15,000astheyexitedatnight fromBigRedCaveinTexasinlatespringandsummer 2003.TheresearchersusedUVlightstolocatemarked cricketsonthesurfaceoveratotalof17samplingnights. Thelocationofall291cricketsonthesurface(markedand unmarked)wasrecordedwithGPSandaflag,andlater measuredandmapped.Abouthalfthecrickets(51.1%) werelocatedwithin40moftheentrance.Densitieswere uniformouttoabout80m,andsome(8.1%)werelocated upto105mfromtheentrance,whichismuchgreaterthan expected.Onaverage,adultswerefoundfurtherfromthe entrancethansub-adults,andnomale:femaledifferencesin distributionwerenoted.Cricketsweretypicallyfoundclose totheground,andalmostevenlydistributedingrasses,leaf litter,orherbaceousvegetation,althoughtheauthors notedthatthevegetationtype,suchascacti,mayhave influencedsearchefforts.Inadditiontomanagingsuitable foragingenvironmentsaroundentrances,theauthors notedtheneedtocontrolfireantsintheseareas. F ORAGING A ND P REDATION R ISK Duringaforagingboutonthesurface,cavecrickets likelyusetheirprodigiousjumpingabilityastheirprimary meansofescapefrompredators.However,cavecrickets’ highlydistensiblecropenablesthemtoincreasetheirweight bymorethan 200%whichcouldcompromisetheir jumpingabilityandthustheirmeansofescapingfrom predators.Helf(2003)showedthatincreasingcropfullness compromisedlargecavecrickets’jumpingability(Fig.9). Thus,cavecricketforagingdecisionsmaybebasedonthe tradeoffbetweenfoodintakeandbioticfactorswiththe strongestimpact(e.g.,perceivedpredationriskorcompetition). Helf(2003)hypothesizedthattheadvantageafullcrop conveystoanadultcricketwouldbeoutweighedbythe negativeeffectsithasontheirjumpingabilityand predictedtherewouldbeanegativecorrelationbetween howmuchfoodlargecavecricketseatatbaitpatchesand itsdistancefromacaveentrance.Helf(2003)usedcolorcodedbaitpatchesplacedatdifferentdistancesfromcave entrancestoexaminewhateffect H.subterraneus perceived riskofbeingeatenhasontheirforagingbehavior.Thedata fromtheseexperiments,numbers,sizes,andfullnessof cricketsthatfedatthebaitpatchesonagivennight,were obtainedbycensusingandweighingcoloredcricketsinthe cavethedayfollowingaforagingbout.Therewasno significantdifferenceinfoodintakeamongbaitpatch distances.Thedatasuggestthatcricketforagingbehavior wasnotaffectedbypredationrisk.Averagefoodintakeat allpatchdistances(ca.100%ofbodyweight)werewell belowcricketcropcapacityof 200%. Helf(2005)foundaggregativeresponsestofoodpatches in Ceuthophilussecretus ,awidespreadspeciesincentral Texas,canalsoleadtointenseintraspecificcompetition (Fig.10).Helf(2005)usedbaitpatchescenteredoncave entrancesatthefourcardinaldirectionssetjustoutside caveentrances,at5m,andat10mawaytoexaminethe foragingbehaviorof C.secretus atsixcavesinGovernment CanyonStateNaturalArea(GCSNA)inSanAntonio, Texas.Duringsummerandfallmonthstheamountoffood consumedby C.secretus declinedsignificantlyasafunction ofpatchdistancefromcaveentrances.Videotapedforaging boutsshowedfierceintraspecificcompetitionamong C. secretus atbaitpatches.Therewasasignificantpositive Table1. H.subterraneus capturedbysizeatthreedifferentenergylevelbaits. BaitLarge a Medium b Small c Total 100%Peanutbutterwith0%cornstarch18172257 50:50Peanutbutterandcornstarch13222358 0%Peanutbutterwith100%cornstarch212225 HFL HindFemurLength(DeLong1989). a Largecrickets HFL 20mm b Mediumcrickets HFL10–19mm c Smallcrickets HFL 10mm Figure9.Effectofcropfullnessonjumpingabilityof varioussizesof Hadenoecus cavecrickets.Errorbarsare 6 1 standarddeviation(Helf2003). K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 125

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correlationbetweentheirtimespentfeedinginbaitpatches andpatchdistance. RedImportedFireAnts( Solenopsisinvicta )were usuallyfoundinlargenumbersatfoodpatches,but 2003,adroughtyear,sawthelargestnumbersof S.invicta usingthebaitpatches.Similarly, C.secretus foodintakeat baitpatcheswashighestduring2003.GCSNAstafftreated S.invicta moundsathalfthestudycaveswithboilingwater thateffectivelyreducestheirnumber.Surprisingly, C. secretus consumedsignificantlylessfoodfrombaitpatches attreatedcavesrelativetountreatedcaves.Thesedata suggestthatatcaveswithreduced S.invicta numbers, C. secretus wasreleasedfrominterspecificcompetitionandso wasabletoexploitallavailablebaitpatches.Atuntreated caves, C.secretus increasedfoodintakewaslikelydueto theiravoidanceofdistantbaitpatchesbeingusedbygreat numbersof S.invicta .Overalltherewerefeweravailable baitpatchesbeingexploitedbymanycrickets.Onone occasiontherewasasignificantnegativecorrelation between C.secretus timespentfeedinginbaitpatches andpatchdistance(Helf,2005). Astudyofnumbersofthreespeciesof Ceuthophilus in threecentralTexascaveswasmadebyElliottandSprouse from1993to1999(Elliott,1994).LakelineCavewas heavilyimpactedbyconstructionofamall,whichleftan undisturbedareaaroundthecaveentranceofonly0.9ha (2.3ac)incomparisontotwoothercavesinlarge undisturbedareas.CavecricketnumbersinLakelineCave showedasteadydeclinewithtimewhilepopulationsinthe othertwocavesremainedstable.Thesecricketsgenerally forage50–60mfromacaveentrance,showingtheneedfor alargerundisturbedareaaroundtheentrance. M OVEMENTAND E LONGATED A PPENDAGES Elongatedappendagesandgracileappearanceare widelyregardedastroglomorphiccharacteristicsofcave animals.Elongatedappendages,particularlyantennae, Figure10.Intenseintraspecificcompetitionamong Ceuthophilussecretus atbaitpatches. T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 126 N JournalofCaveandKarstStudies, April2007

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couldincreasesensoryperception,whileelongatedlegs maybeanadaptationforwalkingonirregularsurfacesin totaldarkness(i.e.,inathree-dimensionaldarkmazewhere steppingacrossgapsmaybesaferthanjumpingorwalking around).Elongatedappendagesalsocouldbeanadaptationformetaboliceconomy;withlongerlegs,theanimal couldmovefartherwitheachstep.ContinuingLevy’s (1976)scavengeronstiltsconcept,longlegsandantennae allowcricketstoreachabovesurfaceboundarylayersto detectfoodormatesbetter.Vandel(1965)generalizesvery broadlythatcavernicolouscricketsshowextremeappendageelongation,evenwithinagroupthattendstohavelong appendages. Studieretal.(2002)didastudyoflegattenuationin arangeofcaveandsurfacecrickets.Whenpossible,they measuredarangeofsizesofindividualsofeachspeciesand foundthatarelationshipexistsbetweenbodymassand alinearmeasurementofhindfemurlength.Inboth H. subterraneus and C.stygius ,therelationshipsdiffer betweensexes,withadultfemalesroutinelybeingheavier thanadultmalesofsimilarHFL.With H.subterraneus ,the relationshipsalsodifferbyseason.Individualsofsimilar HFLarelightestinthespringandheaviestinthefall.We havealimitedamountofinformationfromotherspecies, butadultsofthethree Ceuthophilus speciesfromCarlsbad andthethree Caconemobius speciesfromHawaiigenerally fittheproposedmodel.Anattenuationindexoftheratio ofcropemptyliveweighttohindfemurlength,cubed (CELW/HFL 3 )inverselyranksthestudiedcricketspecies totheirlevelofadaptationtoacavernicolousexistence, andisproposedasapotentiallyusefulnon-lethal quantitativeindicatoroftheextentofcaveadaptationin crickets(Table2). Jumpingbehaviorin H.subterraneus wasstudiedby Sevick(unpublisheddata).Heusedaphotographicsystem withastrobelighttoevaluatethecricketjumpingresponse toathreat.Thepicturesrevealsomethingquiteunexpected;thecricketssomersaultduringtheirescapejump. Hethoughtthatthesomersaultallowsthecrickettomake contactwiththeundersideofaledgeortheceilingofthe cave,whicharesaferplacestoavoidpredatorsthanjust landingonthefloorseveralcentimetersawayfromwhereit started. Theevasivebehaviorof H.subterraneus hasalsobeen studied.Individualcavecricketswerecapturedandtested inthecavebyforcingthemtohoptoexhaustion(Fig.11), definedasbeingunresponsivetotouch(Mason,1989). Cricketswithlongerhindfemurshoppedgreaterdistances bothperhopandcumulatively,whiletheamountoffood inthecropreducedthehoplength,butnotthetotal distancehopped.Inwinter1988,32adultcricketswith HFL 20mm,hoppedanaverageof11.5 6 0.6times (range7–20hops).Theaveragehoplengthwas36.7 6 1.2cm(range23.8–46.9cm)foratotalaveragedistance hoppedof419 6 1.2cm(range212–898cm).Timeto exhaustionwas15.3 6 0.2seconds(range8–24seconds). Thecompassdirectionoftheinitialandsubsequenthops wererandom.Comparingwintertosummer,crickets showedanincreasedabilitytohopforalongertimeand totaldistance,althoughtheaveragehoplengthremained thesame. Helf(2003)measuredtheimpactofsurfacetemperature onlarge H.subterraneus locomotoryabilitybymeasuring thedistancetheywalkedandjumpedoversixtysecondsat atemperatureconducivetoforaging(9 u C)andatemperaturethatprecludedforaging(3 u C).Therewasasignificant decreaseinthedistancewalkedbylargecricketsfrom9 u C to3 u C.Nostatisticalcomparisonwasevenpossiblefor jumpingabilitybetween9 u Cand3 u Cbecausecrickets couldnotjumpduringthe3 u Ctrials.Asanectotherm, H. Table2.Averagesofranges[inbrackets]ofhindfemurlength(HFL),cropemptyliveweight(CELW),andattenuationindex (CELW/HFL 3 )forcricketspecies,bothRhaphidophoridaeandGryllidae. Species Cave status Number Location CELW,mg (S.E.) HFL,mm (S.E.) Attenuation IndexCELW/HFL 3 Rhaphidophoridae Hadenoecussubterraneus TP425KY[11.3–556.8][7–25]0.0334[0.0296–0.0380] Ceuthophiluslongipes TP21NM120.2(0.1)12.6(0.1)0.0602 Ceuthophilusstygius EP/TX247KY[108.5–1338][10–25]0.0996[0.0508–0.1214] Ceuthophilusconicaudus EP/TX20NM166(9.3)10.2(0.2)0.1546 Ceuthophiluscarlsbadensis EP/TX29NM283.6(0.1)11.5(0.1)0.1879 Gryllidae Caconemobiusvarius TB19HI34.0(2.4)6.1(0.1)0.1474 Caconemobiusfori EP/TX19HI59.4(0.1)7.2(0.2)0.1571 Caconemobiussandwichensis EP14HI80.9(4.0)7.4(0.2)0.1998 Grylluspennsylvanicus EP20MI291.7(0.1)10.1(0.1)0.2831 Achetadomestica EP20???142.2(4.0)7.4(0.2)0.3543 Valuesinparenthesesarestandarderrors.Cricketsarerankedspecifica llybyattenuationindexandindecreasingorderbystatusofcaveadaptati onwhereTB troglobite, TP troglophile,TX trogloxene,andEP epigean.(Studier etal .,2002). K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 127

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subterraneus cannotrespondtothenegativeeffectoflow surfacetemperatures,soitwaitsinsidethecaveforbetter conditions. IntheMammothCaveentrancebiomonitoringstudy, Poulson,HelfandLavoieexpressedconcernaboutplansto developgatesforsomeentrancestotheMammothCave system.Theuseofairlockdoorswouldeliminatethe eveningmovementof H.subterraneus outofthecaveto forageandtheirmorningreturntoroostsinthecaves.We wantedtoknowwhatsizeopeningswouldneedtobeleft aroundgatestopermitfreemovementofcavecrickets. Fourlargeadultcricketswereplacedinafiberglass windowscreenbagattachedtoPVCtubingofdifferent lengthsandshapes.Thebagswereplacedhorizontallyon thegroundandthenumberofcricketsremainingafterone hourand12hourswasnoted.Adiameterof1 inwasthe minimumthatallowedforfreemovementofadultcrickets. Theshapeofthetubinghadnoappreciableeffecton cricketmovement,sobafflingthetubesshouldbepossible toreduceairflowwithoutanegativeeffectoncrickets.We recommendedthatseveralopeningsbeincludedinthe designofairlockgates,withasingle3–4inopeninglow downformovementofcaverats( Neotoma spp.)and multipleopeningsof1 inclosertotheceilingforcrickets. Salamanderscouldmakeuseofanyoftheseopenings.The ParkServiceagreed.Caveswithgatedbatentranceswould alreadyallowfreemovementofcricketsandrats,andwere notpartoftheserecommendedmodifications. C RICKETS A S P REY Ifyouhaveeverwatchedanatureshow,youhave probablynoticedthatmanythingsliketoeatcricketsand grasshoppers.Cavecricketsarenoexception.Insidethe cave,theyarepreyeduponbyspidersandsalamanders.In somecaves,specializedbeetlespreyoncricketeggsand injuredyoungcrickets.Outsidethecave,cricketsareeaten bymanyanimals,inparticular,mice.InTexascaves Ceuthophilus areeatenbymanyspeciesincludingascorpion andaspider.Inadditiondeadcricketsarescavengedby arovebeetle,aharvestman,andspringtails,ifother cricketsdonotfindthemfirst. Acavesandbeetle, Neaphaenopstellkampfi ,isaspecializedpredatoroncricketeggsinKentucky.Some aspectsoftherelationshipbetweencricketsandbeetles havebeenwellstudied(Poulson,1975;Nortonetal., 1975;KaneandPoulson,1976;Griffith,1991).Beetlesdig inareasofsandysoilthathavebeendisturbedby oviposition.Ithasbeensuggestedthatfemalecrickets fromcaveswithpopulationsofbeetleshaveco-evolvedto havelongerovipositorsthanfemalesfromun-predated populations(HubbellandNorton1978).Thedifferenceis onlyonemillimeter,butinsertingeggsthatmuchdeeper decreasestheriskoftheeggbeingfoundbyasandbeetle. Inlaboratorystudies,Griffith(1991)carefullymeasured thedepthofburiedcricketeggsandthedepthofholes dugbybeetles.Theoverlapofgraphsshowedthatbeetles arelikelytofindonly25%ofeggslaid.Areducedharvest rateduetolower,seasonalcricketeggavailabilitywas shownbyGriffithandPoulson(1993)todecreasebeetle fecundity.Cavecricketeggsthatescapepredationhatch intonymphsthatmovetotheceilingwheretheyareless vulnerabletopredators(Nortonetal.,1975).Asimilar situationofcoevolutionorparallelevolutionbetween predatorandpreyisseenintheCumberlandPlateauarea, involving H.cumberlandicus andadifferentspeciesofcave beetle, Darlingtoneakentuckensis (HubbellandNorton, 1978;Marsh,1969), Ceuthophilus inTexasby Rhadine subterranea (Mitchell,1968). Ceuthophilusmaculatus ,acavecricket,maybean intermediatehostforanintestinalparasiteofmice.Fish (1974)studiedthefoodoftwospeciesofmeadowmice ( Microtus sp.),anddeterminedthatthemicewouldeat thesecricketswhentheyencounteredtheminaconfined space.Themicediscardedthehardpartsofthecrickets, eatingonlyinternalorgans.Thelackofidentifiablecricket partsinthestomachsofthemicemayhaveledresearchers tounderestimatetheuseofinsectsinthediet. Theuseofcaveentrancesbymice (Peromyscus leucopus )asareliablesourceoffoodintheformofcave cricketswasstudiedbyVieleandStudier(1990).Atsome entrances,numbersofexitingcricketscanbeinthe hundredsoreventhousandspernight.VieleandStudier setupagridoftrapsaroundtheentrancetoasmall, biologicallyrichcaveinMammothCaveNationalPark calledWhiteCave.Shermanlivetrapsweresetat10m intervalsandbaitedwithpeanutbutter.Trapsweresetat nightandcheckedinthemorningforseveraldays.Trapped miceweremarkedtoidentifyspecificindividualsandthen released.Thedatawereplottedtodeterminethehome rangeofeachtrappedmouse.Onlyfourwhite-footeddeer Figure11.Exhausted Hadenoecus cavecricketdoesnot respondtotouchandisunabletouseitshindlegsforjumping (musclesareintetany). T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 128 N JournalofCaveandKarstStudies, April2007

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Figure12.Shermanlivetrapgridof90livetrapsatGreatOnyxcave6–8June ,1996.Theuppergridwascenteredonthe caveentranceusedbycricketsandthelowergridwassetinsimilarterrain withoutacaveentranceseveralhundredmeters awayfromthecavegrid.Alltrapsinthegridwere10mfromthenextnearestt rap.Marksindicatecapturesofwhite-footed mice( Peromyscusleucopus ).Connectedpointsandcircleswithan‘X’indicatemultiplecapturesofo neindividual(Helf2003). K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 129

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micewerecaptured,butthehomerangesofthreeofthe micewerenotrandomlyorevenlydistributed.Threeofthe micehadhomerangesthatoverlappedatthecave entrance,indicatingtheimportanceofthecaveentrance tothemice. Helf(2003)examinedtheeffectofacaveentrance activelyusedbyforaging H.subterraneus onthedensityof P.leucopus atGreatOnyxCaveinMammothCave NationalPark.Helfseta90-trapgridcenteredonthe caveentrancewithanother90-trapgridsetseveralhundred metersawayinsimilarterrainwithoutacaveentrance. Helf(2003)found26 P.leucopus individualswithin50mof thecaveentrancewhereasonlysix P.leucopus individuals werefoundinthecontrolarea(Fig.12).Helfconcluded thatsuchhigh P.leucopus densities,sincetheyare insectivorous,couldaffectthelocalcommunityaround caveentrances. Studier(1996)measuredthesize,mass,nitrogenand mineralconcentrationsofcrop-freecarcassesof H. subterraneus ,theireggs,andtheeggpredatorsandbeetle, Neaphaenopstellkampfi .Bodymagnesium,iron,and nitrogenconcentrationsdecreasewithsizeinthecave crickets,andaccumulationofthesemineralsoccursvery slowlyinhatchlingcavecrickets.Nutrientsneededforegg growthgreatlyexceedneedsofthecricketforgrowth. Comparedtocricketeggs,thebeetlescontainsimilar concentrationsofironandcalcium,lowerconcentrations ofmagnesiumandpotassium,andhigherconcentrationsof nitrogenandsodium.Growthratesofbodymassin cricketsisaboutone-tenththegrowthexpectedforepigean insects,sonitrogenandmineralaccumulationsarelikewise expectedtobeveryslow. Asinglecricketeggrepresentsabout75%ofthemassof a N.tellkampfi ,makingitahugemeal.Basedonaweightlossstudyinthelaboratory(GriffithandPoulson,1993), asinglecricketeggwillsustainabeetlefor2–3weeks beforeithastobeginusingbodyfatreserves(Fig.13).As anexampleofyouarewhatyoueat,thenitrogenand mineralcompositionofthe N.tellkampfi carcassisquite differentfromlevelsfoundinotherbeetles,andmuchmore similartothatofcavecricketeggs(Studier,1996). Female H.subterraneus exhibittwostrategiestoavoid eggpredation.Onestrategyispredatorsatiation,inwhich timingofeggproductionresultsinanoverabundanceof eggsforashortduration.Predatorsbecomesatiatedduring thisshortperiod,andthesurvivingyoungquicklygrow beyondasizeeasilyhandledbythepredator(Smith,1986). Onecricketeggcompletelysatiatesasandbeetlefor approximatelyaweekortwo(Nortonetal.,1975;Griffith andPoulson,1993).Areductioninpredationratesis associatedatthepopulationlevelwithhigheggdensities (KaneandPoulson,1976).Thesecondpredatoravoidance strategyinvolvesmakinglargenumbersofovipositorholes toincreasesearchtimefor Neaphaenops beetles,which preferentiallydiginareasofdisturbedsubstrate.Caged cricketsconsistentlymademoreovipositorholesthaneggs laid.Bothofthesestrategiesmayincreaseeggsurvivalrate. Ovipositedeggshaveaminimalhatchingsuccessrateof 82.6%,withanapproximatetimetohatchingof12weeks, whichagreeswithestimatesbyHubbellandNorton(1978). Femalesmayalsobetestingthesoilforsuitableconditions ofeggdevelopment.Noneoftheseexplanationsis mutuallyexclusive. Ten-metertransects(32.8fttransects)ofnineentrances inMammothCaveNationalParkwerecensusedregularly from1995–1997bytheauthors.Allentranceshad Nesticus spidersorasimilar-sizedspider,whileonlyfivehad populationsofthelargeorb-weaver Metaamericana (Fig.14).Atthefiveentranceswith Meta ,therewas apositivecorrelationbetweenspidernumberandreproduction,andcavecricketabundancebothintransects inacaveandbetweencaves.Thisfindingsuggeststhat cricketpreynumbershaveastronginfluenceonsuccessof thespiderpredator. Fungimayhavethepotentialtoreducecavecricket populations.Inastudyoftheinternalandexternalspecies offungiassociatedwithatrogloxeniccavecricket, Hadenoecuscumberlandicus ,Benoitetal.(2004)isolated arangeofsoilsaprophytesthatyouwouldexpecttofindin acave.Twointernalisolateswerespeciesofplant pathogenicfungi,whichtheyattributedtofeeding.One externalisolatewasagenusoffungusthatisaninsect pathogen.Presencealonedoesnotindicateactivity,butwe occasionallyobservedeadcricketscoveredinawhite myceliumof Isariadensa (Cali,1897).Werefertothemas cricketmarshmallows,forobviousreasons(Fig.15).We arenotsureifthefunguskillsthecricketorgrowsonit afterthecricketdies,butitiscertainlypresentatthetime ofdeath.Thefungusisinaracewithcricketsandother scavengersforthecarcass. Figure13.Masslossin Neaphaenops sandbeetles(mean / SD).Solidcirclesrepresentmasslossinthelaboratory afterconsumingasinglecricketegg(distended).Opencircles arefieldmasses,placedonanextendedline(—)ataslopeof 0.031mg/dthatequalstheaveragerateofmasslossofnondistendedbeetles(GriffithandPoulson1993). T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 130 N JournalofCaveandKarstStudies, April2007

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C AVE C RICKETS A S K EYSTONE S PECIES Thecavecricketisoftenconsideredadominantspecies incaveecosystemsbecauseofthelargenumbersof individualsandtheircontributiontothefoodbasein manycaves.Cavecricketsenhancebiodiversityinfoodlimitedcavesbyacombinationoftheirfeces,eggs,and deadbodies.Thismighthavebeenpredictedjustbytheir highimportancevalueasbyfarthelargest,themost numerous,andthehighestmetabolicratespeciesincaves wheretheyoccur.Theiractualcontributiontobiodiversity hasonlybeenwellstudiedinTexascavesbyMitchell (MohrandPoulson,1966)andinKentucky(Poulson, 1992). IntheMammothCaveareatheirguanounderentrance roostsonlyoccasionallyhastherightmoisturetosupport averydiversecommunity,buttheirscatteredfecesaway fromentrancessupportacommunitythatincludessomeof themosttroglomorphicspringtails,beetles,millipedes,and spiders.Inaddition,theireggsareeatenbyacarabidbeetle, Neaphaenopstellkampfii ,whichoccursinhighdensities wherecricketslaymostoftheireggsinsandyorsilty substratesawayfromentrances.ThebeetleÂ’sfecesinturn supportamoderatelydiversecommunitythatincludes springtails,mites,apseudoscorpion,adipluran,andaspider. InTexascaves Ceuthophilus guanocanalsobean importantcommunityfoodbase,supportingpopulations oftroglobitesandtroglophiles(S.Taylor,personal communication).And,thoughnotstudied,thefecesof acarabidbeetle(Rhadine)thateatscricketeggsare certainlythebasisofanothercommunity. Long-termstudiesofcavecricketguanocommunitiesin twosmallcavesinMammothCaveNationalParkshow largefluctuationsinthenumbersofanimalscensusedover 24yearsbetween1971and1994(Fig.16).Poulsonetal. (1995)posefourhypothesestoexplaintheobserved variation.Thefirsthypothesisisthatanthropogenic disturbancesbycavetourscausethecricketstomovetheir rooststootherareas,thuspreventingrenewaloftheguano. Afterconsideringthefrequency,groupsize,andpath Figure14. Metaamericana spiderwithweb.Theselargespidersareabletocatchandconsumeadultcav ecrickets. K ATHLEEN H.L AVOIE ,K URT L.H ELF AND T HOMAS L.P OULSON JournalofCaveandKarstStudies, April2007 N 131

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followedbytourgroups,werejectedthishypothesis.A secondhypothesisisthatweatherdirectlyaffectstheguano, makingittoodryortwomoisttosupporttheguano community.Thishypothesisisrejectedbecausethedataare notconsistentwiththemodel.Thethirdhypothesisisthat weatherchangedthecavemicroclimate,causingthecrickets toroostelsewhere,whichreducesguanoinputtothe community.However,wehaveobservedthatcricketsdo keepthesameroostsforlongperiodsoftime,andnew guanocommunitiesarenotestablishedelsewhere. Thefinalhypothesis,andtheonesupportedby observations,isthatweathereffectsareindirectlyseenon theguanocommunitiesbecauseweatherforceschangein cricketforaging,guanodeposition,andcricketsurvival. Datacomparingspeciesdiversityandabundanceofthe guanocommunitywithanincreaseincricketnumbers coincidedwithaperiodoffavorableweather.Poorsurface weatherconditionsnegativelyaffectcricketforagingand thetrophiccascadebasedonguanoresupply. P ERSPECTIVES Cavecricketsareoftenimportantkeystonespeciesthat supportcaveecosystemsbyproductionofeggs,carcasses, andguanothatserveasthefoodbaseinmanycaves.Tom Poulsonisfondofusingthephrase,MysteriesoftheCave, whendiscussingsomethingwejustdon’tunderstandabout cavesandcavelife.Thechallengeoffieldresearchistofind answerstothesemysteries(Poulson,1996).Anyresearch projectinthefieldcanbeahumblingexperience.You reviewwhatyouknow,developalternatehypothesesto test,think,plan,andplanagain,getyourmaterials together,builddevices,traveltothefieldsite,andthen nothingworksasyouplanned.Generally,mostexperimentsrequiretwoormoremodifications,andplentyof ducttape,beforetheywork.Cavecricketresearchisno exception.Althoughweknowalotaboutafewspecies, therearestilltremendousopportunitiesforfurtherstudyof cavecricketsinordertosolvemoremysteriesofthecave. A CKNOWLEDGEMENTS WededicatethispapertothememoryofEugeneH. Studier,colleagueandfriend.Wethankthemanyindividualswhohaveworkedwithusovertheyearsonourfield work.SpecialthankstoNationalParkServicepersonnel andstudentsfromtheUniversityofIllinoisatChicago,the UniversityofMichigan-Flint,andtheStateUniversityof NewYorkCollegeatPlattsburgh.RickOlsonandJohn FreyoftheNPSparticipatedinmanycensuscounts.We thankCRFforuseoftheirfieldfacilitiesinKentuckyand NewMexico.Thelong-termbiomonitoringstudywas fundedbyNRP.TheauthorswouldliketothankS.Sevick forpreparationofthephotographshowninFigure1;the photographbyWilliamHullshowninFigure2;the photographbyRickOlsonshowninFigure14;andthe photographbyDianaNorthupshowninFigure15. R EFERENCES Ahearn,G.A.,andHowarth,F.G.,1982,Physiologyofcavearthropodsin Hawaii:JournalofExperimentalZoology,v.222,p.227–238. Altman,P.L.,andDittmer,D.S.,1972,Biologydatabook,2nded.: Bethesda,MD,FederationofAmericanSocietiesforExperimental Biology,p.156–157. Figure15.Cricketmarshmallow:Adead H.subterraneus cricketsurroundedbyadensewhitefungalmycelium. Figure16.Changesinabundanceofcavecricketguano communityorganismsinWhiteCaveover24yearsfrom 1971–1994(Poulson etal., 1995). T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 132 N JournalofCaveandKarstStudies, April2007

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Poulson,T.L.,1996,Researchaimedatmanagementproblemsshouldbe hypothesis-driven:CasestudiesintheMammothCaveregion, in Rea, G.T.,ed.,Proceedingsofthe1995NationalCaveManagement Symposium,SpringMillStatePark,Mitchell,Indiana,Indianapolis, IndianaKarstConservancy,p.267–273. Poulson,T.L.,Helf,K.,andLavoie,K.H.,1998,Distributionand abundanceofcavecricketsatMammothCaveNationalParkdueto weatherfrom1995to1997andentranceretrofittingin1996[abs.]: JournalofCaveandKarstStudies,v.60,no.3,p.181. Poulson,T.L.,Lavoie,K.H.,andHelf,K.,1998,Cavecricketsat MammothCaveNationalPark:Sourceandsinkpopulationdynamics [abs.]:JournalofCaveandKarstStudies,v.60,no.3,p.181. Poulson,T.L.,Lavoie,K.H.,andHelf,K.,1995,Long-termeffectsof weatheronthecricketguanocommunityinMammothCaveNational Park:AmericanMidlandNaturalist,v.134,p.226–236. Richards,A.M.,1971,Anecologicalstudyofthecavernicolousfaunaof theNullarborPlain,southernAustralia:JournalofZoology,v.164, p.1–60. Schneider,S.H.,1989,TheGreenhouseEffect:ScienceandPolicy: Science,v.243,p.771–781. Smith,R.L.,1986,Elementsofecology,2nded.,p.328–333:NewYork, HarperandRowPublishers. Studier,E.H.,1996,Compositionofbodiesofcavecrickets( Hadenoecus subterraneus ),theireggs,andtheireggpredator, Neaphaenops tellkampfi :TheAmericanMidlandNaturalist,v.136,p.101–109. Studier,E.H.,andLavoie,K.H.,1990,Biologyofcavecrickets, Hadenoecussubterraneus ,andcamelcrickets, Ceuthophilusstygius (Insecta:Orthoptera):Metabolismandwatereconomiesrelatedtosize andtemperature:ComparativeBiochemistryandPhysiology,v.95A, p.157–161. Studier,E.H.,Lavoie,K.H.,andChandler,C.M.,1991,Biologyofcave crickets, Hadenoecussubterraneus ,andcamelcrickets, Ceuthophilus stygius (Insecta:Orthoptera):Parasitismbyhairworms:Proceedings oftheHelminthologicalSocietyofWashington,v.58,no.2, p.244–246. Studier,E.H.,Lavoie,K.H.,andHowarth,F.G.,2002,Legattenuation andseasonalfemurlength:massrelationshipsincavernicolous crickets(Orthoptera:GryllidaeandRhaphidophoridae):Journalof CaveandKarstStudies,v.64,no.2,p.126–131. Studier,E.H.,Lavoie,K.H.,Nevin,D.R.,andMcMillin,K.L.,1988, Seasonalindividualsizedistributionsandmortalityofpopulationsof cavecrickets, Hadenoecussubterraneus :CaveResearchFoundation AnnualReport,p.42–44. Studier,E.H.,Lavoie,K.H.,Wares,II.,W.D.,andLinn,J.A.-M.,1986, Bioenergeticsofthecavecricket, Hadenoecussubterraneus :ComparativeBiochemistryandPhysiology,v.83A,p.431–436. Studier,E.H.,Lavoie,K.H.,Wares,II.,W.D.,andLinn,J.A.-M.,1987a, Bioenergeticsofthecamelcricket, Ceuthophilusstygius :Comparative BiochemistryandPhysiology,v.86A,p.289–293. Studier,E.H.,Wares,II.,W.D.,Lavoie,K.H.,andLinn,J.A.-M.,1987b, Waterbudgetsofcavecrickets, Hadenoecussubterraneus andcamel crickets, Ceuthophilusstygius :ComparativeBiochemistryandPhysiology,v.86A,p.295–300. Taylor,S.J.,Krejca,J.,andDenight,M.L.,2005,Foragingandrange habitatuseof Ceuthophilussecretus (Orthoptera:Rhaphidophoridae), akeytrogloxeneinCentralTexascavecommunities:American MidlandNaturalist,v.154,p.97–114. Vandel,A.,1965,Biospeleology:Thebiologyofcavernicolousanimals (Translatedfromthe1964FrencheditionbyFreeman,B.E.):Oxford, PergamonPress,524p. Viele,D.P.,andStudier,E.H.,1990,Useofalocalizedfoodsourceby Peromyscusleucopus ,determinedwithanhexagonalgrid:Bulletinof theNationalSpeleologicalSociety,v.52,no.1,p.52–53. White,C.R.,1989,Digestiveenzymesofthecavecricket, Hadenoecus subterraneus :1988CaveResearchFoundationAnn.Report,p.61– 63. Yoder,J.A.,Hobbs,III,H.H.,andHazelton,M.C.,2002,Aggregate protectionagainstdehydrationinadultfemalesofthecavecricket, Hadenoecuscumberlandicus :JournalofCaveandKarstStudies,v.64, no.2,p.140–144. T HEBIOLOGYANDECOLOGYOFNORTHAMERICANCAVECRICKETS 134 N JournalofCaveandKarstStudies, April2007



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ZOOGEOGRAPHYANDBIODIVERSITYOFMISSOURI CAVESANDKARST W ILLIAM R.E LLIOTT MissouriDepartmentofConservation,ResourceScienceDivision,2901We stTrumanBoulevard,JeffersonCity,MO65102-0180,Bill.Elliot@mdc.mo .gov A BSTRACT : TheMissouriCaveLifeDatabasecontains927speciesandabout12,500 observationandcollectionrecords.About1,038(17%)ofMissouri’s6,20 0cavesand cavespringsarebiocaveswithatleastonespeciesrecord,butonly491sit es(8%)have fiveormorespeciesrecorded.Missourihas82troglobites(67described, 15undescribed), including49aquaticand33terrestrialspecies.Theaquaticsinclude30d escribedandsix undescribedstygobites,plus13describedphreatobites.Theterrestria lsinclude24 describedandnineundescribedspecies.Sixofthetroglobites(fourdesc ribed)may actuallybetroglophiles,edaphobitesorneotroglobites.Thereareabou t215troglophiles (17aquatic),203trogloxenes(20aquatic)and407accidentalsorofuncer tainecological classification(27aquatic). KarstzoogeographicregionsincludethebroadSpringfieldandSalemplat eaus;the Boone,Hannibal,St.Louis,Jefferson-Ste.Genevieve,andPerryvilleka rsts;andan isolatedarea,CaneyMountain.Troglobitesarecurrentlyknownfrom728M issourisites, including597caves(10%ofknowncaves).Twenty-fivetroglobites,eight ofwhichare newspecies,occuratsinglesitesonly.Missourishares48troglobiteswi thotherstates, exhibitingrelativelylowdiversityinterrestrialtroglobitescompare dtoareaseastofthe MississippiRiver,buthighaquaticbiodiversity. Valuesforspeciesrichness(SR),troglobites,siteendemism(SE)andbio diversity(B) werederivedtorankandcomparecavesforconservationplanning.Manyspe ciesand biologicallyimportantbiocaveswereaddedtotheMissouriNaturalHerit ageDatabase andtheComprehensiveWildlifeConservationStrategy,along-range,sta tewide conservationplan.Furtherworkshouldfocusonpoorlyknownregions. I NTRODUCTION Thepurposeofthispaperistosummarizeandanalyze dataderivedfromtheCaveLifeDatabase(CLD),which theauthordevelopedattheMissouriDepartmentof Conservation(MDC)totrackMissouri’scavefauna.Peck andLewis(1978)comparedtheeasternMissouricave faunatoIllinoisandotherregions,andtheyextensively discussedtheoriginsandrelationsofthefaunas.An updatedoverviewoftheState’scavezoogeographyis provided,butthefocusofthispaperismoreoncave biodiversityandhowtoprioritizecavesforconservation planning. ThepurposeoftheCLDistobringtogetherall pertinentchecklistsanddatasourcesintoarelational database.TheCLDdrawsonpublishedandunpublished recordsfromthescientificliterature,agencyreports, speleologicalliterature,databases(suchastheMissouri NaturalHeritageDatabase),andunpublishedrecordsfrom experiencedobserversandbiologists.Thedatabaseisused totrackcollectionsandobservations,toproducechecklists foranycave,county,ortaxon,andtostudyzoogeography, biodiversityandconservationissues.Theanalyseshelpin recognizingknowledgegaps,planningstudiesandwildlife conservationwork,drawingspeciesrangemaps,updating theNaturalHeritageDatabaseanddevelopingeducational materialsandpublications. TheCLDistoolargetopublishhere,sosummary statistics,analyses,tables,maps,photographsandspecies checklistsareprovidedforthetopthreecavesfor biodiversity.Readersmaycontacttheauthorforchecklists andspecializedreports. L ITERATURE R EVIEW Missouricaves(Figs.1and2)arementionedinsomeof theearliestAmericanbiospeleologicalliterature.Girard (1852,1859)reportedoncavecrayfishesanddescribed Typhlichthyssubterraneus (theSoutherncavefish)from Kentucky;thespecieswaslaterfoundinMissouri.Ruth Hoppin(Hoppin,1889)senthercollectionofOzark cavefishfromSarcoxieCave,JasperCounty,in1888to HarvardprofessorsSamuelGarman(Garman,1889)and WalterFaxon.Faxon(1889)described Cambarussetosus theBristlyCaveCrayfish(Fig.3).Schwarz(1891)describedthebeetle, Ptomaphaguscavernicola ,fromMarvel (Marble)Cave,StoneCounty,anditalsowascollectedin 1897byC.H.MerriaminHamiltonCave,Washington County.Stejneger(1892)describedtheGrottosalamander, Typhlotritonspelaeus (now Euryceaspelaea accordingto W.R.Elliott–ZoogeographyandbiodiversityofMissouricavesandkarst. JournalofCaveandKarstStudies, v.69,no.1,p.135–162. JournalofCaveandKarstStudies, April2007 N 135

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BonettandChippindale,2004).Eigenmann(1898,1899, 1901,1909)describedtheOzarkcavefish, Amblyopsisrosae (Fig.4),andpublishedmanyotherpapersonMissouri cavefishandsalamanders. Thefirstthirdofthe20 th centurysawfewreportson Missouricavelife.Atroglophilicspiderwasreportedby Crosby(1905)fromRocheport(Boone)Cave,Boone County;lateritwasdescribedas Cicurinacavealis by BishopandCrosby(1926).J.W.Mackeldencollectedthe GrottosalamanderfromMarbleCave,OregonCounty,in 1906.A.D.Newmancollectedamphipodsfromawellat Harrisonville,CassCounty,from1915–1917.Unknown collectorsworkedinTalkingRocksCavern(FairyCave), StoneCounty,in1919.Grottosalamandersweretakenin SarcoxieCavein1927,apparentlybyB.C.Marshall,and byE.P.CreaserandE.B.Williamsonfromseveralcavesin 1929–1930.Theseearlyrecordscamefromseveralmuseum catalogs. Inthesecondthirdofthe20 th century,Hubbell(1934, 1936)publishedmanydescriptionsof Ceuthophilus crickets (Fig.5),includingfivespeciesinMissouricaves.The legendaryLeslieHubrichtstudiedmanycavesandsprings from1931to1969.Hefoundanddescribednumerousnew speciesofamphipods,isopods,andaquaticsnails(Hubricht,1940,1941,1942,1943,1950,1959,1971,1972; HubrichtandMackin,1940,1949).KennethDearolfand Hubrichtcollectedfourspeciesofmillipedesin1938,which weredescribedbyLoomis(1939),including Causeyella Figure1.Missourikarstmapshowingthethreeprincipalagesofdolomites andlimestones,karstzoogeographicregionsand thetoptenbiocaves.1)TumblingCreekCave,TaneyCounty;2)Devil’sIceb oxCave,BooneCounty;3)MysteryCave,Perry County;4)BeromeMooreCave,PerryCounty;5)RiverCave,CamdenCounty;6 )BransonCave,ShannonCounty;7)Kohms Cave,Ste.GenevieveCounty;8)TomMooreCave,PerryCounty;9)JaggedCan yonCave,CrawfordCounty;10)GreatScott Cave,WashingtonCounty. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 136 N JournalofCaveandKarstStudies, April2007

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dendropus (Fig.6),awidespreadtroglobite.Hubricht publishedthefirstgeneralpaperonOzarkcaveinvertebratesin1950.Hyman(1945,1956)describedtheflatworms Sphalloplanahubrichti fromIllinoisandMissouri, and Macrocotylaglandulosa fromDevilÂ’sIceboxCave, BooneCounty. Macrocotyla wasplacedundertheolder genusname, Kenkia (SluysandKawakatsu,2006). KennethChristiansencollectedspringtailsin42Missouri cavesbetween1950and1986,andheprovidedmanyother identifications(Christiansen,1964,1966)(Table1).ThomasC.Barr,Jr.studiedsevencavesin1958and1965,andhe describedandidentifiednumerousbeetles.Causey(1960) providedakeytosixspeciesofmillipedes,twoofthem troglobites. Inthelastthirdofthe20 th centurycaveresearch increasedasmorespeleologistsbecameactive.JohnR. HolsingermadefourcollectingtripstoMissouribetween 1964and1988,visiting30cavesandspringsinsearchof amphipodsandhydrobiidsnails,attimeswithRusty NortonandRobertHershler(Holsinger,1967,1971, 1989).In1999theauthorworkedinthefieldwith HolsingerÂ’sPh.D.student,StefanKoenemann,andUlrike Englischinsearchof Bactrurus amphipods(Koenemann andHolsinger,2001).Thesetripsandpapersprovided amonographonthesystematicsof Stygobromus (then Stygonectes );descriptionsof S.barri,S.ozarkensis,Allocrangonyxhubrichti and Bactruruspseudomucronatus ;the newfamilyAllocrangonyctidae;andnewlocalityrecordsfor Figure2.Cavedensitybycounty(about6,000caves)andbiocaves(about90 0). W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 137

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S.alabamensis,S.clantoni and B.brachycaudus .Newspecies ofMissouri Stygobromus willbedescribedinthenearfuture. In1966ThomasJ.AleypurchasedTumblingCreek Cave(BearCave),TaneyCounty,andbegantheOzark UndergroundLaboratory,whichsponsoredmanyscientificstudiesoverthenext40years(AleyandThomson,1971; ThomsonandAley,1971;Hershleretal.,1990;Elliottet al.,2005;ElliottandAley2006).JohnL.Craigstudied caveinvertebrates,focusingoncavesthreatenedbythe proposedMeramecParkLakeineasternMissouri(Craig, 1975,1977).LaValetal.(1977)completedanevaluationof batcavesintheproposedMeramecParkLakeandUnion Lakeprojectareas.Manyimportantcaveswouldhave beeninundatedbytheMeramecLake.Thesestudies,along withreportsfromcaverDonRimbachandothers, influencedpublicopinion,andtheprojectsdiedforseveral reasons,includingimminentlossofscenicandrecreational values. Lewis(1974)extensivelystudiedMysteryCave,Perry County,oneofthetopthreeMissouricavesforbiodiversity.Kenk(1975,1977)describedtheflatworms Macrocotyla (now Kenkia ) lewisi and Sphalloplanaevaginata fromPerryCounty;thelatterwaslaterfoundin CamdenCountybySlayetal.(2006).PeckandLewis (1978)comparedtherichnessofeasternMissouricavesto Illinoisandotherareas.Christiansen(1983)analyzedcave CollembolapatternsacrosstheeasternUSA. Since1978MDCÂ’sRichardClawsoncontributed voluminouscensusdataonbatsfrom103cavesandthree minesin38counties,primarilyofendangeredGrayand Indianabats(Table1). From1978to1984,MDCÂ’sJamesE.(Gene)Gardner collectednumerousinvertebratespecimensfrom436caves and10springs,providingimportantbaselineinformation onsubterraneanbiodiversityandthecoredataintheCLD Figure3. Cambarussetosus, Bristlycavecrayfish,Turnback Cave,LawrenceCounty,Missouri. Figure4. Ambyopsisrosae ,Ozarkcavefish,BenLassiterCave, McDonaldCounty. Figure5. Ceuthophilusgracilipes ,afemalecamelcricket. Figure6. Causeyelladendropus (formerly Scoterpes ),SmallinCave,ChristianCounty. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 138 N JournalofCaveandKarstStudies, April2007

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(Gardner,1985,1986)(Table1).Gardnerworkedwith manyagenciesandlandownerstostudytheircavelifeand providemanagementrecommendations.Helisted414 invertebratespecies,ofwhich52species(13%)were consideredtroglobites(39described,13undescribed).The numbersofotherecologicaltypeswereuncertainbecause oflimitedecologicaldata,butwereintherangeof90–130 troglophiles(25–31%),135–167trogloxenes(32–40%)and 142accidentals(34%).NocomprehensivelistofMissouri’s cavevertebrateshasbeenpublished,butacomputer printoutwithalargenumberofobservationswas contributedbyGardnertotheCLD. MDC’sNaturalHistoryDivisionprovidedmany observationstotheNaturalHeritageDatabasefrom 1985–2006,andthesewereimportedintotheCLD. KoppelmanandFigg(1993)publishedapreliminarystudy onthegeneticsofcavecrayfish.WilliamPfliegerpublished importantsummariesofMissouricrayfishes(Pflieger, 1996)andfishes(Pflieger,1997),includingcaveforms. ManyotherMDCstaffparticipatedincavestudies(see Acknowledgments). OeschandOesch(1986)studiedcavesatFortLeonard Wood,PulaskiCounty.ElliottandClawson(2001)studied thetemperaturesofIndianaandGraybatcaves,including FortLeonardWood.TaylorandSlay(pers.comm.) conducteddetailedcaveinvertebratesurveysatFort LeonardWood. MichaelJ.Suttonstudiedatleast174cavesin21 countiesfortheCaveResearchFoundation,mostlyinthe MarkTwainNationalForestandtheOzarkNational ScenicRiverways(Sutton,1993,1998,1999).Healso conductedacensusstudy(2004)ofthePinkPlanarian, Kenkiaglandulosa, inDevil’sIceboxCave,BooneCounty, astygobiteuniquetothatcave.Thespeciesisthreatened bywaterpollution,anditappearstohavevariable populationsize.Suttoncontributedmanyinvertebrate identificationsandobservations(Table1).In2005and 2006,SuttonandSueHagan( pers.comm. )discoveredan undescribedspeciesoftrechinebeetle, Pseudanophthalmus, about5mmlong,inBransonCaveandRoundSpring Cavern,ShannonCounty.ThomasC.Barr,Jr.isstudying thisspecies,whichwouldbethethirdspeciesoftroglobitic beetleinMissouri. DavidC.Ashleystudiedatleast57cavesin17counties withhisstudentsfromMissouriWesternStateUniversity andotherssince1993(Ashley,1993,1996,2003).The studiesincludedbioinventory,communityecology,and manycavesnailcensusesoftheendangered Antrobiaculveri inTumblingCreekCave,TaneyCounty(Table1).Ashley andElliott(2000)providedanoverviewofMissouricave life. Lewis(2002,2004)described Chaetaspisaleyorum apolydesmoidmillipede,and Brackenridgiaashleyi, atrichoniscidisopod,fromTumblingCreekCave.Shear (2003)redescribed Scoterpesdendropus ,placingitinthe newgenus Causeyella ,whichcontainstwootherspeciesin Arkansas. Populationestimatesoftheendangered Antrobia culveri, TumblingCreekCavesnail(Fig.7),byAshley andPaulMcKenzie,UnitedStatesFishandWildlife Service(USFWS),havedocumentedtheirdeclinesince 1996(Ashley2003,U.S.DepartmentoftheInterior2001, 2003).TheTumblingCreekCavesnailWorkingGroupwas foundedbyPaulMcKenzietobringtogetherexpertsfrom theregion. Elliott(2000a,2000b,2001,2003a,2003b,2004,2005, 2006b)joinedMDCin1998,andheworkedwitheight researchpartnersandotherstostudyMissouri’scavelife (seeAcknowledgments).Hecollectedabout1,800invertebratespecimensin130caves,springs,wellsand minesin36Missouricounties,andheobservedan aggregateof860,000animals(1,525,000withassistants). In1999histeamdiscoveredanewspeciesofcavecrayfish, Orconectesstygocaneyi (Fig.8),fromCaneyMountain ConservationArea,asignificantadditiontoourunderstandingofcavecrayfishsystematicsandzoogeography (Hobbs,2001).ElliottandIreland(2002)ledayear-long studyof40caves,involvingmembersoftheMissouri CavesandKarstConservancy.ElliottandAshley(2005) characterizedMissouricaveandkarstcommunities.MDC Table1.PrincipalcontributorstotheCaveLifeDatabase,startingwithG ardner’s1986study.Christiansencollectedan unknownnumberofCollembolarepresenting28species. CollectorObservedCollectedSitesCounties D.Ashleyandstudents5,2001,2005717 K.Christiansen(Collembola)4224 R.Clawson(Chiroptera)9,680,00010635 W.R.Elliottandassistants1,525,0001,80013036 J.E.Gardner390,0004,50044641 M.Sutton483,000 1,00017421 Exclusivetotals16,207,494 12,50096063 Caves647615 Counties5461 W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 139

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cavebiologyinterns,MichaelE.Slay,StephenT. Samoray,SaraGardner,andresidentcaveecologist, JamesE.Kaufmann,contributed860invertebratespecimensandcountedatotalof1,050,000bats,mostlyusing near-infraredvideo(Elliottetal.,2006);theyalsocounted about260othervertebrates.Slayetal.(2006)and Graeningetal.(2006)providednewdataonplanarians and Cambarussetosus intheOzarks. M ATERIALSAND M ETHODS D ATABASE D ESIGN In1998theauthorbeganworkontheCLDforMDC usingaspeciesdatabasethathehadpreviouslydesignedin Texas.Significantamountsofdatawereaddedwiththe helpofresearchpartnersandassistantssince1999 (Table1).Additionalresearchpartnersrecentlyjoined theproject.Thedesignisfrequentlyupgraded,andthe authorisinterestedincollaboratingwithotherstatesthat maywanttoexpandthedatabasetotheirareas. Alargedatabaseofcavelifeimagesalsowasdeveloped, someofwhichispostedonthe Biospeleology website (Elliott,2007).Theimagedatabaseconsistsofhundredsof scannedanddigitalphotographs,mostlyinjpegformat, maintainedintheACDSee H programbyACDSystems, Inc.Adescriptionfieldholdspertinentdataabouteach image,includingthecave,county,state,subject,photographer,dateandkeywords.Imagesmaybefoundby searchingfolders,filenames,orwordsinthedescription field.Thisprogramhasaself-maintainingdatabase function.Manyofthesephotosareavailableforscientific andeducationaluse. TheCLDwasdevelopedusingMicrosoftAccess H aWindows H application.TheCLDisarelationaldatabase withthreecentralrelations:thetablesSpeciesand Localities,andaqueryobject,UniqueCaveNames,which isbasedontheLocalitiestable.Thisquerycouldbe replacedinthefuturebyatableofofficialcavenames derivedfromtheMissouriSpeleologicalSurvey;however, thequeryfunctionswellintrackingknowncounty/cave namecombinations,newcavenamesthatarenotyet registeredwiththeMissouriSpeleologicalSurvey(MSS), and279noncaves,suchaswells,mines,smallersprings, andsomeepigean(surface)sites. Arelationaldatabaseisasoftwaresystemthatties togetherrelateddatathroughcertainkeyfieldsheldin common,suchascountyandcavename,speciesnumber, caveaccessionnumberandsoon.Thistypeofdatabaseis usedforeverythingfrompartsinventoriestobiological data.Spacedoesnotallowacompletedescriptionofallthe manyfieldsandobjectsintheCLD,butsuchisavailable fromtheauthoronrequest. TheSpeciestable,with31fields,containsextensive taxonomicandecologicalinformationabouteachspecies, includingpublishedremarksofvariousauthors.Notations canbeadded.Theconservationstatusofthespeciesinthe MissouriSpeciesandCommunitiesofConservationConcern (MissouriDepartmentofConservation,2005)checklistis notedintheStatusfield,includingwhetheritisathreatened orendangeredspeciesontheMissouriorFederallists.The StatusfieldmatchesinformationinNatureServeÂ’snational NaturalHeritageDatabase,andproposeddatacanbe recordedthereforspeciesthatarenotyetintheHeritage system.Ifaspeciesisrevisedtaxonomically,thosechanges aremadeonetimeintheappropriatefields.Eachspeciesis assignedauniqueSpnum(speciesnumber),whichisused torelateittotheLocalitiestableinaone-to-many relationship.Thus,basictaxonomicinformationdoesnot Figure7. Antrobiaculveri ,TumblingCreekcavesnail,Taney County. Figure8. Orconectesstygocaneyi ,CaneyMountaincavecrayfish,OzarkCounty. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 140 N JournalofCaveandKarstStudies, April2007

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havetoberepeatedforeachnewlocalityrecord.Another field,ITIS,containstheIntegratedTaxonomicInformationSystemÂ’sTaxonomicSerialNumber(TSN),ifsuchhas beenassigned(U.S.DepartmentofAgriculture2006). Currently979speciesareintheSpeciestable,51ofwhich areplaceholdersforgenericidentifications,suchasunsortedcollectionor Stygobromussp. About927speciesare knownfromMissouricaves,82ofwhicharetroglobites (Table2),and57Spnumswereaddedforcooperativework withArkansas.Theauthor,asdatamanager,maintainsthe CLDwithdatafromcolleaguesandtheliterature.Anew versionisissuedoncompactdisctothepartnersonce ayear. TheLocalitiestable,with59fields,containsdataon observationsandcollections.Eachpartnerentersnewdata throughdataentryforms,viewingeitheronespeciesorone caveatatime.OnecanfindaspeciesanditsSpnumin severalways,thenenteritsSpnumforanewrecordwithin acave,inwhichcasethecountyandcavenameare automaticallyinsertedintherecord.Ifoneusesaspecies form,onecanfillinthecountyandcavename,thenthe Spnumforthatspeciesisautomaticallyinserted,thereby insuringthattheproperrelationismaintained.Newdata recordsareautomaticallytaggedsothatthedatamanager canseparatethemfromolddatawhentheuserssendin theirdata.Theusercaninputthedate,numberobserved, numbercollected,temperatures,namesofobservers,field notesandotherfields,whichallowonetorecordifan identificationistentative,specimenandvialnumbers, taxonomist,datecollectionsweresenttoataxonomist, museumcatalognumber,identificationdate,andother data.Thisprovidesacompletetrackingsystemforfield collectionsuntiltheyareindentifiedandcurated.Aspecial queryallowstheprintingofsmallspecimenlabels. Literaturerecordsmaybeenteredandthereferences included. Anothertable,CaveTrips,isrelatedtoUniqueCave Names,andisusedfortripreportsandpreliminarydata. Thesecanbeusedforinputtingapreliminaryreport,from whichausercanthencopydataintothemaintablesvia formsonthesamescreen. Manyquerieswerecreatedforspecialpurposes,and theycanbecopiedtospreadsheetsorageographic informationsystem(GIS)foranalysisandreformatting. Thequeriescanselectfewerfieldsorcompositemultiple speciesrecordsintopresence/absenceform.Trendsinbat colonysizecanbegraphedfromsuchqueries.Report formscanbeprintedforaparticularcave,areaortaxon,or senttoawordprocessorforediting.Thedesignallows expansionofthedatabasetootherstatesorcountries. TheCLDdoesnotincludeprecisecavelocationdata, butonlythecounty,cavenameandcaveaccessionnumber. OngoingcollaborationwiththeMSSandtheMissouri Caves&KarstConservancy(MCKC)enablestheCLDto betemporarilyrelatedtoastatecavedatabase,for zoogeographicanalysisandcavemanagement.Suchdata tablesareusedonlyinasecureGIS.Potentialuseswould becreatingspeciesrangemapsandmappingbiodiversity andconservationproblems.Suchproductsareimportant forenvironmentalreviewofconstructionprojectsthatmay threatencaveresourcesandgroundwater.InMissouri thesetoolswereusedformappingCaveFocusAreasfor long-termwildlifeconservationplanning(Elliott,2006). Theendproductsweremapsatscalesthatdonotreveal precisecavelocations.Manycavesaredegradedby individualswhohavediscoveredcavelocationsontheir own,butitisnotnecessarytoworsentheproblemby publicizingprecisecavelocations. B IODIVERSITY C OMPUTATIONS Forbiodiversitycomputationsinthispaper,Iinclude stygobites(aquatictroglobites)andphreatobitesunderthe generaltermtroglobiteortroglobiont,whichsomeauthors nowreserveforterrestrialtroglobites.InElliott(2003a) andthispaper,Iconsideraphreatobiteaninhabitantof groundwater,exhibitingtroglomorphy,butnotnecessarily limitedtokarstsystems.Manyauthorsmayprefertheterm stygobiteorstygobiontforallsubterranean,aquatic, troglomorphicspecies,andavoidthetermphreatobite. Limitedfundingforcaveconservationworkrequires thatweprioritizecaves.Onegoalwastoidentifycavesrich inspeciesandhighinendemismforlong-range,statewide, wildlifeconservationplanning(Elliott,2003b,2006). Generally,Missouricaveswithrare,endemicspeciesalso havemanyotherspecies,butthatisnotalwaysthecase. Troglobitesgenerallyarethemostendemiccavedwellers, whereastroglophilesoftenhavelargeranges,thereforethe focuswasontroglobitesandspeciesrichness. ForMDCÂ’sMissouriComprehensiveWildlifeConservationStrategyprojectin2004,importantbatcavesand largekarstspringsalsoweretakenintoaccountbecause theyrepresentimportantcomponentsinthekarstecosystem(Elliott,2006). Therearevariousmethodsformeasuringbiodiversity. Theauthordevelopedacavebiodiversityindexfor individualcavesbasedonthreeelementsthatcouldbe computedwithqueriesintheCLD: SR (speciesrichTable2.Ecologicaltypesofcave-dwellingspecies,described andundescribed.Includedastroglobitesare36stygobites,13 phreatobitesand6possibletroglophiles,edaphobitesor neotroglobites.Includedinthetroglophilecategoryare35 possibletrogloxenesand3possiblestygoxenes. EcologicalTypeTerrestrialAquaticTotal troglobites334982 troglophiles19817215 trogloxenes20320223 accidentals38027407 Totals814113927 W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 141

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Table3.TroglobitesandphreatobitesinMissouri(82total,15undescrib edinbold).A aquatic,T terrestrial.Endemismistheinverseofthenumberofsites. ScinameAuthorYearCommonNameEcoTypeHabitatSitesEndemism Allocrangonyxhubrichti Holsinger1971HubrichtÂ’slong-tailedamphipodPBA80.13 Amblyopsisrosae (Eigenmann)1897OzarkcavefishTBA440.02 Amnicolastygia Hubricht1971StygiancavesnailTBA20.50 Antrobiaculveri Hubricht1971TumblingCreekcavesnailTBA11.00 Apochthoniuscolecampi Muchmore1967ColecamppseudoscorpionTPorTBT30.33 Apochthoniusmysterius Muchmore1976MysteryCavepseudoscorpionTBT11.00 Apochthoniustyphlus Muchmore1967StoneCountycavepseudoscorpionTBT20.50 Arrhopalitesclarus Christiansen1966ClaruscavespringtailTBT80.13 Bactrurusbrachycaudus HubrichtandMackin1940Short-tailedground-water amphipod PBA880.01 Bactrurushubrichti Shoemaker1945Sword-tailedamphipodTBA11.00 Bactruruspseudomucronatus Koenemannand Holsinger 2001Falsesword-tailedcaveamphipodPBA230.04 Brackenridgiaashleyi LewistrichoniscidisopodTBT70.14 Caecidoteaancyla (Fleming)1972AncylacaveisopodTBA110.09 Caecidoteaantricola Creaser1931AntricolacaveisopodTBA1060.01 Caecidoteabeattyi LewisandBowman1981BeattyÂ’scaveisopodTBA20.50 Caecidoteadimorpha Mackinand Hubricht 1940DimorphicgroundwaterisopodPBA20.50 Caecidoteaextensolinguala Fleming1972St.FrancoisgroundwaterisopodPBA11.00 Caecidoteafustis Lewis1981FustiscaveisopodTBA160.06 Caecidoteakendeighi Steevesand Seidenberg 1971KendeighÂ’sgroundwaterisopodPBA11.00 Caecidotean.sp. DevilÂ’sIceboxCaveisopodTBA11.00 Caecidoteapackardi Mackinand Hubricht 1940PackardÂ’scaveisopodTBA11.00 Caecidoteasalemensis Lewis1981SalemcaveisopodTBA310.03 Caecidoteaserrata (Fleming)1972SerratedcaveisopodTBA20.50 Caecidoteasteevesi (Fleming)1972SteevesÂ’caveisopodTBA11.00 Caecidoteastiladactyla (Mackinand Hubricht) 1940Slender-fingeredcaveisopodTBA40.25 Caecidoteastygia Packard1871StygiancaveisopodTBA70.14 Cambarusaculabrum Hobbs&Brown1987cavecrayfishTBA11.00 Cambarushubrichti Hobbs1952SalemcavecrayfishTBA230.04 Cambarussetosus Faxon1889BristlycavecrayfishTBA440.02 Causeyelladendropus (Loomis)1939CauseyellacavemillipedeTBT140.07 Chaetaspisaleyorum Lewis2002AleysÂ’cavemillipedeTBT30.33 Cottussp.8 GrottosculpinTBA80.13 Crangonyxpackardi Smith1888PackardÂ’sgroundwater amphipod PBA50.20 Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 142 N JournalofCaveandKarstStudies, April2007

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Table3.Continued. ScinameAuthorYearCommonNameEcoTypeHabitatSitesEndemism Diacyclopsclandestinus YeatmanCopepodPBA11.00 Eumesocampan.sp. cavedipluranTBT60.17 Euryceaspelaea (Stejneger)1892GrottosalamanderTBA2000.01 Fontigensantroecetes (Hubricht)1940EnigmaticcavesnailTBA80.13 Fontigensproserpina (Hubricht)1940ProserpinecavesnailTBA50.20 HaplocampaorLitocampan.sp. 1 cavedipluranTBT50.20 HaplocampaorLitocampan.sp. 2 cavedipluranTBT11.00 HaplocampaorLitocampan.sp. 3 cavedipluranTBT11.00 Islandianaspeophila IviecavespiderTBT20.50 Kenkiaglandulosa (Hyman)1956PinkplanarianTBA11.00 Kenkialewisi Kenk1975LewisÂ’caveplanarianTBA30.33 Mundochthoniuscavernicolus Muchmore1968cavepseudoscorpionTBT11.00 Mundochthoniusn.sp.near cavernicolus cavepseudoscorpionTBT11.00 Oncopodurahoffi Christiansen& Bellinger 1980HoffÂ’scavespringtailTBT20.50 Oncopoduraiowae Christiansen1961SpringtailTPorTBT40.25 Onychiurusn.sp.nr.paro cavespringtailTBorTP?T11.00 Onychiurusn.sp.,nr. pseudofimetarius cavespringtailTBorTP?T50.20 Onychiurusobesus Mills1934ObesespringtailTPorTBT11.00 Orconectesstygocaneyi Hobbs2001CaneyMountaincavecrayfishTBA11.00 Phanettasubterranea (Emerton)1875cavespiderTBT30.33 Porrhommacavernicola (Keyserling)1886cavespiderTBT100.10 Pseudanophthalmusn.sp. Barr(inms)blindtrechinebeetleTBT20.50 Pseudosinellaespana Christiansen1961EspanacavespringtailTBT50.20 Pseudosinellasp.1,argentea group cavespringtailTBT80.13 Sinellaavita Christiansen1960AvitacavespringtailTBT30.33 Sinellabarri Christiansen1960BarrÂ’scavespringtailTBT30.33 Sinellacavernarum (Packard)CavernspringtailTPorTBT50.20 Spelobiatenebrarum (Aldrich)1897CavedungflyTBT900.01 Sphalloplanaevaginata Kenk1977PerryvillecaveplanarianTBA40.25 Sphalloplanahubrichti (Hyman)1945HubrichtÂ’scaveplanarianTBA30.33 Stygobromusn.sp.a Holsinger(inms)caveamphipodTBA11.00 W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 143

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Table3.Continued. ScinameAuthorYearCommonNameEcoTypeHabitatSitesEndemism Stygobromus alabamensisalabamensis (Stout)1911AlabamacaveamphipodPBA230.04 Stygobromusbarri (Holsinger)1967BarrÂ’sground-wateramphipodPBA30.33 Stygobromusclantoni (Creaser)1934ClantonÂ’sground-wateramphipodPBA20.50 Stygobromusn.sp.g Holsinger(inms)GardnerÂ’scaveamphipodTBA270.04 Stygobromus heteropodus (Hubricht)1943PickleSpringsamphipodPBA11.00 Stygobromusn.sp.2,onon.gp. caveamphipod,toberevisedTBA11.00 Stygobromusn.sp.3,onon.gp. caveamphipod,toberevisedTBA11.00 Stygobromusonondagaensis (HubrichtandMackin)1940OnondagaCaveamphipodTBA380.03 Stygobromusozarkensis (Holsinger)1967OzarkcaveamphipodTBA100.10 Stygobromussubtilis (Hubricht)1943Subtleground-wateramphipodPBA11.00 Tingupapallida Loomis1939TingupacavemillipedeTBT720.01 Tomocerusmissus Mills1949MissuscavespringtailTBT60.17 Typhlichthyssubterraneus Girard1859SoutherncavefishTBA290.03 Uncinocytherepholetera (HartandHobbs)1961caveostracodTBA11.00 Uncinocytherexania (HartandHobbs)1961caveostracodTBA11.00 Xenotrechuscondei BarrandKrekeler1967NorthernXenotrechuscavebeetleTBT20.50 Xenotrechusdenticollis BarrandKrekeler1967SouthernXenotrechuscavebeetleTBT20.50 Zosteractisinterminata Loomis1943ZosteractiscavemillipedeTBT50.20 Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 144 N JournalofCaveandKarstStudies, April2007

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Table4.SpecieschecklistforTumblingCreekCave,TaneyCounty,Missour i. RankSpeciesCommonNameTypeStatus 1 Agkistrodoncontortrix CopperheadAC 2 Antrobiaculveri TumblingCreekcavesnailTBS1G1G2 3 Arctoseiuscetratus Long-legsmallshinylongsnoutmiteAC 4 Arrhopalitesclarus ClaruscavespringtailTBS3G4 5 Arrhopalitespygmaeus springtailTP 6 Arrhopaliteswhitesidei springtailTP 7 Athetatroglophila rovebeetleTP 8 Bakerdaniasp. hairymiteAC 9 Banksinomasp. slenderknobby-leggedoribatidmite2AC 10 Bembidionsp. smallblackgroundbeetleTP 11 Brackenridgiaashleyi AshleyÂ’sisopodTBS2G2 12 Bradysiasp. dark-wingedfungusgnatTP 13 Caecidoteaancyla AncylacaveisopodTBS1G1G3? 14 Caecidoteaantricola AntricolacaveisopodTBS4G5 15 Calvoliasp. miteAC 16 Carpelimussp. rovebeetle 17 Castorcanadensis BeaverTX 18 Causeyelladendropus CauseyellacavemillipedeTBSUGNR 19 Ceratozetessp. wingedoribatidmiteAC 20 Ceuthophilusseclusus SecludedcamelcricketTX 21 Ceuthophilussilvestris ForestcamelcricketTX 22 Ceuthophilusuhleri UhlerÂ’scamelcricketTX 23 Chaetaspisaleyorum AleysÂ’cavemillipedeTBS1GNR 24 Cicurinacavealis CicurinaspiderTP 25 Crosbyellasp. harvestmanTPorTB? 26 Cottusbairdi MottledsculpinTX 27 Dendrolaelapsnearlatior short-legsmallshinylongsnoutmiteAC 28 Eptesicusfuscus BigbrownbatTX 29 Ereynetessp. smallvelvetmiteAC 30 Eurycealongicauda Dark-sidedsalamanderTP 31 Eurycealucifuga CavesalamanderTP 32 Euryceaspelaea GrottosalamanderTBS2S3G4 33 Ferrissiafragilis limpetTX 34 Folsomiacandida springtailTP 35 Hesperochernesoccidentalis guanopseudoscorpionTPS3G4G5 36 Histiosomasp. smalllumpymiteAC 37 Hoploscirussp. longsnoutvelvetmiteAC 38 Hydrasp. freshwaterhydra 39 Hypenahumili quadrifidmoth 40 Hypoaspissp. largeshinylongsnoutmiteAC 41 Iphidozerconreticaelatus smallsquatmiteAC 42 Islandianasp. cavespiderTPorTB? 43 Ixodessp. tick 44 Lasiurusborealis EasternredbatTX 45 Lasiuruscinereus HoarybatTX 46 Leptocerasp. smalldungfly 47 Leptoceratenebrarum dungflyTP? 48 Limoniusflavomarginatus clickbeetleTP 49 Lirceussp. LirceusisopodTPorTX? 50 Macroceranobilis webworm,fungusgnatTP 51 Macrochelespenicilliger brownshinymiteAC 52 Macronyssusjonesi blacksquatorhairyshinybatmiteAC W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 145

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Table4.Continued. RankSpeciesCommonNameTypeStatus 53 Monunguisnearstreblida largevelvetmiteAC 54 Multioppieasp. slenderknobby-leggedoribatidmite1AC 55 Myotisgrisescens GraybatTXS3G3SEFE 56 Myotislucifugus LittlebrownbatTX 57 Myotisseptentrionalis Northernlong-earedbatTXS3G4 58 Myotissodalis IndianabatTXS1G2SEFE 59 Neobisniussp. rovebeetleAC 60 Onychiurussp. springtailTP 61 Orconectesneglectusneglectus RingedcrayfishTX 62 Palaeacarussp. black-hairoribatidmiteAC 63 Physagyrina physidsnailTP? 64 Pipistrellussubflavus EasternpipistrelleTX 65 Platynustenuicollis largeblackgroundbeetleTP 66 Plesiodamalussp. hairyknobby-leggedoribatidmiteAC 67 Plusiocampasp. cavedipluran 68 Poecilochirusnecrophori Split-backshinymite 69 Poecilophysisweyerensis rhagidiidmiteTP 70 Polyaspissp. largesquatmiteAC 71 Proctolaelapshypudaei paleshinymiteAC 72 Pseudopolydesmuspinetorum polydesmidmillipedeTP 73 Pseudosinellaargentea springtailTP 74 Pseudozaonasp. pseudoscorpion 75 Psyllipsocusramburii booklouseTP 76 Ptomaphaguscavernicola caveleiodidbeetleTP 77 Ranapalustris PickerelfrogTX 78 Rhizoglyphussp. largeovalmiteAC 79 Sancassania?sp. tinyovalmiteAC 80 Semotilusatromaculatus CreekchubAC 81 Spelobiatenebrarum CavedungflyTB 82 Stigmaeussp. hairymediumovalmiteAC 83 Stygobromusonondagaensis OnondagaCaveamphipodTBS3?G5 84 Stygobromusozarkensis OzarkcaveamphipodTBS3?G4 85 Trichocerasp. wintercraneflyTX 86 Trombidiumsp. thin-leggedchiggermiteAC 87 Tyrophagussp. side-dotmiteAC 88 Undeterminedsp. genericamphipod,crangonyctid 89 Undeterminedsp. genericant,blackAC 90 Undeterminedsp. genericant,redAC 91 Undeterminedsp. genericbeetle,antlikeflowerAC 92 Undeterminedsp. genericbeetle,clickAC 93 Undeterminedsp. genericbeetle,darklingAC 94 Undeterminedsp. genericbeetle,dermestidlarvaAC 95 Undeterminedsp. genericbeetle,groundTP,TXor 96 Undeterminedsp. genericbeetle,roveTP? 97 Undeterminedsp. genericbeetle,wrinkledbarkAC 98 Undeterminedsp. genericbug,bedPR 99 Undeterminedsp. genericbug,jumpingground 100 Undeterminedsp. genericbug,true 101 Undeterminedsp. genericcentipedeTX 102 Undeterminedsp. genericcrayfish 103 Undeterminedsp. genericdipluranED 104 Undeterminedsp. genericfluke,MongeneaPR 105 Undeterminedsp. genericfly,mothTX Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 146 N JournalofCaveandKarstStudies, April2007

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nessornumberofallspeciesinthecave), T (number oftroglobites,stygobitesandphreatobites),and SE (siteendemism,whichistheaggregateoftroglobite endemismatthesite).Lackingtroglobitepopulation estimatesinmostcases,asimplemetricwasfoundfor comparinghowendemicaspeciesiswithinMissouri,as follows. SE e 1 where e (endemism)representsthereciprocalofthenumber ofknownMissourisites.Forexample,theGrotto salamander, Euryceaspelaea ,has200knownsitesin Missouri,so e 1 200 0 005 2 Thetotalnumberofsitesfor E.spelaea ,whichranges throughfourstatesintheOzarkregion,isnotcurrently published,however,forsuchaspeciestheendemismvalue becomessosmallastoberelativelyunimportantin calculatingacaveÂ’s SE .Onecouldalsousethe S or G valuesfromtheNaturalHeritageDatabase,butthese valuesarenotasup-to-dateanddonottakeintoaccount themanyundescribedspeciesthatareknowntocave biologists. Incontrast,theTumblingCreekcavesnail, Antrobia culveri ,isanendangeredspeciesknownfromonecave,so e 1 1 1 3 TumblingCreekCavehasan SE valueof2.92, representingtheaggregateendemismof12speciesof troglobites,atleasttwoofwhichareuniquetothatcave. So,themoreendemicacaveÂ’sfaunais,thehigherthe SE value. Torepresentallthreefactorsinonescorefor eachcave,theyweremultipliedtoobtainaBiodiversity Index B B SR T SE 4 whichisusedforrankingcavesforbiodiversity. B is dimensionless,andminordifferencesbetweencavesprobablyarenotsignificant. B simplyisawayofdigesting complexinformationintooneindexforbroadcomparisons. SE scoresalsowerecomputedforcertaincounties andkarstzoogeographicregions,whichonecouldcallarea endemism,toexaminethesuiteoftroglobiteswithin broaderareas. Onealsocouldadd SR,T and SE tocreateabiodiversityindex,however,theydonotscalethesameand SR usuallywouldbeoveremphasized.Onecantransform SE bymultiplyingitby10or100toobtainavalueinthe sameorderofmagnitudeas SR and T .However,theranks forthetopthreecaveswouldbethesameasmultiplying thethreefactors,althoughsomelowscoringcaveswould rankdifferently.Multiplicationofthefactorsprovides afairlybalancedemphasisof SR,T ,and SE Therelationsof SR,T ,and SE wereexaminedwith linearregressionsandone-wayANOVA.Allregressions werehighlysignificant( p 0.001),indicatingthat SE is highlydependentonhigh SR and T .Howeversome interestingoutliersresulted,whichdidnotconformwellto generaltrends.Somecaveswithhigh SR and T havemuch higher SE thanthegeneraltrendwouldpredict;examples areDevilÂ’sIceboxCave,BooneCounty;MysteryCave andBeromeMooreCave,PerryCounty;RiverCave, Camden;KohmÂ’sCave,Ste.GenevieveCounty;and BransonCave,ShannonCounty.Threeofthesecaves areineasternMissouri,wherethereishighcave RankSpeciesCommonNameTypeStatus 106 Undeterminedsp. genericgnat,fungusTXorTP? 107 Undeterminedsp. genericleafhopperAC 108 Undeterminedsp. genericmidge446TX 109 Undeterminedsp. genericmillipede 110 Undeterminedsp. genericmite,largevelvetAC 111 Undeterminedsp. genericmite,spinturnicidstarPR 112 Undeterminedsp. genericpseudoscorpion,small,white 113 Undeterminedsp. genericspider,pale 114 Undeterminedsp. genericspringtail,hugepigmentedAC? 115 Wespussp. harvestmanAC Manyofthecommonnamesgivenareinformalworkingnames.Ecologicaltype s:TB troglobite(includingstygobites),PB phreatobite(groundwaterforms),TP troglophile,TX trogloxene,AC accidental,ED edaphobite(soil-dweller),PR parasite.StatusisthatgivenintheMissouriNaturalHeritageDatabasea ndtheannual MissouriSpeciesandCommunitiesofConcernChecklist:S1iscriticallyi mperiledinthenationorstatebecauseofextremerarityorbecauseofsome factor(s)makingit especiallyvulnerabletoextirpationfromthestate,withtypicallyfive orfeweroccurrencesorveryfewremainingindividuals( 1000).G1issimilarontheglobalscale.S2and G2areimperiled,S3andG3arevulnerable,S4andG4areapparentlysecure. SEandFErefertostateandfederalendangeredstatus.ThosewithoutStatu shavenotbeenlisted orrated. Table4.Continued. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 147

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Table5.SpecieschecklistforDevilÂ’sIceboxCave,BooneCounty,Missour i. RankSpeciesCommonNameTypeStatus 1 Agabussp. predaceousdivingbeetleTP 2 Agkistrodoncontortrix CopperheadAC 3 Ambystomamaculatum SpottedsalamanderAC 4 Ambystomatexanum SmallmouthsalamanderTX 5 Arrhopalitespygmaeus springtailTP 6 Arrhopaliteswhitesidei springtailTP 7 Bactrurusbrachycaudus Short-tailedgroundwateramphipodPBS4G4 8 Bembidionsp. smallblackgroundbeetleTP 9 Brachinusamericanus groundbeetleAC 10 Bufoamericanus EasternAmericantoadTX 11 Caecidoteabrevicauda Short-tailedgroundwaterisopodTP 12 Caecidoteasp. Caecidoteaisopod,troglobiteTB 13 Cantharis?sp. soldierbeetleTX 14 Ceuthophilusseclusus SecludedcamelcricketTX 15 Ceuthophilussilvestris ForestcamelcricketTX 16 Chrysemyspictabellii WesternpaintedturtleAC 17 Crangonyxforbesi amphipodTP 18 Crangonyxpackardi PackardÂ’sgroundwateramphipodPB? 19 Crangonyxsp.,forbesigroup amphipodTP 20 Dinamicrostoma leechTP? 21 Dineutussp. whirligigbeetleAC 22 Dugesiadorotocephala planarianAC 23 Eptesicusfuscus BigbrownbatTX 24 Etheostomaspectabile Orange-throatdarterAC 25 Eurycealongicauda Dark-sidedsalamanderTP 26 Eurycealucifuga CavesalamanderTP 27 Euryceasp. EuryceasalamanderTP 28 Gammaruspseudolimnaeus amphipodTX 29 Hylaversicolor EasterngraytreefrogTX 30 Kenkiaglandulosa PinkplanarianTBS12G3 31 Lampropeltiscalligastercalligaster PrairiekingsnakeAC 32 Lepomismegalotis LongearsunfishAC 33 Macroceranobilis webworm,fungusgnatTP 34 Mustelavison minkTX 35 Myotisgrisescens GraybatTXS3G3SEFE 36 Myotislucifugus LittlebrownbatTX 37 Myotisseptentrionalis Northernlong-earedbatTXS3G4 38 Myotissodalis IndianabatTXS1G2SEFE 39 Oncopoduraiowae springtailTPorTB 40 Ondatrazibethicus MuskratAC 41 Onychiurusreluctus springtailTP 42 Orconectesvirilis NortherncrayfishTX 43 Physasp. physidsnailTP 44 Pipistrellussubflavus EasternpipistrelleTX 45 Placobdellasp. leechTX 46 Plethodonglutinosus SlimysalamanderTX 47 Porrhommacavernicola cavespiderTBS2G5 48 Procyonlotor RaccoonTX 49 Pseudacriscrucifercrucifer NorthernspringpeeperTX 50 Pseudacristriseriatatriseriata WesternchorusfrogAC 51 Pseudopolydesmussp. polydesmidmillipedeTP 52 Pseudosinellaargentea springtailTP 53 Ptomaphaguscavernicola caveleiodidbeetleTP Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 148 N JournalofCaveandKarstStudies, April2007

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endemism,however,theyhavereceivedextensivestudyby cavebiologists,sotheyprobablyhavehighervaluesas aresult.Ontheotherhand,someprominentcavesare deficientin SE despitehavingahigh SR ,suchasGreat ScottCave,WashingtonCounty;JaggedCanyonCave, BearCaveandOnondagaCave,CrawfordCounty;and GreatSpiritCave,PulaskiCounty.Fourofthefivelatter cavesareintheMeramecRiverbasin,butthatmaynotbe significant,andtheyprobablyhavenotreceivedasmuch studyasdeserved. R ESULTS H IGH B IODIVERSITY C AVES Currentlythereareabout12,500observationand collectionrecords.About1,038(17%)ofMissouriÂ’s approximately6,200cavesandcavespringsarebiocaves (atleastonespecies),butonly491sites(8%)havefiveor morespeciesrecorded.TheCLDhasdataon279other localities,suchassprings,wells,minesandsomesurface sites. Missourihas82troglobites(67described,15undescribed),including49aquaticand33terrestrialspecies (Tables2and3).Theaquaticsinclude30describedandsix undescribedstygobites,plus13describedphreatobites.The terrestrialsinclude24describedandnineundescribed species.Sixofthetroglobites(fourdescribed)maybe troglophiles,edaphobitesorneotroglobites.Thereare about215troglophiles(17aquatic),203trogloxenes(20 aquatic)and407speciesofuncertainecologicaltype(27 aquatic). Specieschecklistsareprovidedforthreeimportant biocaves:TumblingCreekCave,TaneyCounty(Table4); DevilÂ’sIceboxCave,BooneCounty(Table5);and MysteryCave,PerryCounty(Table6).TumblingCreek CaveranksfirstinMissouriforspeciesrichness(115 species),numberoftroglobites(12),andsiteendemism (2.9154),givingitanoverallBiodiversityValueof4,023.25 Table5.Continued. RankSpeciesCommonNameTypeStatus 54 Ranacatesbiana BullfrogAC 55 Ranaclamitans GreenfrogTX 56 Ranapalustris PickerelfrogTX 57 Scalopusaquaticus EasternmoleAC 58 Semotilusatromaculatus CreekchubAC 59 Spelobiatenebrarum CavedungflyTB 60 Thamnophissirtalissirtalis CommongartersnakeAC 61 Tingupapallida TingupacavemillipedeTBS4G4 62 Tomocerusmissus MissuscavespringtailTBSUG4 63 Undeterminedsp. genericamphipod 64 Undeterminedsp. genericbeetle 65 Undeterminedsp. genericbeetle,darklingAC 66 Undeterminedsp. genericbeetle,groundTP,TXor 67 Undeterminedsp. genericbeetle,hister 68 Undeterminedsp. genericbeetle,predaceousdivingAC 69 Undeterminedsp. genericbeetle,roveTP? 70 Undeterminedsp. genericcraneflyTX 71 Undeterminedsp. genericearthworm,lumbricidED 72 Undeterminedsp. genericfly 73 Undeterminedsp. genericfly,sciarid 74 Undeterminedsp. genericmite 75 Undeterminedsp. genericmite,oribatidAC? 76 Undeterminedsp. genericmite,rhagidiid 77 Undeterminedsp. genericspider 78 Undeterminedsp. genericspider,pale 79 Undeterminedsp. genericspringtail,entomobryid 80 Vononessayi harvestmanAC Manyofthecommonnamesgivenareinformalworkingnames.Ecologicaltype s:TB troglobite(includingstygobites),PB phreatobite(groundwaterforms),TP troglophile,TX trogloxene,AC accidental,ED edaphobite(soil-dweller),PR parasite.StatusisthatgivenintheMissouriNaturalHeritageDatabasea ndtheannual MissouriSpeciesandCommunitiesofConcernChecklist:S1iscriticallyi mperiledinthenationorstatebecauseofextremerarityorbecauseofsome factor(s)makingit especiallyvulnerabletoextirpationfromthestate,withtypicallyfive orfeweroccurrencesorveryfewremainingindividuals( 1000).G1issimilarontheglobalscale.S2and G2areimperiled,S3andG3arevulnerable,S4andG4areapparentlysecure. SEandFErefertostateandfederalendangeredstatus.ThosewithoutStatu shavenotbeenlisted orrated. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 149

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Table6.SpeciesChecklistforMysteryCave,PerryCounty,Missouri. RankSpeciesCommonNameTypeStatus 1 Agonumextensicolle groundbeetleAC 2 Ambystomatigrinumtigrinum tigersalamander 3 Amoebaleriadefessa heleomyzidflyTX 4 Anisodactylusopaculus groundbeetleAC 5 Apochthoniusmysterius MysteryCavepseudoscorpionTBS1G1G2 6 Armadillidiumvulgare pillbugisopodTX 7 Arrhopalitesclarus ClaruscavespringtailTBS3G4 8 Arrhopalitespygmaeus springtailTP 9 Athetasp.3 rovebeetleTP 10 Athetasp. rovebeetleTP 11 Atranuspubescens groundbeetleTP 12 Austrotylaspecus conotylidmillipedeTP 13 Bactrurusbrachycaudus Short-tailedgroundwateramphipodPBS4G4 14 Bembidiontexanum groundbeetleTP 15 Bimastostumidus earthwormED 16 Brachinusfumans groundbeetleAC 17 Caecidoteaantricola AntricolacaveisopodTBS4G5 18 Caecidoteabrevicauda Short-tailedgroundwaterisopodTP 19 Caecidotean.sp. CaecidoteaisopodTB 20 Caloglyphussp. acaridmiteTP? 21 Ceuthophiluselegans ElegantcamelcricketTX 22 Cottussp.8 GrottosculpinTBS2G1Q 23 Crangonyxforbesi amphipodTP 24 Cunaxasp. cunaxidmiteTP? 25 Dactylolabismontana craneflyTP 26 Dinamicrostoma leechTP? 27 Diplocardiasp. earthwormED 28 Eumesocampan.sp. cavedipluranTB 29 Fallicambarusfodiens diggercrayfishTX 30 Folsomiacandida springtailTP 31 Fontigensantroecetes EnigmaticcavesnailTBS2G2G3 32 Fontigenssp. cavesnailTP 33 Galeritabicolor groundbeetleAC 34 Gammurustroglophilus amphipodTP 35 Harpalusfulgens groundbeetleAC 36 Hawaiiaminiscula zonitidsnailTX 37 Hypogastruradenticulata springtailTP 38 Hypogastruramatura springtailACorTX? 39 Hypogastrurasp.,denticulatacomplex springtailTP 40 Isotomanotabilis springtailTP 41 Isotomasp. springtailTP 42 Isotomaviridis springtailTX 43 Kenkialewisi LewisÂ’caveplanarianTBS1G1 44 Lycoriellasp. sciaridflyTX 45 Metaovalis CaveorbweaverTP 46 Neobisniussp. rovebeetleAC 47 Oncopodurahoffi HoffÂ’scavespringtailTBS1S3G1G2 48 Paratachyssp.,corruscus groundbeetleAC 49 Pardosasp. lycosidspiderTX 50 Patrobuslongicornis groundbeetleTX? 51 Phagocatagracilis planarianTP 52 Physahalei HaleÂ’sPhysasnailTP 53 Pseudosinellaargentea springtailTP Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 150 N JournalofCaveandKarstStudies, April2007

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(Table7),butitsrankingcouldchangewithfurther studies.Dependingonbiodiversitymeasures,Tumbling CreekCavemayhavethehighestbiodiversityforasingle cavewestoftheMississippiRiver,rivaledbyToothCave andStovepipeCave,TravisCounty,Texas,andperhaps others(Elliott,1997;ElliottandAley,2006).However,the entireEdwardsAquiferinTexasrankshigherinbiodiversity(Longley,1981). K ARST Z OOGEOGRAPHY Althoughkarstregionsandcavefaunalunitswere namedbyearlierauthors,suchareaswereconceived differentlybyeach.PeckandLewis(1978),Dom(2002) andNighandSchroeder(2002)discussedkarstregions,but karstzoogeographicregionsinthispaperarebasedon acombinationoftroglobitezoogeography,physiography, geologyandkarsttype.Theseregionslacksharpboundariesbecauseofwide-rangingtroglobites. Troglobitesarecurrentlyknownfrom728Missouri sites,including597caves(9%ofknowncaves).Twenty-five troglobites,eightofwhicharenewspecies,occuratsingle sitesonly.Aninterestingexampleis Orconectesstygocaneyi (Fig.8),theCaneyMountaincavecrayfish,knownonly fromasmallcavewithaperchedaquiferonahighhill, geologicallyandhydrologicallyisolatedfromthemain SpringfieldandSalemplateaus.Astheonlystygobitic Orconectes westoftheMississippi,itsnearestrelativeis O. pellucidus fromKentucky(AshleyandElliott,2000; Hobbs,2001). Someaquaticspeciesarewide-ranging.Themost ubiquitoustroglobiteis Euryceaspelaea ,theGrotto salamander(Fig.9),with200knownsitesinMissouri, manyothersinArkansasandOklahoma,andonein Kansas.TheauthorconsiderstheGrottosalamanderas thetrademarkcavespeciesoftheOzarkRegion.Itis aneotroglobitethatmayhaveevolvedfromanancestor ecologicallysimilarto Eurycealucifuga (Fig.10),but withinthe E.multiplicata complex(BonettandChippindale,2004).Otherwide-rangingformsarethemillipede Tingupapallida andtheamphipod Stygobromusozarkensis (Fig.11);thelatterrangesacrossmostoftheOzarks (mostlycaves)intoKansas(wells),moreasaphreatobite thanastrictstygobite.Theisopod Caecidoteaantricola (Fig.12)hasanevenlargerrange.Theamphipod Allocrangonyxhubrichti wasconsideredararestygobite, butRobisonandHolsinger(2000)founditinanArkansas wellandSarverandLister(2004)founditin16epigean streamsin14Missouricounties.Individualsfromcaves typicallywerelargerthanthosefromepigeansites,which usuallyweregravelsubstratesinpools. Missourishares48troglobiteswithotherstates (Table8),hasrelativelylowdiversityinterrestrialtroglobitescomparedtoareaseastoftheMississippiRiver,but hashighaquaticbiodiversity.Thereisnearlyequal similaritytofaunaseastandwestoftheMississippiRiver. MissouriranksaboutseventhamongtheUnitedStatesin troglobiterichness(Table9). S PRINGFIELD P LATEAU Thisbroadkarstandphysiographicregion(Fig.1) compriseslimestonesofMississipianage,butithassmaller springsthantheSalemPlateau.Theplateaustretchesinto northernArkansas,northeasternOklahomaandthe southeasterncornerofKansas.Representativespeciesare Amblyopsisrosae ,theOzarkcavefish(44sites,Fig.4),and Cambarussetosus ,theBristlycavecrayfish(44sites, Fig.3),whichco-occurin16sites(22%).Subpopulations ofthesespeciesarefoundinsemi-isolatedpartsofthe aquifer.Thegeologicinfluenceoncavefishdistributions wasdiscussedbyNoltieandWicks(2001).Thereare21 troglobitesinthislargearea,withthesecondhighestarea endemisminMissouri.However,noneofthetop10 biocavesareinthisregion.TurnbackCave,Lawrence County,isthemostbiodiverse,with40species,seven troglobites(includingOzarkcavefishandBristlycave crayfish),butrelativelylow SE (Table7). B OONE K ARST ThiskarstisformedinMississippianlimestones,andit mightbeconsideredanextensionoftheSpringfield Plateau,alongtheMissouriRiverinBooneandadjacent counties.Thiskarstwasnotglaciatedduringthelatest (Wisconsin)glacial,butitmayhavebeenglaciatedduring theIllinoianandearlier.TheBooneKarstlackscavefish RankSpeciesCommonNameTypeStatus 54 Pseudosinellasp.1,argenteagroup cavespringtailTB 55 Rugilusdentatus rovebeetleAC 56 Stratiolaelapssp. laelapidmiteTP? 57 Undeterminedsp. genericbeetle,groundTP,TXor 58 Undeterminedsp. genericmite,laelapidTP? 59 Zonitoidesarboreus snailTPorTX? Manyofthecommonnamesgivenareinformalworkingnames.Ecologicaltype s:TB troglobite(includingstygobites),PB phreatobite(groundwaterforms),TP troglophile, TX trogloxene,AC accidental,ED edaphobite(soil-dweller),PR parasite.StatusisthatgivenintheMissouriNaturalHeritageDatabasea ndtheannualMissouriSpecies andCommunitiesofConcernChecklist:S1iscriticallyimperiledinthena tionorstatebecauseofextremerarityorbecauseofsomefactor(s)making itespeciallyvulnerableto extirpationfromthestate,withtypicallyfiveorfeweroccurrencesorve ryfewremainingindividuals( 1000).G1issimilarontheglobalscale.S2andG2areimperiled,S3andG3 arevulnerable,S4andG4areapparentlysecure.SEandFErefertostateand federalendangeredstatus.ThosewithoutStatushavenotbeenlistedorra ted. Table6.Continued. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 151

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Table7.Thetop50biocavesinMissourirankedbyoverallBiodiversityInd ex(B). RankCaveCounty SRTSEB 1TumblingCreekCaveTaney115122.91544,023.25 2DevilÂ’sIceboxCaveBoone8092.75301,982.18 3MysteryCavePerry59112.68751,744.16 4BeromeMooreCavePerry28102.0205565.75 5RiverCaveCamden4181.6800551.05 6BransonCaveShannon5471.1997453.48 7KohmsCaveSte.Genevieve3871.5208404.53 8TomMooreCavePerry3371.1811272.82 9JaggedCanyonCaveCrawford6470.4478200.63 10GreatScottCaveWashington5560.4222139.34 11BearCaveCrawford6250.4125127.88 12BrawleyCaveShannon2770.6110115.47 13KellyHollowCaveOregon2170.7829115.09 14ChimneyRockCaveBarry4070.4079114.22 15BoundsBranchCaveShannon2341.062397.73 16TurnbackCaveLawrence4070.331892.90 17PossumTrotHollowCaveShannon1841.051375.69 18BatCaveCrawford4240.435473.14 19RoundSpringCavernShannon2550.539467.43 20PantherCaveRipley1051.258562.93 21ZorumskiCavePhelps3021.032361.94 22CreechCaveLincoln2721.011454.61 23HamiltonSpringCaveWashington1560.601654.14 24TurnerSpringCaveOregon3850.262849.93 25FisherCaveFranklin2040.581746.54 26OldSpanishCaveStone1150.785943.22 27UpperCampYarnCaveCarter2250.372841.00 28MushroomCaveFranklin2540.405840.58 29SmallinCaveChristian941.108639.91 30MushroomRockCaveBarry1640.616139.43 31LewisCaveRipley841.091834.94 32CampBranchCaveWashington1131.035734.18 33DavisCaveShannon2750.251934.00 34PowderMillCreekCaveShannon3550.184232.24 35CooksCaveReynolds2720.576931.15 36RunningBullCavePerry850.775631.03 37GreatSpiritCavePulaski4640.165730.50 38OnondagaCaveCrawford5250.117130.46 39MossySpringCaveWashington2850.196527.51 40PipeSpringCaveOregon2360.190726.32 41LoneHillOnyxCaveFranklin3730.225024.98 42BatCaveShannon1950.260624.76 43WoodsCaveSt.Louis2340.256823.62 44MartinCaveShannon1740.339423.08 45WoodCaveChristian2950.155422.53 46GreenCaveWashington2730.262721.28 47MudCaveOzark1021.043520.87 48CreviceCavePerry1240.395819.00 49NewLibertyCaveOregon2360.119916.55 50RiceCaveJefferson850.402416.09 SR totalnumberofspeciesorspeciesrichness, T numberoftroglobitesandphreatobites, SE siteendemismvalue, B SR 3 T 3 SE Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 152 N JournalofCaveandKarstStudies, April2007

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andcavecrayfishanditscavefaunaisdifferent.DevilÂ’s IceboxCaveisalargecavewithanextensivesinkholeplain feedingitsstream,withtwoendemics, Kenkiaglandulosa thePinkPlanarian,andanew,undescribedspeciesof Caecidotea (Table5).Thesystemisnutrient-enrichedfrom sinkholeponds,suburbandevelopmentandlivestock,and ithasalargeGraybatcolonyandabundantcavelife. Otherlargecaves,suchasHunterÂ’sCaveandRocheport (Boone)Cave,havefewtroglobitesandarelargelyfedby epigeanwaters(Lerchetal.,2000).Theareahas10 troglobitesandmoderateendemism. H ANNIBAL K ARST ThiskarstisformedinMississippianrocksandsome DevonianandSilurianrocksnearHannibal,Marion County.Somewhatisolatedfromtheotherkarsts,ithas twocommontroglobites, Bactrurusbrachycaudus (Fig.13) and Tingupapallida ,butithasreceivedlittlestudy. L INCOLN H ILLS K ARST FormedinMississippianrocksalongtheLincolnFold inPikeandLincolncounties,thisregionhasthree troglobitesandamoderateamountofendemism: Bactrurusbrachycaudus,Caecidoteapackardi and Mundochthoniuscavernicolus. S ALEM P LATEAU Thisbroadareaismostlyadolomitickarstof Ordovicianage,withCambrianrocksringingthecentral OzarkDome,astructural,igneousfeatureknownastheSt. Figure9. Euryceaspelaea ,Grottosalamander,Tumbling CreekCave,TaneyCounty. Figure10. Eurycealucifuga ,thetroglophilicCavesalamander, KeyholeCave,ShannonCounty. Figure11. Stygobromusozarkensis ,TumblingCreekCave, TaneyCounty,isastygobitefoundintheSpringfieldPlateau ofsouthwesternMissouriandadjacentpartsofArkansas andOklahoma. Figure12. Caecidoteaantricola ,awidespreadphreatobite/ stygobite,CooksCave,ReynoldsCounty. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 153

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FrancoisMountains.Thisplateaucouldbedividedinto manykarstzoogeographicregions,particularlyriverbasins suchastheMeramec,Gasconade,Osage,Niangua, Current/JacksFork,ElevenPointandothers.However, interbasintransferofgroundwateriscommon,andthere areverylargerechargeareas,thereforestygobitescancross fromonebasintoanother.Forexample,therecordholding,long-distancedyetraceintheUSAranfor64km toBigSpring,CarterCounty(Aley,2000). Highbiodiversityisfoundinsomecavessuchas TumblingCreekCave,TaneyCounty,andBransonCave, ShannonCounty.Acavefish/crayfishpairco-occursin nine(21%)of52caves: Typhlichthyssubterraneus ,Southern cavefish(29sites),and Cambarushubrichti ,Salemcave crayfish(23sites).Thesetwostygobitesareabsentfrom somestreamcaves,eventhoughtheymayoccurinsprings nearby(e.g.,PowderMillCreekCave,ShannonCounty). Anewspeciesoftroglobiticcarabidbeetle,TribeTrechini, wasrecentlyfoundintwocavesneartheCurrentRiver,the first Pseudanophthalmus westoftheMississippiRiverand alinktoeasternfaunas(MichaelJ.SuttonandTomBarr, Jr.,pers.comm.).Thethreekarstregionsbelowcanbe consideredeasternsubdivisionsofthemainSalemPlateau, separatedfromitbytheSt.FrancoisMountains. S T .L OUIS K ARST NighandSchroeder(2002)recognizedtheFlorissant KarstandtheSt.LouisKarst,basedonsurfacevegetation, soilsandgeology,buttheyarelumpedtogetherhere,as thereisnodistinctionincavezoogeography.WoodsCave containsawidespreadspeciesthatisrareinMissouri, Caecidoteastygia. Manyofthecaveshavebeenobliterated byurbanization.Nevertheless,thereare11troglobitesand Table9.Thetoptenstatesintroglobitebiodiversity(describedspecies ).DatafromHobbs,CulverandElliott(2006)andthe CLD.Missourihasatotalof82troglobites(67described,15undescribed) ,including49aquaticand33terrestrialspecies.The aquaticsinclude31describedand6undescribedstygobites,plus13descr ibedphreatobites.Theterrestrialsinclude24described and9undescribedspecies. RankStateStygobitesPhreatobitesTerrestrialTroglobitesTotal 1Texas582119179 2Tennessee401120161 3Alabama232120145 4Virginia381289139 5Kentucky29090119 6WestVirginia3214275 7Missouri31132468 8Indiana2233257 9California874257 10Georgia1602440 Table8.Troglobitesandphreatobitessharedbetween Missouriandotherstates.Numberssharedwithregionseast andwestoftheMississippiareforthoseregionsasawhole. StateSpecies Arkansas22 Iowa4 Kansas7 Oklahoma14 WestofMississippi31 WestofMississippionly23 Illinois22 Indiana10 Kentucky10 Tennessee9 WestVirginia1 EastofMississippi26 Widespreadbothsides6 Missourionly34 TotalsharedwithMissouri48 Figure13. Bactrurusbrachycaudus ,aphreatobite,DevilÂ’s IceboxCave. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 154 N JournalofCaveandKarstStudies, April2007

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slightlymoreareaendemismthantheLincolnHillstothe north.PeckandLewis(1978)recognizedaSt.Louis-Ste. GenevieveCountyFauna,whichareseparatedhereinto theSt.LouisandJefferson-Ste.Genevievekarsts. J EFFERSON S TE .G ENEVIEVE K ARST ThiskarstisformedinMississippianandOrdovician rocksinJeffersonandSte.Genevievecounties,southofSt. Louis.TherearefaunisticsimilaritiestotheSt.Louisand Perryvillekarsts.Mississippianrockscropoutinnorthern andsouthernblockscontainingmostofthecaves,butafew importantbiocaves,suchasFriedmanÂ’sandPleasant Valley,lieinOrdovicianrocksinnorthernJefferson County.Twoendemiccavebeetlesoccur: Xenotrechus condei ,NorthernXenotrechuscavebeetle,and X.denticollis ,SouthernXenotrechuscavebeetle,withonlytwo knowncaveseach.Astygobite, Sphalloplanahubrichti HubrichtÂ’scaveplanarian,occursinIllinoisandinthis area,intwoOrdovicianspringsandinKohmÂ’sCave, alargestreamsystemwithabundantcavelife.KohmÂ’salso has X.denticollis ,atrechinebeetleabout3.6mmlong, whichmayfeedontubificidoligochaetewormsonstream banks. Xenotrechus ismostcloselysimilarto Chaetoduvalius and Geotrechus fromsouthernEurope(Barrand Krekeler1967).Extensivebatstainsontheedgesofdomes indicatethatalargecolonyofGraybatsmayhaveroosted inKohmÂ’sCave,butnolonger.NoGraybatsarecurrently knownfromcavesineasternMissouri.With19troglobites, thiskarsthasthehighestareaendemisminMissouri.Peck andLewis(1978)thoughttheSte.GenevieveFault separatedthisareafromthePerryvilleCountyFaunato thesouth. Figure14.Priority1and2GrayandIndianabatcaves. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 155

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P ERRYVILLE K ARST Someofthedensestknownkarstdevelopmentinthe USAoccursinPerryCounty,inlimestonesofmiddle Ordovicianageorolder.About700caveentrancesare recordedinthelargesinkholeplain,withmanylargeriver caves,suchasCreviceCave,thelongestinMissouriat 45km.Largestreamcavesareespeciallydevelopedinthe CinqueHommesCreekarea.Theuplandsarecoveredwith upto10mofloessderivedfromtheMississippiRiver floodplain(Vandike,1985),andthereisheavyrowcrop agriculture.BiologicallysimilartotheJefferson-Ste. GenevieveKarst,thePerryvilleKarsthasitsownendemics andlackstrechinebeetles.Endemicspeciesinclude Sphalloplanaevaginata, Perryvillecaveplanarian, Kenkia lewisi, LewisÂ’caveplanarian,and Cottus sp.8,the undescribedbutdistinctGrottosculpin(Burretal., 2001),nowonMissouriÂ’sSpeciesofConcernList.Mystery CaveranksasthirdincavebiodiversityinMissouri (Table7).With18troglobites,thiskarsthashigharea endemism. C ONSERVATION Manyspeciesandbiologicallyimportantcaveswere addedtotheMissouriNaturalHeritageDatabaseandthe ComprehensiveWildlifeConservationStrategy,alongrange,statewideconservationplan(Elliott,2006b). Thetermbiocaveisacaveforwhichatleastonespecies wasrecordedintheCLD.Fivewasconsideredthe minimumnumberofspeciesindicatingthattherehadbeen anactualbioinventoryinsteadofacursorycheckor asingle-speciessurvey.Beginningwithasetofabout1200 caveswithbiologicalrecords,asubsetof862biocaveswas Figure15.Cavefishsites. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 156 N JournalofCaveandKarstStudies, April2007

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derived(Fig.2),thenarelationbetweenatableofbiocaves andatableofcavelocationswastemporarilycreatedusing decimal-degreecoordinates,developedwiththehelpofthe MissouriNaturalHeritageDatabaseandHalBaker, MissouriCaves&KarstConservancy. TheCaveFocusAreasthatwerederiveddonotpinpoint caves,butarepolygonstypicallyfourtoeightkilometersin diameter,includingoneormoreimportantcavesorsprings. OncethepolygonshapefileswerecreatedinESRI’s ArcMap H ,theCaveFocusAreascouldbeincludedinan overallGISprojectforwildlifeplanningwithoutrevealing specificcavelocations.Researchersandconservationists mayobtainindividualcavelocationsfromtheHeritage DatabaseortheMissouriSpeleologicalSurveyonaneed-toknowbasis,withwrittenjustification. Caveswererankedfor B (biodiversityindex),asan attributeinArcMaptoexaminethegeographicdistributionofimportantbiocaves(Fig.1).Figure14shows11 Priority1( 25,000–30,000bats)and55Priority2 ( 25,000–30,000)Graybatcaves,andthreePriority1 and16Priority2Indianabatcaves.Theseprioritiesare usedbyMDCtoratethecavesforlarger,moreimportant coloniesofGraybats(maternityandhibernacula)and Indianabats(hibernaculaonly).SeeClawsonetal.(2006). Figure15depictscavefishsites. ThefinalstepindelineatingCaveFocusAreas(Fig.16) wastocreatedatalayersinArcMapoftheaboveelements. Polygonshapefilesweredrawnaroundclustersofimportantcavesandfirstmagnitudekarstsprings,whichflow 2.83m 3 s 1 (100ft 3 s 1 ).Thelatterspringsoftencontain Figure16.Ninety-sevenCaveFocusAreascomprisinghighbiodiversityca ves,importantbatandcavefishcaves,andfirst magnitudesprings. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 157

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importantgroundwaterspeciesandrepresenthydrological connectionsoverlongdistances.Thelargest,BigSpring, CarterCounty,flowsabout12m 3 s 1 (424ft 3 s 1 ),with apeakflowof37m 3 s 1 (1,307ft 3 s 1 ). D ISCUSSIONAND C ONCLUSIONS Hightroglobiteendemismoccursinsomeareas,suchas theJefferson-Ste.GenevieveKarst,SpringfieldPlateau, PerryvilleKarst,andtheSalemPlateau.Areaendemismis generallylownorthoftheMissouriRiver,BooneCounty beinganexception.Endemismgenerallyincreasestothe southandtheeast,buthighbiodiversitycavesoccurover abroadarea.Thetopthreecavesarewidelyseparatedby 260–320km,butmoretopbiocavesarefoundineastern Missourithanelsewhere(Fig.1). TheOzarkRegionlackstherichtroglobiticbeetlefauna thatiscommonintheeasternUnitedStates.Untilrecently theonlytrechinesinMissouriwerethetwo Xenotrechus foundintheJefferson-Ste.GenevieveKarst.Thediscovery ofanewspeciesofrelativelysmall Pseudanophthalmus in ShannonCountyre-opensthequestionofthelownumber oftroglobiticbeetlesintheOzarks,discussedbyBarrand Krekeler(1967)andPeckandLewis(1978).Perhapswe onlyneedtolookforsmallerbeetlestohavesuccess. However,Missouricaveslacklargecoloniesofrhaphidoporidcrickets,withjustfourinstancesintheCLDwhere anobservercountedmorethan100crickets,themaximum being500 C.gracilipes. Incontrast,cricketpopulations oftennumberinthethousandsinTexas(several Ceuthophilus )andKentucky( Hadenoecus and Ceuthophilus ), wheretherearemanytroglobiticandtroglophiliccarabid beetles,suchas Rhadine Pseudanophthalmus ,and Neaphaenops preyingoncricketeggs(Lavoieetal.,2007). Missourirhaphidophoridsarelesscave-loving,whichmay havepreventedtheco-evolutionofcricket-egg-predators, alongwithapossiblelackofancestralcarabidsinvading theOzarksfromtheAppalachians(PeckandLewis,1978). Christiansen(1983)analyzedthedistributionsand troglomorphyofcaveCollembolaeastoftheGreatPlains. Thegreatestbiodiversityoftroglobiteswasintheheartland ofthenonglaciatedAppalachiansandInteriorLow Plateaus,particularlyamongtheEntomobryinae.The Ozarkshaveintermediatebiodiversity,andcavesin glaciatedareashavethelowestlevelofcaveadaptation. Hobbsetal.(2003)providedalisttroglobiticspecies fortheUnitedStates.Culveretal.(1999,2003)analyzed regionalpatternsoftroglobites,stygobitesandphreatobitesacrosstheentireUSA.TheanalysisofCulveretal. lookedattheOzarkRegionandnotMissouri perse .For bothstygobitesandtroglobites,onlynumberofcaves wasasignificantpredictor,andthatseemstobeborne outinthisstudy,atleastineasternMissouri.Distance toPleistoceneglacialedgeswasnotimportant,butthere wassomeinfluencefromproximitytolateCretaceous seamargins,anancientsourceofaquaticcolonizers. Therewasnoeffectfromsurfaceproductivity(vegetation type). Inthisstudysomewhatdifferentconclusionswere drawnthanbyCulveretal.,(2003),butwithoutstatistical testing.Inthisstudy,highbiodiversityasmeasuredinsome Missouricavesseemstoberelatedtoseveralfactors: 1)Areaswithlargerandnumerouscaveswithnumerous aquaticandterrestrialmicrohabitats, 2)LocationgenerallysouthoftheMissouriRiver(away fromPleistoceneglaciation), 3)Moderatetohigh,naturalnutrientloadsfrom recharge(essential)andGraybatguano(notalways essential,asinMysteryCave),asopposedto vegetationtype,and 4)Highscientificandconservationistinterestbythe ownerormanager,andaccessbyqualifiedbiologists. Thetopthreebiocavesprovideexcellentexamplesof thefactorsgivenabove.TumblingCreekCave,theleading Missouribiocaveatthistime,hasreceived40yearsof studybutisstillyieldingnewspecies(ElliottandAley, 2006).Martin(1980)studiedtheextremearthropod diversityofTumblingCreekCave,tabulating28mite species,mostofwhichwereassociatedwithGraybat guano.Insofarashalf(58)ofthe115speciesinTumbling CreekCavearemorphospeciesnotyetidentifiedtospecies, including27thatarenotyetidentifiedtogenus,thereis stillsomepotentialforadditional,new,endemicspecies there.TomAley( pers.comm. )observedtroglobiticcrayfishesonfiveoccasionsinthecave,butnospecimenshave beenobtainedyetforidentification. AnotherexampleoftheabovefourfactorsisDevil’s IceboxCave,managedbyRockBridgeMemorialState Parkasawildliferefugeandwildcavingvenue,where Figure17.Therateofdescriptionofnewtroglobiticspecies fromMissouri,withfittedpolynomialcurve. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 158 N JournalofCaveandKarstStudies, April2007

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Table10.Cavebiodiversityin46Missouricounties,basedontheapproxim atenumberofcavesknownin2005–2006.Sortedby Success5,whichisthecountywidenumberoftroglobitesdividedbyEffort 5(thenumberofbiocaveswithatleastfivespecies dividedbythenumberofcaves). CountyCavesBiocaves1Biocaves5TroglobitesEffort1Success1Effort5S uccess5 Perry656239190.03515420.01371385 Jefferson160513150.3188470.0188800 Newton5720170.3509200.0175399 Lawrence4312190.2791320.0233387 Greene36029440.0806500.0111360 St.Louis130565120.4308280.0385312 Stone2833110110.10951000.0353311 Douglas10817250.1574320.0185270 Ste.Genevieve72174120.2361510.0556216 Shannon53515865240.2953810.1215198 Pulaski3507025140.2000700.0714196 Dade552130.0364830.0182165 Dent9612350.1250400.0313160 McDonald10320460.1942310.0388155 Taney1372714150.1971510.1022147 Christian2204518110.2045540.0818134 Crawford2054524130.2195590.1171111 Camden1464420150.3014500.1370110 Jasper267140.2692150.0385104 St.Francois199150.4737110.052695 Benton425240.1190340.047684 Phelps1464123130.2808460.157583 Boone1053214110.3048360.133383 Washington812816150.3457430.197576 Franklin975423170.5567310.237172 Wright5710780.1754460.122865 Barry1346028130.4478290.209062 Laclede7828970.3590200.115461 Reynolds6616650.2424210.090955 Lincoln364230.1111270.055654 Oregon1408147180.5786310.335754 Ozark80251490.3125290.175051 Miller6418540.2813140.078151 Texas178462160.2584230.118051 Madison208250.4000130.100050 Carter754526140.6000230.346740 Pike384110.1053100.026338 Maries363220.0833240.055636 Howell3919980.4872160.230835 Morgan303110.1000100.033330 Dallas2712220.444450.074127 Ripley93360.3333180.333318 Cole183110.166760.055618 Iron2514850.560090.320016 Hickory2112210.571420.095211 Pettis55221.000020.40005 W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 159

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visitingscientistsandparkstaffoftenconductfaunal surveysandcontributedatatotheCLD.MysteryCave receivedintensivestudybyLewis(1974).Fewhighbiodiversitycavesreceivedonlycursorystudy. Thetrendofdiscoveringanddescribingnewtroglobitic speciesinMissourihasvariedsincethe19 th Century,butit isgraduallyincreasing(Fig.17).Withabacklogof15 undescribedtroglobites,thepaceofdescriptionstillwill increaseifthereisfundingforthefewskilledinvertebrate taxonomists.Theongoingtaxonomiccrisisdoesnot encouragethetrainingofnewinvertebratetaxonomists (Wheeleretal.,2004,Elliott,2006).IftheMissouritrendof discoverycontinues,wecouldseemanymoretroglobites eventually,orelseanever-increasingbacklogofundescribedspeciesandunrecognizedbiodiversity. Additonalworkisneededinmanyareas.ManyMissouri cavesaregoodcandidatesforhavinghighbiodiversity,but theyhavenotyetreceivedadequatestudy.Threeexamples areCarrollCave,CamdenCounty;CreviceCave,Perry County;andBruceCave,PulaskiCounty.Allarelarge,with extensivestreamsandterrestrialhabitats,largerecharge areasandreportedlyabundantcavelife.Table10shows cavebiodiversityin46Missouricounties,basedonthe numberofcavesknownin1998.Ofthe1,274siteswith biologicalrecords,1,038arecavesorcavespringsand491 arecaveswithfiveormorerecordedspecies.Effort1isthe numberofBiocaves1(withatleastonerecordedspecies) dividedbythenumberofcavesinthatcounty.Asimilar calculationwasdoneforEffort5(caveswithatleastfive species).Success1isthenumberoftroglobitesdividedby Effort1foracounty(similarlyforSuccess5).Thelistis rankedindescendingorderofSuccess5,ameasureofsuccess infindingtroglobitesincavesthathavebeenstudied somewhatadequately.PerryandJeffersoncountiesrank highbecausemanytroglobiteswerefoundwithrelatively littleeffort,indicatingthehighendemismfoundinthose karstareas.Table10isaguidetowherefutureworkshould beconcentrated.Besidesthethreeprominentcavesmentionedabove,countieswithmanycaves,butmodestsuccess todate,probablyaregoodcandidatesforintensivestudy. AnexceptionmaybetheurbanareasofGreeneandSt. Louiscounties,butthemoreruralareasmayyetcontain highbiodiversity.Somecountieshavereceivedlittlecave exploration,butstillmayhavehighspeleologicalpotential (e.g.,StoneandDouglascounties). A CKNOWLEDGMENTS SupportforthisstudycamefromtheMissouriDepartmentofConservation,NaturalHistoryandResource Sciencedivisions.Iamgratefultomyresearchpartnersinthe CLD,DavidC.Ashley,RichardL.Clawson,ScottHouse, LawrenceIreland,JamesE.Kaufmann,StevenSamoray, MichaelE.SlayandMichaelJ.Sutton,whocontributed thousandsofobservationsandspecimenstotheshared database.IwanttospecificallythankJimRathertforthe photographthatappearsinFigure4andDavidAshleyfor thephotographthatappearsinFigure7.Dr.Frederick Hartwigisespeciallyacknowledgedforhisgeneroussupport ofcaveprotection,asareconservationistlandownersCathy andTomAley,JudyandLesTurilli,andothers.Ithankthe MissouriCaves&KarstConservancy,whosemembers participatedintheMissouriCaveLifeSurveyof2001–2002, andtheMVOR(MississippiValleyOzarkRegion),National SpeleologicalSociety,whoassistedincaverestoration.I thankthemanybiologists,cavers,studentsandvolunteers whocontributedfieldwork,observations,taxonomic identificationsandlaborwhilestudyingcavelife,building cavegatesandrestoringcaves;thiscanonlybeapartiallist: CathyAley,TomAley,SybilAmelon,HalBaker,Thomas C.BarrJr.,JonathanBeard,JeffBriggler,LeonardButts, RoxieCampbell,StephanieClark,KennethChristiansen, JamesCokendolpher,BobCurrie,KatieDerr,JeffDierking, DanDrees,JodyEberly,UlrikeEnglisch,DennisFigg,Anna Ford,GeneGardner,SaraGardner,BobGillespie,G.O. Graening,SueHagan,PaulHauck,KevinHedgpeth,A.J. Hendershott,JoeHobbs,JohnR.Holsinger,PeggyHorner, MikeHubbard,PaulJohnson,DavidKampwerth,Jim Kennedy,StefanKoenemann,JaneenLaatsch,SteveLaval, BobLerch,JulianJ.Lewis(specialthanksforeditorial review),KennethLister,KimLivengood,BrianLoges, RandyLong,PaulMcKenzie,JeanMayer,RichardMeyers, MarkMcGimsey,PaulMcKenzie,TomMeister,Philip Moss,RonOesch,StevePaes,JustinPepper,BradPobst, BarryRabe,JosephReznik,RhondaRimer,MelissaShiver Scheperle,ScottSchulte,MikeSkinner,TimSnell,Steve Taylor,RickThom,GayleA.UnruhandDavidUrich. R EFERENCES Aley,T.J.,andThomson,K.C.,1971,OzarkUndergroundLaboratory, PartII.OzarkCaver,SouthwestMissouriStateCollege,Springfield, Missouri,v.3,no.6,p.1–19, appendix. Aley,T.J.,2000,Karstgroundwater:MissouriConservationist,v.61, no.3,p.6–9.ReprintedinConservingMissouri’sCavesandKarst, 2002,MissouriDepartmentofConservation. Ashley,D.C.,1993,FieldstudiesinMissourionCave-dwellingsnailsof thegenus Fontigens :TransactionsoftheMissouriAcademyof Science,Abstracts,v.27,92p. Ashley,D.C.,1996,Addingcaveecologytothecollegecurriculum: AdescriptionofBIO398atMissouriWesternStateCollege, in Rea, G.T.,ed.,Proceedingsofthe1995NationalCaveManagement Symposium,Abstracts,SpringMillStatePark,Mitchell,Indiana, October25–28,1995,IndianaKarstConservancy,Inc.,318p. Ashley,D.C.,2003,Afinalreportonthemonitoringprojecttoevaluate thepopulationstatusoftheTumblingCreekcavesnail, Antrobia culveri (Gastropoda:Hydrobiidae):ProgressreporttotheU.S.Fish andWildlifeService,Columbia,Mo.,93p. Ashley,D.C.,andElliott,W.R.,2000,Missouricavelife,Missouri Conservationist,v.61,no.3,p.12–17.ReprintedinConserving Missouri’sCavesandKarst,2002,MissouriDepartmentofConservation. Barr,Jr.,T.C.,andKrekeler,C.H.,1967, Xenotrechus ,anewgenusof cavetrechinesfromMissouri(Coleoptera:Carabidae):Annalsofthe EntomologicalSocietyofAmerica,v.60,no.6,p.1322–1325. 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Bonett,R.M.,andChippindale,P.T.,2004,Speciation,phylogeography andevolutionoflifehistoryandmorphologyinplethodontid salamandersofthe Euryceamultiplicata complex:MolecularEcology, v.13,p.1189–1203. Burr,B.M.,Adams,G.L.,Krejca,J.K.,Paul,R.J.,andWarren,M.L.Jr., 2001,Troglomorphicsculpinsofthe Cottuscarolinae speciesgroupin PerryCounty,Missouri:Distribution,externalmorphology,and conservationstatus:EnvironmentalBiologyofFishes,v.62,p.279–296. Causey,N.B.,1960,TroglobiticmillipedsinMissouri:MissouriSpeleol ogy,MissouriSpeleologicalSurvey,v.2,p.60–65. Christiansen,K.A.,1964,ArevisionoftheNearticmembersofthegenus Tomocerus (Collembola:Entomobryidae):Revued’Ecologieetde BiologieduSol,v.1,p.639–678. Christiansen,K.A.,1966,Thegenus Arrhopalites (Collembola:Sminthuridae)intheUnitedStatesandCanada:InternationalJournalof Speleology,v.2,p.43–73. Christiansen,K.A.,1983,ZoogeographyofcaveCollembolaeastofthe GreatPlains:NationalSpeleologicalSocietyBulletin,v.44,p.32–41. 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Eigenmann,C.H.,1899,ExplorationsinthecavesofMissouriand Kentucky,ProceedingsoftheIndianaAcademyofScience,v.9, p.58–61. Eigenmann,C.H.,1901,Descriptionofanewcavesalamander, Spelerpes stejnegeri ,fromthecavesofsouthwesternMissouri:Transactionsof theAmericanMicroscopicalSociety,v.22,p.189–192,pls.XXVII– XXVIII. Eigenmann,C.H.,1909,CavevertebratesofAmerica.Astudyin degenerativeevolution,CarnegieInstituteofWashingtonPublications,104ix 241pp.,frontispiece,pls.A,1–29. Elliott,W.R.,1997,TheCavesoftheBalconesCanyonlandsconservation plan,ReporttoTravisCounty,TransportationandNaturalResources Department,BalconesCanyonlandsConservationPlan,156p. Elliott,W.R.,2000a,ConservationoftheNorthAmericancaveandkarst biota, in Wilkens,H.,Culver,D.C.,andHumphreys,W.F.,eds., Subterraneanecosystems:EcosystemsoftheWorld,30,Amsterdam, Elsevier,p.665–689[ElectronicreprintonBiospeleologywebsite]. Elliott,W.R.,2000b,BelowMissourikarst:MissouriConservationist, v.61,no.3,p.4–7.[Reprinted,inConservingMissouri’sCavesand Karst,2002,MissouriDepartmentofConservation] Elliott,W.R.,2003a,AGuidetoMissouri’scavelife.MissouriDepartmentofConservation.40p. Elliott,W.R.,2003b,Missouricavebiogeographyandbiodiversity: JournalofCaveandKarstStudies,Abstracts,v.65,no.3,p.174. Elliott,W.R.,2004,Protectingcavesandcavelife, in Culver,D.C.,and White,W.B.,eds.,Encylopediaofcaves:Amsterdam,Elsevier, p.458–467. Elliott,W.R.,2005,GraybattrendsinMissouri:Gatedvs.ungatedcaves, in G.T.Rea,ed.,Proceedingsofthe2003NationalCaveandKarst ManagementSymposium,Gainesville,Fla.,Abstracts,p.43–44. Elliott,W.R.,2006a,Criticalissuesincavebiology, in Rea,G.T.,ed., Proceedingsofthe2005NationalCaveandKarstManagement Symposium,Albany,NewYork,p.35–39. Elliott,W.R.,2006b,Missouri’sCaveFocusAreas, in Rea,G.T.,ed., Proceedingsofthe2005NationalCaveandKarstManagement Symposium,Albany,NewYork,p.48–52. 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Elliott,W.R.,Sutton,M.J.,andAshley,D.C.,2000,Stygobitedistribut ion inMissouri:JournalofCaveandKarstStudies,Abstracts,v.62,p.31. Elliott,W.R.,Samoray,S.T.,Gardner,S.E.,andAley,T.J.,2005, TumblingCreekCave:Anongoingconservationandrestoration partnership:AmericanCaves,v.19,no.1,p.8–13. Elliott,W.R.,Samoray,S.T.,Gardner,S.E.,andKaufmann,J.E.,2006, TheMDCMethod:Countingbatswithinfraredvideo, in Rea,G.T., ed.,Proceedingsofthe2005NationalCaveandKarstManagement Symposium,Albany,NewYork,p.147–153. Faxon,W.,1889,[Descriptionof] Cambarussetosus and Asellushoppinae in Garman,S.,ed.,CaveanimalsfromsouthwesternMissouri: BulletinoftheMuseumofComparativeZoology,v.17,p.237– 238. Gardner,J.E.,1985,InvertebratefaunafromMissouricaves:Missouri Speleology,v.25,no.1–2,p.172–177. Gardner,J.E.,1986,InvertebratefaunafromMissouricavesandsprings. MissouriDepartmentofConservation,NaturalHistorySeries,no.3, p.i–vi,1–72. 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Hobbs,H.H.III,2001,Anewcavecrayfishofthegenus Orconectes subgenus Orconectes ,fromsouthcentralMissouri,U.S.A.,withakey tothestygobiticspeciesofthegenus(Decapoda,Cambaridae): Crustaceana,v.74,p.635–646. Hobbs,III.,H.H.,Culver,D.C.,andElliott,W.R.,2003,AlistofcavelimitedspeciesintheUnitedStatesandCanada,KarstWaters Institute,http://www.karstwaters.org/trogslist.htm[accessedJanu ary 1,2003]. Holsinger,J.R.,1967,Systematics,speciation,anddistributionofthe subterraneanamphipodgenus Stygonectes (Gammaridae):United StatesNationalMuseumBulletin,v.259,176p. Holsinger,J.R.,1971,Anewspeciesofthesubterraneanamphipodgenus Allocrangonyx (Gammaridae),witharedescriptionofthegenusand remarksonitszoogeography:InternationalJournalofSpeleology, v.3,no.3–4,p.317–331,pls.104–110. Holsinger,J.R.,1989,AllocrangonyctidaeandPseudocrangonyctidae, twonewfamiliesofHolarcticsubterraneanamphipodcrustaceans (Gammaridea),withcommentsontheirphylogeneticandzoogeographicrelationships:ProceedingsoftheBiologicalSocietyof Washington,,v.102,no.4,p.947–959. Hoppin,R.,1889,[LetterstoSamuelGarman], in Samuel,G.,ed.,Cave animalsfromsouthwesternMissouri:BulletinoftheMuseumof ComparativeZoology,v.17,no.6,p.225–240,pls.I–II. W.R.E LLIOTT JournalofCaveandKarstStudies, April2007 N 161

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Hubbell,T.H.,1934,Rhaphidophorinae, in Hebard,M.,ed.,The dermapteraandorthopteraofIllinois:IllinoisNaturalHistorySurvey Bulletin,v.20,p.125–279. Hubbell,T.H.,1936,AMonographicRevisionoftheGenus Ceuthophilu s (Orthoptera,Gryllacrididae,Rhaphidophorinae):UniversityofFloridaPublication,BiologicalScienceSeries,v.2,no.1,551p. 38pl. Hubricht,L.,1940,TheOzarkAmnicolas:TheNautilus,v.53,no.4, p.118–122,pl.14. Hubricht,L.,1941,ThecaveMolluscaoftheOzarkregion:TheNautilus, v.54,no.4,p.111–112. Hubricht,L.,1942,Anewlocalityfor Amnicolaproserpina Hubricht: Nautilus,v.55,p.105. Hubricht,L.,1943,StudiesonthenearcticfreshwaterAmphipoda,III: NotesonthefreshwaterAmphipodaofeasternUnitedStates,with descriptionoftennewspecies:TheAmericanMidlandNaturalist, v.29,no.3,p.683–712. Hubricht,L.,1950,TheinvertebratefaunaofOzarkcaves:National SpeleologicalSocietyBulletin,v.12,p.16–17. Hubricht,L.,1959,Malacostraca:Amphipoda, in Edmondson,W.T.,ed., Fresh-waterbiology.2 nd ed.:NewYork,JohnWiley&Sons, p.876–878. Hubricht,L.,1971,NewHydrobiidaefromOzarkcaves:TheNautilus, v.84,no.3,p.93–96. Hubricht,L.,1972, Gastrocoptaarmifera (Say):Nautilus,v.85,p.73–78. Hubricht,L.,andMackin,J.G.,1940,Descriptionsofninenewspeciesof fresh-wateramphipodcrustaceanswithnotesandnewlocalitiesfor otherspecies:TheAmericanMidlandNaturalist,23,p.187–218. Hubricht,L.,andMackin,J.G.,1949,Thefreshwaterisopodsofthegenus Lirceus (Asellota,Asellidae):TheAmericanMidlandNaturalist, v.42,no.2,p.334–349. Hyman,L.H.,1945,NorthAmericantricladTurbellariaXI,New,chiefly cavernicolous,planarians:TheAmericanMidlandNaturalist,v.34, no.2,p.75–484. Hyman,L.H.,1956,NorthAmericantricladTurbellaria15,Threenew species:AmericanMuseumNovitates,no.1808,p.1–14. Kenk,R.,1975,Fresh-watertriclads(Turbellaria)ofNorthAmericaVII, Thegenus Macrocotyla :TransactionsoftheAmericanMicroscopical Society,no.94,p.324–339. Kenk,R.,1977,Freshwatertriclads(Turbellaria)ofNorthAmericaIX, Thegenus Sphalloplana :SmithsonianContribtionstoZoology,no. 246,p.1–38. Koenemann,S.,andHolsinger,J.R.,2001,SystematicsoftheNorth Americansubterraneanamphipodgenus Bactrurus (Crangonyctidae): BeaufortiaBulletinZoologicalMuseumUniversityofAmsterdam, v.51,no.1,p.1–56. Koppelman,J.B.,andFigg,D.E.,1993,Geneticestimatesofvariability andrelatednessforconservationofanOzarkcavecrayfishspecies complex:ConservationBiology,v.9,no.5,p.1288–1294. LaVal,R.K.,Clawson,R.L.,Caire,W.,Wingate,L.R.,andLaVal,M.L., 1977,Anevaluationofthestatusofmyotinebatsintheproposed MeramecParkLakeandUnionLakeprojectareas,Missouri:St. LouisDistrict,U.S.ArmyCorpsofEngineers,136p. Lavoie,K.H.,Helf,K.L.,andPoulson,T.L.,2007,Thebiologyand ecologyofNorthAmericancavecrickets:JournalofCaveandKarst Studies,[thisissue]. Lerch,R.N.,Erickson,J.M.,Wicks,C.M.,Elliott,W.R.,andSchulte, S.W.,2000,WaterqualityintwokarstbasinsofBooneCounty, Missouri:JournalofCaveandKarstStudies,Abstracts,v.62,p.187. Lewis,J.J.,1974,TheinvertebratefaunaofMysteryCave,PerryCounty, Missouri:MissouriSpeleology,v.14,no.4,p.1–19. Lewis,J.J.,2002, Chaetaspisaleyorum ,anewspecisofmillipedfrom TumblingCreekCave,Missouri,withasynopsisofthecavernicolous speciesofChaetaspis(Diplopoda:Polydesmida):Myriapodologica, v.7,no.11,p.101–111. Lewis,J.J.,2004, Brackenridgiaashleyi ,anewspeciesofterrestrialisopod fromTumblingCreekCave,Missouri(Crustacea,Isopoda:Trichoniscidae):ProceedingsoftheBiologicalSocietyofWashington,v.117, no.2,p.176–185. Longley,G.,1981,TheEdwardsAquifer:Earth’smostdiversegroundwaterecosystem?:InternationalJournalofSpeleology,v.11,no.1–2, p.123–128. Loomis,H.F.,1939,ThemillipedscollectedinAppalachiancavesbyMr. KennethDearolf:BulletinoftheMuseumofComparativeZoology, v.86,p.165–193. Martin,B.J.,1980,Thecommunitystructureofarthropodsonbatguano andbatcarcassesinTumblingCreekCave[M.S.thesis]:Chicago Circle,UniversityofIllinois,178p. MissouriDepartmentofConservation,2005,MissouriSpeciesand CommunitiesofConservationConcern,53p. Nigh,T.A.,andSchroeder,W.A.,2002,AtlasofMissouriEcoregions, MissouriDepartmentofConservation,212p. Noltie,D.,andWicks,C.M.,2001,Howhydrogeologyhasshapedthe ecologyofMissouri’sOzarkcavefish( Amblyopsisrosae )andSouthern cavefish( Typhlichthyssubterraneus ):Insightsonthesightlessfrom understandingtheunderground:JournaloftheEnvironmental BiologyofFishes.v.62,p.171–194. Oesch,R.A.,andOesch,D.W.,1986,CaveresourcesofFortLeonard Wood,MissouriDepartmentofConservation,159p. Peck,S.B.,andLewis,J.J.,1978,Zoogeographyandevolutionofthe subterraneaninvertebratefaunasofIllinoisandsoutheasternMissouri : TheNationalSpeleologicalSocietyBulletin,v.40,no.2,p.39–63. Pflieger,W.L.,1996,ThecrayfishesofMissouri,MissouriDepartmentof Conservation,152p. Pflieger,W.L.,1997,ThefishesofMissouri,MissouriDepartmentof Conservation,382p. Robison,H.W.,andHolsinger,J.R.,2000,Firstrecordofthesubterraneanamphipodcrustacean Allocrangonyxhubrichti (Allocrangonyctidae)inArkansas:JournaloftheArkansasAcademyofScience, v.54,p.153. Schwarz,E.A.,1891,AlistoftheblindornearlyeyelessColeopterafound inNorthAmerica:ProceedingsoftheEntomologicalSocietyof Washington,v.2,p.23–27. Sarver,R.J.,andLister,K.B.,2004,Surfacestreamoccurrenceandupdat ed distributionof Allocrangonyxhubrichti Holsinger(Amphipoda:Allocrangonyctidae),anendemicsubterraneanamphipodoftheInterior Highlands:JournalofFreshwaterEcology,v.19,no.2,p.165–168. Shear,W.A.,2003,ThemillipedfamilyTrichopetalidae,Part1:Introductionandgenera Trigenotyla Causey, Nannopetalum n.gen.,and Causeyella n.gen.(Diplopoda:Chordeumatida,Cleidogonoidea): Zootaxa,v.321,p.1–36.www.mapress.com/zootaxa/,[accessed2003] Slay,M.E.,Elliott,W.R.,andSluys,R.,2006,CavernicolousMissouri triclad(Platyhelminthes:Turbellaria)records:TheSouthwestern Naturalist,v.51,no.2,p.251–252. Sluys,R.,andKawakatsu,M.,2006,Towardsaphylogeneticclassificationofdendrocoelidfreshwaterplanarians(Platyhelminthes):A morphologicalandeclecticapproach:JournalofZoologicalSystematicsandEvolutionaryResearch,v.44,no.4,p.274–284. Stejneger,L.,1892,Preliminarydescriptionofanewgenusandspeciesof blindcavesalamanderfromNorthAmerica:Proceedingsofthe UnitedStatesNationalMuseum,v.15,no.894,p.115–117,pl.IX. Sutton,M.J.,1993,Cavesandcavewildlifeinamineralprospectingarea, OregonandShannoncounties,Missouri:MissouriSpeleology,v.33, no.1–4,p.1–138. Sutton,M.J.,1998,Baselinemappingandbiologicalinventoryofcaveson theMarkTwainNationalForest,Doniphan-ElevenPointDistrict, Missouri:Phase2:CaveResearchFoundation,105p. Sutton,M.J.,1999,CavedocumentationinanOzarkprospectingarea: NSSNews,v.57,no.5,p.138–140. Sutton,M.J.,2004,ThePinkPlanariansofDevil’sIceboxCave–Census protocols:CaveResearchFoundation,35p. Thomson,K.C.,andAley,T.J.,1971,OzarkUndergroundLaboratory, PartI:OzarkCaver,v.3,no.5,p.1–24. Vandike,J.,1985,MovementofshallowgroundwaterinthePerryville KarstArea,southeasternMissouri:WaterResourcesReport, MissouriDepartmentofNaturalResources,DivisionofGeology andLandSurvey,Rolla,Missouri. U.S.DepartmentofAgriculture,2006,IntegratedTaxonomicInformation System.http://www.itis.usda.gov/ U.S.DepartmentoftheInterior,FishandWildlifeService,2001, Endangeredandthreatenedwildlifeandplants;ListtheTumbling Creekcavesnailasendangered.[Emergencyrule]FederalRegister,v. 66,no.248),p.66803–66811. U.S.DepartmentoftheInterior,FishandWildlifeService,2003, TumblingCreekCavesnailRecoveryPlan.97p. Wheeler,Q.D.,Raven,P.H.,andWilson,E.O.,2004,Taxonomy: ImpedimentorExpedient?:Science,303(5656):285. Z OOGEOGRAPHYANDBIODIVERSITYOFMISSOURICAVESANDKARST 162 N JournalofCaveandKarstStudies, April2007



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ABRIEFHISTORYOFKARSTHYDROGEOLOGY: CONTRIBUTIONSOFTHENSS W ILLIAM B.W HITE MaterialsResearchInstituteandDepartmentofGeosciences,ThePennsyl vaniaStateUniversity,UniversityPark,PA16802USA,wbw2@psu.edu Abstract: Thehydrologyofkarstaquifershasbeenofinterestsinceearlyhistorict imes withcavesservingaswater-carryingpathways.Themodernperiodofkarst hydrology canbesaidtohavebegunroughlyinthe1960swiththeworkoftheInternatio nal HydrologicDecadeandwiththerecognitionoftherelationshipofcaveexp lorationto groundwaterbasins.Athemeforthe40yearperiodbetweenthe25 th anniversaryofthe NSSandthepresentisthegradualmeldingoftraditionalhydrogeology,wh ichdoesnot workwellinkarst,andthecontributionsofcaveexplorerswhohaveprovid ed tremendousdetailabouttheconduitsystemsinaquifers.Importantprogr esshasbeen madeintechniquesforwatertracinginkarstareasandinsystematicmappi ngofkarst groundwaterbasins.Qualitativestudieshavelargelybeenreplacedbyqu antitative measurementsofspringflowandwaterchemistry.Thecurrentresearchfro ntdealswith theconstructionofflowmodelsforkarstaquifers. I NTRODUCTION Themostdirectinterfacebetweencaveexplorationand theearthsciencesisthehydrologyofkarstaquifers.No wonder.Heregoesasurveyteamofcavers,splashing throughabaselevelwatercaveuptotheirbellybuttons(or chins)inthekarstwatertable.Howmuchmoreintimate aconnectioncantherebe?Cavershaveadeepunderstandingofthemovementofgroundwaterincarbonate rocks,butittooksometimetoconvincetheprofessional communitythattheywereworthlisteningto. Thepurposeofthisarticleistotracethegradual evolutionofunderstandingofkarstaquifersbythe professionalcommunityandtherolethatcavershave playedoverthepast40years.Caverswiththeirdetailed mapsandtheirdeepunderstandingofthelayoutofconduit systemscantakecreditforasubstantialportionofthe modernviewofkarsthydrology.Thearticledoesnotclaim tobeacomprehensivereviewofkarsthydrogeologyas awhole.Formoretraditionalandextensivereviewssee White(1993,1998,2002,2006). S OME H ISTORICAL P ERSPECTIVE Althoughtheprimaryfocusofthisarticleiskarst hydrologyasithasevolvedduringthepast40years,itisof interesttolookmuchfartherbacktoseehowcaveshave figuredintheprecursorhistory.SummariesoftheseprescientificrootsofhydrologymaybefoundinAdams (1954)andLaMoreauxandTanner(2001). A NCIENT H ISTORY Becausesomeoftheearliestwritingsonthenatural worldcomefromGreece,acountrythatislargelykarst,it isnotsurprisingthatspringsandcaveswerestrongly linked.EarlyGreekwriterssuchasPlatoandAristotle incorporatedcavesaschannelwayscarryingwaterfrom theseaupintothemountainsfromwhichitemergedfrom springstoformrivers.Springswereofgreatimportanceas watersourcesintheancientworldandmanywerekarst springs,fedbyobviouscavepassages.Theancientwriters werealsoawareofaversionofthehydrologiccycle, perhapsbestsaidinEcclesiastes(Chapter1,verse7).‘‘All theriversrunintothesea;yettheseaisnotfull;untothe placefromwhencetheriverscome,thithertheyreturn again.’’Itwasnot,however,ourcontemporaryhydrologic cycleinwhichwaterevaporatesfromthesea,driftsover land,andfallsasrain.Themeansbywhich‘‘thitherthey returnagain’’werethoughttobecaves. AfterthelonghiatusoftheDarkAges,oneofthemost elaboratemodelsforcavernousflowofgroundwaterwas proposedbyAthanasiusKircherinhis MundusSubterraneus in1664.Kircherproposedthatwaterfromthesea movedthroughanelaboratesystemofconduitsto dischargeintolargecavernouschambersintheheartsof mountainsfromwhichitemergedasspringsattheheadsof rivers.Kircheralsopostulatedsubterraneanfiresandwhen thefeederconduitspassednearthefires,thewateremerged ashotsprings.Springsandundergroundriversacquired alargeliteraturepriortotheextensiveworkthatappeared inthelate1800sandearly1900s.SeeShaw(1992), especiallyChapters13and14. T HE E ARLY E UROPEAN V IEWSOF K ARST A QUIFERS TwodevelopmentstookplaceinEuropeinthelatter yearsofthe19 th Century.Onewasthebeginningof systematiccaveexplorationespeciallybySchmidlin AustriaandMartelinFrance.Thesecondwasthe emergenceofgeomorphologyasascience.Geomorphology hadtwofathers–WilliamMorrisDavisintheUnited StatesandAlbrechtPenckinVienna,Austria.Thesetwo toweringintellectslaidthefoundationsofgeomorphology WilliamB.White–Abriefhistoryofkarsthydrogeology:contributionsof theNSS. JournalofCaveandKarstStudies, v.69,no.1, p.13–26. JournalofCaveandKarstStudies, April2007 N 13

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andbothhadatleastapassinginterestinkarst.Theyeven participatedinajointexcursionthroughtheAdriatickarst in1899(Davis,1901).Penck’sinfluenceonkarstresearch wasamplifiedbyhisstudentJovanCvijic withhis1893 Das Karstpha ¨nomen ,althoughasequenceofcircumstances greatlydelayedfinalpublicationofhisideas(Cvijic 1960).AnotherPenckdisciple,AlfredGrund,wasthe primarycontributortooneofthemainEuropeanviews ofkarsthydrology.Davis’influenceonkarstresearch remainedminoruntilhisclassicinterpretationofcave originspublishedmanyyearslater(Davis,1930). Europeanthoughtonthebehaviorofwaterinkarst aquifersdividedintotwodistinctschools(Roglic ,1972). Thekarstgroundwaterschool,championedbyGrund (1903),wasthatsinkingstreamsdraineddowninto acentralbodyofgroundwater.Thegroundwaterbody hadawatertablethatrosecontinuouslyfromtheseainto thehinterlandsandwasessentiallystagnant.Underground streamswereperipheraltothemainwaterbody.The opposingviewwasthatwaterdrainedthroughthekarstas independentrivers,flowingatdifferentlevels,andeventuallydrainingthroughspringswithnocommongroundwater.Inmanywaysthesewereanessentiallyphreatic conceptandanessentiallyvadoseconcept.Theindependentundergroundriverconceptwassupportedbythose withthegreatestexperiencewithcaveexplorationandthe observedbehaviorofcaverivers(vonKnebel,1906; Katzer,1909;Martel,1910).Asisfrequentlythecasein geologicaldebates,bothsideswerepartiallycorrect.Later streamtracingresultsshowedthatmanyalpinekarst regionswithrushingundergroundriversalsocontained adeeperandmoreslowlymovinggroundwaterbody(Zo ¨tl, 1961). E ARLY V IEWSOF K ARST A QUIFERSINTHE U NITED S TATES DiscussionofcavesintheUnitedStatesoftenbegins withtheDavis(1930)cave-originpaper.But,infact, studiesofwaterresourceswerewellunderwayinthe UnitedStatesearlyinthe20 th Centuryandmanyofthese studieswereofkarstareas.TherewasGreene(1908)on southernIndiana,Matson(1909)ontheKentuckyBlue Grass,Weller(1927)ontheMammothCavearea,and Piper(1932)ontheCumberlandPlateauofTennessee.All ofthesereportsrecognizedtheroleofjointsandbeddingplanepartingsaspermeabilityinotherwiseimpermeable massivelimestones.Allrecognizedtheinterrelationshipsof sinkingstreams,cavestreams,andsprings.Ingeneral, thesepaperspresentedareasonablequalitativepictureof themovementofgroundwaterinkarstaquifers. Thehydrologyoflimestoneterraneswasrecognized asadistinctsubdivisionoftherapidlygrowingscience ofgroundwaterhydrology(orhydrogeology)inOscar Meinzer’sclassicbook(Meinzer,1942;Swinnerton,1942). However,theDavismonographrecasttheframeworkfrom oneofsinkingstreams,caves,andspringstooneinwhich caveswereremnantfeaturesformedbeneatholdpeneplains andonlyfortuitouslyre-excavatedandusedbycontemporarydrainage.Debateshiftedtothevadose/phreatic mechanismforcaveoriginandtherewerefewerinvestigationsfromahydrologicalperspective. T HE T RANSITIONAL P ERIOD 1942–1966 JHarlanBretz’s(1942)monographmarkedtheendof theearlyperiodforbothkarsthydrologyandcave-origin theory.Thesucceedingseveraldecades,which,curiously, extenduptotheappearanceofthe25 th anniversaryvolume oftheNationalSpeleologicalSocietyBulletin,were aperiodoftransition.Davies’(1966)ownreviewofthe earthsciencesandspeleologyhaslittletosayaboutkarst hydrology.But,infact,thedryperiodfrom1942to1957 hadendedandthemodernperiodofkarstresearchin generalandkarsthydrologyinparticularwaswell underway. OneofthetransitionalmarkerswasDavies’(1960) demonstrationthatcavesaregradedtopresentorpast localbaselevels.Otherthanit’simplicationsforthetheory ofcaveorigin,thispaperreturnedcavestotheirproperrole inthehydrologyofcontemporarykarst-drainagebasins.In Europe,karsthydrologywashighonthelistofpriorities fortheInternationalHydrologicDecade,1964–1974. Researchshiftedfromqualitativedescriptionsofcave systemsandkarstaquiferstoquantitativemeasurements onaquiferpropertiesandgroundwatermovement(IASH, 1965).Thechangeinapproachwasnicelydescribedin BurdonandPapakis’(1963) HandbookofKarstHydrology Unfortunately,thisexceedinglyimportantdocumentappearedonlyasamanualforaUNtrainingcourseand neverappearedasamoreformalpublication.AsacontributiontotheIHD,StringfieldandLeGrand(1969) preparedacomprehensivereviewofkarsthydrology mainlyintheUnitedStates. Itwasatthebeginningofthetransitionalperiodthat theNSSandsystematiccaveexplorationandsurveygot underway.Bytheendoftheperiod,systematiccavedata hadbeenpublishedforseveralstatesincludingCalifornia (Halliday,1962),Illinois(BretzandHarris,1961),Indiana (Powell,1961),Maryland(Davies,1950),Missouri(Bretz, 1956),Pennsylvania(Stone,1953),Tennessee(Barr,1961), Texas(P.J.White,1948),Virginia(Douglas,1964),and WestVirginia(Davies,1949).Conditionswereinplacefor ameldingofthegroundwaterhydrologist’sapproachto karstaquifersandthecaver’sapproachtokarstaquifers. Whathashappenedinthesucceeding40yearsisthetopic fortheremainderofthisreview. C AVE E XPLORATIONAND S URVEY :AN EW P ERSPECTIVE Caveexplorationintheolddayswasastraightforward business.Caverswenttoareaswheretherewereknown caves,talkedtofarmers,hunters,andthegood-old-boys hangingoutatthegeneralstore,andwithsomeluckwere A BRIEFHISTORYOFKARSTHYDROGEOLOGY:CONTRIBUTIONSOFTHE NSS 14 N JournalofCaveandKarstStudies, April2007

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instructedastowheretheycouldfindnewcaves.Having hikedacrossthefieldsfollowing‘‘overyonderinthat clumpoftrees,’’theywouldsometimesberewardedwith anicenewentranceyawningattheheadofawooded ravine.Explorationwasamatterofpokingthroughallof theaccessiblepassages.Somewouldendinbreakdown. Somewerechokedwithsedimentsandsomebyflowstone. Regardless,allcaveswerethoughtofasending.Some cavesdescendedtoflowingstreamsandsomedidnot. Somecaveswereenteredatspringmouthsoratstream sinks.Otherswereenteredhighonthehillsides.Regardless, allcavesweretalliedseparately.Cavecatalogsandcave databaseslistedasseparatecavesthosethatwereclearly fragmentsofaoncecontinuousmastercave.Likewise, everypassagethatcouldbeaccessedthroughthesame entrancewasconsideredtobepartofthesamecave.A largecavemightcontainhighlevelpassagesdatingfarback intothePleistoceneandalsobaselevelstreampassages thatarepartofthecontemporarydrainagesystem.No matter,itwasconsideredtobeasinglecave. Sometimeinthe1960scamethegradualrecognition thatcavesingeneraldonotend.Cavepassagesare fragmentsofconduitsthatoncecarriedwaterfromsome rechargearea,possiblyasinkingstream,toanoutletat aspring.Theseoncecontinuousconduitsarebrokenupby processesofcollapse,truncationbysurfacevalleys,and bysedimentin-filling.Thisgradualrealizationwasnot adocumenteddiscoveryalthoughBrucker(1966)formalizeditasawayofsplicingtogetherthepassagefragments thatmakeupwhatwasthentheFlintRidgeCaveSystem. Withthisunderstanding,itbecamepossibletoconsider individualcavesassimplypuzzlepiecesofalargermaster drainagesystem. Withtheinsightofcontinuousconduits,caveexplorers couldsearchforthemissingpieces,eitherbydigging, movingbreakdown,sumpdivingwithinthecaveorby excavatingnewentrancesfromthesurface.Sometimes alongandpersistenteffortpaidoffwithamapofanentire drainagebasin.Overthepast40years,aconsiderable numberofexampleshavebeendocumented.Oneexample istheMysteryCave–RimstoneRiverCavecomplexin PerryCounty,Missouri(Fig.1).Extensiveexplorationand surveyhaveproducedadetailedmapof40kmofmainly twosouth-northmasterstreampassagesalongwithmany morekilometersofdisconnectedcavefragments(Walsh, 1988,1989).Thosewhothinksuchdataareeasytoobtain areadvisedtoreadWalsh’s(2002)accountoftheactual historyoftheexplorationandsurvey. C AVE M APSAND M APPING Perhapsthecaver’sgreatestcontributiontokarst hydrologyistheircurrent‘‘mapasyougo’’philosophy. Fromtheearliestdays,cavershavepreparedcavemaps. Thereasonissimple.Onthelandsurface,aviewfrom ahighridgeoranoverflightinasmallplanegivesan excellentperspectiveofthelandscape.However,one cannotseeacave.Acavercanseeonlyasmallsectionof passageatanyonetime.Withoutmapping,caversmust dependonmemoryandhavenowaytoaccuratelydisplay thelayoutofthecaveortosharetheirdiscoverieswith others. Anaccuratetraverselineisimportantbutsoalsoisan accuratesketch.Forgeologicalorhydrologicalinterpretationofcavemaps,itistheaccuracyofthesketchingthatis mostuseful.Oneoftheearlypioneersinpreciserenditions ofcavepassageswasthelateBernardSmeltzerin Pennsylvania.Oneofthefinestexamples,drawnin1951, istheFlemingCavesinHuntingdonCounty(Fig.2).There isaccuratefloordetail,thewallsaresketchedwithan artist’seye,andthecrosssectionsshowtherelationofthe cavetothestructureofthebedrock.Otherpioneerswere PaulJohnson,TexYocum,LangBrod,andtheir colleaguesintheMissouriCaveSurvey,whoseoutstanding mapsbeganappearingintheearlyissuesof Missouri Speleology inthelate1950sandearly1960s. Therehavebeengreatstridesintheprocessingand displayofcavesurveydata.Computerprogramsare availableforcompiling,plotting,andadjustingclosure errors.Mapscanbedisplayedelectronicallysothatthey canbeexpanded,contractedandrotated.Mapsstored electronicallycanhaveembeddedphotographsoradditionalpassagedetail.Behindthecomputationalmagic, however,theprimarydatasourceremainsthecompassand tapemeasurementsandthenotebooksketchesofthecavers patientlysloggingtheirwaythroughthecave,stationby station.Fromthepointofviewofthehydrogeologicaluse ofcavemaps,currentconcernswithcaveconservation haveanunfortunatesideeffect.Mostoftheearlycave databases,suchasthosereferencedabove,werepublic documents,manyevenpublicdomaindocuments.As populationhasincreasedoverthepast40years,accessto caveshasbecomemorelimitedatthesametimethatsport cavinghasbecomemorepopular.Cavemapsandcavedata baseshavebecomeproprietaryinformation,oftenhighly restricted.Hydrogeologicinvestigationsthatrequireaccess toextensivequantitiesofcavesurveydataalsorequire investigatorstoestablishconfidenceandgoodworking relationswiththecavingcommunity. C AVE D IVING Theactiveconduit-drainagesystemscanoftenbe accessedeitherfromcaveentrancesatstreamsinksor fromcaveentrancesatspringmouths.Unfortunately,these accessedcavesoftenterminateatsumps.Asequipmentand techniquesforSCUBAdivinghaveimproved,manyof thesesumpshavebeenpenetratedtothegreatimprovementofourunderstandingofconduitsystems. FordandEwers(1978)laidtorestthevadose/phreatic debateofthe1930sbyshowingthatcavescouldformin anyrelationtothewatertabledependingonthelocal geologicsetting.Oneofthemostcommongeologicsettings wasabeddingandfractureguidedconduitthatwould,at W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 15

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baseflow,consistofasequenceofair-filled,open-channelflowcavesegmentsinterspersedwithflooded,pipe-flow segments.Anysegmentthathappenedtohaveanentrance wouldappearasastreamcavesumpedbothupstreamand downstream.Anumberofsuchconduitshavebeen exploredbydiversandindeed,sumpsareoftenrelatively shallow,relativelyshort,andlinksegmentsofair-filled streamcave.Divingalsoshowstheexistenceofdeep conduitswellbelowpresentdaybaselevels. Anexampleofthevalueofdivingaspartof ahydrogeologicalinvestigationisTytoonaCave,Blair County,Pennsylvania,nowanNSSCaveNaturePreserve (Fig.3).TheentrancetoTytoonaCave,inakarstwindow, givesaccesstoabout300metersofopenstreamway.Atthe endisasump,followedbyachamber,asecondsump, asmallchamber,athirdsump,andfinally,along streamwayendinginafourthsump.Fromtheresurgence end,atArchSpring,thereisimmediatelyadeepsump, thenastreamwayendinginadeepsumpwhichislikelythe downstreamendofthe4 th sumpinTytoonaCave.The diverÂ’ssketchmaphererevealsboththeundulating pipe/openchannelflowsystemandalsothepresenceof adeepsystemintowhichthepresentdaydrainagehas collapsed. Figure1.StickmapofMysteryCave,RimstoneRiverCave,andassociatedsm allercavesinPerryCounty,Missouri.These collectionsofcavesrepresenttwomasterdrainagelinescarryingwatern orthtoCinqueHommesCreek.FromWalsh(2002). A BRIEFHISTORYOFKARSTHYDROGEOLOGY:CONTRIBUTIONSOFTHE NSS 16 N JournalofCaveandKarstStudies, April2007

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T RACER T ECHNOLOGY Theroutesofundergroundstreamsfromtheirsurface sourcestotheiremergenceinspringshavebeentracedby avarietyofmethodssincethe19 th Century.Theoriginal methodwastoaddlargequantitiesofdye,oftentensor hundredsofkilograms,atthesinkpointandwaitfor coloredwatertoappearatthespring.Inadditiontothe necessityofhavingobserversstationedatallpossiblerise points,springsandstreamswereoftenturnedgreenorred tothegreatconsternationoflocalcitizensandthe authorities.Althoughothertracerssuchassporesandsalt brinesareoccasionallyused,fluorescentdyeshave remainedthetracerofchoice,althoughwithmanymodern improvements. Thefirstmajorinnovationwastheinventionofthe charcoaldyereceptorbyJ.R.Dunn(1957).Dunn discoveredthatactivatedcoconutcharcoalwouldeffectivelysorbdyefromwaterandmoreimportantly,would notreleasethedyeasmorewaterflushedoverit.This meantthatinexpensivecharcoalpacketscouldbeplaced inallsuspectedresurgencesandcollectedattheinvestigatorÂ’sconvenience.Thedyecouldbeelutriatedwithan alcoholicsolutionofstrongalkalianditspresence determinedbythecolororbythefluorescenceofthe elutriate.Charcoalpacketseliminatedtheneedfor continuousobservation.Thecharcoalalsoaccumulated dyeasthepulsepassedby,thusallowingsmallerchargesof dyetobeusedsothatvisualcoloringoftheresurgenceis unnecessary. Figure2.MapofFlemingCaves,HuntingdonCounty,Pennsylvania.ABernar dSmeltzermapillustratingtheearly presentationofgeologicdetail.MapfromthefilesofthePennsylvaniaCa veSurvey. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 17

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Thesecondmajorinnovationwastheuseofquantitativefluorescencespectroscopytoidentifydyesanddeterminedyeconcentrations.Agreatvarietyofdyeshave beenusedforwatertracingalthoughonlyafeware routinelyused(Table1).Eachhasacharacteristicfluorescencepeakwavelength.Bymeasuringthefluorescence spectruminsteadofsimplyobservingthecolor,multiple dyescanbedistinguishedatthesametime.Fluorescence bandsoforganicdyesarebroadandoverlap,butbecause theline-shapeisGaussian,computerprogramssuchas Peak-Fitcanbeusedtoseparatethedyefluorescence bandsandthusdeterminedyeconcentrationsofeach.Thus multipleinjectionpointsaswellasmultipleresurgence pointscanbetested. Athirdmajorinnovationwastheintroductionof quantitativetestsusingautomaticwatersamplers.Because ofthehighsensitivityofmodernspectrofluorophotometers,smallconcentrationsofdyecanbemeasured directlyfromwatersamplesratherthanfromcharcoal elutriates.Bycollectingwatersamplesatregulartime intervalsandanalyzingdyeconcentrationsineach,adye breakthroughcurvecanbeconstructedthatdisplaysthe dyetraveltimeandsometimesgivesinformationonthe geometryoftheflowpath(Jones,1984). Dyetracingisoneofthemostpowerfultoolsinthe karsthydrogeologist’stoolkit.Followingtheintroduction ofcharcoaldyereceptors,thedrainagepatternsformany undergrounddrainagesystemswereworkedout.The SwagoCreekbasininWestVirginia(Zotter,1963)was anearlyexample.Contaminanttransportoverdistancesof tensofkilometerswasdemonstrated(Aley,1972).Withthe increasedsensitivityofmodernspectrofluorophotometers, dyedetectionlimitsreachedthepartpertrillionlevel.With highsensitivitycamethenecessityforcarefulprotocolsfor dyeinjectionandrecoverytoavoidcross-contamination andmisleadingresults.Useofdyetracinginlegaland regulatoryissuesforcedmorecarefulattentiontoquality controlandchain-of-custodyissues.Dyetoxicitybecame anissuefairlyearly(SmartandLaidlaw.1977;Smart, 1984)andsomeotherwiseusefuldyeswererejected. Moderndyetracingrequiresawell-equippedlaboratory andagreatdealofpracticalexperience.Butinspiteofthe elaborateprecautionsneededandtheequipmentrequired foranalysis,thedetailsoftheproceduresaredescribed mainlyinreportsandprivatepublications(Alexanderand Quinlan,1992;Field,1999;Aley,2002).Europeanpractice, however,islaidoutindetailbyKa ¨ss(1998). T HE C ONCEPTUAL D ESCRIPTIONOF K ARST A QUIFERS Atthetimeofthe25 th anniversaryBulletin,karst hydrologywasprettywelldividedintotwocamps.There Figure3.ProfileofTytoonaCave–ArchSpring,BlairCounty,Pennsylvani a.ConstructedfromsketchesbyJohnSchweyen andotherdivers.Entranceandspringelevationsbyaltimetermeasuremen t. Table1.Somecommonlyusedtracerdyesforwatertracing. CommonNameColorIndex FluorescenceWavelength(nm) a ElutriateWater Sodiumfluoresceine(uranine)AcidYellow73515.5508 EosinAcidRed87542535 RhodamineWTAcidRed388568.5576 SulphoRhodamineBAcidRed52576.5585 FluorescentBrightener351TinopalCBS-X b 398397 DatacourtesyofCrawfordHydrologyLaboratory,WesternKentuckyUniver sity. a Fluorescencewavelengths(intensity)varysignificantlywithdifferin ginstrumentsandmanyofthelistedvalueswillbefoundtobeinvariancewi threportedfluorescence wavelengthsinotherpublications(e.g.,fluorescencewavelengthforso diumfluoresceininwateristypicallyreportedtobe512nm(theeditor). b CommonNameforTinopalCBS-Xprovidedbytheeditor. A BRIEFHISTORYOFKARSTHYDROGEOLOGY:CONTRIBUTIONSOFTHE NSS 18 N JournalofCaveandKarstStudies, April2007

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weretheprofessionalhydrogeologists,welleducatedinthe intricatemathematicaldetailsofgroundwaterbehaviorin porousmediaandtherewerethecavers,notyetquiteready tocallthemselveshydrogeologists.Theprofessionals drilledwells,ranpumptests,andmadecalculations. Sometimes,aswhentheydrilledintoahighlyfractured dolomite,theygotreasonableresults.Sometimes,aswhen theydrilledintoawater-bearingconduit,theirresultswere nonsense.Therewasaconsiderableeffort(Whiteand Schmidt,1966)toconvincetheprofessionalcommunity thatundergroundstreamshadsomethingtodowith hydrology.Caverswereaccumulatingmapsanddataon streamsinks,springs,andunderground-drainagepatterns, butgenerallydidnÂ’tpaymuchattentiontothemassofrock thatsurroundedthecaves.Oneofthemostimportant accomplishmentsofthepast40yearshasbeenmerging thesedivergentpointsofview. T HE G ROUND -W ATER B ASIN C ONCEPT Theframeworkfordiscussionofgroundwateristhe aquifer.Aquifersarecharacterizedbythedistributionand anisotropyofhydraulicconductivityamongthevarious rockunitsthatmakeuptheaquifer.Aquifersoftenhave well-definedthicknesses,butrarelyisoneconcernedwith theareaofanaquifer.Theframeworkfordiscussionof surfacewateristhedrainagebasin.Drainagebasinshave well-definedareasandacertainpatternofstreamchannels. Forgeologicsettingsotherthankarst,groundwater conceptsandsurface-waterconceptsrarelyintersect.In karsttheyarecompletelyentangled. Justasthenotionofreconstructingconduitsfrom observablecavescreptintokarstthinkingwithoutmuch notice,soalsodidtheconceptofthegroundwaterbasin. Atsometimeitbegantooccurtokarstresearchersthatit wasmoreprofitabletothinkofkarsthydrologyinterms ofdrainagebasinswithbothsurfaceandsubsurface componentsratherthanthinkingofakarstaquifer.For themostpart,itwasaconceptintroducedbycavers becauseitprovidedguidanceaboutwheretosearchfor newcaves.Certainlytheconceptwasestablishedwhen Jones(1973)wrotehisreportonthekarst-drainagebasins inGreenbrierCounty,WestVirginia.Joneswasoneofthe firsttouseextensivedyetracingtomapouttheentire drainagesystemandsubdividespringcatchmentsinto distinctgroundwaterbasins.Anevenmoreelaborate groundwaterbasinmapwaspreparedbyQuinlanandRay (1981;QuinlanandEwers,1989)fortheMammothCave areainsouthcentralKentucky.Undergrounddrainagein southcentralKentuckyflowseithernorthwesttothe GreenRiverorsouthwesttotheBarrenRiver.Quinlan andRayusedcavedata,geologicdata,morethan500dye traces,and1400wellobservationstosubdividethe MammothCaveareainto28groundwaterbasins,show themainflowpaths,andcontourthewatertable.Many groundwaterbasinshavenowbeenmapped,especiallyin WestVirginia(Jones,1997)andintheseriesofdrainagebasinmapsforKentuckycompiledbyJ.A.RayandJ.C. Currens. Ifthegroundwaterbasindividecanbeaccurately established,thebasinareacanbemeasured.Precipitation withinthebasinanddischargefromthebasincanbothbe measured.Essentially,theexistenceofabasinboundary putsamass-balanceconstraintonwatermovingthrough thesystem.Thevariousstatisticsdevelopedforsurfacewaterbasinscanbeappliedtogroundwaterbasins.Ifthe basinofinterestdischargesataspring,thespringcanbe gaugedandarecordofdischargeestablishedoverlong periodsoftime.Fromthesedatacanbecalculatedthe meanfloweitheroveronewateryearorovertheentire periodofrecord,themeanbaseflow,andthemeanannual peakflow(knownastheannualfloodforsurfacebasins). Thenormalizedmeanbaseflowisthebaseflowdividedby thebasinarea.Thisquantityhasbeenfoundtobe unusuallysmallforkarsticbasinscomparedwithother surfacewaterbasins(E.L.White,1977)becauseofthelow hydraulicresistanceoftheconduitsystemwhichallowsthe aquifertodrainduringperiodoflowrecharge.If anumericalvalueforthenormalizedmeanbaseflowcan beestablishedforagivenregion,thebasinareasofother springscanbecalculatedbysimplymultiplyingthe measuredmeanbaseflowofthespringofinterestbythe normalizedmeanbaseflowfortheregion.Acomparison ofvariousbasinsbyQuinlanandRay(1995)showedthat thissimplecalculationworkswellifthelocalhydrogeology istakenintoaccount.Thecalculationisapowerfulcheck onspringgroundbasinareasestimatedbyothermethods. Theboundariesofsurfacewaterbasinsareusually clearlydefinedbytopographichighsandcanbeeasily drawnfromtopographicmaps.Theboundariesofgroundwaterbasinsaremoreproblematic.Theboundariesof contributingsinking-streambasinscanbedelineated,but boundariesthroughthekarstmustbeinferredfromknown streamcaves,fromtracertests,fromthelocalgeologyand fromwater-tablemapsconstructedfromdepth-to-water measurementsinwells.Unlikesurface-basinboundaries, groundwaterbasinboundariesmayshiftwithincreasingor decreasingdischarge.Generally,highgradientbasinshave themostsharplydefinedboundarieswhereaslow-gradient basinsmayhavefuzzyboundaries.Tracertestsnearthe basinboundariesmayindicateflowintoseveraladjacent basins.Piracyroutesandhigh-dischargespill-overroutes arealsocommon. P OROSITYAND P ERMEABILITY Thetreatmentofakarstsystemasagroundwaterbasin leadstocertaininsights.Treatmentofthekarstsystemas anaquiferleadstootherinsights.Thesetwoconceptual frameworkshaveexistedcomfortablyside-by-sideforthe 40yearperiodofthisreview.Themostfundamental propertiesofanaquiferareitsporosityandpermeability.It wasrecognizedearlyonthatthepermeability(orporosity) ofkarstaquifershasthreecomponents:thematrix W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 19

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permeabilityofthebedrockitself,thepermeabilityproducedbyfractures(joints,jointswarms,bedding-plane partings,andsomefaults),andthepermeabilitydueto conduits.Thishasnowbeensomewhatformalizedand researchersspeakofthetriplepermeabilitymodel (Worthington,1999). Thematrixhydraulicconductivitiesofmostcompacted limestonesareintherangeof10 9 –10 11 ms 1 andfor mostpracticalpurposescanbeignored.Theexceptionsare theyounglimestones,especiallythoseoncarbonateplatforms,thathaveneverundergonedeepburialorbeen subjecttoorogenicforces.Forthese,thematrixpermeabilitiesareintherangeof10 6 to10 7 ms 1 andmatrix flowisanimportantcomponent.Forinformationonthe hydrogeologyofyounglimestonesseeMartinetal.(2002). MatrixflowinporouslimestonesisDarcianandnot intrinsicallydifferentfromflowinotherporousmedia. Limestonesanddolomitesarebrittlerocksandsubject tofracturingbytectonicforcesandbystressreliefcaused byeithererosionorglacierunloading.Fractureflowoccurs inotherbrittlerockssuchassandstonesandgranites. Groundwaterinfracturesisamajorcomponentofthe storedwaterandisthereasonthatwellsdrilledinto limestoneoftenproduceusefulquantitiesofwaterwithout thewellhavingpenetratedaconduit.Fractureflowis amajoremphasisincontemporaryhydrologicalresearchas attemptsaremadetomodelfractureswithirregular aperturesandalsotomodelfracturenetworks. Thepracticalboundarybetweenfracturepermeability andconduitpermeabilityoccursatanapertureofabout onecentimeter.Ingroundwaterbasinswithtypical gradients,aone-centimeteraperturecorrespondstothe onsetofturbulence,tovelocitiessufficienttobeginto transportclasticsediment,andtoanincreaseintherateof dissolutionofthecarbonaterock.Cavesasconduit fragments,canbemappedbyhumanexplorersdownto anapertureofabout0.5m.Between0.01mand0.5mare solutionopeningsthataretoosmallfordirectmappingbut largeenoughtobehavehydraulicallyasconduits.Very littleisknownabouttheconduitporosityinthissizerange. Someinsightintotheflowbehaviorcanbeobtainedfrom thedistributionoftraveltimesobtainedfromtracertests (Fig.4).Thedistributionislog-normalwithaconsiderable tailofthelowvelocityside.Thesemeasurementsmay indicatetracerdyesmovingthroughsmallandhencelow velocitypathways. I MPORTANCEOFTHE G EOLOGIC F RAMEWORK Theflowofwaterthroughkarstaquifersisdetermined byrelativelysimpleprinciplesoffluidmechanicsandthe interactionofthewaterwiththecarbonatebedrockby relativelysimpleprinciplesofphysicalchemistry.Asin mostoftheEarthsciences,thedevilisinthedetails.Oneof thosedetailsthatwaswidelyoverlookedintheearly developmentofkarsthydrologywasthegeologicsetting. Whatkarsticrocksareavailableandhowarethey arrangedwithrespecttootherrocks?Anykarstgroundwaterbasinisaworkinprogress.Itevolvedfromsome precursorbasintoitspresentconfigurationandthepresent configurationwillevolvefurtherintothefuture.The hydrologyofthebasiniscontrolledtoalargeextentbythe underlyingstratigraphyandstructure. Thegeologicalvariablesthatdistinguishonekarst drainagebasinfromanotherinclude: N Thicknessofkarsticrockunits N Placementofkarsticrockswithrespecttonon-karstic rocksandlocationwithindrainagebasin N Bulklithology:limestone,dolomiteorgypsum N Detailedlithology:micriticlimestone,crystallinelimestone,shaleylimestone N Stratigraphichomogeneity:beddingthickness,lithologic variations,shaleorsandstoneconfininglayers N Largescalestructure:folds,faults N Smallscalestructures:densityandconnectivityof verticaljoints,beddingplanepartings,fewmaster fracturesvs.manysmallerfractures Agreatvarietyofkarstdrainagebasinsispossible dependingonthelistedparameters.Avarietyofplacementsofkarsticrockswithrespecttootherstratawere describedearlyinthereviewperiod(White,1969)andthese possibilitieshavebeenembellishedbyothers.Mostofthe karstofeasternUnitedStatesisdevelopedinatmostafew hundredmetersoflimestoneproducingfluviokarstlandscapes.InlocationssuchastheCumberlandPlateauorthe OzarkPlateau,thecombinationoflowdip,limestones locatedundervalleyfloorsandonvalleywalls,and aprotectivesandstoneandshalecaprockontheplateau surfaceprovidesidealconditionsforthedevelopmentof longcavesandverticalshafts.Otherlocationssuchasthe foldedAppalachians,withcarbonaterocksmainlyinthe Figure4.Distributionoftravelvelocitiesasdetermined from2877tracertestsbetweensinkingstreamsandsprings. FromWorthingtonetal.(2000). A BRIEFHISTORYOFKARSTHYDROGEOLOGY:CONTRIBUTIONSOFTHE NSS 20 N JournalofCaveandKarstStudies, April2007

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valleyfloors,producestrike-orientedcavesandmore limiteddrainagebasins. Themostrecentcalculationsoncavedevelopment (Dreybrodtetal.,2005)showthatthepatternsofconduitdrainagesystemsaredeterminedduringtheinitiationphase ofcavedevelopment.Atthistime,thesystemishighly sensitivetodetailsofthefracturepatternandtothe presenceofconfininglayers.Afewcentimetersofshale interbeddedinthelimestoneissufficienttodeflectthe initialpathwaythatwilllaterbecomeacavepassage. Agreatdealoftheliteratureonkarsthydrology consistsofstudiesshowinghowaparticulardrainage basindevelopedinresponsetoitsspecificgeologicsetting. Q UANTITATIVE H YDROLOGY :S PRING H YDROGRAPHS Theflowofkarstspringsisoftenvariable,risingand fallinginresponsetostorms.Somespringsbecomemuddy duringstormflow.Springscanbegaugedtoproduce acontinuousrecordingofdischargeasafunctionoftime, acurveknownasahydrograph.Thewaterflowingfrom aspringrepresentsacompositeofallinputsandflow systemsupstreaminthebasin.Useofspringhydrographs tocharacterizekarstaquifersdevelopedearlyinEurope (BurdonandPapakis,1963;Milvanovic ,1981)andhas beendevelopedtoaconsiderablemathematicalelegancein France(Mangin,1984;Labatetal.,2001).Onlyinthe 1980sandlaterwerespringhydrographsextensivelyused intheUnitedStates.Inpart,thiswasnotduetoignorance buttothefactthatmostkarsthydrologyresearchwas beingconductedbyacademicsandcaversonshoe-string budgets.Continuousstagerecordingwasdesirablebutnot financiallyachievable. Examinationofalargenumberofspringdischarge recordsrevealsarangeofresponsesonascalebetweentwo end-members.Therearekarstgroundwaterbasinswith veryrapidresponsetimessothatthespringhydrograph haspeakscorrespondingtoeachindividualstorm.The otherextremearespringsthatexhibitessentiallyno responseatalltoindividualstormsandatbestriseand fallalittleinresponsetowetanddryseasons.Inbetween arehydrographswithvaryingdegreesofresponse(Fig.5). Theaquifercharacteristicsthatcontrolhydrograph patternarenotcompletelyunderstood.Theveryflashy responsewithindividualstormpeaksrequiresasmallopen aquiferwithanoveralltransporttimefromrechargeto springlessthatthespacingbetweenstorms.Lesswellresolvedhydrographscanarisefromaquiferssufficiently largesuchthatindividualstorminputsaredampedbefore theyreachthespring.Hydrographswithlittlestormdetail canarisefromaquifersinwhichmostoftherechargeis throughtheepikarstwhichtendstoholdwaterin temporarystorage.Springsfedbyfractureflowwillhave lessdetailintheirhydrographs,butaflathydrographis notevidencefortheabsenceofconduits.ThebigFlorida springshavealmostnodetailintheirhydrographsbut mostareknowntobefedbyverylargewater-filled conduits. Suddenintensestormsthatfollowseveralweeks withoutrainarethebestprobesofaquiferbehavior. Figure6illustratesschematicallytheparametersthatcan bemeasured.Thelagtimebetweenthestormandthetime thatstormwaterappearsatthespringisameasureof traveltimeonlyiftheconduitisanopenstreamwayfrom sinktospring.Ifalloraportionoftheconduitisflooded, risingheadattheupstreamendwillcausewaterto dischargefromthedownstreamendrespondingto apressurepulsethattravelsthroughthesystematthe speedofsound.Thetimebetweenthestormandincreased flowatthespringcanbeveryshort.Theratioofthe maximumflowtobaseflowisameasureoftheflashiness oftheaquifer,althoughthisratioalsodependsonstorm intensity.Therecessionlimbofthehydrographcanusually befittedwithanexponentialcurve(orseveral).Thefitting parameterfortheexponentialhasbeencalledthe exhaustioncoefficientandhasbeenused(Burdonand Papakis,1963)tocalculatethevolumeofwaterheldin dynamicstorage.Theinverseoftheexhaustioncoefficient hasunitsoftimeandcanbetakenastheresponsetimeof theaquifer. C HEMICAL H YDROLOGY Onofthemostimportantaccomplishmentsofthe 40yearperiodwastoworkoutthechemistryofcarbonate dissolutioninconsiderabledetail.Theequilibriumchemistryofbothdissolutionandprecipitationcamefirstandis describedindetailinseveraltextbooks(White,1988; Langmuir,1997).Theequallyimportantkineticsof dissolutionandprecipitationrates,althoughmorecomplicatedandnotsosolidlyestablished,hasbeenlargely workedout.Thedissolutionratesofcarbonateminerals areimportanttomanyareasofscience,resultinginahuge literature.MuchofithasbeenreviewedbyMorseand Arvidson(2002).Dissolutionkineticscombinedwithflow hydraulicsformsthebasisforcurrenttheoriesofspeleogenesis.AmajorcontributorhasbeenWolfgangDreybrodtandhisstudentsandcollaboratorsattheUniversity ofBremeninGermany(Dreybrodtetal.,2005).Studiesof speleogeneticprocessescanbeconsideredaquifermodeling alongthetimeaxisbycalculatingtheevolutionofthe conduitpermeabilitythroughasequenceofinitiation, enlargement,stagnation,anddecayphases.Although muchasbeenaccomplished(Klimchouketal.,2000),this subjectisoutsideofthescopeofthepresentreview. Althoughmanyanalysesofkarstwatershadbeen obtained,aboutthebestthatcouldbedonewiththemwas toplottheconcentrationofdissolvedcarbonatesonthe calculatedcalcitesolubilitycurve,whichthengavesome indicationofwhetherthewatersamplewassaturated, supersaturated,orundersaturated(aggressive)withrespect tocalcite.Intheearly1970stherewereanumberofefforts W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 21

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tomoreaccuratelymeasurethesaturationstateofcave waters.Mostsuccessfulofthesewastheintroductionofthe saturationindexandalsothecalculatedCO 2 partial pressure(Langmuir,1971).Thesecalculationsandother aspectsofaqueouschemistryquicklyevolvedintoacollectionofcomputerprogramsthathavecontinuedtoevolve downtothepresenttime(Jenne,1979;Melchiorand Bassett,1990). Inthelate1960sandearly1970stherebeganstudiesof spring-waterchemistryinwhichthespringsweresampled atregularintervals,typicallyoneortwoweeks(Pitty,1968; ShusterandWhite,1971).Thedissolvedcarbonatecontent ofsomespringsremainsessentiallyconstantthroughthe yearirrespectiveoftheseasonortheinfluenceofstorm flow.Otherspringsexhibitawidelyfluctuatingchemistry andalsoafluctuatingtemperature.Thereensuedadebate concerningthecauseofthechemicalfluctuations,with degreeofconduitdevelopment,percentageofsinkingstreamrecharge,andflow-throughtimebeingoffered. ThencametheresultsofDreiss(1989)whomeasured acontinuousrecordofthechemistryofMeramecSpring, Missouri.Itturnedoutthatthefluctuationsobservedin previousstudieswereduetoasmallnumberofsampling pointsextractedfromacontinuouscurve(nowknownas achemograph).Chemographsofcarbonatespeciestypicallyaretheinverseofhydrographsandrepresentthe dilutionoftheresidentwaterintheaquiferbyinjected stormwater(Fig.6).Sincetheirfirstintroduction, chemographshasbeenconstructedformanychemical parametersincludinggroundwatercontaminants. Theconcentrationofdissolvedcarbonatespeciesin karstaquifersisproportionaltothespecificconductanceof thewater.Becausespecificconductanceiseasytomeasure andeasytorecordonadatalogger,suchmeasurements alloweasydeterminationofcarbonatechemographs. Manysuchhavebeenmeasuredand,incombinationwith hydrographs,provideadditionalinformationonaquifer response.Whatisobservedisthatthereisasharprisein thehydrographinresponsetostorms.However,theremay ormaynotbeanequivalentdipinthechemograph.Ifthe Figure5.Somerepresentativehydrographsforkarstsprings.Thesearese lectedfromU.S.GeologicalSurveysurfacewater recordswhichareavailableonline(http://waterdata.usgs.gov).Alley Springisrepresentativeoftheflashy,fast-response springswhereindividualstormeventsappearonthehydrograph.RainbowS pringdisplaysanannualrainyseason/dryseason responsebutdoesnotrespondtoindividualstorms. A BRIEFHISTORYOFKARSTHYDROGEOLOGY:CONTRIBUTIONSOFTHE NSS 22 N JournalofCaveandKarstStudies, April2007

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risinghydrographandfallingchemographarecoincident, itindicatesthattheconduitisanopenstreamwayandthe risinghydrographmarksthearrivalofstormwateratthe spring.Inothercases,thereisadelaybetweentherising limbofthehydrographandthefallinglimbofthe chemograph.Thisdelay,alongwiththespringdischarge, isameasureofthevolumeofwaterpushedoutofflooded conduitsbythestormpulse(RyanandMeiman,1996). C AN K ARST A QUIFERS B E M ODELED ? Attheendofthereviewperiod,muchcontemporary researchonkarsthydrogeologyconsistsofattemptsto constructauseful,perhapsevenvalid,generalmodelfor karstaquifers.Theobjectofanygroundwatermodelisto reducetherecharge,storage,andflowhydraulicsofan aquifertoacomputerprogram.Withanaccuratemodel, oneshouldbeabletocalculatewellyieldsanddistribution ofhydrostaticheadswithintheaquifer,aswellasthe responseoftheaquifertovaryingrechargeandto extractionofwaterforwatersupply.Forakarstaquifer, anaccuratemodelalsoshouldbeabletoreproducethe expectedspringhydrographsinresponsetoaspecified precipitationevent.Muchkarsthydrologicalresearchover thepastseveraldecadeshasbeeneffortstoconstructsuch amodel.Resultshavebeendecidedlymixed.Summariesof someoftheattemptedapproachesmaybefoundinJeannin andSauter(1998)andPalmeretal.(1999). Theguidingparameterforanygroundwatermodelis thehydraulicconductivity.Thehydraulicconductivitycan beanisotropicanddifferentvaluescanbeusedfordifferent rockformations,butitshouldbeconstantwithinthese constraints.Oneofthemostimportantdifficultiesin modelingkarstaquifersisthatthehydraulicconductivityis scaledependent.ItwaspointedoutbySauter(1991)and Quinlanetal.(1992)thathydraulicconductivitiesfor highlykarsticaquiferscanvaryover8ordersofmagnitude dependingonthescaleofmeasurement(Fig.7).Inan aquiferwiththisrangeinvaluesovershortdistances,any attempttoreducetheaquifertoasinglevalueofhydraulic conductivitycanbestbedescribedasnonsense. Withoutgoingintoverymuchdetail,themain approachestokarst-aquifermodelingaresummarized below.Onlyafewkeyreferencesaregiven.Thissubject isbeginningtodevelopaverylargeliterature. E QUIVALENT P OROUS M EDIA M ODELS Standardporous-mediamodelssuchastheUSGS MODFLOWprogramassumethatatlargeenoughscales, theheterogeneitiesofthekarstaquiferaresmoothedout andcanberepresentedbyanaveragehydraulicconductivity.Scanlonetal.(2003)hadsomesuccessinapplying thistypeofmodeltotheEdwardsAquiferinTexas. Equivalentporousmediamodelsworkbestforaquifersin whichthekarstic-flowpathsaredispersedandconsist mainlyofsolutionally-widenedfractures.Theyworkleast wellforaquiferswithwelldevelopedconduitsystems, particularlythosewithlargeinputsofallogenicrecharge. P IPE F LOW M ODELS Equivalentporous-mediamodelsignoretheconduit permeabilityanditslocalizedturbulentflows.Pipe-flow modelsfocusentirelyontheconduitsystem.Pipe-flow modelstreattheconduitsystemasanetworkofpipes Figure6.Schematichydrographandchemographforakarst springshowingvariousmeasurableparameters. Q B base flow. Q max peakflowforthestormhydrograph.Twotime lagsareshown: t LS forthelagbetweenthestormandthe risinglimbofthehydrographand t LC forthelagbetweenthe risinglimbofthestormhydrographandthedipinthe chemograph.Boththerecessionlimbofthehydrographand therecoverylimbofthechemographcanbefittedwiththe functionsshown. Figure7.Dependenceofhydraulicconductivityonthescale ofmeasurement.FromQuinlanetal.(1992). W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 23

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subjecttotheusuallawsoffluidmechanics.Thedrawback ofthepipeflowmodelsisthatconduitsarenotexactly pipes.Theyhavevaryingcrosssections,complicated interconnections,andareoftenfurthermodifiedby breakdownandsedimentinfillings.Muchdetailabout conduitpatternisneeded.However,calculationsoftravel times,headlosses,anddischargesforknownconduit systemshavebeengenerallysuccessful(Halihanand Wicks,1998;Jeannin,2001). C OUPLED C ONTINUUM /P IPE -F LOW M ODELS Eventually,karst-aquifermodelingmustfacethereality ofthecombinedmatrix,fracture,andconduitcomponents ofthepermeability.Theconduitsystemisstronglycoupled tosurfacewaterthroughsinkingstreamsandclosed depressionsandsohasaverydynamicresponsetostorms. Thefractureandmatrixsystemsreceivemostoftheir rechargethroughtheepikarstandhaveaslowerresponse. Adominantcomponentofthetotalflowsystemisthe exchangeflowbetweentheconduitsandthesurrounding fracturedmatrix.Duringstormflow,headsintheconduit systemriserapidlyandwaterisforcedintothesurrounding fractures.Afterthestormflowrecedes,theconduitsystem drainsrapidly,headsreverse,andthewaterstoredinthe fracturesdrainsintotheconduits. Modelshavebeenconstructedinwhichthefractureand matrixsystemisdescribedasacontinuumwithDarcyflow. Theconduitsareputinbyhandanddescribedbypipe-flow models.Thereisanexchangetermthatdescribestheinflux andoutfluxofwaterbetweenthefracturesystemandthe conduits.ThismodelwasdevelopedfortheGallusSpring insouthernGermany(Sauter,1992).Thismodelworked wellinthesensethatitaccuratelyreproducedthestorm hydrographsmeasuredatthespring.Thedrawbackisthat theconduitsmustbeputinbyhand.Tracerstudiesand caveexplorationmustsupplementthestrictlymodel calculation.Continueddevelopmentofthisapproachto modelinghasbeenverypromising(Baueretal.,2003;Liedl etal.,2003). I NPUT –O UTPUT M ODELS Allofthemodelingapproachesdescribedaboverequire considerableknowledgeoftheaquifer–thegeometryof theconduitsystem,thehydraulicconductivitiesofthe fractureandmatrixsystems,andanygeologic-boundary conditions.Ingeneral,themorepre-knowledgeavailable, themoreaccuratethemodel.Ofcourse,ifallavailable knowledgeisusedtoconstructthemodel,theremaybe nothingleftforthemodeltocalculate.Thediametrically oppositeapproachistotreattheaquiferasablackboxand assumenothingaboutitsinternalproperties.Instead, modelsarebuiltfrominputsandoutputs,bothofwhich canbemeasureddirectly.Thesemodelsmakeuseof linear-systemstheoryaspioneeredbyDreiss(1982,1989) withmorerecentapplicationsdescribedbyWicksand Hoke(1999).Theideaistousemeasuredinputand outputdatatoconstructakernelfunction(theblackbox) whichwillconnectallotherrelationsbetweeninputand output. C ONCLUSIONS Inthe40yearssincethe25 th anniversaryBulletin, knowledgeofkarsthydrologyhasmadegiantforward strides.Byborrowingconceptsfrombothgroundwater hydrologyandsurface-waterhydrology,anexcellent conceptualmodelforkarstaquifershasbeendeveloped. Thereisgoodunderstandingofthephysicalandchemical processesthattakeplaceinkarstaquifers.Thecurrent cuttingedgeisthedevelopmentofareasonableand accuratemodeltodescribetheflowbehaviorwithinthe aquifer.Althoughtherehasbeensomesuccess,acomplete modelhasyettobeobtained.However,theeventual constructionofsuchamodeldoesnotseemasremoteasit didonlyafewyearsago. A CKNOWLEDGEMENTS ReviewersWilliamK.JonesandStephenR.H. Worthingtonarethankedfortheirconstructivesuggestions. R EFERENCES Adams,F.D.,1954,TheBirthandDevelopmentoftheGeological Sciences:NewYork,DoverPublications,506p. 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GEOMICROBIOLOGYINCAVEENVIRONMENTS:PAST, CURRENTANDFUTUREPERSPECTIVES H AZEL A.B ARTON 1,* AND D IANA E.N ORTHUP 2 Abstract: TheKarstWatersInstitute BreakthroughsinKarstGeomicrobiologyand RedoxGeochemistry conferencein1994wasawatershedeventinthehistoryofcave geomicrobiologystudieswithintheUS.Sincethattime,studiesofcavege omicrobiology haveacceleratedinnumber,complexityoftechniquesused,anddepthofth eresults obtained.Thefieldhasmovedfrombeingsparseandlargelydescriptivein nature,torich inexperimentalstudiesyieldingfreshinsightsintothenatureofmicrob e-mineral interactionsincaves.Toprovideinsightintothechangingnatureofcave geomicrobiologywehavedividedourreviewintoresearchoccurringbefor eandafter theBreakthroughsconference,andconcentratedonsecondarycavedeposi ts:sulfur (sulfidicsystems),ironandmanganese(ferromanganese,a.k.a.corrosi onresidue deposits),nitrate(a.k.a.saltpeter),andcarbonatecompounds(speleo themsand moonmilkdeposits).Thedebateconcerningtheoriginofsaltpeterremain sunresolved; progresshasbeenmadeonidentifyingtherolesofbacteriainsulfurcavee cosystems, includingcavernenlargementthroughbiogenicsulfuricacid;neweviden ceprovides amodelfortheactionofbacteriainformingsomemoonmilkdeposits;combi ned geochemicalandmolecularphylogeneticstudiessuggestthatsomeferrom anganese depositsarebiogenic,theresultofredoxreactions;andevidenceisaccu mulatingthat pointstoanactiveroleformicroorganismsincarbonateprecipitationin speleothems. I NTRODUCTION LifeonEarthhasbeenmicroscopicformuchofits3.7 billionyearhistory(SchopfandWalter,1983).Nonetheless,themetabolicactivityoftheseorganismshasleftits markoneveryconceivableplanetarystructure,from isotopicfractionationoforedepositsinthedeepsubsurfacetotheoxygenationoftheatmosphere(Newman andBanfield,2002;SchopfandWalter,1983).Such metabolicactivitiescontinuetobecriticallyimportantin themaintenanceofthebiosphere,wheremicroorganisms sustainhigherformsoflifethroughprimaryproduction, nitrogenfixationandorganiccarbonmineralization.Despitetheplanetaryevolutionofourbio-andgeospheres, historicallyresearcherstendedtoignoremicrobialactivity ingeologicalenvironmentsduetoanabilitytoexplain manygeochemicalreactionsthroughpurelyinorganic chemistriesandtheinabilitytoculturemicroorganisms fromthesesites(Amannetal.,1995).Eventuallythese limitationswereremovedwiththedevelopmentofmolecular-scalegeochemistry,whilemolecularbiologyallowed investigatorstoexaminesuchenvironmentswithoutthe needforcultivation(BanfieldandNealson,1997;Hugenholtzetal.,1998;NewmanandBanfield,2002;Pace,1997). Suchtechniques,andtheirresultantfindings,also facilitatedtheinteractionsofmicrobiologistsandgeologiststounderstandthenaturalhistoryoflifeprocessesand biogenicchangesidentifiedundergeologicconditions (BanfieldandNealson,1997).Thisscientificrevolutionat theboundaryofgeologyandbiology,whichbecame knownasgeomicrobiology,extendedintoallarenasof geologyandrevealedprocessesoccurringunderpreviously unrecognizedphysicalandchemicalconditions(Newman andBanfield,2002).Historically,asinvestigatorsbeganto examinecaveenvironmentsincloserdetail,theyidentified unusualstructuresthathintedattheimportantrolethat microbialspeciesmightplayinthesesystems(Cunningham etal.,1995;Hess,1900;Heg,1946). Increatingacomprehensivereviewoftheadvancesin cavegeomicrobiology,wehavebuiltupontheearlier reviews(NorthupandLavoie,2001;Northupetal.,1997) andhavechosentousetheKarstWatersInstitute BreakthroughsinKarstGeomicrobiologyandRedoxGeochemistry conferencein1994(hereafterreferredtoasthe Breakthroughsconference;SasowskyandPalmer,1994)as awatershedeventinthehistoryofsuchstudieswithinthe US.Thisconferencebroughttogetheraninternational groupofscientiststopresenttheirmicrobiologicalresearch,allowingideastobediscussedanddebatedbetween karstandnon-karstresearchers.Thesecross-disciplinary interactionssparkedagreaterrecognitionandquickening ofcavegeomicrobiologywithintheUS.Indeed,asearchof theliteratureindexedin Scisearch (1977–present), BIOSIS (1969–present),and ZoologicalRecord (1978–present), usingsearchkeywordsrepresentativeofthesecondary *CorrespondingAuthorAddress:DepartmentofBiologicalSciences,Nort hern KentuckyUniversity,SC204DNunnDrive,HighlandHeights,KY41099; bartonh@nku.edu;Ph:859-572-5303;Fax:859-572-5639;www.cavescienc e.com 2 DepartmentofBiology,UniversityofNewMexico,Albuquerque,NM87131 1 DepartmentofBiologicalSciences,NorthernKentuckyUniversity,Highl and Heights,KY41099 HazelA.BartonandDianaE.Northup–Geomicrobiologyincaveenvironment s:past,currentandfutureperspectives. JournalofCave andKarstStudies, v.69,no.1,p.163–178. JournalofCaveandKarstStudies, April2007 N 163

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minerals,microorganisms,andcaves,returned165articles ofwhich134werepublishedafter1994.Tohighlightthe rapidevolutionofcaveandkarstgeomicrobiology,wewill reviewstudiesonthesecondarydepositsidentifiedincaves carriedoutintheyearsprecedingtheBreakthroughs conferenceandthenexaminetherepresentativestudiesthat followed.Thelatterclearlydemonstratestheimpactthat mainstreamgeomicrobiologicaltechniqueshavehadon cavegeomicrobiologyandhowsubterraneanprocessesin caveshavelednewinvestigatorstoenterthefield. C AVE G EOMICROBIOLOGY B EFORE 1994 Initialworkoncavemicrobiologypriortothe1990s tendedtoconcentrateondescriptivestudies,withmany investigatorsnotingthepresenceofmicroorganismsincave secondarymineralenvironments.Generally,suchobservationsweredismissedastheresultoftransportintothe systemthroughairmovementorvectors(animalor human)(Cunninghametal.,1995;Northupetal.,1994; Palmer,1991).Researcherssuggestedthatduetogeologic isolationfromallochthonoussurfaceenergyinput,microbialspecieswouldbelimitedtotherelativelyfewableto eekoutanexistenceinthisextremelystarvedenvironment (Palmer,1991).Nonetheless,certaingeochemicalprocesses weredifficulttoexplainbypurelyinorganicprocesses. Cavenitrate(a.k.a.nitrocalciteorcalciumnitrate)isthe saltpetercommonlyfoundindrycavesedimentsand historicallywasanimportantcomponentofgunpowder manufacture(Faust,1949).Asearlyas1900,Hess questionedtheoriginofsuchdepositsandproposed aseepingground-waterhypothesisinwhichbacterial decompositionoforganicmatterabovethecavereleased nitrateionsthatweretransportedviagroundwater. Subsequently,evaporationofwaterindrypassageswould resultinabuildupofnitrateinthesaltpeterearth(Hess, 1900).Hill(1981),Hilletal.(1983),andPace(1971) proposedmodificationsonthisseepingground-water mechanism,suggestingthatorganic-richammoniaor ammoniumionswerecarriedinfromsurfacesoils.Other suggestedsourcesofnitratesincavesincludedbatguano (Hill,1987);ammonium–ureafromamberat(caveratfeces andurine)(MooreandSullivan,1978);bacterialnitrogen fixation(Faust,1949,1968;Lewis,1992);fertilizersand sewage;volcanicrocks;andforestlitter(Hess,1900;Hill, 1981;Moore,1994).StudiesinMammothCavedemonstratedthepresenceofnitrifyingbacteria,specifically Nitrobacter spp.,indensities100timeshigherthansurface soils,althoughnoconsensuswasreachedonabiogenic sourceforthesenitrates(FliermansandSchmidt,1977). Earlystudiesofsulfurincavesconcentratedon descriptivestudiesofmicroorganismsincaveswithsulfide inputs.Principi(1931)firstproposedsulfuricacid-driven speleogenesis,andsuggestedthatasmallItaliancavewas createdbytheinteractionofsulfidicwaterswithlimestone (notedinVlasceanuetal.,2000,whoalsoreviewsearly non-caveandkarstsulfuricacidcorrosion).Morehouse (1968)firstdescribedcavedissolutionbysulfuricacidin theEnglish-languageliteraturebasedonhisstudiesin LevelCreviceCave,Iowa.Ofparticularinterestin establishingamicrobialroleinsulfuricacid-driven speleogenesiswasthefirstdocumentationofisotopically lightsulfurandgypsumdeposits.Theselighterisotopesare preferentiallyusedbycellularenzymes;andthus,such fractionationusuallyindicatesbiologicalactivity.Hill (1987)providedthefirst d 34 Svaluesforarangeof geologicalenvironments,includingsulfurisotopeanalyses onsulfurandgypsumdepositsfromseveralGuadalupe caves.Thecomparisonofobserveddatawiththeoretical valuesledhertoconcludethatbiologicalfractionationhad occurredinthepathwaysleadinguptothecavedeposits. InalaterpublicationHill(1994)concludesthatbiogenic fractionationcomesfromtheinitialreductionofsulfateto hydrogensulfide;thatthecaveelementalsulfurdeposits arenotbiogenic,whilethegypsumdepositsare.Sincethese earlypapers,otherstudieshaveimplicatedsulfuricacidin theformationofnumerouscaves(Davis,1980;Egemeier, 1981;Galdenzi,1990;Hill1987,1990;Jagnow,1979; KorshunovandSemikolennyh,1994);however,inthese inactivecavesystems,thecauseandeffectofmicrobial metabolismsonspeleogenesisremainedelusive. Anearlymorphologicalstudyoflimestonetypesby ShojiandFolk(1964)firstindicatedthepossiblerolethat microorganismsmightplayincarbonatedeposition,revealinginclusionswithinrockthatwerelatershowntobe microbialinorigin(FolkandChafetz,1980).Atthesame time,geologistswererecognizingamicrobialcomponentto carbonateprecipitationinstromatolitesfromthefossil record(Loganetal.,1964),whichprovideevidenceofsome oftheearliestlifeonEarth(SchopfandWalter,1983). Whilestudiesonstromatolitessuggestedthatmicrobial activitywaslimitedtothetrappingofcalcitecrystalswithin analgalfilm,subsequentworkdemonstratedthatchanges inthemicroenvironmentthroughphotosyntheticactivity inducedthisprecipitationofcalcite(Walter,1976).While muchearlyworkconcentratedonsaltwaterenvironments withphotosynthetically-drivencalciteprecipitation,ChafetzandFolk(1984)begantoexaminecalciteprecipitation infreshwater,travertinedeposits.Theseinvestigatorswere amongthefirsttorecognizethatthehightemperaturesand sulfidechemistryoftheseenvironmentslimitedalgal growthandphotosynthesis.Asaresult,theywereableto demonstratethatasmuchas90%ofthedeposited travertineinthesespringswasbacteriallyprecipitated (ChafetzandFolk,1984).Theseinvestigatorswentonto demonstratethatlocalchangesingeochemistryalteredthe G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 164 N JournalofCaveandKarstStudies, April2007

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crystalstructureofsuchdeposits,allowingthenatureof suchbiogenicdepositstobeidentifiedwithinthegeologic record(Chafetz,1986;ChafetzandFolk,1984;Loveand Chafetz,1988). AtthetimeofthediscoveriesbyChafetzandFolk (1984),thepossibilitythatmicroorganismswereinvolved incalciumcarbonate(CaCO 3 )precipitationwasnotnew. Indeed,theearliestindicationofsuchdepositionwasmade byWollnyin1897(asreferencedinHallandMiller,1905). Laterinvestigatorswentontoconcludethatsuchprecipitationwascausedbybiologicalsurfacesthatcould coordinateionsandfacilitatebiologicallycontrolled mineralization(ChafetzandBuczynski,1992).Nonetheless,itwasnotuntiltheexperimentsofBoquetetal.(1973) whogrewsoilbacteriaonagarplatesthatcontained calcium,butlackedanysourceofcarbonate,thatthe importanceofbacteriallycontrolledmineralization(BCM) wasrealized(Fig.1).Interestingly,theworkofBoquetet al.suggestedthattheabilitytoprecipitatecalcitewas acommonoccurrenceamongsoilbacteriaandisconserved acrossmultipleevolutionarydomains.Buczynskiand Chafetz(1991)wereabletoconfirmtheimportanceof BCMbyshowingthatonlymetabolicallyactivebacteria couldprecipitateCaCO 3 ,andthatthesubsequentmineral structures(calciteversusaragonite)weredependentonthe viscosityofthemediumonwhichtheyweregrown.Such resultsemphasizedtheimportanceoftheterrestrial environmentoncalciteprecipitation(Buczynskiand Chafetz,1991;ChafetzandBuczynski,1992). Withthestimulusofsuchworkbeingcarriedoutin carbonateprecipitation,itisnotsurprisingthatthemyriad ofspeleothemsfoundincavespromptedearlystudiesto examinethepotentialroleofmicroorganismsinthe formationofthesedeposits.Inthe1960s,Thrailkill (1964)wasthefirsttosuggestalinkbetweentheorigin ofcavepopcornandmicroorganisms,whileWent(1969) suggestedthatfungiplayedanimportantroleinstalactite growth(Fig.2),althoughnobiogeniccomponentwas identifiedbyFolkandAssereto(1976).In1983,Danielli andEdingtondemonstratedthatbacterialspeciesisolated fromsecondarycavedepositsdisplayedagreatercapacity toprecipitateCaCO 3 thansurfacespecies(Danielliand Edington,1983).Suchactivityledtheauthorstosuggest ametaboliclinkbetweenusinganorganiccalciumsaltfor energyandexcretingcalciumionsasawasteproduct, whichwouldresultinprecipitationwhenthecalcium exceededthesolubilitythreshold(DanielliandEdington, 1983).Additionalsupportfortheroleofmicroorganisms inspeleothemformationwasprimarilycircumstantialand consistedofanumberofinvestigatorsfindingmicro-fossils withincarbonatespeleothems(e.g.,Coxetal.,1989;Jones andMotyka,1987;PolyakandCokendolpher,1992),until theidentificationofpoolfingersbyDavisetal.(1990). Thesesubaqueouspoolfingersdemonstratedatrulybiogenicstructure,withparabolicu-loopsconnectingpendant fingers,theformationofwhichwasdifficulttodescribe usingsolelyabioticprocesses(Fig.3).Theassociated webulitesseenwiththesepoolfingers(Davis,2000)also appearedbiogenicinorigin,morecloselyresembling microbialbiofilmstructuresthanmineralprecipitates. Anothercarbonatedepositthathaslongattracted microbiologistsismoonmilk,alsoknownasmondmilch andavarietyofothernames(Bernasconi,1981;Reinbacher,1994).Moonmilk,whichhasdifferingstructural Figure1.ScanningelectronmicrographsofcalcitecrystalsformedonBoq uetB-4media(Boquetetal.,1973)bybacteria isolatedfromacaveenvironment.A,Calcitecrystalsformingonabacteri alcolony;filamentsofindividualbacterialcellsare visible(scalebar5 m).B,Individualcalcitecrystalformedonabacterialcolony,confirmed byenergydispersivespectroscopy (EDX;scalebar10 m). H AZEL A.B ARTONAND D IANA E.N ORTHUP JournalofCaveandKarstStudies, April2007 N 165

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forms,fromasoft,granularpastetoalooselyaggregated powder,canbecomposedofcalcite,aragoniteorhydromagnesitecrystals,dependinguponthestructureofthe caveinwhichitisdeposited(HillandForti,1997).Heg (1946),inoneoftheearliestpapersonmicrobial-mineral interactions,suggestedthatthemetabolicactivityof microorganismswasthecauseofmoonmilkdeposition, anidealatersupportedbyDaviesandMoore(1957).In supportofthishypothesiswastheworkofWent(1969), whodemonstratedtheabilityoffungalhyphaetoactas attachmentandnucleationsitesforCaCO 3 precipitation. Nonetheless,withtheformationofsoftdepositedformsof moonmilkonmuchharderbedrock,otherinvestigators suggestedthatcorrosionratherthandepositionmechanismswereresponsible.EarlystudiesbyCaumartinand Renault(1958)andCaumartin(1963)suggestedthat Figure2.Circumstantialevidence,suchasthisfungalmyceliumemerging fromtheendofacalcitesodastrawandits associatedcalcitecrystals,promptedearlyinvestigatorstopostulate onaroleformicrobialspeciesinthedeposition ofspeleothems. G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 166 N JournalofCaveandKarstStudies, April2007

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moonmilkcouldbetheresultofmicrobialmetabolic productsthatcorrodedunderlyingbedrock.Despite numeroushypotheses,atthetimeoftheBreakthroughs conference,noclearpictureemergedofwhetherthese intriguingdepositsarebiogenicorabioticinorigin. Oftheothersecondarymineralspeciesobservedin caves,anabundanceofcircumstantialevidenceforiron biomineralizationexists:CaldwellandCaldwell(1980), Caumartin(1963),Crabtree(1962),DysonandJames (1981),Jones(1991),JonesandMotyka(1987),Klimchouk (1994),Luiszer(1992),Maltsev(1997).Oneoftheonly experimentalstudieswasthatofPeck(1986),whorecoveredtheiron-oxidizingspecies Gallionellaferruginea and Leptothrix sp.fromcavepools,sumpsandmoistFe/ MnstructuresinLevelCreviceCavenearDubuque,Iowa. Thisstudyestablishedthatsterilecontrolsshowednoiron precipitation,whileliveinoculationsofsubterranean bacterialspeciesprecipitatedironhydroxides( Gallionella ferruginea cultures)andiron-impregnatedsheaths( Leptothrix sp).Suchiron-encrustedfilamentswerealsoidentified intherusticlesofLechuguillaCave,whereinDavisetal. (1990)usedscanningelectronmicroscopy(SEM)toshow thefilamentousbacterialshapesassociatedwiththese interestingformations. Severalearlystudiesalsoproposedmicrobialparticipationintheformationofcavemanganesedeposits: Broughton(1971),C lekandFa bry(1989),Crabtree (1962),Hill(1982),Jones(1992),LavertyandCrabtree (1978),MooreandSullivan(1978),Peck(1986)andWhite (1976).Arangeofmanganeseformsarefound,suchas coatingsonwallsorspeleothems(Gascoine1982;Hill, 1982;Kashima,1983;MooreandSullivan1978;Rogers andWilliams,1982),softdepositsinclasticdeposits(C lek andFa bry,1989),andconsolidatedcrusts(Hill,1982;Jones, 1992;Moore,1981;Peck,1986).Moore(1981)found manganese-oxidizingbacteriasuchas Leptothrix inastream inMattsBlackCave,WestVirginia,andattributedthe formationofbirnessiteinthiscavetotheprecipitationof manganesearoundsheathsofbacteria.Thepresenceof rods,sheets,strands,andsmoothspheroidmorphologiesin thefossilremainsofmanganeseprecipitatesinstalactites, karstbrecciaandrootcalcretecrustsinGrandCayman cavesledJones(1992)toconcludethatsomeofthese manganeseprecipitateswerebiogenic;however,aswith muchofthepre-1994cavegeomicrobiologyliterature,many ofthesestudiesprovideonlydescriptive,circumstantial evidence.Thedegreetowhichthephylogeneticallydiverse groupofmicroorganismsknowntooxidizereduced manganesecanpromotesuchoxidation,passivelyor enzymatically,isdebated.Microorganismscanincreasethe rateofmanganeseoxidationbyuptofiveordersof magnitude(Teboetal.,1997)andthelargeaccumulations ofmanganeseoxidesthatoccasionallyoccurincaves representpotentiallymicrobialmediatedproduction. Literatureonotherbiogenicallymediatedmineral structuresfromcavesislimited;studiesofsilicate speleothemsandclaymineralformshavebeenconducted mainlyinJapanandVenezuela.Earlystudiesofmicroorganismsassociatedwithopalspeleothemsdemonstrated thepresenceofmicrobialmorphologiesinthespeleothems (Kunicka-Goldfinger,1982;Urbani,1976,1977). Meolosira ,asilicaceousalgaldiatom,werefoundintwilightzone coralloidsinTogawaSakaidanipdoCave,Japan(Kashima,1986;Kashima,etal.,1989).Littleearlyworkexists onclay-containingspeleothemssuchasvermiculations, althoughAnelliandGraniti(1967)hypothesizedthatthe halosurroundingvermiculationsiscausedbyacidsand otherorganicsubstancessecretedbyfungi. C AVE G EOMICROBIOLOGY A FTER 1994 Atthebeginningofthe1990s,newmoleculartechniquesincreasedthenumberofenvironmentsthatcouldbe successfullystudiedbymicrobiologists(Pace,1997).Such techniquesallowedresearcherstoexaminethecomplex chemicalinteractionsofmicrobialphysiologywithredox activeminerals,inwhathadpreviouslybeenconsidered abiotic,geologicalenvironments(BanfieldandNealson, 1997;NewmanandBanfield,2002).Thebringingtogether ofcavegeologistsandbiologistsattheBreakthroughs conferencemirroredtheevolutionofthescienceof geomicrobiology;biologistsbroughtalternativeprinciples (respirationacrossredoxgradients)anduniquetechniques (DNApurificationandmolecularphylogenetics)totheir geologicpeers(NewmanandBanfield,2002).Geologists likewiseexposedbiologiststotheprinciplesofmineralogy andnoveltechniques(x-raypowderdiffractrometryand energydispersivespectroscopy)(BanfieldandNealson, 1997).Theintroductionofnewtoolsandtechniques Figure3.Small,doubleu-loopsconnectingthependant-like pool-fingersinHiddenCave,NewMexico.Thesesmall structuresweredifficulttoexplainusingabioticprocesses.It isnowknownthatsuchstructuresarebiogenicinorigin. H AZEL A.B ARTONAND D IANA E.N ORTHUP JournalofCaveandKarstStudies, April2007 N 167

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providedopportunitiestoposenovelquestionsincave environments.Whilethisinitialeuphoriawasnotwithout itsdrawbacks[the defacto hypothesisformanybiologists isthateverythingisbiogenic,withtheconversebeingtrue forgeologists(Bartonetal.,2001)],theinitialdiscoveries broughtcavegeomicrobiologytoanewfoundaudience. Thisworkalsoshowcasedthesignificanceofcave microbiologytospeleologistsandallowedthemtorecognizepotentiallyimportantgeomicrobialstructuresduring exploration(Davis,2000;Davisetal.,1990).Themelding ofsuchactivitieshastakenthevalueofsuchresearch beyondtheinterestofspeleologistsandintothebroader scientificrealm(NewmanandBanfield,2002). GeorgeMoore’s1994title,‘‘Whenwillwehavean acceptedexplanationforcavenitratedeposits?’’captures theessenceofadebatethathasspannedmorethan acentury.Despitethesignificanceofcavenitratesinthe earlyhistoryofcavemicrobiology,therehasbeenlittle workthathasadvancedourunderstandingbeyondthe hypothesesreviewedintheearliersectionofthispaper.The stableisotopeworkofJamesonetal.(1994)did demonstratethatsaltpeterisenrichedinthelighterisotope ofnitrogen,supportingthehypothesisthatmicrobial activityisinvolvedintheformationofcavenitrates. Microbiologistshavecontinuedtodebatethedegreeto whichbacteria,suchas Nitrosomonas and Nitrobacter facilitatethecreationofthecavesaltpeterdepositsandthe originofthenitrogen.Nonetheless,todate,noconsensus existstoexplaintheformationofthesemineralsincaves, likelyareflectionofthelossofanycommercialvaluefor suchdepositswiththeadventofindustrialchemistry.Even so,nitrogenisalimitingnutrientformicrobialgrowthin allenvironmentsandaclearunderstandingofhowsuch depositsformwouldleadtoagreaterunderstandingof howmicrobialgrowthcanbesupportedinsubterranean environments(NewmanandBanfield,2002). TheintenseexplorationofLechuguillaCaveandthe discoveriesofmassivesulfurrelateddepositsprovided substantialsupportforthetheoryofsulfuricaciddriven speleogenesis(SpirakisandCunningham,1992;Cunninghametal.,1993,1994)[anexpandedhistoryofthisideain theGuadalupeMountainsistracedinJagnowetal.,2000]. Nonetheless,themetabolicroleofmicroorganismsin producingsuchsulfuricacidwasbasedalmostentirelyon thestudyofinactivecavesystemsinwhichcavern enlargementthroughactivemicrobialprocesseswasno longeroccurring.Therareexceptionwereinitialstudiesin ParkerCave(Kentucky),whichsuggestedthatsulfurand gypsumdepositedonartificialsubstratesinSulphurRiver resultedfromextensivebacterialsulfide-oxidizingactivity (Angertetal.,1998;OlsonandThompson,1988;ThompsonandOlson,1988).Otherinvestigatorsalsobegan examiningmicrobialsulfurcyclinginactivecavesystems, leadingtoagreaterunderstandingoftheroleofbacteriain cavedissolution.Ourdiscussionofthisworkwillbebrief asreadersarereferredtothecurrentreviewofsulfuricacid speleogenesisbyEngel(thisissue). IntheundergroundaquiferoftheBahamasand YucatanPeninsula,thehydrologyresultsintheformation ofanchialinecaves.Thesecavescontainanupper freshwaterlens,abrackishmixingzone(halocline),and underlyingseawaterthatintrudesfromthecoast(Bottrell etal.,1991;Mooreetal.,1992)andcreatesastratified watercolumnwithinthecavesystem,basedonchemical, temperatureanddensitygradients(Mooreetal.,1992; Pohlmanetal.,1997;Stoesselletal.,1993).Withinthe haloclineitself,stratifiedzonesofSO 4 2 ,NO 3 ,NO 2 andpHhavebeenobserved,suggestingthepresenceofan activemicrobialecosystem(Pohlmanetal.,1997;Socki etal.,2001;Stoesselletal.,1993).WorkbySockietal. (2001)hasshownthat d 34 Svaluesforthesulfideinthese systemsareisotopicallylight,asmuchas 63.2 o / oo suggestingthattheH 2 Scomesfrombacterialcycling,and notfromdegradationofplantmaterialenteringthrough thecenote,supportingmicrobiallydrivensulfuric-acid production(Marcellaetal.,1994;MartinandBrigmon, 1994).Theimportanceofsuchsubterraneansulfur-cycling isemphasizedbythediscoverybySarbuetal.(1994)of asulfur-basedcaveecosysteminMovileCave,Romania, whereamacroscopic-ecosystemissupportedbychemoautotrophicbacterialcommunities(Sarbuetal.,1996).The basisofthisecosystemwasastaggeringlevelofdissolved H 2 Sinthewater,approaching1300 M,althoughthe majorityofmicrobialmatsinthissystemdevelopedonthe surfaceofpoolsinisolatedairpockets,ratherthanin astratifiedwatercolumn(Sarbuetal.,1994,1996).The discoveryofsuchadiversesubterraneanecosystemdriven bychemoautotrophicmicroorganismswasasignificant advanceinourunderstandingofbiologicaldiversity.Other cavesystemshavesimilarlycontributedtoourunderstandingofbiologicallymediatedsulfuricacidspeleogenesis, includingCuevadeVillaLuz,Mexico(Hoseetal.,2000), FrasassiCave,Italy(GaldenziandMenichetti1995; Vlasceanuetal.,2000),CuppCoutunnCaveSystem, Turkmenia(Maltsev1997),LowerKaneCave,Wyoming (Engeletal.,2004),andCesspoolCave,Virginia(Engelet al.,2001).Thesesystemsdemonstratemanyofthe subaerialmicrobialactivitiesthoughttohaveoccurred withinLechuguillaCave,confirmingabroaderbiogenic componentinthespeleogenesisofsulfuricacidcaves (Davis,2000). Inordertobetterunderstandthemicrobialmetabolic processesthatleadtocavernenlargement,Engeletal. (2004)demonstratedlocalizeddissolutionofcarbonatesby Epsilonproteobacteria inLowerKaneCave,Wyoming.The bacterialocallyproducedsulfuricacidthatdissolvedthe hostrock,leavingbehindobvioussolutionpocketswhere themicroorganismsattachedtothesurfaceofthemineral G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 168 N JournalofCaveandKarstStudies, April2007

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(Fig.4).Surprisingly,theseinvestigatorsdemonstrated thatdissolvedH 2 Sinthecavespringwasquickly consumedbysulfide-oxidizingbacteriabeforeitcould generateinorganicsulfuricacid,indirectcontradictionto theclassicsulfuricacidspeleogenesismodelofPalmer (1991;Engeletal.,2004).Incontrast,othercavessuchas CuevadeVillaLuzhaveaggressivesubaerialmicrobial activityresultinginthepresenceofmicrobialbiofilm communities(snottites;Fig.5)withobservablesulfuric acidproduction(Hoseetal.,2000).Suchcommunitiesare activelyproducinggypsumprecipitatesthatsloughoffthe wallstoenlargethecaveandrillenkarrenthatweretaken asevidenceofpastmicrobialactivitywithinLechuguilla Cave(Davis,2000).Inordertoidentifythemicrobial activityresponsiblefortheformationofcavesonthescale ofCarlsbadCavernsandLechuguillaCave,Bartonand Luiszer(2005)recentlyproposedametabolicmodel whereinsulfiteandsulfuricacidcouldbeproducedin suchsystemsintheabsenceofsignificantoxygenatedwater input.Thistheoryalsosuggestedthatsubaerialdissolution inthepresenceofoxygenwouldresultinlocalizedpockets ofaggressivedissolution,ashasbeenseeninboth LechuguillaandVillaLuzcavesystems(Hoseetal., 2000;Davis,2000).Whateverthemicrobialmechanismsin place,thereremainimportantquestionsregardingobservabledifferencesinspeleogenesisandcavernenlargementon themolecularandgeologicalscales(Engeletal.,2004; Klimchouketal.,2000)thatpromisetobeanexcitingand innovativeareaincavegeomicrobiologyaswework towardacomprehensivemodelofsulfuricacidspeleogenesis. Inthepastdecade,therehasbeenarapidexpansionin ourunderstandingofcarbonatebiogeochemistryandthe depositionofCaCO 3 inreactionsthatrangefromthe moleculartoenvironmentalscale(BanfieldandNealson, 1997;Banfieldetal.,2005;MozelyandDavis,2005; Neuweileretal.,2000;Newman,2001;Woodsetal.,1999). Together,theseinvestigationsarepiecingtogetheramore completeunderstandingoftherolethatbiologicalprocesses,whetherdirectorindirect,playintheformationof CaCO 3 depositswithinthegeologicrecord(Banfieldand Nealson,1997;BosakandNewman,2003;Neuweileretal., 2000;Woodsetal.,1999).Likewise,theimportanceof speleothemsasterrestrialtravertinedepositshasledto greaterresearchintheseenvironments,increasingour understandingofthepotentialrolethatmicroorganisms playinthestructureandformationofsuchcavedeposits (Cacchioetal.,2004;Frisiaetal.,2002;Galyetal.,2002; Melimetal.,2001;Saiz-Jimenez,1999;Sanchez-Moralet al.,2003;ToothandFairchild,2003).Togetherthiswork indicatesthat,ashasbeenobservedinhotspring travertines,thelocalgeochemistry,temperature,rateof CO 2 off-gassingandprecipitation,andmicrobialactivity allplaycriticalrolesincarbonatedepositionandstructure (Fouke,etal.,2000;Frisiaetal.,2002;Sanchez-Moralet al.,2003). Therehasbeenagreaterrecognitionofthedifferent rolesthatbiologicallyinducedandbiologicallycontrolled precipitationplayinCaCO 3 biomineralization(Bosakand Newman,2005;Braissantetal.,2005);biologicallyinduced precipitation(BIM)referstotheeffectthatorganismal Figure4.Unpreservedcalcitechipandfilamentousmicrobialcells(somewithintracellularsulfurglobules)examined withenvironmentalscanningelectronmicroscopy;calcite chipwasexposedtothemicrobialmatforthreemonths, resultinginanetchingofthesurfacebythemicrobial activity.Scalebar10 m. Figure5.Microbialbiofilms,suchasthesesnottitesfrom CuevadeVillaLuz,producewaterdropletswithapHof0to 2.Suchbiofilmsplayimportantrolesinsecondarydissolutionprocesseswithinsulfidiccavesystems. H AZEL A.B ARTONAND D IANA E.N ORTHUP JournalofCaveandKarstStudies, April2007 N 169

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metabolicactivitiesandby-productshaveonthelocal physiochemicalenvironment,favoringconditionsthat promoteprecipitation(FrankelandBazylinski,2003). Biologicallycontrolledprecipitation(BCM),alsocalled organicmatrix-mediatedmineralizationorboundary-organizedmineralization,referstotherolethatcellular substratesplayinpromotingcoordinationandgrowthof biominerals(BazylinskiandFrankel,2003;Simkissand Wilbur,1989). MicroorganismscanpromoteCaCO 3 precipitation throughprocessesofBCMbyalteringthesaturationindex (SI)ofthesolution,orbyremovingkineticinhibitorsof crystallization,suchasmagnesium,sulfateorphosphate ions(BosakandNewman,2005,andreferencestherein). WhilesuchBCMactivitieshavebeenshowntoplayan importantroleincalcitecrystalmorphology(Bosakand Newman,2005;Braissantetal.,2005;DÂ’Souzaetal.,1999; Ormeetal.,2001;Schultze-Lametal.,1992),ithasbeen moredifficulttoassessaroleforBIMinCaCO 3 deposition andtheroleofmicroorganismsinspeleothemdevelopment.Castanieretal.(1999)havesuggestedthatbacterial autotrophicprocessescauseCO 2 depletionsurroundingthe cell,favoringtheprecipitationofcalciumionsasCaCO 3 Otherinvestigatorshaveproposedthatheterotrophic processesofnitrogenfixationandreleaseplayacritical roleinraisingthepHofthelocalenvironment,again favoringtheprecipitationofcarbonates(Cacchioetal., 2004;HammesandVerstraete,2002).Incyanobacterial species,fixationofCO 2 increasestheconcentrationof bicarbonateions,whichmaybeexcretedintothe extracellularmedium,causingCaCO 3 precipitationif calciumionsarepresent(BadgerandPrice2003;Hammes andVerstraete2002).Whilesuchphotosyntheticreactions arenotpossibleincaveenvironments,thecarbonic anhydrasesresponsibleforCO 2 uptakearecommon amongbacterialspecies(Merlinetal.,2003).McConnaugheyandWelan(1997)alsosuggestedthatbacterial calcificationmaygenerateenergyfornutrientuptakein starvedenvironmentsandmayexplaintheubiquitous natureofcalciteprecipitationoriginallyobservedby Boquetetal.(1973). Intellectuallyaproblemarisesinthatasmicroorganismscarryoutcalciteprecipitation,suchactivityinvariably leadstoentombmentwithinthegrowingcrystalanddeath (Bartonetal.,2001)(Fig.6).Thismakesunderstandingan evolutionaryadvantageforsuchactivitydifficulttoassess. Itisknownthatbicarbonateionscanserveasabuffer, whichallowsmicroorganismstocarryoutcellularprocessesthatwouldotherwiseleadtoacidicconditions;if bicarbonateionswereservingthisfunctionundersuch conditions,Ca 2 wouldquicklyaccumulatetotoxiclevels. Nonetheless,evidenceisstartingtoemergethatbacteria, liketheireukaryoticcounterparts,haveCa 2 antiporter proteinpumpsthatselectivelydetoxifycalciumfromthe cellbypumpingitintotheextracellularmedium(Caiand Lytton,2004).Indeed,astudybyAndersonetal.(1992) demonstratedthatundertoxiccalciumconcentrations, Pseudomonasfluorescens activelyprecipitatedcalcite. ThisworkisfurthersupportedbyCacchioetal.(2004), whodemonstratedaselectiveenrichmentformicrobial speciescapableofcarryingoutCaCO 3 depositionfrom speleothemswithinCervoCave,Italy.Theseinvestigators Figure6.MicroorganismsgrowingonthewallofacaveinKentuckyhavebeco meencasedinacalcitematrix(A),as confirmedbyEDXanalysis(scalebar20 m).Viablebacterialcellswereisolatedfromthisareaandshowntoalsobe come encasedincalciteduringgrowthonB-4media,leavingbehindcell-shaped cavitieswhenwashedfromtheprecipitatedcalcite (B;scalebar5 m). G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 170 N JournalofCaveandKarstStudies, April2007

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demonstratedthatbacterialspeciesisolatedfromdifferent speleothemsdisplayedanunusuallyhighrateofcarbonate precipitation,whencomparedwithorganismsfromnonkarstenvironments;however,theseinvestigatorsreliedon cultivationtechniquesthatfavoredmicroorganismscapableofsurvivingthetransitionfromthestarved,oligotrophicconditionsofcaveenvironmentstotheeutrophic conditionsofanutrientplate.Suchcultivationstrategies selectivelyidentifymicrobialspeciesthatareknownto displaythemetabolicphenotypesconsistentwithcarbonate precipitation,including Pseudomonas and Bacillus species (Boquetetal.,1973;Cacchioetal.,2003,2004;Koch, 1997).Nonetheless,theseinvestigatorsdiddemonstrate usingoxygenandcarbonisotopicfractionationthatthree distinctprocessesappearedtobeinvolvedinbacterial calciteprecipitation(Cacchioetal.,2004).Whateverthe metabolicprocessresponsibleforcalcitedeposition(and theworkofCacchioetal.,(2004)suggeststheymaybe numerous)itisimportanttorememberthatabalancemust existbetweenbiologicalandinorganicprocessesinsuch precipitation(Foukeetal.,2000;Palmer,1996). Regardlessofthemetabolicactivitydirectlyresponsible forCaCO 3 depositionwithincaves,investigatorshave continuedtoexaminesuchdepositsforthepresenceof microfossils,petrographicfabricsthatareindicativeof microbiallymediatedprecipitationandisotopicfractionationofthecarbonate(Melimetal.,2001;Bostonetal., 2001).UsingSEM,Melimetal.(2001)examinedthe layeredcalcitepoolfingers,firstidentifiedbyDavis(2000) aspotentiallybiogenicinorigin.Theseinvestigatorsfound anabundanceoffossilfilamentswithinmicriticlayers,but notintheinter-layeredclearcalcitespar.Theyalsofound asmallshiftinthecarbonisotopecompositionofthe micriticversusclearcalcitelayers.Together,thisassociationsuggestedthatmicroorganismswereinvolvedinthe depositionofthisformation(Melimetal.,2001).Such workwasrecentlysupportedbyBaskaretal.(2006),who demonstratedmicrocrystallinedepositionofcalcitewithin stalactitesthatappearedtobemediatedbymicrobial processes.AstudybyContosetal.(2001)alsodemonstratedthepresenceofsubaqueouscalciteprecipitates associatedwithmicrobialbiofilmsinWeebubbieCave, Australia.Thesedepositsformedinwaterswellbelowthe saturationindexofcalciteanddemonstratedaunique structure,whichcouldonlybereplicated invitro withthe additionoforganicacids(Ormeetal.,2001).Suchresults ledtheinvestigatorstoconcludethatthesurfaceofthe Gammaproteobacteria speciesfoundwithinthebacterial filamentsofthecave(Holmes,etal.,2001)playedacrucial roleincalcitedeposition(Contosetal.,2001). Themostconvincingevidenceofmicrobialinvolvement inspeleothemformationcomesfromtheformationof moonmilk(Can averasetal.,2006).Whilemoonmilkwas oneoftheearliestcalcitecavedepositstobeassociated withmicrobialactivity(Heg,1946),itsneedle-fiber structureisdelicateandeasilyalteredbytheconstructive ordestructiveprocessesofdiagenesis(Jones,2001).Thusit hasremaineddifficulttodeterminetherolethatmicroorganismsplayinthestructuralformationofmoonmilk. Byusingacombinationofcultivation,molecularphylogeneticsandpetrographicanalyses,Can averasetal.(1999, 2006)demonstratedthatmoonmilkdoesnotcontain fungalfilaments,butrathernumerousfilamentous Proteobacteria speciesthatdemonstrateacalciteprecipitation phenotype.Morphologicalevidencesuggestedthatmoonmilkformsthroughthemicrobialcolonizationofrock surfaces,followedbycalcitedepositionalongbacterial surfaces,microstructuralbreakdown,andaccumulationof collapsedfibers(Can averasetal.,2006).Asthisprocess repeatsthroughseasonaloscillations,moonmilkdeposits becomethicker,formingthesignificantdepositsobserved innumerouscaves(Can averasetal.,2006).These investigatorsalsoidentifiedthepresenceof Crenarchaeota membersoftheArchaea,inthesemoonmilkdeposits;their roleinmoonmilkformationremainsunclear(Gonzalezet al.,2006).Together,suchworkrepresentsoneofthemost completepicturesofthephysiologicalandgeochemical relationshipsofbiogenicdepositformationwithincave environments. Whileasignificantamountofworkhasbeengeared towardunderstandingmicrobialinvolvementincarbonate constructiveprocesses,thereisanincreasinginterestinthe destructive,erosionalprocessesofmicrobialactivity (Jones,2001).Evenwhilemicrobialsurfacesmaybind Ca 2 ions,increasingthelikelihoodofcalcitecrystallization (BosakandNewman,2005),certainbiologicalmolecules haveasufficientlyhighaffinityfortheseionsthatthey actuallypromotedissolution(Perryetal.,2004;Friisetal., 2003).Suchstructuresincludeexopolysaccharide(amajor componentofbiofilms),siderophoresandothersecreted chelators,andeventhebacterialcellwall(Perryetal., 2004;Friisetal.,2003).Throughtheirmetabolicprocesses, bacteriaalsosecreteanumberoforganicacids,which activelydissolvecarbonates.Conversely,anumberof microbialstructures,includinglipidsandphospholipids, actuallyinhibitdissolution,whilesoilderivedhumicacids, whichformasignificantportionoftheorganiccarbon foundwithincavedripwaters(Saiz-JimenezandHermosin,1999),alsoinhibitcalcitedissolution.Itislikelythat thegoverningfactorscontrollingmicrobialinvolvementin calciteconstructiveordestructivedevelopmentwillinvolve abalancebetweenthelocalconditions,thegeochemistry andphysiochemistryofthelocalenvironment,andthe microbialmetabolicprocessesthatpredominateundersuch conditions(PohlandSchneider,2002;Vlasceanuetal., 2000). Twodecadesago,Peck(1986)describedthepresenceof microbialspeciesinmanganeseandironoxideswithin cavesandproposedthepossibilityofchemolithotrophic primaryproducersinthesesystems.Unfortunatelymost H AZEL A.B ARTONAND D IANA E.N ORTHUP JournalofCaveandKarstStudies, April2007 N 171

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biologistsdidnotrecognizethesignificanceofthis observation.Suchindifferencemirrorsthegenerallackof interestbymicrobiologists(primarilyduetothefunding climateatthetime),whotendedtoconcentrateon medicallyimportantpathogens.Eventsintheexploration ofLechuguillaCave,firstexploredinthesameyearas PeckÂ’sstudy,wouldprovidetheimpetustoexplore microbe-mineralinteractionsonmanganeseandiron environmentsincaves;oneofthedepositsthatgenerated thegreatestinterestwerethecolorfuldepositsonwallsand ceilings(Cunningham,1991).Theseironandmanganese oxide-richlayerswereinitiallybelievedtobetheinsoluble residuefromtheattackofcorrosiveaironthecarbonate bedrockandwerecalledcorrosionresidues(Queen,1994; Cunningham,1991).Thesecorrosionresidues,nowreferredtoasferromanganesedeposits,occurinarangeof colorsandarediverseincompositionwithvariable amountsofclayandAl-oxideminerals;allarerichin Mn-andFe-oxides(Spildeetal.,2005).Theworkof Cunninghamwasthefirsttorecognizeanassociation betweenmicrobialspeciesandferromanganesedeposits withinLechuguillaCave(Cunninghametal.,1995). InspiredbyCunningham,theteamofBoston,Northup, Spildeandothersestablishedthepresenceofadiverse communityofmicroorganisms,someofwhomwererelated toknownmanganese-andiron-oxidizingbacteriaand otherswhoappeartobepreviouslyunknown(Northupet al.,2003)(Fig.7),anddocumentedthepresenceof metabolicallyactivebacteriainthepunkrockunderlying theferromanganesedeposits(Spildeetal.,2005).Their geochemicalstudiesdocumentedafour-foldenrichmentof reducedmanganesebetweenthebedrockandferromanganesedeposits.Spildeetal.(2005)alsodemonstratedthat someofthemineralspeciesidentifiedinthesedepositscan bereproduced invitro bymicrobialspeciesinoculatedfrom theseenvironmentsandfedachemicaldietofthereduced Figure7.Unusualbeads-on-a-stringmorphologiesofmanganese-oxidizi ngbacterialspeciesareseenthroughoutseveralofthe ferromanganesedepositsfromSnowingPassageinLechuguillaCave.EDXan alysesshowthatthemineralmatrixis manganeseoxide.(Scalebar5 m). G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 172 N JournalofCaveandKarstStudies, April2007

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metalionspresentwithintherockofthecave,whilekilled controlsdidnotproducethecrystallineforms.Whilethis doesnotconclusivelydemonstrateacause-and-effect,it takesasignificantsteptowardunderstandingthemicrobial activitiesresponsiblefortheformationofsuchdeposits. Somewhatsimilardepositstotheferromanganese depositsofLechuguillaCavearethosefoundinOchtina AragoniteCaveinSlovakia.Thesedeposits,termedochres, containgoethite,birnessite,andasbolane(Bosa ketal., 2002).Besidestheco-occurrenceofgoethiteandbirnessite inthesedepositsandthoseinLechuguillaCave,Ochtina ochresalsocontainoccasionaloccurrencesofLa-Ndbearingphosphate.Lechuguillaferromanganesedeposits alsocontaininstancesofrareearthelementsassociated withphosphateminerals.Bosa ketal.(2002)suggestedthat themanganeseoxidesweretheresultofmicrobialprecipitationinpoolbottomsinamannersimilartothat describedbyAndrejchukandKlimchouk(2001).Chelius andMoore(2004)performedaphylogeneticanalysisofthe WindCave(SouthDakota)paleofillsamplesthatcontainedsomemanganeseandiron.Interestingsimilarities existbetweenthearchaealphylogenetictreesofthisstudy andthoseofNorthupetal.(2003).Closestrelativesfor bothincludedclonesequencesfromtheSouthAfricangold minestudy(Takaietal.,2001),whichwereobtainedfrom porewaterthatpassesoverwad(manganeseoxide)fill (T.C.Onstott, pers.comm. ).Whatrolearchaealspecies mayplay,ifany,inproductionofmanganeseoxidesis currentlyunknown. Additionalformsofpoorlycrystallinemanganese oxidesandhydroxides(pyrolusite,romanechite,todorokite,andrhodochrosite)havebeendescribedfromcaves (Onac,etal.,1997;Gradz nskietal.,1995;Northupetal., 2000).Irregularlyshapedcrustsofmanganeseflowstone (2–20mmthick)arefoundinJaskiniaCzarnaCave(Tatra Mountains,Poland).Filamentsandglobularbodiesare interpretedasbacterialorfungalcellsthatparticipatedin theformationoftheflowstones,asevidencedbytheir three-dimensionalmorphologyandtheamorphouscharacterthatismorecommoninbiogenicmanganeseoxides. ThehighMn/Feratioof72.1:1inthecrustswasattributed byGradz nskietal.(1995)tobiologicallymediated precipitation.Alittlestudiedtypeofferromanganeseoxide depositistheblackcoatingsoflittoralMediterranean submarinecaves.AlloucandHarmelin(2001)concluded thatblackcoatingsinthesecaveswerebiosedimentary depositsthatformfromtheinteractionofslime,associated withmicroorganisms,anddissolvedmanganesefromthe seawater.ThestudyincludessomefascinatingSEM micrographsofbiofilmandmicrobialstructuresandmakes theobservationthattheMn/Feratioisnegatively correlatedwithlevelofnutrients. KasamaandMurakami(2001)attemptedtoascertain themicrobialcontributiontoironprecipitationonstalactitescomposedofferrihydrite.Microscopystudiesshowed avarietyofmicrobialmorphologiesassociatedwiththe stalactites.Theirexperimentsdemonstratedthatincomparisontoinorganicprocesses,microorganismsenhanced precipitationratesbyuptofourordersofmagnitude.The authorsarguedthatexopolysaccharidesandmicrobial surfacecharacteristicsweremoreimportantthanmetabolic processesintheprecipitationofironinthiscave. F UTURE P ERSPECTIVESON G EOMICROBIAL A CTIVITIESIN C AVE S YSTEMS Sincetheemergenceofgeomicrobiologyasascience, ourunderstandingofmicrobialinteractionswithminerals hasevolvedbeyondapreliminaryappreciationoftheirrole incarbon,sulfurandnitrogencycling.Itisnowrecognized thatmanyimportantmineraltransformations,originally consideredtobeinorganicinnature,canbemediatedby microorganisms;fromthemicrobialprecipitationof dolomiteingroundwater(Robertsetal.,2004;Warthmann etal.,2000);transformationofsmectitetoilliteclay(Kim etal.,2004);totheproductionofiron,uraniumandeven golddeposits(NewmanandBanfield,2002).Likewise, throughamorethoroughunderstandingofgeochemistry, wehaveexpandedourknowledgeoftherangeofhabitable environmentsonEarth;fromendolithicenvironmentsof extremetemperatures(FriedmannandOcampo,1976;Bell, 1993)tothedeepsubsurface,wherehydrogenproduced fromvolcanism,serpentinizationandevenradiolysis providessufficientenergytosupportmicrobialgrowth (Chapelleetal.,2002;Coveneyetal.,1987;Linetal., 2005).Whilesuchworkallowsusamorecomprehensive understandingoflifeonEarth,italsoopensawindowinto thepossibilityoflifeunderothergeochemicalconditions, suchasonMarsorEuropa.Duetotheabsenceofliquid wateronthesurfaceoftheseplanetarybodies,extantlife willberestrictedtothesubsurface(Bostonetal.,1992), makingitcriticaltounderstandtheprocessesthatsupport microbiallifeinallsubsurfaceenvironments. While,asthetitlesuggests,thisreviewprimarily addressestheinteractionsbetweenmicrobesandminerals incaveenvironments,microbiologyincaveenvironments alsoprovidesinformationonsubterraneanchemolithotrophicecosystems(Bartonetal.,2004;Cheliusand Moore,2004;Grothetal.,1999,2001;Laizetal.,1999, 2003;Schabereiter-Gurtneretal.,2002).Togetherthese investigationssuggestthatwithoutsunlightenergyand throughgeologicisolation,cavesareextremelystarved environmentswherethelevelsofavailableorganiccarbon tosupportheterotrophicmicrobialgrowthareoften athousand-foldlowerthanstarvedterrestrialenvironments(Barton,unpublished,2006).Examiningmicrobial ecosystemssurvivingundersuchstarvedconditionssuggeststhattheyproduceamyriadofenergyconserving reactions;fromobtainingenergyfromtheminuscule organicmaterialpercolatingintothesystemandfixing availablenutrientsfromtheatmosphere,toreducingthe tracemineralswithintherockofthecaveitself(Bartonet H AZEL A.B ARTONAND D IANA E.N ORTHUP JournalofCaveandKarstStudies, April2007 N 173

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al.,2004;CheliusandMoore,2004;Northupetal.,2003; andSpildeetal.,2005).Recentstudieshavealsosuggested thattheArchaeamayplayimportantrolesincave microbialecosystems(CheliusandMoore,2004;Gonzalez etal.,2006;Northupetal.,2003),althoughanidentifiable metabolicroleforthesemicroorganismshasyettobe determined. Byunderstandinghowmicroorganismssurvivethe extremestarvationofcaves,wecanunderstandandlimit humanimpactsonsuchhypogeanenvironments(Cigna, 1993).Indoingso,suchworkcanpreservecultural treasures,suchasPaleolithicpaintingsinthecavesof northernSpain,wheretouristactivityalteredthecave environmentandbroughtinheterotrophicmicroorganisms thatthreatentodamagetheseimages(Can averasetal., 2001;Grothetal.,1999;Laizetal.,2003).Anunderstanding ofsuchprocessesalsofacilitatedthedevelopmentof microbiallyprecipitatedcalcitecoatings,whichcanhelpto preservehistoricalmonumentsandsculptures(Hoppertet al.,2004;Rodriguez-Navarroetal.,2003).Presentlyitis hardtopredictthesimilaroutcomesfromtheincreasing numberofmicroorganismsbeingculturedfromcave environments,althoughtheyrangefromsuchbeneficial activitiesasbioremediationtodrugdiscovery. Evenaswewritethisreview,newtechniquesarebeing developedinmaterialsscience,chemistry,physics,geology andbiologythatwillallowinvestigatorstoaskmore complexquestionsoftheinteractionsbetweenmicroorganismsandmineralsurfaces.Forexample,inmaterials science,attenuatedtotalreflectanceFouriertransformed infra-red(ATR-FTIR)spectroscopyallowsreal-timeanalysisofchemicalchangesonsurfacesthroughmicrobial activity(Omoikeetal.,2001),whileatomicforcemicroscopyallowsustoexaminetheintra-molecularforcesthat allowmicroorganismstoacquireenergyfrommineral surfaces(Loweretal.,2001).Withinmicrobiology,new techniquesthatallowustoprobeinter-speciesand ecosysteminteractions(Caldwelletal.,2000),andadvancesingenomics,metagenomicsandproteomics,will allowustoaskquestionsofcommunityinteractionswithin cavesthatcouldpreviouslyonlybeaddressedunder invitro conditions.Allthewhile,cavescontinuetobediscovered, presentingnewenvironmentstobeexamined.Asaresult, ourunderstandingofmicrobialactivityinsuchsubterraneansystemscanonlycontinuetogrow,aspresent questionsareaddressedandnewquestionsareposed.As welookbackovertheadvancesincavegeomicrobiology sincetheBreakthroughsconference,wecanpredictthatthe scienceofcavegeomicrobiologywillcontinuetogrowin bothprominenceandregardwithinthegreaterscientific community. 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Tebo,B.M.,Ghiorse,W.C.,vanWaasbergen,L.G.,Siering,P.L.,and Caspi,R.,1997,Bacteriallymediatedmineralformation:insightsinto manganese(II)oxidationfrommoleculargeneticandbiochemical studies:ReviewsinMineralogy,v.35,p.225–266. Thompson,D.B.,andOlson,R.,1988,Apreliminarysurveyofthe protozoaandbacteriafromSulphurRiverinParkersCave,Kentucky USA:BulletinoftheNationalSpeleologicalSociety,v.50,p.42–46. Thrailkill,J.V.,1964,Originofcavepopcorn[abs.]:Bulletinofthe NationalSpeleologicalSociety,v.27,p.59. Tooth,A.F.,andFairchild,I.J.,2003,Soilandkarstaquiferhydrologic al controlsonthegeochemicalevolutionofspeleothem-formingdrip waters,CragCave,southwestIreland:JournalofHydrology,v.273, p.51–68. Urbani,P.F.,1976,O palo,calcedoniaycalcitaenlacuevadelCerro Autana(Am.11),TerritorioFederalAmazonas,Venezuela.Bolet n delaSociedadVenezolanadeEspeleolog a,v.7,p.129–145. Urbani,F.,1977,Novedadessobreestudiosrealizadosenlasformas ca rsicasypseudoca rsicasdelEscudodeGuayana:Bolet ndela SociedadVenezolanadeEspeleolog a,v.8,p.175–197. Vlasceanu,L.,Sarbu,S.M.,Engel,A.S.,andKinkle,B.K.,2000,Acidic cave-wallbiofilmslocatedintheFrasassiGorge,Italy:GeomicrobiologyJournal,v.17,p.125–139. Walter,M.R.,1976,Introduction, in Walter,M.R.,ed.,Stromatolites: Developmentsinsedimentology,Elsevier,Amsterdam,v.20,p.1–7. Warthmann,R.,vanLith,Y.,Vasconcelos,C.,McKenzie,J.A.,and Marpoff,A.M.,2000,Bacteriallyinduceddolomiteprecipitationin anoxiccultureexperiments:Geology,v.32,p.277–280. Went,F.W.,1969,Fungiassociatedwithstalactitegrowth:Science,v.16 6, p.385–386. White,W.B.,1976,Cavemineralsandspeleothems, in Ford,T.D.,and Cullingford,C.H.,eds.,Thescienceofspeleology,London,Academic Press,p.267–327. Woods,A.D.,Bottjer,D.J.,Mutti,M.,andMorrison,J.,1999,Lower Triassiclargesea-floorcarbonatecements;theiroriginandamechanismfortheprolongedbioticrecoveryfromtheend-Permianmass extinction:Geology,v.27,p.645–648. G EOMICROBIOLOGYINCAVEENVIRONMENTS :P AST CURRENTANDFUTUREPERSPECTIVES 178 N JournalofCaveandKarstStudies, April2007



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SUBTERRANEANBIOGEOGRAPHY:WHATHAVEWE LEARNEDFROMMOLECULARTECHNIQUES? M EGAN L.P ORTER DepartmentofBiologicalSciences,UniversityofMarylandBaltimoreCou nty,Baltimore,MD21250USA Abstract: Subterraneanfaunashaveuniquedistributionalattributes,includingr elatively smallrangesandhighlevelsofendemism.Twogeneralmodelshavebeenprop osedto accountforthesedistributionalpatterns–vicariance,theisolationof populationsdueto geographicbarriers,anddispersal,anorganism’sabilitytomovetoandc olonizenew habitats.Thedebateovertherelativeimportanceofeachofthesemodelsi nsubterranean systemsisongoing.Morerecently,biogeographicalstudiesofsubterran eanfaunausing molecularmethodshaveprovidednewperspectivesintothedistributiona lpatternsof hypogeanfauna,reinvigoratingthevicarianceversusdispersaldebate. Thisreviewfocuses ontheapplicationofmoleculartechniquestothestudyofsubterraneanbi ogeography,and particularlythecontributionofmolecularmethodsinestimatingdisper salabilityand divergencetimes.Sofar,molecularstudiesofsubterraneanbiogeograph yhavefound evidenceforthecommonoccurrenceofmultipleindependentcolonization softhe subterraneanhabitatincave-adaptedspecies,haveemphasizedtheimpor tanceofthe geneticstructureoftheancestralsurfacepopulationsindeterminingth egeneticstructure ofsubsequenthypogeanforms,andhavestressedtheimportanceofvicaria nceoramixed modelincludingbothvicariantanddispersalevents. I NTRODUCTION Cave-adaptedfaunahaveintriguedscientistsforcenturies.Partofthisfascinationhasbeenfocusedonunderstandingtheuniquegeographicdistributionpatterns overspaceandtime(i.e.,biogeography)ofsubterranean organisms.However,theuniquesuiteofregressive(eye andpigmentloss)andprogressive(appendageelongation, enhancednon-visualsensorymodes)traitstermedtroglomorphy(Christiansen,1962)characterizingcavernicoles oftenhinderdistributionalstudiesbecausethehighly convergentformcanobscuretaxonomicrelationships amongcave-adaptedspeciesandamongcloselyrelated caveandsurfacespecies.Comparedtosurfacespecies, cave-adaptedfaunasgenerallyhavesmallgeographic rangesandhighlevelsofendemismatallscalesof measurement,makingtheirbiogeographydistinct(Culver andHolsinger,1992;GibertandDeharveng,2002;Christmanetal.,2005).Therearenumerousrecordsofsingle caveendemicsinbothterrestrial(troglobionts)andaquatic (stygobionts)cave-adaptedspecies(PaquinandHedin, 2004;Christmanetal.,2005).Thesedistinctivegeographic patternshaveleadtoinvestigationsofhow,why,andwhen speciescolonize,adapt,andpersistinsubterranean environments.Ingeneral,understandingthebiogeography ofcave-adaptedfaunaoffersinsightsnotonlyintothe evolutionofthetroglomorphicform,butalsointothe formationandpersistenceofsubterraneanfaunas,providingimportantinformationrelativetocaveconservation andmanagementissues. Therehasbeenalongrunningdebateregardingthe mechanismsresponsibleforthedistributionofcaveadaptedfauna,beginningasearlyasthelate1800s (Packard,1888).Thecruxofthedebatehasbeenover therelativerolesofdifferentbiogeographicmodels, particularlydispersal(anorganism’sabilitytomoveto andtocolonizenewhabitats)andvicariance(isolationof populationsduetogeographicbarriers).Overtheyears, variousstudieshavesupportedonemodelortheother(see Culveretal.,2007forabriefhistoricalreview).However,it hasrecentlybeenrecognizedthatsubterraneanfaunal distributionsaremoreclearlyexplainedbyacombination ofbothvicarianceanddispersalevents,withmany reflectingprocessesoccurringinancestralsurfacepopulationsbeforetheinvasionofthesubsurface(Christiansen andCulver,1987;Verovniketal.,2004;Buhayand Crandall,2005;Lefe bureetal.,2006).Withrespecttothe classicdebate,subterraneandistributionpatternsarelikely theresultofcomplexprocessesbothinternal(e.g.,dispersal capabilities)andexternal(e.g.,vicariantevents,habitat connectivity)tothespeciesofinterest.Therefore,rather thaninvestigatingbiogeographicalpatternsintermsofone mechanismversusanother,ithasbecomemoreimportant tounderstandthecombinationoffactorsinvolvedin creatingcurrentdistributionpatterns,includingdispersal ability,potentialvicariantevents,andratesofevolution andextinction(Holsinger,2005;Culveretal.,2007). Giventhatthereareecologicaldisparitiescontrolling thedistributionaldifferencesbetweentroglobioticand stygobioticspecies(e.g.,modesofcolonization,ratesof migrationandextinction,typesofgeographicbarriers), considerationsinsubterraneanbiogeographyfirstinclude understandingtheroleofhabitatonthesefactors(Holsinger,2005).Subterraneanaquaticenvironmentsare MeganL.Porter–Subterraneanbiogeography:whathavewelearnedfrommol eculartechniques? JournalofCaveandKarstStudies, v.69,no.1,p.179–186. JournalofCaveandKarstStudies, April2007 N 179

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generallyconnectedoverwiderareas(duetohydrology) comparedtotheconnectivityofkarsticterrestrialhabitats. Hydrologicconnectivityprovidesstygofaunagreaterdispersalpotentialand,therefore,generallylargerdistributionalranges(Culveretal.,2007).Furthermore,the relativecontributionofdispersalversusvicarianceis dependentonfactorssuchasthescaleofinvestigation, rangingfromfaunaldistributionsunderindividualrocks, withincavestreamriffles,incavestreamsegmentsfrom asinglesystem,withincaveandkarstbasinsofasingle riverdrainage,fromcavesystemsindifferentdrainages,to regionalandcontinentalpatterns(CulverandFong,1994). Investigatingthesediversegeographicalandgeological scalesproducesdistributionalpatternscorrespondingto differencesintimeanddominantprocesses,withlargescale patterns(cavesystems,regions,continents)occurringover geological/evolutionarytimescalesbeingstronglyaffected byvicariantanddispersalevents,anddistributionswithin cavesystemsoccurringinecologicaltimescaleswith influencesfromprocessessuchascompetition,predation, mutualism,andmigration. Assubterraneanbiogeographersbegintoassessthe relativerolesofdispersalandvicarianceinsubterranean faunaldistributions,moleculartechniques,involvingthe characterizationofgeneticmateriallikeDNA,RNA,and proteins,havebecomeanincreasinglypowerfultool, complementingthesignificantamountsoftaxonomicand biogeographicresearchdevotedtosearchingcaveandkarst systemsforanimals.Themaingoalofthisoverviewisto explorethecontributionsofmoleculardatatoour understandingofsubterraneanbiogeography.Iwilldiscuss howrecentmolecularmethodshaveprovidedtheanalytical toolstoestimatephylogeneticrelationships,population parameters(e.g.,migrationrates,populationstructure), anddivergencetimesessentialforgainingdeeperinsights intothecolonization,persistence,andadaptationoffauna insubterraneansettings.Molecularperspectivesarealso presentedonseveraldifferentscales,includingpopulations versusspeciesandkarstbasinsversuscontinentaldistributions. T HE M OLECULAR P ERSPECTIVE Althoughclassicalgenetics,whereindividualsfrom differentpopulationsarecrossedtoexaminetheheritabilityofparticulartraits,havealonghistoryinbiospeleology (Breder,1943;Sadoglu,1956),moleculartechniquesaimed atinvestigatingthegeneticvariabilityofcavepopulations onlybeganinthe1970swiththedevelopmentofthefirst majormolecularmarkers,allozymes(proteinvariants) (AviseandSelander,1972;Carmodyetal.,1972;Hetrick andGooch,1973;Laingetal.,1976;Cockleyetal.,1977; TuranchickandKane,1979;Sbordonietal.,1979).Asthe availablenumberofmolecularmarkersincreasedandthe associatedanalysesbecamemoresensitiveandrefined, investigationsofsubterraneanbiogeographyfromagenetic perspectivebecamefeasible(seeSbordonietal.,2000for review). Currently,molecularstudiesusingmitochondrialgene sequencestoinvestigatepopulationandspecieslevel questionsarecommon,includingthegenesfor12Sand 16SrRNA,cytochromeoxidaseI,cytochromeB,and NADHdehydrogenase.Nucleargenes(e.g.,28SrRNA) havebeenlesscommonlyused,andaregenerallymore suitableforhigher-level(amongspecies,genera,families) phylogeneticstudies.Atthelevelofpopulations,genetic analysesutilizingmoleculardata,suchasmicrosatellites(a sequenceofDNAcontainingtandemlyrepeatedunits, wherethenumberofrepeatsvarieswithinandamong populations)andDNAsequences,nowallowforavast rangeofparameterstobeestimatedandassessedfor aparticularspecies.Theseparametersincludeestimatesof thenumberofgeneticpopulations,migrationrates(i.e., levelsofgeneflow),andeffectivepopulationsizes( N e is ameasureofgeneticdiversity,calculatedasthesizeof ahypotheticalpopulationwherealloftheadultscontribute gametestothenextgeneration; N e isusuallysmallerthan theactualnumberofindividualsinapopulation)(see PearseandCrandall,2004forareviewofrecentadvances inpopulationgenetics).Athighertaxonomiclevels(species andgenera),molecularmarkersofferlargenumbersof characterstobeusedinphylogenetic(evolutionary) methods,increasingthesensitivityandresolutionofthe analyses.Thefollowingsectionsdescribespecificareasof investigationwhere,incoordinationwiththestrong foundationsoftraditionalbiogeographicstudies,moleculartechniqueshavethepotentialtosubstantiallyincrease ourunderstandingofsubterraneanbiogeography. D ISTRIBUTIONSOF C AVE A DAPTED S PECIES Oneofthefoundationsofbiogeographicstudiesis asolidunderstandingofthedistributionofthespeciesof interest,whichcanbedifficultforcave-adaptedspeciesfor severalreasons.First,cave-adaptedfaunasarecharacterizedbyasuiteofuniquemorphological(lossofeyesand pigmentation,elongationofappendages,hypertrophyof non-opticsensoryorgans)andphysiological(increasedlife spansanddevelopmenttimes,reducedmetabolicratesand numbersofeggs)traits.Thesetroglomorphictraits, exhibitedonaglobalscaleacrossdiversetaxonomic groups,areoneofthemostpowerfulexamplesof habitat-drivenconvergenceofform(PorterandCrandall, 2003)andoneofthefewdemonstratedcaseswhere convergentmorphologycanstronglymisleadphylogenetic analyses(Wiensetal.,2003).Thecombinationofregressive (lost)andprogressive(enhanced)featuresfoundincaveadaptedfaunascanleadtotheexistenceofcrypticspecies, wheretwogeneticallydifferentspeciesaregivenonename basedonmorphologicalsimilarities.Evenwhenspeciesare diagnosedproperly,convergentmorphologiesoftenleadto hypothesesofcloseevolutionaryrelationshipsamong highlycave-adaptedspecies,wheninfacttheyrepresent S UBTERRANEANBIOGEOGRAPHY :W HATHAVEWELEARNEDFROMMOLECULARTECHNIQUES ? 180 N JournalofCaveandKarstStudies, April2007

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moredistantlineages(Wiensetal.,2003).Insomecases, troglomorphicmorphologieshaveledtoincorrecttaxonomicdesignationsabovethespecies-level;molecular studiesofthestygobioticcatfish Prietellaphreatophila and Prietellalundbergi indicatethateachismoreclosely relatedtospeciesfromdifferentgenerathantheyareto eachother( P.phreatophila to Ictalurus speciesand P. lundbergi to Ameiurus species;Wilcoxetal.,2004).Inthe absenceofobviousmorphologicaldifferencesdueto extremeconvergence,molecularphylogeneticstudiesof troglobioticandstygobioticspecieshavebeensuccessfulat diagnosingthepresenceoftaxonomicincongruenciesbased oncrypticmorphologies,therebychangingourunderstandingofthedistributionofsubterraneanfauna,and theirrelationshipswitheachotherandwithepigeanspecies (Chippindaleetal.,2000;Parra-Olea,2003;Buhayand Crandall,2005). Duetolowpopulationdensities,therarityofencounteringsomespecies,andthedifficultiesassociatedwith collectinginsomecaveenvironments,ourunderstandingof thedistributionofcavefaunaisalsohamperedbythe difficultyinobtainingadultspecimens,whicharerequired foraccuratespeciesidentificationandtaxonomicscrutiny. Theseconstraintscanbeovercomebyusingmoleculardata tocompareimmaturespecimenstoadulttypesofknown species.Forexample,thisapproachhasbeenused successfullywiththe Cicurina speciesfromTexas,extendingtherangeofthefederallyendangered C.madla tomore thantwicethenumberofpreviouslyreportedcaves; however,itisnotedthatthisapproachmustremainapart ofabalancedtaxonomicapproachbymaintaining ataxonomicframeworkbaseduponmultipletypesof biologicalinformation(e.g.,morphology,molecules,and ecology[PaquinandHedin,2004]). D ISPERSAL A BILITY Thephrase‘‘limiteddispersalability’’iscommon throughoutthebiospeleologicalliterature(Holsinger, 1991;Coineau,1994;CacconeandSbordoni,2001;Baratti etal.,2004).Thisassumptionleadstohypothesesrelatedto theisolationandspeciationofcavefaunas;limited dispersalabilitiesresultinlittletonogeneticexchange betweenpopulations,allowingisolatedpopulationsto becomegeneticallydistinct,ultimatelytothepointof becomingdifferentspecies.However,thisdispersalassumptioncanbedifficulttotestempirically,particularly forspeciesthatmayspendasignificantamountoftime traversingrealmsofthekarstlandscapeandassociated ground-waterhabitatsthatareinaccessibletothehuman researcher.Forexample,BuhayandCrandall(2005)used molecularstudiesofthemitochondrial16SrRNAgeneto investigatethestygobiotic Orconectes speciesinthe Appalachians;largerthanexpectedeffectivepopulation sizeswereusedtoinfertheoccurrenceofaground-water networkunknowntohumansbutaccessibletothecrayfish. Furthermore,limiteddispersalabilityisaqualitative statement,providingnoinformationusefulfordetermining dispersalcapabilitiesrelativetohabitatorotherspecies. Yet,thistenetoflimiteddispersalisacentralassumption topostulatesoftheimportanceofvicarianceinsubterraneandistributions. Usingmolecularmethods,biospeleologistshavebegun toquantifythedispersalabilityofsubterraneanfauna,in bothrelativeandabsoluteterms.Comparingestimated geneflowamongpopulationsofcaveandforest-dwelling cricketspecies,CacconeandSbordoni(1987)demonstrate thatcavespecieshavelowerratesofgeneexchangethan epigeanspecies,withthedegreeofgeneticdifferentiationin hypogeanspeciescorrelatedwiththecontinuityofthe limestonehabitat.Similarly,inaquaticsystems,population differentiationisrelatedtohabitatconnectivity(Sbordoni etal.,2000).Giventhatecologicalstudieshaveshownthat wide-rangingmovementsarepossibleforsomestygobiotic species,particularlythosecapableofmovingthrough interstitialhabitats,suchasostracods(Danielopoletal., 1994),andthataquatichabitatshavegenerallyhigher connectivity,stygobiontsshouldhavegreaterdispersal potentialandcapabilitiesthantroglobionts(Lamoreaux, 2004). Attheheartofthisissuearebasicquestionssuchas: Whatconstitutesacavepopulation?Whatisthevagilityof aparticularspecies?Howconnectedarethesepopulations? Ishabitatconnectivitylimitingdispersal?Wasthehabitat moreorlessconnectedinthepast?Thesequestionsare affectedbothbyintrinsicandextrinsicfactors,making acompleteanswerdependentonunderstandingboththe ecology(dispersalcapability)andhabitat(dispersalpotential)ofanorganism.Molecularmethodscanaddressallof thesequestions,astheevolutionaryhistory(includingpast andpresentdispersalevents)isreflectedinthegenetic differencesamongpopulations,species,andgeneraof subterraneanfauna.Bydelineatingpopulationsusing genotypicclusteringmethods,theconnectivityofasystem canbeinvestigated.Forexample,differentcavesinthe samehydrologicsystemrepresentingasingle,randomly matingpopulationcanreadilybeidentified.Conversely, patternsofgeneticdifferentiationcanbeusedtoidentify eitherunseenbarrierstogenefloworgeneflowacross hypothesizedgeographicbarriers;byestimatingthephylogeneticstructureanddivergencetimesofthestygobiotic amphipod, Niphargusvirei ,Lefe bureetal.(2006)found evidenceforrecentdispersalthroughapparentgeographic barriers. Oneofthefewcaseswheremolecularstudiesshow strongsupportforanactivemigration(dispersal)modelis intheanchialinegastropod, Neritiliacavernicola (Kano andKase,2004). N.cavernicola isastygobiontfoundin anchialinecavesontwoislandsinthePhilippinessituated 200kmapart.Geneticstudiesfoundnoevidenceof isolationbetweentheislands,indicatingthepresenceof amarineplanktotrophicphasecapableofmigrating betweentheislandsviaoceancurrents(KanoandKase, M EGAN L.P ORTER JournalofCaveandKarstStudies, April2007 N 181

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2004).KanoandKasehypothesizethatthisactive migrationmodel,dependentonalarvalstagetolerantof marinewaters,maybecommoninanchialinestygobiotic faunaexhibitingdisjunctinsulardistributions. Migrationratesandpopulationstructuresmaybethe mostinterestinggeneticparameterstoestimateamong troglobiontsandstygobiontsasamethodtotestthe hypothesisthatcave-adaptedspeciesareindeedpoor dispersersrelativetoepigeanorganisms,andtoquantify thedifferencesindispersalabilitiesamongtroglobiontsand stygobionts,andamongstygobiontsfromdifferentsubterraneanhabitats(epikarsticvs.phreatic). V ICARIANCE Intheclassicmodelofvicariance,aoncewidely distributedancestralspeciesisfragmentedwithinitsrange byanexternal(geologicalorclimatic)event.This fragmentationleadstoisolationofdifferentsegments (populations)ofthespecies,allowingforgeneticdifferentiation,andoftenspeciation.Importanttothismodelis timing;datingtheeventleadingtofragmentationalso providesthetimesincedivergenceofthederivedsetof species.Becausethismodelistiedtoexternalevents, examplesofvicariance-drivenbiogeographypatternsare mostobviousatlargescales,includingcontinentalmovementsviatectonicevents(Holsinger,2005;Culveretal., 2007).Oneofthemostwidelyused(andconvincing) methodsinbiogeographytodemonstratetheselargescale vicariancepatternsistolookforcongruenceinarea cladogramsconstructedfordifferentsetsofspeciesthat havesimilardistributions.Basically,evolutionaryrelationshipsarereconstructedamongdiversesetsofspeciesfrom agivenarea,andcorrelatedwithgeography.Ifsimilar patternsofgeographicpatterningpartitionedbyevolutionaryrelationshipsemergeinmanydifferenttaxa,there isstrongevidenceforlarge-scalevicariantevents.Krejca (2005)proposedanevenmorerigoroustest,wherean apriori hypothesisofdivergencepatternsiscreatedbased ongeologichistoryofaregion,whichisthentestedby comparisontophylogeniesconstructedforthesubterraneanfaunaofthatregion.Molecularphylogeneticmethods assisttheseendeavorsbymakingitpossibletoquickly generatecladogramsforlargenumbersofpopulationsand species.However,thesetypesofbroadstudiesusing moleculardatahavenotyetbeenwidelyemployedto investigatesubterraneanbiogeography(seeKrejca,2005 foranexample). Theclearestexamplesofvicarianteventsinkarst systemsare1)marineregressions(Culveretal.,2007) and2)extirpationofsurfacepopulationsfromaspecies withbothepigeanandhypogeanpopulations.However,in karstsystems,patternsresultingfromthesetypesof vicarianteventsarevirtuallyindistinguishablefromadistributionresultingfromdispersal(Culveretal.,2007). Therefore,perhapsthemostpromisingwaytoinvestigate therelativeinfluenceofdispersalversusvicarianceinkarst settingsistostudyspecieswherebothhypogeanand epigeanpopulationsstillco-existorwherecloselyrelated surfacespecieshavenotyetbeenextirpated.However,even ifasurfaceancestorstillexists,itcanbedifficulttoidentify duetotheradicalmorphologicalchangespresentinthe subterraneanmorphotype.Higher-levelmolecularphylogeneticstudiesofferincreasedresolutionforcomparisons acrosslargegeographicscalesbyprovidingmorecharactersforphylogeneticanalysesinorganismswhere convergencecanmakemorphologicalcharactersdifficult, andcanhelpelucidaterelationshipsamongextanthypogeanandepigeanrelationships(Cooperetal.,2002;Wiens etal.,2003). Someofthebest-studiedexamplesofspecieswithboth epigeanandhypogeanpopulationsincludetheisopod, Asellusaquaticus ,andthefish, Astyanaxmexicanus (Fig.1).Inthesespecies,cave-adaptedpopulationsoccur inthesamedrainagesasepigeanpopulations,offeringthe abilitytoinvestigateprocessesinvolvedinthecolonization andisolationofsubsurfacepopulationsattheincipient stagesofspeciation. Molecularstudiesof A.aquaticus incorporatingestimatesofpopulationstructureindicatethatsurface populationscolonizedcavestoformstygobioticpopulationsthreetimeswithintheDinarickarstofSlovenia (Verovniketal.,2004).Furthermore,estimatesofdivergencetimeindicatethatthesubsurfacewasinvaded aftertheancestralpopulationswereisolatedbyvicariant fragmentation,demonstratingthegeneticfootprintancestralsurfacepopulationstructuresleaveinhypogean populationsandspecies.Similarly,molecularinvestigationsof A.mexicanus indicatemultipleoriginsofcave populations,representingatleasttwoindependentinvasionsfromsurfacepopulations,withnomeasurablegene flowoccurringbetweensurfaceandcavepopulations (Dowlingetal.,2002;Streckeretal.,2003).Again,the phylogeneticanalysesindicatethattheevolutionaryhistory ofthesurfaceancestorscontrolsthegeneticdifferentiation Figure1.Epigean(A)andhypogean(B)formsof Astyanax mexicanus .ScalebarinA 1cm.Epigean(C)and hypogean(D)formsof Asellusaquaticus (photosprovided byB.Sket).Specimenlengthineachpanel ca.10mm. S UBTERRANEANBIOGEOGRAPHY :W HATHAVEWELEARNEDFROMMOLECULARTECHNIQUES ? 182 N JournalofCaveandKarstStudies, April2007

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ofthehypogeanpopulations,withthreeofthefourcave populationsinvestigatedoriginatingfromanancestral sourcedifferentfromthecontemporarysurfacepopulations(Streckeretal.,2003,2004). Usingmoleculartechniques,thispatternofmultiple invasionsintosubterraneanaquatichabitatshasbeen documentedformanystygobioticspecies(KanoandKase, 2004;Lefe bureetal.,2006),includingthestygobiotic dytisciddivingbeetlefaunafoundincalcreteaquifersfrom westernAustralia(Cooperetal.,2002;Leysetal.,2003). Thedytiscidfaunafromthisregionhasinvadedthe subsurfaceindependentlyatleast26times(18timeswithin thetribeBidessiniandeighttimeswithinthetribe Hydroporini;Leysetal.,2003)andbasedondivergence timeestimationshowsanevolutionarypatternconsistent withaclimaticvicariantevent,whereincreasingaridityin theregionextirpatedawidespreadepigeanancestor, drivingtheevolutionofthesubterraneandivingbeetles (climaticrelicthypothesis;Cooperetal.,2002;Leysetal., 2003). Fromthesestudies,theimportanceofthedistribution andgeneticstructureoftheancestralsurfacespeciesis emphasizedincontrollingsubterraneanbiogeographic patternsandcurrentgeneticrelationships.Thedifficulty liesinelucidatingtheinfluenceofextinctepigean populationstructureonsubterraneanbiogeographyfrom processesoccurringafterthecolonizationofcaves. D IVERGENCE T IMES Perhapsoneofthemostimportantparametersthatcan beestimatedusingmoleculardataislineageages.Placing datesontheoriginsofaparticularcave-adaptedlineageis aninterestingandthought-provokingexercise,which leavesopenthetemptationtocorrelatedivergencetimes withtimingofcavecolonization.However,itisnecessary torememberthattheageofaparticularlineagedoesnot necessarilycorrelatewiththetimeofcaveinvasion (Verovniketal.,2005).Particularlyinhighlyfragmented surfacehabitats,epigeanpopulationscanbehighly isolated,andthereforegeneticallydivergentpriortocave invasion(seeprevioussection[Verovniketal.,2004]);this situationresultsinestimatedlineageagesmucholderthan timeofcaveoccupancy,leadingtomisinterpretationof biogeographicdeterminants.Conversely,ifdispersaland subsequentisolationareanimportantdeterminantof subterraneanbiogeography,itispossibleforlineagestobe youngerthantimeofkarstinhabitation.However,by knowingthesestipulationsandactingconservatively, estimatinglineageagesisstillaworthwhileendeavor. Whencombinedwithinformationonregionalgeologic histories,large-scalebiogeographicpatternscanbelinked toeithervicariantordispersalevents.Interestingly,mostof thestudiesestimatingdivergencetimesusingmolecular clockmethodshaveinvestigatedstygobionts,andhave postulatedvicariancemodelsoramixedmodelofrepeated rangeexpansionsandvicariantisolation(Table1)(Ketmaieretal.,2003;BuhayandCrandall,2005;Lefe bureet al.,2006).Inthosestudieswheremixedmodelswere invoked,however,vicarianteventswererelatedtolarger scalephenomenawhiledispersalwaslinkedtosmallerscale phenomenawithinkarstbasins. Manymolecularstudiesofcavefaunahaveusedgene sequencedatatoestimatedivergencetimesbasedon molecularclocks,theassumptionthatDNAsequences changeataconstantrateovertime(Table1)(Zuckerkandl andPauling,1965).Withanestimateofsequencedivergence betweentwospeciesandamutationrateinnumberofbase pairsubstitutionsperunittime,preferablycalibratedtothe taxonofinterest,theagesincethesplitcanbeinferred. Thereareanumberofcaveatsassociatedwiththistypeof analysis,however.Whenratesofevolutionarecompared withincloselyrelatedspeciesforthesameDNAregion,itis generallyassumedtheydisplayclock-likebehavior;however,mostdatasetsappeartoviolatetheclockmodel(Graur andMartin,2004).Yetthisassumptionisrarelytestedin studiesofcaveanimals(seeCacconeandSbordoni,2001 andLeysetal.,2003forexamplestestingtheassumptionof amolecularclock)andtheprevalenceofmanyancientcave adaptedlineagesmaysignificantlyviolateanyassumptionof clock-likeevolution.Second,usuallymutationrateshave notbeenestimatedforthespeciesofinterest,somutation ratesfromother,sometimesnotsocloselyrelated,organismsareused.Asthisrateisusedtoconvertsequence divergencetotime,thisisacriticalassumption.Third, becausemutationratesvaryamonggenes,usuallyestimates arebasedonasinglegeneticmarker.However,even consideringalloftheseissues,intheabsenceofgoodfossil dataorgeologiceventsofaknownage,molecularclock estimatesprovideareasonablefirstapproximationoftime (Cooperetal.,2002).InastudyoftroglobioticBathysciine beetlesfromSardiniausingmitochondrialsequencedata fromthecytochromeoxidaeIgene(COI),Cacconeand Sbordoni(2001)illustratehowthesecaveatscanberesolved. First,theassumptionofamolecularclockwastestedby investigatingthelinearityofevolutionintheCOIgene. Next,ratesofCOIevolutionwereempiricallyderivedby calibratingsequencedivergencetodatesfromwell-defined geologicaleventsrelatedtothesplittingofthebeetlelineages (CacconeandSbordoni,2001).Thesetypesofstudiesare extremelyusefulforcalibratingratesofevolutionincave fauna,forinvestigatingtheevolutionofthetroglomorphic form,andforprovidingrateestimatesfordivergencetime estimationsincavespecieswherewell-definedgeological eventscorrelatingtolineagesplittingarelacking. Morerecentphylogeneticmethodsinestimatingdivergencetimesrelaxtheassumptionofclock-likesequence evolutionandallowformultiplemolecularmarkerstobe incorporatedintotheestimate(Thorneetal.,1998; Sanderson,2002;ThorneandKishino,2002;Yang, 2004),butthesemethodsalsorequirecalibrationpoints (i.e.,fossilsorgeographiceventsassociatedwithlineage splittingofknownages)tocalculatedivergencetimes M EGAN L.P ORTER JournalofCaveandKarstStudies, April2007 N 183

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Table1.Representativestudiesusingmoleculardatatoinvestigatetheb iogeographyoftroglobioticandstygobioticspecies. TaxaGenes a Biogeographic model b Region EstimatedAgesof BiogeographicEventsReference Troglobiotic Arachnida Araneae Nesticus ND1V,D,CAppalachians,U.S.A. Hedin,1997 Hexapoda Coleoptera Ovobathyscioloa COIVSardinia,ItalySealeveloscillations16–5.5MaCacconeandSbordon i,2001 Patriziella COIVSardinia,ItalyPlioceneclimatechangeCacconeandSbordoni,2001 Orthoptera Dolichopoda 16S,COIVMediterraneanPleistoceneAllegruccietal.,2005 Crustacea Isopoda Littorophiloscia COIV,DHawaii,U.S.A. Riveraetal.,2002 Hawaiioscia COIV,DHawaii,U.S.A. Riveraetal.,2002 Stygobiotic Hexapoda Coleoptera Dytiscidae COI,16S, tRNA leu ND1 VWesternAustraliaLateMiocene/EarlyPlioceneCooperetal.,2002;Leys etal., 2003 Crustacea Amphipoda Niphargusvirei COI,28SV,DFrance13MaLefe bureetal.,2006 Isopoda Asellusaquaticus COI,28SV,DDinaricKarst,Europe8.9–2.9MaVerovniketal.,2004,2005 Typhlocirolana 12S,16SVMediterraneanbasinTethyaneventsBarattietal.,2004 Stenasellus COIV,DCorsica,Sardinia, Tuscany,Pyrenees, Italy MioceneeventsandQuaternary glaciations Kentmaieretal.,2003 Decapoda Orconectes 16SV,DAppalachians,U.S.A.CretaceousBuhayandCrandall,2005 Gastropoda Neritiliacavernicola COIDPhilippines KanoandKase,2004 Vertebrata Teleostei Astyanaxmexicanus cytB,ND2V,DNorthandCentral America 4.5–1.8MaDowlingetal.,2002;Strecker etal.,2003;Streckeretal.,2004 a Generegionabbreviations:COI cytochromeoxidaseI,cytB cytochromeB,ND1 NADHdehydrogenasesubunit1,ND2 NADHdehydrogenasesubunit2,16S 16SribosomalRNA,12S 12SribosomalRNA, tRNA leu leucinetransferRNA,28S 28SribosomalRNA.Allgenesincludedinthistablearemitochondrial,exc eptfor28Swhichisanucleargene. b V vicariance,D dispersal,C competition. S UBTERRANEANBIOGEOGRAPHY :W HATHAVEWELEARNEDFROMMOLECULARTECHNIQUES ? 184 N JournalofCaveandKarstStudies, April2007

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acrossaphylogeny.Theseschemesareonlyrecentlybeing appliedtosubterraneanbiogeographicquestions(Leyset al.,2003;Lefe bureetal.,2006),andofferinteresting researchavenuesthatcancorrelatetheageofacavewith phylogeneticestimatesofhypogeandivergencetimes. Usingamethodthatrelaxesthemolecularclockassumption,Leysetal.(2003)investigatedthetimingofthe transitionfromsurfacetosubterraneanlifeintheremarkablediversityofstygobioticdytiscidaefoundincalcrete aquifersinWesternAustralia.Byestimatingdivergence timesbetweenepigeanandhypogeanspecies,andbetween closelyrelatedspeciespairsthatdivergedafterinvasionof thesubterraneancalcretehabitat,awindowwasestimated forwhenthehypogeantransitiontookplace.The estimatedagesfortheeightpairsofspeciesoccurringin thesamecalcreteaquifersrangedfrom3.6–8.7Ma, representingtheminimumageofthesubterraneanlineages. Estimatesfromhypogeanspeciespairsoccurringin differentcalcreteaquifers(representingindependentsubterraneaninvasions)provideamaximumagefrom4.8– 8.9Ma,makingthewindowoftransitionfromsurfaceto subterraneanhabitatsfrom8.9–3.6Ma.Interestingly, therewasalatitudinalpatternindivergencetimescoincidingwiththeonsetofaridity,withspeciespairsfrom northernlocalitiesdivergingearlierthansouthernlocalities (Leysetal.,2003). T HE F UTUREOF S UBTERRANEAN B IOGEOGRAPHY Thereisstillmuchtolearnabouttheprocessesdriving currentdistributionalpatternsoforganismsfromcaves andkarstsystems,andthecombinationofmolecular techniqueswiththeextensiveworkofsubterranean biogeographersoffersthepotentialtorefinethequestions beingasked.Molecularphylogeneticsandpopulation geneticsoffersubterraneanbiogeographytheabilityto identifycrypticspecies,tolinkunidentifiablejuvenile specimenstorareadultmorphotypestoexpanddistributionalranges,todeterminedispersalabilitiesviaestimates ofgeneflow,populationstructure,andmigrationrates, andtoestimatedivergencetimes.Currentmolecular studiesofhypogeanpopulationsoverwhelminglyinvoke eithervicarianthypotheses,ofeithertheancestralsurface orcavepopulations,orproposeamixedmodel,linking vicariancewithrangeexpansions(i.e.,dispersal),toexplain subterraneandistributionalpatterns(Streckeretal.,2004; Verovniketal.,2004;BuhayandCrandall,2005;Lefe bure etal.,2006);fewstudieshavefoundevidencefor adispersal-onlymodelofbiogeography(KanoandKase, 2004).However,atsmallerscales(karstbasins),molecular investigationsofdispersalabilitiesofferinsightsintothe connectivityofthesubterraneanrealm.Asmolecular estimatesofparameterssuchaspopulationstructure, migrationrates,anddivergencetimes,becomemore common,itwillbepossibletoinvestigatehowthe disparitiesbetweentroglobioticandstygobioticspecies affectgeneticdivergenceandspeciation,andtobeginto quantifythedispersalabilitiesofcaveorganismsingeneral. Themolecularbiogeographicalstudiesofsubterranean faunathusfarhaveprovidednewperspectivesintothe distributionpatternsofhypogeanfauna,reinvigoratingthe vicarianceversusdispersaldebate.Finally,manyofthe molecularanalysesusedinbiogeographicstudies(populationstructure,geneflow,distributions)arealsoofsupreme importancewhenconsideringconservationandmanagementissuesforsubterraneanfauna(BuhayandCrandall, 2005).Continuedmolecularinvestigationswillprovide informationnecessaryforidentifyingthemostimperiled cavespeciesneedingconservation. A CKNOWLEDGEMENTS ThankstoD.C.Culver,D.Fong,andH.H.HobbsIII forvaluableinsightsanddiscussionsregardingsubterraneanbiogeography,andforthesuggestiontowritethe manuscriptinthefirstplace.IamgratefultoW.R.Jeffery andB.SketforprovidingphotographsandtoD.C.Culver, K.DittmardelaCruz,A.S.Engel,andM.Pe rezLosada forhelpfulcommentsregardingthemanuscript. 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OBSERVATIONSONTHEBIODIVERSITYOFSULFIDIC KARSTHABITATS A NNETTE S UMMERS E NGEL DepartmentofGeologyandGeophysics,LouisianaStateUniversity,Baton Rouge,LA70803USA,aengel@geol.lsu.edu Abstract: Recognitionofthemetabolicprocessofchemosynthesishasrecently overthrowntheecologicaldogmathatalllifeonearthisdependentonsunl ight.In completedarkness,complexecosystemscanbesustainedbytheenergyandn utrients providedbychemosyntheticmicroorganisms.Manyofthesechemosyntheti cally-based ecosystemsresultfrommicrobialmanipulationofenergy-richsulfurcom poundsthatcan befoundinhighconcentrationsingroundwater.Subsurfaceenvironments ingeneralcan behighlystressfulhabitats(i.e.,darkness,limitedfood,etc.),butin thecaseofsulfidic groundwaterhabitats,organismsmustalsotolerateandadapttodifferen tstresses(e.g., toxiclevelsofgasesorlethallylowoxygenconcentrations).Neverthele ss,thesehabitats, andspecificallycaveandkarstaquifers,havearichlydiversefauna.Thi sreviewfocuses onthebiodiversity(asthenumberandtypesofspecies)ofsulfur-basedca veandkarst aquifersystems.Therelationshipsamongecosystemproductivity,biodi versity,and habitatandecosystemstressesareexplored.Therelativelyhighnumbers ofspeciesand complextrophiclevelscouldbeattributedtotherichandplentiful,chem osyntheticallyproducedfoodsourcethathaspermittedorganismstosurviveinandtoadap ttoharsh habitatconditions.Thegeologicageandthehydrologicalandgeochemica lstabilityof thecaveandkarstaquifersystemsmayhavealsoinfluencedthetypesofeco systems observed.However,similartonon-sulfidickarstsystems,moredescript ionsofthe functionalrolesofkarstaquifermicrobesandmacroscopicorganismsare needed.As subterraneanecosystemsarebecomingincreasinglymoreimpactedbyenvi ronmental andanthropogenicpressures,thisreviewandthequestionsraisedwithin itwillleadtoan improvedunderstandingofthevulnerability,management,andsustainab ilitychallenges facingtheseuniqueecosystems. I NTRODUCTION Cavesrepresentdiscontinuouscontinentalsubsurface habitatsthatarecharacterizedbycompletedarkness, nearlyconstantairandwatertemperatures,relative humiditynearsaturation,andgenerallyapoorsupplyof nutrients.Excludingclimaticfluctuationsthatcouldbring thermally-orchemically-contrastingairorwaterinto acave’sinterior,thephysicalarrangementsandconstraints ofmostsubterraneanhabitatshaveremainedrelatively unchangedforthousands,ifnotmillions,ofyears(e.g., Gale,1992).Formostpeoplewhohavesatinthesunless silenceofacave,theconceptthatlifecouldflourishinsuch conditionsforevenashortperiodoftimeisprofound. Indeed,colonizingthesubsurfacerequiresspecificadaptationstothestressesoflivingindarknessandtotheextreme environmentalconditionsencountered,suchasnutrient andenergylimitations,thepossibilityofexperiencing oxygendeprivation,high-waterpressuresduetolivingat deepaquiferdepths,orgeochemicallyvariablesolutions. Recently,studieshavefocusedonthemetabolicand evolutionarymechanismsthataddressthesurvivalof subsurface-orcave-adaptedfaunas(e.g.,Jonesetal., 1992;Howarth,1993;Hervantetal.,1999a;Porterand Crandall,2003;HervantandMalard,2005;Hu ¨ppop,2005; Lefe bureetal.,2006).Duetosuchspecializedadaptations, manyspeciesofobligatesubsurfacetroglobites(livingin terrestrialhabitats)orstygobites(livinginaquatichabitats) havehighdegreesofendemism(Barr,1967;Culveretal., 2003). Thepaucityofacontinuousnutrientsupplyisoneof thecriticalextremeconditionsaffectingsubsurfaceadaptedfauna,asmostarequitedependentontheflux ofnutrientsandenergyfromthesurface,specifically fromphotosynthetically-producedorganicmatter.Often, thismaterialcomesintheformofwind-blown,meteoric-, andstream-deriveddetritus(e.g.,particulatematterlike leavesorwoodydebris,orasdissolvedorganiccarbon), orfrombatandotheranimalguano(Barr,1967;Culver, 1976;Brownetal.,1994;PoulsonandLavoie,2000; GibertandDeharveng,2002;Simonetal.,2003; Hu ¨ppop,2005).Consequently,organismsreliantonthe transportofeasily-degradedorganicmattermayexperienceprolongedperiodsofstarvation.Numerousstudies haveshownthatincreasedfeedingefficiency,lower metabolicrates,slowergrowthrates,andreduced fecundityarelinkedtonutritionalstress(e.g.,Hervant etal.,1999b;Hu ¨ppop,1985,2005).However,agrowing bodyofevidencerevealsthatsomesubsurfaceandcave ecosystemsdonotrelyexclusivelyonsurface-derived AnnetteSummersEngel–Observationsonthebiodiversityofsulfidickars thabitats. JournalofCaveandKarstStudies, v.69,no.1, p.187–206. JournalofCaveandKarstStudies, April2007 N 187

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organicmatter(e.g.,Stevens,1997;Krumholz,2000; AmendandTeske,2005). Intheabsenceoflight,reactiverocksurfacesand mineral-richgroundwaterprovideawideassortmentof potentialenergysourcesthatmicrobial chemolithoautotrophs (translatedlooselyasrock-eatingself-feeder)can usetogaincellularenergywhilemakingorganiccarbon moleculesfrominorganiccarbon(i.e.CO 2 ,HCO 3 ). Chemolithoautotrophsaredistinguishedfromphotosyntheticorganismsbasedonwhethertheenergysourceis frominorganicchemicals( litho)orfromlight( photo). Conversely, heterotrophs useorganiccarbonforcellular energyandasacarbonsource,and chemoorganotrophs useorganiccompoundsforacarbonsourceandobtain cellularenergyfromchemicaltransformations.Chemolithoautotrophsareimportanttoglobalbiogeochemical cyclesandecosystem-levelprocessesbecausetheycan cyclevariouselementssimultaneouslywhilegenerating considerableamountsoforganiccarbonandservingas thebaseofecosystemfoodwebs.Someresearchershave hypothesizedthatsubsurfacechemolithoautotrophicprimaryproductivitymaysurpasstheactivityofphotosyntheticorganismsontheEarth’ssurface(e.g.,Stevens, 1997). Priortothe25 th anniversaryissueoftheBulletinofthe NationalSpeleologicalSocietyin1966,andintheyears thatfollowed,theconceptthatchemosynthesiscould sustainsubsurfaceecosystemswasnotcommonlyaccepted (norunderstood),aschemolithoautotrophicactivitywas consideredinsufficienttosupportecosystem-levelprocesses(e.g.,Schreiber,1929;WoltersandSchwartz,1956; Barr,1966,1967;Caumartin,1963;PoulsonandWhite, 1969;GinetandDecou,1977).Thediscoveryofchemolithoautotrophically-basedecosystemsatthedeep-sea hydrothermalventsinthelate1970s(e.g.,Jannasch, 1985;DemingandBaross,1993)toppledthedogmathat alllifeonearthwasdependentonsunlight.In1986, anotherimportantbreakthroughfurtherchangedperceptionsoflifeinthecontinentalsubsurface,andofcave ecosystemsingeneral;thatdiscoverywastheuniquely diversechemolithoautotrophically-basedecosystemfrom thehydrogensulfide-rich( sulfidic )groundwaterassociated withtheMovileCave,Romania(Sarbu,1990;Sarbuetal., 1996). Sulfur,asthe14 th mostabundantelementinthe Earth’scrust,isbiogeochemicallyimportantbecause proteinsandothercellularcomponentsofalllifeare comprisedofatleast0.5–1%sulfurbydryweight (ZehnderandZinder,1980).Nearlyallorganismsget theirrequiredsulfureitherfromconsumingorganicsulfur compoundsorfromassimilatorysulfatereduction.Sulfur existsinavarietyofvalencestates,fromthemost reducedformashydrogensulfide(H 2 S)tothemost oxidizedformassulfate(SO 4 2 ).Changesinvalencyare attributedtothegeochemicallyreactivenatureofthe varioussulfurcompounds(e.g.,Milleroetal.,1987; Megonigaletal.,2005),andprokaryotes(fromthe domains Bacteria and Archaea )cangainenergyby transformingonevalencestatetoanother.Manyofthe transformationswithinthesulfurcyclearecatalyzed almostexclusivelybymicroorganisms,andbiological sulfurcyclingmustbetightlycoupledwithoxidationreduction(redox)reactionstoout-competetheabiotic reactions(forareview,seeMegonigaletal.,2005).The relationshipbetweenthemetabolicrequirementsfor sulfurandoxygen(O 2 )causesmanysulfur-dependent microbestooccupyinterface,orgradient,habitatswith arangeofO 2 concentrationsfromhighly-oxygenated ( aerobic )toO 2 -deprived( anaerobic ). Chemolithoautotrophicecosystemshavebeenidentified frommarinesediments(e.g.,D’Hondtetal.,2002;Amend andTeske,2005),continentalaquifers(e.g.,Stevensand McKinley,1995;Stevens,1997;AmendandTeske,2005), andothercavesandkarstsettings(e.g.,Pohlmanetal., 1997;Vlasceanuetal.,2000;Engeletal.,2004a).Insome deep,isolatedcontinentalaquifers,chemolithoautotrophic methanogenicmicrobialcommunitiesaresupportedbythe geochemicalproductionofmolecularhydrogen(H 2 ) (StevensandMcKinley,1995;AmendandTeske,2005). Nohighertrophiclevels,includingmicroscopiceukaryotes,havebeenreportedtodatefromthesemicrobial ecosystems;thisstarklycontrastswiththetrophicdiversity foundatthedeep-seaventsandfromsulfidickarstsystems wheresulfurcompoundsareexploitedbychemolithoautotrophs(e.g.,Jannasch,1985;Sarbuetal.,1996;Engel, 2005). HereIexplorethebiodiversityofsulfidiccaveandkarst ecosystems.Themotivationforthisreviewwastoevaluate therelationshipsamongecosystemproductivity,biodiversity(asthenumberandtypesofspecies),andhabitatand ecosystemstresseswithrespecttoecosystemstability.Of theknownlocationsforsulfidickarst(Fig.1),thereis generallyaclumpeddistributionofsystemsinNorth AmericaandEurope.Thiscouldrelatetotheabundanceof (bio)speleologistsonthesecontinents,butalsotothe geologicandhydrostratigraphichistoryofthekarst.Itis likelythatmoresulfidickarstsystemsaredistributed worldwide;assuch,considerableadventuresawait.This reviewconcludeswithaperspectiveonthedirectionsof futurework. O RIGINOF S ULFIDIC C AVEAND K ARST S YSTEMS Theclassicspeleogenesismodelinvokescarbonicacid dissolutionofcarbonaterocks,usuallyatshallowdepths andrarelyfarbelowthewatertable(e.g.,Palmer,1991). Thealternativekarstificationprocessofsulfuricacid speleogenesiswasinitiallyproposedbyS.J.Egemeierfrom workinLowerKaneCave,Wyoming(Egemeier,1981), wheregroundwaterbearingdissolvedsulfidedischargesas springsintothecavepassage.Hydrogensulfidegas O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 188 N JournalofCaveandKarstStudies, April2007

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volatilizesfromthegroundwatertothecaveatmosphere 1 andisoxidizedtosulfuricacidonmoistsubaerialsurfaces: H 2 S 2O 2 < H 2 SO 4 1 Theacidreactswithandreplacescarbonatewithgypsum (CaSO 4 2H 2 O), CaCO 3 H 2 SO 4 H 2 O < CaSO 4 2H 2 O CO 2 2 Thisspeleogeneticprocesshasbeensuggestedtoexplain theformationalhistoryofactivecavesystemsglobally (Hubbardetal.,1990;Sarbuetal.,1996;Galdenziand Sarbu,2000;Hoseetal.,2000;Sarbuetal.,2000),ancient caveslikeCarlsbadCavern,NewMexico(Hill,1996; PolyakandProvincio,2001),andsomecontinentalkarst aquifersatorjustbelowthewatertable(Hill,1990,1995; Schindeletal.,2000).LoweandGunn(1995)suggestthat sulfuricacidmaybeimportantforallnascentsubsurface carbonateporositygeneration,andPalmer(1991,1995) furtherspeculatesthatsulfuricacidspeleogenesisismore importantfortheevolutionofcarbonate-hostedpetroleum reservoirsthanitisfortheoriginofcaves,astheprocess hasbeenlinkedtothekarstificationofreservoirs,e.g.,the LisburnefieldinPrudhoeBay,Alaska(Jameson,1994; Hill,1995). Variousbiological,geologic,andhydrostratigraphic parametersgenerateH 2 S.Asalllifegeneratessmall amountsofH 2 Sfromthebreakdownofsulfur-containing organiccompounds(e.g.,proteins),H 2 Sisproduced duringthedecayanddecompositionoforganicmatter, suchasinswamps.Microbialreductionofsulfate-bearing minerals,suchasgypsum,ordissolvedsulfateinmarineor freshwatergeneratesH 2 S(seediscussionbelow).Microbial 1 ASafetyNote: Caveexplorersandresearchersworkinginactivesulfidiccavesare exposedtoharshconditions,includingtoxicgasesandthepossibilityof reduced oxygenlevels.Hydrogensulfideisacolorlessflammablegasthatcancaus e headaches,dizziness,nausea,andirritabilitywithprolonged,low-lev elexposure.The rotteneggsodor(detectableto0.5ppbvinair)isnotagoodindicatorofth e atmosphericconcentration;exposuredullsthesenseofsmell.Athighere xposure levels,thisdesensitizationcanleadtocomaanddeath.Above20ppmv,H 2 Scauses eyeandmucousmembraneirritation,andpulmonaryedemainfewcases.Inso me caves,concentrationsexceeding100ppmvhavebeenreported(e.g.,Hosee tal., 2000).ItisrecommendedthatcaveairbemonitoredforH 2 Sandoxygen,aswellas othergases(CH 4 ,CO)usingamultigasmonitor(e.g.,PhDUltraAtmospheric Monitor,Biosystems,Middleton,CT)atalltimeswhileworkinginactives ulfidic caves.AlthoughtheconcentrationofH 2 SmaybelessthanboththeOSHAand NIOSHshorttermexposurelimit(STEL)of10ppmvfor10min,acuteirritati onis possible.Level-Crespiratoryprotection,suchasahalf-faceair-purif yinggasmask withorganic/acidvaporcartridges(H 2 Sescape),shouldalsobeworn.Suchmasks areeffectiveforSO 2 ,organosulfurgases,andradon,buthaveonlyshortterm protectionagainsthighH 2 S.Athighlevels,afull-facemaskshouldbeusedto protecttheeyesandfacialmucousmembranes.Cartridgesshouldbechange d regularlywhenworkinginsulfidicconditions.H 2 Sgasnegativelyaffectsthe sensitivityofoxygensensors,andanyairmonitoringdeviceshouldbeche cked periodically.Ambientaircontainsapprox.20.8%oxygen;undernocircum stances shouldanyoneenteracaveorpassagewhenoxygenconcentrationsare 19.5% unlesstheyhavesuppliedoxygenavailabletothem.AccordingtoOSHA,phy sical workatoxygenlevels 19.5%,evenwithnotoxicgases,isimpairedduetoreduced coordination,dizziness,irritability,andpossiblypoorcirculation. Atoxygenlevels 10%,vomiting,mentalfailure,andunconsciousnessoccur.Concentratio ns 6% for8mincancauserespiratoryfailureanddeath. Figure1.Approximatelocationsforsulfidiccavesandkarstaquifersrep ortedintheliterature.Someofthesitesarediscussed indetailherein. A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 189

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sulfatereductioniscommonlyassociatedwithpetroleum reservoirs,andbasinalbrinesolutionsnaturallyassociated withpetroleumoftenhavehighconcentrationsofH 2 S;the gaswillmigrateupdipfromreservoirsanddissolveinto groundwater.Stablesulfurisotoperatioanalysishas establishedthatthesourceofsulfideformanycaveand aquifersystemscanbeattributedtomicrobialsulfate reduction(e.g.,Ryeetal.,1981;Stoesselletal.,1993;Hill, 1996).Whenkarstisproximaltovolcanicterranes, volcanismgivesoffH 2 Sandothergases.Groundwater dischargingasgeysers,hotsprings,orunderwatervents willoftenhavehighdissolvedsulfidecontent.For example,thesourceofH 2 Sandothergaseswasevaluated byanalyzingtheN 2 /HeandHe/ArcontentandHe isotopesofthespringsdischargingintoCuevadeVilla Luz(alsoknownasCuevadelasSardinas),Mexico (Spildeetal.,2004).Thedissolvedgaseswerefoundto haveanuppermantleoriginthatcouldberelatedtoEl Chicho nvolcano 50kmtothewestofthecavesystem (Spildeetal.,2004). M ICROBIAL D IVERSITYWITHINTHE S ULFUR C YCLE Someoftheearliestmicrobiologicalresearchregarding chemolithoautotrophicmetabolismwasdoneinthelate 1880swithsulfurbacteriafromsulfidicsprings(e.g., Winogradsky,1887).Muchlater,themicrobiologyof sulfidiccaveswasobservationalandpredominatelyinvolvedmicroscopyandculturing(e.g.,Caumartin,1963; SymkandDrzal,1964;Hubbardetal.,1986,1990; ThompsonandOlson,1988;Grubbs,1991;Stoessellet al.,1993;Brigmonetal.,1994;SasowskyandPalmer,1994; Mattisonetal.,1998;Ulrichetal.,1998;Humphreys,1999; Latellaetal.,1999b).Becausecellmorphologydoesnot accuratelydeterminespeciesidentity,andbecausemost microbesinnaturehavenotbeengrowninlaboratory cultures,especiallyautotrophs(ithasbeenestimatedthat 1%ofknownmicrobesareculturable;Amannetal., 1995),researchershaveturnedtogeneticstudies(cultureindependentmethods;Amannetal.,1990;Amannetal., 1995)involvingthecharacterizationandcomparisonof (predominately)16SrRNAgenesequencesandtheir evolutionaryrelationships.Recently,Barton(2006)summarizedsomeculture-independentgeneticmethodsthat havebeenusedtodescribemicrobesfromcaves.Moreover, tounderstandthemicrobialmetabolicpathwaysandthe consequencesofmicrobialmetabolismonecosystem function,stableandradiolabelledisotoperatioanalyses ofthehabitat(water,rocks,air,etc.)andthemicrobial biomasshavebeendone(e.g.,Langeckeretal.,1996;Sarbu etal.,1996;Airoldietal.,1997;Pohlmanetal.,1997; Humphreys,1999;Porter,1999;Vlasceanuetal.,2000; Engeletal.2004a;Hutchensetal.2004). Theuseofgeneticmethodshassignificantlyexpandedour knowledgeofthemicrobialdiversityinactivesulfidiccave andkarstsystems(Vlasceanuetal.,1997;Angertetal.,1998; Vlasceanuetal.,2000;Engeletal.,2001;Holmesetal.,2001; Brigmonetal.,2003;Engeletal.,2003a;Engeletal.,2004a; Hutchensetal.,2004;BartonandLuiszer,2005;Herbertet al.,2005;Meisingeretal.,2005;Macaladyetal.,2006). Evaluationof16SrRNAgenesequencesretrievedfrom microbialmatsfromactivesulfidickarstsystemsreveal adiverserangeofmicroorganisms.Available16SrRNAgene sequenceswerecompiledfromvarioussourcesandpublic databases(e.g.,GenBank http://www.ncbi.nih.gov/ );this fileconsistsof345partialandfull-lengthsequences(as ofMay2006)andisprovidedassupplementaldatafor futureanalyticalwork http://geol.lsu.edu/Faculty/Engel/ geomicrobiology_publications.htm .Asimplecomparison oftheavailablesequencesindicatesthatmembersofthe Bacteriodetes/Chlorobi and Proteobacteria phyla,andespeciallybacteriaassociatedwiththegammaandepsilonproteobacterialclasses,havebeenidentifiedfromallofthe studied,activesulfidiccaves(Table1).Itisnoted,however, thatnoneofthecaveshavebeenexhaustivelysampledto verifythatamicrobialgroupistrulyabsentfroman ecosystem.Moreover,thesimpleretrievalofgenesequences fromaparticularhabitatdoesnotnecessarilymeanthatthose microbesareactiveinacommunity.Similarly,metabolic functionofunculturedmicroorganismsisonlycautiously assumedfromclosegeneticaffiliationtoculturedorganisms. Toplacethemicroorganismsthathavebeenidentified fromsulfidiccavesandkarstsystemsintothecontextof thesulfurcycle,anoverviewofthemetabolicdiversityof organismsfollows.Itisnotmyintentiontoexhaustively covereachsulfurcycletransformationpathwayhereand thereaderisguidedtoexcellentrecentreviewsformore information(e.g.,Amendetal.,2004;Brimblecombe, 2005;Canfieldetal.,2005;Megonigaletal.,2005). Figure2illustratesthesulfurcycleinthecontextofother elementalcycles,includingthecarbon,nitrogen,and oxygencycles. S ULFUR O XIDATION Despitethefactthathighconcentrationsofreduced sulfurcompounds,likeH 2 Sgasorelementalsulfur(S 0 ),are toxictomostorganisms(e.g.,Someroetal.1989; Megonigaletal.,2005),thesecompoundsserveaselectron donorsformicrobialmetabolism,suchasinH 2 Soxidation. O 2 istheelectronacceptorinthisreaction: H 2 S 2O 2 < SO 2 4 2H 3 Forthepurposesofthisreview,anymicrobecapableof oxidizinganyreducedsulfurcompoundwillbegenerally referredtoasasulfur-oxidizer.Foravastmajorityofthe sulfur-oxidizingmicrobes,sulfateistheendproduct(e.g., Canfieldetal.2005).Forothers,intermediateproducts mayform,likesulfite(SO 3 2 ),thiosulfate(S 2 O 3 2 ) (Equation4),tetrathionate(S 4 O 6 2 ),andS 0 asintra-or O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 190 N JournalofCaveandKarstStudies, April2007

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extra-cellularsulfurglobules(Equation5);theseintermediatescanbefurtheroxidizedtosulfate(Equations4 and6)(Fig.2): S 2 O 2 3 H 2 O 2O 2 < 2SO 2 4 2H 4 HS 1 2 O 2 H < S 0 H 2 O 5 4S 0 6O 2 4H 2 O < 4SO 2 4 8H 6 Becauseofthelargecellsizeandfilamentousnatureof somespecies(Fig.3A),sulfur-oxidizingbacteriacanbe readilyobservedinconspicuousandsometimesextensive microbialmatsthateitherattachtosubstrataorfloatinthe watercolumninsulfidiccavestreams(Fig.3B),inkarst aquifers(Fig.3C),orinanchialinecaveandstratified cenotesystems(water-filledsinkholes)(Fig.3D,inthiscase showingnon-whitemats)(e.g.,Hubbardetal.,1986,1990; OlsonandThompson,1988;ThompsonandOlson,1988; Grubbs,1991;Brigmonetal.,1994;Sarbuetal.,1996; Airoldietal.,1997;Vlasceanuetal.,1997;Angertetal., 1998;Mattisonetal.,1998;Humphreys,1999;Hoseetal., 2000;Sarbuetal.,2000;Garyetal.,2002;Engeletal. 2003a;GarmanandGarey,2005;BartonandLuiszer,2005; Macaladyetal.,2006;Randall,2006).Manyofthespecies fromthealpha-( a ),beta-( b ),gamma-( c ),and epsilonproteobacterial( e )classesfoundinmicrobialmats fromcavesareassociatedwithsulfuroxidation.Although some Archaea havebeenidentified(e.g., Thermoplasma acidophilum fromtheGlenwoodHotPoolSpring,Colorado;BartonandLuiszer,2005), Archaea capableofoxidizing reducedsulfurcompounds(e.g.,Canfieldetal.,2005)have notbeenfoundfromsulfidiccavestodate. Table1.Majoraffiliationsformicrobialcommunitiesfoundinsulfidicc aveorkarstsystems. MajorTaxonomicAffiliation Movile Cave (Romania) a Frasassi Caves (Italy) b LowerKane Cave (Wyoming) c ParkerÂ’s Cave (Kentucky) d BigSulphur Cave (Kentucky) e Cesspool Cave (Virginia) f Glenwood Springs (Colorado) g Bacteria Acidobacteria NNN Actinobacteria NN Bacteroidetes/Chlorobi NNNNNNN Chloroflexi NNN Deferribacteres N Fibrobacter N Firmicutes/lowG C NNNN Flexistipes N Nitrospirae NNN Proteobacteria N Alphaproteobacteria NN Betaproteobacteria NNNNN Deltaproteobacteria NNNNN Gammaproteobacteria NNNNNNN Epsilonproteobacteria NNNNNNN Planctomycetes NNN Spirochaetes N TermiteGut1 N Verrucomicrobium NNN CandidateDivisions NNNNN Archaea Euryarchaeota Thermoplasmata N Methanomicrobia NNN Fungi NN a 16SrRNAgenesequencesfromVlasceanuetal.(1997),Vlasceanu(1999),Hu tchensetal.(2004),andEngelandPorter(unpublisheddata). b 16SrRNAgenesequencesfromVlasecanuetal.(2000)andMacaladyetal.(20 06). c 16SrRNAgenesequencesfromEngeletal.(2003a),Engeletal.(2004a),and Meisingeretal.(2005). d 16SrRNAgenesequencesfromAngertetal.(1998). e 16SrRNAgenesequencesfromEngelandPorter(unpublisheddata). f 16SrRNAgenesequencesfromEngeletal.(2001)andEngelandPorter(unpub lisheddata). g 16SrRNAgenesequencesfromBartonandLuizer(2005),andEngelandPorter (unpublisheddata). A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 191

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Recentresearchdemonstratesthatsulfur-oxidizing bacterialcommunitiesincavemicrobialmatsdependon relativelystableO 2 concentrationsandavailability(Engelet al.,2004a),althoughsomespeciescantolerate,andmay evenprefer,extremelylowconcentrationsofO 2 ( 1mgL 1 dissolvedO 2 )forprolongedperiodsoftime(e.g.,Takaiet al.,2003).IftheconcentrationofO 2 istoolowforgrowth, nitratecanbeusedasanelectronacceptor(e.g.,Sayamaet al.,2005);dependingonthemetabolicpathway,eitherN 2 (Equation7)orammonium(NH 4 )canform(Equation8): 5H 2 S 8NO 3 < 5SO 2 4 4N 2 4H 2 O 2H 7 H 2 S NO 3 H 2 O < SO 2 4 NH 4 8 Somemicrobes,suchas Beggiatoa spp.,formS 0 fromthe oxidationofH 2 Swithnitrate(Equation9),whichcanbe furtheroxidizedwithnitrate(Equation10)(e.g.,Sayamaet al.,2005): 4H 2 S NO 2 3 2H < 4S 0 NH 4 3H 2 O 9 3NO 3 4S 0 7H 2 O < 3NH 4 SO 2 4 2H 10 Becausemanyfreshwatersystemsarenitrogen-limited,the nitrate-reducingsulfur-oxidizingbacteria(NRSOB)generatenitrogencompoundsthatotherorganismsinthe ecosystemcanuse(e.g.,NH 4 ),therebylinkingthesulfur cycletothenitrogencycle(Fig.2).NRSOBhavebeen identifiedfromseveralcaveandkarstaquifers(e.g., LawrenceandFoster,1986;Mattisonetal.,1998),and theseorganismsmayextendthedepthstowhichsulfur,and consequentlycarbonandnitrogen,arecycledinoxygendepletedwatersofsulfidickarstaquifers(Engeletal., 2004b). Thepresenceof e proteobacteria inallofthesulfidic cavesstudiedthusfarisexciting.Arecentstudyof e proteobacteria byCampbelletal.(2006),usingalarge datasetofgeographic,genetic,andecologicalinformation, revealsthatmembersofthisclassarenotonlyinsulfidic caves,butalsonumerousothersulfur-richhabitats, includingmarinewatersandsediments,deep-seahydrothermal-ventsitesandvent-associatedanimals,groundwaterassociatedwithoilfields,andfromterrestrialand marinesulfidicsprings.Thebeststudiedterrestrialsystem where e proteobacteria havebeendescribedisLowerKane Cave(Campbelletal.,2006).Quantificationofdifferent microbialgroupsusinggeneticapproachesrevealsthatup to100%ofsomesamplesiscomprisedof e proteobacteria makingLowerKaneCavethefirstnon-marinenatural systemknowntobedrivenbytheactivityoffilamentous e proteobacteria (Engeletal.,2003a).Themajorityofthe16S rRNAsequencescouldbeassignedtotwolineagesdistinct atthegenuslevel,LKCgroupIandLKCgroupII(Engel etal.,2003a;Engeletal.,2004a),andLKCgroupIIwas foundtobepredominatelyresponsibleforsulfuricacid Figure2.Schematicofintegratedbiogeochemicalcyclinginmicrobialec osystemsrelatedtothesulfur,oxygen,carbon,and nitrogenelementalcycles. O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 192 N JournalofCaveandKarstStudies, April2007

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dissolutionofthecavehostlimestone(Engeletal.,2004b). Certain e -proteobacterialgroupscorrelatedtohighdissolvedsulfideandlowdissolvedO 2 contentinthecave streams,suggestingthatsomespeciespreferdifferent geochemicalconditions(Engeletal.,2004a). AnotherdiversegroupofmicrobesthatuseH 2 S(orH 2 ) asanelectrondonorduringanoxygenicphotosynthesis includesthepurplesulfurbacteria(e.g., Chromatium Thiocapsa Ectothiorhodospira ),thepurplenonsulfurbacteria(e.g., Rhodobacter ),thegreensulfurbacteria(e.g., Chlorobium Pelodictyon ),thegreennonsulfurbacteria ( Chloroflexus Oscillochloris ),andthe Heliobacteria (e.g., Brimblecombe,2005;Canfieldetal.2005).Someofthe speciesoxidizereducedsulfurcompletelytosulfate (Equation11),whileothersformintermediatesulfur compounds(Equation12),whereCH 2 Orepresentsorganic carboncompoundsmadeduringphotosyntheticCO 2 fixation: 3CO 2 H 2 S 2H 2 O < 2CH 2 O SO 2 4 2H 11 CO 2 2H 2 S < CH 2 O H 2 O 2S 0 12 Theseorganismshavebeenfoundinsulfidicsprings(e.g., Elshahedetal.,2003;BartonandLuiszer,2005)and cenotes(e.g.,Stoesselletal.,1993;Humphreys,1999;Gary etal.,2002;Herbertetal.,2005)(Fig.3D),andarelikelyto besignificantcontributorstoecosystemsulfurandcarbon cyclinginthosehabitats.Becauseoftheneedto photosynthesize,thesegroupsshouldnotbefoundin Figure3.(A)Filamentousandrod-shapedmicrobialcellsofsulfur-oxidi zingbacteria.Arrow,sulfurglobules.Scaleis10 microns.(B)Whitemicrobialmatinsulfidicstream,LowerKaneCave,Wyom ing.(C)Arrowspointingtowhitefilaments suspendedinsulfidicwaterofanopen-holewellintheEdwardsAquifer.Fi eldofviewis 6inches.Numberatupperleftrefers towelldepthinfeet(183.5m)fromthesurface(imagedigitallycapturedf romvideoprovidedbytheEdwardsAquifer Authority,SanAntonio,Texas).(D)Biofilmofpurplesulfurbacteriacov eringcarbonaterockinLaPilitacenote,ofthe SistemaZacato n,Mexico. A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 193

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completedarkness;however, Chloroflexus spp.havebeen describedfromLowerKaneCave(Meisingeretal.,2005) andtheFrasassiCaves(GrottaGrandedelVento-Grotta deFiume-GrottaSulfurea),Italy(Macaladyetal.,2006) (Table1),andmaybepresentinCuevadeVillaLuz (CuevadelasSardinas),Mexico(Hoseetal.,2000).Itis suspectedthatthesespeciesmaybeabletogrowinthe darkusingalternativepathwaysforenergyandcarbon fixation(e.g.,Canfieldetal.,2005). Generally,abioticconditionsinfluencethetypesof organismsthatahabitatcansupport.MostsulfuroxidizersrequireneutralpHconditionstobuffermetabolic acidity(Ulrichetal.,1998;Brimblecombe,2005),andthe bufferingcapacityofdissolvingcarbonatesmaybeone reasonwhysulfur-oxidizersareprevalentinkarst.Yet, somesulfur-oxidizers(e.g., Acidothiobacillus )thriveinlow pHenvironmentsasacidophiles(acid-lovers).Inactive sulfidiccaves,suchasinCuevadeVillaLuz,extremelylow pHhabitatshavebeendescribed,especiallyonsubaerial cave-wallsurfaces.Biofilmsonsubaerial,cave-wallsurfaces(alsodescribedassnottites,mucotites,microbial draperies,orcave-wallbiofilmsbydifferentinvestigators overtheyears)havebeendescribedfromactivesulfidic cavesandmines(Johnson,1998;Vlasceanuetal.,2000; Engeletal.,2001;Engeletal.,2003b).InCuevadeVilla Luz,forexample,measuredcave-wallpHassociatedwith ‘snottites’was0(Hoseetal.,2000).Culture-dependentand culture-independentstudiesrevealeddiversepopulationsof Thiobacillus,Sulfobacillus Acidimicrobium ,andother groups,suchasthe Firmicutes (Hoseetal.,2000;Vlasceanu etal.,2000;Engeletal.,2001;Engeletal.,2003b). S ULFATE R EDUCTIONAND S ULFUR D ISPROPORTIONATION Reducedsulfurcompoundsoriginatefromseveral sources,includingabioticprocesses(e.g.,volcanism),the degradationoforganics(e.g.,proteins),ordissimilatory sulfatereductionwherebyoxidizedcompounds(e.g., SO 4 2 )serveaselectronacceptorsunderanaerobic conditions;elementalsulfurcanalsobereducedtoH 2 S (Fig.2).Sulfate(orS 0 )canbereducedusingH 2 asthe electrondonor(Equation13)orusingorganiccompounds, suchasacetate(Equation14)orlactate(although numerousorganiccompoundscanbeused): 4H 2 SO 2 4 H < 4H 2 O HS 13 CH 3 COO SO 2 4 < 2HCO 3 H 2 S 14 Theutilizationoforganiccompoundsbysulfate-reducers, eitherascompleteoxidation(e.g.,acetate)toCO 2 orthe incompleteoxidationofothercompounds,againlinksthe sulfurandcarboncycles. Molecularinvestigationsofsomesulfidicaquifers, includingthoseassociatedwithoilfields,havedocumented sulfate-reducers(Voordouwetal.,1996;Ulrichetal., 1998);thusfar,studiesidentifyingtheseorganismsinactive sulfidiccaveshavebeenlimitedtoLowerKaneCaveand theFrasassiCaves(Engeletal.,2004a;Meisingeretal., 2005;Macaladyetal.,2006).Ageneticallyvariedgroupof microbesareknowntocarryoutdissimilatorysulfate reduction,butthesulfate-reducersthathavebeenfoundin sulfidickarstsystemspredominatelyfallwithinthe d proteobacteria class(Table1).Theothergroupsof sulfate-reducersgrowat70to105 u C(Brimblecombe, 2005;Canfieldetal.,2005),wellabovethetemperaturesof currentlyexplored,activesulfidiccaveanddeepaquifer systems. Anotherrecentlyrecognized,environmentallysignificantsulfurtransformationpathwayisdisproportionation (e.g.,Brimblecombe,2005;Canfieldetal.,2005).During disproportionation,intermediatesulfurcompoundsthat wereproducedduringincompleteoxidation,suchasS 0 or S 2 O 3 2 (Equation15),formbothreducedandoxidized formsofsulfur(Fig.2): S 2 O 2 3 H 2 O < H 2 S 3SO 2 4 15 Severalgroupsofmicrobesdisproportionatesulfurcompounds,includinganoxygenicphototrophs,somesulfatereducers(e.g., Desulfovibrio and Desulfobulbus spp.),and sulfate-reducingbacteriathatperformsulfurdisproportionationastheirsolemetabolism(e.g., Desulfocapsa spp.). Ingeneral,characterizationofsulfate-andS 0 -reducingor sulfur-disproportionatingmicrobesfromsulfidiccavesand aquifershasnotbeenthoroughlydone,although Desulfocapsathiozymoxenes hasbeenfoundinLowerKaneCave andtheFrasassiCaves(Engeletal.,2004a;Meisingeret al.,2005;Macaladyetal.,2006).WhereO 2 canabiotically oxidizereducedsulfurcompounds,thereductiveand disproportionationpathwaysgeneratesupplementalsulfide thatsulfur-oxidizingbacteriawithinthemicrobialmatscan use(Engeletal.,2004a). F AUNAL I NVENTORIES Thefaunaofcaveandkarstaquiferecosystemshave notbeenexhaustivelysamplednorcharacterized(i.e.large, conspicuousanimalsareeasytoseeanddescribe),and obligatecavefaunahavebeeninadequatelyidentified(e.g., Culveretal.,2004).Similarly,microscopiceukaryotes(e.g., fungi,molds,protozoa)andmicro-invertebrates(e.g., copepods)arealmostvirtuallyunknownformostsubterraneansystems,despitetheextensiveworkdoneon microbesinvolvedinsulfurcyclinganddescriptionsofthe chemolithoautotrophicmicrobialcommunities(seeprevioussectionoftext)(e.g.,Angertetal.,1998;Engeletal., 2004a;Hutchensetal.,2004;BartonandLuiszer,2005; Macaladyetal.,2006)(Table1).Nevertheless,Culverand Sket(2000)illustratethatsomeofthemostbiologically diversekarstecosystems(basedonthenumbersofspecies, exclusively)areassociatedwithsulfidicwaters,especially O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 194 N JournalofCaveandKarstStudies, April2007

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whenconsideringsystemswithahighnumberofendemic populations.SuchsystemsincludetheMovileCave,the EdwardsAquiferinTexas,andtheanchialineWashinghamCavesinBermuda.Mostnotableontheirlististhe chemolithoautotrophically-basedecosystemoftheMovile Cave,with30terrestrialspecies(24arecave-adaptedand endemic)and18aquaticspecies(9cave-adaptedand endemic)(Sarbuetal.,1996;CulverandSket,2000). However,notallsulfidiccavesoraquifersareknownfor highspeciesnumbers,asisthecaseforLowerKaneCave withonlyfouridentifiedspecies(Porter,unpublisheddata) (Table2).Partofthisdifferenceinthenumberofhigher trophiclevelspeciesinsulfidiccaveandkarstsystemsmay beattributedtotheinvasionhistoryofanimalsinthe region(e.g.,ChristmanandCulver,2001)andtheageof thesystem,asLowerKaneCaveislikelytobequiteyoung geologically(e.g.,Stocketal.,2006)comparedtotheother caves(e.g.,Longley,1986;Oettingetal.,1996;Engel,1997; GroscehenandBuszka,1997;Sarbuetal.,2000). Forthepurposeofthisreview,theknownfaunal inventoriesforsomesulfidiccavesandkarstaquifers areprovided(Table2);thecompiledlistsofspecies numbers(availableat http://geol.lsu.edu/Faculty/Engel/ geomicrobiology_publications.htm )resultfromcombing throughtheliterature,theWorldWideWeb( http:// www.karstwaters.org/kwidata.htm ),andbypersonally contactingindividualresearchgroups.Tomyknowledge, nosummarylikethishasbeenpreviouslyassembledfor sulfidiccaveandkarstaquifersystems.Anoteofcaution: theselistsarenotinclusiveandtheylikelycontainerrors becausetheywerecompiledfrommanydifferent,including previouslyunpublished,sources.Althoughthebiodiversity ofsomesubmarinecaveshasbeenstudied(e.g.,Grotta Azzura;Mattisonetal.,1998),thefocusofthenextsection islimitedtocontinentalsystems. Inshort,samplingcavesistrickywork,butsampling sulfidiccavesisdefinitelymorecomplicated(seefootnote 1).Similarly,samplinggroundwatercanalsobedifficult (e.g.,GhiorseandWilson,1988;Krumholz,2000). Therefore,samplingbiasesmayhavecausedtheincomplete andinaccuratepictureofspeciesrichnessanddistribution forsulfidicsystems(e.g.,Culveretal.,2004;Schneiderand Culver,2004;vanBeynenandTownsend,2005).Certainly, thenoveltyoftheMovileCaveecosystemmayhave promptedtheyearsofinvestigations(e.g.,Plesa,1989; Sarbu,1990;GeorgescuandSarbu,1992;Decuand Georgescu,1994;Decuetal.,1994;Georgescu,1994; PoinarandSarbu,1994;WeissandSarbu,1994;Sarbuet al.,1996;Vlasceanuetal.,1997;Manolelietal.,1998; Porter,1999;Vlasceanu,1999;Hutchensetal.,2004). Moreover,insomefaunaldescriptions,organismswere onlycharacterizedtothefamilyororderlevels,andsome genus-andspecies-levelidentificationshavechangedover theyearsduetomoredetailedsystematicsandmolecular phylogenetics.Futureworkshouldconcentrateoncompletingandverifyingthelistbecausetheseissuesobviously inhibitathoroughstatisticalcomparisonofsulfidickarstsystembiodiversityandpresentlyhinderanyevaluationof thepossibleeconomicvalueofthesesystems(e.g.,Fromm, 2000;GibertandDeharveng,2002;vanBeynenand Townsend,2005). M ICROSCOPIC E UKARYOTES Thediversityofthemicrobialeukaryotes(e.g.,fungi, protists,etc.)insulfidiccaveandkarstaquifershasbeen poorlymeasured,despitetheimportanceoftheseorganismstoecosystemfunction.Severalfungalgroupshave sulfur-basedmetabolism,likesulfurgasesconsumption andproduction,andfungialsoplayaroleinconcrete corrosionassociatedwithmethanethiol(CH 3 SH)consumption.Thesestudiessuggestthatfungimaybean overlookedpartofthesulfurcycleinthesesystems,and maybeimportanttolimestonedissolution(e.g.,Burfordet al.,2003).Fungi,ciliatedprotozoa,androtifershavebeen describedfromthesulfidicwatersinGrottadiFiume Coperto,Italy(Latellaetal.,1999a;Maggietal.,2002) (Tables1and2).NotshowninTable2,however,arethe resultsfromasurveyfromtheSulphurRiverpassageof ParkerÂ’sCave,Kentucky,whichidentified13generaof protozoa(fromeightorders),includingspeciescommonto sulfidichabitatsandassociatedwithgrazing(Thompson andOlson,1988).Fungiandrotifers(alsounclassified) havebeenreportedfromMovileCave(Sarbu,1990). I NVERTEBRATES PhylumPlatyhelminthes Althoughthediversityoftheflatwormsishighinnonsulfidicsubterraneansettings,only Dendrocoelum sp.has beenreportedfromMovileCave(Sarbu,1990).Flatworms havealsobeenobservedinLowerKaneCaveandCueva deVillaLuz,butnoidentificationwasdone. PhylumNematoda Severalnewspeciesofstygobiticnematodeshavebeen describedfromsulfidickarstaquifers(e.g.,Moravecand Huffman,1988;PoinarandSarbu,1994).Although Chronogastertroglodytes sp.n.fromMovileCaveis bacterivorous, Rhabdochonalongleyi sp.n.fromthe EdwardsAquiferwasfoundinfectingtheintestinesofthe twoblindcatfishes, Trogloglanispattersoni Hubbs&Bailey 1947and Sataneurystomus Eigenmann1919(Moravecand Huffman,1988). PhylumAnnelida Thisgroupisrepresentedbyaquaticwormsandleeches, bothofwhichhavebeendescribedfromjusttwosulfidic cavesystems(Table2).Mostnotableis Haemopiscaeca Manoleli,Klemm&Sarbu1994,thecaveleechendemicto MovileCaveandthesurroundingsulfidickarstaquifer (Manolelietal.,1998).Annelidshavebeenreportedfrom theSulphurRiverpassageofParkerÂ’sCave,butnodetails aregiven(ThompsonandOlson,1988).Tubificidworms A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 195

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Table2.Estimatednumberofspeciesreportedforsulfidiccavesandkarst aquifers,includingaccidentals(i.e.surfaceinvaders);batsandsalam andersarenotincludedintheaquaticcounts.*referstoapossibleoccurr ence,butnoformaldescription(the symbolisalsousedifanorigincouldnotbeverified).Notethatsomeorgan ismsarenotlimitedtothesulfidicportionsofthesystems,buthavebeend escribedfromthefreshwatercomponentofacaveoraquifer(e.g.,intheca seoftheFrasassiCaves).For theEdwardsAquifer,however,taxarecordedfromonlythesulfidicpartof thesystemareenumerated.Fullspecieslistscanbefoundat http://geol.lsu.edu/Faculty/Engel/geomicrobiology_publications. htm MovileCave(Romania)FrasssiCave(Italy)GrottadiFiumeCoperto(Italy )CuevadeVillaLuz(Mexico) EdwardsAquifer (Texas)aquatic LowerKaneCave(Wyoming) terrestrialaquaticterrestrialaquaticterrestrialaquaticterrestri alaquaticterrestrialaquatic Oligohymenophorea(ciliateprotozoa) 1 Rotifera 21 Platyhelminthes(flatworms) 1 ** Nematoda(roundworms) 3 1 Annelida Oligochaeta(aquaticworms) 31 Hirudinea(leeches) 11 Mollusca Gastropoda(snails) 1121*11 Archnida Acari(mites,ticks) 11 80 Aranaea(spiders) 553131 Pseudoscorpiones(falsescorpions) 3126 Schizomida(whipscorpions) 1 Scorpiones(scorpions) 1* Crustacea Copepoda(copepods) 33* Ostracoda(ostracods) 1 Amphipoda(amphipods) 211* Isopoda(isopods) 41131* Decapoda(shrimp,crayfish,crabs) 1 Myriapoda Chilopoda(centipedes) 33 Diplopoda(millipedes) 11 Symphyla(gardencentipedes) 1 Hexapoda Ellipura(collembola) 32231 Insecta Coleoptera(beetles) 4236 Diptera(flies) 22*1 Hymenoptera(wasps,ants,bees) 10 Orthoptera(crickets,cockroaches) 2* Lepidoptera(moths,butterflies) 1* Hemiptera(bugs,aphids) 1 Heteroptera(truebugs) 112 Psocoptera(barklice,booklice) 1 Thysanura(silverfish) 2 Vertebrata Osteichthyes(fish) 12 Anguilliformes(eel) ** Totals 27191232310 143 6322 O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 196 N JournalofCaveandKarstStudies, April2007

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havealsobeendescribedfromsedimentsinsulfidiccave streamswheresurfacewatercanback-floodintothecave passages(e.g.,LowerKaneCave),althoughnoformal descriptionshavebeenmade. ClassMollusca Eventhoughnon-sulfidiccavescanbecolonizedby bothterrestrialandaquaticsnails,fewdescriptionsof gastropodsfromsulfidiccavesandaquifersareknown (Table2).Inthecaseoflandsnails,thisismostlikelydue tothelackofcommunicationwiththesurfacewhereby snailscanbewashedintoacave.Describedaquaticsnails includetheendemicprosobranchsnail, Heleobiadobrogica Bernasconi1991,fromMovileCave(Bernasconi,1997), populationsof Islamia spp.inthesulfidicstreamportions oftheGrottadiFiumeCopertoandtheFrasassiCaves (Latellaetal.,1999a;Sarbuetal.,2000;Maggietal.,2002), andtheendemicsnail Physella (formerly Physa ) spelunca Turner&Clench1974fromthesulfidicstreamsinLower KaneCave(Porteretal.,2002;WethingtonandGuralnick, 2004).Asisterspecies, Physellajohnsoni Clench1926,has alsobeenreportedfromsulfidicsprings(oneinacave)on SulphurMountaininBanffNationalPark,Canada (Lepitzki,2002;WethingtonandGuralnick,2004).The P.spelunca populationinLowerKaneCaveistremendous, withanestimated6,800individualspersquaremeter (Porteretal.,2002). P.spelunca wasoriginallydescribedas beingtroglomorphic(i.e.pigmentless,noeyes),but observationsindicatedtherewereatleasttwoothercolor morphs(redandblack)althoughgeneticvariationfromthe cavepopulationshasnotbeenidentifiedtodate(Porteret al.,2002).Twospeciesofsnails,withhighpopulation densities,havebeenobserved,butnotyetdescribed,from CuevadeVillaLuz(K.Lavoie,personalcommunication). ClassArachnida Becausemanyofthesulfidiccavesareinpoor communicationwiththesurface,thecolonizationofthese cavesbyarachnids(e.g.,mites,spiders,scorpions)hasbeen limited,exceptinthecaseofsystemswithmanyentrances orwithlargebatpopulations.Thesehavehigharachnid diversity(Table2).Mostnotablearethenumbersof differentarachnidspeciesreportedfromCuevadeVilla Luz,andthe 80speciesofacarians,representingfive orders.Themicroarthropodshavebeenthesubjectof extensiveresearchbyonegroupandofseveralMasters theses(Palacios-Vargasetal.,1998;Palacios-Vargasetal., 2001;Estrada,2005;Pastrana,2006);theaccountofthe arachnidsinthisonecaveislikelyduetothatconcentrated effort.Moreover,sevenspeciesofbatsrepresentingthree differentfamilieshavebeendescribedfromCuevadeVilla Luz,andmostofthemicroarthropodswerefound associatedwithbatguanoorsurface-derivedmaterial proximaltocaveentrances(Palacios-VargasandEstrada, personalcommunication).Severalacarians( Sejus sp., Gamasellodes sp., Protolaelaps sp.)arefoundnearthe sulfidiccavestreamandthemicrobialmats(PalaciosVargasandEstrada,personalcommunication).Two possiblynewspeciesofmites, Dactyloscirus sp.and Neoscirula sp.(Cunaxidaefamily),havebeenfoundnear themicrobialmatsinthesulfidicwaterofCuevadeVilla Luz(EstradaandMej a-Recamier,2005).Undescribed acarianshavealsobeenreportedfromtheSulphurRiver passageofParkerÂ’sCave(ThompsonandOlson,1988). TroglobiticspidershavebeendescribedfrombothMovile Cave(fivespecies,eachrepresentingtheirownorder)and theFrasassiCaves(twospeciesfromoneorder)(e.g., GeorgescuandSarbu,1992;Georgescu,1994;Weissand Sarbu,1994;Sarbuetal.,2000). Nesticus spp.havebeen reportedfromacidiccavewallsinbothofthesecaves,and spiderwebscommonlyhavelowpHdropletshangingfrom them.Dropsalsoformonwebsfromthelinyphiidspider, Phanettasubterranea Emerton1875,intheSulphurRiver passageinParkerÂ’sCave(ThompsonandOlson,1988). SubphylumCrustacea Muchlikethemicrobialeukaryotes,micro-invertebrateshavebeenpoorlystudiedfromsulfidiccavesand karstaquifers.Severalspeciesofcopepodsandostracods havebeendescribedfromonlytwocaves(Table2).Movile Cavehostsanendemiccopepodandostracod(Plesa,1989). Additionally,withintheOrderAmphipodatherearefew describedspeciesfromsulfidiccavesoraquifers(Table2); however,giventheprevalenceanddiversityofamphipods innon-sulfidiccavesglobally(e.g.,CulverandSket,2000; GibertandDeharveng,2002),andtheirmetabolicflexibilityandhightoleranceofhypoxia(e.g.,Macneiletal.,1997; Hervantetal.,1999a;Hervantetal.,1999b;Kellyetal., 2002;Lefe bureetal.,2006),itissurprisingthatmore amphipodshavenotbeenidentified.Afewstygobitic isopodshavebeencharacterizedfromsulfidicsystems, althoughcomparativelymoretroglobiticisopodshavebeen described(Table2). Onehabitatthathashighpotentialforcrustaceansis sulfidicgroundwater(despitethefactthatevenfresh groundwaterhasnotbeenadequatelysampled).Longley (1981)assertedthattheEdwardsAquiferinCentralTexas hadthepotentialtobethemostdiversesubterranean biologicalcommunityonearth,althoughlittleworkhas beendonetoverifytheproclamation.Thesulfidic(badwater)portion(Ryeetal.,1981;Oettingetal.1996;Ewing, 2000)oftheaquiferhasbeenvirtuallyunexploredbiologicallyandhasthepotentialtohostauniquefauna(see descriptionbelowoftheOsteichthyes),includingmicrobes (e.g.,Grubbs,1991).Thenon-fungalmicrobiologyhas recentlybeendescribedforaportionofthesulfidicaquifer intheSanAntonioarea(Randall,2006;Engel,unpublisheddata).Overall, 91speciesorsubspeciesof animalshavebeendescribedfromtheentireEdwards Aquifer,including44endemicstygobites(Oursoand Horning,2000).OnesampledartesianwellinSanMarcos, Texas,reportedlyhas 10speciesofamphipods,from A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 197

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numerousfamilies(Holsinger,1980).Severaldescriptions ofstygobiticamphipodsindicatethatsomespecies,suchas Artesiasubterranea Holsinger1980,wereretrievedfrom warmmineralwaterfromartesianwells(Holsinger,1966, 1980),whichmaybetakentomeanthatthespecieswas retrievedfromasulfidicwell.Thisphenomenalcrustacean diversitydeservesattention,andverificationisneededif anyofthesespeciesarelivinginthesulfidicportionofthe aquifer. SuperclassHexapoda Thetypesofhexapodsdescribedfromsulfidiccaveand karstsystemsincludecollembolansandinsects,andthe groupisdominatedbyterrestrialspecies(Table2).Among thespeciesdescribed,endemictroglobiteshavebeen reportedfromMovileCave(e.g.,DecuandGeorgescu, 1994)andtheFrasassiCaves(Sarbuetal.,2000). Numeroushexapods,particularlyamongcollembolans andhymenopterans,havebeeninventoriedfromCueva deVillaLuzaspartofthesisresearch(Estrada,2005; Pastrana,2006).Althoughconsideredaterrestrialtaxon, thelarvastageofchironomidmidgeisfoundinhigh abundanceinthesulfidicwatersinCuevadeVillaLuz (LavoieandEvans,2002).Manyhexapodsareconsidered tobegrazersinthecavefoodwebs,predominantly consumingmicrobialbiofilms;somemayalsobeomnivorous.Onenotableheteropteranistheendemic,stygobitic waterscorpion, Nepaanophthalma Decuetal.1994,from MovileCave(Decuetal.,1994); Nepacinerea Linnaeus 1758hasbeenidentifiedfromGrottadiFiumeCoperto (Latellaetal.,1999a). V ERTEBRATES Amongtheorganismsfoundincaves,perhapsthe vertebrateshaveelicitedthemostattention,eventhough manyareaccidentalincaves(frombirdstoskunks).Batsare frequentvisitorstosulfidiccaveswithentrancestothe surface,suchasCuevadeVillaLuzandtheFrasassiCaves (Hoseetal.,2000;Sarbuetal.,2000)(aspecieslistis providedinthesupplementat http://geol.lsu.edu/Faculty/ Engel/geomicrobiology_publications.htm ,butnotin Table2).Forthisreview,onlyaquaticvertebratesare describedindetail. ClassOsteichthyes Twodifferentfamiliesoffisheshavebeendescribed fromsulfidickarstsettings. Poeciliamexicana Steindachner 1863(thecavemolly,familyPoecilidae)isprevalentinthe sulfidicwatersofCuveadeVillaLuzandnearbysulfidic springs(Langeckeretal.,1996;Hoseetal.,2000;Tobleret al.,2006).Thissmallfish,havingreducedeyesizeandpale colorationcomparedtosurface-dwellingpopulations,is thecenterofattentionfortheritualcelebrationofnative villagers(Langeckeretal.,1996;Hoseetal.,2000).For probablyathousandyears,kilogramsoffisharesacrificed annuallyduringtheceremony,butthepopulationappears toberobust(Tobleretal.,2006).Thesourcesoffoodfor thefishareconsideredtobemicrobialmatsand chironomidlarvae(Langeckeretal.,1996;Lavoieand Evans,2002). ThedeepsulfidicwatersoftheEdwardsAquiferhost thetwoendemicblindcatfishes, T.pattersoni and S. eurystomus (bothfromfamilyIctaluridae),whoseorigin hasbeentracedbacktothePlioceneorMiocene (LangeckerandLongley,1993).Bothfishshowremarkable adaptationstothedeepaquifer,havingbeenretrievedfrom over400mwaterdepth,includingthelackofpigment,loss ofeyesandpinealorgans,andthelackoftheswim-bladder (whichistypicalfordeep-seafishes).Eachoftheaquifer speciesalsohasuniquemorphologicalfeaturesthatare attributedtotheirrespectiveecologicalniches. T.pattersoni hasasucker-likemouthdistinctfromanyotherspeciesin thefamilythatissuggestiveofgrazing(Langeckerand Longley,1993),andLongleyandKarnei(1978)report partiallydegradedfungusinthegut.Thecatfishwas probablyfullofsulfur-oxidizingbacteriainsteadoffungus, asthebacteriaformextensivebiofilmsontheaquiferwalls (Grubbs,1991;Randall,2006)(Fig.3C).Incontrast, S. eurystomus hadgutcontentsresemblingstygobites(e.g., amphipods),suggestingthatitwasprobablyapredator (LangeckerandLongley,1993). ClassAnguilliformes Hundredsofwell-preserved,30–70cmlong,adulteel fossils( Anguillaanguilla )havebeenfoundintheFrasassi caves, 5mabovethepresentdaywatertable(Marianiet al.,2004).Isotopiccomparisonsbetweentheeelsandriver andcaveanimalsindicatedthattheeelswerenotendemic tothesulfidiccavewaters,butinsteadtothesurfaceriver. Reconstructed 14 Cageswereconsistenttothecave paleolevels,datingbackasfaras9,000yearsago.Aneel hasbeenreportedfromCuevadeVillaLuz(Hoseetal., 2000),althoughitisunclearwhetheritisendemicor accidental. T HE R OLEOF C HEMOLITHOAUTOTROPHYIN S HAPINGTHE B IODIVERSITYOF S ULFIDIC K ARST E COSYSTEMS Aspreviouslydiscussed,themajorenergyandfood sourcesinmostcaveandkarstaquifersarefrom photosynthetically-producedorganicmatterthatis broughtintothesystemfromthesurfacebyair,water, oranimals.Prolongedperiodsoflimitedtonofoodcan causewidespreadstarvation(e.g.,Hu ¨ppop,2005),which undoubtedlyresultsinstress(seediscussionbelow) (Howarth,1993).Accordingly,individualswhoarestressed mayexpendgreaterenergyforsurvivalandwouldrequire morefoodinordertocopewithhabitat-inducedpressures (e.g.,Howarth,1993;Hu ¨ppop,2005;Parsons,2005).For sulfidicsystems,oneoftheconsequencesofchemolithoautotrophicprimaryproductivityisanincreaseinthequality andquantityoforganiccarbon(PoulsonandLavoie,2000; O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 198 N JournalofCaveandKarstStudies, April2007

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Engeletal.,2004a).Thisrichandabundantfoodsource mayhaveasignificantimpactonbiodiversityandan organism’sabilitytoendurehabitatstresses. Thecarbontonitrogenratio(C:N)ofmicrobial biomasscanberelatedtofoodquality.Thelowerthe ratio( 3–5),thebetterthequalitybecauseoflimitedinflux andprocessingofsurface-derivedmaterialthatwould increasethenitrogencontentoftheorganicmatter(Engel etal.,2004a).MicrobialbiomassfromMovileCaveand LowerKaneCavehaveC:Nvaluesof 5andare comparabletoperiphytoninsurfacestreamsandbacteria fromdeep-seavents(KinkleandKane,2000;Engeletal., 2004a).Incontrast,highC:Nratiosindicatethatthereis anabundantcarbonsupply,likelyduetostorageof biomass,butareductioninnitrogenavailability. Stableisotoperatioanalyses(SIRA)andradiolabeledcarbonassimilationstudiesconfirmedthatchemolithoautotrophicprimaryproductivitywasprevalentinthe microbialmatsfromvariouscaves(Sarbuetal.,1996; Airoldietal.,1997;Pohlmanetal.,1997;Mattisonetal., 1998;Humphreys,1999;Porter,1999;KinkleandKane, 2000;Sarbuetal.,2000;Vlasceanuetal.,2000;Engeletal., 2004a;Hutchensetal.,2004).Forcarbonisotope systematics,thetwocarbonisotopesofimportanceare 12 Cand 13 C,wherebytheincorporationofcarboninto livingtissuesinvokessignificantkineticisotopefractionation.Specifically,biological(e.g.,enzymatic)processes discriminateforthelighterisotope( 12 C),leavingthe heavierisotope( 13 C)behind.Differencesintheisotopic compositionareexpressedintermsofthedelta( d )notationofaratiooftheheavyversusthelightisotopic valuesforasamplerelativetoastandard,measuredinper mil( % ).Ingeneral,biogeniccarbonisisotopicallylighter (morenegative)thantheinorganicreservoir(e.g.,CO 2 or dissolvedHCO 3 );chemolithoautotrophiccarbonfixation pathwayshavesomeofthelargestfractionationeffects, withresulting d 13 Cvaluesofchemolithoautotroph-dominatedmicrobialbiomassrangingbetween 30and 45 % comparedtosurfaceorganicmatterat 20 % (Fig.4). Variationsinthe d 13 Ccompositionofmicrobialbiomass areduetothetaxonomicgroupspresentanddifferent compositionsofdissolvedinorganiccarbon.Excretion, respiration,andheterotrophiccarboncyclingare(forthe mostpart)considerednegligiblecarbonisotopefractionationprocesses,andtheisotopiccompositionofheterotrophicorganicmatterwillbethesameas,orslightly higherthan,thesourceorganiccarbon(essentially,in SIRA,theyou-are-what-you-eatmottoprevails). Theliteraturedescribingelaboratefoodwebsis extensiveforsurfaceecosystems(e.g.,forests,soils,lakes), butstudiesofchemolithoautotrophically-basedecosystems andthestructureanddynamicsoftheirfoodwebsare fairlylimited(Sarbuetal.,1996;Pohlmanetal.,1997; Vlasceanuetal.,2000;Sarbuetal.,2000).Trophic structureofmostcaveecosystemsischaracterizedbyalack ofpredatorsandextensiveomnivory(GibertandDeharveng,2002).Therehasbeenrelativelylittledonewith regardtoevaluatingthebiogeochemicalandecological rolesofthedominantgroupsinthesulfidicecosystems. ThelimitedSIRAstudiesdosupportthatpredatorsare lackinginsulfidicsystems,althoughitispossiblethatthe predatorsarenotknownorthattheidentifiedspecieshave notpreviouslybeenconsideredpredators(e.g.,amphipods; Kellyetal.,2002).Truepredators(e.g.,spiders)arepresent intheMovileCaveecosystemandthe d 13 Cvaluesforthose organisms( 37to 44 % )demonstratethattheyeat grazers,whointurnhave d 13 Cvaluesconsistentwith consumptionofthemicrobialmats(Fig.4).The d 13 C compositionsofthemicrobialmatssuggestchemolithoautotrophicproductivity,andaredistinctfromsurface organicmatter(Fig.4).Langeckeretal.(1996)explored thefoodwebofCuevadeVillaLuzusingsulfurSIRAand foundthattheanalysescouldonlypartiallydefineenergy flowwithinthefoodweb. Assimilationstudieshavebeendonewithmicrobial biomassfromseveralsulfidiccavesystemsusing 14 Cbicarbonatetoestimatechemolithoautotrophicproductivityand 14 C-leucinetoestimateheterotrophicproductivity (Porter,1999;Engeletal.,2001)(Fig.5).Autotrophicrates Figure4.Stablecarbonandnitrogenisotoperatioanalyses forMovileCave(solidsymbols)theFrasassiCaves(open symbols),andLowerKaneCave(shadedsymbols)from Sarbuetal.(1996),Vlasceanuetal.(2000),andEngeletal. (2004a),respectively.Circlesaremicrobialmatsamplesfrom eachcave;trianglesareforgrazers;crossesareforpredators (onlyMovileCavehaspredators);diamondsaresurface organics.Variationsinthe d 13 Ccompositionofmicrobial biomassforthecavesareduetothetaxonomicgroups present,whichmayhavedistinctcarbonfixationpathways, anddifferentstartingcompositionsofdissolved inorganiccarbon. A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 199

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werehighestfortheMovileCaveandlowestforCesspool Cave,butinallofthecavesexamined,autotrophic productivitywassignificantlygreater(fromonetofive times)thanheterotrophicactivities(Porter,1999;Engelet al.,2001).Similarratesofautotrophicproductivitywere estimatedformicrobialmatsfromthesubmarinecave, GrottaAzzura,atCapePalinuro,Italy(Mattisonetal., 1998).Microbialheterotrophicprocessingofautotrophic biomasswaslow,withheterotrophsprocessingaminor fractionoftheavailableautotrophicproductivity(Porter, 1999;Engeletal.,2001).ForLowerKaneCave,the estimateis 30%oftheautotrophicproductivityis processedthroughheterotrophyinLowerKaneCave, whichcompareswellwithestimatesof 20–40%of autotrophicproductivityprocessingbyheterotrophyfor theopenoceans(Porter,1999). Theconsequencesofarichandabundantfoodsource relatetobiodiversity(asthenumberofspecies),ecosystem function,andfoodwebdynamics.First,nutritionalstress maysimplybenegligiblebecausemembersofthe ecosystemdonotneedtorelyonoutsidefoodorenergy (e.g.,Howarth,1993).Organismsconsumingthechemolithoautotrophically-producedfoodmayalsohaveagreater abilitytoendurehabitatstresses,suchaslowO 2 andhigh H 2 S(seediscussionbelow).Moreover,thelowC:Nratios andlowheterotrophicproductivityindicatethatthereis alimitedmicrobialdetritalloopandthatnutritional qualityofthebiomassishigh.Thesefactorsshould correlatetoahighnumberofgrazersandothertrophic levelsthatcouldbesupportedbymicrobialmatconsumption(Engeletal.,2001).However,oneargumentasserts thatarichandplentifulfoodsourcemayincrease functionalredundancyatvarioustrophiclevels(thereby increasingthetotalnumberofspeciesinanecosystem;e.g., Wohletal.,2004;Hooperetal.,2005),ifthefoodcannot beaccessedbyhightrophiclevels.Anotherargument suggeststhatthestabilityoftheoverallhabitatandtherich foodsourcemaysupportlowerdiversity(Gibertand Deharveng,2002;Wohletal.,2004),especiallyifthereis alimitedinfluxofsurfaceorganismstoreplenishthegene poolortoincreasecompetition(e.g.,BarrandHolsinger, 1985;Hooperetal.,2005).Asisapparentinthepreceding Figure5.(A)Set-upforradiolabelled-isotopeexperimentintheFrasass iCaves,Italy.(B)SamplinginCesspoolCave, Virginia;arrowpointingtomats.(C)Floatingmicrobialmats(arrow)inM ovileCave,Romania.Gridis 10cmonaside.(D) SamplingstreammatsintheFrasassiCaves,Italy;arrowspointingtomats .(E)Comparisonbetweencavemicrobialmatsfor 14 C-bicarbonateand 14 C-leucineincubationstoestimatechemolithoautotrophicprimaryprodu ctivityandheterotrophic productivity,respectively(Porter,1999).Autotrophicproductivityo nlywasestimatedforGrottaAzzura,Italy(ND nodata forleucinetest)(Mattisonetal.,1998). O BSERVATIONSONTHEBIODIVERSITYOFSULFIDICKARSTHABITATS 200 N JournalofCaveandKarstStudies, April2007

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faunalinventories,morethoroughdescriptionsofthe functionalrolesoftheorganismsinsulfidickarstsystems areneededtoaddresstheseargumentsfully. T HE R OLEOF H ABITAT S TRESSIN S ULFIDIC K ARST E COSYSTEMS Subsurfaceenvironmentscanbehighlystressfulhabitatsforlife,withstressdefinedasapotentiallydamaging conditioninthebiologicalsystem(e.g.,Howarth,1993). Theabilityofsubterraneanorganismstotolerate,adapt, andevolveunderstressfulhabitatconditionshasbeenthe subjectofrecentresearch(e.g.,Howarth,1993;Hu ¨ppop, 2005).Formostorganisms,stressavoidanceisprobably thefirstlineofdefense(e.g.,Badyaev,2005;Parsons, 2005).However,obligatetroglobitesandstygobiteshave conspicuousadaptationstosubsurfaceconditions(i.e. darkness,limitedfood,etc.),includingthereductionin andlossofstructures(eyes,pigments,wings,etc.),lossof time-keepingabilities(andcircadianrhythm),slower metabolicrates,andreducedfecundity,butalsothe elongationofappendages,enhancedsensorystructures, etc.Organismslivinginthesulfidicconditionsnotonly manifestsimilarmorphological,behavioral,andphysiologicaladaptationscomparedtonon-sulfidicsubsurface animals,buttheyalsomustdealwithdifferentenvironmentalstresses,suchastoxiclevelsofgaseslikeH 2 S,CO 2 andCH 4 ,andvariablepH. Excludingnutritionalstress,oneofthemostsignificant stressesfororganismslivinginsulfidichabitatsishypoxia (dissolvedO 2 concentrations 2.0mgL 1 )(Hervantetal., 1997;MalardandHervant,1999;HervantandMalard, 2005).Note:thesolubilityofoxygeniscomplicatedby temperature,pressure,elevation,andsalinity,butin generalthesolubilitydecreaseswithincreasingtemperature andsalinity;soinmesothermal( 10 u C)watersthatare commonforcontinentalsulfidicsystems,dissolvedO 2 levelscanbe 0.01mgL 1 ,orconsideredanoxic.Because darknessprecludesphotosynthesis,O 2 isnotproduced in situ ,andabioticandbioticconsumption,particularlyif organiccarbonisplentiful,canrapidlydiminishthe concentrationofO 2 .Moreover,slowtonegligibleair exchangewithgroundwater,orlimitedaircirculationin cavepassages,notonlyresultsinatmosphericstagnation, butalsocausestheaccumulationofnoxiousgases,suchas CO 2 ,CH 4 ,andH 2 S.UtilizationofO 2 asanelectron acceptorformetabolicprocesses(e.g.,throughsulfur oxidationorheterotrophy)wouldalsokeeptheconcentrationofdissolvedO 2 exceedinglylow.Therefore, microbialcommunitiesplayafundamentalroleinmaintaininghabitatphysicochemistry,suchaspossiblycausing andmaintaininghypoxiainsulfidicaquifers. Althoughitseemsthatmicrobescaneasilyandreadily adapttoextremehabitatconditions,andthatchemolithoautotrophyprovidesarichandplentifulenergysource foranimals,onequestionremains:howdohigher organismsliveinsuchaharshhabitat?Muchlikethe dogmathatalllifeonearthisdependentonsunlight,there hasbeenanecologicaltenetthatalllifeonearthrequires O 2 ,andalotofit,tolive.Clearly,thebiologicaldiversity ofgroundwatersystemsingeneral,andsulfidiccaveand karsthabitatsspecifically(Table2),pointstowardthefact thatlifecertainlyhasadaptivestrategiestolivinginthese extremeenvironments(e.g.,Howarth,1993;Badyaev, 2005;Parsons,2005). Numerousstudieshaveshownthatgroundwater crustaceanscanliveandgrowunderhypoxicconditions forseveralmonthsandcansurviveanoxiafor 48hr.This isinstarkcomparisonwithsurface-dwellingcrustaceans whocouldsurviveforonlyafewhourstooneday(Malard andHervant,1999;HervantandMalard,2005).Moreover, Bishopetal.(2004)foundthattherespirationratesof sevenordersofstygobiticcrustaceanslivingatdissolvedO 2 levelsof 0.6mgL 1 inanchialinecaveswerelowerthan surface-dwellingorganismsorsimilartoorganismsliving atslightlyhigherO 2 levels.Metabolicstrategiesand adaptationshavebeenexaminedforstygobitesand troglobites(e.g.,HervantandMalard,2005),wherebythe activityofvariousenzymes,andspecificallyhighlevelsof malatedehydrogenase,indicatethatsomestygobitesare poisedforanaerobicmetabolism(Bishopetal.,2004).The researchalsodemonstratesthatorganismsrapidlyrecover fromprolongedhypoxiabyefficientremovaloflactateand otheranaerobicwasteproducts(Hervantetal.,1999a; HervantandMalard,2005).Similarresultshavebeen reportedfordeep-seaventorganisms,inthatthoseanimals useanaerobicmetabolismtosupportactivityatlowO 2 levels,whileregulatingO 2 consumption,andmaintaining efficientcirculatorysystemsandhigh-affinityhemoglobin. Despitetheseadaptations,however,livingathypoxia stillbringsnoxiousgases,suchasH 2 S,intoanorganism’s body.Toleranceof,andsurvivalin,highH 2 Sconcentrationsforcaveanimalsinsulfidicsettings(suchasanchialinecaves)havenotbeenstudiedindetail.Forsome organisms,likethoseatthedeep-seavents,symbiosiswith microbesmaybeanevolutionarymechanismtodealwith highH 2 Slevels(e.g.,Someroetal.,1989).However,some studiesofpolychaetetubewormsdemonstratetheanimals cansurviveuptofourdayswhentheyswitchtoanaerobic metabolismunderanoxicconditionswithhighsulfide(up tomillimolarlevels),whichmaybeaidedbyspecial epidermaltissuestructuresindependentofbacterialsymbiosis(Hourdezetal.,2002;Menonetal.,2003). C LOSING R EMARKS Cave-adaptedorganismshavethepotentialtobesome oftherarestandmostthreatenedspeciesonEarth(e.g., vanBeynenandTownsend,2005).Subterraneanbiodiversityisquitehighglobally(GibertandDeharveng, 2002),andisconsideredtobestronglylinkedtothe (hydro)geologicageandpermanenceofthekarstsetting A NNETTE S UMMERS E NGEL JournalofCaveandKarstStudies, April2007 N 201

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(e.g.,Culver,1976;BarrandHolsinger,1985;Jonesetal., 1992).Withcontinualisolationfromthesurface,organismsdisperseandmigrate,andpopulationscanbecome separatedfromeachotherandspeciationcanoccur.For non-sulfidickarstsystems,ithasbeenestimatedthat 50% ofobligatecave-adaptedspeciescanbefoundin 1%of theland,atleastfortheUnitedStates(Culveretal.,2000). Forsulfidichabitats,localgeologicalandhydrostraigraphiccontrols(e.g.,ChristmanandCulver,2001)will impactthedistributionoforganismsendemictosulfidic systems,asconditionsthatleadtosulfideproductionare needed.Consequently,thedistributionofspeciesinsulfidic karstaquifersmaybeevenmorerestricted.Howdoesone actuallymeasurethespatialdistributionofananimal whosepotentialhabitatisa100km 2 aquifer?Isthisasmall distribution,oralargedistribution? Althoughitisevidentthattheintimatedependenceof subsurfaceecosystemsonsurface-derivednutrientsand energyhascatalyzedthemandatoryprotectionofmany karstsystemsfromabove-ground,usuallyanthropogenic, disturbances(vanBeynenandTownsend,2005),sulfidic ecosystemsmaynotrelyonsurface-derivedorganicsand maybepotentiallybufferedfromsuchdisturbances.To attempttounderstandmorefullythevulnerability,management,andsustainabilitychallengesfacingthesesystems, aswellasthepotentialthatthesesystemsmayhave amonetaryvalue,theamountoffutureworkisconsiderable.Isuggestthatexcitingavenuesforfutureresearchwill notonlybeintheexplorationofnewsystems,butintherediscoveryofoldsystems.Wehaveknownaboutsomeofthe sulfidiccavesandkarstaquifersfornearly100years,butwe stillmustshedlightonmanyoutstandingquestions, including:whatisthetruenatureofspeciesdiversityand distribution,howaretheecosystemsstructured,whatarethe ecologicalfunctionsoforganismswithinthesystem,howdo speciesadapttohabitatstresses,howdoeshabitatstress affectecosystemdiversityandstructure,andwhatarethe rolesofgeochemistryandgeologyonhabitatdevelopment andmodificationofthesesubterraneansulfidicecosystems? Uncoveringtheanswerstothesequestionswillcertainly provideyearsoffruitfulstudy. A CKNOWLEDGEMENTS Conversationsovertheyearswerethestimulifor conceptspresentedinthisreview(althoughfartoo numeroustoname,Iincludeherejustalistofthemost influentialandloudestvoices:M.L.Porter,P.C.Bennett, L.A.Stern,H.H.Hobbs,III,andD.C.Culver). GratitudeisexpressedtoJ.G.Palacios-Vargasandhis colleaguesandstudentsforgraciouslyprovidingdatafor CuevadeVillaLuz(CuevadelasSardinas,Mexico),and toM.RampiniandC.DiRussofordatafromGrottadi FiumeCoperto(Italy).G.SchindelandW.Elliottoffered informationregardingtheEdwardsAquiferbad-water fauna,andB.Kinklesuppliedunpublished16SrRNAgene sequencesfromMovileCave.S.EngelandK.Lavoie providedinsightfulcommentsforthemanuscript.Partial fundingwasprovidedbytheFacultyResearchCounciland CollegeofBasicSciencesatLouisianaStateUniversity, andbytheBoardofRegents(LEQSF[2006-09]-RD-A-03 andNSF/LEQSF[2005]-pfond-04).ThankstoMarcusO. GaryforthephotographinFigure3D. 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EDITORIAL Sixty-FiveandStillGoingStrong JournalofCaveandKarstStudies M ALCOLM S.F IELD Itiswithgreatpleasureandsatisfactionformethat withthisSpecialIssueofthe JournalofCaveandKarst Studies wemarkthe65 th AnniversaryoftheNational SpeleologicalSociety(NSS)whichoccurredin2006.The lastsuchspecialissuemarkedthe25 th Anniversaryofthe NSS. Thisparticularspecialissueisespeciallygratifying becauseitalsorepresentsamajorchangeinthewaythe Journal isnowputtogether.Authors,associateeditors (AEs),reviewers,andnumerousotherswillfindwhatI believearemajorimprovementstothe Journal publishing process. A RTICLESIN T HIS I SSUE First,IwanttopointoutthatforthisAnniversaryIssue severalindividualsconsentedtowritingspecialarticles markingtheprogressincaveandkarststudiessincethe inceptionoftheNSS.Backin1966,whichmarkedthe25 th AnniversaryoftheNSS,aspecialissueoftheold Bulletin oftheNationalSpeleologicalSociety (vol.28,no.1) includedmanuscriptsonearthsciencesandspeleology, evolutionofcavebiologyintheUnitedStates,cave explorationtechniques,andanearlyhistoryoftheNSS. ManuscriptsacceptedforthisspecialAnniversaryissue followtheoriginalconceptappliedinthe25 th Anniversary issuebyaddressingthemajorareasofcaveandkarst studiescoveredbythe Journal andsomecurrentlyless prominentareas,allbysomeofthemostrecognized researchersincavesandkarst. Forexample,earthscienceandbiologypapersmakeup thebulkofpaperssubmittedforpublicationinthe Journal Earthsciencepapersinthisissueincludemanuscriptson thehistoricalaspectsofspeleogenesisandcavegeology(A. Palmer),islandcaveandkarstformation(J.MylroieandJ. Mylroie),cavemineraologyandtheNSS(C.HillandP. Forti),hydrology(W.White),cavesedimentsandpaleoclimates(W.White),groundwatertracing(S.Worthington),andpseudokarst(W.Halliday).Lifesciencespapers includemanuscriptsonzoogeographyandbiodiversityin Missouricaves(W.Elliott),andbiologyandecologyof cavecrickets(K.Lavoie,K.Helf,andT.Poulson). Microbiologicalpapersincludemanuscriptsonmolecular techniquesusedinsubterraneanbiogeography(M.Porter), historicalperspectivesandfutureresearchongeomicrobiologyincaveenvironments(H.Barton),biodiversityof sulfidickarsthabitats(A.Engel);thelattertwocrossingthe earthscienceandbiologicaldivisionsofcavekarststudies. Othersignificantareasofcoverageinthe Journal inthe past,butnowmorerarelysubmittedforpublicationare archaeology,exploration,andsocialsciences.CavearchaeologyandtheNSS(G.Crothers,P.Willey,andP.Watson) documentsdirectionsthefieldhastakenovertheyears. Theimportanceofcaveexplorationandscientificresearch, asubjectareathatmayberegardedasthelegacyofthe NSSbutthathasbeensorelylackingoverthepastseveral years,iscoveredinthisissue(P.Kambesis).Evenmore rarely,asocialsciencepaperonthecreationofakarst database(L.FloreaandB.Fratesi)hasbeenincluded. Lastly,apaperonthehumanhealthaspectsofexploring andworkingincaveswithelevatedlevelsofradonhasbeen included(M.Field). P UBLISHING C HANGESWITH T HIS I SSUE AsofMay2007the Journal isnowacceptingall manuscriptsviaAllenTrack,aweb-basedsystemforonlinesubmission.TheAllenTrackwebsite,http://jcks. allentrack2.net,willbeaccessibledirectlyfromtheNSS JournalofCaveandKarstStudies website,http://www.caves.org/pub/journal/.AllenTrackisthesameorganization thathandlespublishingofsuchrespectedjournalsas AmericanMineralogist Geology GeologicalSocietyof AmericaBulletin GroundWater,JournalofPaleontology and JournalofSedimentaryResearch soitislikelythatmany authorswillalreadybefamiliarwiththeon-linesubmission process.Thischangeinourpublishingprocessrepresentsamajoraccomplishmentandshouldgreatly enhancethe Journal whilereducingoverallpublishingcosts. TheAllenTracksystemisfullyintegratedsothatthe editorialstaffcanfullymonitorthereviewprocessandmore effectivelykeeptheprocessmovingforward.Manuscripts willnolongerneedtobemailedintriplicate;norwillauthors beresponsiblefordeterminingwhichAEshouldreceive aparticularmanuscript.Byincludingselectedkeywordson thewebsitewhensubmittingamanuscript,theappropriate AEwillautomaticallybedetermined,butwhichmaybe overridden,asappropriate,byme.AllAEsandreviewers willhaveaccesstothesystemwheneverandwhereverthey areaslongastheyhaveaccesstotheinternet,soreviewsand decisionscanbemadewhiletraveling.Overall,everyone shouldfindtheprocessremarkablyeasy. E DITORIAL JournalofCaveandKarstStudies, April2007 N 1

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M ANUSCRIPT A UTHORS Manuscriptsubmissionisquiteeasy.Afteraccessingthe siteforthefirsttime,authorscreatealoginandpassword andthenwillenternecessarypreliminarymanuscript information(authors,addresses,manuscripttitle,etc.). Thenanauthorwilluploadtheirmanuscript,figurefiles, andtablefilespreferablyintheoriginalformatinwhich theywerecreated(e.g.,DOC,WPD,RTF,TXT,orLaTeX formanuscriptsandtables;Excelfortables;andTIFF, EPS,orPDFforfigures).Alternatively,manuscriptscan besubmittedasPDForHTMLfilesforreviewpurposes only;ifacceptedthemanuscriptwillneedtoberesubmitted inoneofthelistedacceptedformats.Tablesandfigures maybeappendedtothemaindocumentwhensubmittedor tablesandfiguresmaybeuploadedseparatelyfromthe maindocument. Onceuploaded,thesystemwillconvertalluploaded filestoasinglePDFinapproximately10minutesand aconfirmationwillbesenttoauthorsviae-mail.Manuscriptsalreadyinthesystemwillbeuploadedbytheeditor, buteffectiveJune2007itisexpectedthatallauthorswill submitmanuscriptsusingthenewinternet-basedsystem. A SSOCIATE E DITORSAND R EVIEWERS Associateeditorsandreviewerswillbeabletoaccess submittedmanuscriptson-lineandwillbeabletoconduct reviewson-lineaswell.Alternatively,ifahardcopyofthe submittedmanuscriptisdesired,thenacopymaybe downloadedandprintedaswell.ReviewerÂ’ssummary opinions,comments,andrecommendationsforeditors,as wellasanydetailedcommentsforauthors,willallbe submittedviatheAllenTracksystem.Annotatedcomments onhardcopiescanstillbereturnedtoAEsifdesired,but arenolongernecessary. AssociateEditorrecommendationsandtheEditorÂ’s decisionregardingeachmanuscriptwillbesentouttothe correspondingauthorviae-mail.Author-requiredrevisions willalsousetheAllenTrackwebsiteaswillfinaledits. Becausethisissuchasignificantchangeintheway manuscriptswillbehandledinthe Journal, itwilllikely requiresomepatiencebyeveryoneconcernedaswework throughthenewprocedures.However,itisexpectedthat thisnew Journal processwillresultinmonetarysavingsand speedupthepublicationprocess.Overall,itshouldbe abenefittoallconcerned. E DITORIAL 2 N JournalofCaveandKarstStudies, April2007



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RISKSTOCAVERSANDCAVEWORKERSFROM EXPOSURESTOLOW-LEVELIONIZING a RADIATION FROM 222 RNDECAYINCAVES M ALCOLM S.F IELD OfficeofResearchandDevelopment,U.S.EnvironmentalProtectionAgenc y,Washington,D.C.20460,field.malcolm@epa.gov Abstract: Humanhealthrisksposedbyexposuretoelevatedlevelsof 222 Rnincavesare notwelldocumented.Variousstudiesthroughouttheworldhavedetailedt heoftenvery high 222 Rngasconcentrationsincavesandexposurestocaversandcommercialtour guidesandotheremployees,butwithoutaconsequentassessmentoftheove rallimpact onhumanhealth.Although 222 Rnconcentrationsincavesareconsideredhighrelativeto mostabovegrounddwellings,thelevelsidentifiedarealsoconsideredto belowfor ionizing a radiation.Low-levelionizingradiationimpactsonhumanhealtharededu ced byapplicationofthelinearno-thresholdtheory(LNT)ofradiationcarci nogenesis. Comprehensivereviewsofthepublishedliteratureandanunderstandingo fexposure timesuggeststhatcommercialcaveworkers(e.g.,tourguides)andcommer cial 238 U-mine workersarebothexposedforthesamenumberofhourspermonth( 170h),butcave workersareexposedtomuchlower 222 Rnconcentrationsthanaremineworkers.Cavers willgenerallybeexposedforasmallernumberofhourspermonth.Riskesti mates suggestthatcaverswilllikelybesubjecttoinsignificantrisks,buttha tcaveworkersmay besubjecttolow-levelrisksofdevelopinglungcancersfromelevatedlev elsof 222 Rngas concentrationsincaves. I NTRODUCTION ThispaperwasdevelopedtoprovidetheNational SpeleologicalSocietyreaderwithanintensiveinvestigation ofthepotentialhealtheffectsposedbyexposuretoelevated levelsofradonincaves.Totheauthor’sknowledge,no otherpublicationonradonincaveshasdelvedintothe riskstocaversfromexposuretoradonincavestothe extentthatthispaperdoes. Radon-222isgenerallyregardedasanaturallyoccurring inertradioactivegaswithahalflifeof3.824daysandis producedwithinthe 238 Udecayseries(Fig.1),theprocessof whichisdescribedindetailinField(1994,p.52–60)and wherethephenomenonofradioactivityisdescribedindetail inIvanovich(1992,p.1–33).Infact, 222 Rnisonlypartly inert.Radon-222mayalsoberegardedasametalloid 1 ,an elementthatliesonthediagonalofthePeriodicTable betweenthetruemetalsandnonmetals(Fig.2).Because 222 Rnisametalloid,itexhibitssomecharacteristicsofboth metalsandnonmetals,suchasformingaseriesofclathrate compounds 2 (inclusioncompounds),andreactsreadilywith fluorineandfluorides(Stein,1987;Cigna,2005). Radon-222posesasubstantialthreattohumanhealth whenbuild-upoccursinconfinedspacessuchashomes, mines,andcaves(ICRP,1994a,p.1)andwhenexposure timeissufficientlylong.Theaverageannualperperson radiationdosefromexposureto 222 Rnfromcavesis estimatedtobe1nSv(0.1 rem) 3 ,althoughcaversandcave workersareexpectedtoreceivemuchhigherdoses(ATSDR, 1997,p.217).Showcavesarearecognizedhazardinterms of 222 Rnexposuretocaveworkers(tourguides,maintenancepersonnel,employeesworkinginshopsbuiltovercave entrances,etc.)(IAEA,2003,p.5–6and46),butbecauseof thesensitivenatureofcaveenvironments,high 222 Rngas concentrationscannoteasilyberemediated(IAEA,2003, p.60).Forcedairventilationincavesisregardedas unthinkablebecauseofthelikelydeleteriouseffectsonthe microclimatesandbiota(YarboroughandMeyers,1978, p.28and73).TheU.S.EnvironmentalProtectionAgency (EPA)believesthattherisksposedtohumanhealthbylow levelsof 222 Rngasinsingle-familyresidencestobemore significantthantheriskstouraniumminersexposedtovery highlevelsof 222 Rngasbecausetheminersareonlyexposed for170hpermonthinthemine(1WorkingLevelMonth) whilehomeownersspendmoretimeintheirdwellingsand receiveagreateroverallexposure(Abelson,1991).The principalthreatisbytheformationoflifespanshortening lungcancer,pulmonaryemphysema,andpulmonary fibrosisthroughdamagetotherespiratoryepithelium (Samet,1997;Cross,1987,p.215–216). Theexistenceofelevatedconcentrationsof 222 Rnin cavesiswellestablishedintheliterature(Table1).Table1 isasamplingoftheliteraturethatcontainsextensive 222 Rn concentrationvalues,butdoesnotlistallofthebasic literatureoncavesand 222 Rn(seeforexample,Cigna, 2005;Gunn,2003,p.617–618).However,therisksto Disclaimer: Theviewsexpressedinthispaperaresolelythoseoftheauthoranddo notnecessarilyreflecttheviewsorpoliciesoftheU.S.EnvironmentalPr otection Agency. MalcolmS.Field–Riskstocaversandcaveworkersfromexposurestolow-le velionizing a radiationfrom 222 Rndecayincaves. Journal ofCaveandKarstStudies, v.69,no.1,p.207–228. JournalofCaveandKarstStudies, April2007 N 207

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caversandcaveworkersfromexposuretotherelatively high 222 Rnconcentrationsincavesarepoorlyunderstood andrarelyreportedintheliterature(Kobaletal.,1986, 1987;Vaupotic etal.,1998,2001). Thepurposeofthispaperistoexploretherisksposed tothehealthofcaversandtourguidesasaresultof exposuretolow-levelionizingradiationfrom 222 Rngas anditsprogeny.Radon-219and 220 Rn(commonlyknown asthoron)donotrepresentasseriousaconcernasdoes 222 Rnbecause(1) 219 Rnisrelativelyrareandhasavery shorthalflife( T 4s)and(2) 220 Rnhasaveryshort halflife( T 56s)(ATSDR,1990,p.11).Radon-219has onlyrarelybeenfoundatelevatedlevelsincaves (YarboroughandMeyers,1978,p.42). Particularattentionwillbedirectedatthelinearnothresholdtheory(LNT)ofradiationcarcinogenesisbecausethisistheacceptedmodelforestimatingrisksposed byexposureto 222 Rngasanditsprogeny(Dicus,2001; KellererandNekolla,2000;NCRP,2001;NAS,2005; NRC,1999,p.69)eventhoughthereissomedisputeasto itsappropriateness(e.g.,Bondetal.,1996;Cohen,2000). Thereis,however,goodreasontocontinuerelyingonthe LNTevenwithallitsattendantproblemsbecauseitis areasonableriskmodel(Oughton,2006). T HREATS P OSEDBY 222 R NANDITS P ROGENY Radon-222istheheaviestofthenoblegasesandbecause itisarelativelynonreactivegasthatexistseverywhereinthe environment,ittendstomigratetoandconcentratein enclosedspaces(e.g.,basements,caves,tunnels,etc.). However, 222 Rnisnotamajorhealthriskbyitself. Highconcentrationsof 222 Rnprogeny( 218 Po, 214 Pb, 214 Bi,and 214 Po)arewidelyrecognizedasasourceoflung cancerandpossiblyothercancers(Henshawetal.,1990; Bridgesetal.,1991)throughtheemissionof a -and b particleswithdenseionizationalongtheirtracksalthoughit isthe a -particlesthataremostresponsiblefortheresulting high-linearenergytransfer(LET) 4 becauseofitslarge 2 chargeandrelativelylargemass( 8,000timesthatofan electron).Emissionof b -particles(high-energyelectrons) resultsinlow-LETbecauseofits 6 1chargeandmuch smallermassthan a -particles.Ineithercase,bothlowand highLETinteractionscancausesignificantDNAdamage (ATSDR,1997,p.30–31),butitisthedenselyionizing radiationproducedby a -particledecaythatcausesmany doublestrandDNAbreaksthataremostdifficultforcell repairandaremostlikelytogiverisetocancerformation (CravenandSmit,2006).AccordingtoCravenandSmit, sparselyionizingradiationtypicallyresultsinsinglestrand DNAbreakswhicharemucheasierforcellstorepair. Cothern(1989)statesthat‘‘between4,000and30,000 fatallungcancersoccureachyearduetoexposuretoradon inindoorair,’’butdoesnotofferanysupportingdataor referencesforsuchacontention.TheEPAhadprojected Figure2.Arrangementofthemetalloidelements(dark shading)inthePeriodicTable(modifiedfromStein(1987). Figure1.Uranium-238decayseries.Thehorizontalscale, Z,isthenumberofprotonsinthenucleus,andthevertical scale,N,isthenumberofneutronsinthenucleus.Also shownarethehalf-lives,typeofdecay(eitherby a -or b particles),andthemajorradiationenergies(inMeV)of 238 U anditsprogeny.ModifiedfromCothern(1987,p.7)and NRC(1988,p.26).Negligiblepercentagedecaysincluded eventhoughtheyarenotahumanhealthconcern.See Table12intheAppendixforthehistoricnamesofthe 222 Rnprogeny. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 208 N JournalofCaveandKarstStudies, April2007

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14,000lung-cancerdeathsperyearfromresidential 222 Rn exposurewithanuncertaintyrangeof7,000to30,000 (Page,1993),butnowestimates21,000lung-cancerdeaths peryearfromresidential 222 Rnexposurewithanuncertaintyrangeof8,000to45,000(U.S.EPA,2006).In fact,theexpectedlungcancersandotheradversehealth effectsmaybemorearesultofsmokingthanofinhalation of 222 Rngas(Pisaetal.,2001).Inaddition,theexpected lungcancersincaversandcaveworkersappeartobe conspicuouslymissingfromthepublishedliterature, perhapsbecausenoonehasyetlinkedlungcancersin caversandcaveworkerstolong-termexposuretohigh 222 Rnconcentrations(Halliday,2003). Riskstocaversandcaveworkersbyexposurestohigh levelsof 222 Rnmaynotbeasseriousasisoftenpresented. Thepotentialoverestimationoftherisksposedbyelevated levelsof 222 Rnandthebeliefbymanyindividualsthat overestimationmayactuallybethecase,havecausedsome consternationamongsomeresearchers(Cothern,1989, 1990;Little,1997).Thepossibilitythat 222 Rnandits progenymayberesponsibleforsomecancersotherthan lungcanceralsoisnotstronglysupportedintheliterature (Tomaseketal.,1993).Forexample,Lawetal.(2000)were unabletoestablishanassociationbetweenhousehold exposureto 222 Rnandthedevelopmentofleukemiain adultsinGreatBritain.Lauieretal.(2001)obtained similarresults. Asignificantreasonwhy 222 Rnanditsprogenymaynot beasseriousathreattocaversandcaveworkersmaybe becausealthough 222 Rnconcentrationsincavesare consideredtobeelevated,theselevelsarealsoconsidered toberelativelylowintermsofionizingradiation.For example,employeesexposedtoradiationintheworkplace inGreatBritain(e.g.,cavetourguides)arenotallowedto receiveannualeffectiveradiationdoses 5 above50mSv yr 1 (10WLMyr 1 )withanactionlevelof15mSv Table1.Summaryof 222 Rnliterature(modifiedfromHylandandGunn(1994).Notethatmanyofther eferencesinclude 222 Rn measurementsfromseveralsources a Country Mean 222 Rn Concentration (Bqm 3 ) Numberof 222 Rn Measurements Max. 222 Rn Concentration (Bqm 3 ) Min. 222 Rn Concentration (Bqm 3 )Reference Australia6102744,0459Solomonetal.(1996) China b 1413227838Wiegandetal.(1995) CzechRepublic1,2356021,000200BurianandStelcl(1990) GreatBritain2,90782046,08010HylandandGunn(1994) GreatBritainÂ…2,000155,000100HylandandGunn(1994) GreatBritain35,89034155,0007,400Gunnetal.(1991) GreatBritain9,3061312,55268Gillmoreetal.(2000) GreatBritain365423,18726Gillmoreetal.(2002) GreatBritain315283,04734Gillmoreetal.(2002) Greece25,179688,060185Papastefanouetal.(1986) Hungary3,3002514,000500Somogyietal.(1989) Hungary2,468813,200200Lenartetal.(1990) Ireland4,127267,940200Duffyetal.(1996) Japan11520 1MikiandIauthora(1980) Malaysia596391,978100Gillmoreetal.(2005) Poland1,1662794,18060Przylibski(1999) Russia2,390148,550373Gunn(1991) Slovenia1,4121017,22015Kobaletal.(1986) Slovenia965665,92060Kobaletal.(1987) Spain1083014885Duen asetal.(1998) Spain3,5648,5877,120186Larioetal.(2005) SouthAfrica267632,3193Gamble(1981) Switzerland25,000640,0002,000Surbeck(1990) UnitedStates1,927609,35037Yarborough(1976) UnitedStates2,589119,460370Ehemanetal.(1991) UnitedStates1,475Â…2,350740Ahlstrand(1980) UnitedStatesÂ…8601,850333AhlstrandandFry(1976) UnitedStates11,6783782,17711Bashor(undated) a Dataqualitycontrollikelyvariesforeachstudyconductedforeachcount rywhichshouldberegardedasproblematic. b MeasurementstakeninChinesecavedwellingsbuiltintheChineseLoessPl ateauwhichismainlycomposedofMesozoicsandstonesoverlainbyTertiar yredclaysthatare coveredbyQuaternaryloesstenstooveronehundredmetersthick(Wiegand etal.,1995)wherethenumberofinhabitantsexceedthreemillion(Yanada ,2003) M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 209

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Table2.Inhalationexposurestudiesof 222 Rn(modifiedfromATSDR,1990,pp.13–15).Superscriptnumbersnexttoeac hentrycorrespondtodatapointnumbers inFigure3. Species Exposure Frequency/ DurationEffect NOAEL (Bqm 3 ) LOAEL(Effect) Reference LessSerious(Bqm 3 )Serious(Bqm 3 ) AcuteExposure Mouse 1 1dDeath8.14 3 10 9 (30dLD 50 )Morken(1955) Mouse 2 1dHemato8.14 3 10 9 (anemia)Morken(1955) 5–40h IntermediateExposure Rat 3 4–6moDeath1.11 3 10 5 Chameaudetal.(1984) 2dwk 1 1hd 1 Rat 4 LifespanDeath1.78 3 10 8 (declifespan)Palmeretal.(1973) 2dwk 1 90hwk 1 Mouse 5 LifespanDeath1.55 3 10 7 (declifespan)MorkenandScott(1966) 150hwk 1 Hamster 6 LifespanDeath1.78 3 10 8 (declifespan)Palmeretal.(1973) Rat 7 LifespanResp1.78 3 10 8 (metaplasia)Palmeretal.(1973) 2dwk 1 Other1.78 3 10 8 (decbw) 90hwk 1 Mouse 8 LifespanResp1.55 3 10 7 (metaplasia)MorkenandScott(1966) 150hwk 1 Hemato1.55 3 10 7 (declymph) Other1.55 3 10 7 (decbw) Mouse 9 LifespanResp1.78 3 10 8 (fibrosis)Palmeretal.(1973) 2dwk 1 Other1.78 3 10 8 (decbw) 90hwk 1 Hamster 10 LifespanResp1.78 3 10 8 (metaplasia)Palmeretal.(1973) 2dwk 1 Other1.78 3 10 8 (decbw) 90hwk 1 Dog 11 1–50dResp2.04 3 10 7 (fibrosis)Morken(1973) 5dwk 1 20hwk 1 Rat 12 2.5–8wkCancer1.11 3 10 7 (CEL-lung)Chameaudetal.(1982) 4dwk 1 3–6hd 1 Rat 13 25–115dCancer2.78 3 10 7 (CEL-lung)Chameaudetal.(1974) 4–5hd 1 Rat 14 6–6moCancer1.11 3 10 7 (CEL-lung)Chameaudetal.(1984) 2dwk 1 1hd 1 R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 210 N JournalofCaveandKarstStudies, April2007

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Species Exposure Frequency/ DurationEffect NOAEL (Bqm 3 ) LOAEL(Effect) Reference LessSerious(Bqm 3 )Serious(Bqm 3 ) ChronicExposure Hamster 15 LifespanDeath1.15 3 10 7 Crossetal.(1978) 5dwk 1 6hd 1 Hamster 16 1mo 18yr (occup) Resp 3.70 3 10 3 (tuberculosis)Waxweileretal.(1981) Hamster 17 LifespanResp9.62 3 10 6 (hyperplasia)Crossetal.(1978) 5dwk 1 Hemato1.15 3 10 7 6hd 1 Other9.62 3 10 6 (decbw) Human 18 0.5–23yr(occup)Cancer1.26 3 10 4 (CEL-lung)GottliebandHusen (1982) Human 19 (occup)Cancer7.40 3 10 3 (CEL-lung)Morrisonetal.(1981) Human 20 0–14yr(occup)Cancer3.70 3 10 3 (CEL-lung)Sollietal.(1985) Human 21 29yr(occup)Cancer2.22 3 10 3 (CEL-lung)EdlingandAxelson (1983) Human 22 1– 20yr (occup) Cancer1.85 3 10 3 (CEL-lung)DamberandLarsson (1985) Human 23 48wkyr 1 Cancer1.85 3 10 3 (CEL-lung)Howeetal.(1987) 48hwk 1 (occup) Human 24 10yr(occup)Cancer1.11 3 10 3 (CEL-lung)Snihs(1973) Human 25 2–30yr(res)Cancer5.55 3 10 1 (CEL-lung)Svenssonetal.(1989) Human 26 (occup)Cancer8.88 3 10 3 (CEL-lung)Foxetal.(1981) Human 27 1mon–18yr (occup) Cancer3.70 3 10 3 (CEL-lung)Waxweileretal.(1981) Human 28 1mon–30yr (occup) Cancer1.48 3 10 4 (CEL-lung)Roscoeetal.(1989) CEL CancerEffectLevel hemato hematological resp respiratory occup occupational dec decreased bw bodyweight res residential Table2.Continued. M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 211

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(1.5rem)(HylandandGunn,1994).Thistotalannual effectivedoseof50mSvyr 1 isalsoapplicableinsome instancesintheUnitedStates(U.S.Navy,2001,p.4-1and NRC,2005,p.5),although20mSvyr 1 (4WLMyr 1 )is generallytheacceptedlevel(OSHA,1988,41CFR 57.5038)whiletheNCRP(1993,pp.34–35)hassuggested moreflexibilitytocontrolworkerexposure.However,lowradiationdosesareconsideredtorangefromnear0to 100mGy 6 (0to10rad),mediumdosesfrom100mGyto 1Gy(10to100rad),andhighdosesfrom1Gyto20– 60Gy(100to2,000–6,000rad)(NRC,2005,p.374). Bythisdefinitionitwouldappearthatanactionlevel basedonaneffectivedoseof15mSvmaybeoverly protective.Thehumanequivalentdose H T isestimated usingEquation(1) H T R W R D T R 1 andtheeffectivedose E D isestimatedfrom E D T W T i R W R D T R 2 Using W R 20for a -particles(ICRP,1980,p.94)results inanabsorbeddose D T,R of0.75mGy,whichisatthe lowerspectrumofalow-radiationdose.Using W T L 0 12 forthelung(0.24forlungs)(ICRP,1991,p.68)resultsin 6.25mGywhichisstillatthelowerspectrumofalowradiationdose. 222 R N P ROGENY Althoughitistruethat 222 Rnrepresentsarisktocavers intermsoflungcancer,itsrelativelylonghalflife(3.824d) willmoreoftenresultintheexhalationof 222 Rnpriorto emanationofan a -particlethatcouldpenetratethe epitheliumofthelungtocauseacancerousgrowth.So eventhoughtheenergyassociatedwiththeemissionofan a -particlefrom 222 Rnisrelativelyhigh(5.49MeV)anditis possiblethat a -particleemissionfrominhaled 222 Rngas mayhaveanadverseaffectonhumanhealth,itisnotlikely that a emissionwillactuallyoccurduringthetimethatthe 222 Rngasresidesinthelung.Thissituationisconsiderably differentfor 222 Rnprogeny. Thefour 222 Rnprogeny( 218 Po, 214 Pb, 214 Bi,and 214 Po) areeithermetals( 214 Pband 214 Bi)ormetalloids( 218 Poand 214 Po)thatarerelativelyshort-livedandemit a -particles withrelativelyhighenergyand b -particleswithrelatively lowenergy(Fig.1).Itisthesefeatures,principallythe a particles,thatrepresentthemainriskposedby 222 Rn.Each ofthefourprincipal 222 Rnprogenyarequitereactive, whichcausesthemtoplate-out 7 inthelungaswellas enhancingtheirtendencytoadsorbtosmokeanddust particles.Theriskoflungcanceroccurrenceisexacerbated bysmokeanddustparticlesbecausethesemetalsand metalloidsreadilyreactwithandadsorbtotheparticles whichareeasilyinhaled. Threatsfrom 218 Po Polonium-218hasahalflifeof3.05minandisthe immediateprogenyresultingfromthedecayof 222 Rn. When 218 Podecays,itemitsan a -particlewitharelatively highenergyof6.12MeV.Withahalflifeof3.05minitis possiblethat 218 Powillemitan a -particleduringthetime thatitresidesinthelung.However,itsrelativelyshorthalf lifetendstopreventitsbeingeasilydistributedthroughout thebodyfromthelungs. Threatsfrom 214 Pband 214 Bi Lead-214and 214 Biaremetalswithhalflivesof 26.8minand19.7min,respectively.Thesetworadioisotopesdecaybylowenergy b emission,butarestill athreattohumanhealth,althoughlesssothantheother short-lived 222 Rnprogenythatdecayby a emission (Fig.1).Theirrelativelylongerhalflivesandlowenergy relegate 214 Pband 214 Bitoaslightlylesserthreatstatus.In addition,theirhalflivesarestilltooshorttoallowfor substantialdistributionthroughoutthebody. Threatsfrom 214 Po Polonium-214hasaveryshorthalflife(164 s).Itemits an a -particlewithahighenergyof7.69MeV.Withahalf lifeofjust164 sitishighlylikelythat 214 Powillemitan a particleduringthetimethatitresidesinthelung.Itsvery shorthalflifeandhighenergymakes 214 Poasignificant threattohumanhealth.Althoughtheveryshorthalflifeof 214 Popreventsitsdistributionthroughoutthebody,the relativelylonghalflifeofitsimmediateprogeny 210 Pb (22.3yr)canresultinseriousharminpartsofthebody otherthanthelungsfromthedecayof 210 Pb. Poloniumradionuclideshavemanyofthecharacteristicsofrare-earthelements,areamphoteric,andtendto formhydroxidesandradiocolloids invitro 8 and invivo 9 Thelattertendstocausepoloniumtobecomephagocytized 10 bycellsofthereticuloendothelialsystem 11 for eventualdepositioninthespleen,lymphnodes,bone marrow,liver,andkidneysafterparenteraladministration 12 (NRC,1988,p.161).Fortunately,thehalflivesof thepoloniumradionuclidesintheimmediate 222 Rn-decay seriesareofsuchashortduration( T for 218 Po 3.05minand T for 214 Po 164 s)theseproblemsare generallynotamajorconcern.However, 210 Pbwithits muchlongerhalflife( T 22.3yr)isofconcern. H EALTH E FFECT E STIMATESFROM E XPOSURESTO 222 R N ANDITS P ROGENY Inhalationexposuretosignificantlevelsof 222 Rnandits progeny(assumedtobeinequilibrium)havebeenshownto causeacuteandchroniceffectsonlaboratoryanimalsand humans(Table2andFig.3)(ATSDR,1990,p.12–27). However,theprocesseslinkinginhalationof 222 Rnandits progenytoincreasedlungcancerriskarecomplex(ICRP, 1994a,p.2)primarilybecauseofthenumerousconfoundR ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 212 N JournalofCaveandKarstStudies, April2007

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ingfactors 13 (ICRP,1994a,p.7)(e.g.,smoking).Forthis reason,manyoftheepidemiologicalstudiesonminersand animalsareinadequatesothathealthresearchcontinues. R EVIEWOF S ELECTED A NIMALAND H UMAN S TUDIES The 222 Rnconcentrationsusedinthestudiescitedby ATSDR(1990,p.12–27)rangedfromalowof56Bqm 3 (humanstudies)toahighof8.14 3 10 9 Bqm 3 (animal studies).Inthehumanstudies,acancereffectlevelinlungs wasidentified(actualexposurefrequency/durationwas from 2–30yr).Intheanimalstudies,mousemortality anddevelopmentofhematological(anemia)symptoms occurredaftera30dMedianLethalDose(LD 50 )study (actualexposurefrequency/durationwasfrom5–40h). AnimalStudies Themousestudiesobviouslyinvolvedmuchhigher dosesof 222 Rnthanwouldtypicallybeexperiencedby acaver(seeTable1),buttheexposuretimewouldbe comparable.Thehumanstudyandothersimilarstudies citedbyATSDR(1990)include 222 Rnconcentrationsthat atypicalcavermaybeexposedto,buttheexamined exposuretimesaregenerallylongerthanwouldbetypical foracaver(anexceptioncanbemadefortourguides, maintenanceworkers,etc.). TheanimalstudieslistedinTable2resultedinfewlung cancers(21%indogs,zeroinmice,and1.3%inSyrian hamsters)eventhoughthe 222 Rndosestowhichthe animalswereexposedwereextremelyhigh(NRC,1999, p.43).Syrianhamstersdidnotdevelopanytumorsat exposuresbelow3.89 3 10 5 Jsm 3 (3.0 3 10 4 WLM) whereasratsshowedahighincidenceofrespiratory-tract tumorsafterexposureto 222 Rn.However,accordingto NRC(1999,p.43–44)themechanisticbasesofthese interspeciesdifferencesaresuchthatspecies-to-species extrapolationsofabsoluteriskcannotbeused.Asaresult, directextrapolationofanimaldatatohumanscannotbe usedtopredictabsoluterisk. HumanStudies Epidemiologicalstudiesontheeffectsof 222 Rngasand itsprogenyonhumanhealthconsistprimarilyofstudieson 238 Uandphosphateminers( 238 Uisassociatedwith phosphatedeposits).Thehumanstudies,exceptforthe Svenssonetal.(1989)study(number25inTable2and Figure3),mostlytendtoclusterinthecancerregionfor 222 Rnconcentrationsaround1,000to10,000Bqm 3 (Figure3).Theseepidemiologicalstudiesofcohortsof minersconfirmthatlong-termexposuretohighlevelsof 222 Rngasanditsprogenyrepresentaveryseriousthreatto humanhealth. Onehumanstudy(Svenssonetal.,1989)while suggestingaclearlinkbetween 222 Rnandsmallcell carcinomainthelung,alsonotesthatcancerswereless prevalentintheruralcohortovertheurbanizedcohort whereambientairpollutionwasapositiveconfounder. Thisdiscrepancyisregardedbytheauthorsasaserious flawinthestudy.Additionally,accordingtoSnihs(1973) noconclusionsregardingdoseandeffectbelow50mSv (5rem)maybedrawnbecauseofthelargeuncertainties andstatisticalerrors.Thissuggeststhattheriskstocavers andcaveworkersfromexposureto 222 Rnincavesmaynot beoverlysignificant. E XPOSUREOF C AVERSAND C AVE W ORKERSTO 222 R N ANDITS P ROGENY Theformationof 222 Rnanditsprogenyisshownbythe decaysequenceinFigure1.Radon-222readilymigratesto areaswithanegativeairspace,suchascavesandtunnels.Itis alsosolubleinwaterandwillresideincavewatersand atmospheresinequilibrium(Fig.4).Inaddition,the 222 Rn parent, 226 Ra,willreactwithandprecipitateoncavewallsas RaCO 3 andthusprovidesacontinuoussourceof 222 Rn.The netresultisthat 222 Rnconcentrationsincavesareconsiderablyhigherthantypicallyoccurinabovegroundresidences, butaresignificantlylessthanthosefoundin 238 Umines. Figure3.Levelsofsignificantinhalationexposureto 222 Rn (modifiedfromATSDR,1990,pp.16–17).Numbersnextto eachdatapointcorrespondtosuperscriptsforeachentryin Table2.AcuteandIntermediateeffects aandchronic effects b. M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 213

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C UMULATIVE E XPOSURE Thedecayof 222 Rntoitsprogenyresultsinsecular equilibrium,providednoneofitsprogenyplateout(i.e., adsorbtocavewalls).Cumulativeexposure C E has historicallybeencalculatedintermsofworkinglevels (WL)with170hforaworkinglevelmonth(WLM)andis calculated(inSIunitsofJhm 3 )using(NRC,1999, p.178) C E n i 1 C Rn i t i 170 3 where( C R n ) i istheaverageconcentrationof 222 Rndecay productsduringanexposureintervalexpressedinJm 3 and t i isthenumberofhoursoftheexposure. ThesignificancetocaversofEquation(3)isthehours ofexposure.AccordingtoNRC(1999,p.178),the cumulativeexposureforindividualswhocontinuously occupyaresidence(commonlyknownasshut-ins)at agivendecayproductconcentrationisgreaterthanfour timesthatforanoccupationalexposure(8,766hcompared to2,000hworkedonanannualbasis).Thismeansthatfor cavetourguideswhoworknomorethan170hoursper monthwillbeexposedtoonequarterthatofindividuals whodonotleavetheirdwelling.Forrecreationalcaving, exposurewillgenerallybeconsiderablyless. Thenetresultisthatindividualslivinginaboveground dwellings,butarenotnecessarilyshut-ins,areannually exposedto4.8mSvof 222 Rn,ascomparedtocoalandmetal minerswhoareannuallyexposedtojust0.7and2.7mSvof 222 Rn,respectively(Wrixonetal.,2004,p.40).Forcavers andcaveworkers,radiationdosesarelikelytobemuchless because,although 222 Rnconcentrationsincavesarelikelyto besimilartothatofcoalmines,theywillbelowerthanin 238 Umineswhileexposuretimeswilltypicallybemuchless thanthatofanoccupantofadwelling. ComparativeDosimetry Theactivityofthe 222 Rndecayproductsisdescribedby thePotentialAlpha-EnergyConcentration(PAEC)which isanon-equilibriummixture.ThePAECisobtainedfrom thepotentialalphaenergyperunitofactivity(Bq)ofthe consideredradionuclideaccordingto e p / l r ( e p T 1/2 /ln2) (ICRP,1994a,p.3).ThetotalairbornePAECmaybe obtainedfrom(ICRP,1994a,p.4) C p i C i e p i l r i 4 wherevaluesfor e p and l r arelistedinTable3.Thehalflife of 214 Poissoshort( T 164 s;seeFig.1)thatforall practicalpurposesitisalwaysinequilibriumwithitsparent Figure4.Factorscontrollingtheingrowthanddecayof 222 Rnequilibriumactivitiesinacavesystem(modifiedfromSmart andFriederich,1986;Smart,1991).Radon-222ingrowthanddecayprocess esinkarstaquiferwatersprovidedbyPeterSmart ( pers.comm. ).Otherimportantfactorsincludedilutionandvolatilization.Cavebre athingeffectson 222 Rnconcentrationsare describedinCunninghamandLaRock(1991);YarboroughandMeyers(1978,p p.22–42.PrecipitationofRaCO 3 onconduit wallsisdescribedinField(1994,pp.59–61).Radon-222secularequilibr iumisestablishedafter26days. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 214 N JournalofCaveandKarstStudies, April2007

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214 Biandisnotneededinthedecaychaincalculations (NRC,1999,p.137).ThePotentialAlpha-EnergyExposure (PAEE)maythenbecalculatedfrom(ICRP,1994a,p.4) P p t t 0 C p t 5 wheretime t isexpressedastheamountoftimeanindividual isexposed(e.g.,oneweek,onemonth,etc.). Theequilibriumfactor F isdefinedastheratioof 222 Rn decayproductconcentrationtothatof 222 Rnandisgiven by(Hopkeetal.,1995) F 1 18 10 8 C p C Rn 6 wherethevalueof F rangesfrom0.2to0.8,buttypically rangesfrom0.35to0.40.Adefaultindoorvalueof0.4is recommendedbyICRP(1994a,p.20).However,because ofthedifficultyofestimating 222 Rndecayproduct concentrationsincaveswhichrangefrom0.04to0.95, ameanvalueof0.5isusuallyassignedto F forcavestudies (seeforexample,HylandandGunn,1994)although astrongbasisforthiscontentionhasnotbeenreported. Aleyetal.(2006)suggestedthat,forsomenotable exceptions, F formostshowcavesprobablyrangesbetween 0.5and1.0,althoughastrongbasisforthiscontentionwas notsupportedinthisinstanceeither. UsingEquation(6)itispossibletocalculatetheactual EquilibriumEquivalentExposure(EEQ)from(ICRP, 1994,P.4) P eq t t 0 C eq t 7 where C eq FC Rn 8 TheEEQisameasureoftheexposureto 222 Rnandits progenythatanindividualreceivesforagiven 222 Rn concentration.ItistheEEQthatdetermineshowseriously anindividualhasbeenexposedtoagivenconcentrationof 222 Rnanditsprogenyforagivenperiodoftime. R ECOMMENDED 222 R N E XPOSURES AllowableexposurestocaveworkerstoPAEChave variedovertheyearsascancerriskshavebecomebetter understood.InitialU.S.Governmentregulationswerefirst setin1976,butwerelaterrevised. 1976Recommendations In1976,theNationalInstituteofOccupationalSafety andHealth(NIOSH)recognizedthat 222 Rnprogenyat severalcavesmanagedbytheNationalparkService(NPS) wereneartheoccupationallimitsassetforthinOccupational SafetyandHealthAdministration(OSHA)standardsfor 238 Uminers.NPScavesinwhichthePAECexceeded6.24 J m 3 (0.30WL)includeCarlsbadCavernsNationalPark, N.M.,LehmanCavesNationalMonument,Nev.,MammothCaveNationalPark,Ky.,OregonCavesNational Park,Ore.,andRoundSpringCaveinOzarkNational ScenicRiverways,Mo.Additionally,thePAECinsidethe cavesandabovegroundbuildingscooledbycaveairat MammothCavewere12.48 Jm 3 (0.60WL)(Baier,1976). SpecificrecommendationsbyNIOSHareshowninTable4. CurrentRecommendations Currentrecommendedregulationsregardingexposures ofworkersto 222 RnarelistedinTables5and6.The recommendationslistedinTable5areintendedtobe conservativelyprotective.Theselevelsareapplicableto caveworkers(e.g.,tourguides),butareoverlyrestrictive forinfrequentcaveexplorers.AccordingtoStrometal., (1996,p.5)(citingNCRP,1993,p.49)effectivedoseinthe workplaceshouldnotexceed5cSv(5rem)inanyoneyear with A ge 3 1cSvasalifetimelimit.IftheICRP(1994a) recommendationsareapplied,thenthetheNCRPrecommendationsconvertto5cSv(5rem)inanyoneyearwith A ge 3 7.08mJhm 3 or A ge 3 1cSvasalifetimelimit. Regulationsspecifictocaveworkers(andminers)are showninTable6.Thecaveworkerregulationswere developedandpublishedbyOSHA(OSHA,1988)and MineSafetyandHealthAdministration(MSHA)(MSHA, 1989).OSHAsetsanindividualexposurelimitequalto 14.0mJhm 3 20.0mSvyr 1 (4.0WLMyr 1 )(OSHA, Table3.Potential a -energyperatomandperunitactivity(modifiedfromICRP,1994a,p.3). Radionuclide Half-Life (min) Potential a -Energy perAtomperUnitofActivity, e p (MeV)(10 12 J)(MeVBq 1 )(10 10 JBq 1 ) 222 RnProgeny 218 Po3.0513.692.193,6155.79 214 Pb26.87.691.2317,84028.6 214 Bi19.97.691.2313,25021.2 214 Po2.73 3 10 6 7.691.232.0 3 10 3 3.0 3 10 6 Total(atequilibrium), perBqor 222 Rn 34,71055.6 M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 215

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1988,41CFR 57.5038).MSHAalsosetsamaximum cumulativedoseequalto14.0mJhm 3 20.0mSvyr 1 (4.0WLMyr 1 )(MSHA,1989,30CFRPart57). However,ICRP65wasalittlemorespecificinthatitset arecommendedeffectivedoseat14.0mJhm 3 20.0mSvyr 1 (4.0WLMyr 1 )averagedoverfiveyears and35.0mJhm 3 50.0mSvyr 1 (10.0WLMyr 1 )in anysingleyear(ICRP,1994a,p.21). Aleyetal.(2006)laysoutastrategyforreducingtotal a radiationexposuresofshow-caveemployeestoAsLow AsReasonablyAchievable(ALARA 14 )levels.Although notyetapprovedin2006,itislikelythatsomeformofthe strategywillbeapprovedbytheNationalCavesAssociationinwhicheachmemberwillberequiredtodevelop aCaveRadiationManagementPlanfollowingguidelines developedbyOSHA. D ETERMINING 222 R N R ISKSTO C AVERS Therisksposedbyexposuretoelevatedlevelsof 222 Rn gashavenotadequatelyaddressedexposurestorecreationalcaversandcaveworkers.Regulationsnotspecificto caveshavebeenpromulgated(e.g.,MSHA,2005, 57.5037– 57.5046)whileregulationsspecifictocaveshave beendeveloped(NPS,1980)andarebeingupdated(NPS, 2005).Theseregulationsgenerallyspecifyacceptable WorkingLevelsforindividuals,butnotexposurerates, absorbeddoses,oreffectivedoseswhicharenecessaryfor determiningrisks.However,becausehumanhealtheffects causedbyelevated 222 Rnconcentrationsarebasedon epidemiologicalstudiesofminerssubjectedtomuchhigher 222 Rnexposures(concentrationsandtimes)aswellas confoundingfactors(smoking,dust,etc.),riskestimatesfor caversandcaveworkersneedtobeestablishedusingthe linearno-thresholdtheory(LNT)eventhoughtheassociateduncertaintyinthecancerriskperunitdoseatlowdose anddoserateisdifficulttoquantify(Eckermanetal.,1999, p.11–12). A PPLICATIONOFTHE LNT TO 222 R NANDITS P ROGENY TheLNTforradiationcarcinogenesisisbasedonthe conceptthatallradiationdoses,nomatterhowsmall,can causecancer(i.e.,thereisnoacceptableradiationthreshold atwhichcancerswillnotbeinitiated).Accordingtothis Table4.RecommendedregulationsbyNIOSHforexposureofcaversto 222 Rndecayprogenyin1976(modifiedfrom Baier,1976). PAECLevel RecommendedRegulation ( Jm 3 )(WL) 2.08 0.1All-undergroundsmokingstopped 2.08–4.160.1–0.2Monitorworkspaceatleastquarterly 4.16 6.240.2–0.3Monitorworkspacequarterly 6.24 0.3Monitorworkspaceweeklyandmaintainexposurerecordsonallexposed employees 20.80 41.601.0–2.0ImmediatecorrectiveactiontolowerPAECbelow20.80 Jm 3 (1.0WL) 41.60 2.0WithdrawallworkersnotnecessarytolowerPAECbelow20.80 Jm 3 (1.0WL) Cumulativeindividualexposureshallnotexceed14.0mJhm 3 yr 1 (4.0WLMyr 1 ). Table5.RecommendedregulationsbyDOEforexposureto 222 Rn-decayprogenyin1996(modifiedfromStrometal.,1996, p.6). Country a PAECPAEE ( Jm 3 )(WL)(mJm 3 yr 1 )(mSvyr 1 )(WLMyr 1 ) UnitedStates6.93 14.020.04.0 Canada,France,GreatBritain8.320.416.824.04.8 ……17.525.05.0 b ……35.150.010.0 c ……35.150.010.0 d a TheUnitedStatesvaluesarebasedonU.S.EnvironmentalProtectionAgenc y(EPA),U.S.DepartmentofEnergy(DOE),andU.S.NuclearRegulatoryComm ission(NRC) regulations. b Valuesareforanysingleyear— A ge 3 3.54mJhm 3 ( A ge 3 1WLM). c Valuesareforanysingleyear— A ge 3 7.08mJhm 3 ( A ge 3 2WLM). d Valuesareforanysingleyear—14.0mJhm 3 yr 1 (4.0WLMyr 1 )averagedover5yr. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 216 N JournalofCaveandKarstStudies, April2007

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theorythen,ifexposureto1Gy(100rad)causesacancer risk R ,theriskfromexposureto10 2 Gy(1rad)is R /100, theriskfromexposureto10 5 Gy(1mrad)is R /10 5 ,and soon,whichmeansthatonlyazeroradiationdosewill resultinazeroriskofcancer(Cohen,2002). C ANCER R ISK M ODELINGFOREXPOSURETO 222 R NAND ITS P ROGENY Modelsintendedtoaddresscancerrisksfromexposure to 222 Rnanditsprogenyhaveevolvedovertheyears, althoughallhavefollowedtheLNT(Yuetal.,2006).The mostcurrentmodelwasdevelopedandpublishedin ICRP66(ICRP,1994b). HumanRespiratoryTractModelforEffectiveDose Estimation UsingtheprogramL UNGDOSE. F 90 (NikezicandYu, 2001)whichwasdevelopedaccordingtotheHuman RespiratoryTractModel(HRTM),anestimatedequilibriumfactor F equalto0.366wasobtained,whichclosely matchestheICRP65recommendedvalue( F 0.4)(ICRP, 1994a,p.5)andtheBEIRVIarithmeticaveragevalueof 0.408(Jamesetal.,2003).Anaverageinhalationrate I h 2.16 3 10 4 m 3 s 1 inaresidenceresultedinanestimated thoracicdose D T of79.20nSv(Bqhm 3 ) 1 (126.112 mSvWLM 1 ).Mostinterestingly,L UNGDOSE. F 90 resulted inanestimateforaDoseConversionFactor(DCF)equal to9.50nSv(Bqhm 3 ) 1 (15.13mSvWLM 1 )whichis considerablylargerthantheepidemiologicalestimate foraDCFequalto3.18nSv(Bqhm 3 ) 1 (5.06mSvWLM 1 )forworkersand2.44nSv(Bqh m 3 ) 1 (3.88mSvWLM 1 )forthepublic(ICRP,1994a, p.13).Thisdiscrepancyemphasizesthecomplexitiesand uncertaintieswhencalculatingrisksposedbyexposureto PAEC(Gourmelonetal.,2005,p.19). ThedifferencebetweentheL UNGDOSE. F 90 estimatefor aDCFequalto9.50nSv(Bqhm 3 ) 1 (15.13mSv WLM 1 )andtheICRP65estimateforaDCFequalto 3.18nSv(Bqhm 3 )(5.06mSvWLM 1 )isnotregarded assignificantlylargebecauseofthecomplexphysicaland biologicalissuesinvolvedandreasonablymatchesapreviouslyepidemiologically-estimatedvalueof9.0nSv(Bqh m 3 ) 1 (14.33mSvWLM 1 )(UNSCEAR,2000,p.107). Anevaluationofthediscrepancyhasresultedinthe suggestionthattheepidemiologically-basedestimatefor DCFwillneedtobeincreasedandthatfornow,thelarger DCFvalueestimateddosimetricallyusingtheHRTMis recommendedforuseinriskcalculations(UNSCEAR, 2000,p.107).However,othersfeelthattheepidemiologically-basedestimatesaremorescientificallysound(Neal Nelson, pers.comm. ). UsingthevaluesestimatedfromLungdose.F90developedbyNikezicandYu(2001)with I h 3.33 3 10 4 m 3 s 1 toaccountforacombinationofresting,lightand heavyexercise(Jamesetal.,2003)typicalofcaving,the 222 RnconcentrationslistedinTable1andEquation(9) (Wiegandetal.,1995) E DA C Rn FT i D CF 9 producedtheannualeffectivedoses E DA for 222 Rn exposurestorecreationalcavers(50hyr 1 ),professional cavers(600hyr 1 ),part-timecaveworkers(1,760h yr 1 ),andfull-timecaveworkers(2,000hyr 1 )(Table7). Realistically,thereisnoreliablewaytoestimatethe averagenumberofhoursexperiencedbyrecreational cavers,professionalcavers,andpart-timecaveworkers. Thenumberofcavinghoursperyearforcavers(50h yr 1 and600hyr 1 )areconsideredreasonableestimates. Part-timecaveworkerhoursequalto1,760hyr 1 was usedasanestimatebecausethisvalueisrecommendedfor Table6.PublishedregulationsbyOSHAandMSHAforexposureofcaversto 222 Rn-decayprogenyin1976(modifiedfrom ATSDR,1990,p.93–94). PAECLevelPAEELevel PublishedRegulationsReference ( Jm 3 )(WL)(mSvyr 1 )(WLMyr 1 ) ……20.04.0IndividualexposurelimitOSHA a 2.080.1……MonitorworkspaceatleastonceyearlyOSHA b 2.08–6.240.1–0.3……MonitorworkspacequarterlyOSHA c 6.24 0.3……Monitorworkspaceweeklyandmaintain exposurerecordsonallexposedemployees OSHA d 20.801.0……ImmediatecorrectiveactiontolowerPAECOSHA e 20.801.0……InstantaneousmaximumMSHA f ……20.04.0MaximalcumulativedoseMSHA f a (OSHA,1988,41CFR 57.5038). b (OSHA,1988,41CFR 57.5087). c (OSHA,1988,41CFR 57.5037). d (OSHA,1988,41CFR 57.5037). e (OSHA,1988,41CFR 57.5041). f (MSHA,1988,30CFRPart57). M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 217

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outsideexposurebyUNSCEAR(2000,p.107),even thoughUNSCEARrecommendedalargerequilibrium factorof(0.6)forexternalexposures,butwhichwasnot usedinthecalculationsbecauseitisnotappropriatefor caves. An I h 3.33 3 10 4 m 3 s 1 resultedinagreater D T and agreateroverall E DA forcaversandcaveworkersthan whenan I h 2.16 3 10 4 m 3 s 1 wasusedbecauseofthe muchgreaterbreathingactivity.Meanannualeffective doses E DA listedinTable7typicallyrangedfrommuchless (0.03mSvyr 1 )tomuchgreater(339.27mSvyr 1 )than therecommendedmaximumsof20to50mSvyr 1 Unfortunately,thegreatrangeofdataandvariability evidencedmakeitverydifficulttorealisticallyestimatethe risksposedtocaversandcaveworkersfromtheestimated E DA .However,itappearsfromTable7thatrecreational caversand,forthemostpart,professionalcaversarelikely tobeonlyminimallyexposedtoexcess 222 Rnconcentrationswhereascaveworkersshouldbemoreconcerned aboutexposuretoexcess 222 Rnconcentrationsforthefive countrieswithhighmean 222 Rnconcentrations(Great Britain,Greece,Japan,Switzerland,andtheUnitedStates) (Table7). Figures5–8illustratethethreattocaversandcave workersfromexposuretoelevatedlevelsof 222 Rngasin cavesrelativetoacceptablelimits.FromFigures5–8itis Table7.EstimatedannualeffectivedosesusingtheL UNGDOSE. F 90 program a forexposurestocaversandcaveworkersformean 222 RnconcentrationslistedinTable1.Superscriptnumbersnexttoeachentr ycorrespondtothex-axisonFigures5–8.Entries withoutasuperscriptwerenotplotted. Country RecreationalCaver b ProfessionalCaver c Part-TimeCaveWorker d Full-TimeCaveWorker e (mSvyr 1 )(WLMyr 1 )(mSvyr 1 )(WLMyr 1 )(mSvyr 1 )(WLMyr 1 )(mSvyr 1 )(WLMyr 1 ) 1 Australia 0.140.031.730.355.071.015.771.15 2 China f 0.030.010.400.081.170.231.330.27 3 CzechRepublic 0.290.063.500.7010.272.0511.672.33 4 GreatBritain 0.690.148.241.6524.184.8427.485.50 GreatBritain… ………………… 5 GreatBritain 8.481.70101.7720.35298.5359.71339.2467.85 6 GreatBritain 2.200.4426.395.2877.4115.4887.9617.59 7 GreatBritain 0.090.021.040.213.040.613.450.69 8 GreatBritain 0.070.010.890.182.620.522.980.60 9 Greece 5.951.1971.4014.28209.4441.89238.0047.60 10 Hungary 0.780.169.361.8727.455.4931.196.24 11 Hungary 0.580.127.001.4020.534.1123.334.67 12 Ireland 0.980.2011.702.3434.336.8739.017.80 13 Japan 0.01 0.010.030.010.090.020.100.02 14 Malaysia 0.140.031.690.344.960.995.631.13 15 Poland 0.280.063.310.669.701.9411.022.20 16 Russia 0.560.116.781.3619.883.9822.594.52 17 Slovenia 0.330.074.000.8011.752.3513.352.67 18 Slovenia 0.230.052.740.558.031.619.121.82 19 Spain 0.030.010.310.060.900.181.020.20 20 Spain 0.840.1710.112.0229.655.9333.696.74 21 SouthAfrica 0.060.010760.152.220.442.520.50 22 Switzerland 5.911.1870.8914.18207.9541.59236.3147.26 23 UnitedStates 0.460.095.461.0916.033.2118.213.64 24 UnitedStates 0.610.127.341.4721.544.3124.474.89 25 UnitedStates 0.350.074.180.8412.272.4513.942.79 UnitedStates… ………………… 26 UnitedStates 2.760.5533.126.6297.1419.43110.3822.08 a Lungdose.F90program(NikezikandYu,2001)estimateforDCF 12.92nSv(Bqhm 3 ) 1 (20.75mSvWLM 1 )and D T 107.63nSv(Bqhm 3 ) 1 (171.38mSvWLM 1 ) for I h 3.33 3 10 4 m 3 s 1 b Recreationalcavers 50hyr 1 ofcaving. c Professionalcavers 600hyr 1 ofcaving. d Part-timecaveworker 1,760hyr 1 ofcavework. e Full-timecaveworker 2,000hyr 1 ofcavework. f Themeasured 222 RnconcentrationsfortheChinadatalistedinTable1arebetterrepresent edby7,000hyr 1 exposurewithan I h 2.16 3 10 4 m 3 s 1 becausethesedataare fromcavedwellingsresultinginan E DA 3.43mSvyr 1 (0.69WLMyr 1 ). R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 218 N JournalofCaveandKarstStudies, April2007

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apparentthatcaversaregenerallynotatriskwhilecave workersappeartobeminimallyatrisk. Aseriesofnotchedboxplots(seeChambersetal.,1983, foradescriptionofnotchedboxplots)usingthedatalisted inTable7andshowninFigure9furtherdemonstratethat onlycaveworkerswillbeminimallyimpactedatthelower E DA limitof20mSvyr 1 (4WLMyr 1 ).However,the medianlineofeachnotchedboxplotforthepart-timeand full-timecaveworkersarealsobelowtheminimum acceptablelimitforexposure,suggestingthatneitherthe part-timenorthefull-timecaveworkersareimpactedat thelower E DA limit,andonlythethemoreextremevalues Figure5.Plotofmean,minimum,andmaximumannual effectivedosevaluesforrecreationalcaversfromTable7 relativetopublishedacceptablelimitsof20 50mSvyr 1 (4 10WLMyr 1 ).Thex-axisnumericalvaluescorrespond tothesuperscriptlabelsinTable7.(Notethatdatasets listedinTable7missingmeanvalues[GreatBritainand UnitedStates]arenotplotted). Figure6.Plotofmean,minimum,andmaximumannual effectivedosevaluesforprofessionalcaversfromTable7 relativetopublishedacceptablelimitsof20–50mSvyr 1 (4–10WLMyr 1 ).Thex-axisnumericalvaluescorrespond tothesuperscriptlabelsinTable7.(Notethatdatasets listedinTable7missingmeanvalues[GreatBritainand UnitedStates]arenotplotted). Figure7.Plotofmean,minimum,andmaximumannual effectivedosevaluesforpart-timecaveworkersfromTable7 relativetopublishedacceptablelimitsof20–50mSvyr 1 (4– 10WLMyr 1 ).Thex-axisnumericalvaluescorrespondto thesuperscriptlabelsinTable7.(Notethatdatasetslistedin Table7missingmeanvalues[GreatBritainandUnited States]arenotplotted). Figure8.Plotofmean,minimum,andmaximumannual effectivedosevaluesforfull-timecaveworkersfromTable7 relativetopublishedacceptablelimitsof20–50mSvyr 1 (4– 10WLMyr 1 ).Thex-axisnumericalvaluescorrespondto thesuperscriptlabelsinTable7.(Notethatdatasetslistedin Table7missingmeanvalues[GreatBritainandUnited States]arenotplotted). M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 219

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(i.e., 90thpercentile)exceedthe50mSvyr 1 (10WLM yr 1 )limit. ExposureofCaversto 222 RnanditsProgeny. Exposureof caveworkersandcaversto 222 Rnanditsprogenyis obtainedfrom(Eckermanetal.,1999,p.F4) P eq t C i t 0 e ln2 t T 1 2 10 whichconsidersthedecayseriesof 222 Rnthroughits progeny,ofwhichonlytheprincipalprogenyidentifiedin Figure1areusedinthecalculations.Eachprogeny concentrationisestimatedfromtheconcentrationofits respectiveparent.Accordingtothenucleardecaydata listedinEckermanetal.(1999,p.G19–G20),each radionuclideforthe 222 Rndecayseriesdecaystobetween 99.98%and100%toitsprincipalprogeny(e.g.,99.98%of 218 Podecayresultsin 214 Pb)(Table8),whichrenders insignificanttheotherprogenyshowninFigure1(e.g., 218 ATand 218 Rn). ApplyingEquation(10)allowsforexposuresto caversfrom 222 Rnanditsprogenytobeestimatedfrom the 222 RnconcentrationslistedinTable1.Estimated exposuresarelistedinTable9,whereitmaybenotedthat thesmallestestimatedexposureisproducedby 214 Po.This appearscontrarytothenotionthattheveryshorthalflife of 214 Po( T 164 s)willresultinthegreatestlungdoses because 214 Powilllikelyemitan a -particlebeforeitcanbe exhaled.Polonium-214decaysonlyonce,butisinsecular equilibriumwithitsparentradionuclide 214 Bi.However, 214 Pohasthegreatestnumberofdecaysperunitintakeof 222 Rninequilibriumwithitsprogeny.Itshalflife, therefore,isnotafactor(N.Nelson,pers.comm.). RiskstoCaversfromExposureto 222 RnanditsProgeny. Riskstocaveworkersandcaversneedtobeestimatedfrom theexposureslistedinTable9andriskcoefficients determinedfromepidemiologicalstudieswhenavailable. Risksincludebothmortalityandmorbidity. Therisksofmortality(cancerdeath)andmorbidity (cancerwithorwithoutdeath)fromexposureto 222 Rnandits progenyareestimatedfrom(Eckermanetal.,1999,p.F-8) R M i P eq i S C I h M R i 11 whereascalingcoefficient S C of1.11forinhalationwas consideredappropriate(Eckermanetal.,1999,p.E-5)and thevaluesforthemortality 15 andmorbidity 16 riskcoefficients M R i arelistedinTable10. TheEPAestimatesmortalityrisksfromexposureto 222 Rn gasasafunctionofWLM;specifically,EPAexpects5.4 3 10 – 4 lungcancerdeathsperWLM.Thismethodologywasnot usedherebecausetheWLMdoesnotaccountforsuchfactors asbreathingrates,tidalvolumes,orthefractionofprogeny unattachedtoaerosols,whichmodifytherelationship betweenexposureandrisk(Cothern,1987,p.26). Morbidityriskstocaversandcaveworkerscannotbe directlycalculatedbecausetherelevantmorbidityrisk coefficientsexistonlyfor 214 Pband 214 Bi(Table10).The differencebetweenthemortalityandmorbiditycoefficients for 214 Pband 214 Biarerelativelyinsignificant,butthesame cannotbesaidfortheotherradionuclideslistedinTable10.Ingeneral,itisreasonabletoexpectthat theriskofmorbiditytocaversandcaveworkerswillbe somewhatgreaterthanistheestimatedriskformortality. Inordertodeveloparoughestimatefortheriskof morbidityforcaversandcaveworkers,thevaluesforthe Figure9.Notchedboxplotsofestimatedannualeffective dosesrelativetoacceptablelimits.(Notethatdatasetslisted inTable7missingmeanvalues[GreatBritainandUnited States]arenotplotted). Table8.Nucleardecayproductsandfractionsfor 222 Rnanditsprogeny(modifiedfromEckermanetal.,1999,p.G19–G20). Radionuclude T Decay Mode RadioactiveDecayProductsandFractionalYield RadionuclideFractionRadionuclideFraction 222 Rn3.8325d a 218 Po1.0000…… 218 Po3.05min ab 214 Pb0.9998 218 At0.0002 214 Pb26.8min b 214 Bi1.0000…… 214 Bi19.9min ab 214 Po0.9998 210 Tl0.0002 214 Po164.3 s a 210 Pb1.0000…… R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 220 N JournalofCaveandKarstStudies, April2007

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morbidityriskcoefficient M R B for 214 Pband 214 Biwere takenfromTable10.Fortheotherradionuclides,the mortalityriskcoefficients M R T listedinTable10were increasedbyafactorof1.5ontheassumptionthatsuchan increasewillreasonablyrepresentamorbidityriskcoefficient M R B forthoseradionuclidesforwhichmorbidity riskcoefficientsarenotyetavailable. Mortalityandmorbidityrisks(Table11)wereaveraged overallagesandbothgendersforapopulationwith specifiedmortalityandmorbidityforthemeanexposures listedinTable9.Themeanrisksofmortalityand morbidityrangedfrom10 5 (1in100,000)to10 7 (1in 10,000,000)where10 6 (1in1,000,000)isusually consideredanacceptablerisk. Thesignificanceofthemortalityandmorbidityinhalationrisksposedtocaversandcaveworkersisshownin Figures10and11.ItwillbenotedfromFigures10and11 thatthemajorityofthemeanvaluesareveryclosetothe 10 6 acceptablerisklevel,butthemaximummeasured risksappearconsiderablygreaterthanthe10 6 acceptable risklevel.Onlydatasetsrepresentedbynumbers5(Great Britain),6(GreatBritain),9(Greece),22(Switzerland), and26(UnitedStates)exhibitedmeanvaluessubstantially greaterthanthe10 6 acceptablerisklevel. Table9.Estimatedtime-integratedconcentrationexposuresto 222 Rnanditsprogenyforcaversforthemean 222 Rn concentrationslistedinTable1 a Country InhalationExposure 222 Rn 218 Po 214 PbZ 14 Bi 214 Po (Bqs 1 m 3 )(Bqs 1 m 3 )(Bqs 1 m 3 )(Bqs 1 m 3 )(Bqs 1 m 3 ) Australia4.82 3 10 7 3.35 3 10 4 3.35 3 10 4 3.35 3 10 4 5.58 3 10 4 China1.11 3 10 7 7.74 3 10 3 7.74 3 10 3 7.74 3 10 3 1.29 3 10 4 CzechRepublic9.76 3 10 7 6.78 3 10 4 6.78 3 10 4 6.78 3 10 4 1.13 3 10 3 GreatBritain2.30 3 10 8 1.60 3 10 5 1.59 3 10 5 1.59 3 10 5 2.66 3 10 3 GreatBritainÂ…Â…Â…Â…Â… GreatBritain2.84 3 10 9 1.97 3 10 6 1.97 3 10 6 1.97 3 10 6 3.28 3 10 2 GreatBritain7.35 3 10 8 5.11 3 10 5 5.11 3 10 5 5.11 3 10 5 8.51 3 10 3 GreatBritain2.88 3 10 7 2.00 3 10 4 2.00 3 10 4 2.00 3 10 4 3.34 3 10 4 GreatBritain2.49 3 10 7 1.73 3 10 4 1.73 3 10 4 1.73 3 10 4 2.88 3 10 4 Greece1.99 3 10 9 1.38 3 10 6 1.38 3 10 6 1.38 3 10 6 2.30 3 10 2 Hungary2.61 3 10 8 1.81 3 10 5 1.81 3 10 5 1.81 3 10 5 3.02 3 10 3 Hungary1.95 3 10 8 1.35 3 10 5 1.35 3 10 5 1.35 3 10 5 2.26 3 10 3 Ireland3.26 3 10 8 2.26 3 10 5 2.26 3 10 5 2.26 3 10 5 3.77 3 10 3 Japan8.69 3 10 5 6.04 3 10 2 6.04 3 10 2 6.04 3 10 2 1.01 3 10 5 Malaysia4.71 3 10 7 3.27 3 10 4 3.27 3 10 4 3.27 3 10 4 5.45 3 10 4 Poland9.21 3 10 7 6.40 3 10 4 6.40 3 10 4 6.40 3 10 4 1.07 3 10 3 Russia1.89 3 10 8 1.31 3 10 5 1.31 3 10 5 1.31 3 10 5 2.19 3 10 3 Slovenia1.12 3 10 8 7.75 3 10 4 7.75 3 10 4 7.75 3 10 4 1.29 3 10 3 Slovenia7.63 3 10 7 5.30 3 10 4 5.29 3 10 4 5.29 3 10 4 8.82 3 10 4 Spain8.53 3 10 6 5.93 3 10 3 5.93 3 10 3 5.93 3 10 3 9.87 3 10 5 Spain2.82 3 10 8 1.96 3 10 5 1.96 3 10 5 1.96 3 10 5 3.26 3 10 3 SouthAfrica2.11 3 10 7 1.47 3 10 4 1.46 3 10 4 1.46 3 10 4 2.44 3 10 4 Switzerland1.98 3 10 9 1.37 3 10 6 1.37 3 10 6 1.37 3 10 6 2.29 3 10 2 UnitedStates1.52 3 10 8 1.06 3 10 5 1.06 3 10 5 1.06 3 10 5 1.76 3 10 3 UnitedStates2.05 3 10 8 1.42 3 10 5 1.42 3 10 5 1.42 3 10 5 2.37 3 10 3 UnitedStates1.17 3 10 8 8.09 3 10 4 8.09 3 10 4 8.09 3 10 4 1.35 3 10 3 UnitedStatesÂ…Â…Â…Â…Â… UnitedStates9.23 3 10 8 6.41 3 10 5 6.41 3 10 5 6.41 3 10 5 1.07 3 10 2 a Onlythemeantime-integratedconcentrationexposuresareshownhere.Ma ximumandminimumexposurevalueswerecalculatedfromthemaximumandmin imum 222 Rn concentrationslistedinTable1butarenotshownhereduetospacelimitat ions. Table10.Mortalityandmorbidityriskcoefficientsfor 222 Rn anditsprogeny. Radionuclide RiskCoefficients MotalityMorbidity (Bq 1 )(Bq 1 ) 222 Rn a 3.21 3 10 11 Â… 218 Po a 9.44 3 10 11 Â… 214 Pb b 9.31 3 10 10 9.81 3 10 10 214 Bi c 7.45 3 10 10 7.84 3 10 10 214 Po a 7.12 3 10 17 Â… a Riskcoefficientssource:PuskinandNelson(1994,p.53). b Riskcoefficientssource:Eckermanetal.(1999,p.71). c Riskcoefficientssource:Eckermanetal.(1999,p.72). M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 221

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Figure12showsasetofnotchedboxplotsforthe mortalityandmorbidityinhalationrisks.FromFigure12 itcanbeseenthatthemedianmeasureofthemeanrisk valuesisonlyslightlygreaterthanthe10 6 acceptablerisk level,butthenotchesextendtothe10 6 acceptablerisk level,suggestingthattheoverallrisksmaybeacceptable. However,inindividualcavesandlocationswithincertain caves,risksmaybesignificant,asevidencedbythefactthat the75thpercentile,the90thpercentile,andvariousoutliers extendwellbeyondthe10 6 acceptablerisklevel. D ISCUSSIONAND C ONCLUSIONS Attemptshavebeenmadetoregulateexposuresto caversandcaveworkerstoexcesslevelsof 222 Rngasin caveseversincehighlevelsof 222 Rngaswerediscoveredin somecavesadministeredbytheNPS(Yarboroughand Meyers,1978,p.19).Protectionlevelsforcaveworkers wereimplementedattheearliestpossibletime(Baier,1976) andhavecontinuedtoevolveasmoreislearned.Unfortunately,littleisstillknownabouttheeffectsoflowlevelionizing a radiationfrom 222 Rnanditsprogeny.Still, itiswidelyrecognizedthatthedevelopmentoflungcancers maybeexpectedbasedonnumerousanimalstudiesand epidemiologicalstudiesofminers. Measuring 222 Rnisoflittlevalueunlesstheseconcentrationsareconvertedtoriskestimates.Calculatingannual effectivedoses(mSvyr 1 orWLMyr 1 )isthegenerally acceptedmethodfordetermininghuman-healththreats. Usingappropriatelimits(20mSvyr 1 to50mSvyr 1 ) helpstoputthecalculatedvaluesinahealth-riskcontext. Ingeneral,itwouldseemthatrecreationalandprofessionalcaversareminimallyatriskofdevelopinglung cancersfromexposureto 222 Rn,part-timecaveworkersare Table11.Inhalationrisksfrom 222 Rnanditsprogenyforexposurestocaversandcaveworkersforthe 222 Rnconcentrations listedinTable1.Superscriptnumbersnexttoeachentrycorrespondstoth ex-axisonFigures10and11.Entrieswithout asuperscriptwerenotplotted. Country InhalationMotalityRiskInhalationMorbidityRisk MeanMaximumMinimumMeanMaximumMinimum 1 Australia5.9 3 10 7 3.9 3 10 6 8.8 3 10 9 8.8 3 10 7 5.9 3 10 6 1.3 3 10 8 2 China1.4 3 10 7 2.7 3 10 7 3.7 3 10 8 2.0 3 10 7 4.0 3 10 7 5.5 3 10 8 3 CzechRepublic1.2 3 10 6 2.0 3 10 5 1.9 3 10 7 1.8 3 10 6 3.0 3 10 5 2.9 3 10 7 4 GreatBritain2.8 3 10 6 4.5 3 10 5 9.7 3 10 9 4.2 3 10 6 6.7 3 10 5 1.4 3 10 8 GreatBritainÂ…1.5 3 10 4 9.7 3 10 8 Â…2.2 3 10 4 1.4 3 10 7 5 GreatBritain3.5 3 10 5 1.5 3 10 4 7.2 3 10 6 5.2 3 10 5 2.2 3 10 4 1.1 3 10 5 6 GreatBritain9.1 3 10 6 1.2 3 10 5 6.6 3 10 8 1.3 3 10 5 1.8 3 10 5 9.8 3 10 8 7 GreatBritain3.6 3 10 7 3.1 3 10 6 2.5 3 10 8 5.3 3 10 7 4.6 3 10 6 3.8 3 10 8 8 GreatBritain3.1 3 10 7 3.0 3 10 6 3.3 3 10 8 4.6 3 10 7 4.4 3 10 6 4.9 3 10 8 9 Greece2.5 3 10 5 8.6 3 10 5 1.8 3 10 7 3.6 3 10 5 1.3 3 10 4 2.7 3 10 7 10 Hungary3.2 3 10 6 1.4 3 10 5 4.9 3 10 7 4.8 3 10 6 2.0 3 10 5 7.2 3 10 7 11 Hungary2.4 3 10 6 1.3 3 10 5 1.9 3 10 7 3.6 3 10 6 1.9 3 10 5 2.9 3 10 7 12 Ireland4.0 3 10 6 7.7 3 10 6 1.9 3 10 7 6.0 3 10 6 1.1 3 10 5 2.9 3 10 7 13 Japan1.1 3 10 5 1.9 3 10 8 7.2 3 10 10 1.6 3 10 8 2.9 3 10 8 1.1 3 10 9 14 Malaysia5.8 3 10 7 1.9 3 10 6 9.7 3 10 8 8.6 3 10 7 2.9 3 10 6 1.4 3 10 7 15 Poland1.1 3 10 6 4.1 3 10 6 5.8 3 10 8 1.7 3 10 6 6.0 3 10 6 8.7 3 10 8 16 Russia2.3 3 10 6 8.3 3 10 6 3.6 3 10 7 3.5 3 10 6 1.2 3 10 5 5.4 3 10 7 17 Slovenia1.4 3 10 6 7.0 3 10 6 1.5 3 10 8 2.0 3 10 6 1.0 3 10 5 2.2 3 10 8 18 Slovenia9.4 3 10 7 5.8 3 10 6 5.8 3 10 8 1.4 3 10 6 8.6 3 10 6 8.7 3 10 8 19 Spain1.1 3 10 7 4.8 3 10 7 4.9 3 10 9 1.6 3 10 7 7.1 3 10 7 7.2 3 10 9 20 Spain3.5 3 10 6 6.9 3 10 6 1.8 3 10 7 5.2 3 10 6 1.0 3 10 5 2.7 3 10 7 21 SouthAfrica2.6 3 10 7 2.3 3 10 6 2.9 3 10 9 3.9 3 10 7 3.4 3 10 6 4.3 3 10 9 22 Switzerland2.4 3 10 5 3.9 3 10 5 1.9 3 10 6 3.6 3 10 5 5.8 3 10 5 2.9 3 10 6 23 UnitedStates1.9 3 10 6 9.1 3 10 6 3.6 3 10 8 2.8 3 10 6 1.4 3 10 5 5.4 3 10 8 24 UnitedStates2.5 3 10 6 9.2 3 10 6 3.6 3 10 7 3.7 3 10 6 1.4 3 10 5 5.4 3 10 7 25 UnitedStates1.4 3 10 6 2.3 3 10 6 7.3 3 10 7 2.1 3 10 6 3.4 3 10 6 1.1 3 10 6 UnitedStatesÂ…1.8 3 10 6 3.2 3 10 7 Â…2.7 3 10 6 4.8 3 10 7 26 UnitedStates1.1 3 10 5 8.0 3 10 5 1.1 3 10 8 1.7 3 10 5 1.2 3 10 4 1.6 3 10 8 Riskswereestimatedforthemean,maximum,andminimum 222 RnconcentrationslistedinTable1eventhoughexposuresforthemaximuma ndminimum 222 Rn concentrationsarenotshowninTable9. LabelnumbersrefertodatapositioninFigures10and11. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 222 N JournalofCaveandKarstStudies, April2007

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somewhatmoreatriskinsomecaves,andfull-timecave workersmoreso(Table7).Thisconclusionwassimilarly obtainedbyCravenandSmit(2006)fornon-smokers. Unfortunately,thelargedegreeofuncertaintyassociated withthecalculationsandpotentialdiscrepanciesinthe 222 Rnmeasurements,necessitatethatthecalculationslisted inTable7beviewedwithsomedegreeofskepticism(itis notpossibletodetermineifthecalculatedannualeffective dosesinTable7aretoohighortooloworbyhowmuch). However,theannualeffectivedoseslistedinTable7 shouldstillbeviewedasrepresentativeofthepotential riskscaversandcaveworkersmightbesubjecttowhen spendinganysignificantamountoftimeunderground. Alesscommonmethodofcalculatingrisksposedby low-levelionizing a radiationfrom 222 Rnanditsprogeny, butwhichisamoretypicalmethodofcalculatingrisksin general,istousecancerslopefactors(mortalityand morbidityriskcoefficients M R i )toproducedimensionless riskestimates.Themortalityandmorbidityriskestimates listedinTable11forthe 222 Rnconcentrationslistedin Table1areofnegligibleconcern. Forshort-termexposures,typicalofrecreationalcavers, therisklevelslistedinTable11forthemean 222 Rn concentrationsareprobablyoflittleconcern.Thesameis probablytrueforprofessionalcavers.However,forlongtermexposures,typicalofcaveworkers,theserisklevels warrantsomedegreeofminorconcernespeciallyinareas ofpoorventilation(Kobaletal.,1988).Ifthemaximum 222 RnconcentrationslistedinTable1areconsidered,the riskswillincreaseslightly,whichmaywarrantagreater concern. Overall,itappearsthatriskstocaversandcaveworkers aregenerallylow,butinselectedcavesriskstocave workersmaybesignificant.However,propercaveworker precautionsforcaveswithelevated 222 Rnconcentrations willminimizetherisks.Inaddition,giventheuncertainties associatedwithuseoftheLNT,concernsoverriskstocave workersmayneedtodependontheeventualimprovements orabandonmentoftheLNT.ChangestotheLNTmay resultinareductionorincreaseintheestimatedrisksto caversandcaveworkersfromexposuretoelevatedlevelsof 222 Rn.Otheruncertainties,suchasextremeseasonal Figure10.Plotofmean,minimum,andmaximummortality riskvaluesfromTable11relativetoa10 6 acceptablerisk. Thex-axisnumericalvaluescorrespondtothesuperscript labelsinTable11.(NotethatdatasetslistedinTable11 missingmeanvalues[GreatBritainandUnitedStates]are notplotted). Figure11.Plotofmean,minimum,andmaximummorbidityriskvaluesfromTable11relativetoa10 6 acceptable risk.Thex-axisnumericalvaluescorrespondtothe superscriptlabelsinTable11.(Notethatdatasetslistedin Table11missingmeanvalues[GreatBritainandUnited States]arenotplotted). Figure12.Notchedboxplotsofestimatedmortalityand morbidityrisksrelativetoa10 6 acceptablerisk.(Notethat datasetslistedinTable11missingmeanvalues[Great BritainandUnitedStates]arenotplotted). M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 223

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variationsinmeasured 222 Rnconcentrations(Yarborough andMeyers,1978,p.22)[e.g.740versus22,165Bqm 3 in MagicGarden,PostojnaCave(Kobaletal.,1988)],further complicateriskcalculations. A PPENDIX R ADON -222P ROGENYAND H ISTORIC N AMES Whenfirstdiscovered,thecurrent 222 Rnprogenywere knownasdecayproductsof 226 Raandwereformerly designatedasRadiumA–RadiumF.The 222 Rnprogeny arenowknowntobetheisotopeslistedinTable12. R ADIATION SIU NITSAND C ONVERSIONTO T RADITIONAL U NITS Radiationunitshaveevolvedovertheyears.Asaresult, radiationunitscanbequiteconfusing.Toalleviatesomeof theconfusion,selectedradiationparametersareidentified inTable13alongwiththeSIspecialname,symbol,SI derivedunits,andtraditionalunits. A CKNOWLEDGMENTS TheauthorwouldliketothankDr.DragoslavNikesicfor providingmewithhisprogramL UNGDOSE. F 90 afterconvertTable12. 222 Rnprogenycurrentandhistoricnames. CurrentHistoric SymbolNameSymbolName 218 PoPolonium-218RaARadiumA 214 PbLead-214RaBRadiumB 214 BiBismouth-214RaCRadiumC 214 PoPolonium-214RaC RadiumC 210 TlThallium-210RaC RadiumC 210 PbLead-210RaDRadiumD 210 BiBismuth-210RaERadiumE 210 PoPolonium-210RaFRadiumF Table13.InternationalSystem(SI)unitsandequivalentsfortraditiona lunits(modifiedfromTaylor,2001,1995;Nero,1988, p.39). Parameter SIDerivedUnit ConversionfortraditionalUnit Special Name Special Symbol Expressedin Termsof OtherSIUnits Expressedin TermsofSI BaseUnits ActivitybecquerelBqs 1 1Ci 3.7 3 10 10 Bq(1pCi 0.037Bq) ConcentrationBqm 3 1pCiL 1 37Bqm 3 PAEC a Jm 3 1WL 1.3 3 10 8 MeVm 3 2.08 3 10 5 Jm 3 EEDC b Bqm 3 1WLPAEC 3740Bqm 3 ExposureJsm 3 1WLM 12.97Jsm 3 3.60 3 10 3 Jhm 3 ExposureBqsm 3 1WLM 73.9Bqyrm 3 ExposureRateJm 3 1WLMyr 1 4.11 3 10 7 Jm 3 ExposureRateBqm 3 1WLMyr 1 73.9Bqm 3 AbsorbedDosegrayGyJkg 1 m 2 s 2 1rad 1cGy 10 2 Gy AbsorbedDoseRateGys 1 m 2 s 2 1rads 1 10 2 Gys 1 DoseEquivalent c sievertSvJkg 1 m 2 s 2 1rem 1cSv 10 2 Sv 10 2 J kg 1 EffectiveDoseJsm 3 1WLMyr 1 5mSvyr 1 a PotentialAlpha-EnergyConcentration(PAEC). b Equilibrium-EquivalentDecay-ProductConcentration(EEDC). c AlsoknownasBiologicallyEffectiveDose. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 224 N JournalofCaveandKarstStudies, April2007

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ingrelevantportionstoEnglish.Thisprogramhasbeen essentialtotheunderstandingof 222 Rnriskstocavers.The authorwouldalsoliketothankMs.LindseyBenderandDr. NealNelsonoftheU.S.EnvironmentalProtectionAgency’s OfficeofRadiationandIndoorAirfortheirsupportand guidanceandforprovidingspecificradiationriskguidance materials.Lastly,theauthorthanksDr.NealNelsonandDr. IvanKobaloftheJoz efStefanInstitute(Ljubljana,Slovenia) fortheircriticalreadingofthemanuscript. N OTATION A ge ageofanexposedindividual(dimen.) C eq EEDC— 222 Rnconcentrationthatwouldresult if F 1 C E cumulativeexposure(Jhm 3 ) C i activityconcentrationsfor 222 Rnanditsprogeny(Bqm 3 ) C p PAEC—total a -particleenergypotentially emittedbyanymixtureof 222 Rnperunitvolume ofair(Jm 3 ) ( C R n ) i averageconcentrationof 222 Rndecayproducts duringexposureinterval(Jm 3 ) C Rn 222 Rnconcentration(Bqm 3 ) D CF DoseConversionFactor D T,R meanabsorbedradiationdosetotissue T from radiation R (Gy) E DA annualeffectiveradiationdosetoorgansand tissues(Svyr 1 ) E D effectiveradiationdosetoorgansandtissues (Sv) F equilibriumfactor(dimen.) H T humanequivalentradiationdosetotissue T (Sv) I h inhalationrate(m 3 s 1 ) M R B morbidity-riskcoefficientfor 222 Rnandits progeny(Bq 1 ) M R T mortality-riskcoefficientfor 222 Rnandits progeny(Bq 1 ) P eq EEQ—time-integratedexposuretoEEDC(Bq s 1 m 3 ) P p PAEE—time-integratedexposuretoPAEC(Js m 3 ) R risk R M B riskofmorbidity(dimen.) R M T riskofmortality(dimen.) S C scalingcoefficientforacurrent(mobile)populationtoastationarypopulation(dimen.) t time(T) T i exposuretime—subscript i referstoexposure forpart-timecavers(50hyr 1 ),full-timecavers (600hyr 1 ),part-timecaveworkers(1,760h yr 1 ),andfull-timecaveworkers(2,000hyr 1 ) (hyr 1 ) T radioactivehalf-lifeofconsideredradionuclide (T) W R radiationweightingfactorforvarioustypesof radiation(dimen.) W T i tissueweightingfactorfordifferingsensitivities ofvarioushumantissuestoradiations(dimen.) e p potentialalphaenergyperunitofactivity(Bq) l r decayconstantforconsideredradionuclide(dimen.) A CRONYMS DCFDoseConversionFactor DNADeoxyribonucleicAcid DOEU.S.DepartmentofEnergy EEDCEquilibrium-EquivalentDecay-ProductConcentration EEQEquilibriumEquivalentExposure EPAU.S.EnvironmentalProtectionAgency HRTMHumanRespiratoryTractModel LD50MedianLethalDose LETlinearenergytransfer LNTlinearno-thresholdtheory LOAELLowestObservedAdverseEffectLevel MSHAMineSafetyandHealthAdministration NIOSHNationalInstituteofOccupationalSafetyand Health NOAELNoObservedAdverseEffectLevel NPSNationalParkService NRCU.S.NuclearRegulatoryCommission OSHAOccupationalSafetyandHealthAdministration PAECPotentialAlpha-EnergyConcentration PAEEPotentialAlpha-EnergyExposure N OTES 1 Ametalloidisanelementwithpropertiesintermediatebetweenthose ofmetalsandnonmetals. 2 Clathratecompoundsareformedbytrappingthe 222 Rninthelattice ofsurroundingatomsratherthanformingchemicalbonds. 3 SeeTable13intheAppendixforabriefoverviewofradiationSI unitsandconversiontotraditionalunits. 4 Thelinearenergytransfer(LET)ofradiationisameasureofthe spatialenergydistributionstatedintermsoftheamountofenergydeposi ted perunitlengthofparticletrack, dE / dx ,withtypicalunitsofkeV m 1 (NRC,1990,p.11).Itistheenergylostbychargedparticlesinelectronic collisionsperunittracklengthwherealow-LETistakenas 10keV m 1 andahigh-LETistakenas 10keV m 1 (NRC,2005,p.375). 5 Inradiationbiology,dosespecificallypertainstotheamountofenergy ionizingradiationdepositsinanorgantissue(ATSDR,1997,p.35). 6 Effectivedose(Sv)convertstoabsorbeddose(Gy)accordingto1Sv 1Gy 3 W R 7 Theterm‘‘plate-out’’referstotheattractionofthenegatively chargediontosurfacessuchasacavewallortheepitheliumofthelung. 8 Invitro referstothetechniqueofperformingexperimentsinatest tubeorinalivingorganism. 9 Invivo referstoexperimentsconductedonlivingtissueofawhole livingorganismasopposedtoapartialordeadorganism. 10 Phagocytizedreferstotheingestionofparticlesororganismsby phagocytosis. 11 Thereticuloendothelialsystemconsistsofagroupofcellscapableof phagocytosis. 12 Parenteraladministrationreferstotherouteofparticleadministration(transport)throughthebody. M ALCOLM S.F IELD JournalofCaveandKarstStudies, April2007 N 225

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13 Confoundingfactorsareassociatedwiththefindingofan associationforthewrongreason.Itisassociatedwithboththeriskand thediseasebeingstudied,butneednotbeariskfactorforthedisease understudy.Theconfoundingvariablecaneitherinflateordeflatethetr ue relativerisk(Wartenbergetal.,2000). 14 ALARAmeansmakingeveryreasonableefforttomaintain exposurestoradiationasfarbelowthedoselimitsinthispartasis practicalconsistentwiththepurposeforwhichthelicensedactivityis undertaken,takingintoaccountthestateoftechnology,theeconomicsof improvementsinrelationtostateoftechnology,theeconomicsof improvementsinrelationtobenefitstothepublichealthandsafety,and othersocietalandsocioeconomicconsiderations,andinrelationto utilizationofnuclearenergyandlicensedmaterialsinthepublicintere st (U.S.NRC,2006,10CER,2006,10CFR 20.1003). 15 ‘‘Amortalityriskcoefficientisanestimateoftherisktoanaverage memberoftheU.S.population, perunitactivityinhaledoringestedfor internalexposuresorperunittime-integratedactivityconcentrationi nairor soilforexternalexposures ,ofdyingfromcancerasaresultofintakeofthe radionuclideorexternalexposuretoitsemittedradiations’’(Eckerman et al.,1999,p.1). 16 ‘‘Amorbidityriskcoefficientisacomparableestimate[mortality estimate]oftheaveragetotalriskofexperiencingaradiogeniccancer, whetherornotthecancerisfatal’’(Eckermanetal.,1999,p.1). 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Yarborough,K.,1976,Investigationofradiationproducedbyradonand thoroninnaturalcavesadministeredbytheNationalParkService, in Aley,T.,andRhodes,D.,eds.,ProceedingsoftheNationalCave ManagementSymposium:Albuquerque,N.M.,Speleobooks,p.59–69. Yarborough,K.,andMeyers,C.,1978,Sputumcytologyandpersonnel exposuresatNationalParkServiceadministeredcaves, in Conference/ WorkshoponLungCancerEpidemiology&IndustrialApplicationsof SputumCytology,Golden,Colo.,ColoradoSchoolofMines,p.17–82. Yu,K.N.,Lau,B.M.F.,andNikezic,D.,2006,Assessmentof environmentalradonhazardusinghumanrespiratorytractmodels: JournalofHazardousMaterials,v.132,p.98–110. R ISKSTO C AVE W ORKERSFROM E XPOSURESTO L OW -L EVEL I ONIZING a R ADIATIONFROM 222 R N D ECAYIN C AVES 228 N JournalofCaveandKarstStudies, April2007



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THEREFLECTIONOFKARSTINTHEONLINEMIRROR:A SURVEYWITHINSCIENTIFICDATABASES,1960–2005 L EE J.F LOREA 1 ,B ETH F RATESI AND T ODD C HAVEZ 2 Abstract Thefieldofcaveandkarstscienceisservedbyaliteraturethatisdispers ed acrossfar-flungtopicaljournals,governmentpublications,andclubne wsletters.Aspart ofaninter-institutionalprojecttoglobalizekarstinformation(KIP,t heKarst InformationPortal),theUSFLibraryundertookastructuredbatteryofli terature searchestomapthedomainofkarstliterature.Thestudyused4,300indivi dualsearches andfourliteraturedatabases:GeoRef,BIOSIS,AnthropologyPlus,andGP OAccess. Thesearcheswerebasedonalistof632termsincluding321karst-relatedk eywords culledfromthreeleadingencyclopediasandglossariesofcaveandkarsts cience.An examinationofyearlychangesinpublicationrateindicatesthatforthel ast45years,the numberofcaveandkarstpublicationshasincreasedsteadily,ashasthenu mberof journalsinwhichtheyappear.Inparticular,thepasttenyearscoveraper iodofrapid growthwherekarst-specificjournalsachievedpeer-reviewstatus,andi ndividualjournals acceptedmorecaveandkarstpapersforpublication. I NTRODUCTION Partofwhatattractsstudentsofgeologyisthefield experience,theideathatthefirstchallengeinstudyingan outcropisgettingtoit.Biologyandarchaeologysharethis elementofexpedition.Thischallengeisever-presentin karst,evenmoresothaninmostotherfields.Cavescienceis notonlylogisticallydemandingandphysicallychallenging, butalsoconceptuallyintricateanddifficulttocategorize: Theideathatthereisascienceofspeleologythatincludes everythingthatonemightliketoknowhasprovedinfeasible. Insteadofaninwardlyfocusedstudyoncaves,thecurrent generationofcavescientistsarefindingoutthattheyneedtolook outwardratherthaninward.Tounderstandcaves,onemustalso understandthelandscape,drainagebasins,androckunitsinwhich theyoccur.Onemustdrawongeochemistry,fluidmechanics, crystallography,andmanyotherdisciplinesthatprovideessential understandingoftheprocessesthatoccurincaves. -WhiteandWhite,1998,p.40 Karstresearchersencounteradditionalchallengesin managinganinformationenvironmentwhereinalarge amountoftheinformationpertainingtokarstoriginates outsideoftheacademicworld.TheNationalSpeleological Societyisperhapsthelargestsourceandrepositoryfor cavedata(intheformofmaps,tripreports,etc.)inthe UnitedStates,eventhough,accordingtoa2005survey, onlyaround15%ofNSSmembersconsiderthemselves professionalscientists.Thus,askarstscientists,weenjoy anddependuponthecooperationandcompanionshipof industryprofessionals,explorers,andamateurscientists whosestandardsfordata-gatheringmaymeetorexceed thoseofthescientificinstitution. Traditionally,littleofthedatacollectedbynon-scientist caversmakesitintoliteraturewithwidespreaddistribution; theinformationendsupinconsultingreports,expedition summaries,andcaving-clubnewsletters.Thesepublicationsaretermedgrayliteraturebyvirtueofbeingunavailablethroughconventionalchannelsoflibraryacquisition (Bichteler,1991).Libraryprofessionalsfindguidebooksto beparticularlyfrustrating,brandingthem‘‘sneaky,fly-bynight,changecoatpublications[thatare]hardtoidentify, hardtoacquire,hardtocatalogandretrieve,andhardto preserve’’(Walcott,1990).Thesegrayliteraturevenues rarelyfindtheirwayintostandardbibliographicindices, andarenotonlydifficultforresearcherstotrackdown,but mayonlyexistinpersonallibrariesthatcansufferfrom damageorloss.Academicscientists,however,aremore concernedwiththefactthatmuchgrayliteraturemanages tomakeitswayintoprintwhileavoidingthepeer-review process(Bichteler,1991,p.40). Despitetheseconcerns,recentdataindicatesthat scientistsacrossseveraldisciplinesarecitingmoregray literature(e.g.,Mili,2000,ineconomics;Osif,2000,inthe transportationsciences).Inoneparticularstudyofpapers fromafisheriesmanagementconference,Lacanilao(1997) foundthat92percentofthetotalnumberofcitationswere tograyliterature. Grayliteraturepublicationsserveanimportantrolein supportingthesciences(Cordes,2004;Luzi,2000).Researchappearingasanunreviewedabstractorproceedings papermayyetbeinnovativeandisoftentimestheonly workonaparticularsubject.Inthekarstcommunity,gray literaturepublicationsmaydocumentthefirstobservations withinacave,thefirstidentificationsofnewspecies,orthe locationsofimportantarcheologicalsites. For65yearsthe JournalofCaveandKarstStudies has providedoneavenuebywhichkarstscientistscanplace 2 UniversityLibraries,UniversityofSouthFlorida4202E.FowlerAve,Tam pa,FL 33620,tchavez@lib.usf.edu 1 DepartmentofGeology,UniversityofSouthFlorida4202E.FowlerAve,SCA 528,Tampa,FL33620,lflorea@chuma1.cas.usf.edu,sfratesi@mail.usf. edu LeeJ.Florea,BethFratesi,andToddChavez–Thereflectionofkarstinthe onlinemirror:asurveywithinscientificdatabases,1960– 2005. JournalofCaveandKarstStudies, v.69,no.1,p.229–236. JournalofCaveandKarstStudies, April2007 N 229

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theirresearchonpermanentrecordandcommunicatewith non-sciencecaversintheUnitedStatesandabroad. GeoRef ,aleadingearthsciencecitationdatabase,classified thisjournal’spredecessor,the NSSBulletin ,asanon-peerreviewedjournal.Thischangedin1995withthechangein name.Moreover,the Journal hasbeenindexedwiththe InstituteforScientificInformation(ISI)since2003. Oneexampleofapioneeringefforttodocumentgray elementsofthekarstliteratureisthebibliographyof Northupetal.(1998).Publishedin1998, AGuideto SpeleologicalLiteratureoftheEnglishLanguage,1794– 1996 documents3,558worksinprintconcerningcavesas of1996.Asthispaperdemonstrates,thegrowthin publicationofkarstrelatedresearchhasincreasedsubstantivelyduringthesucceedingdecade,afactthathasled inparttotheKarstInformationPortal(KIP)initiative.As apartnershipwithkarstresearchersfrommanyperspectives,theKIPpromisestobeadynamicdescendenttothe typeofbibliographyrepresentedbyNorthupetal.(1998), providingaccesstowhiteandgrayinformationsourcesin multipleformats,arepositoryfacility,andexpertevaluationofkeyresources. T HE K ARST I NFORMATION P ORTAL ScientistsandinformationspecialistsfromtheNational CaveandKarstInstitute(NCKRI),theUniversityofNew Mexico(UNM),andtheUniversityofSouthFlorida (USF),concernedaboutthefragmenteddistributionof dataandliteratureaboutkarstresources,haveinitiatedthe KIP.TheintentoftheKIPistogathercontentand metadatafromdisparatemassesofkarstresearchintoone onlinesearchableportalandtofacilitatecommunication amongkarstscientists. Withaninternationalfocus,designersintendtheKIPto serveasaone-stopsourceforsharinginformationabout karstliterature.TheKIPwillincludematerialthatisoften hardtolocate,suchastechnicalreports,conference proceedings,thesesanddissertations,newsletters,maps, databases,andphotosofkarstresources. Ascertainingthedomainofkarstliteratureisonevital steptowardestablishingtheKIP.Forinstance,identifying journalsthatpublishkarstliteraturewillassistinformation specialistsinacquisitions.Trackingpublicationtrendsin karstwillhelpplanforthefutureneedsoftheKIP. Understandingwherekarstresearchoccursandhowthe karstliteratureclustersaroundfieldsofstudyandsubject keywords,willprovideametricbywhichadministrators canassessthecontentoftheKIPagainstthereal distributionofkarstliterature. E XPLORING K ARSTTHROUGH O NLINE D ATABASES TolaygroundworkfortheKIP,weundertookasurvey oftheexistingkarstliterature.Thissurvey,primarily conductedbetweenOctober,2005andJanuary,2006, consistedofmorethan4,300literaturesearchesacrossfour majorscientificdatabases: GeoRef ,aleadingearth-science databaseadministeredbytheAmericanGeologicalInstitute(AGI); BIOSISPreviews ,themedicalandlifesciencedatabaseofthe ISIWebofKnowledge ownedbythe ThompsonCorporation; AnthropologyPlus ,managedby EurekaandcombiningtheAnthropologicalLiterature fromHarvardUniversityandtheAnthropologicalIndex fromtheRoyalAnthropologicalInstituteintheUK;and GPOAccess ,theprimarysearchengineforpublications publishedbytheUSGovernmentPrintingOffice. Partofthegoalofthisstudyistofindoutwhatsortof ontologybestcapturestherelevantliterature.Ourclassificationofsearchtermsisthereforesomewhatrudimentary.Weculledalistof321cave-andkarst-relatedterms fromtheglossariesofthe EncyclopediaofCaves (Culver andWhite,2005), ALexiconofCaveandKarstTerminologywithSpecialReferencetoEnvironmentalKarstHydrology (Field,1999),andtheonline GlossaryofSpeleological andCavingTerms (ASF,2004). Wecombinedlistsoftermsfromallthreeglossariesand deletedtheduplicates.Tosupplementthelistof1,875 wordsthatremained,weincludedalistof30namesof importantcavesaroundtheworld,26fieldsofstudy relatedtocavesandkarst,24geographicsettingswhere cavesandkarstfeaturesarefound,allsevencontinents with37sub-regionswithinthesecontinents,and187 independentnations,formercountries,andalternate spellingsofthesecountries.Inall,thisrefinedlistincluded 2,186terms. Fromourrefinedlist,weextractedashortlistof15 primarywordslikelytocapturealargenumberofthe English-languagecitationsrelevanttocavesandkarst studies.Thesewordsincludedthewordstemskarst,cave, andseverallinguisticvariationsthereof(e.g. cueva ).Major relatedwordswereincludedinthislist–spring(s), conduit(s),andbats,forinstance. Nextweoutlinedtwogroupsofmodifiersforthewords intheoriginallist.Thehigher-levelgroupconsistsof locations,scientificdisciplines,andsettingswithinwhich karstmightbefound.Forexample,thetermspaleontology,marine,andRomaniaareallhigher-levelmodifiers. Thelower-levelgroupincludes321keywordsthatwould fallwithinthekarstfielditself(eitherphysicallyor bibliographically).Thesearegenerallymorespecific,such assedimentandmodel.Theremaining1,539termswere eithertoospecificortoogeneraltocapturerelevant citationsandwereeliminated. Onesetofsearchesutilizestheprimarytermsappliedto allfourdatabasesinthisstudy.Thesecondsetofsearches consistsofeachtermfromthetwolistsofmodifiers, combinedwiththetermcaveorkarstandtheappropriate wildcardsymbols,suchasanasterisk(*),tocaptureallof thederivatives.Itisimportanttonotethattheresultsof thesesearchesarenotfilteredforrelevance;theyare presentedinthispaperasreturnedbythesearchengine. T HEREFLECTIONOFKARSTINTHEONLINEMIRROR : ASURVEYWITHINSCIENTIFICDATABASES ,1960–2005 230 N JournalofCaveandKarstStudies, April2007

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Weperformedanadditionalsetofsearchestonetthe entirebodyofcitationsrelatedtocavesorkarstwithin GeoRef foreachyearbetween1960and2005.Weseparated thesebypublicationtypeandextractedasubsetofpeerreviewedjournalarticles.Weperformedsimilargeneral karstsearcheswithintheabstractarchivesoftheGeologicalSocietyofAmerica. T HE D OMAINOF K ARST L ITERATURE PrimaryTerms Theprimarysearchtermresultsaredominatedbythe termspring,whichdoesnotspecificallyrefertokarst springs(Table1).Thesearchresultsforspringin GPO Access reflectstheloosenatureofthissearchengine: asearchherereturnshitsonanydocumentwithinallU.S. governmentwebsites.Theresultsarenotrestrictedto scientificdocuments;thusthetermspringreturnsalmost 350,000citations,mostofwhichprobablyrefertothe seasonofrebirth,ratherthanapointofresurgence (Table1).Becausetheresultsfromthissearchengine appeartohavelittlerelevancetothedesiredbodyof literatureandlittleadvantageoveraconventionalwebsearchengine,weeliminated GPOAccess fromallsubsequentsearches. Secondandthirdinorderofprevalenceintheprimary searchtermsarethewordskarstandcave,themostgeneral oftheremainingEnglish-basedterms(Table1).Citations within AnthropologyPlus referalmostexclusivelytocaves, withcomparativelyfewreferencestokarst. BIOSISPreviews hadfourtimesmorereferencestocavesthantokarst, whereasin GeoRef theyoccuraboutthesamenumberof times(Table1). Therelatednessoftermstospecificdisciplinesinfluencestheirdistributionamongthedatabases.Forexample, thebiology-relatedtermsbats,stygo-,andtroglo-returned byfarthemostresultsfrom BIOSISPreviews ,while geologicaltermssuchascarbonateaquiferandlimestone aquiferaremoreprevalentin GeoRef (Table1). Higher-OrderModifiers Resultsforthesearchesofhigher-ordermodifiersare includedinTables2and3,separatedintosetting,location, fieldofstudy,andsubjectkeywords. Table1.Searchresultsfortheprimarysearchterms. SearchTerms GeoRef a BIOSIS Previews b Anthropology Plus c GPO Access d All PeerReviewJournalConferenceBooks bats251107215411616,0629625,253 carbonate aquifer(s) e 3479127817863311497 carso f 3,6631,4023,237802346316039,655 cave24,1805,19921,2656,6902,59523,9618,45064,988 conduit(s) g 2,8401,1312,4661,2203236,7311126,738 cueva(s)998210768380212178853451 grotte9108986016345631,81360 grotto(s)6733763264407549754 karst h 27,3796,57023,69810,0313,4075,2342697,800 limestone aquifer(s) 1,6403901,375684235500495 sink7,8932,5016,8032,87093713,62515858,659 spring(s) i 71,98629,01865,50431,3614,87387,5281,211349,274 spel(a)eo j 10,4521,7489,5633,410828696370621 stygo2910271014880158 troglo8427702154,8534301,291 a Searchincludedentirereference. b Topicsearch. c Keywordsearch. d Generalsearch. e Thesearchstring,carbonateaquifer(s),includesthephrase,carbonate aquifer,andthepluralform,carbonateaquifers.Thisconstructionappl iestoallsearchstringswith asimilarformat. f Thesearchstring,carso,includestheword,carsoandallderivativestha tusecarsoasaprefix.Thisconstructionappliestoallsearchstringswit hasimilarformat. g Thesearchstring,conduit(s)resultsinmanycitationsthatareunrelate dtokarststudies. h Thesearchstring,karst,includestheword,karst,andallderivativesth atusekarstasarootwordandhaveprefixesorsuffixes.Thisconstruction appliestoallsearchstrings withasimilarformat. i Thesearchstring,springs,resultsinmanycitationsthatareunrelatedt okarststudies. j Thesearchstring,spel(a)eo,includesalltermsthatcontaintheroot,sp eleo,orthealternatespelling,spelaeo. L EE J.F LOREA ,B ETH F RATESI AND T ODD C HAVEZ JournalofCaveandKarstStudies, April2007 N 231

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Themodifierseaappearsasthemostfrequentgeographicsettingmentionedinkarst-relatedGeoRefcitations (Table2).Thisisnotsurprising;eveninstudiesofmidcontinentalkarst,itisdifficulttodiscusskarstdevelopmentwithoutinvokingsea-levelorreferringtoabaselevel ofsomesort.Itshouldbenotedthatthereislikely considerableoverlapbetweenseaandthesecondandthird rankinggeographicmodifiers,marine,andisland(Table2). WithaglanceatTable2,karstappearsasadecidedly Eurocentricdiscipline:Europeisbyfarthemost-cited continentincaveandkarstreferences,withmorethan threetimesthenumber-twocontinent,Asia.However, althoughNorthAmericacomesinatadistantthirdplace asacontinent,theUnitedStatesisthecountrymentioned themosttimesoverall,withaboutasmanycitationsasthe continentofEuropeitself(Table2).Thesenumberssurely reflectthehistoryofkarst(withitsEuropeanorigins),the distributionandimpactofjournalsindifferentcountries, theamountofkarstaccessibletoeachregion,andother scientificandsocio-economicinfluences,aswellasvagaries ofthesearchprocess.Forexample: 1)Thereareaboutasmanyreferencesin BIOSIS Previews tokarstinNorwayastherearereferences tocavesintheUnitedStates(Table2).Wefindthat thisisbecauseofreferencestotheNorwegianspruce ( Piceaabies (L.)Karst).Only21referencesremain whenthespeciesnameisexcludedfromthesearch. 2)Ontheotherhand,bothFranceandSpainhave anomalouslylargenumbersofreferencestocavein AnthropologyPlus (Table2).Nodoubtthesecitations reflectalonganddistinguishedrecordofcave archeology,particularlyasitrelatestofamous PaleolithiccaveartatsitessuchasLascauxand Altamira. Thepredictablepartialityofeachdatabasetoitsown sub-disciplineisclearlydemonstratedinoursearchresults forthefieldsofstudy(Table2):thegeologyandgeomorphologypapersareinprimarilyin GeoRef ,thebiology andecologypapersaredominantin BIOSISPreviews ,and archaeologypaperscomprisethemajorityofthe AnthropologyPlus results. Resultsforthe30mostcommonlyoccurringkeywords arepresentedinTable3.Generalratherthanspecific keywordscomposemostofthislist.Yet,afewmore specifictermsthatrefertospecificscientificmethods,such asisotope,makethelist.Thephrasecavesystemseemsto permeatebiologicalliterature,whereasphrasessuchas karstwaterandkarsthydrologyoccurcommonlyin geologicalliterature. AnnualPublicationRatesintheGeoRefDatabase Searchesforkarst-relatedGSAabstractsshowcontinued,rapidgrowthofthefieldduringthepasttenyears (Fig.1).Karst-relatedabstractsnowconstituteabout2.5% ofallGSAabstractsproducedeachyear,morethantwice thepercentagein1995.Thepatternofpeer-reviewed articlesnotassociatedwithconferenceproceedingsshows aslightlydifferentprofile(Fig.2).Growthofthefield duringthe1990syieldstoaslightdownturnafter2003. Thismaysimplybethemanifestationofalagtimeofdata entryin GeoRef Theincreaseinjournaldiversitymirrorstheincreasein numberofarticlesoncavesandkarst(Fig.2).Between 1960–2005,karstarticlesappearedin437differentpeerreviewedjournals.However,asistrueofmostscientific disciplines,themajorityofthekarstliteratureisconcentratedinafewcorejournals(Bradford,1934).Thetop25 journalsaccountfor46%ofthekarst-relatedcitations. Figure2showsthislistof25journals,rankedbythetotal numberofkarstandcavearticlesfrom1960to2005. Whilekarst-specialtyjournalsaccountforonly8%of thepeer-reviewedpublicationsforthistimeperiod,ithas onlybeeninthelasttenyearsthatthe JournalofCaveand KarstStudies CaveandKarstScience ,and ActaCarsologica havebeenincludedin GeoRef aspeer-reviewed journals,allthreewithshortbutintensehistoriesof publishingkarstpapers(Fig.2). EnvironmentalGeology whilenotexclusivelyakarstjournal,hasasimilar publicationprofile.The JournalofHydrology hasincluded severalarticlesconcerningkarsteachyearformostyears sinceitsinception,makingitthetopsourceforkarstrelatedarticlesfrom1960to2005. Generalsciencejournalssuchas Nature and Science have alonghistoryofintermittentlyincludingkarstarticlesthat arecitedby GeoRef (Fig.2).Theseaccumulatelarge numbersofkarstcitationsthroughtheirlonglifespans.In themajorgeologicalsub-disciplinejournalssuchas ChemicalGeology and GroundWater ,weseeasubstantialincrease inthenumberofarticlesoverthepasttenyears(Fig.2). C ONCLUDING R EMARKS Thisstudyrepresentsoneinaseriesofstepstodesigning aninformationportalforthekarstsciences;aportalthat willfacilitateworldwidecommunicationonresearchon karstphenomena.Theseriesof4,300literaturesearchesthat composethisstudyidentifythescopeofcave-andkarstrelatedliteratureandthechangesthroughtimethatkarst literatureexperienced.Karstasascienceisgrowing,andthe pasttenyearsencompassmuchofthatgrowth.Oursearches revealseveralfactorsthatpartiallyexplaintheincreasing volumeofpeer-reviewedkarstliterature: 1.Thekarst-heavyjournalsachievedpeer-reviewstatus; 2.Thenumberofjournalsthatpublishkarst-related articlesincreased;and 3.Thenumberofcaveandkarstarticlesineachjournal increased. Withrespecttothefirstpoint,obtainingpeer-review statuswasacriticalstepforestablishingthecredibilityof T HEREFLECTIONOFKARSTINTHEONLINEMIRROR : ASURVEYWITHINSCIENTIFICDATABASES ,1960–2005 232 N JournalofCaveandKarstStudies, April2007

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Table2.Rankedsummaryofsearchresultsforthetopfivegeographicsetti ngs,allcontinents,andthetop25countries. SearchAreaRank SearchEngine Totals GeoRef a BIOSISPreviews b AnthropologyPlus c Cave d Karst e CaveKarstCaveKarst GeographicSetting Sea17411,2494661912112,669 Marine25588746771981002,317 Island3728624506796602,003 Plateau456681497952511,598 Mountain57095291571413931,578 Continents Europe18,74910,3871,2031,3424354022,156 Asia22,4153,67152618325427,051 NorthAmerica32,45572288724218824,496 Africa41,0966525375535902,699 Australia59513954176415031,980 SouthAmerica6530320294622801,234 Pacific f 733419918925671815 Antarctica80000000 Countries UnitedStates g 112,7959,3361,60426567424,071 France23,6181,7803982051,264177,282 Germany h 32,2801,25113825313894,069 UnitedKingdom i 42,90349714845003,593 China51,1051,9611799512623,468 Spain687897435813572153,071 Italy71,145988423246382,813 Mexico81,0166564227021742,385 Australia99513954196424532,077 Norway1029598481,629322,075 Canada111,006600120921401,832 U.S.S.R. j 125471,063115721501,812 Austria13978508696255111,683 SouthAfrica147261202861137101,514 Switzerland1567238174513621,216 Czechoslovakia k 165064893410639191,193 Yugoslavia l 1721663916811231151,181 Hungary183424605142508953 Poland1934636492112179940 Slovenia2030435976741310836 Japan214358824026330822 Israel2227314898192401779 Romania232652781684270760 Greece24168320125211102746 Brazil2519317724742551715 a Searchincludedentirereference. b Topicsearch. c Keywordsearch. d Thesearchstring,cave,includesthewordcaveandallderivativesthatus ecaveasaprefix. e Thesearchstring,karst,includesthewordkarstandallderivativesthat usekarstastherootwordandhaveprefixesorsuffixes. f Thoughnotacontinent,weincludedPacificinthissectionbecauseitincl udesavarietyofislandnationsnotincludedwithintheothercontinents. g Thecountrysearch,UnitedStates,alsoincludesthesearchUSA,U.S.A.,a ndAmerica. h Thecountrysearch,Germany,includesthepreviousstatesoftheFederalR epublicofGermanyandtheGermanDemocraticRepublic. i Thecountrysearch,UnitedKingdom,alsoincludesthesearchphrasesUK,U .K.,Britain,andEngland. j Thecountrysearch,U.S.S.R.,doesnotincludeSovietUnionorRussiawhic hareseparatesearches. k Thecountrysearch,Czechoslovakia,doesnotincludeCzechRepublicorSl ovakiawhichareseparatesearches. l Thecountrysearch,Yugoslavia,doesnotincludesearchesforanyofthepr esentcountriesthatcomprisetheformerYugoslavia. L EE J.F LOREA ,B ETH F RATESI AND T ODD C HAVEZ JournalofCaveandKarstStudies, April2007 N 233

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Table3.Rankedsummaryofsearchresultsforthetop10fieldsofstudyandt hetop30subjectkeywords. FieldofStudyand SubjectKeywordRank SearchEngine Totals GeoRef a BIOSISPreviews b AnthropologyPlus c Cave d Karst e CaveKarstCaveKarst FieldofStudy Geomorphology111,5548,736223219320,366 Geology212,4775,40872950191819,214 Ecology34875196,3733,14644110,570 Biology4234706,3323,85518010,509 Arch(a)eology f 51,618409476276,592809,202 Hydrology61,9656,3781867008,428 Hydrogeology72,1343,876542106,058 Pal(a)eontology83,93333474136514,420 Exploration92,0651,911123178604,202 Engineering102,1461,8997925204,151 SubjectKeyword System(s) g 11,8593,02620,1232,11138427,161 Vertebrat h 24,06773817,6566030123,065 Mammal33,23857516,43642087020,756 Environment(s)43,0885,6856,5383,3851611118,868 Water54,08910,2121,8651,6596117,832 Sediment66,3309,610491282148716,868 Region73,0875,0496,0582,1241892016,554 Hydro84,14710,0908864843015,590 Human(s)992582511,7272367341014,457 Morphology101,3229387,9062,01754212,239 Cainozoicor Cenozoic 117,1414,429307790011,956 Ground(-)water i 122,8038,3331262713311,539 Quaternary136,7663,12845198102410,549 Limeston143,1575,0973433111218,921 Carbon155,5281,0885035225937,703 Development161,4002,3152,5791,2401537,552 Strat173,3422,778812245297107,484 Species185812094,8081,838807,444 Pleistocene193,8771,5481,23818029497,146 Deposit(s)202,1373,21489641219326,854 Isotop211,7851,5742,7331544126,289 Mine(s)ormining221,2482,9351,1628685556,273 Evolution231,8382,6761,21024324246,213 Mineral(s)241,7492,2511,0468392845,917 Radio251,3168393,39410818455,846 Invertebrate(s)26289194,619907005,834 Aqui271,1384,39372227215,833 Fossil282,6366741,65438841245,768 Reproduce2957365,138424105,656 Model301,2772,3744484482805,644 a Searchincludedentirereference. b Topicsearch. c Keywordsearch. d Thesearchstring,cave,includesthewordcaveandallderivativesthatus ecaveasaprefix. e Thesearchstring,karst,includesthewordkarstandallderivativesthat usekarstastherootwordandhaveprefixesorsuffixes. f Thesearchstring,arch(a)eology,includesarcheologyandthealternate spellingarchaeology.Thisconstructionappliestoallsearchstringswi thsimilarformat. g Thesearchstring,system(s)includesthewordsystemandthepluralforms ystems.Thisconstructionappliestoallsearchstringswithsimilarform at. h Thesearchstring,vertebrat,includesalltermsthatbeginwiththerootv ertebrat.Thisconstructionappliestoallsearchstringswithsimilarfo rmat. i Thesearchstring,ground(-)waterincludestheformsgroundwater,groun d-water,andgroundwater. T HEREFLECTIONOFKARSTINTHEONLINEMIRROR : ASURVEYWITHINSCIENTIFICDATABASES ,1960–2005 234 N JournalofCaveandKarstStudies, April2007

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karstasascience.Papersinthe JournalofCaveand KarstStudies andotherkarst-orientedjournalsnow reachamuchbroadercommunityofscientistsand resourceprofessionals,facilitatedbycurrenttrendsin on-linepublishing.Furthermore,allthreepointsreflect uponaconsciouseffortoverseveraldecadesby dedicatedcaversandkarstprofessionalstoadvance thesciencetoapointofacceptancebythegreater scientificcommunity,particularlywithintheearth sciencedisciplines.Overall,thenumbersfromthisstudy elaborateonastatementthatkarstscientistsare gratifiedtohear: Cavegeologyhascomeofage.Thegeologicalstudyofcavesis nowanintegratedpartofthegeologicalsciencesratherthan aportionofanexoticborderlandsciencecalledspeleology. -WhiteandWhite(1998,p.41) A CKNOWLEDGMENTS Researchassistanceforthisprojectwasprovidedinpart bythePatelCenterforGlobalSolutions,theUniversityof SouthFloridaLibraries,andtheUSFDepartmentof Geology.Weappreciatethegracioussupportofthe NationalCaveandKarstResearchInstituteandthe UniversityofNewMexicointhisendeavor.Diana Northupandananonymousreviewerprovidedconstructiveinputonanearlierversionofthismanuscript. Figure1.Percentofabstractsrelatedtocavesandkarst atGeologicalSocietyofAmericameetings.Priorto1985 percentagesareaveragedoverfiveyears. heightofasingleblackbarrepresentsthenumberofrelevant papersforthatyear.Forscalereference,thetotalheightof eachhorizontal,graybarcorrespondstotenarticles.The lengthofeachgraybarspansthelifespanofthejournal. Figure2.Rankedsummaryofthenumberofcave-andkarstrelatedpublicationseachyearbyjournal.Thetopgraphisthe numberofpeerreviewedjournalsin GeoRef thatpublish papersaboutcavesandkarst,andthelowergraphisthe numberofpeer-reviewedpapersin GeoRef aboutcavesand karst.Eachbargraphprovidesinformationonthecaveand karstpublicationhistoryforanindividualjournal.Thetotal L EE J.F LOREA ,B ETH F RATESI AND T ODD C HAVEZ JournalofCaveandKarstStudies, April2007 N 235

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R EFERENCES ASF,2004,GlossaryofSpeleologicalandCavingTerms,Australian SpeleologicalFederationInc.,3October,2005,http://home.mira.net/ gnb/caving/glossary/index.html[accessedJuly3,2004]. Bichteler,J.,1991,Geologistsandgrayliterature:Access,use,and problems:Science&TechnologyLibraries,v.11.3,p.39–50. Bradford,S.C.,1934,Sourcesofinformationonspecificsubjects: Engineering,v.137,p.85–86. Cordes,R.,2004,IsGreyLiteratureEverUsed?UsingCitationAnalysis toMeasuretheImpactofGESAMP,AnInternationalMarine ScientificAdvisoryBody:TheCanadianJournalofInformationand LibraryScience,v.28,no.1,p.49–67. Culver,D.C.,andWhite,W.B.,2005,EncyclopediaofCaves.,Elsevier AcademicPress,Amsterdam,654p. Field,M.S.,1999,ALexiconofCaveandKarstTerminologywithSpecial ReferencetoEnvironmentalKarstHydrology:,UnitedStates EnvironmentalProtectionAgency,EPA/600/R-99/006. Lacanilao,F.,1997,ContinuingProblemswithGrayLiterature: EnvironmentalBiologyofFishes,v.49,p.1–5. Luzi,D.,2000,TrendsandEvolutionintheDevelopmentofGrey Literature:AReview:TheInternationalJournalofGreyLiterature, v.1,no.3,p.106–116. Mili,F.,2000,TrendsinPublishingAcademicGreyLiterature:Examples fromEconomics:TheInternationalJournalofGreyLiterature,v.1, no.4,p.157–166. Northup,D.E.,Mobley,E.D.,Ingham,K.L.,andMixon,W.W.,1998,A GuidetoSpeleologicalLiterature,CaveBooks,St.Louis,Mo.,539p. Osif,B.,2000,InternationalTransportationLiterature:AnAnalysisof CitationPatterns,Availability,andResearchImplicationstothe TransportationCommunity:TheInternationalJournalofGrey Literature,v.1,no.4,p.149–156. Walcott,R.,1990,Guidebookproblemsfromthelibrarian’spointofview, FrontiersinGeoscienceInformation. in ProceedingsoftheTwentyFourthMeetingoftheGeoscienceInformationSociety,November6– 9,1989,St.Louis,Mo.,Mary,B.,andAnsari,M.B.,eds.,Alexandria, Va.,GeoscienceInformationSociety,p.185–192. White,W.B.,andWhite,E.L.,1998,Geology, in AGuidetoSpeleological Literature,Northup,D.E.,Mobley,E.D.,Ingham,K.L.,andMixon, W.W.,eds.,p.40–41. T HEREFLECTIONOFKARSTINTHEONLINEMIRROR : ASURVEYWITHINSCIENTIFICDATABASES ,1960–2005 236 N JournalofCaveandKarstStudies, April2007



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CAVEARCHAEOLOGYANDTHENSS:1941–2006 G EORGE C ROTHERS 1 ,P.W ILLEY 2 AND P ATTY J O W ATSON 3 Abstract: Likemostotherbranchesofspeleology,cavearchaeologyintheU.S.grew anddevelopedsignificantlyduringthemidtolatetwentiethcentury.Ori ginallyviewedas marginaltomainstreamAmericanistarchaeology,pursuitofprehistoric andhistoric archaeologyundergroundisnowwidelyacceptedasmakingvaluablecontri butionsto knowledgeofhumanpast.TheNationalSpeleologicalSocietyplayedacent ralrolein thatdevelopmentandcontinuestodoso.Weoutlinetheestablishmentandg rowthof cavearchaeologyinNorthAmerica,withspecialemphasisonrelationsbet weentheNSS andarchaeologyperformedindarkzone,deepcaveinteriors. I NTRODUCTION TheNSShasdirectlyparticipatedincavearchaeology throughcooperation,education,andconservation.MembersoftheSocietyhavemadenotablecontributionstothe sciencebyreportingthelocationofarchaeologicalsites, participatingintheirinvestigation,andbyequipping scientistswiththetechniquesandtechnologyneededto worksafelyinthecaveenvironment(Damon,1991,p. 283). CavearchaeologywasacentralNSSconcernfromthe firstdaysoftheSociety’sexistence.Therewasan ArchaeologyCommitteeaswellasCommitteeson Membership,Grottos,Records,Publications,Photography,Exploration,Mapping,andPublicityatleastasearly as1948(Damon,1991,p.196).AtthesecondAnnual MeetingoftheNSSin1945(thefirstsuchmeetingwasin 1941;thethreesubsequentmeetingswerecancelledbecause ofWorldWarII),afeaturedspeakerwasFrankHibben talkingabouthisarchaeologicalworkinSandiaCave,New Mexico,andaboutputativelypre-Folsomartifactsfrom thatsite.Afewyearslater,Hibbenwasthebanquet speakeragainatthe1953NSSconvention,presenting alectureentitled‘‘AncientCaveLifeintheSouthwest.’’ ArchaeologistswerealsoincludedontheNSSaward listsduringthe1950s.EmilHaury(1951),HenriBreuil (1955),andCarlMiller(1957)allreceivedHonorary MembershipintheNSSfortheirworkincavearchaeology:HauryforhisVentanaCave,Arizona,research,Breuil forhisresearchonPaleolithicpaintedcavesinFrance,and MillerforhisexcavationsinRussellCave,Alabama. AccordingtobriefsummariesinDamon(1991), papersonarchaeologicaltopicswereoftenpresentedin theannualconventionsessions.Specificmentionofsuch papersismadeinpassingforthe1949,1952,1953,1954, and1956conventions.In1958,CarlMillerasthebanquet speakerdescribedhisarchaeologicalworkatRussellCave showingmoviesmadetherebytheNationalGeographic Society.Atthe1970convention,someofRussellTrall Neville’ssilentmoviesfilmedinvariouscaves(including SaltsCave,Kentucky)wereshown.TheNSSstillowns copiesoftheseNevillefilms,whichweremadeduringthe 1920sand1930sby‘‘theCaveman,’’asNevillewasoften called. DespiteinterestincavearchaeologywithintheNSS governanceandsomeportionofthemembershipduring thefirstfewdecadesaftertheorganizationwasformed, systematic,long-termarchaeologicalresearchbyprofessionalarchaeologistsinthedarkzonesofbigcavesin theAmericasdidnotgetunderwayuntilthe1960s.There areprobablyseveralreasonsforthis,butprimaryamong themisthedifferencebetweenrockshelterarchaeology andarchaeologyconductedinsubterraneanspacesnever illuminatedbynaturallight.Researchinrocksheltershas beenanormalpartoffieldarchaeologysincetheearliest daysofthedisciplineeverywhereitwaspracticed,butthe onlyaspectofcavearchaeologywidelyrecognizedbefore the1980swasdocumentationofUpperPaleolithic paintingsinsouthwesternEurope.(And,infact,the authenticityofthosedark-zonepaintingswasestablished onlyafteralongperiodofheateddebatebeginninginthe late1800sandcontinuingwellintotheearlytwentieth century.)Mostarchaeologistsspecializingintheearly culturehistoryoftheAmericasdidnotthinkthatcave darkzones,iftheythoughtaboutthematall,wereplaces frequentedbyorevenknowntoancienthumangroups. Therefore,caveinteriorswereoutsidetheresearchrealm ofmainstream,mid-twentiethcenturyAmericanistarchaeology. Nevertheless,astheNSSandaffiliatedorassociated organizations,suchasstateandregionalsurveys(e.g., theTennesseeCaveSurvey)andvoluntarybutformally constitutedresearchgroups(e.g.,theAssociationfor MexicanCaveStudiesandtheCaveResearchFoundation) grewandproliferated,caversbeganmakingarchaeological, biological,geological,andpaleontologicaldiscoveriesthat drewincreasingnumbersofnon-caverscientistsintothe undergroundworld. 1 DepartmentofAnthropology,UniversityofKentucky,Lexington,KY40506 USA,george.crothers@uky.edu 2 DepartmentofAnthropology,CaliforniaStateUniversity-Chico,Chico, CA95929 USA,pwilley@csuchico.edu. 3 2870SolterraLane,Missoula,MT59803USA,pjwatson@artsci.wustl.edu. GeorgeCrothers,P.Willey,andPattyJoWatson–CavearchaeologyandtheN SS:1941–2006. JournalofCaveandKarstStudies, v.69, no.1,p.27–34. JournalofCaveandKarstStudies, April2007 N 27

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AS HORT H ISTORYOF D ARK -Z ONE C AVE A RCHAEOLOGY INTHE U NITED S TATES Becauseourfocushereisoncavearchaeologyin subterraneanspaceswithextensivedarkzones,wemaintainadistinctionbetweenarchaeologyinrocksheltersand smallcaveswithnotruedarkzones,andarchaeological researchinthedarkzonesofdeepcaveinteriors.The distinctionmeritsemphasisbecauserocksheltersareso oftenreferredtoascaves,andbecause Inthemostfundamentalsense,archaeologyincavesissimply archaeology,withallthecharacteristicsoffieldarchaeologydone anywhere....But,ofcourse,archaeologyundergroundis differentinonesignificantdetailfromarchaeologydoneinother terrestriallocales:archaeologydoneinsideacaveinteriormeans archeologydoneinthedark.Adequatelightingisaproblemfor everysingleindividualateverymoment(Watson,1998,p.5;see alsoWatson,2001). Moreover,sofarasweknow,noancientpeopleever actuallyinhabitedcavedarkzones,althoughthereisample evidencethattheyoftenexploredthem,quarriedthem,and/ orusedthemasstoragelocales,depositoriesforthedeador placestocontactthespiritworld.Hence,archaeologically speaking,culturaldepositsindeepcavecontextsareusually specialpurposesites,secularorsacredorboth.Moreover,in drycaves,whichmakeupalargeproportionofdarkzone sites,preservationofanythingandeverythingleftin aspecificundergroundlocationisvirtuallycompleteno matterhowdelicateorhowoldoryoungitmaybe.This meansthatthebasictechniquesusedinabovegroundsites (includingrocksheltersanddepositsatthemouthsoflarge orsmallcaves)foridentifyingrelativeagesandcultural sequencescanseldombeappliedunderground.Radiocarbonorotherarchaeometricmeansofdating(allofwhichare ratherexpensive)mustbesecuredforindividualitemsto obtainthebasicchronologicalinformationthatallarchaeologistsrequire:howoldaretheseremains? Technicalproblemsofthesortjustindicatedmayhelp explainthemarginalpositionofcavearchaeologyinthe U.S.beforethe1980s,butinfactanyandallcavesciences weregenerallyregardedasratherperipheralendeavorsuntil thelatterpartofthetwentiethcentury(e.g.,White,2003). T HE B EGINNINGSOF S YSTEMATIC C AVE A RCHAEOLOGY : 1890–1960 Inthelateeighteenthandearlynineteenthcenturies, whenEuroamericansbeganexploringlarge,drycavesin theeasternU.S.,suchasMammothandSaltscavesin KentuckyandBigBoneandHubbardscavesinTennessee, theynotedthatprehistoricpeoplehadprecededthemin manyinstances.MuchoftheEuroamericanexploration wasdrivenbythesaltpeterminingbusiness,especially duringtheWarof1812andonasmallerscaleduringthe AmericanRevolution.Archaeologicalremainspreservedin thesedrycavesbecameantiquariancuriosities,especially thedesiccatedormummifiedbodiesofprehistoricIndians foundinremotepassagesorunearthedduringnitrate mining(George,1990). Storiesofthesediscoveriesquicklyspreadinprintand infolklore,withnumerousartifactsandafewofthe mummiescomingtorestinmuseums.Whilethese discoveriesgeneratedfurtherinterestincavesandhelped buildafledglingcavetouristbusinessfollowingtheWarof 1812,archaeologyasadisciplinedidnotdevelopas ascientificfielduntilthelatenineteenthandearly twentiethcenturies. Beginningin1858,WilliamPengelley’ssystematicexcavationofarchaeologicalandpaleontologicaldepositsat BrixhamCaveandKent’sCaverninEnglandwasarevolutionaryadvanceinarchaeologicalrecordingtechniques,and helpedprovetheco-existenceofhumansandextinct PleistoceneanimalsinEuropebydemonstratingtheircooccurrenceinthesamegeologicaldeposits(seeMcFarlane andLundberg,2005).Ayoungarchaeologist,HenryMercer, usedthesenewtechniquesinAmericainanattemptto answerasimilarquestion:theantiquityofhumansinthe NewWorld(e.g.,Mercer,1896,1897,1975).WhileMercer neversuccessfullyidentifiedhumanremainsorartifactsof humanmanufactureinthesamestratigraphiclayerwith Pleistoceneremains,hesystematicallysoughtoutcavesites fromeasternNorthAmericatotheYucatan,includingdarkzonedeposits,inwhatwasoneofthefirstformallyscientific archaeologicalresearchprogramsintheAmericas. Alaterexampleofsystematicworkindark-zonecave archaeologywasthatofAlonzoPond.Anarchaeologist employedbytheNationalParkService,Pondwassentto MammothCavebytheNPSChiefHistorianin1935to investigateadesiccatedbodydiscoveredbytwocave guides.ThebodyofthisprehistoricIndianwasfoundon aledgesometwomilesintothedarkzonefromthenatural entrance.Theancientcaverhadbeencrushedtodeathby alargebreakdownblockhehadapparentlyundermined whilediggingthroughcrystal-bearingsedimentunderlying it.MostofPond’sworkinthecavewastooverseeraising themulti-tonboulderandremovingthebody,buthealso collectednumerousartifactsfromotherlocalesinthecave andmadeobservationsonthenatureofprehistoricmining activitythere(Pond,1937). C AVE A RCHAEOLOGY C OMESOF A GE :1960–1970 InterestinthearchaeologyofMammothCaveacceleratedinthe1960s,asreflectedinpopularpublicationsby DouglasSchwartz(1960,1965)andRobertHall(1967). TheCaveResearchFoundation(CRF)alsobeganlongtermarchaeologicalworkintheMammothCaveareaat thistime.TheCRFArcheologicalProject,directedby PattyJoWatson,beganworkinginSaltsCave(Watson, 1969a),theninMammothandothersmallercavesinand nearMammothCaveNationalPark(Watson,1974). TheCRFArcheologicalProjectmarksthebeginningof moresystematicintegrationofthecavingcommunityinto C AVEARCHAEOLOGYANDTHE NSS:1941–2006 28 N JournalofCaveandKarstStudies, April2007

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scientificarchaeologicalwork.AlthoughCRFwasorganizedasaprivatenon-profitfoundationdistinctfromthe NationalSpeleologicalSocietyinordertoconductresearch inNationalParkServicemanagedcaves,mostofits membersarealsomembersoftheNSS.TheCRF ArcheologicalProjectalsowasthebeginningofconcerted effortstobringdark-zonecavearchaeologyintothe mainstreamofscientificarchaeologicalresearchand publicationintheU.S.ResearchundertakenbytheProject wasfundedinpartbytheNationalEndowmentforthe Humanities,theNationalGeographicSociety,andthe NationalScienceFoundation.WatsonandotherCRF archaeologistsfrequentlypresentedpapersatregionaland nationalarchaeologicalconferences,suchastheannual meetingoftheSocietyforAmericanArchaeology,and publishedtheirresultsin AmericanAntiquity ,theleading archaeologicaljournalforworkintheAmericas(Benningtonetal.,1962;Robbins,1971;WatsonandYarnell,1966). ResultsofresearchbyCRFArcheologicalProjectpersonnelwerealsopublishedinthe NSSNews (Ehman1966; Watson,1966),inthe NSSBulletin (Freemanetal.,1973), andinthe Proceedings forthe4thInternationalCongress ofSpeleology(Watson,1969b). WhiletheCRFArcheologicalProjectwasunderwayin Kentucky,NSScaversmadeaspectaculararchaeological discoveryinthesouthwesternU.S.(EllisandHammack, 1968).FeatherCave,NewMexico,wasawell-knownsite thathadbeenexcavatedduringthe1950s.In1964,members oftheSandia,PecosValley,andElPasoNSSgrottosjoined forcestoexploreasmallleadthathadnotbeeninvestigated bythearchaeologists.Aftercrawlingapproximately12metersthroughthetightpassage,theNSScaversentered aroomofmoderatesizethatseemedtobeundisturbed,and containedmassesofceremonialofferingsincludinghundredsofminiaturearrows,miniaturebows,andpahos (prayersticks),aswellasseveralpictographs.Realizingthe significanceoftheirdiscovery,thecaverslefttheremains undisturbedandreportedthemtotheregionalchairmanof theNSS,RobertWillis,whocontactedarchaeologist FlorenceHawleyEllis.Becausenewsofthediscoveryhad spread,itwasdecidedtocollectallmaterialsinthecaveafter everythinghadbeenrecordedanddocumentedinplace.It wassuggestedthatthecavewasaMogollonshrine dedicatedtoEarthMotherandSunFather,visitedduring biannualsolarceremonies,andwasprobablyabout 600yearsold.Today,suchafindwouldprobablynotresult inremovaloftheartifacts.Rather,thefirstprioritywouldbe tokeepthediscoveryquiet,gateandotherwiseprotectthe site,leavingthematerialinplacetorespectthebeliefsof PuebloIndianswhostillvisitsuchcavesforritualpurposes. C AVE A RCHAEOLOGY E NTERS M AINSTREAM A MERICANIST A RCHAEOLOGY :1970– PRESENT Duringthelate1970sand1980s,NSScaversbegan reportingarchaeologicalremainsinseveraldark-zone cavesoftheeasternU.S.Agroupofcavers,exploringand mappingalargeTennesseecavethatcametobeknownas JaguarCave,discoveredaremotepassagecontaining aseriesofhumanfootprintspreservedinthemudfloor. Carefullyavoidingthetrackway,thecaverskepttheir discoveryquietbutalertedWatsontothefind.Over anumberofyearsthefootprintpassagewascarefully mapped,resultinginthedocumentationof274complete footprintsleftbyninedifferentindividuals.Radiocarbon datingoftorchcharcoalassociatedwiththeprints indicatesthattheprehistoriccaversenteredthispassage some5,400yearsago(basedoncalibratedradiocarbon ages),theearliestdark-zonecaveexplorationyetknown fortheeasternU.S.(Robbinsetal.,1981;Watsonetal., 2005). OtherdiscoveriesbyNSScaverssoonfollowedthe JaguarCavework.3rdUnnamedCave,Tennessee,first reportedtocontainafewaboriginalfootprintspreservedin aremotepassage,wasfoundduringsubsequentarchaeologicalinvestigationbyWatsontobeasignificantchert quarry,whichalsocontainedpetroglyphsontheceilingof thequarrypassage.Theglyphsandassociatedquarrying activity,whichdatestotheLateArchaicandEarly Woodlandperiods,wasfirstpublishedbyCharlesH. Faulkner(1988),andlaterwasmorethoroughlydescribed byJanSimek(etal.,1998).Twelveoffourteenradiocarbon datesfrom3rdUnnamedCavefallbetween2800and 3800yearsB.P.(calibratedages;Crothersetal.,2002). Analysisofthechertquarryingactivityeventuallybecame JayFranklin’sMaster’sthesisprojectattheUniversityof Tennessee,Knoxville(Franklin,1999). Alsoduringthe1980s,membersoftheDetroitUrban Grotto,whoweremappingtheFisherRidgecavesystem eastofMammothCaveNationalPark,discoveredafew isolatedprehistoricfootprintsandalargecrosshatched petroglyphfarbackinthedarkzoneofthisextensivecave. CRFArcheologicalProjectpersonneldocumentedthe printsandpetroglyphandobtainedtworadiocarbondates onassociatedcharcoal(2800–3600calibratedyearsB.P.; Kennedyetal.,1984),butthesitehasnotbeenfully published. UndertheauspicesoftheCRFArcheologicalProject, CrotherscompletedaSeniorHonorsThesisatWashington Universityin1981documentingtheremainsleftbywouldberescuersinSandCave,Kentucky,duringtheirfailed attemptstofreeFloydCollins,whowastrappedanddied therein1925.Oneofthefirstapplicationsofhistorical archaeologytoacavesetting,thisthesiswaspublishedin the NSSBulletin (Crothers,1983). Intheearly1980s,alocalcaverdiscoveredprehistoric drawingsonmud-coatedwallsinaneastTennesseecave, whichhereportedtoHowardEarnest,aU.S.Forest Servicearchaeologist,andCharlesH.Faulkneratthe UniversityofTennessee,whoagreedtoinvestigatethesite. FaulknerenlistedthehelpofNSScaversfromtheEast Tennesseearea,especiallytheSmokyMountainGrotto, todocumentandultimatelytogatethisimportantlate G EORGE C ROTHERS ,P.W ILLEY AND P ATTY J O W ATSON JournalofCaveandKarstStudies, April2007 N 29

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prehistoric(Mississippian)ceremoniallocale(Faulkneret al.,1984;Faulkner,1986).Faulkner’sworkatthissite, whichcametobeknownasMudGlyphCave,initiated acavearchaeologyprogramatTennesseethatcontinues today.TheMudGlyphCaveprojectwasparticularly importantbecauseitalertedthecavingcommunitytothese fragileremains,andmanymoresuchsubtlydecorated caveshavenowbeenreportedfortheKentucky-TennesseeAlabama-Georgiakarstregion(e.g.,Faulkner,1988,1997; FaulknerandSimek,1996;Simeketal.,1997). InMay1986,forexample,NSScaversattendingthe annualLouisvilleGrotto’sSpeleofestfoundanextensive arrayofgeometricrenderingstracedinthemudfloorof alarge,lowroomwellbackinthedarkzoneofacavenow knownasAdairGlyphCave.ThecaversnotifiedPhilip DiBlasi,aUniversityofLouisvillearchaeologist,who subsequentlyobtainedaradiocarbondeterminationfor charcoalintheglyphroom,indicatingthattheglyphsdate totheLateArchaicperiod(3500–4200calibratedyears B.P.;DiBlasi,1996),similarintimetothe3rdUnnamed Cavedates. Anotherveryimportantdiscoveryofancientsymbolic renderingsinacavedarkzonewasmadeduringtheearly 1990satasiteinMissouriknownasPictureCave(DiazGranadosandDuncan,2000,Plates12–17).Incontrastto AdairGlyphCaveandMudGlyphCave,theartworkin PictureCave(whichislateprehistoric,hencemuchcloser inagetotherenderingsinMudGlyphthantothosein AdairGlyphCave)consistsprimarilyofpictographs createdinred,black,and,rarely,whitepigments.Many oftheitemsandentitiesdepictedcanbefairlyreadily referredtothemes,events,orsupernaturalbeingsdescribed inthecomplexoraltraditionsofethnographicallyand ethnohistoricallyknownmidcontinentalAmericanIndian groups. In1981,NSScaversfromtheClaytonCountyCavers Grottorediscoveredevidenceofprehistorichumanactivity inBigBoneCave,Tennessee(BlairandSneed,1983; Matthews,2006,p.145),thesamecavethatHenryMercer visitedin1896.BlairandSneeds’smuchmorerecent discoveriesandsubsequentreportingtoWatsoneventually ledtoCrothers’sMaster’sthesisprojectattheUniversity ofTennessee(Crothers,1986,1987).BigBoneCave,like MammothandSaltscaves,hasexceptionalpreservation andcontainsnumeroustorchremnants,gourdbowls, wovenbags,andfootwearleftbyprehistoricgypsum miners.Infact,oneimportantresultofBigBoneCave archaeologyisdemonstratingthatpre-Columbiangypsum miningwasawidespreadactivityextendingwellbeyond theMammothCaveregion. LarryMatthews’summaryofBigBoneCavespeleologicalhistoryhasjustbeenpublishedbytheNSS (Matthews,2006).Thisvolumecontainsnumerousillustrationsanddescriptionsofhistoricandprehistoric remainsinthecave,andisagoodguidetotheabundant literatureonthisfamousTennesseesite. In1988,NSScaversdiscoveredasmallcave,highup intheColoradoRockyMountains,thattheynamed Hourglass.Subsequently,whilemappingpassagesseveral hundredmetersintothedarkzoneofHourglassCave,they cameuponhumanskeletalremainstheythoughtwere prehistoric.Theycontactedarchaeologistsandother appropriatepersonnelwhoseinvestigationsrevealedthat thebonesarethoseofamanapproximately45yearsold whodiedinthecavenearly8000yearsago(Mosch andWatson,1997).Thisseemstobetheearliestrecord intheAmericasofdark-zoneexplorationinahigh-altitude cave. Beginninginthe1960swhentheAssociationfor MexicanCaveStudieswasinitiated(forahistory,see http://www.amcs-pubs.org/),andbecomingespeciallynoticeablesincethe1980s,NSScavershavebeenactively involvedinMesoamericancavearchaeology.Onerecent resultistheNSSMayaCavesProject(SchaefferandCobb, 1991).Archaeologistsandcavershavebeenparticularly activeinBelize(McNatt,1996;Moyes,2002;Peterson, 2006),Guatemala(BradyandScott,1997),andMexico (HapkaandRouvinez,1997;Rissolo,2003).TheNSS2004 RalphStoneGraduateFellowshipwasawardedtoastudy ofkarsticandsacredlandscapesataLateClassicsitein Guatemala.Evenmorerecently,severalNSSmembers exploringhigh-altitudecavesinSouthAmerica(Peru)have foundnumerousarchaeologicalmaterials,includinghumanremains(Knutson,2006). Throughthe1980sandintothe1990snewarchaeologicaldiscoveriesincavesclearlyhadasynergisticeffect, drivingdiscoveriesofmorearchaeologicalmaterialin cavedarkzones.Ascaversreportedsitesandthesefinds becameknownthroughpresentationsandpublications, morecaverscameforwardwithotherdiscoveries.Watson alsotaughtasummerfieldcourseincavearchaeology duringthemid-1980satMammothCavethrough WesternKentuckyUniversity’sCenterforCaveand KarstStudiesthatwaspopularamongNSScavers. Somewhatlaterinthe1980sand1990s,twoEarthwatch Institutefundedvolunteerprojectswerebegunthat integratedcaversintostructuredarchaeologicalresearch projects.OneistheMayaCeremonialCavesProject (1988–1992),theotheristheCulturalResourcesSurvey ofMammothCave(1993–2005).Suchspecializedcourses andactivearchaeologicalprojectsthatwelcomevolunteerscanintroducecaverstothenatureofarchaeological remainsfoundincavesandtothewealthofinformation thatcanbeobtainedwhenresourcesareprotectedand carefullystudied. B IOARCHAEOLOGYINTHE D ARK Z ONEOF C AVES Bioarchaeologyisthestudyofhumanbiologyrevealed inarchaeologically-recoveredhumanremains,mostoften wholeorpartialskeletons.Thisinformationprovides insightsintothelivesandbiologicalcharacteristicsofpast C AVEARCHAEOLOGYANDTHE NSS:1941–2006 30 N JournalofCaveandKarstStudies, April2007

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peoples,suchaspopulationstructure,health,illness,and diet.Cavebioarchaeologyisbioarchaeologyappliedto humanremainsfoundincaves. Cavebioarchaeologyfocusesuponseveraldifferent datasources:humanskeletalandmummifiedremains, paleofeces,andfootprints.Beforeinformationofanysort canbegained,however,suchmaterialsmustberecognized andreportedtorelevantspecialistswhocancarryout appropriateresearchwhileprotectingthesefragileremains (Hubbard,1996).TheNSSanditsmembershave contributedtobioarchaeologicalknowledgebyreporting humanremainsfoundunderground. Humanremainsincavesareeithermummiesor skeletons.Asnotedabove,mummieshavebeendescribed fromcavesinPeru(Knutson,2006)aswellasfrom KentuckyandTennesseecaves(Robbins,1971;Tankersley etal.,1994;WatsonandYarnell,1986).Contraryto nineteenthcenturypractices(seeGeorge,1990,1994; Meloy,1971),mummiesarenowusuallyexamined insitu incavesandleftthereifsecuritycanbeguaranteed.Where remainsarenotthreatenedbydestruction,preservationin placeisthepreferredalternativetocollectionandcuration ofhumanremains,indeferencetowishesofmanyNative Americans. Moreoftenthanmummies,prehistoricskeletonsor partialskeletonsarefoundincaves.ThereareseveralNSSrelatedsummariesconcerningcaveskeletonsforseveral southeasternU.S.states(HubbardandBarber,1995,1997; Turner,1985;Willey,1985). Sometimesskeletonsincaveshavebeenstudied insitu andinothercasestheyhavebeenremovedforlaboratory analysisandcuration.Asjustnotedformummiesfoundin caves,itispreferabletoleavehumanskeletalremains in situ undergroundunlesstheyarethreatenedbylootingor otherdestruction. Insitu analysismaylimittheinformationthatcanbegathered,butinsomesituations,suchas pitcaveswhereremainsareexposedinthetaluscone,basic datacanbecollectedwithoutdisturbingthebones.Bull ThistleCave,Virginia,isanexampleofanundisturbedpit cavewherehumanbonesexposedonthefloorofthepit weredocumented,andthenthecavewasgatedtoprotect thesite(WilleyandCrothers,1986). Unfortunately,remainsincavesarevulnerableto looting,sobioarchaeologistsmayhavetoremoveskeletal materialforcurationaboveground.Thereare,however, someinstancesofremainslootedfromTennesseecaves thatweresubsequentlyrecovered,analyzed,andpublished (WhyteandKimball,1997;Willeyetal.,1988). Reportsofrecentlyexcavatedanddescribedcave skeletonsincludethosefromTexaspits(Bementand Turpin,1991;Ralphetal.,1986;Turpin,1985),from HourglassCaveintheRockyMountains(Moschand Watson,1997),fromanorthwestGeorgiacave(Crothers, 1991;SneedandSneed,1991;Willey,1991),from southwestVirginiacaves(BoydandBoyd,1997),from centralKentuckycaves(Haskins,1988),andfromanEast Tennesseecave(Faulkner,1987).Inonecase,analysisof skeletonsoccurreddecadesaftertheywereexcavated (Tucker,1989). Mostoftheseskeletalreportsaredescriptive,usually includingbasicdataforeachindividual(ageatdeath,and sex),paleopathology(diseasesandinjuries,suchashealed fractures),andalterationstothebonesafteroriginal deposition.Suchreportsarequitegeneral,andusually lackproblem-orientedapproaches.Incontrast,thereare afewspecializedanalysesofhumanbonesfromcaves. Theseincludetheuseofgeographicinformationsystems andestimationsoftheminimumnumberofindividuals fromHondurancaves(Herrmann,2002),rodentmodificationsofbonesinaMiddleTennesseecave(Klippel andMeadows,1991),reconstructionofdietbasedonthe dentalpathologycharacteristicofremainsfoundin aTexascave(Marksetal.,1991),DNAanalysisofthe HourglassCaveskeleton(StoneandStoneking,1996), andinferenceofprehistoricdietsbasedonstableisotope dataforskeletonsfromaVirginiacave(Trimbleand Macko,1997). Themostcommonbioarchaeologicalremainsfoundin caves,otherthanhumanbone,arehumanpaleofecal deposits.Paleofecalanalysiswasanimportantpartofthe CRFArcheologicalProjectbecauseofthedirectdietary informationtheycontain(GremillionandSobolik,1996; Marquardt,1974;Stewart,1974;Yarnell,1969,1974).In additiontodietaryconstituentsofthepaleofeces,analysts havestudiedpollen(Bryant,1974;Schoenwetter,1974)and endoparasites(DusseauandPorter,1974;Fry,1974),and haveevenretrievedhormonaldatatodeterminesexofthe defecator.Inastudyof12specimens,alltwelveindicated malehormonalratios(Soboliketal.,1996).Inastudyof humanpaleofecesfromBigBoneCave,CharlesT. Faulkner(Faulkner,1991;Faulkneretal.,1989)examined dietarycomponentsandevidenceforendoparasiticinfection.HisanalysiswasaidedbyagrantfromtheNSSto radiocarbondateoneofthespecimens. Prehistoricfootprintsareperhapstherarestofall bioarchaeologicalmaterials,havingbeenfoundinonly afewcaves.NSScaversdiscoveredmostoftheprehistoric footprintsdocumentedinNorthAmericancaves.Sofar, onlytheprehistoricfootprintsinJaguarCavehavebeen adequatelydescribed(Robbinsetal.,1981;Watsonetal., 2005;Willeyetal.,2005),thanksinlargeparttosupportby NSSmemberswhoreportedthediscovery,mappedthe cave,andaidedinphotographingandcastingthefoot impressions. C ONCLUSIONS Archaeologyinthedarkzonesofcaveshascomeinto itsownastheNSScelebratesitssixty-fifthanniversary. Thereareagrowingnumberofarchaeologistswho specializeinthenuancesofdoingarchaeologyunderground.Itisnowmorecommontoincludechapterson G EORGE C ROTHERS ,P.W ILLEY AND P ATTY J O W ATSON JournalofCaveandKarstStudies, April2007 N 31

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thearchaeologyofcaveresourcesinsyntheticand regionalworks(e.g.,Crothersetal.,2002),andthere arenowenoughpractitionerstomakeuplargeportions ofeditedvolumes(e.g.,CarstensandWatson,1996)or entirejournalissues(e.g.,SherwoodandSimek,2001; Steele,1997).Nationalandregionalarchaeologicalconferencesnowcommonlyhaveentiresymposiadedicated toarchaeologicalcavetopics(e.g.,Symposium:Cave ArcheologyintheAppalachianMountains,Journalof CaveandKarstStudiesv.59,p.132–165).Archaeologists arealsobeginningtoinvestigatesaltpeterminingcave sitesinasystematicfashion(Duncan,1997),anaspectof historicarchaeologyincavesthathasbeentoolong neglected. InadditiontotheCRFArcheologicalProjectandseveral Mesoamericancavearchaeologyprojects(seetheMesoamericanCaveArchaeologyNetworkhttp://www.calstatela.edu/ academic/anthro/mesocave.htmlforacurrentlisting),there areactivecavearchaeologyprogramsatCaliforniaState University-LosAngeles(directedbyJamesBrady),the UniversityofKentucky(directedbyGeorgeCrothers),and theUniversityofTennessee-Knoxville(directedbyJan Simek).Althoughtherearenowmanymoreformallytrained specialistscarryingoutresearchincavearchaeologythanever before,NSSavocationalcaverswillcontinuetobeindispensabletothediscoveryanddocumentationofarchaeological remainsinthedarkzonesofcaves. A CKNOWLEDGEMENTS Wewouldliketothankthemanycavers,overtheyears, whohavediscovered,reported,andprotectedmanyofthe archaeologicalsitesdescribedhere.CharlesH.Faulkner andRonaldC.Wilsoneditedandprovidedcommentson themanuscript.Weespeciallythankthemfortheirinterest andcontributionstocavearchaeology.Wealsothank MalcolmFieldforhisinvitationtocontributetotheJCKS anniversaryissue. R EFERENCES Bement,L.C.,andTurpin,S.A.,1991,Preliminaryresultsofthe archaeologicalinvestigationofBeringSinkhole:Astratifiedsinkhole cemeteryincentralTexas[abs.]:BulletinoftheNationalSpeleological Society,v.53,no.2,p.37. Bennington,F.,Melton,C.,andWatson,P.J.,1962,Carbondating prehistoricsootfromSaltsCave,Kentucky:AmericanAntiquity, v.28,p.238–241. Blair,L.O.,andSneed,J.M.,1983,ArchaeologicalinvestigationsinBig BoneCave,Tennessee:NSSNews,v.41,p.211–212. Boyd,C.C.,andBoyd,D.C.,1997,Osteologicalcomparisonofprehistoric NativeAmericansfromSouthwestVirginiaandEastTennessee mortuarycaves:JournalofCaveandKarstStudies,v.59,p.160–165. Brady,J.E.,andScott,A.,1997,Excavationsinburiedcavedeposits: implicationsforinterpretation:JournalofCaveandKarstStudies, v.59,p.15–21. Bryant,Jr.,V.M.,1974,Pollenanalysisofprehistorichumanfecesfrom MammothCave, in Watson,P.J.,ed.,ArcheologyoftheMammoth Cavearea:NewYork,AcademicPress,p.203–210. Carstens,K.C.,andWatson,P.J.,1996,OfCavesandShellMounds: Tuscaloosa,UniversityofAlabamaPress,209p. Crothers,G.M.,1983,ArchaeologicalinvestigationsinSandCave, Kentucky:BulletinoftheNationalSpeleologicalSociety,v.45, p.19–33. Crothers,G.M.,1986,Finalreportonthesurveyandassessmentofthe prehistoricandhistoricarchaeologicalremainsinBigBoneCave,Van BurenCounty,Tennessee:DepartmentofAnthropology,University ofTennessee,Knoxville. 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McNatt,L.,1996,CavearchaeologyinBelize:JournalofCaveandKarst Studies,v.58,p.81–99. Meloy,H.,1971,MummiesofMammothCave:Shelbyville,Indiana, MicronPublishing,42p. Mercer,H.C.,1896,CaveexplorationbytheUniversityofPennsylvaniain Tennessee:TheAmericanNaturalist,v.30,p.608–611. Mercer,H.C.,1897,ThefindingoftheremainsofthefossilslothatBig BoneCave,Tennessee,in1896:ProceedingsoftheAmerican PhilosophicalSociety,v.36,p.36–70. Mercer,H.C.,1975,TheHill-cavesofYucatan:Norman,Universityof OklahomaPress,183p.Originallypublished1896,Philadelphia,J.B. Lippincott. Mosch,C.J.,andWatson,P.J.,1997,AnancientRockyMountaincaver: JournalofCaveandKarstStudies,v.59,p.10–14. Moyes,H.,2002,TheuseofGISinthespatialanalysisofan archaeologicalcavesite:JournalofCaveandKarstStudies,v.64, p.9–16. Peterson,P.A.,2006,AncientMayaritualcaveuseintheSibunValley, Belize:Austin,AssociationforMexicanCaveStudies,Associationfor MexicanCaveStudiesBulletin16,148p. Pond,A.W.,1937,LostJohnofMummyLedge:NaturalHistory,v.39, p.176–184. 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Steele,J.F.,ed.,1997,CavearchaeologyinNorthAmericaand Mesoamerica,specialissueofJournalofCaveandKarstStudies, v.59,no.1. Stewart,R.B.,1974,Identificationandquantificationofcomponentsin SaltsCavepaleofeces,1970–1972, in Watson,P.J.,ed.,Archeologyof theMammothCavearea:NewYork,AcademicPress,p.41–47. Stone,A.C.,andStoneking,M.,1996,Geneticanalysesofan8000yearoldNativeAmericanskeleton:AncientBiomolecules,v.1,p.83–88. Tankersley,K.B.,Frushour,S.S.,Nagy,F.,Tankersley,S.L.,and Tankersley,K.O.,1994,ThearchaeologyofMummyValley,Salts Cave,MammothCaveNationalPark,Kentucky:NorthAmerican Archaeologist,v.15,p.129–145. Trimble,C.,andMacko,S.,1997,Stableisotopeanalysisofhuman remains:Atoolforcavearchaeology:JournalofCaveandKarst Studies,v.59,p.137–142. Tucker,C.,1989,Areanalysisoftheosteologicalandculturalremains fromAusmusBurialCave,ClaiborneCounty,Tennessee(3CE20) [MAthesis]:Knoxville,UniversityofTennessee,112p. Turner,K.R.,1985,HumanbonesinAlabamacaves[abs.]:Bulletinofthe NationalSpeleologicalSociety,v.47,no.2,p.58. Turpin,S.A.,compiler,1985,SeminoleSink:excavationofaverticalsha ft tomb,ValVerdeCounty,Texas:Austin,UniversityofTexas,Texas ArchaeologicalSurveyResearchReportNo.93,216p. Watson,P.J.,1966,Preliminaryreport:archaeologicalandpaleoethnobotanicalinvestigationsinSaltsCave,MammothCaveNationalPark: NSSNews,v.24,p.177. Watson,P.J.,1969a,TheprehistoryofSaltsCave,Kentucky:Springfield IllinoisStateMuseum,ReportsofInvestigationsNo.16,86p. Watson,P.J.,1969b,ArchaeologicalinvestigationsinSaltsCave, MammothCaveNationalPark,Kentucky:ProceedingsoftheIVth InternationalCongressofSpeleologyinYugoslavia,v.4–5, p.403–407. Watson,P.J.,ed.,1974,ArcheologyoftheMammothCavearea:New York,AcademicPress,255p.Reprinted,1997,St.Louis,CaveBooks. Watson,P.J.,1998,Archaeology, in Northup,D.,Mobley,E.,Ingham, III,K.,andMixon,W.,eds.,Aguidetospeleologicalliteratureofthe Englishlanguage1794–1996:St.Louis,CaveBooks,p.5–9. Watson,P.J.,2001,Theoryincavearchaeology:MidcontinentalJournal ofArchaeology,v.26,p.139–143. Watson,P.J.,andYarnell,R.A.,1966,ArchaeologicalandpaleoethnobotanicalinvestigationsinSaltsCave,MammothCaveNationalPark, Kentucky:AmericanAntiquity,v.31,p.842–849. Watson,P.J.,andYarnell,R.A.,1986,LostJohn’slastmeal:The MissouriArchaeologist,v.47,p.241–255. Watson,P.J.,Kennedy,M.C.,Willey,P.,Robbins,L.,andWilson,R.C., 2005,PrehistoricfootprintsinJaguarCave,Tennessee:Journalof FieldArchaeology,v.30,p.25–43. G EORGE C ROTHERS ,P.W ILLEY AND P ATTY J O W ATSON JournalofCaveandKarstStudies, April2007 N 33

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White,W.B.,2003,Science,theNSS,andtheJournalofCaveandKarst Studies:isitsciencewithoutajournal?:JournalofCaveandKarst Studies,v.65,p.91–92. Whyte,T.R.,andKimball,L.R.,1997,Scienceversusgravedesecration: thesagaofLakeHoleCave:JournalofCaveandKarstStudies,v.59, p.143–147. Willey,P.,1985,HumanbonesinTennesseecaves[abs.]:Bulletinofthe NationalSpeleologicalSociety,v.47,no.2,p.58. Willey,P.,1991,ExcavatedhumanskeletonsfromLittleBeaverCave[abs. ]: BulletinoftheNationalSpeleologicalSociety,v.53,no.2,p.36–37. Willey,P.,andCrothers,G.,1986,Archaeologicalandosteologicalsurv ey ofBullThistleCave(44TZ92),Virginia:ReportsubmittedtoVirginia DivisionofHistoricLandmarks,Richmond,43p. Willey,P.,Crothers,G.,andFaulkner,C.H.,1988,Aboriginalskeletons andpetroglyphsinOfficerCave,Tennessee:TennesseeAnthropologist,v.13,p.51–75. Willey,P.,Stolen,J.,Crothers,G.,andWatson,P.J.,2005,Preservatio n ofprehistoricfootprintsinJaguarCave,Tennessee:JournalofCave andKarstStudies,v.67,p.61–68. Yarnell,R.A.,1969,Contentsofhumanpaleofeces, in Watson,P.J.,ed., TheprehistoryofSaltsCave,Kentucky:Springfield,IllinoisState MuseumReportsofInvestigationsNo.16,p.41–54. Yarnell,R.A.,1974,IntestinalcontentsoftheSaltsCavemummyand analysisoftheinitialSaltsCaveflotationseries, in Watson,P.J.,ed., ArcheologyoftheMammothCavearea:NewYork,AcademicPress, p.109–112. C AVEARCHAEOLOGYANDTHE NSS:1941–2006 34 N JournalofCaveandKarstStudies, April2007



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CAVEMINERALOGYANDTHENSS: PAST,PRESENT,FUTURE C AROL A.H ILL 1 AND P AOLO F ORTI 2 Abstract: ThepurposeofthispaperistotracetheNationalSpeleologicalSociety’s past,present,andfutureinvolvementwiththescienceofcavemineralogy ,inaccordance withthecelebrationoftheNSS’s65 th Anniversary.IntheNSS’sfirstdecade(1940s), anumberofarticlescoveringmineralogytopicswerepublishedingrotton ewsletters,the NSSNews and NSSBulletin ,butitwasn’tuntilthe1950sand1960sthatitpublished professionalscientificpapersonthissubject.TheSociety’sfirsthuge commitmenttothis fieldwasintheirpublicationof CaveMinerals in1976,thefirstbookintheworldon cavemineralsandthefirstbookeverpublishedbytheNSS.Thebookseries Cave MineralsoftheWorld ,thesecondeditionofwhichwaspublishedin1997,hasbecomethe standardreferenceonthesubject.Importantfieldsoffutureresearchin cavemineralogy thattheNSSmaybecomeinvolvedwitharethoseofpaleo-environments,mic robiology, andmineralsontogeny. I NTRODUCTION TheNationalSpeleologicalSociety(NSS)hasbeen instrumentalinpromotingthescienceofcavemineralogy throughitspublicationofthe NSSBulletin (nowthe JournalofCaveandKarstStudies ),the NSSNews ,and threeeditionsof CaveMinerals / CaveMineralsofthe World .Wewillfirstdescribetheearlyyearsfrom1940 (whenthefirstissueofthe NSSBulletin cameout)to1976 whentheSocietypublisheditsfirstbook, CaveMinerals Thenwewillspecificallytracethehistoryofthe Cave Minerals bookseriesinvolvingbothoftheauthors,and finallywewillpresentwhatwefeelaresomepromising areasforfuturecavemineralogywork.Foravoluminous, descriptivetextoncavemineralsandspeleothems,the readerisreferredtotheNSS’sbook CaveMineralsofthe World (HillandForti,1997).Forshorterreviewsonthe differentclassesofcavemineralsandspeleothemtypes refertothearticlesbyHillandForti(2004a,b)andForti andHill(2004)inthe EncyclopediaofCavesandKarst Science P AST T HE E ARLY Y EARS (1940–1975) TheNationalSpeleologicalSociety’ssupportofcave mineralogyintheearlyyearswasmainlythroughthree avenuesofpublication: (1)Grottopublications,wherememberswritingtrip reportsoncavestheyhadbeenmappingorexploring alsomentionedthemineralsandspeleothemsobserved therein.Anexcellentexampleofsuchearlygrotto publicationsisthenumerousreportsbyWilliam Hallidayinthelate1940sand1950sinthe California Cave rand SaltLakeCityGrottoNewsletter (2) NSSNews publicationofshortmineraldescriptions regardingspecificcaves. (3) NSSBulletin publicationofscientificreportsrelatedto cavemineralogy. Thesereportsconstitutedthemostimportantaspectofthe NSS’searlyinvolvementwithcavemineralogybecause theysetthefoundationforfuturescientificpublications, includingthefirst CaveMinerals book. Whileitisnotwithinthescopeofthispapertoinclude alloftheearlyarticlesthatcontributedtothisscientific foundation,someofthemoreimportantworkwillbe mentioned,bothwithregardtotherecognitionofnew mineralsorspeleothemtypes,andwithregardtoearlyNSS attemptstoformcommitteesorsymposiaonthetopicof cavemineralogy. Thefirstpublishedaccountofcaveminerals/speleothemsinthe NSSBulletin wasbyRoyHoldenin 1940,intheveryfirstissueofthe Bulletin ,wherehe describedtheLurayCavernshelictitesandofferedmodes oforigin(Holden,1940).Holdenwasalsothefirstto reportthefluorescenceofcalcitespeleothemsinaUnited Statescavein1944(Holden,1944a),andhechairedthe firstNSScommitteeonmineralsandformationsin1944 (Holden,1944b).WilliamFosterin1949reportedon mineralogicdatainspeleothemwork,andhealsochaired theNSScommitteeonformationsandmineralogyin1951 (Foster,1949,1951).Henderson(1949)wasthefirstto describeanthoditesasaspeleothemtypefromSkyline Caverns,Virginia,andWarwick(1950)wasthefirstto observeandreportinthe NSSBulletin theoccurrenceof calcitebubbles,whichalsobecameanewspeleothemtype. Whileallofthese1940articleswereimportantfirst attemptstodescribecavemineralsandspeleothems,overall 1 EarthandPlanetarySciences,UniversityofNewMexico,200YaleBlvd.,No rthrop Hall,Albuquerque,NM,USA87131,carolannhill@aol.com. 2 InstitutoItalianodiSpeleologia,ViaZamboni67,Bologna,Italy40127, forti@geomin.unibo.it. CarolA.HillandPaoloForti–CavemineralogyandtheNSS:past,present,f uture. JournalofCaveandKarstStudies, v.69,no.1, p.35–45. JournalofCaveandKarstStudies, April2007 N 35

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therewasn’tmuchhappeningintheNSSincave mineralogypriortothe1950s. In1952,GeorgeMooreintroducedthetermspeleothem foranysecondarymineraldepositformedincaves(Moore, 1952).Despitesomeobjectionstothistermovertheyears,it hasstuckandisnowtheofficialnameinthe Glossaryof Geology forwhatusedtobereferredtoasacaveformation. Laterinthe1950s,Crisman(1956)reportedbothmonocrystallinehelictitesandstalactitesfromtheCavernsof Sonora,Texas,thefirstreportofmonocrystallinespeleothems inaUnitedStatescave.DaviesandMoore(1957)werethe firsttoreportacaveoccurrenceofthemineralsendelliteand hydromagnesiteanywhereintheworld,andGood(1957), alsoworkinginCarlsbadCavernatthesametimeasDavies andMoore,wasthefirsttoreportacaveoccurrenceofthe mineralmontmorilloniteanywhereintheworld. Intheearly1950sayoungundergraduatechemistry student,whotookaspecialinterestincavemineralogy, emergedfromtheNSScaverrankstobecomeoneofthe leadersinthisfieldforthenextfivedecades:WilliamB. White.Whitepublishedanumberofmineraldescriptionsin grottopublicationsinthelate1950sandwentontopublish areviewofcavemineralstudiesfor1955–1960in1961 (White,1961),andalsotochairthefirstNSSsymposiumon cavemineralogy(White,1962).Thissymposiumwasheldin December,1960attheNewYorkmeetingoftheAmerican AssociationfortheAdvancementofScience,andwasoneof thefirstattemptstomergecavemineralogyintomainstream science.Thissymposiumwasalsothemostprofessionalof allthepublicationsdonebytheNSSoncavemineralogyup tothistime. GeorgeMoorecontinuedtowriteseminalpapersinthe NSSBulletin ,oneontheoriginofhelictitesin1954 (Moore,1954)andanotheronthegrowthofstalactitesin 1962(Moore,1962),plushewasthefirsttoreport dolomiteasacavemineralin1961(Moore,1961).Another NSSmemberwhocontributedimportantscientificpapers oncavemineralogyinthe NSSBulletin inthe1960s–early 1970swasRaneCurl,whopublishedonthearagonitecalciteproblemin1962andontheminimumdiameterof stalactitesandstalagmitesin1971(Curl,1962,1971). Thayer(1967)wasthefirsttoproposeinthe NSSBulletin thenameconuliteforanewspeleothemtypethathe describedassimpledrip-drilledmudpitslinedwithcalcite. Amongalloftheearly(1940–1975)workersinU.S. cavemineralogywhopublishedwiththeNSS,William (Bill)Halliday,GeorgeMoore,andWilliam(Will)White standoutasthethreepersonswhoprobablycontributed themostinformationtothisfield. H ISTORYOFTHE N ATIONAL S PELEOLOGICAL S OCIETY’S B OOK C AVE M INERALSOFTHE W ORLD 1970 ItallbeganonJanuary18,1970,whenAllanP.Haarr, formerNSSExecutiveVicePresidentandmemberof ElaineHackerman’sMiscellaneousPublicationsCommittee,askedCarolHilltowriteachapteroncaveminerals andspeleothemsfortheNSS’s Caver’sHandbook .Al HaarrknewthatCarolwasinterestedincavemineralogy andthatshehadbeencollectinganumberofarticlesonthe topic.HealsoknewthatbecauseCarolhadmovedtoNew Mexico,shehadbeenworkingonthemineralogyof CarlsbadCavernandothercavesintheGuadalupe Mountains.Thus,AlHaarraskedCaroltocontributean approximately50page-longchaptertothe Caver’s Handbook ,remarking:‘‘Iseethischapterasafairly completearticleonthevariousspeleothemsandtheir theoriesofformation.’’WhatAlHaarrdidn’tknowisthat inCarol’sviewcompletereallymeantcomplete,andthat Carolrarelywritesanythingshort.Thusbeganthesagaof CaveMineralsoftheWorld 1970–1971 FortwoyearsCarolHillgatheredtogetherallofthe UnitedStatescavemineral/speleothemarticlesshecould find,andfromthisinformationandherownpersonal researchwroteachapteroncavemineralogyforthe Caver’sHandbook .However,thismanuscriptturnedoutto bemuchlongerthanthe50pagesoriginallyintendedby theMiscellaneousPublicationsCommittee.Alsobythis time,anumberofphotographshadbeenobtainedforthe chapter,especiallyfromcavephotographerPeteLindsley. ThusadilemmaarosewithintheNSS:Whattodowith thismuch-longer-than-anticipatedmanuscript? 1972 Toresolvethisdilemma,DaveIrving,thenontheNSS boardofgovernors(BOG),suggestedthatthechapterbe madeintoabooktobesoldexternallytothepublicaswell astoNSSmembers.Thissuggestiongeneratedamajor controversywithintheNSS,thefearbeingthatthebook wouldpromotevandalismoncethegeneralpublicfound outwhattreasuresactuallyexistincaves.AlHaarr remarkedinhisFebruary8,1972lettertoCarolHillthat: ‘‘Ifeelyourchapterisneededandusefulbutnotworthan internalfight’’(withintheNSS),andhethusfavored publicationonlytoNSSmembersandgeologists,andthen onlyifthebookcontainedastrongconservationmessage. OtherNSSboardmembersdisagreedandthoughtthatthe publicationofabookoncavemineralswasanexcellent waytoeducatethepublicastocaveconservation.Also, saleofthebookcouldbeawayofbringingmuchneeded revenueintotheNSS.ItwasfinallydecidedthatCarol’s book, CaveMinerals ,wouldbepublished,albeitwith astrongconservationmessageandwithnocavelocations divulged.ASpecialPublicationsCommitteethenemerged fromtheformerMiscellaneousPublicationsCommitteeto handle CaveMinerals andotherpotentialbookmanuscripts.InJuneof1972, SpeleoPress providedthelowest bidoutoffive,andwasawardedthecontracttoprint Cave Minerals C AVEMINERALOGYANDTHE NSS: PAST,PRESENT,FUTURE 36 N JournalofCaveandKarstStudies, April2007

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1973 ItwastheNSS’splantohave CaveMinerals printed andavailableforsalebythe1973NSSConvention,butby thistimetheactofpublishingthebookhadturnedinto atotalfiasco,toquoteAlHaarr.Theproblemsweretwofold:(1)CarolHillhadneverwrittenabookbefore,and (2)theNSShadneverpublishedabookbefore.Therewas nopersonontheSpecialPublicationsCommitteethat actuallyhadtheexperiencetohandlesuchthingsasdealer quotes,bookorders,pricefixing,reprintrights,production schedules,interfacingwithprinters,advertising/marketing, etc.,allofwhichneededtobespelledoutandapprovedby theBOG.Inaddition,BOGmemberDwightDealfelt compelled(orwascompelledbytheBOG)totakeonthe dauntingtaskofmakingsurethebookmetprofessional standardsandwasproperlyreviewed.Sothepublicationof CaveMinerals draggedonandon. 1976 ByMarchof1976,thebookhadbeenlanguishingat SpeleoPress formanymonthsandhadstillnotbeen printed.Therefore,then-NSSExecutiveVicePresident James(Moose)Dawsongave SpeleoPress anultimatum: eitherhavethebookprintedintimefortheMorgantown, WestVirginiaConventioninJune,ortheNSSwould cancelitscontractwith SpeleoPress .Thusitwasthat Cave Minerals becamethefirstbookpublishedbytheNational SpeleologicalSocietyforageneralaudience,andthevery firstbookintheworldpublishedonthetopicofcave mineralogy(Hill,1976). CaveMinerals was137pageslong andcontained475references,whichincludedmostofthe U.S.cavemineralogyliteratureandsomereferencesfrom GreatBritainandAustralia,butwhichbarelytouched uponthenon-EnglishEuropeanliterature.Thebookhad acoloredcover:TheButterflyfromCavernsofSonoraby PeteLindsley(Fig.1),buttherestofthephotographswere inblackandwhite. 1978 By1978thesaleof CaveMinerals hadwanedbecauseof thefailureoftheNSStoadvertisethebook,eventoNSS cavers,whoapproachedCarolHillaskingwherethey couldbuythebook.ThispromptedCaroltowritetothenNSSpresidentCharlieLarsonandtheBOGtoaskforan NSScommitmenttoproperlysellthebook.However,one importantpersonwhowasabletobuyacopyof Cave Minerals wasPaoloFortioftheInstituteofSpeleologyin Bologna,Italy.Paolowasperhapsonlyoneofacoupleof Europeanswhoreadallofthe NSSNews issues,andinthis wayhehadbecomeawareoftheexistenceofCarol’sbook. Paoloimmediatelyboughtprobablythefirstcopyof Cave Minerals soldinEurope.Paolowasextremelyinterestedin Carol’sbookbecauseatthattimehewasputtingtogether ashortbookletofhisownonEuropeancaveminerals. Paolosentacopyofthisbooklet,andmanyotherofhis publications,toCarolandamutualcorrespondence flourished.BynowCarolrealizedthatthebulkofwhat hadbeenwrittenoncavemineralsresidedinEurope,and that CaveMinerals hadbarelyscratchedthesurfaceofthis knowledgebase. 1981 CarolHillmetPaoloFortiforthefirsttimeatthe8 th InternationalCongressofSpeleologyinBowlingGreen, Kentuckyinthesummerof1981.SincetheNSShad expressedaninterestinpublishinganothereditionof Cave Minerals ,CarolaskedPaolotobeco-authorofthisnew edition,nowtobeentitled CaveMineralsoftheWorld Paolowasveryhappyandexcitedtobeaco-author,but didnotyetrealizethetremendousamountofworkthat thiscommitmentwouldentail.Theambitiousintentof CarolandPaolowasfor CaveMineralsoftheWorld to includealloftheworkdoneincavemineralogyaroundthe worlduptothattime,includingallofthepaperswrittenon speleothemsintheveryearlyyearsofspeleology(Fig.2). Thus,theyinvitedcavehistorianTrevorShawofGreat BritaintowriteaHistoricalIntroductiontothebook. 1982–1985 In1982thecollaborationofCarolandPaoloonthe firsteditionof CaveMineralsoftheWorld (CMW1)began, butwiththeAtlanticOceanseparatingthemandwithno internetavailableatthattime.Fortwoyearstheauthors laboredonthemanuscript,withPaoloFortidoingthe lion’sshareofthenewworkbecauseoftheenormous amountofEuropeanliteratureonthesubjectinavariety oflanguages.Paolo’swifeGiovannacomplainedthatshe wasnotabletoseemuchofhimduringthistimebecausehe wasalwaysreadingandtranslatingcavemineralogyrelatedarticles.In1984,whentheCMW1manuscript wasalmostfinished,theNSSdecidedtoprintthebookin ItalybecauseitwasenvisionedthatmostoftheEuropean saleswouldoccurduringtheforthcomingInternational CongressinBarcelona,Spain.SoCMW1wascontracted toanItalianprintinghouseforaprescribedamountof Italianlira,whichatthattimewasveryweakwithrespect totheU.S.dollar.Inthesummerof1985,Paoloflewto Albuquerqueinordertopreparethefinalmanuscriptand choosephotoswithCarol,andafterfivefulldaysof immersion(withonlyonehourofwalkinginthegarden duringthosefivedays),CMW1wasreadytogotothe printers.Asa‘‘gift’’toPaolo,CarolandherhusbandAlan tookPaoloonawhirlwindtripthroughCarlsbadCavern. 1986 Thefirsteditionof CaveMineralsoftheWorld (CMW1)waspublishedjustintimeforthe9 th InternationalCongressofSpeleologyinBarcelona,Spain,butnot withoutproblems(HillandForti,1986).Itturnedoutthat between1984and1986theexchangerateofdollarstolira hadloweredmorethan30%,andasaconsequencethis causedamajordisagreementinpricingbetweentheNSS C AROL A.H ILLAND P AOLO F ORTI JournalofCaveandKarstStudies, April2007 N 37

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Figure1.Coverof CaveMinerals ,publishedin1976bytheNSS.ThisphotobyPeteLindlseyof‘‘TheButterfl y’’inthe CavernsofSonorawastheonlycolorphotointhebook. C AVEMINERALOGYANDTHE NSS: PAST,PRESENT,FUTURE 38 N JournalofCaveandKarstStudies, April2007

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andtheItalianprintinghouse.Thisdifficultsituationled averyfrustratedgo-betweenwithPaoloFortionthe EuropeanendofthingstowritetoCarolHillinJulyof 1986:‘‘IamaUniversityProfessor,notaclerkofthe NSS.’’However,CMW1didmakeittoBarcelonaontime andsoldwellattheCongress.Theprimeobjectivesofthis firstCMW1editionwereto:(1)setaclassification standardforthefieldofcavemineralogy,and(2)cover cavemineralsandspeleothemsworldwide.Thefirst edition,CMW1,containedover3,000referencesandwas 238pageslong.Ithadafront(Fig.3)andbackcolored coverandaninsertsectionof33colorplates.However,this endeavorsoexhaustedCarolandPaolothatneitherof themplannedtowriteanotheredition. 1994 In1994PaoloForti,whowasbynowrestedfrom writingCMW1,becameconvincedthatthereneededtobe yetanothereditionof CaveMineralsoftheWorld that would:(1)bringCMW1up-to-datesince1986,(2)provide anewformat(reorganization)ofthebook,whichwouldbe moreprofessionalandeasiertouse,and(3)includethe finestandmostcompletesetofphotographsofcave minerals/speleothemseverassembled.SoPaolo,duringthe Workshop,BreakthroughsinKarstGeomicrobiologyand RedoxGeochemistry,heldinColoradoSprings,Colorado inFebruaryof1994,convincedareluctantCarolthat anothereditionwasneeded. Thejobofdoing CaveMineralsoftheWorld ,second edition(CMW2)turnedouttobemucheasierthanCMW1 duetothefactthattheinternetande-mailnowallowedus toworktogetherinrealtime.Becauseofthetimeshift betweenItalyandNewMexico,Paolo’supdatescould reachCarolbyearlyafternoon,whileCarol’smaterial couldthenreachPaolobyearlythenextmorning,histime. Thisadvancementincomputerexchangeofinformation alsoallowedCaroltomorequicklyeditPaolo’s‘‘Fortian’’ writing(ahybridofEnglish-Italian)intostandardEnglish. Thistimearoundthemostdifficulttaskwastoobtainfull informationoncavemineralresearchinEasternEuropean Figure2.Acumulativegraphshowingthenumberofidentifiedcavemineral sandprintedpapersoncavemineralogyfrom 1800tothepresent.Notehowthisexplosionofknowledgehasincreasedalm ostexponentiallywithtime.FromHilland Forti(1997). C AROL A.H ILLAND P AOLO F ORTI JournalofCaveandKarstStudies, April2007 N 39

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Figure3.Frontcoverof CaveMineralsoftheWorld ,firstedition,publishedbytheNSSin1986.ThisfirsteditionofCMW1 hadcolorfrontandbackcoversandaninsetseriesof33colorplates. C AVEMINERALOGYANDTHE NSS: PAST,PRESENT,FUTURE 40 N JournalofCaveandKarstStudies, April2007

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countries,whichhadbeenunder-representedinCMW1 becauseoftheadversepoliticalconditionsthereintheearly 1980s.Overatwo-yeartimeperiod,Paolowasobligedto flytoRussia(threetimes),Bulgaria(twotimes),Romania, Slovenia,andtheCzechRepublicbesidestravelingto Spain,France,Switzerland,andAustria.Duringthesetrips over10,000slideswereselectedandover200hoursof discussionwerespentbyPaolowithlocalcaversand scientists.Truly,thisbookhadnowbecome CaveMinerals oftheWorld Inthesummerof1996,anotherrushtripwasmadeby PaolototheHillhouseinAlbuquerque(onthisvisit,the timewassoshortthatnotevenawalkinthegardenwas permitted)inordertoselectallofthephotographsfor CMW2andtofinalizethemanuscript.FromAlbuquerque, PaoloandCaroldrovebycartotheNSSConventionin Salida,Colorado,whereallofthematerialforCMW2was giventoDavidMcClurg,chairoftheSpecialPublications Committee.ThistimeCMW2wouldbeprintedinthe UnitedStatesunderDavidÂ’sdirectscrutiny. 1997 Thesecondeditionof CaveMineralsoftheWorld (CMW2)arrivedatthe199711 th InternationalCongressof SpeleologyinLaChauxdeFonds,Switzerlandontime, duemainlytotheHerculeaneffortofDavidMcClurg.At theSwissCongressCMW2wontheUISawardforBest CaveBookforthepreviousfouryears(sincethe HungarianCongress).Thesecondeditionof CaveMinerals oftheWorld is463pageslongandhas28co-authorsofthe SpecialTopicandTopTenCavessections,overandabove thecontributionsofauthorsHillandFortiandagain-coauthorTrevorShaw(Fig.4).CMW2waspublishedbythe NSSin full color,includingthebackandfrontcovers (Fig.5)and333colorphotosandfigures.Italsoincludes morethan5,000references,whichessentiallydidinboth CarolandPaolo.Theauthorsnowconsidertheirwork tofinallybe complete andanticipatewritingnofurther editions.And,asapositiveassuranceofthat,after publicationofCMW2,CarolHillmailedallofher Cave MineralsoftheWorld materialtoPaoloFortiathis InstituteofSpeleologyinBologna,whereitnowresidesfor alltoaccess. P RESENT InthedecadesinceCMW2waspublishedbytheNSS, thebookhashadagreatimpactamongcaversand scientists,astestifiedbythefactthatitisthespeleological bookwhichhasobtainedthehighestnumberofcitationsin bothspeleologicalandnon-speleologicalpapers.The namesandrelatedpropertiesofthemainspeleothemtypes andsubtypeshavebeendefinitivelystandardized.The bookhasalsobeenimportantinincreasingthenumberof scientistsinvolvedincavemineralresearchalloverthe world,whereasbeforethistimesuchresearchwaslimited toadozenorsopersonsworkinginrelativelyfew countries.AsaconsequenceoftheNSSpublishingthis seriesofthreebooks,newminerogeneticprocessesarenow understoodandnewmineralsforsciencehavebeen described.Andhappily,thefearoftheNSSintheearly 1970s,thatthebookwouldpromotevandalism,hasnot beenrealized.Rather,thepublicationofthe CaveMineral bookserieshashelpedtoeducatethepublicastothe importanceofconservingcavemineralsandspeleothems. Finally,thebookhasbeenessentialinmakingallpeople awareofthebeautyandfragilityofthecaveenvironment anditsneedforprotection. F UTURE TheauthorsrecognizethatCMW2isnotthefinal wordincavemineralogy,butthatthissciencewill evolveandbecarriedonbyanewgenerationof speleologists.Asawayofpromotingthatfuture,the authorswillattempttoidentifythreeareasoffuture researchthattheyfeelarepromisingforadvancingthefield ofcavemineralogy. P ALEOE NVIRONMENTS /P ALEOCLIMATOLOGY Oneofthemostimportantfutureareasofresearchin cavemineralogyisthestudyofpaleoclimateandpaleoenvironmentasitrelatestothecurrentconcernoverglobal warming.Anexcellentoverviewpaperconcerningthe datingofcalcitespeleothemsanditsapplicationtopaleoenvironmentsisbyDerekFord(1997),whohasbeenone ofthepioneersandleadersinthisfieldforthelastthree decades.However,whileuptothepresentcalciteand aragonitespeleothemshavebeenusedalmostexclusively forsuchanalyses,inthelastfewyearsothercaveminerals havebeguntobeusedtodeterminepaleo-environments, mineralssuchaselementalsulfurasanindicatorofhigh hydrogensulfideconcentration,oropalsubstitutingfor calciteasanindicatorofrainfallincreaseovertime.An explosionofinterestisexpectedtowardthehundredsof differentcavemineralswhosedepositionincavesis controlledbyboundaryconditions,whichinturnare relatedtotheenvironmentorpaleo-environment. Theapplicationofspeleothemstopaleoclimatestudies notonlyinvolvesdating.Italsoinvolvesdeterminingstable isotope,trace-element,color-banding,andluminescent analysesandprofilesofthesespeleothems(White,2007). Especiallyimportanttotheproblemofglobalwarmingare paleoclimatestudiesdoneonHolocene-agespeleothems, suchaswasdonebyPolyaketal.(2001),whodepicted changesinclimateoverthelast3,200yearsfromstudying mitespreservedinstalagmitesfromHiddenCave,New Mexico.Thepresenceofthesemites,encasedintravertine thatwasdatedbytheuranium-seriesmethod,impliesthat awetterandcoolerclimateexisted3,200yearsagothanis presenttodayintheGuadalupeMountains. C AROL A.H ILLAND P AOLO F ORTI JournalofCaveandKarstStudies, April2007 N 41

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M ICROBIOLOGY Anotherfieldwhereitisanticipatedthatresearchwill developsubstantiallyistheinter-relationshipbetween microbiologyandcavemineralogy.Microorganisms (mainlybacteria)areresponsibleformany,ifnotmost, ofthelowenthalpyprocessesleadingtothedepositionof caveminerals(Forti,2002;Contos,2001).Suchstudies, mostofwhichareonlyafewdecadesorlessold,alsohave economicimportancebecausetheyreflectthesame mechanismsthatcausethemobilizationand/orre-depositionoforebodiesinchemoautotrophicenvironments (Onacetal.,2001).Biominerals,suchasformincaves,may alsohaveapplicationtoindustryandmedicine. Oneofthemostimportantareasoffutureresearchwith respecttomicrobiology-cavemineralogyisthatofproving biogenicity,thatis,catchingmicrobesintheactofforming minerals.Thisprovestobeaverydifficulttask,asthe productsofmicrobialprecipitationoftenmimicthose formedduringinorganicprocesses(Bartonetal.,2001; Jones,2001).Andjustbecausefossilizedmicrobesexistin speleothemsdoesnotnecessarilymeanthattheyplayed activerolesintheprecipitationofthatspeleothem.Even whendealingwithlivingmicrobes,provingbiogenicityis difficultbecausebiogenicmineralproductioncannotbe verifiedwithculturingtechniquesalone.Asdiscussedby Northup(2006),aprocesscalledmolecularphylogenymust beusedwherebyextractingandanalyzingDNAprovides agenetictreethatcanhelpidentifytherolethatmicroorganismsplayinthecreationofmineraldeposits.These resultscanthenguidemicrobialculturingeffortstomore closelystudytheactualmineralproductionbymicroorganisms.Suchstudiesareontheforefrontofknowledgein understandingthedualorganic-inorganicreactionsinvolvingtheprecipitationofcavemineralsandspeleothems. M INERALS O NTOGENY CaveMineralsoftheWorld ,likeDanaÂ’sclassic Manual ofMineralogy ,ismainlya descriptive work,onethat Figure4.PaoloFortiandCarolHillautographingcopiesoftheirupdateds econdeditionof CaveMineralsoftheWorld whichmadeitsdebutattheInternationalCongressofSpeleologyinLaChau xdeFonds,Switzerland,inthesummerof1997. Manyofthe28co-authorsofCMW2wereattheCongressandformedalonglineo fbookautographersalongsideofCarol andPaolo. C AVEMINERALOGYANDTHE NSS: PAST,PRESENT,FUTURE 42 N JournalofCaveandKarstStudies, April2007

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Figure5.Frontcoverof CaveMineralsoftheWorld ,secondedition,publishedbytheNSSin1997.Thissecondeditionwasin fullcolor,containing333colorphotographsandfiguresaswellascolorf rontandbackcovers. C AROL A.H ILLAND P AOLO F ORTI JournalofCaveandKarstStudies, April2007 N 43

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describeswhataspeleothemorcaveminerallookslike. Oneofthemostimportantfuturesofcavemineralogylies inthesubjectofmineralsontogeny,whichstudiesthe growthofspeleothemsandcavemineralsfroma genetic perspectiveratherthanfromadescriptiveperspective. Ontogenyofcavemineralsasascientificstudyhasbeen developedinRussia,butispoorlyunderstoodintheWest. Asafirststepinbringingthissubjecttothegeneral attentionofspeleologistsandcavers,CharlesSelfand CarolHillpublishedanintroductiontomineralsontogeny intheAugust,2003issueoftheNSS’s JournalofCavesand KarstStudies (SelfandHill,2003).Thispaperintroduced thebasicprinciplesofmineralsontogenyandexplained ahierarchyschemewherebymineralbodiescanbestudied ascrystal individuals aggregates ofindividuals,associationsofaggregates(termed koras bytheRussians),andas sequencesofkoras( ensembles ).However,ontogenyisnot simplyanewclassificationsystemforminerals.Itis amethodbywhichpastcrystallizationenvironmentscan bedecipheredfromthemineralbodiesthemselves.(For example,needlesinfrostwork-typespeleothemsnever toucheachotherbecauseofthetypeofselection encounteredwithinacapillaryfilmenvironment.)The structureandtextureofmineralbodiescanbedirectly relatedtoenvironmentalfactors,andspeleothemsincaves provetobeidealsubjectsforthistypeofstudy. InSeptember,2005,attheAthens-Kalamos,Greece, InternationalCongressofSpeleology,theUISCommission onCaveMineralogyformedasub-committeecomposedof CharlesSelf(chair)ofGreatBritain,BogdanOnacof Romania,KyungSikWooofKorea,andWilliamWhite andCarolHilloftheUnitedStates,tofurtherinvestigate andpromotethesubjectofmineralsontogeny.Asofthis writing,WillWhiteiscomposingapaperforpublication entitled:‘‘Speleothemmicrostructure/speleothemontogeny: AcomparisonofcrystalgrowthconceptsbetweenWestern andRussianconceptualframeworksandbetweenmineralogy,ceramics,metallurgy,andsemiconductortechnology.’’ Perhapstheseendeavorsinmineralsontogenywillturninto thesubjectofanothercavemineralogy-relatedbookthatthe NSSwillpublishsometimeinthefuture. C ONCLUSION TheNationalSpeleologicalSocietyistobecommended onits65yearsofprotectingthecaveenvironment,and specificallythespeleothemsandcavemineralswithinthat environment.TheauthorsespeciallythanktheNSSfor disseminatingthewonderfulandbeautifulworldofcave mineralstocaversandthepublicalikethroughtheirbooks CaveMinerals and CaveMineralsoftheWorld A CKNOWLEDGMENTS TheauthorsthankWillWhiteforhiscontributionsto thepasthistoryandpaleo-environmentsections,and PennyBostonandDianaNorthupfortheircontribution tothemicrobiologysection.Theauthorswouldalsoliketo thankthesephotographersforthecoverphotographs:Pete Lindsley(Fig.1),PhilippeCrochet(Figure3),Dave Bunnell(Figure4),andPatrickCabrol(Figure5). R EFERENCES Barton,H.A.,Spear,J.R.,andPace,N.R.,2001,Microbiallifeinthe underworld:Biogenicityinsecondarymineralformations:GeomicrobiologyJournal,v.18,p.359–368. Contos,A.,2001,Biomineralizationincaves[Ph.D.dissertation]:Sydn ey, UniversityofSydney,221p. Crisman,R.,1956,Acavewithalonghiddensecret:National SpeleologicalSocietyNews,v.14,no.4,p.38–40. Curl,R.L.,1962,Thearagonite-calciteproblem:NationalSpeleologica l SocietyBulletin,v.24,pt.2,p.57–73. Curl,R.L.,1971,Minimumdiameterofstalactitesandstalagmites[abs.] : NationalSpeleologicalSocietyBulletin,v.33,no.4,p.147. Davies,W.E.,andMoore,G.W.,1957,Endelliteandhydromagnesite fromCarlsbadCaverns:NationalSpeleologicalSocietyBulletin, v.19,p.24–27. Ford,D.C.,1997,Datingandpaleo-environmentalstudiesofspeleothems in Hill,C.A.,andForti,P.,eds.,CaveMineralsoftheWorld: Huntsville,Ala.,NationalSpeleologicalSociety,p.271–284. Forti,P.,2002,Biogenicspeleothems:anoverview:InternationalJourn al ofSpeleology,v.30,no.1–4,p.39–56. Forti,P.,andHill,C.A.,2004,Speleothems:Evaporite, in Gunn,J.,ed., EncyclopediaofCavesandKarstScience:London,FitzroyDearborn, p.692–695. Foster,W.J.,1949,Mineralogicaldatainspeleologicalwork:National SpeleologicalSocietyBulletin,no.11,p.51–54. Foster,W.J.,1951,Committeeonformationsandmineralogy:NSSNews, v.9,no.1,p.3. Good,J.M.,1957,NoncarbonatedepositsofCarlsbadCaverns:Bulletin oftheNationalSpeleologicalSociety,v.19,p.11–23. Henderson,E.P.,1949,SomeunusualformationsinSkylineCaverns, Virginia:BulletinoftheNationalSpeleologicalSociety,v.11, p.31–34. Hill,C.A.,1976,CaveMinerals:Huntsville,Ala.,NationalSpeleologic al Society,137p. Hill,C.A.,andForti,P.,1986,CaveMineralsoftheWorld,firstedition: Huntsville,Ala.,NationalSpeleologicalSociety,238p. Hill,C.A.,andForti,P.,1997,CaveMineralsoftheWorld,second edition:Huntsville,Ala.,NationalSpeleologicalSociety,463p. Hill,C.A.,andForti,P.,2004a,Mineralsincaves, in Gunn,J.,ed., EncyclopediaofCavesandKarstScience:London,FitzroyDearborn, p.511–514. Hill,C.A.,andForti,P.,2004b,Speleothems:Carbonate, in Gunn,J.,ed., EncyclopediaofCavesandKarstScience:London,FitzroyDearborn, p.690–692. Holden,R.J.,1940,Notesoncertaincavedeposits:Bulletinofthe NationalSpeleologicalSociety,no.1,p.18–20. Holden,R.J.,1944a,Lessonsinfluorescenceandcaveclimate:Bulletino f theNationalSpeleologicalSociety,no.6,p.50–51. Holden,R.J.,1944b,Reportofthecommitteeonmineralogyand formations:BulletinoftheNationalSpeleologicalSociety,no.6,p.53. Jones,B.,2001,Microbialactivityincaves—ageologicalperspective: GeomicrobiologyJournal,v.18,p.345–358. Moore,G.W.,1952,Speleothem—anewcaveterm:NSSNews,v.10, no.6,p.2. Moore,G.W.,1954,Theoriginofhelictites:NationalSpeleological SocietyOccasionalPapers,no.1,16p. Moore,G.W.,1961,Dolomitespeleothems:NSSNews,v.19,p.82. Moore,G.W.,1962,Thegrowthofstalactites:BulletinoftheNational SpeleologicalSociety,v.24,pt.2,p.95–106. Northup,D.E.,2006,Partneringwithbiologists:betteranswersthrough collaboration, in Land,L.,Lueth,V.W.,Raatz,W.,Boston,P.,and Love,D.L.,eds.,CavesandKarstofsoutheasternNewMexico: NewMexicoGeologicalSociety,57 th AnnualFieldConference, p.41–42. C AVEMINERALOGYANDTHE NSS: PAST,PRESENT,FUTURE 44 N JournalofCaveandKarstStudies, April2007

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Onac,B.P.,Veni,G.,andWhite,W.B.,2001,Depositionalenvironment formetatyuyamuniteandrelatedmineralsfromCavernsofSonora: EuropeanJournalofMineralogy,v.24,no.1,p.135–143. Polyak,V.J.,Cokendolpher,J.C.,Norton,R.A.,andAsmerom,Y.,2001, WetterandcoolerlateHoloceneclimateinthesouthwesternUnited Statesfrommitespreservedinstalagmites:Geology,v.29,no.7, p.643–646. Self,C.A.,andHill,C.A.,2003,Howspeleothemsgrow:Anintroduction totheontogenyofcaveminerals:JournalofCaveandKarstStudies, v.65,no.2,p.130–151. Thayer,C.W.,1967,Mudstalagmitesandtheconulite:National SpeleologicalSocietyBulletin,v.29,no.3,p.91–95. Warwick,G.T.,1950,Calcitebubbles–anewcaveformation?:National SpeleologicalSocietyBulletin,no.12,p.38–42. White,W.B.,1961,Cavemineralstudies,1955–1960:NSSNews,v.19, no.8,p.94. White,W.B.,1962,Introductiontothesymposiumoncavemineralogy: NationalSpeleologicalSocietyBulletin,v.24,pt.2,p.55–56. White,W.B.,2007,Cavesedimentsandpaleoclimate:JournalofCaveand KarstStudies,thisissue. C AROL A.H ILLAND P AOLO F ORTI JournalofCaveandKarstStudies, April2007 N 45



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CAVEGEOLOGYANDSPELEOGENESISOVERTHEPAST 65YEARS:ROLEOFTHENATIONALSPELEOLOGICAL SOCIETYINADVANCINGTHESCIENCE A RTHUR N.P ALMER DepartmentofEarthSciences,StateUniversityofNewYork,Oneonta,NY13 820-4015,palmeran@oneonta.edu Abstract: TheNationalSpeleologicalSocietywasfoundedin1941,neartheendof aremarkableperiodinthehistoryofspeleogenesis.Manywell-knowngeol ogistshad publishedonthetopicduringthepreviousdecade.Forvariousreasonsthe NSSdidnot benefitfromthiswaveofinterest,anditsmemberswerefacedwithreconst ructingthe subjectfromafreshbeginning.Thetopicwasdevelopedmainlybyindividu alswho startedascaveexplorersandextendedthatinterestintoscience.Someof theadvances overthepast65yearsincludenewfieldandlaboratorytechniques,models ofcaveorigin, introductionofsulfuricacidspeleogenesis,coastalcavestudies,reco gnitionofmicrobial mediationofcaveprocesses,geochronologyandpaleoclimatology,digit almodeling,and growingattentiontowardlavacaves. I NTRODUCTION Sinceitsfoundingin1941,theNationalSpeleological Society(NSS)hasgrownfromasmallregionalgroupinto oneoftheworld’slargestandmostinfluentialorganizationsincavescience.Overthepast65yearsithashelpedto fostersomeofthemostnotableadvancesincavegeology andspeleogenesis.Thispaperconcernsthehistoryofthis fieldandtherolethattheNSShasplayedinits development.Thereisnoneedforarigoroushistorical recordoradetaileddescriptionofideas,astheseare providedinrecentbookseditedbyKlimchouketal.(2000), Gunn(2004),andCulverandWhite(2005).Instead,the aimistolookbehindthescenesattheinteractionamong cavegeologistsandhowtheirideasdeveloped. Insummarizingtheadvancesinkarstgeologyforthe 25 th anniversaryoftheNSS,Davies(1966)notedthatearly progressinthatfieldhadtakenplaceinspurts,with interveningperiodsofrelativeinactivity.Hepredicted aburstofquantitativeadvancesinspeleologyintheyears tocome,andthevalidityofhispredictionisillustrated here. B EGINNINGS TheNSSwasconceived,asDickenswouldhavesaid,in boththebestoftimesandtheworstoftimes.Duringthe priordecadetherehadbeenafloweringofinterestincave origin,andmanyoftheclassicAmericanpapersonthe subjectwereproducedatthattime.Theauthorsinclude someofhistory’sbest-knowngeologists.WilliamMorris Davis,whowrotea154-pagepaperoncaveorigin(Davis, 1930),isprobablythemostinfluentialgeomorphologist whoeverlived.JHarlenBretz(noperiodaftertheJ)was oneofAmerica’sboldestandclear-sightedgeologists.Most ofhisworkoncavesfollowedthebirthoftheNSS(e.g., Bretz,1942),buthehadmadehisreputationlongbefore. ClydeMalott,whowasamongIndiana’sforemost stratigraphersandgeomorphologists,devotedmuchof hisattentionforseveraldecadestocavesandkarst(e.g., Malott,1937).AllynSwinnertonwasawell-knownprofessorofgeologyatStanford,Harvard,andAntioch College(Swinnerton,1932). Therewasconsiderabledisparityofopinionamong theseearlyauthors.DavisandBretzchampioneddeepphreaticcaveorigin.Swinnertonfavoredcaveoriginator justbelowthewatertable.Malottdescribedcavesinterms ofinvasionbysurfacestreams.Thisbriefoutlinedoesno justicetoanyoftheauthorsandomitsmanyothers,butit isenoughtosetthestage.FordetailsseeWatsonand White(1985)andLowe(2000). ThefoundingoftheNSSneartheendofthisperiod placeditinapositiontoridethewaveofenthusiasmfor speleogenesis,butforseveralreasonstheorganization gainedlittlebenefitfromit.First,noneofthecontributors totheclassicpaperswereinvolvedinfoundingtheSociety. Thefoundersweremainlycaveexplorers,andalthough theyregardedscienceasimportant,theyhadfewcredentialsinthefield. Asecondproblemwasthattheideasdevelopedduring thisclassicperiodofspeleogenesiscontradictedone another.Theywerepublishedbeforecavemapswere widelyavailable,andinterpretationslackedthebenefitof diversefieldexperience.Withnoconsensus,itseemedthat littlesolidgroundhadbeengained. ContinentalEuropeans,withtheirlongtraditionincave science,wereastonishedbythemanycontradictory Americanmodelsforcaveorigin.Thewell-knownFrench speleologistBernardGe `zeoncesaid(translatedloosely fromTrombe,1952),‘‘ItseemsthattheAmericansare tryingtoreinventspeleologyrightfromsquareone.’’Butat thesametime,westernEuropeansmadealmostno ArthurN.Palmer–Cavegeologyandspeleogenesisoverthepast65years:ro leoftheNationalSpeleologicalSocietyinadvancingthe science. JournalofCaveandKarstStudies, v.69,no.1,p.3–12. JournalofCaveandKarstStudies, April2007 N 3

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referencetothevastamountofcontemporarywork accomplishedineasternEurope.Thisinsularattitude canbeclearlytracedtothebarriersoflanguage, geography,andpolitics.Thefieldismuchmorecosmopolitantoday. ThegrowthofsciencewithintheNSSisclearfromthe first10–20yearsofthe BulletinoftheNationalSpeleologicalSociety (nowthe JournalofCaveandKarstStudies ). NSSBulletin No.1waspublishedbytheshort-lived precursoroftheNSS,theSpeleologicalSocietyofthe DistrictofColumbia.Itscoverincludesacartoonof agroupofcaversscramblingoverstalagmites,withone teammemberburningtheseatofthepersonaheadwithhis carbidelamp.Theissuecontainsmainlytripreports,and althougheachshowsawell-definedpurpose,thereisno coordinatedscientificfocus.Interestinsciencegrew, however,andwithinafewyearsscientificarticles dominatedthe Bulletin .Severaloftheearlychampionsof cavegeology,includingMalott,Swinnerton,andBretz, weremadehonoraryNSSmembers,andtheyresponded favorablybycontributingarticles.Americanstudiesof speleogenesisbegangraduallytorebuild.In1949the Bulletin includedpapersonthesubjectbyRalphStoneand ClydeMalott.In1950,AllynSwinnertoncontributed apaperoncavemapping,buthedidnotpursuehisideas oncaveorigin. AF ORKINTHE R OAD TheremaybeareasonforSwinnerton’sdiminished interestinspeleogenesis.In1940,oneofthegreatestfigures inpetroleumgeologyandhydrology,M.KingHubbert, publishedaseminalpaper, Thetheoryofgroundwater motion ,inthe JournalofGeology ,inwhichhedeveloped theprinciplesofhydraulicpotentialandtheinfluenceof potentialfieldsonground-watermotion.Init,heexplicitly criticizedSwinnerton’sdiagramsofcaveoriginforbeing incompatiblewithpotentialtheoryandviolatingthelawof conservationofmass.AlthoughHubbertwasnotentirely wrong,hefailedtotakeintoaccountthedistortionof laminarground-waterpatternsbyconduitgrowth(Hubbert,1940). Hubbert’spaperwashardlynoticedbyspeleologistsat thattime,butitwasaturningpointforground-water hydrologists.Formany,groundwaterbecameatechnical fieldthatreliedasmuchonmathematicsandphysicsas ongeology.TodayHubbertisbestrememberedforhis conceptofpeakoil,buthislegacyinhydrologyalsolives on. Althoughnoonerealizeditatthetime,thiswas thethirdandgreatestobstaclefacedbycavegeologists duringtheearlyyearsoftheNSS.Sincetheturningof hydrologyinmathematicaldirections,speleologyhasbeen dismissedashardlyascienceatallbymosthydrologists, theverypeoplewhocouldbenefitthemostfromcave geology. AF RESH S TART Bythe1950s,severalNSSmembersemergedasleadersin cavegeology.RalphStone(formerStateGeologistof Pennsylvania)contributedanentire NSSBulletin onCaves ofPennsylvania(Stone,1953)anupdateofworkthathehad preparedearlierfortheStateGeologicalSurvey,andwhich includesconsiderablegeologicdetail.WilliamDavies,of theU.S.GeologicalSurvey,wrotebooksonthecavesof Maryland(Davies,1950)andofWestVirginia(Davies, 1959).Healsoadvancedthestudyofspeleogenesiswith observationsofcavelevelsandtheircorrelationwithriver terraces(e.g.,Davies,1957).BothheandStoneservedas NSSpresident.BretzwroteabookoncavesofMissouri (Bretz,1956)andco-authoredanotheronthecavesof Illinois(BretzandHarris,1961).E.R.Pohl,long-time KentuckygeologistandoneofthefoundersoftheCave ResearchFoundation,contributedimportantworkonthe originofverticalshaftsinlimestonecaves(e.g.,Pohl,1955). GeorgeMoore,oftheU.S.GeologicalSurvey,recognizedthatitwastimeforAmericanspeleologiststoreview thestatusofspeleogenesis.In1959,heconvenedasymposiumoncaveorigin,sponsoredjointlybytheNSSand theGeologicalSocietyofAmerica.Theproceedingswere publishedas NSSBulletin 22,No.1(Moore,1960).This wasprobablythemostimportantpointinNSShistoryin termsofadvancingthefieldofspeleogenesis.Besides Moore,participantsincludedBretz,Davies,RaneCurl, GeorgeDeike,WilliamHalliday,ArthurLange,John Thrailkill,andWilliamWhite.BretzandDavieswere alreadywellknowninthefield,andeachoftheothersalso wentontomakesubstantialcontributionstospeleogenesis. Somearestillactiveincavegeologytoday. White(1959)hadalreadypublishedadiscussionof speleogenesisinhislocalgrottonewsletter.Hereviewedthe classicpapersofthe1930sandearly1940sandcametothe conclusionthatnooneagreedonanything.Butitwas madeclearduringthe1959symposiumthatmuchofthe confusionwasonlyamatterofconflictingterminology.In thewordsofHalliday(1960), Thereseemstobelessandlessdivergenceofbasicconcepts,and moreandmoreargumentoverclassificationandterminology, whichcanbecarriedtothepointthattwoauthoritiesholding similarviewsareunabletorecognizetheiragreement. Thiswarningappliesaswelltodayasitdidin1959.Butat thattime,fieldexperienceandcavedataweregrowing rapidly,andtheanswerstomanyfundamentalquestionsin speleogenesisseemedwithinreach.Littledidthesymposiumparticipantsrealizehowfartheyhadtogo. P HYSICSAND C HEMISTRY E NTERTHE P ICTURE Anunderstandingofspeleogenesisrequiresasmuch knowledgeofhydraulicsandchemicalkineticsasitdoesof C AVEGEOLOGYANDSPELEOGENESISOVERTHEPAST 65 YEARS:ROLEOFTHE N ATIONAL S PELEOLOGICAL S OCIETYINADVANCINGTHESCIENCE 4 N JournalofCaveandKarstStudies, April2007

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geology.Laboratoryexperimentsbynon-speleologists Kaye(1957)andWeyl(1958)showedthattherateof limestonedissolutiondependsonthevelocityofacidic water.Thisapproachpromisedtosolvesomeofthebasic questionsaboutcaveorigin,buttheyusedhydrochloric acid,whichbehavesdifferentlyfromcarbonicacid,which isinvolvedinmostcavedevelopment,andsotheresults werenotashelpfulastheyonceseemed.Theydid, however,pointtheway.Fromhisexperiments,Weyl estimatedthatacidicwatercouldnotpenetrateveryfar alongatypicalfractureinlimestonebeforelosingmostof itssolutionalcapacity. Onthebasisofthisresearch,WilliamWhiteandJudith Longyearconcludedthatnoneofthepreviousconceptual modelsofcaveoriginwereincorrect,butthattheywereall irrelevant.Ineachmodel,cavesweretiedtotheirposition relativetothewatertable,whereas,infact,theyform wherevertheground-waterflowisgreatest(Whiteand Longyear,1962).WhiteandLongyearalsopredicted asubstantialjumpindissolutionratewhentheflow changesfromlaminartoturbulentastheconduitgrows. AlanHowardappliedchemistryandhydraulicstocave originandestimatedthatthelaminar-turbulenttransition wouldincreasethesolutionratebyafewtimes(Howard, 1964a).ThisestimatewasmuchsmallerthanWhiteandLongyearÂ’s,butmoreaccurate.Severalotherprojectsandacademic dissertationsbyNSSmembersweredevotedtopursuingthe kineticsofcarbonatedissolution,withthespecificgoalof clarifyingratesofcaveorigin(e.g.,HowardandHoward,1967; RauchandWhite,1970;HermanandWhite,1985). Theideaofathresholdincavedevelopmentwas expandedfurtherbyWhite(1977).Henotedthatasacave growsanditsflowbecomesturbulent,thewateralso acquirestheabilitytotransportsedimentatnearlythe sametime.Fromthenon,sinkholesopenmorerapidly, andabrasioncanaugmentthedissolutionrateincaves. WhitealsoappliedexperimentaldatafromPlummerand Wigley(1976)toshowthat,inatypicalcave,the dissolutionrateofcalciteincreasesabruptlyataboutthe sametimeastheonsetofturbulenceandsediment transport.Allthreeprocessesenhancethegrowthrateof cavesatmoreorlessthesamepointinacaveÂ’sevolution. RaneCurl,sincethelate1950s,hadbeenconcerned withtheoriginofsolutionalscallopsinthebedrock surfacesofcaves.Byapplyinghydraulicsanddimensional analysis,heshowedhowitispossibletodeterminepast flowvelocitiesfromscalloplengths.Thisgaveagreatboost totheinterpretationofcavepaleohydraulics.Hislatest paperonthetopic(Curl,1974)isthemostaccessible. Curlalsoinvestigatedthestatisticalaspectsofcave distributionandmorphology.Byquantifyingthesevariables,theprocessesthatformcavescanbediscriminated. Hecontinuedtopursuethesetopicsforseveraldecades (e.g.,Curl,1986).Thisapproachisusefultoscientists,such aspetroleumgeologists,whoneedtopredictthedistributionofporosity. Similaradvancesweretakingplacesimultaneouslyin Europe.Itisworthnotinghowburstsofactivityoftentake placealmostsimultaneouslyaroundtheworldunderthe directionofafewleadingresearchers,assuggestedby Davies(1966).Today,withrapidworldwidecommunication,thistendencyisevenmoreprevalent. A CADEMIC A LLIANCES WilliamWhitebecameaprofessoratPennsylvania StateUniversity,wherehenurturedalongstringof graduatestudentswithinterestsincavegeologyand hydrology,ashecontinuestodotodayinsemi-retirement. Speleogenesiswasgraduallybecominginseparablefrom karsthydrology.Onebyone,heandhisstudentstackled thefundamentalproblemsinthesefields. Intheearly1960s,DerekFordarrivedinNorth AmericafromBritainandsoonjoinedthefacultyat McMasterUniversity(Hamilton,Ontario).Hethrew himselfintoexploringandinterpretingthekarstofhis vastnewhomelandandalmostsinglehandedlyputCanada onthemapofimportantkarstregions.HejoinedtheNSS andbeganpublishinginthe Bulletin .Alargenumberof talentedgraduatestudentsobtainedtheirtrainingunderhis direction,andthelistcontinuestogrowtoday. Asteadystreamofkarstscientistsfromoverseasbegan topassthroughbothMcMasterUniversityandthe PennsylvaniaStateUniversitytoobservetheresearch programsattheseschoolsandoftentolingerasvisiting scholars.Inevitably,thetwogroupsbegantomeet periodicallytocombinesocializingandscience.Karst geologyandspeleogenesiswereamongthemaintopicsof discussion.Theseoccasionalmeetingsweresosuccessful thatotherkarstscientistsbegantotakepartfromallover thecontinent.Soonsomeofthemeetingswereheldat otherlocations.In1974,atameetingattheUniversityof WestVirginia,thestill-informalgroupacquiredthe nameFriendsofKarst.Therewerenorules,noofficial membership,officers,dues,ornewsletter.Sincethen,many FOKmeetingshavebeenheldthroughoutNorthAmerica, aswellasinPuertoRico,SanSalvador,andRomania. Meanwhile,severalPennStateandMcMasterstudents wentontoestablishtheirownacademicprogramsinkarst orrelatedfields,whilesimilarprogramsatotheruniversitiessproutedfromdifferentseeds.Aspiritofcamaraderie boundthemalltogether,asitstilldoestoday,partlyowing totheeclecticnatureofcavescience.Itisdifficulttoretain oneÂ’sprofessionaldignitywhilecrawlingthroughmud. Someoftheunityalsostemmedfromtheimpressionthat fewotherpeopleseemedtocareaboutcaves. D EVELOPMENTSIN C AVE G EOLOGY Earlystudiesofspeleogenesiswerehamperedbythe paucityoffielddataoncavegeology.Inthefirsthalfofthe 20 th centurytherewasalmostnoquantitativeinformation A RTHUR N.P ALMER JournalofCaveandKarstStudies, April2007 N 5

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ontherelationbetweencavesandtheirsurrounding geology,beyondvisualandnon-systematicobservations. Atthattime,thesituationwasmorefavorableinEurope, wherestandardsofcavemappingweremoreadvanced.By thelate1940s,Americangeologistsbegantorelatecave patternstodetailsinthesurroundinggeology.Suchstudies weremostnumerousintheAppalachians(E.L.Krinitzky, 1947;Davies,1959,1960;Deike,1960),andinMammoth Cave,Kentucky(Deike,1967).IntheBlackHillsofSouth Dakota,Deal(1962)andHoward(1964b)relatedJewel CaveandWindCavetotheircomplexgeologicand hydrologicsettings. Inthe1960s,RichardPowell,oftheIndianaGeological Survey,developedhand-levelingtechniquestomapthe subtlegeologicstructureofcavesinstratawithdipsso gentlethattheycannotbedistinguishedbyeye.Hiswork atWyandotteCave,Indiana,wasperhapsthefirstofits type(Powell,1968,1976).Hisassociates,Arthurand MargaretPalmer,extendedthetechniquetocaveselsewhereinthecountry(e.g.,Palmer,1972,1989).Recently, RoyJamesonhasusedthelevelingmethodtoobtaineven greaterdetailthroughananalysisoftheindividual segmentsineachcavepassage(Jameson,1985,2006). Thisworkshowedthateveninplacesofalmostnegligible dip,thetrendsofmanycavepassagesarecontrolledbylocal structuresthataretoosubtletoappearongeologicmaps basedonsurfaceexposures.Suchdetailsprovidethe necessarycriteriafordistinguishingwhethercavelevels (i.e.,stories,ortiers)arecontrolledbygeomorphicevents, bygeologicstructure,orbyfavorablestratigraphy.Earlier studies,suchasthoseofDavies(1957)showedageneral relationshipbetweencaveelevationsandriverterraces. Detailedgeologicmappingmakesitpossibletovalidatethe relationshipbetweencavelevelsandformerbaselevelsin somecaves(e.g.,Powell,1970)andtorejecttherelationship inothers(e.g.,PalmerandPalmer,1989).Asacomplication, stressreleasearoundentrenchedsurfacevalleyshelpsto localizecavedevelopment(SasowskyandWhite,1994).As thedatingofcavedepositsbecomesmoresophisticated, cavesthatareconvincinglyrelatedtobase-levelhistorycan beusedtointerpretthedrainagehistoryofentiredrainage basins(e.g.,Grangeretal.,2001;seedetailsbelow). Specializedtopicsincavegeologyhaveemerged.In cavemineralogy,forexample,Moore(1952)promotedthe word speleothem torefertosecondarymineraldepositsin caves.Theliteratureonthesubjectissovastthatreaders arereferredsimplytothemassivesummarybyHilland Forti(1997).Bycomparison,detritalcavesedimentshave receivedlittleattention,eventhoughtheyareintegral featuresofcavesandimportanttocavedevelopment. StudiesbyWilliamDaviesandE.C.T.ChaoatMammoth Caveshowedhowitwaspossibletointerpretsourceareas forcavesediments(DaviesandChao,1959).Elizabethand WilliamWhitedescribedthedynamicsofsedimenttransportthroughcavesandtherelationshipbetweensediments andcaveorigin(WhiteandWhite,1968).Current knowledgeoncavedeposits,bothmechanicalandchemical,issummarizedinabookeditedbySasowskyand Mylroie(2004). Acommontopicatmeetingsistheregionalapproachto karstandcavescience,inwhichallaspectsofthesubject arediscussedwithinagivengeomorphicprovince.An exampleistheAppalachianKarstSymposium,heldat RadfordUniversity,Virginia,withproceedingseditedby KastningandKastning(1991). Inrecentdecades,cavescientistshavebeguntoapply theirknowledgetootherfieldsnotgenerallyassociated withcaves.Examplesincludetherelationshipofcavesto petroleumgeologyandmining(Furman,1993;Hill,1995), dolomitization(Thrailkill,1971),theevolutionofporosity incarbonaterocks(Queen,1973,1994),andtheinterpretationoftectonichistoryfromthedistributionof caves(DuCheneandCunningham,2006).Otherexamples ofhowcavescanprovideinformationaboutthegeologic historyofthesurroundingregionaredescribedbelow. C ONCEPTUAL M ODELSOF C AVE O RIGIN Devisingconceptualmodelsofcaveorigincontinuesto beacommongoalofAmericanspeleologists.Thetangled webleftfromearlierdecadeshasfinallybeensortedout, sothatthedisparateinterpretationsfinallymadesense. Noneoftheearlyworkhasbeendiscarded.Insteadit isperiodicallyre-examinedinthelightofnewknowledge andincorporatedintonewmodelswhereappropriate.Over thepastfewdecades,severalconceptualmodelshavebeen proposedinanattempttoexplaintheoriginofallcaves withasinglemodel. R ELATIONTO A QUIFER T YPE WilliamWhitedescribedkarstaquifersaccordingto theirhydrogeologicsettingsandnotedthetypesofcaves thatweremosttypicalineach(White,1969andlater). Diffuse-flowaquiferscontainfewcaves,andtheytendtobe smallandirregular.Free-flowaquifersmayormaynotbe overlainbyaninsolublecap-rock.Sinkholesarethemain waterinputsintheexposedtype,andshortcaveswithhigh sedimentloadarecommon.Cappedaquifersarefedby verticalshaftsaroundtheerodedperimetersofthecap-rock, andlongintegratedcavesextendbeneaththecap-rock. Confinedaquifersinwhichimpermeablebedsforcewaterto flowbelowtheregionalbaseleveltendtocontaininclined three-dimensionalmazes,andthesandwichvarietyof confinedaquifer,whichisconfinedbetweenthinimpermeablebeds,containshorizontaltwo-dimensionalmazes. R ELATIONTO F ISSURE F REQUENCY DerekFordproposedamodelofcavepatternsbasedon theevolutionoffissurefrequency(spatialdensity)withinan aquifer(Ford,1971).Fissurefrequencyislowatfirstbut increaseswithtimeaserosionandcavedevelopment proceed.Theresultisafour-statemodel:(1)Atlowfissure C AVEGEOLOGYANDSPELEOGENESISOVERTHEPAST 65 YEARS:ROLEOFTHE N ATIONAL S PELEOLOGICAL S OCIETYINADVANCINGTHESCIENCE 6 N JournalofCaveandKarstStudies, April2007

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frequencyonlyafewphreaticloopsdevelop,whichextend wellbelowthewatertableandriseintheirdownstreamends. (2)Withincreasingfissurefrequency,loopsbecomemore abundantbutshallower.Thewatertabledropsasthe permeabilityincreases.(3)Eventuallyamixtureofphreatic andwater-tablecavesegmentsdevelops.(4)Fissure frequencymaybecomesogreatthatphreaticloopscannot form,andcavepassagesdevelopalmostentirelyalongthe watertable.Manycavesexhibitmorethanonestate,orthey maybypassoneormoreofthem.Twootherconditionsare possible(Ford,1988):state0,inwhichnofissuresatallare presentandcavescannotdevelop;andstate5,inwhichthere aresomanysmallopeningsthatgroundwateristoodiffuse toformsignificantcaves.Artesianconditionsareconsidered aspecialcaseinwhichmazecavesformbyslow,lengthy dissolution. L INKAGEOF C AVE P ASSAGES RalphEwersdemonstratedhowindividualcavepassageslinktogethertoformcomplexcaves(Ewers,1982). Givenvariousinputsatdifferentdistancesfromanoutlet, thosewiththeshortestpathsarethefirsttoformcave passages.Incipientcavesfedbymultipleinputscompete witheachother,andthefirsttobreakthroughtoaspring outletbecomesthemainconduit.Astheheaddecreasesin themainpassage,theflowfrommoreremoteinputsis drawntowardittoformtributaries.Todevelopthese concepts,Ewersusedmodelsconstructedofgypsum, plaster,andsalt,intowhichheinjectedwaterunder pressurealongartificiallypreparedfissures.Insomethe waterwasinjectedalongtheflatbottomofthesoluble blockandviewedfrombelowthroughatransparent bladderpressedagainsttheblock.Thelinkagemechanism issorobustthattherewaslittleornointerferencecaused bythecontrastsinhydraulicgradientanddissolution kineticsbetweenthemodelsandrealkarstaquifers.As theseideasdeveloped,theywerecombinedwiththoseof Fordinasinglepaper(FordandEwers,1978). O RIGINOF C AVE P ATTERNS ArthurPalmerattributedbranchworkcavestorecharge throughkarstsurfaces(e.g.,throughsinkholesandminor sinkingstreams)(Palmer,1975).Incontrast,heconsidered thatmazecavesformeitherbyintensefloodwaters(e.g.,by rechargefrommajorsinkingstreams)orbydiffuse rechargesuchasseepageintosolublerockthrough overlyingorunderlyinginsolublerocks.Themodelwas laterexpanded(Palmer,1991)bycombininghydraulics andchemicalkinetics,withtheaidofearliermeasurements oflimestonedissolutionrate(e.g.,Plummeretal.,1978): Earlycaveenlargementdependsontheratioofdischarge Q toflowlength L ( Q/L ).Theenlargementrateincreaseswith Q ,butonlyuptoacertainlimit.Furtherincreasein Q raisestheenlargementrateonlyslightly.Foraflowpathto growintoacave,itsdischargemustincreasewithtime. Onlyafewoftheoriginalflowpathsreachcavesize,asis typicalofbranchworkcaves.Theexceptioniswhereall openingsgrowathighratesfromthebeginning,toform mazecaves,inwhichmanyalternaterouteshavelarge Q/L Examplesincluderechargethroughanadjacentinsoluble rock(small L ),orperiodicfloodwaters(large Q ). Aggressivenessproducedbymixing,oxidationofsulfides, orcoolingofthermalwateralsotendstoproducemazes. Fullyconfinedartesianconditionsarenotsufficientby themselvestoformmazecaves.Thetimerequiredtoform acaveincreaseswithflowdistanceandtemperature,and decreaseswithinitialfissurewidth,hydraulicgradient,and CO 2 concentration. V ERTICAL L AYOUTOF C AVES StephenWorthington,asanoutgrowthofhis1991 Ph.D.dissertationatMcMasterUniversity,contributed twoimportantpapersontheverticaldistributionofcave passages(Worthington,2004,2005).Henotesthatmost largespringsdrainingregionalkarstaquifershavehigh sulfateconcentrations,andthatthecavesbeinginitiated withinthemmustencountersolublegypsumoranhydrite beds.Maximumcavedepthbelowtheoriginalwatertable isrelatedtotheextentofthecavefromheadwatersto spring.Here-interpretedcavelevels,notintermsof successivestagesofvalleyentrenchment,butinsteadas beingpartofthenaturalevolutionofacave.Hebasedhis ideaonthefactthatwarmwateratdepthhasalower viscositythancoldwaterandisabletoflowfasterunder agivenhydraulicgradient.Utilizingalargepersonaldatabaseoncavesfromaroundtheworld,hedevisedempirical formulasforcavedepthinrelationtoend-to-endlength andothervariables.Becauseofitsrelianceonfielddata,it isarareexampleofapredictivemodel. TheseconstitutethemainspeleogeneticmodelsdevelopedinAmericainrecentdecades.Othershavebeen offeredbyEuropeanspeleologists(seeKlimchouketal., 2000).Despitethedifferentapproaches,alloftheseideas arecomplementary.Eachauthorisacquaintedwiththe workoftheothersandhasalengthyfamiliaritywithcaves. Thereisstillhealthydebateaboutdetails,butonehopes thatthisalwaysremainsthecase. Besidesthegeneralmodelsforcaveorigindescribed above,therehavebeenseveralmoretangibleadvancesin cavegeology.Additionalstylesofbedrockdissolutionhave beendocumented,beyondthetypicalcarbonicacid reactioninmeteoricwater.Newmethodshavebeen developedfordeterminationofcaveagesandpaleoclimates.Digitalmodelsofcavegrowthhavebeendevised. Caveinformationhasbeenwidelyappliedtotheinterpretationofregionalgeologichistory.Thesetopicsare discussedindetailbelow. S EACOAST C AVES Studiesinthe1970sbytheU.S.GeologicalSurvey(e.g., Plummer,1975;Backetal.,1984)establishedthat A RTHUR N.P ALMER JournalofCaveandKarstStudies, April2007 N 7

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carbonatedissolutioncouldbecausedbymixingbetween freshwaterandseawateralonglimestonecoasts.This processwasacceptedwithoutdebatebyspeleologists, especiallybyscubadivers,butitwasnotuntilthelate 1980sthatfullattentionwasgiventothetopic.Theleaders inthefieldhavebeenJohnMylroieandJamesCarew,both ofwhomwereformerNewYorkerscapableoffacingthe rigorsofresearchontropicalbeaches.Theirstudiesinthe Bahamas(e.g.,MylroieandCarew,1990)clarifytheorigin, distribution,andagesofcavesincarbonateislands,aswell astheirrelationtopresentandformersealevels.Thetopic issummarizedinthecarbonateislandcavemodel(Mylroie andVacher,1999).Theresultofthisworkhasbeen embracedbyadiversegroupincludingsedimentologists, geochronologists,paleoclimatologists,andpetroleumgeologists.Cavestudiesaremostwelcomewheretheyhelpto addressproblemsinotherfields. S ULFURIC A CID C AVES Inthe1970s,whenitseemedthatthemaincontroversies inspeleogenesiswerefinallybeingironedout,anunexpectedmodeofcaveoriginwasrevealed.Inapreviewof thingstocome,DavidMorehousesuggestedthatsulfuric acidfrompyriteoxidationcouldaccountforcertaincaves ineasternIowa(Morehouse,1968).Soonafterward, StephenEgemeier,forhisdissertationatStanfordUniversity,chosetostudyagroupofcavesinWyomingÂ’sBighorn valley(suchastheKaneCaves),whichsmelledstronglyof hydrogensulfide.Hesoonrealizedthatthecaveswerestill intheprocessofformingbysulfuricacidproducedbythe oxidationofH 2 S,bothinthecavestreamandonthewalls andceilingsabove(Egemeier,1973,1981).Sulfuricacid attackofthebedrockleftarindofgypsum,which occasionallyspalledoff,felltothefloor,andwascarried awayinsolutionbycavestreams.Egemeierbrieflyvisited CarlsbadCavern(NewMexico)andnotedsimilaritiesto whathehadobservedinWyoming. Thiswasnotthefirsttimesulfuricacidhadbeenlinked tocaveorigin.Asearlyasthe1930s,researchersinItaly, Russia,Hungaryindependentlyproposedtheprocess,but theirstudieswereneitherdetailednorwellpublicized. Theideaofsulfuricacidspeleogenesistookholdamong severalwesternspeleologists(e.g.,Davis,1980).Meanwhile,DavidJagnowrecognizedtheroleofsulfuricacidin theoriginofcavesintheGuadalupeMountains,New Mexico,butattributedthemtooxidationofpyritein overlyingbeds(Jagnow,1977).Independently,J.Michael Queennotedgypsumreplacementinthewallsofcavesin theGuadalupeMountainsofNewMexicoandinterpreted thecaveinceptiontomixingbetweenfreshwaterand underlyingsulfate-richbrine(Queen,1973). CarolHillmeasuredsulfurisotopesintheCarlsbad gypsumandfoundalightisotopicratiothatsuggested biologicalredoxreactions,andthattheoriginalH 2 Smust havecomefromreductionofdeep-seatedsulfates,followed byoxidationtosulfuricacidwheretheH 2 Srosetothe watertableintheadjacentlimestonemountains(Hill, 1981).Bythetimeshepublishedherfullstudy(Hill,1987), theconceptofsulfuricacidspeleogenesiswaswellaccepted bymostspeleologists.Thetopiciscoveredthoroughlyin aspecialissueofthe JournalofCaveandKarstStudies (DuCheneandHill,2000). TheGuadalupecavestudieswerehamperedbythefact thatthecavesareinactiverelics.Evidencetosupport asulfuricacidoriginiscircumstantial.EventuallyNSS researchersbecomeawareofanH 2 Scavefarmoreactive thantheonesEgemeierhadstudied.Inthelate1980s,James PisarowiczandWarrenNethertonwereapparentlythefirst AmericanstoenterCuevadeVillaLuz,inTabasco,Mexico. ItcontainssickeninglyhighH 2 Sconcentrations,aswellas gypsumcrusts,longmicrobialfilamentswithhighlyacidic drips,andmanyfeaturesresemblingthoseoftheGuadalupes.Acombinedteamofgeologistsandbiologists examinedthecaveandgavesupporttotheinterpretations ofcaveoriginandmodificationthathadbeendevelopedin theGuadalupes(Hoseetal.,2000).AlthoughVillaLuzis muchmorepotentthantheKaneCaves,re-visitstothe KaneCavesshowedthattheycontainmanyofthesame features(e.g.,Engeletal.,2004). Therecognitionofsulfuricacidspeleogenesisopened thedoortoothertypesofdeep-seatedcaveorigin.Thiswas afieldwellknownineasternEuropebutbarelyrecognized inAmericauntilthemid-1980s(e.g.,Bakalowiczetal., 1987).Inoneoftheclearestexamples,FredLuiszer combinedastudyofcavesedimentswithgeochemical analysisofnearbyspringstoshowthatColoradoÂ’sCaveof theWindsistheproductofmixingbetweendeephigh-CO 2 waterandshallowlow-CO 2 water(Luiszer,1994). Apromisingnewtoolinhydrologyistheuseofrare elements,includingheliumisotoperatios,toidentifywater thathasrisenfromdeepigneoussources.MichaelSpildeet al.(Spildeetal.,2005)haveusedthistechniqueto determinethatabout6%ofthewaterinCuevadeVilla Luzcomesfromthesedeepsources. T HE G EOMICROBIOLOGYOF C AVE O RIGIN Thestudyofactivesulfuricacidspeleogenesisledtoan explosionofinterestincavegeomicrobiology.Before1990, reportsoffossilbacterialfilamentsinpaleokarstweremet withskepticism.Werethesesimplyageologicaberration? Onlyafewyearslater,atameetingoftheKarstWaters Institute,atwhichbiologistsandgeologistsfrommany diversefieldswerebroughttogether,theideasuddenly gelledthatmicrobiologyisthekeytomanykarstprocesses (seeproceedingseditedbySasowskyandPalmer,1994). Themainimportancetospeleogenesisisthatmicrobial mediationcontrolsmanykarst-relatedredoxreactions, includingtheproductionrateofH 2 Sandsulfuricacid (Cunninghametal.,1995;Northupetal.,2000).The quantitativeeffectofmicrobialmediationisstilluncertain, C AVEGEOLOGYANDSPELEOGENESISOVERTHEPAST 65 YEARS:ROLEOFTHE N ATIONAL S PELEOLOGICAL S OCIETYINADVANCINGTHESCIENCE 8 N JournalofCaveandKarstStudies, April2007

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butnoonequestionsitssignificance.Cavemicrobiology hasbranchedoffasamajorfieldofcavebiology.An intriguingoffshootofthesestudiesistheideathatcave microbiologymayprovideawindowtoextraterrestriallife (Boston,2000). G EOCHRONOLOGYAND P ALEOCLIMATOLOGY Speleogenesiscanbeunderstoodonlyintermsof geologictime,andquantitativemethodsofdatingcave depositshavehelpedgreatlytoadvancethefield.Manyof thetechniquesinradiometricdatingofspeleothemswere developedatMcMasterUniversitybyDerekFord,Henry Schwarcz,andtheirstudents(e.g.,Harmonetal.,1975). Mostspeleothemdatinginvolvesuranium-seriesmethods, whichyieldfairlyaccurateresultsasfarbackas600,000 years(tentimestherangeofC-14methods).Recent advancesinuranium-leaddatingcantheoreticallyreach backasfarasEarthÂ’sorigin,butthetechniqueisfairly complexanddoesnotworkwithallsamples.Anexample ofthetechniqueisgivenbyLundbergetal.(2000). TheMcMasterteamwasalsoamongthefirsttoapply oxygenandcarbonisotopicsignaturestotheinterpretation ofpaleoclimatesandchangesinoverlyingvegetation.This approachmakesitpossibletodetermineconditionson apreciselocalscale,whereasmostothermethodsprovide generalizedglobalaverages.Inthepastcoupleofdecades thisfieldhasbeentakenupbymanyresearcherswhodo notconsiderthemselvestobespeleologists. Throughoutgeologictime,themagneticfieldofthe earthreversesitselfperiodically,andthischangeis recordedinatinyresidualmagnetismlockedinrocks andsediments.VictorSchmidt(Schmidt,1982)measured thepaleomagnetismofsedimentsinMammothCave, Kentucky,anddeterminedthatthemiddlelevelsofthe cavepre-datethelastmagneticreversal,i.e.,theyareolder than780,000years.Thisapproachhasbeencarriedonby IraSasowskyandGregSpringertoclarifyentrenchment ratesinTennesseeandWestVirginia(e.g.,Sasowskyetal., 1995;Springeretal.,1997).Paleomagnetismcanalsobe measuredinmanycalcitespeleothems(Lathametal., 1979),and,whereitisalsopossibletodatethem radiometrically,thehistoryofmagneticvariationscanbe calibrated. Oneproblemwithdatingcavedepositsisthatthedates areinevitablyyounger(oftenmuchyounger)thanthecaves thatcontainthem.Butsomemineralsarealteration productsofsulfuricacidattackonclayandpresumably datefromthelatestphaseofsulfuricacidspeleogenesis. Some,likealunite(KAl 3 (SO 4 ) 2 (OH) 6 )canbedated radiometrically.VictorPolyakandhisco-researchers sampledthismineralincavesatvariouselevationsinthe GuadalupeMountainsandshowedthattheiragesrange from12millionto4millionyears,fromhighesttolowest elevations(Polyak,etal.,1998).Manyresearchersassume thatthedecreaseincaveagewithdecreasingaltitude indicatesagradualriseoftheGuadalupeblockwithtime, whilethewatertablestayedfixedatapproximatelythe sameelevation.Incontrast,DuCheneandCunningham (2006)suggestthatadeclineinthewatertablewascaused bylossoftheoriginalcatchmentareabythefounderingof faultblocksintheheadwaterregions.Thealunitedating techniqueisnowbeingappliedelsewhere,suchasGrand Canyon,inanattempttodeterminethehistoryoftectonic upliftandriverentrenchment. Quartz-richsedimentattheearthÂ’ssurfaceiscontinuallybombardedbycosmicradiation.Minuteamountsof radioactivealuminumandberylliumisotopes( 26 Aland 10 Be)areproducedinacertainratio.Whenthesediments areburiedorcarriedunderground,theseisotopesareno longerreplenished,andtheremainingonesdecay. 26 Al decaysfasterthan 10 Be,sowithtimethe 26 Al/ 10 Beratio decreases.Bymeasuringthisratio,theageofthesediment burialcanbeestimated.DarrylGrangerwasthefirstto applythistechniquetocaves(e.g.,Grangeretal.,2001; AnthonyandGranger,2004).Thesestudieshavehelpedto sortouttheevolutionoftheOhioRiverdrainage.After morethanacenturyofexplainingcavesintermsofsurface erosion,speleologistscannowreversethetrendbyusing cavestoexplainthehistoryofsurfaceerosion. D IGITAL M ODELING Ascomputertechnologyhasbecomemorepowerful andaccessibleoverthepastfewdecades,digitalmodeling ofcaveoriginhasbecomefeasible.Thefirstworking modelsoflimestonecavedevelopmentweredevelopedin theearly1980sbyArthurPalmertodeterminethe functionalrelationshipsamongthevariablesinvolvedin speleogenesis(initialfissurewidth,hydraulicgradient,flow distance,etc.).Theresultsformedthebasisforoneofthe conceptualmodelsdescribedabove(Palmer,1991).Chris GrovesandAlanHowarddevelopedsimilarmodelsin two-dimensionalgridsbutfoundthatcomputertechnology wasnotyetadvancedenoughforthemtorealizethefull potentialofthemethod(GrovesandHoward,1994; HowardandGroves,1995).Grovesreportsthatonemodel tiedupthemainframecomputeratWesternKentucky Universityforanentirenight. Soonafterward,astechnologyadvanced,karstresearchersinGermanyandFrancedevelopedcomputer modelscapableofsolvingcomplextwo-dimensional problemsofspeleogenesis.Workinthisfieldhasprogressedatarapidpace.Theresultstendtosupportearlier conceptualmodels,buttheyalsoprovidequantitative estimatesoftherelativeimportanceofsuchprocessesas mixingbetweenwatersofdifferentchemistry.Dreybrodt andhisco-researchershavesummarizedtheadvancesin thefieldinabookaccompaniedbyaninteractivecompact disk.TheyandotherEuropeanresearchersarenowthe undisputedleadersinthedigitalmodelingofkarst (Dreybrodtetal.,2005). A RTHUR N.P ALMER JournalofCaveandKarstStudies, April2007 N 9

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N ON-SOLUTIONAL C AVES ThroughoutthehistoryoftheNSS,therehasbeen continuedbutlow-levelinterestinnon-solutionalcavesand pseudokarst,butinthepast15yearsthestudyoflavacaves hasgrownenormously(Halliday,2004).KazumuraCave, a60-km-longlavacaveinHawai‘i,isnotonlytheworld’s longestexploredlavacave,butalsobyfarthedeepest Americancaveofanykind(deep,thatis,ingreatest verticalextent,butnotindepthbelowthesurface).The HawaiianSpeleologicalSurveyandCaveConservancyof Hawai‘inowinvolvemanylocalresearchersaswellas frequentvisitorsfromthemainland.Newdiscoveriesare madeeveryyear,especiallyonthebigislandofHawai‘i, andtheyprovideafreshperspectiveoncaveorigin. C URRENT R OLEOFTHE NSS IN C AVE G EOLOGY TodaytheNSSworkscloselywithmanyotherkarst organizations,bothinAmericaandinothercountries. OverthehistoryoftheNSS,manyaffiliatedgroupshave branchedoff,buttheyhaveallcomplementedthegoalsof theSocietyandhavemanymembersincommon.The scientificstatusoftheNSShasbeenstrengthenedbythis mutualcooperation. TheNSShasrecentlypublishedthebook Speleogenesis: Theevolutionofkarstaquifers ,editedbyaninternational team(Klimchouketal.,2000),whichincludescontributionsfromauthorsaroundtheworld.Thisbookhas providedafoundationfortheWebsitewww.speleogenesis. info,whichpublishesarticlesinthefield,bothnewand fromrelatedjournals,andservesasaclearing-housefor informationaboutthetopic.The JournalofCaveandKarst Studies includesreviewsofallothermajorinternational karstjournals,whichhelpstopublicizeworkinspeleology throughouttheworld.TheNSSalsooffersseveralresearch grants,thelargestandmostprestigiousofwhichisthe RalphStoneGraduateFellowshipinCaveandKarst Studies. ThestatusofgeologiccaveresearchinAmericahas blossomedinrecentyears.Forexample,specialsessions andsymposiainthefieldarefrequentlysponsoredbyNSS membersatannualandregionalmeetingsoftheGeological SocietyofAmerica.Atsomerecentnationalmeetings, karstsessionsoutnumberedthoseinallbutahandfulof majorfieldsingeology.In2004,DerekFordandWilliam WhitewerejointlyhonoredbyGSAfortheirlifetime contributionstokarst(seecommemorativevolumeedited byHarmonandWicks,2006). Thereasonsforthisexplosionofinterestareclear. Recentadvancesindating,paleoclimatology,porosity evolution,andgeomicrobiologyhaveapplicationstomany otherfields.Severalhigh-profilejournalarticlesincave geologyandspeleogenesishavebroughtwidespread attention.Highlyregardedbooksonkarsthydrologyand geomorphologyhavebeenproducedbyNSSmembers (e.g.,White,1988;FordandWilliams,1989;Whiteand White,1989).Newacademiccentersofkarstresearchhave appearedinrecentyears,asaquickWebsearchcanshow. Anorganizationdoesnotmakescientificdiscoveries: individualsdo.ButtheNSSasawholehascontributedto thefieldinauniqueway.TheSocietyprovidesasenseof sharedpurposeinwhichthescientistssharecommon groundwithexplorersandmappers,withoutwhose achievementsthesciencewouldnotbewhereitistoday. A CKNOWLEDGMENTS IthankreviewersDerekC.FordandRichardA.Watson fortheirvaluablesuggestions.Ialsoextendmyadmiration toallcontributorstocavegeology,includingthemanywho arenotcitedinthisbriefoutline. R EFERENCES Anthony,D.M.,andGranger,D.E.,2004,ALateTertiaryoriginfor multilevelcavesalongthewesternescarpmentoftheCumberland Plateau,TennesseeandKentucky,establishedbycosmogenic 26 Aland 10 Be:JournalofCaveandKarstStudies,v.66,no.2,p.46–55. Back,W.,Hanshaw,B.,andVanDriel,J.N.,1984,Roleofgroundwater inshapingtheeasterncoastlineoftheYucata nPeninsula,Mexico, in LaFleur,R.G.,ed.,Groundwaterasageomorphicagent:Boston, Massachusetts,AllenandUnwin,Inc.,p.281–293. 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THEIMPORTANCEOFCAVEEXPLORATIONTO SCIENTIFICRESEARCH P ATRICIA K AMBESIS 1906CollegeHeightsBlvd,HoffmanEnvironmentalResearchInstitute,We sternKentuckyUniversity,BowlingGreen,Kentucky42101, Pat.Kambesis@wku.edu Abstract: Ofthemanyobjectsofscientificinterest,cavespresentauniquechallen ge because,exceptforentranceareas,cavesarelargelyhiddenfromview.As aconsequence, caveshavenotgenerallyattractedtheattentionofmainstreamscientist s.Withthe exceptionofcaveentrancesnotedonsometopographicmaps,mostcavesare not apparentfromtopographicmaps,satelliteandLANDSATimagery,oraerial photographs.Cavesandtheirfeaturesexistinanenvironmentwithnonatu rallight andcontainamyriadofphysicalandpsychologicalobstacles.Itisthecav eexplorerwho venturespasttheseobstacles,motivatedbycuriosityandthedesiretofi ndanddocument placespreviouslyunknown.Systematiccaveexplorationisatwo-foldpro cessthat involvesthephysicalpursuitanddiscoveryofcavesandcavesystems,and field documentationthatprovidesbaselinedataintheformofcavesurveydataa ndnotes, caveentranceandcave/karstfeaturelocationsandinventories,written observations,and photo-documentation.Thesedataaresynthesizedintocavemaps,topogra phicoverlays, narrativedescriptions,andreportsthatserveasexplorationtoolsforf indingmore passagesandcaves.Systematicdocumentationanditsderivativeproduct salsobringthe hiddennatureofcavesandtheirfeaturestotheattentionofscientistsan dprovideabasis notonlyforcave-relatedresearchbutforawiderangeofrelatedscientif icendeavors. I NTRODUCTION Cavespresentauniquechallengetoscientificstudy because,exceptforentranceareas,cavesarelargelyhidden fromview.Asaconsequence,caveshavenotgenerally attractedtheattentionofmainstreamscientists.Withthe exceptionofcaveentrancesnotedonsometopographic maps,mostcavesarenotapparentfromtopographicmaps, satelliteandLANDSATimagery,oraerialphotographs whicharethetoolsthatmanyearthscientistsuseto visualizetheshape,form,andorientationoflandforms (Kambesis,2003).Cavesandtheirfeaturesexistinan environmentwithnonaturallightandcontainamyriadof physicalandpsychologicalobstacles.Itisthecaveexplorer whoventurespasttheseobstacles,motivatedbycuriosity, andthedesiretofindanddocumentplacespreviously unknown. Inscientificresearch,thereareavarietyofquestions thatprovidedirectiontothepursuitofknowledge.Incave exploration,theinitialquestionisverysimple:Doesitgo? Thisisthequestionthathooksthecaveexploreranddrives her/hiscuriositytowardananswer.Butthatansweronly bringsmorequestionssuchashowfar,howlong,how deep?Duringtheexplorationprocess,asacavesystemor cavearearevealsitscomplexity,thequestionsalsochange. Forexample,whatisthecave’srelationshiptothesurface, andtosurroundingcaves?Whatarethefeaturesand obstaclesthatthecavecontains?Thoseinvolvedinserious caveexplorationknowthattheonlywaytoanswerthese questionsiswithsystematicdocumentationintheformof caveandsurfacesurveys,detailednotesandobservations, cave/karstfeaturelocationsandinventories,andphotodocumentation.Thedataaresynthesizedintocavemaps, narrativedescriptions,andreportsthatcanserveasasetof explorationtoolsforfindingmorepassagesandcaves.The fielddocumentationanditsderivativeproductsalsoserve asthebaselinedataforalltypesofcave-relatedresearch. Themostimportantderivativeproductsofsystematic caveexplorationaremaps,whichillustratetheextentand layoutofthecave,shapesofpassages,andifaprofileis included,thethreedimensionalrelationshipofthepassages.Amapnotonlyportraysthegeographyofacave, butdependingonitslevelofdetail,canshowthelocation offeatureswithinthecave.Cave/karstfeatureinventories arebecomingmorecommoninthedocumentationprocess, especiallybecauseoftheincreasedavailabilityandaccess toGIStechnologywhichallowsmoredetailedcave/karst featuredatatobeintegratedwiththesurveyand cartographicdata.Photographyisanotherimportant aspectofcavedocumentation;adescriptionofunderwater helictites,u-loops,orchandemitespalesincomparisonto thephotographsthatrecordtheirexistence.Systematic documentationanditsderivativeproductssuchascave maps,topographicoverlays,reports,inventories,and photographsbringthehiddennatureofcavesandtheir featurestotheattentionofscientistsandprovideabasis notonlyforcave-relatedresearch,butforawiderangeof scientificendeavorssuchasarchaeology,evolutionary biology,hydrogeology,geology,geomicrobiology,mineralogy,andpaleoclimatestudies,tonamejustafew. PatriciaKambesis–Theimportanceofcaveexplorationtoscientificrese arch. JournalofCaveandKarstStudies, v.69,no.1,p.46–58. 46 N JournalofCaveandKarstStudies, April2007

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Inorderforexplorationdocumentationtobeofvalue, itmustbeaccessible.Muchoftheearlyinformation generatedbycaveexplorationintheUnitedStateswasnot publishedinpeer-reviewedjournals,publications,or popularmagazines.WiththeformationoftheNational SpeleologicalSocietyanditsmanychapters(grottos)came nationalandregionalpublicationsthatservedasvenuesfor accountsofcaveexplorations,maps,cavesurvey/research projectreports,andphotographs.Statecavesurveys, usuallyorganizedbyactivecaverswithinastateorregion, servedasarchivesandcatalogsofcavedata.Manyofthe statecavesurveyspublishedmaps,reports,regional overviews,andresultsofscientificresearchincavesof theirrespectiveareas.Oftenthesearetheresourcesthat scientistsusetoaccessinformationaboutcaves,their characteristics,andfeatures. Systematiccaveexplorationanddocumentationprovideanessentialfoundationforcaveresearch.Inturn,the resultsofcaveresearchalsoservethecaveexplorerinher/ hiseffortsinfindingmorecave.Twocasestudiesare presentedtoillustratehowcaveexplorationaffectsthe courseofcavescienceandviceversa.SystematicexplorationsintheMammothCaveareainKentucky,andinthe GuadalupeMountainsofNewMexico,aresubmittedas examplesofhowthetangibleresultsofcaveexploration (i.e.,surveynotes,initialobservations,andphotographs), andtheirderivativeproducts(i.e.,cavemaps,topographic overlays,fieldnotes,andsummaryreports)providedthe basisforthecaveresearchthatfollowed. C ASE S TUDY 1:E XPLORATIONAND S CIENTIFIC R ESEARCH INTHE M AMMOTH C AVE A REA EffortstosurveyMammothCavebeganaftertheWar of1812(Smith,1960)withthepurposeofestablishingthe relationshipbetweencavepassagesandsurfaceproperties forcommercialdevelopmentofcavesfortourism.Other surveysweremadeinsupportofconstructionprojectsfor touristentrances,walkways,andlightingsystems.Dueto commercialcompetitionamongshowcavesintheMammothCaveareaandthemarketabilityofcalciteandsulfate deposits,mostofthesurveysandmapswerekeptsecret. Accesstothecavesforscientificstudywasusuallydenied (SmithandWatson,1970). In1930,world-renownedgeographerandgeomorphologistWilliamMorrisDavispublishedascientificpaper arguingthatcaveswerenotformedabovethewatertable, aswascommonlysupposed,butwereinsteadtheresultof undergroundwatercirculatingdeepbelowthewatertable (Davis,1930).BecauseofDavisÂ’longandimpressive reputationasanearthscientist,thepaperwasembracedby theU.S.scientificcommunitythoughitcontainedlittle supportingfieldevidence.Davisusedsomeoftheexisting mapsofMammothCavetohelpdevelophistheory (WatsonandWhite,1985).Unbeknownsttohim,mostof theearlymapswerenotaccuraterepresentations,butwere atbest,fancifulrenditionsofthecavewhichportrayedits morphologyasagiantlabyrinth(Fig.1),ratherthan havingamodifieddendriticpattern(WatsonandWhite, 1985).In1942,JHarlenBretzpublishedapaperoncave developmentthatattemptedtoprovidefieldevidencein supportofDavisÂ’theory(Bretz,1942).Whatfollowedwas afifteenyearhiatusinwhichlittleofconsequenceappeared inthescientificliteratureofNorthAmericaoncave development(White,1973).Itwasnotuntilsystematic explorationsintheMammothCaveareabegandocumentingthenature,extent,andlayoutoftheMammothCave system,wasitrealizedthatDavisÂ’theoryoncave developmentmightbeflawed(Whiteetal.,1970). M ODERN E XPLORATIONUNDER F LINTAND M AMMOTH C AVE R IDGES ModernexplorationintheMammothCaveareabegan onFlintRidgein1947byDr.E.R.Pohl,JimDyer,and BillAustin.Theirfocusincludednotonlyextendingthe physicallimitsofthecavesunderFlintRidge,butalso conductingscientificinvestigations.In1954theNational SpeleologicalSocietysponsoredaweek-longexpeditionin CrystalCave,whichinthepasthadbeenoperatedas ashowcave.Thoughnomajordiscoveriesweremade duringthatexpedition,itprovedtobealearning experienceincaveprojectmanagementandinsystematic explorationandsurveytechniques,andultimatelyresulted intheestablishmentoftheCaveResearchFoundation (CRF)in1957.ThegoalofCRFwastoexploreandmap cavesforthepurposesoffurtheringscientificresearchand understandingofcaves(Watson,1981). CRFadoptedamethodofsystematicexplorationthat involvedmappingcavepassages,correlatingthesurveyed cavepassagesandtheirelevationswithtopographicmaps, aerialphotographs,andelevationcontrolssuchasgeographicsurfacebenchmarks(Bruckeretal.,1966).Detailed tripreportscontainingpassageandfeaturedescriptions werealsoimportanttothesystematicdocumentation process.Withthesetools,theextentoftheFlintRidge andMammothRidgecavesbegantoberealizedalongwith theestablishmentofageographiccontextforscientific workoncaveoriginanddevelopment. CRFÂ’sworkbeganonFlintRidgewherefivemajor cavesandanumberofsmallercaveswerelocated.The impetusfortheseeffortswasthepotentialforconnections betweenthemajorcavesoftheMammothCavearea.This potentialwasfirstexpressedbyE.A.Martelafterhe visitedMammothCavein1912(Martel,1912).He predictedthatFlintRidgeandMammothCavesystems wouldsomedaybephysicallylinkedtomakeasystem 241kminlength(BruckerandWatson1976).Accomplishingsuchachallengewasagreatmotivatortothecave explorersanddrovethemtodiligentlypushandmapall varietiesofcavepassageslargeandsmall,dryandwet, magnificentandmiserable. SystematicexplorationsinFlintandMammothridges notonlyrackedupsignificantsurveyfootage,butalso P ATRICIA K AMBESIS JournalofCaveandKarstStudies, April2007 N 47

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providedimportantobservationsthatwouldimpactfuture explorationsandscience.Mapoverlaysshowedthatcave passagescouldextendoutfromthemajorridgesandunder thevalleysintheMammothCavearea(Smith,1960). Manyofthelargecavepassagesweredeterminedtobe segmentedpiecesoflongerpassagesthathadbeen dissectedbyvalleydevelopment(Brucker,1966).Vertical shaftsthatwereverycommonintheMammothCavearea couldpenetratethroughtiersofhorizontalpassagesgiving accesstopreviouslyunexploredcave(Bruckeretal.,1972). By1961,themajorcavesofFlintRidge,including Crystal,Unknown,Colossal,andSaltsCavewereconnected(Fig.2).Inadditiontothespeleologicalaccomplishmentofconnection,systematicexplorationalsobegan toconfirmandanswergeologicalquestionsandtocast doubtonDavisÂ’theoriesontheoriginsoflimestonecaves (Smith,1960).Surveynotes,workingdraftmaps,written observations,anddetailedreportsrevealednotonlythe geographicextentofthecaves,butnotedthecrosssectionalshapesofpassagesandthefeatureswithinthe passages.Thesewerethetypesofdetailsnecessaryto successfullyexploreacavesystem,andalsotobegin understandinghowcavesystemsformed.Topographic overlaysgavegeographiccontexttothemorphologyand extentofcavepassages.Ineffect,exploringanddescribing theFlintRidgeSystemmadeitpossibletobeginarational descriptionofboththecavern-formingprocessingeneral, andthehistoryoftheFlintRidgecavecomplexin particular(Smith,1964). Oneofthefirstgeologicquestionsthatwasaddressed bythesystematicexploration/surveymethodwastheorigin ofverticalshaftsinthecavesofFlintRidge.Though anumberoftheorieswereproposedtoexplainthem, ageographiccontextwasmissing.Pohl(1955)setforth thehypothesisthattheverticalshaftswererelatedtothe solutionalenlargementofverticalcrossjointsandthat theirdevelopmentwasrelatedtotheprocessofheadward andarealadvanceofsurfacevalleys.Cavesurveyswhich locatedverticalshafts,whenaddedtothetopographic overlays,confirmedthatthevastmajorityofthesefeatures wereindeedlocatedattheedgesofthesandstone-capped ridges(Fig.3).Observationsmadeduringsurveytrips indicatedthattherewasnorelationshipbetweenthe verticalshaftsandlateralpassagesandthatshaftdrainages uselateralpassagesonlywhenthesepassagesoccuratbase levelandbeneathactivelyformingshafts(Smith,1957). Systematicexplorationconfirmedthatverticalshaftswere notspeleogeneticallyrelatedtothevastpassagesand roomsthattheyintersected(Bruckeretal.,1972). Theoccurrenceandsignificanceofbreakdownwas anotherquestionwhoseanswerwasaugmentedbythe observationsofcaveexplorers.Accordingtoobservations byDavies(1951),limestoneandsandstonebreakdowncan occurwherepassagesareclosetothesurface,especially wherehorizontalcavepassagesareintersectedbyhillsides. Theintersectionoflargepassagescouldalsoresultin breakdown.However,therewereareasintheFlintRidge caveswherenoneofthoseconditionsexisted,but Figure1.StephenBishopÂ’smapofMammothCave,1842(CRF,1976) T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 48 N JournalofCaveandKarstStudies, April2007

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breakdownstilloccurred.Caveexplorersreportedwhite crystallinecoatingsandcrustsassociatedwithbreakdown, andthesamplesbroughtbackbyexplorerswereidentified asgypsumandothersulfates.Withthatinformation,itwas determinedthat insitu mineralgrowthofgypsumand othersulfatesalongbeddingplanesandjointsputpressure onthesezonesofweaknessandcausedtherocktopeeloff theceilingandwalls,thusformingbreakdown(Smith, 1957). ExplorationofnewpassagesinFlintRidgerevealed unusual,previouslyundescribedspeleothems.Photographs weremadeofthenewfeaturesandsampleswerelater collectedbytheexplorationteam.Laboratoryanalysis showedthatgypsumcouldcombinewithothersoluble sulfatestoproducemetastablesulfatemineralslike mirabilite.Theresultsofthisstudywerepublishedinan issueofScience(Bennington,1959)andrevealedthat thermodynamicallyunstablemineralphasesdevelopingat relativelylowtemperaturesmightindicatetheoccurrence ofcomplexheterogeneousreactionsworthyoffurther kineticstudies(Smith,1960). Blackcoatingsobservedontheceilingsofpassagesin MammothandSaltsCaveswereinitiallythoughttobe manganese.However,analysisrevealedthatthecoatings wereorganic;specificallysoot(Smith,1960).Exploration teamsreportedthatsootcoatingswerealwaysfoundin associationwitharchaeologicalmaterial(unpublished CaveResearchFoundationreports1957–1965).Assystematicexplorationprogressedintopreviouslyunknown territories,morearchaeologicalartifactsandtracesof activitieswerediscovered.In1962,Watsonbeganasystematicinventoryofarchaeologicalfeatures.Notonlydid shedeterminethatancientpeoplehadusedthecavefor miningpurposes(Watson,1969),herresearchultimately revealedthattheprehistoricpeopleinKentuckyandthe EasternWoodlandswereamongthefewindigenous populationsintheworldtoindependentlydevelopan agriculturaleconomy,wellbeforedomesticatedplantswere introducedfromMexico(Watson,1992).Watsonwas inductedintotheNationalAcademyofSciencesinpart becauseofthiswork. Figure2.FlintRidgeSystem1962(CRF,1966). Figure3.VerticalshaftsintheMammothCavearea(from White,1988). P ATRICIA K AMBESIS JournalofCaveandKarstStudies, April2007 N 49

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CRFhelpedsupportbiologicresearchoncaveanimals byproducingcavemapsforbaselineecologicstudies.The mapofCathedralCave(Fig.4)inMammothCave NationalPark,withbaselinetransectsnoted,wasprovided toresearcherswhowereconductingstudiesonpopulation dynamicsofcavefauna(CRF,1961).Thiswasthe beginningofmanybiologicstudiesintheMammothCave area.Theobservationsbysurveyteamsaboutthe compositionofsedimentsandothermaterialoncave passagefloors(substrates)providedimportantinformation forresearchoncaveecology.KaneandPoulson(1976) studiedtheforaginghabitsofcavebeetlesinheterogeneous mixesofsubstratesandhomogeneoussubstrate(uncompactedsand)inLittleBeautyCaveandinGreatOnyx Cave,respectively.Studiesonthelong-termeffectof weatheroncricketpopulationswithinWhiteCaveand LittleBeautyCavedemonstratedtheimportanceof weatherpatternsoncricketpopulations(Poulson,etal., 1995).Poulson(1991)establishedthataquaticsubterraneanfaunalpopulationswereimportantindicatorsof groundwaterquality. ThesystematicexplorationconductedbyCRFprovidedthefieldevidencenecessaryforscientiststobeginto formulatearegionaloverviewofthegeologicprocessesand cavedevelopmentoftheMammothCavearea.Asaresult ofthisextensivefieldworkandtheinterpretationofthe databyWhiteetal.(1970),apapertitled‘‘TheCentral KentuckyKarst’’waspublishedin TheGeographical Review .Thepaperdiscussedthegeology,mineralogy, andhydrogeology,andtheirrelationshiptounderground karstfeatures.Theworkoutlinedthephysiographic evolutionoftheMammothCaveareaandclassifiedkarst asadynamicsystem.Thisnewperspectiveoncave developmentreplacedtheDavisianmodelofdeepphreatic-cavedevelopmentfortheMammothCaveregion. Afterthe1961connectionsatFlintRidge,CRF extendedtheireffortstoMammothandJopparidges.In 1969theFlintRidgeSystembecamethelongestinthe worldat108kminsurveyedlength.Concurrentsystematic explorationsatMammothCavebroughtitssurveyed lengthto73kmmakingitthethirdlongestbehind Hoelloch(Switzerland).Theseimpressiveaccomplishments inspeleologywerejustinterimgoalsforthosewhowere dedicatedtosystematicexploration.Withtheireyesonthe nextprize,CRFexplorersaimedatconnectingthefirstand thirdlongestcavesintheworld.Longanddifficultcave tripsguidedbyworkingmapsandtheobservationsand reportsofmanysurveyteamspushedthelimitsoftheFlint RidgeSystemunderHouchinsValleyandintoMammoth Ridge.In1972,asmallteamofCRFcavers,representing thecumulativeeffortsofallofthosebeforethem, connectedtheFlintRidgeSystemtotheMammothCave Systemmakingitthelongestcaveintheworldwithalength of232km(BruckerandWatson,1976). In1978,caveexplorersdiscoveredasubterraneanriver underJoppaRidgeanditwasultimatelyconnectedtothe Flint-MammothCaveSystem.Systematicexploration pushedtheupstreamextentoftheLogsdonRivereast underavalleytowardTooheyRidge,thehomeofRoppel Cave,whoseexplorationandsurveywasaprojectofthe CentralKentuckyKarstCoalition(CKKC).In1983,CRF andCKKCconnectedRoppelCavetotheFlint-Mammoth CaveSystem(BordenandBrucker,2000).Thenew connectionbroughtthesurveyedlengthoftheFlintMammoth-RoppelSystemto493km. Whileactiveexplorationeffortsextendedthephysical limitsoftheFlint-MammothCaveSystemintotriple digits,scientificresearchthatutilizedthebaselinedataand derivativeproductsgeneratedfromcavesurveysflourished. Intheearlyseventies,researchersbeganalevelingand geologicsurveyinFloydCollinsCrystalCavewiththe goalsofdeterminingthestratigraphicsectioninwhichthe Flint-MammothCavesystemisdeveloped,toclarifythe presenceofpassagelevelsandtheirgeomorphicsignificance,andtomakeadetailedmapofthecave(Palmer, 1987).Theyusedcopiesoftheoriginalsurveynotesthat spannedtwenty-fiveyearsofexplorationefforttoconstruct abasemap.In1974,thestratigraphiccolumnfromCrystal Cavewasextrapolatedtomostofthemajorcavepassages intheFlint-MammothCaveSystem.Passagelevelswere Figure4.CathedralCave,MammothCaveNationalPark (CRF,1961) T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 50 N JournalofCaveandKarstStudies, April2007

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describedandcorrelatedwiththegeomorphichistoryof thesurroundinglandscape(MiotkeandPalmer1972).The relevanceofthepassageleveldatafromthegeologicand levelingstudywasaugmentedwithcosmogenicdatingof gravelsfromMammothCave.Theresultsofthiscollaborationillustratedthefar-reachingeffectsofPleistocene glaciationontheevolutionoftheOhioRivervalley,onthe GreenRiver,andultimatelyontheFlint-MammothCave System(Grangeretal.,2001). Hydrogeologyisanimportantresearchfrontierinthe MammothCavearea.Withacurrentextentofover 608km,theFlint-MammothCaveSystemconsistsof ahugecollectionofactive,semi-active,andinactive conduitsthatarepartsofavastkarstaquifer. EarlyworkonhydrogeologyintheMammothCave areawasconductedbyWhiteetal.,(1970),White(1976), HessandWhite(1973,1974),andMiotke(1975).Extensive dyetracingandgeochemicalanalysisbyJimQuinlan,who workedasthegeologistforMammothCaveNational Park,augmentedtheongoinghydrogeologicstudies. Quinlanmaintainedthatsystematiccaveexploration/ surveywasthekeytodiscoveringandunderstandingthe hydrologyoftheflowsystemofaprinciplekarstaquifer (Quinlanetal.,1983).CRFprovidedsupportforQuinlanÂ’s hydrogeologicstudiesintheformofcavemapsthathe consideredcriticalforhisresearchinsideMammothCave NationalPark(Zopf,1982).Quinlanalsoutilizedteamsof caveexplorerswhoworkedoutsideoftheNationalParkto providethedataandinsightnecessarytostudythevast aquiferoftheMammothCaveregion(Quinlanetal., 1983).HisteamsdiscoveredanddocumentedanundergrounddistributarysystemontheGreenRiver,the HiddenRiverComplexthatwashydrogeologicallyrelated toHiddenRiverCaveinHorseCave,Kentucky(Coons, 1978).Theyalsodiscoveredandconductedsystematic explorationinWhigpistleCavewhichQuinlanprovedvia dyetracestobehydrogeologicallyconnectedtotheFlintMammothCaveSystem(Coons,1978).Exploration-relateddataaugmentedQuinlanÂ’sstudyofthemovementof groundwaterintheMammothCaveregion.Hisresearch ultimatelyrevealedthatagriculturalandindustrial contaminantswereenteringtheFlint-MammothCave Systemfromplacesoutsideofthenationalpark(Quinlan, 1989). Aspecificexampleofthepracticalapplicationof QuinlanÂ’sfindingsinvolvedhisidentificationofasewage treatmentplantinHorseCave,Kentuckyasasourceof groundwaterpollution.Theseriousnessofthepollution wasreflectedinHiddenRiverCave,locatedinthemiddle oftown.Thestenchofsewagerosefromthecaveentrance andpermeatedthedowntownarea.Thetreatmentplant wasdischargingheavymetalsintothegroundwaterand Figure5.CavesoftheMammothCaveregion(BordenandBrucker,2000). P ATRICIA K AMBESIS JournalofCaveandKarstStudies, April2007 N 51

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wasnoteffectivelytreatingsewage(Quinlan,1989).Once thephysicalfunctioningofthesewagetreatmentplantwas upgraded,thereweresignificantimprovementsinthewater andairqualityofHiddenRiverCave. The1978discoveryoftheLogsdonRivermadeit possibleforscientiststostudythebehaviorandcharacteristicsofakarstaquiferfromtheinside.Basedoncave surveyandcaveradio-locations,Quinlaninstigatedthe drillingofanentranceshaftandaseriesofwellsdirectly intotheLogsdonRivertofacilitateongoinghydrogeologyrelatedresearch.Thenewentranceshaftallowedthe installationofdata-loggingequipmentthatmonitored changesinstreamflowandgroundwaterchemistryover avarietyoftimescales.GrovesandMeiman(2001)were abletoquantifythatlargestormeventsplayasignificant roleonkarstaquiferdevelopment.Grovesetal.(2001)also observedthatinterstitialcave-streamfluidsshowedevidenceofbacterialfunctionsthatmayinfluenceaquifer evolution. AregionalmapoftheMammothCavearea(Fig.5) showstheresultsoffiftyyearsofsystematiccave explorationintheregion.Over833kmofpassageshave beenexploredandmappednotonlywithintheFlintMammothCaveSystem,butinothercaveslocatedoutside ofthenationalpark.Quinlanetal.,(1983)suggestedthat thepotentialforover1,600kmofhuman-sizedpassages existsintheMammothCavearea.Thispotentialcontinues tomotivatecaveexplorerstoextendthelimitsofthe worldÂ’slongestcavesystem,andforcavescientiststo expandthefrontiersofknowledgeaboutsuchtopicsas karstaquifers,ancienthumanuseofcaves,water-rock interactionsandtheireffectsoncavedevelopment,andthe roleofmicrobiologyinspeleogenesis. C ASE S TUDY 2:C AVE E XPLORATIONAND S CIENCEINTHE G UADALUPE M OUNTAINS ,N EW M EXICO ThecavesoftheGuadalupeMountainshavelongheld thefascinationofcaveexplorersandcavescientistsalike. Intheearlydaysofcaveexplorationandresearch,the cavesprovedtobeenigmatictobothgroupsbecauseofthe morphologyandlayoutofthecaves,bytheseeminglackof relationshipbetweencaveandsurfacefeatures,andbythe occurrenceofmassivegypsumdepositsandotherunusual mineralogy.Thefirsttwofactorsmadecavesdifficultto find,explore,andmap.Allthreeprovedpuzzlingwithin thescientificcontextofwhatwasknownaboutcave development. EarliestexplorationsofcavesintheGuadalupe Mountainsbeganinthelatterpartofthe19 th century (Kunath,1978).JimWhitefirstenteredCarlsbadCavernin 1898(Selcer,2006)andextensivelyexploreditforthirty years(White,1932).Intheearlypartofthetwentieth Figure6.AsectionofEndlessCave,NewMexico(fromKunath,1978). T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 52 N JournalofCaveandKarstStudies, April2007

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century,Nymeyer(1978)photographedmanyofthecaves intheGuadalupeMountainsandpublishedphotographs alongwithaccountsofhisexplorationsinabooktitled Carlsbad CavesandaCamera .However,systematic explorationandmappingofGuadalupeMountaincaves didnotbeginuntilthe1960s(Kunath,1978)withworkby theTexasSpeleologicalSurvey,theGuadalupeCave Survey(whichlaterbecamepartofCaveResearch Foundation)and,someofthelocalgrottosinTexasand NewMexico.Thecavemapsproducedfromthoseefforts illustratedthecomplexthree-dimensionalmorphologyof thecaves(Fig.6).Somesectionsofcavemapswere intentionallyomittedduetothedifficultyofgraphically renderingmulti-levelmazesintwodimensions(Lindsley andLindsley,1978).Detaileddescriptivesummaries writtenbycaveexplorersprovidedinformationaboutcave features(Kunath,1978)andreportedonunusualmineralogy(Davis,1973). ThefirstgeologisttostudyGuadalupeMountaincaves wasWillisT.Lee.Heparticipatedintwoexpeditionsto CarlsbadCavernsponsoredbytheNationalGeographic Society.LeeÂ’scontributionsweremostlydescriptivein natureandhemadeapreliminarysurveyofthecavern whichwaspublishedinNationalGeographicMagazine alongwithphotographsbyRayDavis(Lee,1924,1925).J HarlenBretzconductedscientificfieldworkinGuadalupe Mountaincavesin1948(withoutthebenefitofcavemaps), proposingthatthecaveswerephreaticinorigin.Bretz (1949)identifiedthegypsumdepositsheobservedasatype ofgypsumflowstone.Othergeologistshypothesizedthat massivegypsumwastheresultofalate-stagebackupof waterfromtheCastileFormationoftheDelawarebasin (Jagnowetal.,2000). Ascavescientistsbegantodevelopmodelsfor speleogenesisintheGuadalupeMountains,theyrealized thatthemodelsneededtotakeintoaccountthemorphologyandlayoutofthecaveshadtoexplainthelackof relationshipbetweencaveandsurfacefeatures,andneeded toaccountfortheoccurrenceofmassivegypsumdeposits andotherunusualmineralogy(Smith,1978). Queen(1973)andPalmeretal.,(1977)suggestedthat thegypsumdepositsmightberelatedtoaprocessof speleogenesisratherthanbeingtheresultofvadose secondarymineralization.Accordingtotheirspeculations, theoriginofthegypsumdepositscouldresultfrom replacementofcarbonaterocksbygypsumasaresultof freshmeteoricwatermixingwithgypsum-saturatedbrine alreadyintherock.Palmerprefacedthehypothesisby expressingcautioninacceptingitwithoutsubstantialfield evidence(Smith,1978). StephenEgemeiersuggestedthatCarlsbadCavernmay havebeendissolvedbysulfuricacid(Egemeier,1971). Othergeologistsbegantoseeevidencefromtheirfield workandobservations,ofthepossibilityofasulfuricacid originofcavesintheGuadalupeMountains(Davis,1973; Jagnow,1978;Hill1981). In1986,animportantcaveexplorationbreakthroughin LechuguillaCaveprovidedauniqueopportunitytotest andexpandtheideasofasulfuricacidspeleogenesismodel andultimatelyshiftedthefocusofresearchfromCarlsbad CaverntoLechuguillaCave(Jagnowetal.,2000). E XPLORATIONOF L ECHUGUILLA C AVE:A B IGGER P IECE OFTHE P UZZLE Fordecades,caveexplorershadbeenintriguedby asmallguanocavelocatedaboveWalnutCanyonin CarlsbadCavernsNationalPark.Thecavehadavertical entrance,wasnotveryextensive,anddidnotcontainany speleothemsofinterest.Itwasminedforguanoforashort time,butthenabandoned(Frank,1988).However,agale ofairissuedfromabreakdownpileatthebaseofthe entranceshaft.Onsomedays,itsoundedlikeanundergroundfreighttrainandwispsofdustysedimentwere blownupthe27mlongentranceshaft.Thesourceofthat windenticedcaveexplorerstoattemptdiggingthe sedimentencrustedbreakdownpileatthebaseofthe entranceshaft.Severaldiggingprojectswereconductedby differentcavinggroupsbeginninginthe1950Â’s.Agroupof Coloradocaversre-energizedthediggingeffortin1984 andinMayof1986theyluckedoutwhenasectionof breakdowncollapsedintogoingcavepassage(Bridges, 1988).ThebreakthroughinLechuguillaCavewould becomeoneofthemostsignificantdiscoveriesofthe twentiethcenturybothintermsofcaveexplorationand cavescience(TurinandPlummer,2000). Thegale-forcewindsissuingfromthebreakdownpilein theentranceofLechuguillaCavepracticallyguaranteed theexistenceofavastcavesystem.Andcaveexplorers knewthatthegeologyoftheareaprovidedthepotential forsignificantdepth.TheLechuguillaCaveProject(later replacedbyLechuguillaExplorationandResearchNetworkformedin1991)wasformedin1987toprovide structuretothesystematicexplorationeffort.Survey standardswereestablishedthatweresimilartothose utilizedbyCRF.However,amuchstrongeremphasiswas placedonverticalcontrolandallsurveyswererequiredto includerunningverticalprofiles(KambesisandBridges, 1988). CaveexplorersfromallovertheUSandtheworld participatedintheexplorationandsurveyofLechuguilla Cave.Explorationandmappingmovedatbreakneckspeed withthediscoveryof33kmofnewpassageswithinthefirst year(Reamesetal.,1999).Inordertokeepupwiththe largevolumeofsurveydatageneratedbytheexploration effort,computerprogramswerespecificallywrittento processandplotthesurveydata(Petrie,1988).Project memberstookturnsinputtingsurveydatatotheeverexpandingdatabasethatgrewbyleapsandboundsafter eachtrip.Thismodeofexplorationandsurveyassuredthat thenextteamwhocontinuedtheexplorationwouldhave aplotofpassagesthathadalreadybeenmappedandaview oftherelationshipbetweenareasofongoingexploration. P ATRICIA K AMBESIS JournalofCaveandKarstStudies, April2007 N 53

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Thistag-teamstyleofexplorationensuredthatsurveydata wascontinuouslybeingproducedfortheentiredurationof eachexpedition(Bridges,1988).Explorationteamsconsultedthesurveynotes,lineplots,andtripreports,and usedtheinformationtoplantheirnextpush. Photographywasaregularpartofthedocumentation effort.Asexplorationprogressed,sodidphoto-documentationofincrediblenewareas,spectacularspeleothems, andhighlyunusualsedimentsandmineralogy.Eachsurvey teamwasrequiredtowriteadetailedaccountoftheir findings,includingroutestothesurveyarea,descriptions ofunusualcavefeatures,observationsaboutairmovement,locationofwater,andasummarylistofunexplored leads.Attheendofeachexpedition,adetailedsummary report,withsurveystatistics,lineplots,andtripreports wassubmittedtothecavespecialistatCarlsbadCaverns NationalPark.Photographswereprovidedastheybecame available. Witheachexpedition,thedepthofthecavesurvey plummeteduntilitwasstoppedinthelowerpartofawaterfilledfissurewherethecaveattainedaverticalextentof 489m(Davis,1990).Explorersspeculatedthatthiswasthe watertable,whichwasanunprecedentedfindinanycave oftheGuadalupeMountains(Kambesis,1991).Explorationreportsdescribedtheexistenceofsuperlativespeleothems,someneverbeforedocumented(Davis,1990). Fluffypilesofsediment,initiallyidentifiedascorrosion residues,wereobservedtooccurinhuesoftan,red,yellow, black,andbrown.Massivegypsumglaciers(Fig.7)and moundsofsulfurcoveredthefloorsofsomepassages. ThoughthecavewassituatedundertheChihuahuan Desert,eachexpeditionrevealedtheexistenceofmore poolsandlakesthroughouttheverticalextentofthecave. FlowingwaterwasevenobservedintheFarEastsectionof thecave(Kambesis,1991).By1990,theexplorersof LechuguillaCavehaddiscoveredandmappedover83km ofpassages.In1998thecavelengthhadreached166km withaverticalextentof489m. O NTHE H EELS ofE XPLORATION Theavailabilityoflineplotsandpreliminarymaps, elevationdata,detailedreports,andspectacularphotographsfromtheexplorationeffortinstigatedfieldworkfor caveresearchtofollowontheheelsofexploration. WhentheprofilemapofLechuguillaCavewas correlatedtothestratigraphicsectionoftheGuadalupe Mountains,itrevealedthatthecavespannedmostofthe Permian-agedreefcomplexfromthebackreefYates formation,throughthemassiveCapitanFormationand downtotheGoatsSeep(Jagnow,1989).Theprofile illustratedthatthecavecutthroughtheheartofthefossil reef(Jagnow,1989;DuChene,2000).Fromthestudyofcave mapscameinsightsintothecharacteristicmorphologiesand patternsofcavesformedbysulfuricacid(Palmer,1991). ResearchersconductedageologicsurveyofLechuguilla CaveandothercavesintheGuadalupeMountainsin ordertorelategeomorphicfeaturesofthecavestopast hydrologic-andgeochemical-dissolutionregimes(Palmer andPalmer,2000).Thediscoveryofalunite,natroalunite, anddickiteinLechuguillaCave(PalmerandPalmer, 1992),andthesubsequentfindingofthesamemineralsplus asuiteofuranium-vanadiummineralsandhydrobasaluminteinotherGuadalupeMountaincaves(Polyakand Mosch,1995;PolyakandProvencio,1998)establishedthat theseminerals,alongwithsulfurandgypsum,andthe occurrenceofgypsumdeposits,werecharacteristicofthe sulfuricacidmodeofcavedissolution.Inaddition,the sulfuricacidmodelofspeleogenesisseemedtoaccountfor thecavepatternsandmorphologies,andexplainedthelack ofrelationshipbetweensurfaceandcavefeaturesin Figure7.MassivegypsuminLechuguillaCave. T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 54 N JournalofCaveandKarstStudies, April2007

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Figure8.Underwaterhelictites,LechuguillaCave. Figure9.WebulitesinLechuguillaCave. P ATRICIA K AMBESIS JournalofCaveandKarstStudies, April2007 N 55

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GuadalupeMountaincaves.Themodelalsoestablished acharacteristicsetofmineralsthatwereconsidered definitiveindicatorsofsulfuricaciddissolution.And finally,from 40 Ar/ 39 Ardatesonalunite,absolutedates weredeterminedforfourelevationlevelsthatwere correlatedacrossaseriesofGuadalupeMountaincaves (PolyakandProvencio,1998). Watersamplinginthenumerouspoolsscattered throughouttheverticalextentofLechuguillaCave commencedshortlyafterthesefeatureswerefirstreported. Wateranalysesindicatedthatthepoolsrepresented isolatedsamplesofvadose-zonewaterinfiltratingalong separateandindependentflowpaths(TurinandPlummer, 2000).Poolcomposition,whichisafunctionofprecipitationchemistry,bedrock,andtheoccurrenceof gypsumdeposits,couldalsoaffectthedevelopmentof somespeleothemssuchasunderwaterhelictites(Fig.8). Thegeochemistryofwaterfromthedeeppointsinthecave confirmedthatthewatertablehadindeedbeenreached (TurinandPlummer,2000). Analysesofpiecesofsomeofthemoreunusual speleothemsreportedonandcollectedbycaveexplorers (withpermissionofCarlsbadCavernsNationalPark) revealedatotallyunexpectedresult.Featuressuchas webulitesandu-loops(Fig.9)appearedtobecalcified filamentousmicroorganisms(Cunninghametal.,1995). Poolfingers(Fig.10)providedevidenceofpossible bacterial/mineralinteractionintheirformation(Northup etal.,1997).Ironoxidespeleothems(rusticles)showedthe presenceoforganicfilamentsintheircores(Davisetal., 1990).Corrosionresidues,whicharecommonthroughout LechuguillaCaveandalsooccurinmanyothercavesinthe GuadalupeMountains,arecomposedofironoxideand manganesematerialscontainingbacterialandfungal communities(Cunningham,1991;Cunninghametal., 1995).Northupetal.(1997)proposedthatmicrobescould dissolvecavefeaturesviaacidicmetabolicbyproducts. Recentstudiesontheecologicinteractionsofbacteria thatexistinLechuguillaCavehaveshownthattheenzymes theyproducemaybebeneficialtothetreatmentand potentialcureforsomehumandiseases(Northup etal.,1997).ResearchersfromNASA,whohavebeen lookingforextremeenvironmentsontheearththat maybeanalogoustolifeonotherplanets,havebeen studyingthemicroorganismsinLechuguillaCave(Boston, 2000). Thoughexplorationandsurveyhavebeenongoingin LechuguillaCaveforthepasttwentyyears,thefullextent Figure10.PoolfingersinLechuguillaCave. T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 56 N JournalofCaveandKarstStudies, April2007

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ofthecavesystemhasnotyetbeenrealized.Despitegreat progressindefiningtheprocessesthatformedthecave,the boundaryconditionsthatresultedinitsdevelopmentare notyetfullyunderstood.Asexplorersventureinto unknownterritoriesintheirpursuitofmorecavepassages, theywilluncovermoreevidencethatwillresultinthe continuedevolutionoftheoryonGuadalupeMountain cavedevelopment.Cavescientistswillcontinuetopursue thefruitsofexplorationforanalysisandstudy. C ONCLUSION Systematiccaveexplorationinvolvesnotonlythe physicalpursuitanddiscoveryofcavesandcavesystems, butalsoincludesthesystematicdocumentationofthose discoveries.Thefielddocumentationthatdefinessystematiccaveexplorationincludescaveandsurfacesurveys, detailednotesandobservations,caveandkarstfeature inventories,andphoto-documentation.Thedataare synthesizedintocavemaps,narrativedescriptions,and reportsthatcanserveasasetofexplorationtoolsfor findingmorepassagesandcavesandalsoserveasthe baselineforalltypesofcave-relatedresearch.Cave explorationisafundamentalelementofcaveresearch andcave-relatedscience. A CKNOWLEDGEMENTS TheauthorwouldliketothankDaveBunnellforthe photographsthatappearinFigures7through10. R EFERENCES Bennington,F.,1959,Preliminaryidentificationofcrystallinephases in atransparentstalactite:Science,v.120,p.1227. Borden,J.D.,andBrucker,R.W.,2000,BeyondMammothCave, SouthernIllinoisUniversityPress,CarbondaleandEdwardsville, Illinois. 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White,W.B.,1988,GeomorphologyandHydrologyofKarstTerrains, OxfordUniversityPress,NewYork,464p. White,W.B.,Watson,R.A.,Pohl,E.R.,andBrucker,R.,1970,The CentralKentuckyKarst:TheGeographicalReview,v.60,p.88–114. Zopf,R.B.,1982,CartographyandexplorationintheMammothCave Region, in CaveResearchFoundationAnnualReport1982,Palmer, M.V.,ed.,34p. 1 Editor’sNote:Quinlan(1989)hasneverbeenpublishedalthoughitwasrel eased selectivelyindraftform. T HEIMPORTANCEOFCAVEEXPLORATIONTOSCIENTIFICRESEARCH 58 N JournalofCaveandKarstStudies, April2007



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DEVELOPMENTOFTHECARBONATEISLAND KARSTMODEL J OAN R.M YLROIEAND J OHN E.M YLROIE DepartmentofGeosciences,MississippiStateUniversity,MississippiS tate,MS39762USA,mylroie@geosci.msstate.edu Abstract: Thedevelopmentofacomprehensiveconceptualmodelforcarbonateisland karstbeganintheBahamasinthe1970s.Theuse,initially,ofcaveandkars tmodels createdfortheinteriorofcontinents,onrockshundredsofmillionsofye arsold,wasnot successful.Modelsdevelopedinthe1980sfortheBahamas,thatrecognize dthe youthfulnessofthecarbonaterock,theimportanceoffresh-watermixing withseawater, andthecomplicationsintroducedbyglacioeustaticsea-levelchangepro ducedthefirst viablemodel,theflankmargincavemodel.Thismodelexplainsthelargest cavesin carbonateislandsasbeingtheresultofmixingzonedissolutioninthedis talmarginofthe fresh-waterlens,undertheflankoftheenclosinglandmass.Theflankmar ginmodel, takenfromtheBahamastoIsladeMona,PuertoRico,intheearly1990s,prov idedthe firstviableexplanationfortheverylargecavesthere.Fieldworkintheg eologicallycomplexMarianaIslandsinthelate1990sresultedinthedevelopmentofth eCarbonate IslandKarstModel,orCIKM,whichintegratedthevariouscomponentscont rolling caveandkarstdevelopmentoncarbonateislands.Thesecomponentsare:1) Mixingof freshandsaltwatertocreatedissolutionalaggressivity;2)Movementof thefresh-water lens,andhencethemixingenvironments,by100 masaresultofQuaternary glacioeustasy;3)Theoverprintingofglacioeustaticchangesbylocalte ctonicmovements, wherepresent;4)Theuniquebehaviorofeogenetic(diageneticallyimmat ure)carbonate rocks;and5)Theclassificationofcarbonateislandsintosimple,carbon atecover, composite,andcomplexcategories.Currentresearchinvolvestheuseoff lankmargin cavesaspredictorsofpastandpresentfresh-waterlensconfiguration,t heanalysisof flankmargincavemorphologyasameasureoftheprocessesthatcreatethem ,andthe CIKMasanindicatorofpaleokarstdistribution. I NTRODUCTION ThispaperisdesignedtopresenttotheNational SpeleologicalSocietyreaderanunderstandingofthe uniqueandunusualtypesofcavesandkarstthatformin tropicalcarbonateislands.Itwillalsosummarizehow,for thelast35years,wehavepursuedislandcavesaroundthe world,andattemptedtofigureoutwhytheyarethere,and howtheyformed.Giventhatithasbeen40yearssincethe JCKSpublishedananniversaryissuesuchasthisone,the timeframeisaboutrighttopresentareviewarticlethat takesthereaderthroughthedevelopmentofideasabout cavesandkarstonislands,andwhatweunderstandtoday. TheresearchbeganintheBahamas,whichaswillbeseen, wasfortuitousastheyrepresentsomeofthesimplest carbonateislandsthatcanbefoundanywhere.(Weusethe termcarbonateisland,insteadoflimestoneisland,totake notethattherockswearedealingwithcontainthree carbonateminerals:calciteandaragonitewhichare differentforms(orpolymorphs)ofcalciumcarbonate, CaCO 3 ;anddolomite,acalcium-magnesiumcarbonate, CaMg(CO 3 ) 2 .) Weexploredandmapped(crudely)ourfirstislandcave, Hunt’sCaveonNewProvidenceIsland,Bahamas,while onatouristvisitin1971.AsnortheasternU.S.cavers,we foundtheheatofthecavesandtheever-presentbiota, especiallycockroaches,tobequiteashock(wecameback in1990andmappeditproperly).In1974weaccompanied ArtandPegPalmer,ofOneontaStateUniversity,to BermudaattheinvitationofMikeQueen(thenatthe BermudaBiologicalStation),tomapcavesandtoexamine theunusualkarstprocessesinoperation.Asitturnedout, Bermudacavesaresomewhatunique,evenamongisland caves,andtheteamcouldnotagreeonhowthecaveswere forming.Beginningin1976,webeganmakingannualfield tripswithJamesCarew,nowattheCollegeofCharleston, andourstudentstotheBahamas,firsttoNorthAndros Islandin1976,thentoSanSalvadorIslandfrom1977to thepresent.Thehookwasset,andwehavebeencaptivated andintriguedbyislandcaveseversince.Theresearch beganasatwostepsforward,onestepbackward experienceasourignoranceofislandkarstprocesses wasslowlyreplacedbyagrowingappreciationforthe specializedenvironmentwewereobserving. E ARLY R ESEARCH Foroveradecadeweappliedthemodelsandtheoriesof cavedevelopmentestablishedbyresearchoncontinental cavestothecavesoftheBahamas,andwehadlittleluckin J.R.MylroieandJ.E.Mylroie–Developmentofthecarbonateislandkarstm odel. JournalofCaveandKarstStudies, v.69,no.1,p.59–75. JournalofCaveandKarstStudies, April2007 N 59

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understandingwhatwasgoingon.In1991,Palmer(1991) describedtwomajorclassificationsofcaves:epigeniccaves thatarecoupledtothesurfacehydrology,andcommonly havesinkingstreams,cavesasturbulentflowconduits,and springs.Thesecondclassificationwashypogenic,meaning thatthecaveformedbydissolutioninthesubsurfaceas aresultofmixingofwatersofdifferentchemistry;these caveslacksinkingstreaminputsorconduitscarrying turbulentflowtodiscretespringsbecausetheyare uncoupledfromthesurfacehydrology.OurinitialinvestigationstreatedthecavesoftheBahamasasepigenicin type,althoughthetermhadn’tbeenpublishedyet.Wethen begantoconsiderwhatwasuniqueabouttheislandsetting, andstartedtobackawayfromcontinentaltheories.We recognizedthatsealevelcontrolledthepositionofthe fresh-waterlensinislands,butwestillwereconceptually tiedtotheideaofcontinentalstreamcaves(Carewetal., 1982;Mylroie,1983;MylroieandCarew,1988a).Someof theseideas,inhindsight,arequiteamusing.Wealso generatedsomepapers,basedonaminoacidracemization (AAR)datingofrocksintheBahamas,thatattemptedto portraycavedevelopmentasoccurringinveryshort timeperiods(MylroieandCarew,1986a,1986b,1987).It turnsoutthatwewerecorrectabouttherapidcave development,wejusthadthewrongtimewindowinthe QuaternarybecauseofthebaddatesfromtheAARwork (seeCarewandMylroie,1997,foradiscussionoftheAAR problem). Palmeretal.(1977),drawingonthegeochemicalwork ofBo ¨gli(1964, in Bo ¨gli1980)andPlummer(1975),had advancedatheorythatmixingofmarineandfreshwaters undercarbonateislandscouldcreateanenvironmentof enhanceddissolution,andsoexplaincavedevelopmenton Bermuda.Inthelate1970sandearlytomid1980s,Bill Backandhisco-workerspublishedaseriesofpapers(Back etal.,1986andreferencestherein)thatusedthemixingof seawaterandfreshwaterundercarbonatecoastsas awayofexplainingporosityandpermeabilitydevelopment,dolomitization,andcoastlineevolutioninthe YucatanPeninsula.Theessentialgeochemistryispresented inFigure1(Dreybrodt,2000).Becausethesaturation curveforCaCO 3 isconvexupward,waterssaturatedattwo differentinitialconditions,asatAandBinthefigure, whenmixedcreateawaterbody,C,thatisbeneaththe saturationcurve,andsoisunsaturated.Thiswaterbody nowhasreneweddissolutionalpotentialandwilldissolve CaCO 3 untilitagainreachesthesaturationcurveatD.The amountofCa 2 putinsolutionisshownbythestepfrom C toD .Seawater,andthefresh-waterlensincarbonate islands,areusuallysaturatedwithrespecttoCaCO 3 ,but theydidsoatdifferentinitialconditions.Thereforetheir mixingproducesanunsaturatedsolution,anddissolution willcreatecaves.Itwasalsorecognizedthatdescending vadosewater,uponreachingthetopofthewatertableat thefresh-waterlens,couldalsomixandcreateasiteof reneweddissolutionalaggressivity. Examinationofhowtheseideascouldaffectisland karstwerepresentedinapaperpublishedin1988(Mylroie andCarew,1988b),thatfocusedonthemigrationofthe fresh-waterlensassealevelchangedduringtheQuaternary (Fig.2).Animportantmisconceptionaroseoutofthis figure.Thefresh-waterlenswasdrawnascommonlyfound intextbooksandresearchpapers,thatis,withvertical exaggerationthatshowsthehaloclinedescendingsteeply downwards.However,a1km-wideislandcommonlyhas afresh-waterlenslessthan10mthick,sotheaspectratiois 10m/1000m,or1partin100.Thelensmargindoesnot dipsteeply.Theideaofasteeplydescendinglensmargin Figure1.EquilibriumcurveforCaCO 3 ,afterDreybrodt (2000).Seetextforexplanation. Figure2.Figure6ofMylroieandCarew(1988b).This figureshowswatertablecavesasmixingchambersandnot trueconduits.Thehaloclinecave’sapparentsteepdipis aresultofverticalexaggeration,andisshownasaconduit dischargingdirectlytothesea.Sealevelcontrolsare alsoevident. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 60 N JournalofCaveandKarstStudies, April2007

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wasreinforcedbythereportofcavediversRobPalmerand DennisWilliams(PalmerandWilliams,1984),who reportedthattheywereabletofollowthehalocline downwardsincavepassagesatarelativelysteepangle. Wenowrecognizethattheexistenceofthecavepassage distortedtheflowpatterninthelens,causingthelensto utilizethecavepassageasashort-cuttothesea.Assea levelhasmigratednumeroustimesduringtheQuaternary, manydissolutionalenvironmentshavebeenoverprinted, creatingacomplexofdissolutionvoidsandcollapses, formingcaveswithasignificantverticalcomponent.Itis thesecavesthatappeartobedistortingthemodernfreshwaterlens,asopposedtothemodernlenscreatingthe entirecavecomplex(thehaloclinecaveofFig.2). AfteradecadeoffieldworkintheBahamas,webegan toseeapatterninthelargestdrycavesfoundontheislands (forareviewofBahamiangeology,seeCarewandMylroie, 1995a;1997).Thelargecavescommonlywereentered whereahillsidehadbeenbreachedbyerosionorhad collapsed.Thecaveswerefoundatelevationsof1to7m, whichwasinagreementwiththepositionofatleastone earliersealevelduringtheQuaternary,thelastinterglacial associatedwithOxygenIsotopeSubstage5e(OIS5e), whichlastedfrom131to119ka(Chenetal.,1991).This sealevelreached6mhigherthanatpresent,asglacialice meltedbackabitmorethanithastoday.Giventhatthe Bahamasaretectonicallystable,onlyaglacioeustaticsealevelhighstandcouldhaveelevatedthefresh-waterlens abovemodernsealevel,andsoplacedthefresh-waterlens at,andslightlyabove,thatelevation.Cavemorphology waspredictableandconsistent:largechambersnearthe edgeofthehillcontainingthecave,numerousramifying passagesnearthebackofthecave,andmanycross-links andconnections.Cavechamberswerewiderthantheywere high,withcurvilinearandcuspatemargins.Remnant bedrockpillarswerecommon.Passagesheadinginland commonlyendedinblankbedrockwalls.Asimportantas whatthecavescontainedwaswhattheydidnotcontain:no turbulentflowmarkingssuchaswallscallops,nostreamlaidsediments,nosinkingstreamorspringentrances.To explainthesecaves,wedevelopedthe flankmargincave modeltointerpretthesize,shape,positionandconfigurationofthecaves(MylroieandCarew,1990).Thenameis derivedfromtheinterpretationthatthecavesdevelopin thedistal margin ofthefresh-waterlens,justunderthe flank oftheenclosinglandmass(Fig.3).Atthislocation, themixingenvironmentofthevadoseinputtothewater tableissuperimposedonthemixingenvironmentofthe fresh-waterlenswithunderlyingmarinewater,increasing dissolutionbeyondwhateitherenvironmentcoulddo alone.Additionally,thelenscrosssectiondecreasesatthe lensmargin,soflowvelocitiesincrease,transporting reactantsin,andproductsout,fasterthanelsewherein thelens(RaeisiandMylroie,1995).Finally,boththetopof thelens,andthehalocline,aredensityinterfacesthatcan traporganicmaterial.Oxidationoftheorganicscreates CO 2 thatcandrivemoredissolution;excessorganicscan createanoxicconditionsanddriveH 2 S-mediateddissolution.TheH 2 Smodelappearssupportedby 34 Sanalysisof intergranulargypsumfromsomeflankmargincaveson SanSalvador,whichshoweddepletionvaluesassociated withbiomediationofsulfurinanoxiczones(Bottrelletal., 1993). Cavedevelopmentbymixingdissolutioninthemargin ofthelens,undertheflankofthelandmass,explainedthe featuresfoundinthecaves(Fig.4).Thecaveswerenot conduits,butmixingchambers,sothecavesshowedno evidenceofturbulentflow.Thegreatestamountofmixing tookplacenearthehillside,which,duringanelevatedsea level,wastheshoreline.Thisactionplacedthelargest chambersnearthehillside.Theramifyingandcross-linked passagesrepresentedmigrationofthedissolutionalfront inland.Thelargewidthtoheightratiomimickedtheshape ofthedistalmarginofthelens.Thewallmorphology displayeddissolutionbymixedwaters,andmimicked wallandpassagemorphologiesfoundinothermixedwaterenvironments,suchasthehypogeniccavesofthe GuadalupeMountainsofNewMexico(Palmer,1991). Onlyasmallamountofhillsideerosionwasnecessaryto breachintothecaves,whichformedinitiallywithout human-accessibleentrances.Itseemedthatasignificant puzzleregardingislandcavedevelopmenthadbeen explained. Flankmargincaveswerethelargest,butnottheonly, typeofcavefoundintheBahamas.Twoothertypesofdry caveswereabundant.Pitcavesarefoundalloverthe Bahamas,sometimesinverydenseclusters,andoccasionallyatthetopofhills.Asthenamesuggests,theseare verticalshaftsthatdescendtypically5to10m(Fig.5). Theyrarelyintersectflankmargincaves.Theirwallsshow classicverticalgroovesformedbysupercriticallaminar flowofdescendingvadosewater.Duringmajorrainevents, theycanbeobservedtoefficientlycollectwaterfromthe epikarstandconductitdownwardsasvadosefast-flow routes.Theirhighdensityinplaceswasinitiallythought, basedonwaterbudgetconsiderations,toindicatemuch higherrainfallconditionsatapasttime.Thehighpitcave densityisnowunderstoodtoreflectcompetitionandpiracy amongpitcaves,suchthatsomelosetheirrechargeto upstreamcompetitors(Harrisetal.,1995).Thesecavescan becomplexasaresultofthiscompetition,which commonlyleadstointersectionofpitcavesbyoneanother. Pitcavesformindependentlyofsealevelandfresh-water lensposition,andcanforminanyexposedcarbonaterock onanisland. Theremainingmajordrycavetypeisthebananahole. Bananaholesarecirculartoovalchambers5to10min diameter,and1to3mhigh,withphreaticmorphologies butlackingthesizeandpassageramificationsfoundin flankmargincaves(Fig.6).Theyarelocatedinpositions of0to7mabovesealevel,butlaterallywellawayfrom wherethelensmarginwouldhavebeenwithsealevelat J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 61

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thatelevation.Theyareenteredwheretheirceilingshave collapsed,orrarelywhereapitcavehasintersectedthem. Theycanbefoundindenseconcentrations,upto3000per km 2 (Harrisetal.,1995).Occasionally,acollapsedbanana holehasaconnectionwithanadjacent,uncollapsed bananahole.Theirnameisderivedfromtheirusetogrow specialtycrops,suchasbananas.Thecollapsescommonly collectsoil,vegetativedebris,andwater,andsoprovidean excellentlocationforcropgrowth.Bananaholeswere initiallythoughttobevadosestructures,formedby preferentialdissolutioninlowspotsonthegroundsurface (SmartandWhitaker,1989).Theselowspotswouldcollect extrawaterandorganicdebris,andgenerateCO 2 todrive dissolutionatlevelsabovewhatcouldbesupportedby simplemeteoricwateronadjacent,higherareas.The presenceofwallmorphologiesofaphreaticnature,andthe discoverythatchamberswithintactroofsexisted,required thatanotherexplanationbeconsidered.Downwardworkingvadoseprocessescouldnotbeinvokedforroofed chambersshowingphreaticmorphology.Dissolutionatthe topofthefresh-waterlens,bymixingofthelenswaterwith descendingvadosewater,appearstobethemechanism (Harrisetal.,1995).Thedominantoccurrenceofbanana holeshasbeenintheBahamas,whichcanbeexplained byconsideringthereliefofthoseislands.Muchofthe Bahamasarealowlandplain6to8mabovesealevel.San Salvador,forexample,is49%suchtopography(Wilsonet al.,1995).Duringthelastinterglacial,thefresh-waterlens wouldhavebeenveryclosetothelandsurface,suchthat thephreaticdissolutionalvoidsformedbyvadosewater/ fresh-waterlensmixingwouldhavehadverythinroofs,in theorderof0.5to2mthick.Thesevoidswouldbeprone toexpressionbycollapse.Oncedrainedbysea-levelfall andopentothesurface,theymayhaveenlargedbythe vadoseorganic-matmechanismenvisagedbySmartand Whitaker(1989).Thelackofbananaholereportsfrom carbonateislandsotherthantheBahamasmayreflectthe greaterreliefofthoseislands,suchthatbananaholevoids areroofedbytensofmetersofrock,anddonotexpressby collapse.Theoccasionallowandwidephreaticchambers foundindeepquarriesandhighroadcutsintheinteriorof islandssuchasGuammayrepresentbananaholes. InadditiontothedrycavesoftheBahamas,thereare manycavesthatareunderwaterandareaccessibleonlyby cavedivers.Themostspectacularofthesearethefamous blueholes,whichcanrangefromlittlemorethanponds,to sensationaldeepshaftsandkilometers-longcavesystems (Fig.7).Unlikeflankmargincavesandbananaholes, whichhadtobegeneratedintherelativelyshorttimethat sealevelhasbeenabovemodernlevels,blueholesreflect theaccumulatedspeleogenesisofmanysea-leveloscillations.Duringsea-levellowstands,vadosespeleothemssuch asstalagmitesandflowstonegrewinwhatwereair-filled shaftsandcaves.TheU/Thdatesoftheseformationsrange from15kabacktothelimitoftheU/Thtechniqueat 350ka(CarewandMylroie,1995b).Thefresh-waterlens anditsmixingzoneshavepassedupanddownthesection ofrockcontainingtheblueholesmanytimesduringthe Figure3.Figure22C&DofMylroie,1988(reprintedinMylroieandCarew,19 90).Firstdisplayoftheflankmarginmodel, showingsuperpositionofthemixingzonesatthetopandbottomofthefresh -waterlens. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 62 N JournalofCaveandKarstStudies, April2007

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Quaternary.Theamountofover-printingbyfresh-,mixedandsalt-waterenvironments,vadoseconditions,and collapseisimmense.Becauseoftheextensiveuseofblue holesbyrecreationaldivers,inthelate1980stherewas confusionaboutwhatablueholewasandhowtheyshould bedefined.AfterconsultingwithBahamianbluehole explorerRobPalmer,cavescientistPeteSmart,and BahamasgeographerNeilSealey,thefollowingdefinition forblueholeswasproposed(Mylroieetal.,1995a,p.225): ‘‘subsurfacevoidsthataredevelopedincarbonatebanks andislands;areopentotheearth’ssurface;containtidallyinfluencedwatersoffresh,marine,ormixedchemistry; extendbelowsealevelforamajorityoftheirdepth;and mayprovideaccesstosubmergedcavepassages.’’Asblue holescanbefoundinislandinteriors,orinlagoons, afurtherdescriptionwasadded:‘‘oceanholesopendirectly intothepresentmarineenvironmentandcontainmarine water,usuallywithtidalflow;inlandblueholesareisolated bypresenttopographyfrommarineconditions,andopen directlyontothelandsurfaceorintoanisolatedpondor lake,andcontaintidally-influencedwaterofavarietyof chemistriesfromfreshtomarine’’(Mylroieetal.,1995a,p. 225).Adifferentapproachtodefininganddescribingblue holescanbefoundinSchwabeandCarew(2006).Blue holesarepolygenetic,formingbydrowningofpitcaves, flankmargincavesandbananaholes;byprogradational collapse;bybankmarginfailure;andbymarinefloodingof paleoconduits(Fig.8).Blueholesareknowntoreactto tides,sometimeswithstrongcurrents,especiallyforocean holes.Smallerholes,foundoninlandwaterbodiesinthe Bahamas,havebeencalledlakedrains(Mylroieetal., 1995b).Theseareverycrypticfeaturesthathelpregulate Figure4.SaltPondCave,LongIsland,Bahamas.A)Mapofthecave,showingp assageshapeandconfiguration.B)Interior ofSaltPondCave,showingalong,tubularpassageendinginablankbedrock wall;thesiteofthedissolutionfrontwhensea levelfellattheendofthelastinterglacialsea-levelhighstand.C)Inte riorofSaltPondCave,demonstratingthegreatwidth relativetoheightinflankmargincaves,indicativeoftheirformationin thethindistalmarginofthefresh-waterlens. J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 63

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thesalinityofinlandwaterbodiesbysupplyingnormal salinityseawater,buttheirnatureandconfigurationis unknown. T HE S ECOND R ESEARCH P HASE Asnotedearlier,theBahamas,withtheiryouth, relativelysimplegeology,andlackoftectonicswereagood startingpointtofigureoutthecomplexitiesofcaveand karstdevelopmentincarbonateislands.Therecordofcave genesisforthedrycavesoftheBahamaswaswell understood,butquestionsremainedaboutwhathad happenedduringthesea-leveloscillationsoftheQuaternary.Thefirstopportunitytoexaminethisquestioncame intheearly1980s,whentheJohnsonSeaLinksubmarine wasmadeavailabletoresearchersonSanSalvadorIsland (CarewandMylroie,1987).Divesweremadeonthewallof thecarbonatebankonwhichSanSalvadorrests,toadepth of1000feet(305m;thedepthgaugeofthesubmarinewas calibratedinfeet,asareU.S.scubadiverdepthgauges,so thoseunitsarereportedfirsthere).Thepurposewasto locatepossiblehorizonsofcaveopeningsthatmightreflect pastsealevel,andhencefresh-waterlens,positions.Inthe 1980s,studiesfromblueholesshowedthattheydidnot exceed300feet( 90m)indepth.Thatdepthvaluewas takeninsomequartersasanindicationthatthemaximum sea-levellowstandwasat 300feet( 90m),andhence blueholesdidnotpenetrateanydeeper.Subsequently (Wilson,1994),DeanÂ’sBlueHoleonLongIsland, Bahamaswasfoundtobeanastounding660feet(201m) deep,indicatingthattherewasnogeologicfloortoblue holedepth.Drillingrecordsindicatedlargevoidsasdeepas 4,082m(MeyerhoffandHatten,1974).Thesubmarine diveswereanothermeansofcheckingtheblueholedata. Thedivesdidnotexaminethewalloftheislandatdepths above200feet( 60m),asmoderncoralovergrowth obscuredthebedrockwall.Caveswerefound13timesat adepthof343feet(105m),andtwicemoreat412feet (126m),butnowhereelsebetween200feetand1000feet depth(CarewandMylroie,1987).Thesedatasuggestasealevellowstandatthosedepths.The126mdepthagrees withtheoxygenisotopesea-levelcurve,whichindicatesthe maximumeustaticsea-levellowstandintheQuaternaryto beabout 125m.Theimplicationoftheseobservationsis thatduringQuaternarysea-leveloscillations,sealevelis rapidlychanging,eitherrisingorfallinginresponsetoice volumechangeonthecontinents,andthereforethefreshwaterlensisneverinonespotlongenoughtodevelop large,observableflankmargincaves.Onlywhensealevel hasreachedapeak(asduringthelastinterglacial,OIS5e), orreachedatrough,andsealevelmustthenreverseits positiontomakethenextoscillation,isthefresh-waterlens atonepositionlongenoughtomakeflankmargincaves. Thetroublewiththecavesfoundbythesubmarineisthat wedonÂ’tknowtheirages.WhiletheBahamasare tectonicallystable,theyareslowlysubsidingatarateof 1to2mper100ka(CarewandMylroie,1995b).Itcould bearguedthattheobservedcavescouldhaveformedat shallowerdepths,andhavesubsidedtotheirobserved location.Thecavescannotbetooold,however,asthe steepwallsoftheBahamaBankscommonlyfractureand fail(Daughertyetal.,1987;MullinsandHine,1989),and flankmargincaveswouldbepreferentiallyremoved.The twohorizons,at105mdepth,and125mdepth,may indicatethesea-levellowstandsassociatedwithOIS4 ( 50ka)andOIS2( 20ka),respectively. TheBermudacavesremainedaconcern,astheydidnot fitintothecavedevelopmentmodelcreatedforthe Bahamas,despitehavingverysimilargeology(Mylroieet al.,1995b).Similar,however,isnotidentical.Bermudahas twomaindifferencesfromtheBahamas.First,itisin awetterclimate,whichmeansitssurfacerockserodeby meteoricdissolutionfasterthanlandsurfacesdointhe drierBahamas(especiallySanSalvadorIsland,whichhas anegativewaterbudget).Second,Bermudasitson avolcanicpedestalthatismantledbythecarbonatesthat makeupBermudaÂ’slandsurface.IncontrasttheBahamas carbonatesextendcontinuouslytoadepthof5kmormore (MeyerhoffandHatten,1974).Flankmargincavesarerare inBermuda,knownonlyfromafewlocations.Thereason isclimatic.Inthehigherdenudationenvironmentof Bermuda,hillsideserodemorerapidlythaninthe Figure5.TripleShaftCave,apitcavecomplex,San SalvadorIsland,Bahamas.Meteoricwatercollectedinthe topfewmetersoftheepikarstpassesdownwardthroughthe vadosezone,formingpitcaves,whichcompeteandinteract toproducecomplexesasshownhere. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 64 N JournalofCaveandKarstStudies, April2007

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Bahamas,andtheflankmargincavesformedduringOIS 5esea-levelhighstand,125ka,arenowerodedaway (Mylroieetal.,1995b).Theirpositionofformationunder theflankoftheenclosinglandmassmadethemvulnerable tosurficialerosiveprocesses.Thefamouscavesof Bermudaareinsteadlargecollapsechambers,with extensivepilesofbreakdownthatcanbefollowedby scubadiverswellbelowsealevel.Rocksurfacesshowing phreaticdissolutionareextremelyrareinthesecaves.The mixingdissolutionmodelproposedforBermudabyPalmer etal.(1977),whichprovedtobethekeytounderstanding flankmargincavedevelopment,doesnotseemtobethe majorcave-formingfactoronBermuda.Thevolcanic pedestalofBermudaisnowalmostentirelybelowsealevel, suchthatafresh-waterlensexistsacrossthelengthand breadthoftheisland.However,duringglacialicemaxima intheQuaternary,sealevelwouldhavebeenupto125m lower,andthevolcanicpedestal,thoughmantledby carbonates,wouldhavebeenabovesealevel,partitioning thefresh-waterlens.Descendingvadosewaterwouldhave hitthecarbonate/volcaniccontact,andfollowedthe topographyofthatinterfacedownwardtothefresh-water lens.Suchaggregationofwaterastraditionalstream passageswouldhavecreatedlargechambers.Itisthe subsequentcollapseofthesechambers,andtheirprogradationupwardtotheelevationsseentoday,thathavecreated theuniquecavesofBermuda(Mylroie,1984;Mylroieet al.,1995b). In1992,attheinvitationofJoeTroesteroftheU.S. GeologicSurvey,researchbeganonIsladeMona,Puerto Rico,locatedintheMonaPassagehalfwaybetweenPuerto RicoandtheDominicanRepublic.Monaislocatedvery neartheboundarybetweentheNorthAmericanplateand theCaribbeanplate,andsoisinatectonicallyactivearea. Theislanditselfhasbeenupliftedsuchthatithasvertical cliffsonthreesides,whichareupto80mhigh(Fig.9). Theislandisentirelycarbonate,asalimestoneunit overlyingadolomite.OurinitialinterestinMonawas thatitlookedtoday,becauseoftectonicuplift,asSan Salvadorwouldhavelooked20,000yearsagoduringthe glacialicemaximum,whensealevelwasfarbelowtodayÂ’s position.Weknewfrompublishedreportsthatithadmany largecaves,andwethoughttheflankmarginmodelmight apply,asearlierreportshadobviouslybeenuncertainhow thecavesformed.JimQuinlan(Quinlan,1974)had describedthecavesasphantasmagorical,andreluctantly Figure6.A)MapofCliftonBananaHole,NewProvidenceIsland.Dissolutio natthetopofthefresh-waterlenscreatesvoids. B)Bananahole,unnamed,SanSalvadorIsland;theproximityofthelandsur facetothetopofthelenscreatesthinceilingsthat arepronetofailurebycollapse. J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 65

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placedthemintheseacavecategory,asherecognizedthat thecaveswerenottraditionalturbulent-flowconduits. Uponfieldexamination,wedeterminedthecaveswere clearlyflankmargincaves(Franketal.,1998),butatan immensescale.TheLirioCaveSystemeventuallymapped outat20km,andwrappedaroundthecurvingedgeofthe island(Fig.10).Thequestionthenbecamewhywerethe cavessolarge?Cavesofover1kmoflinearsurveyare knownintheBahamas,but20kmwasastounding.The answerlayintheageofthecaves.WorkingwithBruce Panuska,fromourGeosciencesDepartment(Panuskaet al.,1998),weestablished,basedonpaleomagneticreversal patternsincavesedimentsandspeleothems,thatthecaves wereatleast1.8millionyearsold.Thecaveshaddeveloped inthePliocene,beforetheonsetofthehighamplitude, shortwavelengthsea-leveloscillationsthatcharacterizethe Quaternary.Thereforesealevel,andfresh-waterlens position,hadbeenstableatagivenhorizonforamuch longertimethanhadbeenavailableintheyoungerrocksof theBahamas.Thislongertimeoflensstabilityhadallowed extremelylargeflankmargincavestodevelop.Upliftthen hadplacedthecavesfarabovetheinfluenceofQuaternary sea-levelchange,effectivelypreservingthecaves.The Bahamasdemonstratedthatsignificantflankmargincaves couldforminshorttimewindowsofapproximately 10,000years.Monashowedthatonceformed,suchcaves couldsurviveformorethanamillionyears.Flankmargin cavesarehigh-resolution,long-durationrepositoriesof speleologicalinformation. TheworkinBermudaandtheBahamaswassummarizedinMylroieetal.(1995b)andtheIsladeMonawork wassummarizedinMylroie&Carew(1995)andinFrank etal.(1998).Oneoftheresultsofthisearlyworkwasthe recognitionthatclosedcontourdepressions(commonly labeledinkarstareasassinkholes,uvalas,poljes,etc.)in theseyoungislandswereprimarilyconstructional.Thatis, thedepressionsweretheresultofdifferentialdepositionof thecarbonaterocktocreateclosedcontourdepressions thatdrainedbykarstprocessesandthereforeavoided becominglakesandponds.IntheBahamas,theswales betweenlargecarbonateeolianduneshadtheappearance ofverylargecloseddepressionscoveringthousandsof squaremeters.Inothercases,thecloseddepressionwas aformerlagoon,developedduringthe6msea-level highstandofthelastinterglacial(OIS5e),andnowdrained becausesealevelisnotashighasitwasat125ka.Most sinkholesinthe1to10mdiameterrangefoundinthe Bahamasarecavecollapses,themajorityaresultofbanana holeformationthatwasdiscussedearlier.TheBahamas differfromcontinentalkarstnotonlyinthecaves,butalso inthedepressions.Whereasmostdepressions,largeand small,incontinentsaretheresultofdissolutionalprocesses actingfromthesurfacedownward,intheBahamasthe largedepressionsareconstructionalandthesmallonesare collapsefeaturesfromdissolutionactingatavarietyof depths,inahypogenicmode. Figure7.DeansBlueHole,LongIsland,Bahamas.This blueholeisthedeepestintheBahamasat200m.Itsposition inalagoonmakesitanoceanhole,subjecttodirectmarine influence.Peopleonfarcliffforscale. Figure8.Fourwaysinwhichblueholescouldform.A)By floodingofsinksandpits.B)Byprogradationalcollapseof deepvoids.C)Bybankmarginfailure.D)Byfloodingof conduitcaves;noteheretheverticallensexaggeration mentionedinFigure2,stillcreatingtheincorrectimpression. AdaptedfromMylroieetal.,1995a. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 66 N JournalofCaveandKarstStudies, April2007

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T HE C URRENT R ESEARCH P HASE In1997,JohnMylroiewasaskedtopresentakeynote addresson‘‘LandUseandCarbonateIslandKarst’’atthe SixthMultidisciplinaryConferenceonSinkholesandthe EngineeringandEnvironmentalImpactsofKarst heldin Springfield,MissouriinAprilofthatyear.Thepaper publishedfromthatconference(MylroieandCarew,1997) madethefirstattempttoviewkarstdevelopmenton carbonateislandsasaresultofapredictablehierarchy (Fig.11).Thedifferencesbetweensometypesofisland caveandkarstdevelopmentcouldbeattributedto interactions(orthelackthereof)ofcarbonaterockswith non-carbonaterocksthatarecommonlyfoundonmany islands.Theannouncedpresentationoncarbonateisland karstinducedJohnJenson,oftheWaterandEnergy ResourceInstituteoftheWesternPacific(nowtheWater andEnvironmentalResearchInstitute,orWERI)atthe UniversityofGuam,toattendtheconferencetotalkabout hiskarstlanduseproblemsinGuam.Fromthatmeeting beganafruitfulcollaborationtoinvestigatethetectonically active,geologicallycomplexcarbonateislandsofthe MarianaArchipelago. WorkintheMarianaIslandsbeganonGuaminJuly of1998.AswithIsladeMona,thecarbonaterocksin theMarianas,whileCenozoic,wereolderthanthoseof theBahamas,andtectonicupliftplayedanimportant role.UnlikeIsladeMona,however,non-carbonate rocksoutcroppedonthesurface.Theseoutcropscreated allogenicrecharge,whichuponreachingthecontactwith carbonaterocks,formedsinkingstreams,streamcaves,and cavesprings;typicalepigeniccaves.Guamprovidedfield proofofthepredictedthirdislandcategoryfromFig.11C. Inthevicinityofnon-carbonateoutcrops,allogenicwater createdcavessimilartowhatcanbefoundoncontinents. Inthecarbonateoutcropatadistancefromthosenoncarbonaterocks,autogenicrechargecontrolledkarst development.Andinthecarbonatecoastalareas,classic flankmargincavedevelopmentdominated.IsladeMona, whiletectonicallyuplifted,didnotshowanyevidenceof upliftinthelast125ka(Franketal.,1998).Guamandthe otherMarianaislandsshowedevidenceofupliftthroughouttheQuaternaryanduptothepresentday(Dickenson, 1999).TheMarianaIslandspresentedanislandkarst environmentofmuchgreatercomplexitythanhadpreviouslybeenstudied.Thefieldwork,doneincollaboration withJohnJensonandhisstudents,resultedinthefirst comprehensiveinterpretationofcaveandkarstdevelopmentonGuam(Mylroieetal.,2001).TheM.Sc.thesis fromtheGuamworkbyDankoTaboros i(Taboros i,2000) instigatedaseriesofpublicationsaddressingkarren formation(Taboros ietal.,2004),cavedevelopmentand distribution(Taboros ietal.,2005),andspeleothem formation(Taboros i,2006)aspartofaPh.D.program atHokkaidoUniversity.TheMarianasworkcontinuedon toSaipan(Wexeletal.,2001),Aquijan(Staffordetal., 2004),Tinian(Staffordetal.,2005),andRota(Keeletal., 2006)islands,culminatinginareviewarticleofthecaves andkarstoftheMarianasArchipelago(Jensonetal., 2006).TheSaipanwork(Jensonetal.,2002)resultedin amodificationoftheislandcategoryhierarchytoinclude afourthcategory,thecomplexisland,torepresent situationsinwhichcomplexfaulting,andsyndeposition ofcarbonatesandvolcaniclasticsresultedinverycomplex compartmentalizationofthefresh-waterlens.Oneofthe unusualoutcomesofsuchcompartmentalizationisprotectionofwaterresourcesfromupconingandsaltwater intrusionduringaquiferpumping.Anotherunexpected Figure9.UpliftednorthsideofIsladeMona,PuertoRico.Cliffis70mhigh ,withflankmargincavesvisibleatthetop,along thelimestone/dolomitecontact. J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 67

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outcomewasthedevelopmentofconfinedaquifers, creatingphreaticlifttubestocarrywateroutoftheaquifer compartment,asinKalaberaCave,Saipan(Jensonetal., 2006). Theislandcategories(Fig.11)establishedinMylroie andCarew(1997),weremodifiedinMylroieetal.(2001)to reflectadvicefromH.LenVacherattheUniversityof SouthFlorida(MylroieandVacher,1999)thatnotall carbonateislandsshowingnon-carbonateoutcropshadthe carbonaterocksasarim,sothethirdcategorywas modifiedfromcarbonate-rimmedislandtocomposite island.Thataction,andtheadditionofthecomplexisland categoryresultedinthecreationofanew,fourpanelfigure toexpresstheislandtypehierarchy(Fig.12). Understandingofwaterflowdynamicsincarbonate islandshadbeenpioneeredbyH.LenVacher(e.g.,Vacher, 1988).Thekeytothatworkwastherecognitionthat carbonateaquifersareuniqueinhydrologyinthattheyare capableofextensiveself-modificationthroughdissolutionalanddepositionalprocessesinvolvingCaCO 3 .This self-modificationisextremelyimportantintheyoung carbonaterocksthatmakeupcarbonateislandstoday. Oneoftheunexpectedoutcomesofthisworkwasthatthe longerafresh-waterlenssatinagivensectionofyoung carbonaterock,themorepermeabletherockbecame.As showninFigure2,thefresh-waterlensexistsbecause aslope,orhead,ofwaterisneededtodrivethemeteoric watercollectedatthewatertabletotheislandperimeter. Thelesspermeabletherock,thesteeperthenecessaryslope (asananalogy,consideracaronaslope;iftheaxlesare rusted,ittakesasteepslopetomovethecar;iftheaxlesare greased,thecarmovesonagentlerslope).Asthefreshwaterlensfloatsina1to40ratiobasedonitsdensity differencewithseawater(1.000versus1.025gcm 3 ),the lensis40timesasthickbelowsealevelasitisabovesea levelasaresultofbuoyancy.Therefore,asthelens becomesmorepermeablebydissolution,itsslopebecomes less,itselevationabovesealevelbecomesless,soits thicknessbecomesless.IntheBahamas,thethickestfresh waterlensesarefoundintherecentHolocenesands(Wallis etal.,1991).Whilethesesandshaveveryhighprimary porosity,thatporosityisnotorganizedintohighpermeability,andthelensisrelativelythickaswaterflowisnot efficient.Intheadjacent,olderPleistocenerocks,which mayhaveseentwoormoresea-levelhighstandsand associatedfresh-waterlensevents,thepermeabilityis higherandthelensisthinner.Buildingonthesestudies, VacherandMylroie(2002,p.183)definedtheterm eogenetickarstas‘‘thelandsurfaceevolvingon,andthe poresystemdevelopingin,rocksundergoingeogenetic, meteoricdiagenesis.’’Thetermeogeneticwasderivedfrom ChoquetteandPray’s(1970,p.215)studiesofrockageand diagenesis;theydefined‘‘thetimeofearlyburialas eogenetic,thetimeofdeeperburialasmesogenetic,and thelatestageofassociatedwitherosionoflong-buried carbonatesastelogenetic.’’Mostkarstincontinental settingsistheresultofdissolutionalprocessesactingon telogeneticrocks,rocksthatarediageneticallymature, recystallized,andlacksignificantprimaryporosity.In eogenetickarst,cavesarecreateddirectlywithinthe eogeneticrocks,bypassingdiageneticmaturation,uplift, andtelogeneticdissolution(Fig.13). Theparametersthatcontrolledthedevelopmentofkarst onislandswereinitiallyoutlinedbyMylroieandVacher (1999)andcodifiedastheCarbonateIslandKarstModel,or CIKM,whichfirstappearedbythatnameaftertheinitial studyofGuam(MylroieandJenson,2000;Mylroieetal., 2001).TheCIKMhasbeentweakedandmodifiedoverthe years.TheprinciplesoftheCIKMinclude: 1.Mixingoffreshandsaltwaterattheboundariesofthe freshwaterlensresultsinalocalizedareaof preferentialporosityandpermeabilitydevelopment. Collectionoforganicsattheseboundariesmayalso Figure10.MapoftheLirioCaveComplex,IsladeMona, PuertoRico.Notethatthecaveismaze-like,withlarger chamberstowardsthecoast;thatthecavedoesnotpenetrate veryfarinlandbutdoeswraparoundtheislandcoastline. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 68 N JournalofCaveandKarstStudies, April2007

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enhancedissolution.Themaximumdissolutionoccurs atthelensmargin,wherethewatertableandhalocline mixingzonesaresuperimposed. 2.Glacioeustacyhasmovedsealevel,andthusthefresh waterlensposition,upanddownmorethan100m throughouttheQuaternary. 3.Localtectonicmovementcancauseoverprintingof dissolutionalanddiageneticfeaturesdevelopedduring differentglacioeustaticevents. 4.Thekarstiseogeneticinthatithasdevelopedonrocks thatareyoungandhaveneverbeenburiedbelowthe zoneofmeteoricdiagenesis. 5.Carbonateislandscanbedividedintofourcategories basedonbasement/sealevelrelationships(Figs.11 and12). A.SimpleCarbonateIsland—Onlycarbonaterocks arepresent(Fig.11A).Meteoriccatchmentis Figure11.Firstpresentationofakarstclassificationofcarbonateisla nds,fromMylroieandCarew(1997).TheBahamasfit the(A)Category,Bermuda(atsea-levellowstands)fitsthe(B)Category, andGuamfitsthe(C)Category. J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 69

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entirelyautogenicandflowwithinthefreshwater lensiscontrolledentirelybypropertiesofthe carbonaterock.TheBahamasareexamplesof simplecarbonateislands. B.Carbonate-CoverIsland—Onlycarbonaterocks areexposedatthesurfaceandthecatchmentis entirelyautogenic(Fig.11B).Non-carbonate rocksexistundercarbonaterocksandmay partitionandinfluenceflowwithinthelens, includingconduitflowatthecontact.Bermuda, atasea-levellowstand,isanexampleofacarbonate-coverisland. C.CompositeIsland—Bothcarbonateandnoncarbonaterocksareexposedatthesurface (Fig.12),allowingforallogenicandautogenic catchment.Thelensispartitionedandconduit cavesystemscandevelopatthecontactofthe carbonateandnon-carbonaterocks.Barbados andGuamareexamplesofcompositeislands. D.ComplexIsland—Carbonateandnon-carbonate rocksarecomplexlyinterrelatedbydepositional relationshipsand/orfaulting(Fig.12).Perching, isolation,andconfiningofthefresh-waterlensis possible.Saipanisanexample. VacherandMylroie(2002)alsodifferentiatedbetween islandkarst,andkarstonislands.Islandkarstdevelops undertheinfluenceoftheCIKM.Karstonislands developsinupliftedregionsofislandinteriors,andbehaves muchthesamewayaskarstoncontinentsatthesame latitude.TheflankmargincavesofIsladeMonaorthe Bahamasareexamplesofislandkarst.Thecockpitsof Jamaica,orthemogotesofPuertoRico,areexamplesof karstonislands,astheyareisolatedfromglacioeustasy andfreshwater/saltwatermixing.Theyaresimilartothe karstlandformsofBelize,atropicalbutcontinental setting. Thekarren(dissolutionalsculptureatthecentimeterto meterscale)ofcarbonateislandsdifferfromthosefoundin continentalinteriorsofthemidtohighlatitudes,where mostkarrenresearchhasbeendone.Thejagged,pittedand irregularkarrenofthecoastalenvironmentoftropical carbonateislandsiswellknown,andtheclassicstudyisby Folketal.(1973).Thatwork,andmanylaterworks(e.g., Viles,1988)ascribedtheuniquenatureofthisislandkarren tomarinespray,boringendolithicalgae,andgrazingby gastropods,amongotherreasons.Folketal.(1973)called it phytokarst ,basedonthelargedegreetowhichthe endolithicalgaehadpenetratedandpermeatedtherock surface.Taboros ietal.(2004)wereabletodemonstrate thatthekeyfactorwastheeogeneticnatureoftherock. Thelackofdiageneticmaturitymadeallweathering processes,organicandinorganic,responsivetothetexture, composition,porosity,andcementationoftheallochems (particles)thatmadeuptheyoungcarbonates.Taboros iet al.(2004)calledsuchkarstetchingeogenetickarren. Endolithicalgaewereabletocolonizesuchweakand porousrockinhighabundance,whichinitiatedtheentire organicaspectofkarrendevelopmentinthecoastal carbonatesoftropicalislands.Endolithicalgaedonot colonizedense,recrystallizedteleogeneticrockstoasimilar extent.OnsouthernGuam,intheinteriorawayfrom CIKMeffects,arelimestoneunitsranginginagefrom Figure12.Updatedkarstclassificationofcarbonateislands,changingFigure11Cfromcarbonate-rimmedislandto compositeisland,andaddinganewcategory,thecomplex island,bestrepresentedbySaipan. Figure13.Theevolutionofeogenetickarst.Slantingsolid linesarehydraulicconductivity,K,inm/day.Slanteddashed linesaretubedensity(numberoftubesperunitarea,orN/A), ameasureofthedegreeofenlargementoftheporestructure (withaconsequentdecreaseinporenumber).Eogenetickarst takesashortcutfromtheoriginaldepositionalenvironment tocavedevelopmentwithoutgoingthroughburial,massive diagenesis,anduplift.AfterVacherandMylroie,2002. D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 70 N JournalofCaveandKarstStudies, April2007

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OligocenetoPliocene.Analysisoftheserocksandtheir karrenshowedthatasdiageneticmaturityincreased,the karrenbecamelessdistinctiveaseogenetickarren,and resembledmorecloselythetelogenetickarrenofcontinentalinteriors(Taboros ietal.,2004). F UTURE R ESEARCH Thecurrentstateofaffairsregardingislandkarstisvery promising.Oneoftheinterestingappliedresearchareasis thepotentialforislandkarsttobepreservedaspaleokarst intherockrecord,thereforebecomingahostfor mineralizationorhydrocarbons.Aseogeneticcarbonate rocksarefoundproximaltotheirenvironmentofdeposition,allthatneedstohappentopreservethoserocks, andanyincludedkarstfeatures,isforsubsidencetolower themandcontinuedcarbonatedepositiontoburythem.To preserveanexistingtelogeneticconduitcavesystemin acontinentalinteriorsettingwouldrequiremajoradjustmentofplatetectonicmotion,todepressthelandmassand allowburialtooccur.Whileallthisplateadjustmentwas occurringovermillionsofyears,theexistingcavesystem wouldneedtoavoiddestructionbyerosion.Itisclearthat eogenetickarstispredisposedtopreservation,andthat paleokarstintherockrecordismostlikelyformer eogenetickarst. Tolocateandassesspaleokarstinthesubsurface,itis importanttodeterminewhattosearchfor.Imaginealarge carbonateunitinthesubsurface,adisk100mthickand 10kmindiameter,onceexposedattheearth’ssurfaceand subjectedtokarstprocesses,andnowburied.Ifone assumestelogenetic,conduitcavekarst,thenonelooksfor voidsextendingfromthecenterofthedisktothemarginin afewplaces,asconduitcavesthatdrainedtheinteriorof thefeature.Ifoneassumesthateogeneticmixingzonekarst wasactive,thenonelooksfordissolutionalvoidsspaced aroundtheperimeterofthefeature.Thereisa90 u differenceinsearchstrategydependingonwhichmodelis chosen. Theuniquepatternofflankmargincaveshascalled attentiontohowtheydevelop.Unliketeleogeneticconduit caves,forwhichalargeandextensivedatabaseexists,the eogeneticislandcavedatabasehasbeenbuiltfromscratch overthelastthreedecadesbyaverysmallgroupof workers.Asaresult,untilrecentlythepatternsthatdrive eogeneticcavessuchasflankmargincaveswerenoteasily interpreted.Arankorderplotofflankmargincavesbased onarealfootprint(Fig.14),fromtheBahamas,showsthat thecavesself-selectintothreesizecategories(Rothetal., 2006).Arealfootprint,orcavearea,wasselectedasthesize determinerbecauseitisthebestmeasureofhowmuch dissolutionhasoccurred.Giventhatflankmargincaves forminthedistalmarginofthefresh-waterlens,their verticalvariationisminimalasthelensissothinatthat location.Calculatingareausingtheoutsideperimeter,and removingtheareaofanyinnerbedrockpillars,creates ameasureoftheamountofdissolution.Forstreamcaves intelogeneticsettings,cavelengthisagoodmeasureofthe amountofdissolution,asthosecavesareverylong comparedtotheirwidths. Flankmargincavesbeginastinyvoidsthatgrow throughtime.Asthedissolutionalenvironmentisrestricted totheedgeofthelens,thisdissolutionoccursinaband thatrunsfromthecoastlineoftheislandinlandjustafew tensorhundredsofmeters.Insuchasetting,thegrowthof smallvoidscancontinue,butatsomestage,adjacentvoids, ofvarioussizes,willintersect.Whentheydo,cavesizethen makesanimmediatejumpinsize.Asthesecaveclusters continuetogrow,theythenintersectotherclusters,and thereisagainalargejumpincavesize.Fig.14showsthree straightlinesegments,withslopesthatareapproximately thesquareofthepreviousslope,thatrepresentsmall (100m 2 orless),medium(100–1000m 2 )andlargecaves (over1000m 2 ).Thedataindicatethatassmalldissolutionalvoidsgrowatrandominthethinlensmargin,their amalgamationoccursasdiscretesteps,eventhoughwithin eachsizecategorythereisawiderangeofsizesdepending ontheinitialsizeoftheindividualchambers,andhow manybecameconnected.Dissolutioncontinuesafter chamberamalgamation,andsuchamalgamationshave agreaterchanceofaddingtochambersbyconnectionthan thesmallersizeclassdoes.Computermodelingofthiscave generationproceduregenerateslineslopesthatare identicaltotheempiricaldatabase(Labourdetteetal., 2006),butincludea4 th setat1–2m 2 inarea.This4 th small Figure14.Rankorderplotsofflankmargincavesize(as determinedbyarealfootprint).A)Completeplot,whichhas 3straightlinesegments,eachreproducedin(B)smallcaves, 100m 2 R 2 0.9805,slope 6.024;(C)mediumcaves,100– 1000m 2 R 2 0.956,slope 31.815;and(D)largecaves, over1000m 2 R 2 0.9302,slope 1,113.3.Thelineslope changesindicatethepointatwhichmajorcavechamber intersectionsoccur,creatingajumpincavesize.From Roth(2004). J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 71

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areagroupdoesnotappearintheislanddatabaseasvoids thatsmallarenotmappedascaves. Afurthertestofcavegrowthbyaggregationofsmaller cavescanbedonebyplottingcaveareaversuscave perimeter.Forthesedata,theinternalareaofbedrock columnsand‘‘islands’’wasremovedfromtheareal footprint,buttheperimeterofsuchinternalfeatureswas retained,asitwasawater-rockcontactduringcave development.Astheperimetergrowslinearly(m),but areabythesquare(m 2 ),simplegeometricshapesproduce anexponentialcurveastheygetlarger(Fig.15).Flank margincaves,however,plotasanapproximatestraight line,whichindicatestheirperimetersmustbeprogressively morecomplexasthecavesincreaseinsize,compensating fortheincreaseinareabythesquare.Theeasiestwayto createthisperimetercomplexityistoaggregatesmaller caveclusterstocreatearamiformpattern,supportingthe datacreatedbytherank-orderversusareaplot(Fig.14). Flankmargincavegrowthbycaveaggregationismuch differentthanconduitcavegrowthbysurfacewater capture,furtherreinforcinghowdifferentislandkarstis fromcontinentalkarst. Areaissuesworknotonlyatthecavelevel,butalsoat theislandlevel.Asislandsgetbigger,theirperimeter becomeslessrelativetotheislandarea.Or,inhydrological terms,therechargeareaincreasesexponentially,butthe dischargeregionincreasesonlylinearly.Asislandsget bigger,everlargeramountsofmeteoricwatermustexit throughtheperimeter.Forexample,inanislandwith aradiusof1km,itsarea( A )is3.14km 2 ,anditsperimeter ( P )is6.28km,foran A/P ratioof0.5km.Iftheislandhas a100kmradius, A is31,416km 2 P is628kmforan A/P ratioof50km.MylroieandVacher(1999)hypothesized thatatsomeperimeter/arearelationship,diffuseflowinthe fresh-waterlensmustbecomeinefficient,andconduitflow willinitiate.Evidenceofsucharelationshipcanbeseen todayintheBahamasandBermuda.Thedryflankmargin cavesseentodayformedinhillsthatatapast 6msea level,wereislandswithlineardimensionsofafewkm. However,ifsealeveldropped20mbelowtoday’slevel,the broad,shallowBahamaBankswouldbecomeverylarge islands,withlineardimensionsofhundredsofkm.The sameistrueforBermuda.Didthislargersizecross athresholdandgenerateconduitflowsystems?Cavedivers havefoundlong,linearconduitcavesatdepthsof20to 30monGreatBahamaBank(FarrandPalmer,1984),and atasimilardepthontheBermudaPlatform(Vacherand Harmon,1987).Thesedepthsarelessthan60m,andso werenotobservedduringthesubmarineworkonSan SalvadorIsland.Thefieldevidencewouldsuggestthat islandsizecontrolswaterflowfromislands,favoring conduitflowatlargeislandsizes. Asnotedearlier,someofthemostclassicworkonfresh water/saltwatermixinganddissolutionwasdoneinthe Yucatanarea(Backetal.,1986).Thelarge,complexcave systemsofQuintanaRooStateareknownasintricate conduitsystemsdischargingwaterfromtheinteriortothe sea(Smartetal.,2006).TheYucatanPeninsulacanbe consideredaverylargeisland,whichwouldbeexpectedto generateconduitflow.Onequestionis:Doesthatconduit flownegatethedevelopmentofflankmargincavesinthe areasalongtheperimeterwhereconduitsarenotpresent? FieldworkintheAkumalareaofQuintanaRoohas demonstratedthatthePleistocenecoastaleolianitesthere containflankmargincaves(Kelleyetal.,2006).Duringthe lastinterglacial(OIS5e),whiletheinterioroftheYucatan Peninsulawasdischargingfreshwatertotheseaatdepths of10to20m,anentirelydifferentsortofcavewas developingunderhypogenicconditionsinthedistalmargin ofthefresh-waterlens.Epigenicconduitflowcavesand hypogenicflankmargincavescanformandfunctioninthe samelocalityandatthesametime. RecentworkhastakenustoFaisIsland,220kmeastof Yap,FederatedStatesofMicronesia,inthefarwestern Pacific.Theislandisanupliftedcarbonateplatform1.2km by2.9km,withelevationsupto28m.Theislandobtainsits freshwaterfromrainfallcatchment,andfollowingdroughts ortyphoons,suffersfromwater-supplyproblems.Research wasundertakentodetermineiftheCIKMcouldassistin determininghowtoexploittheisland’sground-water resources.Theislandbeachesareunderlainbyatightlycementedreefflatthatextendsseaward,andthatactsasan aquitard,restrictingfresh-waterlensdischargetothesea. Flankmargincaveswerenotfoundinhighgroundbehind thebeaches,butonlywhereheadlandscrossedthereefflat towardstheopenocean.Theseobservationsindicatedthat fresh-waterdischargeinthepastwasdirectedthroughthese headlandstobypassthelow-permeabilityreefflats.Analysis ofupliftedflankmargincavescouldbeusedasaproxyto locatepreferreddischargesforfreshwatertoday.Usingthe Figure15.Plotofflankmargincaveperimeterversusarea, comparedtostandardgeometricalobjects.Globulardissolutionchamberswouldexpecttoplotasacurve,muchlike circlesandsquaresdo.Thehighdegreeofperimeter complexity,producedbyintersectionofdissolutionalvoids, createsalinearplotinstead,approximatingarectanglewith a1to100aspect(widthtolength)ratio.FromRoth(2004). D EVELOPMENTOFTHECARBONATEISLANDKARSTMODEL 72 N JournalofCaveandKarstStudies, April2007

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lowestnegativetidesoftheyear,itwasfound(Mylroieetal., 2005)thatancientflankmargincavepositionsabovemodern sealevelidentifiedexistingfresh-waterdischargesites.Itwas alsofoundthatwhatwasbelievedtobeablueholeoralarge cavecollapsefeaturewasactuallyasand-filledembayment, andadugwellfromtheJapaneseoccupationpriortoWWII. AswiththeHolocenesandaquifersoftheBahamas discussedearlier,thissand-filledembaymenthadthelargest amountoffreshwater.Inthislattercase,itwastheabilityof theCIKMtosuccessfullyinterpretapseudokarstfeature thathelpedaddressthewaterproblem. S UMMARY ThedevelopmentoftheCarbonateIslandKarstModel, orCIKM,requiredfourmajoraccomplishments: 1)Intellectualseparationfromcaveandkarstdevelopmentmodelsthathadbeenproducedincontinental settings,intelogeneticrocksassumingconduit(or epigenic)flow. 2)Understandingtheuniqueflowsystemsandgeochemistryofisolatedcarbonateislandaquifers,and applyingthoseunderstandingstocaveandkarst development. 3)Collectionofasufficientlylargedatabasewithineach islandtypetoallowpatternstobeexpressed.Inother words,find,explore,andmapalotofcaves. 4)Studyofawidevarietyofcarbonateislandtypesto allowcompareandcontraststudiestobemade.In otherwords,gotoalotofislands,andfind,explore, andmapalotofcaves. Theprogressionofthefieldworkfromthesimplest environment,intheBahamas,toprogressivelymore complexenvironmentsinBermuda,IsladeMonaandthe MarianasallowedtheCIKMtobebuiltmodularly, expandinginalogicalprogressiontoaccommodateeach successivecomplication.Ifwehadstartedourworkinthe Marianas,wemayhavewellflounderedfordecadesbefore piecingthepuzzletogether. Caveandkarstscienceislikeanyotherscience: discoverycomesatunexpectedtimesasaresultof persistence,preparation,anopenmind,andalittlebitof luck.Forthelast35yearswehavetraveledwidelyand soughtoutislandsandtheircaves.Initiallyitwasenough tofindthecaves.Thenitwasenoughtomapthem.But finally,itwasn’tenoughuntilweunderstoodwhytheywere there.Wedidn’tsetouttobecomeislandcaveandkarst experts,butitsurehasbeenfun. A CKNOWLDGMENTS Overmorethanthreedecades,ourlivesandourscience havebeenupliftedbythemanypeoplewhoworkedwithus inallthemanyislands.ArtandPegPalmertookusonour firstscientificislandtripandformanyyearshaveprovided friendshipandscientificinsightthathashelpeduswithour work.JimCarewhasbeentheultimateislandpartnerand buddy,workingwithustoconstructgeologicalandkarst modelsintheBahamasthatledtothefoundationofideas thatnowguideourresearch.JoeTroesterinitiatedtheIsla deMonawork,andwasachampionofislandkarst.Len Vacherhasbeenasourceofsolidscientificexpertiseand intellectualcompanionshipthathaskeptusontask,aware ofreality,andfullofthefunofdoingscience.JohnJenson sweptusawaytothePacific,showeduswhattrue complexitycanbeinislands,andbeenasteadfastfriend andsourceofinspiration.Otherswhoshowedushowto thinkaboutislandsinscientifictermshavebeengreat friendsandcolleagues:MikeQueen,NeilSealey,Pete Smart,FionaWhitaker,andthelateRobPalmer.Wethank allthemanystudents,graduateandundergraduate,who laboredandstruggledtodothefieldworkandexploreideas aboutislands.WemustthankDonGerace,founderofthe GeraceResearchCenter(GRC)onSanSalvadorIsland (formallytheBahamianFieldStation),whoprovided encouragement,resources,friendship,andoccasionaldisciplineandcatapultedourcareerforward,alongwithDan Suchy,KennyBuchan,andVinceVoegeli,GRCExecutive Directors.MurrayStateUniversityandMississippiState Universityprovideduswithanacademichome,resources, andintellectualsupporttoaccommodateourresearchin distantareas.CarolWicksandananonymousreviewer providedhelpfulinput.Finally,wethankthemany governmentagencies(domesticandforeign),publicworkers,andprivatelandownersinmanycountriesandislands, whoassisteduswithaccess,permits,resources,and encouragement.TheauthorswouldalsoliketothankMarc OhmsforthecartographythatappearsinFigure10. 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Roth,M.J.,Mylroie,J.E.,Mylroie,J.R.,Ersek,V.,Ersek,C.C.,and Carew,J.L.,2006,FlankMarginCaveInventoryoftheBahamas, in Davis,R.L.,andGamble,D.W.,eds.,Proceedingsofthe12 th SymposiumontheGeologyoftheBahamasandOtherCarbonate Regions,GeraceResearchCenter,SanSalvador,Bahamas, p.153–161. Schwabe,S.J.,andCarew,J.E.,2006,Blueholes:Aninappropriate monikerforwater-filledcavesintheBahamas, in Davis,R.L.,and Gamble,D.W.,eds.,Proceedingsofthe12 th Symposiumonthe GeologyoftheBahamasandOtherCarbonateRegions,p.179–187. Smart,P.L.,andWhitaker,F.,1989,ControlsontheRateand DistributionofCarbonateBedrockSolutionintheBahamas,in Mylroie,J.E.,ed.,ProceedingsoftheFourthSymposiumonthe GeologyoftheBahamas,BahamianFieldStation,SanSalvador Island,Bahamas,p.313–321. Smart,P.L.,Beddows,P.A.,Coke,J.,Doerr,S.,Smith,S.,andWhitaker, F.F.,2006,CavedevelopmentontheCaribbeancoastoftheYucatan Peninsula,QuintanaRoo,Mexico:GeologicalSocietyofAmerica SpecialPaper404,p.139. Stafford,K.W.,Mylroie,J.E.,Taboros i,D.,andJenson,J.W.,2004, Eogenetickarstdevelopmentonasmall,tectonicallyactive,carbonate island:Aguijan,MarianaIslands:CaveandKarstScience,TransactionsoftheBritishCaveResearchAssociation,v.31,no.3, p.101–108. Stafford,K.W.,Mylroie,J.E.,Taboros i,D.,Jenson,J.W.,andMylroie, J.R.,2005,KarstdevelopmentonTinian,Commonwealthofthe NorthernMarianaIslands:Controlsondissolutioninrelationtothe carbonateislandkarstmodel:JournalofCaveandKarstStudies, v.67,no.1,p.14–27. Taboros i,D.,2000,KarstfeaturesonGuam[M.S.thesis]:Mangilao, Guam,UniversityofGuam,324p. Taboros i,D.,Jenson,J.W.,andMylroie,J.E.,2004,Karrenfeaturesin islandkarst:Guam,MarianaIslands:ZeitschriftfurGeomorphologie. N.F.,v.48,p.369–389. Taboros i,D.,Jenson,J.W.,andMylroie,J.E.,2005,Karstfeaturesof Guam,MarianaIslands:Micronesia,v.38,no.1,p.17–46. Taboros i,D.,Mylroie,J.E.,andKirakawa,K.,2006,Stalactiteson tropicalcliffs:Remnantsofbreachedcavesorsubaerialtufadeposits?: ZeitschriftfurGeomorphologie,v.50,p.117–139. Vacher,H.L.,andHarmon,R.S.,1987,PenroseConferenceFieldGuideto BermudaGeology.,SouthernMethodistUniversity,Dallas,Texas,48p. Vacher,H.L.,1988,Dupuit-Ghyben-Herzberganalysisofstrip-island lenses:GeologicalSocietyofAmericaBulletin,v.100,p.223–232. Vacher,H.L.,andMylroie,J.E.,2002,Eogenetickarstfromthe perspectiveofanequivalentporousmedium:Carbonatesand Evaporites,v.17,no.2,p.182–196. Viles,H.A.,1988,Organismsandkarstgeomorphology, in Viles,H.A., ed.,Biogeomorphology:NewYork.BasilBlackwell,Ltd.,p.319–350. Wallis,T.N.,Vacher,H.L.,andStewart,M.T.,1991,Hydrogeologyofthe freshwaterlensbeneathaHolocenestrandplain,GreatExuma, Bahamas:JournalofHydrology,v.125,p.93–100. Wexel,C.,Jenson,J.W.,Mylroie,J.R.,andMylroie,J.E.,2001, CarbonateIslandKarstofSaipan:GeologicalSocietyofAmerica AbstractswithPrograms,v.33,no.6,p.A–6. Wilson,W.L.,1994,Morphologyandhydrologyofthedeepestknown caveintheBahamas:Dean’sBlueHole,LongIsland, in Boardman, M.R.,ed.,SeventhSymposiumontheGeologyoftheBahamas, BahamianFieldStation,SanSalvadorIsland,Bahamas,Abstract, p.21. Wilson,W.L.,Mylroie,J.E.,andCarew,J.L.,1995,Cavesasageologic hazard:AquantitativeanalysisfromSanSalvadorIsland,Bahamas, in Beck,B.F.,ed.,KarstGeohazards,Brookfield,A.A.Balkema, p.487–495. J.R.M YLROIEAND J.E.M YLROIE JournalofCaveandKarstStudies, April2007 N 75



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CAVESEDIMENTSANDPALEOCLIMATE W ILLIAM B.W HITE MaterialsResearchInstituteandDepartmentofGeosciences,ThePennsyl vaniaStateUniversity,UniversityPark,PA16802USAwbw2@psu.edu Abstract: Thispaperisareviewofcavesediments:theircharacteristicsandtheir applicationaspaleoclimatearchives.Cavesedimentscanbeseparatedin totwobroad categories,clasticsedimentsandchemicalsediments.Ofthese,streamtransportedclastic sedimentsandcalcitespeleothemsareboththemostcommonandalsothemos tusefulas climaticrecords.Techniquesfordatingcavesedimentsincluderadiocar bonandU/Th datingofspeleothemsandpaleomagneticreversalsandcosmogenicisotop edatingof clasticsediments.Cosmogenicisotopedatingofclasticsedimentsincav eswithmultiple levelsorwhichoccuratdifferentelevationsprovideageomorphicrecord ofcaveages andriversystemevolutionoverthepast5Ma.Isotopeprofiles,traceelem entprofiles, colorbandingandluminescenceprofilesofspeleothems,mainlystalagmi tes,produce adetailedpaleoclimaterecordwithveryhightimeresolutionoverthepas tseveral hundredthousandyears.Thereispotentialapplicationofthesemethodst olateHolocene climateswithimplicationsforevaluationofcurrentconcernoverglobal warming. I NTRODUCTION Cavesareopencavitiesintheearth.Assuchtheyare naturalsedimenttraps.Nocaverneedstoberemindedthat cavesaremuddy.Closerinspection,however,showsthat cavedepositsareremarkablycomplicatedasarethe transportmechanismsthatcarrythesedimentsintothe caves.Cavesedimentshavebeenrecognizedforaslongas therehasbeenscientificinterestincaves.However,onlyin thepastseveraldecadeshasitbeenrecognizedthatcave sedimentscontainbothhydrogeologicalandpaleoclimatologicalrecords.Inpart,thislaterecognitionisduetothe recentdevelopmentoftechniquesforassigningdatesto cavesediments.Withanaccuratechronology,thecave archivescanbecorrelatedwitheventsonthelandsurface above.Theinvestigationofcavesedimentshasmovedfrom anobscurecornerofkarstsciencetooneoftoday’shottest topics(e.g.,SasowskyandMylroie,2004).Thereisthevery realpossibilitythatcavesedimentswilltaketheirplace alongsideofoceansedimentcoresandcontinentalice cores(GreenlandandAntarctica)asthemostimportant recordsofhowEarth’sclimatehasevolvedoverthepast severalmillionyears. Theobjectiveofthepresentpaperistosummarizesome ofthecurrentstateofknowledgeofcavesediments.Aswill beseen,thesubjecthasgrownmuchbroaderthanitwasin 1966ontheoccasionofthe25 th anniversaryvolume.The literaturehasbecomeverylarge.Whatfollowsare examplestogivesomefeelforwhathasbeenaccomplished, particularlyinthepast10–20years.Itisnotacomprehensivereview. S OME H ISTORICAL B ACKGROUND Therehasalwaysbeenadistinctionbetweenspeleothemsandclasticsedimentsincaves.Speleothemsare aestheticallypleasingandtheirbizarreshapesgivecaves muchoftheircharm.Ittakesaspecialpointofviewtosee thesamescientificvalueinamudbankasinaclusterof stalagmites. Thefirstdescriptionsofspeleothemsarelostinthe mistsofantiquity.Shaw’s(Shaw,1992)monumental treatiseoncavesciencepriorto1900devotes13chapters tospeleothemsincludingaccountsofearlyandsomewhat fancifulattemptstoexplainthem.Manydescriptionsofthe variousformsofspeleothemshaveappeared,andoneof thebestandmostdetaileddescriptionsoftheircrystal structureswaswrittennearlyacenturyago(Prinz,1908). Thecorrectchemicalreactionforthedepositionofcalcite incaveswasdescribedasearlyas1812byCuvierandin 1820byBenjaminSillimantheelder(Shaw,1992).Inanow classicpaper,Hollandetal.(1964)setforthadetailed chemicalmodelforcalcitedepositionthatremainsthe acceptedexplanationtothepresenttime. Clasticsedimentsarerarelymentionedpriorto1900 (Shaw,1992).Thetwomaincategories,breakdownand streamdeposits,areonlybrieflymentionedinthetwomost importantearly19 th Centurytextbooks(Kyrle,1923; Trombe,1952).Clasticsedimentsdidplayacentralrole intheBretz(1942)modelforcavedevelopment.According toBretz,cavesformeddeepbelowthewatertableandthen filledwithredunctuousclaywhichfiltereddownfrom overlayingsoils.Laterdissectionofpeneplainsand drainingofthecavesallowedthesedimentstowashout, leavingbehindtheopencavepassagesweseetoday.Many ofBretz’sfieldobservationswereinMissouricaveswhere thestickymudsareparticularlycommon.Inresponse, Reams(1968)devotedanentirePh.D.dissertationto demonstratingthatmanyoftheMissouricavesediments are,infact,riversedimentscarriedinthroughsinkholes andbysinkingstreams.Incontrast,Davies(1960)used thesandandgravelsedimentsinAppalachiancavesto WilliamB.White–Cavesedimentsandpaleoclimate. JournalofCaveandKarstStudies, v.69,no.1,p.76–93. 76 N JournalofCaveandKarstStudies, April2007

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demonstratethatthecaveswereformedbyfast-moving waterclosetolocalbaselevelsandnotbyslowpercolation deepbelowthewatertable. Cavessedimentscameintotheirownasasignificantpart ofcavescienceinthe1960swithanimportantsymposium onbothchemicalandclasticsediments(Dell’Oca,1961)and thecomprehensiveresearchofRenault(1967–1969).The paleoclimaticsignificanceofclasticsedimentswasrecognizedinEuropeanalpinecavesbySchmid(1958).Thefirst twoEnglishlanguagetextbooksoncaves(Jennings,1971; Sweeting,1972)hadchaptersdevotedtocavesediments althoughthecoveragewaspredominantlyonchemical sediments.ClasticsedimentresearchintheUnitedStatesgot underwayinthemid-1960swiththeworkofFrank(1965) onthecavesofTexasandlaterworkinAustralia(Frank, 1969,1971).Manyoftheseearlystudiestreatedclastic sedimentsincavesasapeculiarsortofsedimentaryrock withemphasisonin-cavestratigraphyandprovenanceof thesediment.Oneofthemostcomprehensivestudiesof sedimentsourceanddepositionwasanunpublishedPh.D. thesis(Wolfe,1973)describingcavesedimentsinthe GreenbrierkarstofWestVirginia. C LASSIFICATIONOF C AVE S EDIMENTS Thereisnogenerallyacceptedclassificationschemefor cavesediments.Eachofthemorerecenttextbooksoncaves andkarst(Bo ¨gli,1980;White,1988;FordandWilliams, 1989,Gillieson,1996)presentsaclassificationofsediments. Thesehavemanypointsincommonbutalsosignificant differences.TheclassificationinFigure1isacompromise. Itliststhemaincategoriesofsediment,butdoesnot attempttoprovideapigeonholeforeverypossible materialthatmightaccumulateinacave. Sedimentsaredividedintotwobroadcategories:clastic sedimentsandchemicalsediments.Clasticsedimentsare movedmechanicallywhereaschemicalsedimentsare formedinplace,precipitatedfromsolutioninseeping, dripping,orflowingwater.Clasticsedimentscanthenbe subdividedagainintomaterialsthatarederivedlocally withinthecaveandmaterialsthataretransportedintothe cavefromtheoutside.Theseareknownrespectivelyas autochthonoussedimentsandallochthonoussediments. Chemicalsedimentsaresubdividedintocategoriesbased ontheircomposition. Locallyderivedclasticmaterialconsistsofweathering detritus,breakdown,andguano.Weatheringdetritusisthe insolublecomponentofthebedrock,leftbehindwhenthe bedrockdissolved.Weatheringdetritusisonesourceofthe stickyclaysfoundinsomecavesthathavenoevidenceof streamaction.Weatheringdetrituscanincludesand, silicifiedfossilfragments,andchert,thelatterinsome limestonesbeingamajorcomponentoftheclastic sediment.Breakdownconsistsoffragmentsofbroken bedrockinawiderangeofsizes.Theclassificationof breakdownandthegeologicprocessesresponsibleforcave passagecollapseismorecomplexthanexpected(Whiteand White,1969;Jameson,1991).Guanoisthefecalmaterial depositedincavesbybatsandbirds.Incaveswithlargebat populations,guanoispresentinsufficientquantitiestobe classifiedasasediment. Thecompositionofallochthonoussedimentvaries dependingontherocktypesandothermaterialsavailable inthedrainagebasininwhichthecaveisembedded.Cave entrancesareusuallysitesofintensiveweatheringandthe combinationofbreakdown,downslopemovementfrom otherrockunitsabovethecave,soilslumping,and incorporatedplantmaterialcreatesacharacteristicpileof roughlystratifieddebrisknownasentrancetalus.Entrance talusisofimportancebecauseitoftenhousespaleontologicalorarchaeologicaldeposits.Infiltratesaresediments thatmigrateintothecavefromthelandsurfaceabove. Theysubdivideintosoilwashdownwhichismainlysoil fromtheepikarstthatiswashedintothecavethrough solutionally-widenedfractures,andgravitationaldebris whichiscoarser-grainedmaterialthatfallsdownopen shafts.Sinkingstreamscarryagreatvarietyofmaterials intocavesincludingalluvialsediment,glacialtills,volcanic ashandanyotherunconsolidatedmaterialthatmaybe pickedupbythestream.Debrisflowsareessentially avalanchesthatflowunderground.Theseproviderarebut Figure1.Aclassificationofcavesediments. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 77

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dramaticcavedeposits,forexamplethosefoundinthe cavesoftheNewGuineahighlands(Gillieson,1986). Finally,quantitiesofsandandloesscanbeblowninto cavesdirectlybywindactiontoproduceaeoliandeposits. Mostcommonofthechemicalsedimentsarethe travertines.Thewordtravertineishereusedasablanket labelforfresh-watercarbonatedepositsofalltypes. Travertineisusedasarocknamewhereasspeleothemrefers tothespecificexternalmorphologyofthedeposits.Cave travertinesarechemicallysimilartothecalcareoustufas foundasspringandfreshwaterdepositsthroughoutthe worldandtothegeothermaltravertines(FordandPedley, 1996).Tufasgenerallyareporousandcontainagreatdealof plantmaterialincomparisontobothcaveandgeothermal travertines,whichareusuallydenseandcompact.Tufasalso containpaleoclimaticrecords(Andrews,2006). Thetermevaporiteisusedforcavesedimentsinmuch thesamewaythatitisusedforsurfacesediments; assemblagesofmineralsformedbyevaporatingwater. Mostcommonincavesisgypsum,CaSO 4 2H 2 O,butthere existaselectionofothersulfatemineralsaswellas occasionalhalitedeposits.Theremainingcategoriesof chemicalsedimentslistedinFigure1arevolumetrically ratherminor.Phosphates,mainlyhydroxyapatite,are associatedwitholdanddecomposedguanodeposits.The resistates,ironandmanganeseoxides,areusuallylimited tocoatings.Perennialiceoccursinalpinecavesandsocan reasonablybeconsideredacavesediment. C LASTIC S EDIMENTS Figure1providesasystematiccategorizationofclastic sedimentsintermsofsourcearea.However,theconduit systemactsasamixingchambersothatthesediments observedincavesoremergingfromkarstspringscontain componentsfromallofthesources.Figure2givesthe overallconcept.Thekeyparametersareflowvelocities, flowvolumes,particledensity,andparticlesize.Although theremaybesomecontributionofrelativelylightorganic material,mostclay,silt,sand,cobblesandbouldershave densitiesnotgreatlydifferentfromthatofquartz(2.65g cm 3 ).Densityvariationsarenotaverysignificant variable.Thesizeofclasticparticlesvariesoversixto eightordersofmagnitudefromsub-micrometercolloidal andclayparticlestobouldersapproachingonemeter.The clasticsedimentsremainingincavesandthefluxofclastic sedimentsthroughtheaquiferaredeterminedmainlyby stormflowandbyparticlesize.Clasticparticlesflushed throughthesystemarepartofthehydrology;clastic particlesremainingafterthecavesaredrainedbecomethe sedimentrecord. T RANSPORT M ECHANISMS Sedimenttransportinopenchannelsoccursbytwo mechanisms:suspendedloadandbedload.Thesuspended loadconsistsofparticlestakeninsuspensionbythe turbulenceofstreamflow.Suchparticlestendtosettleout, butareheldinsuspensionbytheturbulence.Theenergy requiredtoholdparticlesinsuspensionandtherateat whichtheysettleoutofsuspensiondependonparticlesize. Ifflowvelocitiesdecrease,forexamplebyanexpansionof thepassagecross-sectionorbypondingofwaterbehindan obstruction,coarsesedimentsdropoutrapidlybutvery fine-grainedsedimentsmayremaininsuspension.Flowing watermovesbedloadbydraggingitalongthebedbecause oftheboundaryshearbetweenthemovingwaterandthe bedmaterial.Itisnotrequiredthattheseflowsbeturbulent althoughtheyusuallyare.Theboundaryshearnecessaryto putbedparticlesinmotionincreasesalmostlinearlywith theparticlesizeandwiththesquareoftheflowvelocity. Thereisawiderangeinparticlesizesforthematerial injectedintotheconduitsystemsfromthesourcessketched inFigure2.Velocitiesvaryalongtheconduitdependingon whetheraparticularsegmentispipe-fullorflowinginan openchannel,dependingonpassagecross-sectionalarea, anddependingonobstaclesorblockageswithinthe conduit.Velocitiesalsovarydependingonwhetherthe systemisatbasefloworstormflow,andifatstormflow, onthemagnitudeofthestorm.Asaresultthereisavery complexmixingandpartitioningofsedimentwithinthe conduitsystem.Smallparticlesinthecolloidalorfineclay sizerangemayremaininsuspensionandprovide acontinuousfluxofsedimentatthespringevenduring baseflowconditions.Clayandsiltsizedparticlesmaysettle intotemporarystorageduringbaseflowbutareresuspendedandcarriedtothespringduringstormflow, thuscausingthespringtobecomemuddy.Verycoarse pebbletocobblesizesedimentsmaybesweptintothe conduitsystemduringlargestormsandremaininthe systeminlong-termstorageuntiltheyaresweptonthrough byanotherexceptionalstorm.Thereisacontinuous interchangeofsedimentdependingonflowconditions. Muchrecentresearchhasbeenconcernedwiththe hydraulicsofsedimenttransportandwiththeappearance ofsuspendedsedimentsatkarstsprings.Becauseofthe openconduits,manyspringsdischargeverysmallparticles Figure2.Sketchshowingclasticsedimentsourcesandthe roleoftheconduitsystemasamixingchamber. C AVESEDIMENTSANDPALEOCLIMATE 78 N JournalofCaveandKarstStudies, April2007

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evenunderbase-flowconditions(Atteiaetal.,1998).The fine-grainedparticlesareofimportancebecausethey provideatransportmechanismforbacteria(Mahleret al.,2000)andheavymetals(VesperandWhite,2003). Turbidormuddyspringwatermakesthespringsunsuitableaswatersuppliesandasaresulttherehavebeenmany studiesofsuspendedsedimenttransporttosprings(Mahler andLynch,1999;Drysdaleetal.,2001;Amraouietal., 2003;Masseietal.,2003;DogwilerandWicks,2004). Therehasbeenrelativelylittlerecentworkonthe mechanismsoftransportofthecoarsefractionthatmakes upmuchofthesedimentseenincaves.Gale(1984)was abletousetheobservedsedimentparticlesizestoback calculatethehydrauliccharacteristicsoftheconduitin whichtheywerefound.Onerecentstudy(Hartand Schurger,2005)estimatedtherateofsedimentinjection throughsinkholestobe111Mgkm 2 yr 1 forawatershed incentralTennessee. L ITHOFACIES Ultimately,ofcourse,thecomposition,mineralogy,and lithologyofcaveclasticsedimentsdependonthematerial availableinthesourceareas.Withinthisconstraint, however,thesedimentarydepositsdependontheinternal dynamicsoftheconduitsystem.Thus,caveclastic sedimentsoccurinfaciesthatreflectthewayinwhich injectedsedimenthasbeenrearrangedanddeposited. Therehavebeenanumberoffaciesschemesproposed dependingonthecriteriausedforidentifyingthefacies (e.g.,Gillieson,1986;SpringerandKite,1997).Thescheme sketchedinFigure3(BoschandWhite,2004)describes faciesaccordingtoparticlesizeandthedegreeofsorting.It willbenotedthattheaxesinFigure3havenoscale. Further,theboundariesbetweenthefaciesdomainsare exceedinglyfuzzy. Thewidestrangeofparticlesizeandparticlesorting occursinthemostcommonstreamdepositsincaves,the channelfacies.Theyoccurasroughlystratifiedlayersof sands,silts,andcobbledepositsmosteasilyobservedwhere morerecentstreamshavecutthroughearliersediments thusexposingthelayeringinthestreambank.Anygiven exposureofchannelfaciesislikelytoshowdistinct bedding,butthisstratigraphyisrarelycontinuousalong thecavepassage.Thethalwegfaciesisaderivativeofthe channelfacies.Thalwegfaciesarethecoarsecobble armoringthatformsthebedsofmanyactivecavestreams. Thecoarsematerialisaresidualdepositformedbystream actionwinnowingoutthefine-grainedmaterialfromthe channelfacies.TheotherthreefaciessketchedinFigure3 eachinvolvedifferenttransportprocesses. Slackwaterfaciesarethethinlayersoffinegrainedsilt andclaythatoftenformthefinaltoplayerofclastic deposits.Thisfaciesisoftenfoundinblindsidepassages, pockets,andothernichesincavesunlikelytobereachedby flowingstreams.Theslackwaterfaciesappeartobe depositedfromsuspendedsedimentthathassettledout offloodedcavepassages.Risingfloodwatersfillall availablespacesandarethenpondedforextendedperiods oftimeuntilthefloodrecedes.Duringthetimewhenthe passageiswater-filled,suspendedsedimentshavetimeto settleoutandformasedimentlayer.Aninvestigationof thisfaciesinAgenAllweddCaveintheUK(Bull,1981) revealeddistinctlaminaewhichwereinterpretedtobethe resultofarhythmicpulsingofsediment-ladenwaterinto subterraneanlakesinresponsetosurfaceclimate.Careful examinationofthismicrostratigraphyrevealedasequence ofclimaticeventsextendingback17,000years(Bull,1980). Diamictonfaciesaretheresultofdebrisflows.These arechaoticdepositscontainingparticlesrangingfromclays tocobblestossedtogetherwithnobeddingandnosorting. Specialcircumstances,mainlyextremestormintensities andhighgradientcavepassages,allowentiresediment depositstobetakenintosuspensionandsweptdownacave passagetolaterbedepositedinanundifferentiatedmass. Diamictonfaciesweredescribedfromthehighgradient cavesinNewGuinea(Gillieson,1986). Insomecaves,particularlynetworkmazes,flow velocitiesneverreachthresholdvaluesforsedimenttransport.Thesedimentsinthesecavestendtobelocally derived,eithertheresidualinsolublematerialfrom dissolutionofthelimestoneorinfiltratingsoilfromthe landsurfaceabove.Theterm‘‘backswampfacies’’was chosenbecause,hydraulically,networkmazesandother slow-flowcavestendtobehaveastheunderground equivalentofswamps. C HEMICAL S EDIMENTS M INERALOGY Caves,wheretemperature,watervaporpartialpressure, carbondioxidepartialpressureandotherenvironmental Figure3.Faciesofclasticsediment.Adaptedroughlyfrom BoschandWhite(2004). W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 79

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parameterseitherremainconstantorcyclethroughfixed patternsoverlongperiodsoftime,areeffectivedeposition sitesforasurprisingrangeofminerals.Hill(1976) described74mineralsmainlyfromcavesintheUnited States.By1997whentheexpanded CaveMineralsofthe World reachedasecondedition(HillandForti,1997),the numberofidentifiedcavemineralshadreached255.Very fewoftheseoccurinsufficientvolumetobeimportantas cavesediments. Ionsthatoccurcommonlyincarbonategroundwaters andwouldbeavailablefortheformationofcaveminerals areCa 2 ,Mg 2 ,Na ,HCO 3 ,andSO 4 2 ,plus,ofcourse, water.Becausecaves,withsomeinterestingexceptions,are oxidizingenvironments,theresultingmineralscanbe describedintermsoftheircomponentoxides.Thesystem wouldbeCaO–MgO–Na 2 O–CO 2 –SO 3 –H 2 O.Because anymaterialobjectcontains100percentstuff,thetotal concentrationsofallcomponentsmustaddupto100 percent.Therefore,thenumberofindependentcompositionvariablesisalwaysonelessthanthenumberof components.Thechemicalsystemofsixoxidesrequires afive-dimensionalspacetoplotthecompositionswhichis difficultonatwo-dimensionalsheetofpaper.Figure4 showsthetopologicalrelations.Ifthecomponentsare selectedfouratatime,thecompositionsofanymineralsin thesesub-systemscanberepresentedinthreedimensions, namelybyplottinganycombinationoffourcomponents ontheapicesofaregulartetrahedron.TheprincipalCaMg-carbonatemineralscanbedisplayedinthisfashion (Fig.5). OfthemineralsplottedonFigure5,onlycalciteandto alesserextentaragonitearesignificantconstituentsofcave sediments.Inspiteofthecommonoccurrenceofcavesin dolomiterocks,dolomiterarelyprecipitatesfromkarst waters.Magnesiumappearseitherasasolidsolutionin calciteorasthefine-grainedhydratedmagnesiumcarbonatemineralsknownasmoonmilk. Thesulfatemineralsrequirethefive-componentsubsystemCaO–MgO–Na 2 O–SO 3 –H 2 Otocoverthe commonminerals.Gypsum,CaSO 4 2H 2 Oisthesecond mostcommoncavemineraland,intermsofsediment volume,isbyfarthemostimportantsulfatemineral. Othersincludeepsomite,MgSO 4 7H 2 Oandmirabilite, Na 2 SO 4 10H 2 O.Botharehighlywater-solubleandare foundonlyinextremelydrycaves.Thestabilityofthese mineralscanbedescribedintermsofthetemperatureand watervaporpartialpressure(White,1997). D EPOSITIONOF C ALCITEAND A RAGONITE Thedepositionofbothcalciteandaragoniteincavesis describedbythedeceptivelysimplechemicalreaction Ca 2 2HCO 3 ? CaCO 3 CO 2 H 2 O 1 Thesamereactionwritteninreversedescribesthe dissolutionoflimestone.Theequilibriumconcentration ofdissolvedcarbonatedependsonthepartialpressureof CO 2 ,thetemperature,reactionsamongthevarious carbonatespecies,andalsoontheionicstrength,other ionsinsolution,andvariouscomplexesthatmayform. Carbonatechemistryisnowunderstoodinconsiderable detailandappearsinavarietyoftextbooks(e.g., Langmuir,1997).TheequilibriumconcentrationofdissolvedCa 2 inasystemopentoCO 2 isgivenby m Ca 2 P 1 3 CO 2 K 1 K C K CO 2 4 K 2 c Ca 2 c 2 HCO 3 1 3 2 Inthisequation, K 1 and K 2 arethefirstandsecond dissociationconstantsforcarbonicacid, K CO 2 isthe Henry’slawconstantforthesolubilityofCO 2 andthe c ’saretheactivitycoefficientsfortheCa 2 andHCO 3 ions.Thesameequationdescribesthesolubilityof aragoniteif K C ,thesolubilityproductconstantforcalcite, isreplacedby K A ,thesolubilityproductconstantfor Figure4.Interconnectionsofthesixoxidecomponentsthat makeupmostcommoncaveminerals. Figure5.Compositionsofthecavecarbonateminerals representedonaregulartetrahedron. C AVESEDIMENTSANDPALEOCLIMATE 80 N JournalofCaveandKarstStudies, April2007

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aragonite.Numericalvaluesfortheconstantsatvarious temperaturesaregivenbyWhite(1988).Calculated solubilitiesforcalciteandaragoniteareplottedinFigure6. ThesolubilitycurvesinFigure6provideamodelfor thechemistryofcarbonatemineraldeposition.Rainwater containsCO 2 attheconcentrationof0.037volumepercent ( logP CO 2 3 43)butessentiallyzerodissolvedcarbonate.Whenrainwaterpercolatesthroughorganic-richsoils, theCO 2 concentrationmayriseashighas10% ( logP CO 2 1).WhentheCO 2 -richwaterreachesthe bedrockitdissolvesthelimestonetakingCa 2 ionsinto solution.Ca 2 -ionconcentrationsmayreachvaluesinthe rangeof400mgL 1 asCaCO 3 asgivenbyequation(2). TheseCO 2 -andCa 2 -richpercolationwatersseepdownwardalongjointsuntiltheyemergefromtheceilingsand wallsofcavepassages.TheCO 2 concentrationincave atmospheresistypicallyabouttentimesthatofthesurface atmosphere( logP CO 2 2 5)sointhisenvironment,the drippingwatersarehighlysupersaturated.CO 2 isdegassed intothecaveatmosphereandCaCO 3 isprecipitated,until (atequilibrium)theconcentrationfallsbacktoabout 100mgL 1 .Becausethecaveenvironmentisusually water-saturated,thesurfacesofthegrowingspeleothems remainwet.Eachsuccessivedropdepositsitssmallloadof CaCO 3 inregisterwiththeionsalreadypresentonthe growingcrystalsurface.Thusindividualcalcitecrystalsin speleothemsinsealedcavestendtobelarge,oftenmuch largerthananythathavebeengrowninthelaboratory. Therateatwhichcalcitedissolveshasbeenthesubject ofahugenumberofinvestigations(forreviewseeMorse andArvidson,2002).Dissolutionratestudiesarepertinent totheinterpretationofcavedevelopment(speleogenesis). Thereverseratesforcalciteoraragoniteprecipitationand thusofspeleothemgrowthatsaturationconditionsfar fromequilibriumtendtofollowthesamelawsascalcite dissolution(withsomesignsreversed)(Reddyetal.,1981). Nearequilibrium,whichistheconditioninmostcave depositionalenvironments,themechanismsaremuchmore complicated.Inorderforcalcitecrystalstogrow,thefeed solutionsmustbesupersaturated.However,ifthesupersaturationistoolarge,newcalcitecrystalswillbenucleated and,insteadofonelargecrystal,thespeleothemwill consistofmanysmallcrystals.CaCO 3 growthrateshave beenstudiedinthelaboratorybycontrollingsupersaturationsandmeasuringgrowthrates(Gutjahretal.,1996). Moreinsightintothedetailsoftheprocessatthe atomicscalehavebeenobtainedbyusingtheatomicforce microscopetoactuallymeasuretherateofgrowthof individuallayerswithinthecrystal(Tengetal.,2000).The agreementisgenerallygoodbetweenlaboratorymeasurements,calculationsofgrowthrate,andgrowthrates directlymeasuredincaves(Bakeretal.,1998).Thetradeoffbetweengrowthratesofindividualcrystalsandthe nucleationandgrowthofmultiplecrystalsresultsin avarietyofmicrostructures(alsocalledfabricsortextures) inspeleothemswhichcanbeexaminedbypolarizedlight microscopyorbyscanningelectronmicroscopy(Frisiaet al.,2000).TracequantitiesofMn 2 orrareearthelements fluoresceundercathode-rayactivation,providingabetter visualimageofgrowthpatternsthanthosethatcanbeseen bywhitelightmicroscopy.Cathodoluminescencemicroscopyhasbeenusedtoobservegrowthpatternsin speleothemsandproduceapaleoclimaticinterpretation (Richteretal.,2004). Ithaslongbeenestablishedthatcalciteisthestable polymorphofCaCO 3 atalltemperaturesunderambient pressures(Carlson,1983).Pressuresof300–500MPaare requiredtostabilizetheorthorhombicaragonitestructure. Inwhatseemstobeadirectviolationofthermodynamics, aragoniteoccurscommonlyincavesforminganthodites, frostwork,aragonitebushes,andbulkstalactitesand stalagmites.Theliteratureonthearagoniteproblemis verylarge(seereviewbyCarlson,1983).Twofactorsseem toberesponsible.Oneisthesensitivityofcalcitenucleation andgrowthtothepresenceofimpurities.Theotheristhe solubilityofaragonitewhich,asametastablephase,must belargerthanthatofcalcite.However,asshownbythe Figure6.Solubilityofcalciteandaragoniteasafunctionof CO 2 pressure.Calculatedfromequation(1)for10 u Cand 20 u C. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 81

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curvesinFigure6,thesolubilityofaragoniteisonlyabout 10%greaterthanthatofcalciteoverawiderangeofCO 2 pressuresatthesametemperature.Indeed,thearagonite curveat20 u Cisalmostcoincidentwiththecalcitecurveat 10 u C.Unlikecalcite,aragonitenucleateseasilyandits growthisrelativelyinsensitivetoimpurities.Itisonly necessarytoinhibitcalcitenucleationsufficientlytoallow thesupersaturationtobuildpastthearagonitesolubility curveandaragonitewillprecipitate.Sr 2 enhances aragonitegrowthbyprecipitatingaSr-richnucleuswith thearagonitestructure.Thisactsasatemplateonwhich aragonitecangrow.Mg 2 haslongbeenknownasacalcite growthinhibitor(Berner,1975),aneffectconfirmedby morerecentdirectmeasurementswiththeatomicforce microscope(Davisetal.,2000). Growthofbulkspeleothems,ofwhichstalagmiteshave beenofgreatestinterest,combinesconsiderationofthe growthofindividualcalcitecrystalswithconsiderationsof precipitation,flowpathsfromthesurfacetothecave,and carbondioxideconcentrationcontrastsbetweenthesoil andthecaveatmosphere.Afurtherconsiderationfornearentranceenvironmentsistheroleofevaporationas acompetitiveprocesswithCO 2 loss.Becausedrip-rate (relatedtoprecipitation)andCO 2 pressurevaryseasonally inmostlocations,speleothemsdevelopanannuallayering withlayersthatvaryintextureandalsosometimesin calcite/aragonitecontent.Therateofgrowthcanbe determinedbydatingthestalagmitelayers,eitherby countingthelayersincontemporarystalagmitesorbyU/ Thdatingofsamplestakenalongthestalagmiteaxis. Typicalvaluesareintherangeof0.01to0.1mmy 1 .The relationshipbetweengrowthrateandstalagmiteshapehas beenmodeledbyKaufmann(2003). Thethickness,texture,andmineralogydependprimarilyonprecipitationasthemostimportantexternal parameter,thusmeasurementofthesequantitiesprovides apaleoclimateindicator.Growthlayeringhasprovided informationfromthepastseveralmilleniawhereconfirmationfromhistoricalrecordsispossible.Suchmeasurementgavearainfallproxyrecordforthepastfive centuriesinMadagascar(Brooketal.,1999).Several thousandyearsofrecordoftheintensityofIndian monsoonswasextractedfromastalagmitefromNepal (Dennistonetal.,2000a).Spectralanalysisofthelayering patternintheShihuaCave,Chinaappearedtotrack climaticcycles(Qinetal.,1999).Olderrecordsarealso possible. D EPOSITIONOF G YPSUM Gypsumdepositionisamatteroftheevaporationof sulfate-bearingsolutions.Nochemistryisinvolved.The reactionis: Ca 2 SO 2 4 2H 2 O ? CaSO 4 2H 2 O 3 Theconcentrationofdissolvedgypsumexactlyinequilibriumwithcrystallinegypsumisgivenby C gyp M gyp K gyp c Ca 2 c SO 2 4 1 2 4 C gyp istheconcentrationofdissolvedgypsuming/L,M gyp isthemolecularweightofCaSO 4 2H 2 O, K gyp isthe solubilityconstantforgypsumandthegammasarethe activitycoefficientsforcalciumandsulfateions. M gyp 172.17atomicmassunits.Thesolubilityofgypsumdoes notdependonpHorCO 2 pressurebutdoesvarywith temperature.Otherionsinsolutionaffectgypsumsolubilitythroughtheactivitycoefficients. K gyp asafunctionoftemperatureisgivenby log K gyp 68 2401 3221 51 T 25 0627log T 5 Equation(5)istakenfromLangmuirandMelchior(1985). Inthisequation, T istheabsolutetemperatureinkelvins. Atthestandardreferencetemperatureof25 u C,the calculatedvalueislog K g yp 4 581,avaluethathas beenacceptedbyseveralcontemporarytextbooks(e.g., Langmuir,1997;Drever,1997).Thisnumberisbasedon directsolubilityexperimentsandisrecommendedagainst othervaluesthathavebeencalculatedfromthermodynamicdata. Thesourcesofgypsumincavesvarydependingonthe specificcave.Sourcesthathavebeenidentifiedinclude: N Dissolution,transport,andredepositionofgypsumbeds thatoccurinterbeddedwiththecarbonateunits. N OxidationofH 2 Stosulfuricacidfollowedbyreaction oftheacidwiththelimestonetoformgypsum.Thisis thesourceofgypsuminsulfuricacidcaves. N Oxidationofpyrite,FeS 2 ,thatoccursdispersedinthe limestonefollowedbyreactionwiththelimestoneto formgypsum. N Oxidationofpyritefromoverlyingstratafollowedby transportofsulfate-bearingsolutionstothecavewhere reactiontogypsumtakesplace. Residualgypsumisakeypartofthemechanismforthe formationofsulfuric-acidcaves(Hill,1987,1990).Thus far,gypsumhasnotbeenfoundtocontainanysignificant paleoclimaticrecord.Anothersulfatemineral,alunite, KAl 3 (SO 4 ) 2 (OH) 6 ,hasbeenfoundtoretain 40 Arfrom thedecayof 40 Ksothat 40 Ar/ 39 Ardatingofthealunite fromCarlsbadCavernsandotherGuadalupeMountain caveswaspossible(Polyaketal.,1998).Agesrangedfrom 3.89MainCarlsbadCaverntotheoldestandhighestcave examined,CottonwoodCave,at12.26Ma. I CE Seasonaliceformsinmanycaveswherewinter temperaturesfallbelowfreezing.Oftentheicetakesthe formofspectacular,iftransient,speleothemsnearcave entrances.Caveswithperennialicearelesscommonand C AVESEDIMENTSANDPALEOCLIMATE 82 N JournalofCaveandKarstStudies, April2007

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usuallyoccuronlyathighaltitudes.FossilMountainIce CaveinWyomingisanexampleintheUnitedStates.Best knownarethebigicecavesoftheEuropeanAlpssuchas theEisriesenweltandtheRieseneisho ¨hleinAustria.Some ofthebestpaleoclimaticrecordshavebeenrecoveredfrom icecoresdrilledinthecontinentalglaciersofGreenlandor Antarctica.Itwouldseemthatdrillingtheperennialicein anicecavewouldbevaluable.StudieshavebeenundertakenintheSca ris oaraicecaveintheApuseni MountainsofRomania(Racovita andOnac,2000) (Fig.7). R ESISTATES :I RONAND M ANGANESE O XIDES Amongthemorewidespreadminorcavesedimentsare theoxidesandhydroxidesofironandmanganese.These compoundsarehighlyinsolubleinneutralpHwaterandso areknownasresistates. Goethite(FeOOH),ferrihydrite(Fe(OH) 3 )andother hydratedandhydroxylatedironoxidesoccurwidelyin caves.GoethiteisusuallycrystallineattheX-raydiffractionscalebuttheotherironoxidesandhydroxidesare usuallynon-crystallineattheX-rayscale.Speleothemsof ironhydrateshavebeenfoundandarewelldevelopedin Rohrer’sCave,LancasterCounty,Pennsylvania(Whiteet al.,1985)(Fig.8). Blackcoatingsthatoccurwidelyonstreamsediments areusuallydescribedasmanganeseoxide.Usuallythe manganeseoxidesappearonlyasthin( 1mm)coatings althoughthickerandmoremassivedepositsoccur. Althoughatleastninemanganeseoxidemineralshave beenreportedfromcaves(HillandForti,1997),mostof theidentifieddepositsarecomposedofbirnessite,the d polymorphofMnO 2 ,butwithacompositionapproximately(Na,Ca,Mn 2 )Mn 7 O 14 2.8H 2 O.Themanganese oxidesactasscavengersforheavymetals.Concentrations frompartspermilliontomorethanonepercentofZn,Cu, Ni,Co,V,andCrhavebeenfound.Likewise,rareearth elementshavebeenfoundinmanganeseoxidedeposits (Onacetal.,1997).Depositionofthemanganeseoxide mineralsrequiresoxidationofMn 2 inthecavewaterto Mn 4 ,aprocessthatislikelymicrobiallymediated(Teboet al.,1997;NorthupandLavoie,2001). Figure7.Icespeleothems,Sca ris oaraIceCave,Romania. Figure8.Ferrihydritespeleothems,RohrersCave,Pennsylvania. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 83

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A GE M EASUREMENTSON C AVE S EDIMENTS Thewidespreadinterestincavedepositsaspaleoclimate archivesarisesbecauseofwell-developedandreliable methodsforassigningdatestothedeposits.Different sedimentsprovidedifferentinformationanddifferent methodsareusedtodatethem.Thesectionsthatfollow giveashortsummaryofthemostimportantofthedating techniques. C ARBON 14 Spallationof 14 Nbycosmicraysintheupper atmosphereproducestheradioactiveisotopeofcarbon, 14 C.The 14 Cisoxidizedto 14 CO 2 whichthenmixeswith other 12 CO 2 intheloweratmospherethusproducing aconstantradioactivecomponent.Thesameconstant radioactivebackgroundispresentinplantswhichgrowby extractingCO 2 fromtheatmosphere.ThebasisforC-14 datingisthatwhenplantsdie,theexchangeofCO 2 with theatmosphereceases,theincorporated 14 Cbeginsto decayaccordingtoits5730yearhalf-life.Measurementof theresidual 14 Cinwoodandcharcoalthenallowsthe calculationofthetimethathaselapsedsincethewoodor charcoalwaspartofagrowingplant.Theusualtimelimit forC-14datingisabouttenhalf-livesor50,000years,but therearemanycorrectionsandcaveatstothecalculationof dates(Tayloretal.,1992). Thecalciteinspeleothemsisderivedfromlimestone dissolvedatthesoil/bedrockcontactabovethecavefor whichthechemicalreactionis CaCO 3 CO 2 H 2 O ? Ca 2 HCO 3 6 Inthecavethecalciumandbicarbonateionsare recombinedtoprecipitatecalciteinthegrowingspeleothem.Halfofthecarbonintheprecipitatedcalcite comesfromCO 2 andtheotherhalffromtheCaCO 3 inthe limestone.TheCO 2 isderivedpartlyfromtheatmosphere andpartlyfromthedecompositionoforganicmaterialin thesoil.Theorganicmaterialoriginatedaslivingplants andthusalsocontainsthebackgroundconcentrationof 14 C.Onemightexpect,therefore,thatthecarboninthe bicarbonateionsthatformspeleothemsshouldconsistof abouthalfyoungcarbonfromtheatmosphereandsoil CO 2 andhalfold,dead,carbonfromthelimestone.C-14 datingofspeleothemsshouldthereforebepossibleby takingaccountofthefractionofyoung,zeroage,carbonin thecalcite. Theisotopicchemistryofcalcitedepositionismore complicated.Thereiscarbon-isotopeexchangeinthesoil andinthedissolutionanddepositionprocesses.Asaresult, speleothemstypicallycontainabout85%youngcarbon, acircumstancethatactuallymakesC-14datingalittle easier.TherehavebeenrelativelyfewC-14datesof speleothems.Onecriticalcomparisononspeleothemsin theLobatseIICave(Holmgrenetal.,1994)showedthatC14datescomparedwellwithU/Thdatesbackto20,000 years. U/T H D ATINGOF S PELEOTHEMS U/Th-datinghasbecomethegoldstandardforspeleothemdating(Doraleetal.,2004;RichardsandDorale, 2003).Thecommonuraniumisotope, 238 U,undergoes alongandcomplicateddecaychainbeforereachingthe stableisotope 206 Pb(seeFigure1inField,2007).Along thatchainofmostlyshort-livedintermediatesaretwolonglivedisotopes, 234 U(halflife 248,000years)and 230 Th (half-life 75,200years).Measurementoftheratioof 234 U/ 238 Uand 230 Th/ 234 U,assumingnothoriuminthe initialsample,allowsthecalculationofanage.What makesU/Thisotopedatingparticularlyusefulforcalcite speleothemsisaquirkinthegeochemistryofthesetwo elements.Bothuraniumandthoriumhave4 valence stateswhichproducecompoundsthatarehighlyinsoluble. Uraniumalsohasa6 valencestatewhichusuallyappears astheUO 2 2 ion.Thoriumdoesnot.Theuranylionfurther complexesincarbonatewatersandbecomeshighlymobile (Langmuir,1997).Asaresult,speleothemsoftencontain tenstohundredsofpartspermillionuraniumbutno thorium.Theradiogenicthoriumthataccumulatesinthe calciteisadirectmeasureofthetimeelapsedsincethe calcitewasdeposited. Uranium/thoriumdatingofspeleothemswaspioneered byDerekFord,HenrySchwarcz,andtheirstudentsat McMasterUniversity.Agedatescombinedwithoxygen isotoperatiosanddeuteriumratiosproducedpaleoclimatic recordsforcavesinWestVirginia(Thompsonetal.,1976). Theseearlymeasurementsusedalphaparticlespectroscopy tomeasureuraniumandthoriumisotopeconcentrations, atechniquethatrequiredtensofgramsofsample(Harmon etal.,1975).Manydateswereobtainedbymultiple laboratoriesandapicturewasframedfornorthernNorth AmericaandnorthernEuropeofabundantspeleothem growthduringtheHoloceneandduringtheEemian (Sangamon)interglacial(isotopestage5;100,000–130,000 yearsB.P.).Relativelylittlegrowthoccurredduringthe periodsofglacieradvancement(Hennigetal.,1983; Gascoyne,1992).AlthoughsomeU/Thdatingbyalphacountingcontinues,forexample,thedemonstrationoffour episodesofspeleothemdepositioninlevelIVofthe DemanovaCavesinSlovakia(Hercmanetal.,1997), betterresolutionisnecessarytoprobethepaleoclimate recordsindetail.Thebreakthroughwastheuseofheavy ionmassspectroscopytomeasureisotopeconcentrations (Lietal.,1989).Morepreciseisotopeconcentrations allowedextensionofthedatingrangefrom350,000years foralphacountingtechniquestoapproachingthetheoreticallimitofabout600,000years.Heavyionmass spectroscopyandlateracceleratormassspectroscopyalso reducedtherequiredsamplesizesothatdatescouldbe obtainedfrommilligramsratherthantensofgram quantitiesofspeleothem.Thusastalagmitecouldbe C AVESEDIMENTSANDPALEOCLIMATE 84 N JournalofCaveandKarstStudies, April2007

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sectionedalongitslongaxis,thensampledatclose intervalsalongtheaxistoobtainacompletechronology ofthestalagmiteÂ’sgrowthhistory. P ALEOMAGNETIC C HRONOLOGIES TheEarthÂ’smagneticfieldreversesatirregularintervals duringwhichthemagneticnorthpoleandthemagnetic southpoleexchangeplaces.Intervalswherethenorthpole isnearitspresentlocationarecallednormal;theother intervalsarecalledreversed.Thegeophysicsofthe magneticfieldhavebeenextensivelyinvestigated(e.g., Channelletal.,2004)andageomagneticstratigraphy establishedwellbackintogeologictime.ThepaleomagnetictimescaleshowninFigure9hasbeendrawnonlyfor thepastfivemillionyearssincethisisthetimeintervalof mostinterestinkarstprocesses. Fine-grainedclasticsedimentscontainsmallamountsof magneticminerals.Asthesesedimentssettle,themagnetic grainsrotatetoorientwiththeEarthÂ’smagneticfieldasit wasatthetimeoftheevent.Oncethegrainshavesettled, theirmagneticorientationislockedinplaceandcanbe determinedbycarefulmeasurementofthemagnetic propertiesoforientedsamples.Themeasurementsrequire veryhighsensitivityequipmentbecausethereareonly asmallnumberofmagneticgrainsandmostofthesehave onlyweakmagneticmoments Ifpaleomagneticreversalscanbeidentifiedincave sediments,theyprovidetimemarkersandthusdatesfor sedimentsandthepassagesinwhichtheyoccur.Becauseof thelongtimespansbetweenreversals,themethodisbest appliedtotieredcaveswherethetotalsequenceofcave passagesandtheirsedimentsrepresentequallylongtimes. Withinasinglecavepassage,sedimentsareexpectedtobe stackedintheusualstratigraphicfashionwiththeoldest sedimentsonthebottom.Cavepassages,however,are arrangedintheoppositeorder,withtheyoungestpassages nearpresentdaybaselevelsandolderpassageshigheron theridges(Fig.10).Thisarrangementmustbetakeninto accountintheinterpretationofpaleomagneticdata.The bestsamplesareobtainedfromtheslackwaterfacieswhere thesedimentgrainssettleoutinquietwater.Oftenwhatis availablearethechannelfacies,andthesemayverywell havebeenreworkedbylaterfloodeventssothatthe paleomagneticsignalsarescrambled.Ifacompletesedimentarysequenceisnotavailable,identificationofareversalinasedimentpileinahigh-lyingcaveleavesopenthe questionofwhichreversalisbeingobserved. Paleomagneticstratigraphyhasbeendeterminedfor clasticsedimentsinMammothCave(Schmidt,1982),the cavesoftheObeyRiverGorgeinthewesternCumberland EscarpmentofTennessee(Sasowskyetal.,1995),thecaves oftheCheatRiverGorgeinWestVirginia(Springeretal., 1997),andKookenCave,Pennsylvania(Sasowskyetal., 2004).Becauseoflimitedavailabilityofsensitivemagnetic measuringapparatus,andbecausethereversalsprovide onlywidelyspacedtimemarkers,thismethodofsediment datinghasseenlimitedapplication. C OSMOGENIC I SOTOPE D ATING TheEarthisunderconstantbombardmentbycosmic rays,whichareextremelyenergeticparticlesfromspace. Theseparticlestreamsandtheirspallationproductsfrom collisionsintheupperatmosphere,raindownonthe surfacewheretheycaninducenuclearreactionsinsurface Figure9.GeomagnetictimescalethroughthePliocene. DrawnfromdataofCandeandKent(1995),Berggrenetal. (1995)andSingeretal.(2004).Theprecisedatesforsomeof thereversaleventsarenotincompleteagreementbetween literaturesources.Labelingatbottomgivesthemain paleomagneticperiods(orchrons).Attoparelabeledsome secondaryevents. Figure10.Sketchshowingsedimentstratigraphicrelations intieredcaves.Theschematicsedimentlayersarenumbers fromyoungesttooldest,1to10. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 85

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materials.Thesereactionproductsareknownascosmogenicisotopesandcanbeusedasaninterpretativetool (GosseandPhillips,2001).Theisotopesofimportancefor cosmogenicisotopedatingofcavesedimentsare 10 Be(halflife 2.18Ma)and 26 Al(half-life 1.02Ma).Bothare formedfromthesecondarycosmicrayneutronandmuon bombardmentofquartz, 10 Befromoxygenand 26 Alfrom silicon. Ifquartz,eitheraspebblesorsand,isleftexposed onornearthelandsurface,acertainverytinyconcentrationof 10 Beand 26 Alwillbuildup.Ifsinkingstreamsthen washthequartzsedimentintoacave,thequartzwillbe shieldedfromcosmicraysandtheaccumulated 10 Beand 26 Alwillbegintodecay.Althoughtheinitialconcentrationsofthecosmogenicisotopesarenotknown,theratio oftheconcentrationswillchangesothatthetimesince burialcanbeextracted(GrangerandMuzikar,2001). Carefulsamplepreparationisneededand,because concentrationsaremeasuredinmillionsofatoms,an acceleratormassspectrometerisneededtodeterminethe isotoperatios. Cosmogenicisotopedatingisoneofthemostpromising recenttechniques.Itcoversatimescalebackto5Ma whichisthetimescaleformostactivekarstsystems.The quartzthatisdatedispartofthechannelfaciessediment loadandthesematerialsareusuallydepositedwhenthe cavepassageispartoftheactivedrainagesystem.To areasonableapproximation,thecosmogenicdateofthe sedimentisalsoameasureoftheageofthecavepassage. Byusingcosmogenicisotopedatingofcavesediments,it waspossibletoestablisharateofdowncuttingforriversin theSierraNevada(Stocketal.,2004). T HE P ALEOCLIMATIC R ECORD A VAILABLE A RCHIVES Thestudyofcavesediments,ashasbeendemonstrated above,hascomealongway.Fromabeginningofsimply tryingtounderstandwhyspeleothemshavetheirobserved shapesandmineralogy,investigationsofcavesediments arenowdelvingintosedimentsasarchivesofcritically importantpaleoclimaticinformation.Cavesedimentshave comeintotheirownastheunopenedhistorybookofthe Pleistocene. OfthemainclassesofcavesedimentslistedinFigure1, carbonatespeleothemshavethegreatestinformation content.Clasticsedimentsappearasfacieswhichreflect thehydraulicsoftheflowsystemsthatdepositedthem. Previousepisodesofintensivefloodingcansometimesbe recognized,butclasticsedimentsdonotrecordmuchdetail anddonotprovidemuchtimeresolution.Speleothems,in contrast,aredepositedfromsolutionandthuscarry arecordoftexture,mineralogy,traceelementcontent, andisotopecontent.Datedspeleothemsprovideamicrostratigraphywithaveryhightimeresolution(Perrette, 1999). Cylindrical(broomhandle)stalagmitesarethespeleothemofchoice(Fig.11a).Stalagmitesgrow,layerby layer,aswaterdripsontotheirtops.Astalagmiteof uniformdiameterisevidenceofuniformgrowthrateover longperiodsoftime.Uniformgrowthalsoimpliesuniform dripratesanduniformchemistry.Stalagmitegrowthrates mostlyfallintherangeof0.01to0.1mmy 1 .Ifthereare nobreaksinthegrowth,suchstalagmitesprovidetime spansof100,000yearsto10,000yearspermeterof stalagmite.Moststalagmitesexaminedthusfarhavebeen lessthantwometersinlength.Muchlargerstalagmites exist(Fig.11b).Measurementsonthesestalagmitespose thetechnicalproblemofremovingandlongitudinally sawingthespecimen.Speleothemworkalsoraisesavery seriousethicalquestion:Isthescientificinformation obtainedfromthestalagmiteworththedamagedoneto thecaveinordertocollectit? Becauseannualgrowthlayersinatypicalstalagmiteare fractionsofamillimeterthick,hightimeresolution Figure11.Cylindricalstalagmites.(a)Typeofstalagmites typicallysampledforpaleoclimaticstudies.SitesCave, PendletonCounty,W.Va.(b)LargestalagmitesinFurong Cave,ChongqingProvince,China. C AVESEDIMENTSANDPALEOCLIMATE 86 N JournalofCaveandKarstStudies, April2007

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dependsonmicro-samplesandmicro-analysis.With sufficientmicro-samplingitispossibletoconstruct parameterprofilesalongthestalagmiteaxis,which,of course,isalsoatimeaxis.Quantitiesthathavebeen measuredinclude: N Oxygenisotoperatios N Carbonisotoperatios N Deuterium/hydrogenratios N Traceelements–typicallyMg,SrandBa,andmany others N Layer-to-layercolorvariations(colorbanding) N Layer-to-layervariationsinluminescenceintensity (luminescencebanding) Mostwidelymeasuredaretheisotoperatiosfor 18 O/ 16 O and 13 C/ 12 C.Theoxygenisotoperatioisrelatedto temperatureandiswidelyinterpretedasapaleoclimate thermometer.However,atemperaturecalibrationdepends onspeleothemdepositionunderconditionsofisotopic equilibriumwhichmaynotbeachieved(Hendy,1971; Mickleretal.,2006).Thecarbonisotoperatioisrelatedto thetypeofvegetationonthelandsurfaceaboveandhas beenusedtodistinguishforestfromgrassland. Calcitespeleothemsappearinavarietyofcolorsmostly rangingfromwhitetoshadesoftan,orange,andbrown. Themostcommonsourcesofcolorarehumicsubstances derivedfromtheoverlyingsoil(White,1981).Likewise, speleothemcalciteisusuallystronglyphosphorescent underlongwaveUVexcitationduemostlytothefulvic acidfractionofthehumicsubstances(vanBeynenetal., 2001).Animportantdiscoverymadeinthe1980sbyYavor Shopov(Shopovetal.,1994)isthattheluminescenceis bandedonamicrometerscaleandthattheindividual bandsrepresentanannualcycle.Therehasbeenatremendousamountofinterestinluminescenceandcolor banding.Theseappeartobeameasureofprecipitation, butcalibrationintermsofspecificclimaticvariableshas beendifficult. Therearearangeofpertinenttimescalesandassociated questions.Thesearedealtwithindividuallyinthe followingsections.Foramuchmorecompletediscussion oftheotherpaleoclimaticdataintowhichthespeleothem resultsaremerged,seeBradley(1999). T HE P LIOCENE /E ARLYTO M IDDLE P LEISTOCENE :5M A TO 300ka Muchoftoday’slandscape,includingmostofthecaves andsurfacekarst,hasbeensculpturedduringthepast 5Ma,thatisthePliocene,thePleistoceneandthe Holocene.Nearthebeginningofthisperiodthemild climateoftheEoceneandMiocenegavewaytoaclimatic cyclingfromwarmtocoldandbacktowarmperiods.In highnorthernandsouthernlatitudesandathighaltitudes thesecycleswereaccompaniedbyadvancesandretreatsof glaciers.Sealevelroseandfellassignificantvolumesof waterweresequesteredincontinentalicesheetsandlater releasedastheicemelted.Theclimaticoscillationsoccurin regularcycles:41,000yearsatthebeginningoftheperiod ofoscillationsandswitchingtoa100,000yearcycleabout 800,000yearsago.Thecyclesareknowninconsiderable detailbecauseofdataextractedfromthelongicecores drilledinGreenlandandAntarctica(Fig.12). Eventspriortoabout500,000yearsarebeyondthe rangeofU/Thdating.InformationfromthePlioceneand EarlytoMiddlePleistocenemustbeextractedfromclastic sedimentswhichcanbedatedbycosmogenicisotope methodsandbypaleomagneticreversals.Ataboutthetime thatthe25 th anniversaryissueofthisjournalwasbeing published,Davies’(1960)viewthatmastertrunkcaves wereformedclosetoregionalbaselevelswasbecoming accepted(WhiteandSchmidt,1966).Fossilcavescould,in principle,bedatedbytheirrelationtonearbyriver terraces.However,theevolutionofsurfacevalleysis destructive,withearliervalleyfloorsandchannelsbeing dissectedandlostassurfacestreamscontinuetodowncut. Asaresult,thedatingofterraceswasalwayshighly uncertain.Inrecentyears,thesituationisreversed. Cosmogenicisotopedatingofclasticsedimentinmaster trunkcavesgivesveryaccuratedateswhichcanthenbe appliedtotheterraceleveltowardwhichthecavepassage isgraded. Cosmogenicisotopedatinghasbeenusedtoestablish achronologyforthemaintrunkpassagesinMammoth Cave(Grangeretal.,2001)andformajorcavesinthe westernCumberlandPlateauofKentuckyandTennessee (AnthonyandGranger,2004).Thecaveschosenfordating spantheentiretimeperiodofcaveandkarstdevelopment inthesouth-centralKentuckykarstandtheAppalachian plateaus.Themainconclusionsfromtheseinvestigations aresummarizedinFigure13.Thesestudieshavelockedin atimescaleformostcavedevelopmentintheeastern Figure12.Climaticcyclesoverthepast1.5Mabasedon icecorerecords.FromBrooketal.(2006).Oxygenisotope dataarethebenthicrecord.VostokandEpicaDomeCare icecoresfromAntarctica. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 87

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UnitedStates.ByrelatingtheoldestCumberlandPlateau cavestothedissectionoftheHighlandRimsurfaceat5.7 to3.5Ma,byimplication,thesametimescaleshouldapply tocavesrelatedtotheHarrisburgSurfaceintheValleyand RidgeProvinceoftheAppalachians(WhiteandWhite, 1991). OneoftheeventscommontobothMammothCaveand theCumberlandPlateauwasamassivesedimentin-filling atabout800,000yearsB.P.Suchasedimentationevent implieshighprecipitationandfloodingonthelandsurface above.Thistimeintervalalsocorrespondstothetransition from41,000yearto100,000yearclimaticcycles.Whether thisismerelyacoincidenceorwhetherthecavesedimentationisrecordingtheglobalshiftinclimaticcyclesshould befurtherinvestigated. T HE L ATE P LEISTOCENEAND T HE E EMIAN I NTERGLACIAL TheyoungerendofthePleistoceneliesinthetimerange forU/Thdatingsothatfullusecanbemadeofthe speleothemrecords.Forreference,Figure14givesthe usualtimedivisions.Itwasaperiodofextensiveclimatic variationwithbothglacialandinterglacialperiods. Inareasofcoastalkarst,loweringsealevelsduringthe glacialmaximaallowedthedevelopmentofair-filledcaves thatwerethenfloodedwhentheglacialicemelted.These cavesoftencontainspeleothemswhichcanbeU/Thdated andtheremaybeovergrowthsonthespeleothemsthat depositedafterthecavesre-flooded.Oneofthefirst accomplishmentsofU/Thdatingofspeleothemswasto identifysea-levelloweringduringtheIllinoianglaciation (Gascoyneetal.,1979).Sealevelminimacanbetrackedby datingspeleothemsfromsubmergedcaves(Lundbergand Ford,1994;Richardsetal.,1994).Likewisesealevelstands higherthanpresentsealevelcanbemeasuredbydatingthe overgrowthsthatformunderphreaticconditions(Vesicaet al.,2000). OxygenisotopeprofilesalongTasmanianstalagmites producedanoxygenisotopeprofilefromtheEemian interglacialwellintotheWisconsinglacialperiod(Goedeet al.,1986;Goedeetal.,1990).Theprofileswereinterpreted intermsoftemperaturechangesduringtheperiodof record.Deuterium/hydrogenprofilesobtainedbyextractingfluidinclusionsindatedspelethemstracedtemperature overthepast140kaintheeasternMediterranean (McGarryetal.,2004).Ithaslongbeenarguedthatthe aridregionsoftheNear-Eastweremuchwetterduring interglacialperiods.AspeleothemrecordfromOman showsrapidcalcitegrowthandanoxygenisotoperecord consistentwithhighrainfallat6.5–10.5,78–82,120–135, 180–200,and300–325ka(Burnsetal.,2001).Anoxygen andcarbon-isotoperecordinthreestalagmitesfrom Missouriclearlyshowstransitionsfromforesttosavanna toprairietoforestthroughtheWisconsinglacialperiod,75 to25ka(Doraleetal.,1998). T HE E NDOF T HE L AST I CE A GE :E XTREME C LIMATIC O SCILLATIONS TheendoftheWisconsiniceagewasatumultuoustime withsomeextremeclimaticexcursionsbeforetheclimate settledintothemorestableperiodoftheHolocene. Figure14namestheseperiodsandgivestheirapproximate timeintervals.Itshouldbenotedthatnotallsourcesgive thesametimeboundariesfortheseperiods.Thecold glacialclimateoftheOldestDryasgavewaytoaperiodof warming,butoscillatingclimateintheBlling/Older Dryas/Allerd.Atabout12,900yearsB.P.,accordingto icecoredata(Alleyetal.,1993),thenorthernclimate plungedintoa1300yearcoldperiod,theYoungerDryas, fromwhichitemergedwithanabruptwarmingmarking thebeginningoftheHoloceneat11,640yearsB.P.The transitionfromglacialcoldtopre-borealclimateapparFigure13.Chronologiesforcavesanderosionsurfacesin theMammothCaveareaandtheCumberlandPlateau. InformationcompiledfromGrangeretal.(2001)and AnthonyandGranger(2004). Figure14.Sketchshowingclimateperiodsofthelate PleistoceneandthePleistocene-Holocenetransitionalperiod, theperiodmosteasilyaccessibletoU/Thdating. C AVESEDIMENTSANDPALEOCLIMATE 88 N JournalofCaveandKarstStudies, April2007

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entlyrequirednomorethanadecade.Thelastgaspofthe iceagewasaneventat8200yearsB.P.,anabruptcoldsnap thatlastedforabout200years.Itwasidentifiedinicecores amongotherrecords(Alleyetal.,1997). Muchofthedataonclimaticeventsatthecloseofthe lastglaciationcomefromstudiesatnorthernlatitudes. Thereisalwaysthequestionofhowtheseclimatic excursionsappearedintemperateortropicalclimatesor inthesouthernhemisphere.Theintensecoolingperiodof theYoungerDryasappearedinaspeleothemrecordfrom Australia(Goedeetal.,1996).Climaticfluctuations appearedinspeleothemrecordsfromNewZealand (Williamsetal.,2004).Speleothemtexturecombinedwith traceelementconcentrationsandheavymetalisotopes wereusedtosortoutwet/dryandwarm/coolperiodsinthe SoreqCave,Israel(Ayalonetal.,1999). IntheAmericanSouthwest,therewastheonsetofawet climateat12,500yearsB.P.nearthebeginningofthe YoungerDryas.Basedonstalagmitegrowthasdatedby U/Thmethods,thewetperiodpersistedabout2000years takingitintobeginningoftheHoloceneandendingat 10,500yearsB.P.whentheclimateshiftedtothepresent aridregime(Polyaketal.,2004).The8200yearB.P.event appearedasaweakenedmonsoonintropicalCostaRica accordingtospeleothemdata(Lachnietetal.,2004).Itwas alsofoundasananomalyintraceelementprofilesin astalagmitefromCragCave,southwesternIreland (Baldinietal.,2002) T HE H OLOCENE: 11,650Y EARSTO P RESENT TherewereclimaticfluctuationsduringtheHolocene, buttheseweregenerallylesspronouncedthanthoseatthe endoftheglacialperiod.TheHoloceneisusually consideredtoextendfromabeginningat11,500to 11,700yearsB.P.(variablystatedindifferentsources)to thepresent.ThebeginningdategivenaboveisfromAlley etal.(1993).Shiftsinclimateasreflectedintheoxygen isotopeprofilesofdatedspeleothemshavebeenmeasured forEurope(McDermottetal.,1999),Israel(Frumkinet al.,1999),southernAfrica(Lee-Thorpeetal.,2001),and China(Wangetal.,2005;Zhangetal.,2004). Aseriesofstudiesofcarbonisotopesfromavarietyof cavesintheAmericanMidwesthasallowedthetrackingof vegetationoverthecourseoftheHolocene(R.G.Bakeret al.,1998;Dennistonetal.,1999a;Dennistonetal.,1999b; Dennistonetal.,2000b).Nearlyalltrees,shrubs,andcoolseasongrassespreferentiallyareenrichedinthe 12 Cisotope (C 3 vegetation)whereasgrasslands(C 4 vegetation)contain moreofthe 13 Cisotope.Apatternofshiftsfromforestto grasslandandbacktoforesthasbeendocumented,butthe timingoftheshiftsvarieswithlocation.Generally,thereis goodagreementwithpollenrecords. Measurementof 87 Sr/ 86 Srratiosinaspeleothemfrom Harrison’sCave,Barbados,showedasystemicchange throughtheHolocene(Banneretal.,1996).Thisrecord correlateswithrainfall. T HE H ISTORIC P ERIOD :T HE P AST S EVERAL T HOUSAND Y EARSOF T HE H OLOCENE Anissueofnationalandinternationalimportanceatthe timeofthiswritingisthatofglobalwarming.Itseemsthat ontheaverage,wintershavebecomewarmer,summers hotter,glaciersareretreating,hurricaneshaveincreased intensity,andsealevelsarerising.Ononesidearethose whoassignthesechangestoagreenhouseeffectbroughton bytheanthropogenicincreaseincarbondioxideandother greenhousegasesintheatmosphere.Ontheothersideare somewhoassertthatthewholeideaofhuman-induced globalwarmingisamythandthatthesefluctuationsare partofanaturalcycle.Theimplicationsareenormous. ProlongedwarmingsufficienttomelttheGreenlandand Antarcticicecaps(aswellasotherglacialice)wouldraise sealevels,shiftoceancurrents,drowncoastalcities,and changeatmosphericcirculationpatternssothatproductive farmlandsmightbecomedustbowls.Arehumanbeings creatingadisasterorarewesimplyridingyetanother climaticcycle,thisoneonacenturiestimescale? Climatehasindeedoscillatedoverthepastseveral millenniawithaperiodofoscillationofseveralcenturies (Fig.15).Thewarmclimatesduringthefloweringofthe RomanEmpiregavewaytocoldclimatesinEuropeduring whatisknownastheDarkAges.Climatewarmedagain duringtheMedievalperiodandthenshiftedintowhat historicallyhasbeencalledtheLittleIceAge.Sincethelate 19 th Century,climateinNorthAmericaandEuropehas beenwarming.The‘‘grandfatherwinters’’arefadingfrom memory. Thereissomeaccumulatingevidencethatthesemore subtlerecentclimaticeventscanbeteasedfromthe speleothemrecord.Spikesinthe 13 Crecordinastalagmite fromBelizeovera30yearperiodfrom1970to2000 correlatedwiththesouthernoscillationindex–ameasure ofElNin oevents(Frappieretal.,2002).Oxygenisotope profilestakenfromthreestalagmitesfromacavein southernOmanprovideda780yearrecordofmonsoon activity.Therecordrevealedthetransitionfromthe MedievalWarmPeriodtotheLittleIceAgeatAD1320 (Fleitmannetal.,2004).SpeleothemrecordsfromSouth AfricaindicatethattheLittleIceAge,whichextended fromroughlyAD1300to1800,wasabout1 u Ccoolerthan presentwhiletheMedievalWarmPeriodmayhavebeen 3 u Cwarmer(Tysonetal.,2000).Theboldestproposalhas Figure15.Sketchshowingclimateperiodsforthehistorical periodasrecordedinEurope.Theboundariesarenotsharp andvarysomewhatbetweenregions. W ILLIAM B.W HITE JournalofCaveandKarstStudies, April2007 N 89

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beentocalculatea3000yeartemperaturerecordfrom stalagmitecolorbandingfromSouthAfrica(Holmgrenet al.,2001).Whatisneeded,andwhatmoreaccurately calibratedspeleothemrecordsmayprovide,isanassessmentofwhetherthepresentdaywarmingiscomparableto otherwarmperiodsofthepastseveralmillennia,or whetherweareenteringanew,andpossiblyquite dangerous,climaticregime. C ONCLUSIONS Cavesedimentshavethepotentialforproviding detailedpaleoclimatearchiveswithvaluecomparableto icecoresanddeepseasedimentcores.Techniquesfor establishingaccuratedatesonhighresolutionrecordsin speleothemsareinplaceforthetimescalefromthelate Pleistocenetothepresent.Cosmogenicisotopedatingof clasticsedimentsextendsthemeasurabletimescalebackto theearlyPliocenebutwithmuchlesstimeresolution.The problemremainsofestablishingreliablerelationships betweenmeasurableparameters,traceelementprofiles, isotopeprofiles,colorandluminescenceprofiles,andthe actualclimaticvariablesforwhichthemeasurementsare aproxy(McDermott,2004). Climate,asrecordedincavesediments,isverymuch amatterofthelocalclimateintheimmediatevicinityofthe cave.Inordertoobtainabroaderregionalorevenglobal pictureofclimateatsometimeinterval,manymoredata areneeded.Cavesediment–paleoclimatestudiesarein theirinfancy. A CKNOWLEDGEMENTS Thispaperisareviewandsodrawsontheworkofmany investigatorsasindicatedbytheextensivereferencelist. SpecificcavesedimentresearchatPennStatewas supportedbytheNationalScienceFoundationandby theArmyResearchOffice.ElizabethKnappandEvan Hartarethankedfortheircarefulandthoughtfulreviews. R EFERENCES Alley,R.B.,Meese,D.A.,Shuman,C.A.,Gow,A.J.,Taylor,K.C., Grootes,P.M.,White,J.W.C.,Ram,M.,Waddingon,E.D., Mayewski,P.A.,andZielinski,G.A.,1993,Abruptincreasein GreenlandsnowaccumulationattheendoftheYoungerDryas event:Nature,v.362,p.527–529. Alley,R.B.,Mayewski,P.A.,Sowers,T.,Stuiver,M.,Taylor,K.C.,and Clark,P.U.,1997,Holoceneclimaticstability:Aprominentwidespreadevent8200yrago:Geology,v.25,p.483–486. 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GROUNDWATERRESIDENCETIMESINUNCONFINED CARBONATEAQUIFERS S TEPHEN R.H.W ORTHINGTON WorthingtonGroundwater,55MayfairAvenue,Dundas,Ontario,Canada,L9 H3K9,sw@worthingtongroundwater.com A BSTRACT : Tracershavebeenwidelyusedinunconfinedcarbonateaquiferstomeasure groundwatervelocitiesandtraveltimes.Injectedtracershavelargelyb eenusedto measuretraveltimesfromsinkingstreamstosprings.Environmentaltrac ershavelargely beenusedtoestimateoverallresidencetimesinanaquifer,andgivetimes thatare typicallyonehundredtimeslongerthanestimatesfrominjectedtracers. Useofboth environmentalandinjectedtracershasenabledresidencetimesandstora gevolumestobe calculatedforbothdiffuseandconduitcomponentsinanumberofaquifers .Withthe additionofpermeabilitydataitispossibletocalculatestorageandflow componentsfor thematrix,fractureandchannelcomponents.Resultsshowthatthematrix oftherock providesalmostallstorage,buthasverylongresidencetimes,especiall yinolder carbonates.Channelsprovidelittlestorage,accountformostoftheflow ,andhavevery shortresidencetimes.Fracturesplayanintermediaterolebetweenthema trixand channelsandhavelowstorageandmoderateresidencetimes.Thesesamecon trastsare foundinmanydifferentaquifersandarelikelytobefoundinallunconfine dcarbonate aquifers.Thustheseaquifersaremarkednotsomuchbyrangingfromcondui tflowto diffuseflowtypes,butratherinhavingtripleporositywithcontrasting flowandstorage propertiesinthematrix,fracturesandchannels.Thecombinationofenvi ronmentaland injectedtracersprovidesapowerfultoolforelucidatingthesecontrast ingproperties. I NTRODUCTION Therearewidelydivergentviewsongroundwater residencetimesinunconfinedcarbonateaquifers.Oneview isderivedfromthelonghistoryofmeasuringgroundwater velocities;ithasbeenestimatedthatmorethan90%ofall groundwatertraceshavetakenplaceincarbonates(Quinlan,1986).Suchtestingaswellascaveexplorationhasledto theviewthatmostcarbonateaquifersaredominatedbyflow throughconduits.Acontrastingviewusuallycomesfrom welltests,wheretransmissivityandhydraulicconductivity valuesarebroadlysimilartothosefromsandaquifers. Consequently,manyhydrogeologistsassumethatcarbonate aquifersfunctioninasimilarwaytosandaquifersand behaveasequivalenttoporousmediawiththewater,in general,movingslowlythroughtherock. WhiteandSchmidt(1966)recognizedthatcarbonate aquifershavebothlocalizedflowinconduitsanddiffuse flowthroughfracturesandthematrixoftherock,and Atkinson(1977)calculatedtheproportionsofconduit anddiffuseflowfortheCheddargroundwaterbasinin England.Itappearedtobelogicalthattheremightbe arangebetweencarbonateaquiferswherediffuseflow dominatesandthewaterseepsslowlythroughtheaquifer, andotherswhereconduitflowdominates,andanumberof suchconceptualmodelshavebeenproposed(White,1969; AtkinsonandSmart,1981;SmartandHobbs,1986; Quinlanetal.,1992). Analternativepossibilityisthatbothdiffuseflowand conduitflowarepresentinmost,ifnotall,carbonate aquifers,andthattheperceiveddifferencesarelargely afunctionofthetypesofmeasurementsmade.Thus tracertestsfromsinkingstreamstospringsarean excellentwaytodemonstrateconduitflowwithrapid velocities,whereasaboreholeisunlikelytointersect amajorconduitsopumpingtestresultsgenerallyreflect diffuseflowproperties.Worthingtonetal.(2000)analyzed datafromfourcontrastinglimestoneanddolostone aquifersintermsofflowandstorageinchannels,fractures andthematrix.Theyconcludedthatatleast96%of storageisinthematrixandthatatleast94%offlowis throughchannelsintheaquifersstudied,thusshowing thatwidelydifferentcarbonateaquifersfunctioninsimilar ways. Tracershavebeenveryusefulinhelpingdeterminethe proportionsofmatrix,fractureandchannelflowin carbonates,andthispaperreviewsanumberofstudies withcontrastingresults. I NJECTEDAND E NVIRONMENTAL T RACERS U SEDTO M EASURE T RAVEL T IMES Themostcommontracingincarbonateaquifersis betweensinkingstreamsandsprings,andwelloverten thousandsuchtestshavebeencarriedout.Worthington (1999)compiledthedatafrom2,877suchtests,whichhave anapproximatelylog-normaldistributionwithageometric meanof1,770md 1 .Inthedatasetthereisawiderange indistancetraced,withthemediandistancebeing4,000m and576tracesbeingoverdistancesofatleast10km StephenR.H.Worthington–Ground-waterresidencetimesinunconfinedca rbonateaquifers. JournalofCaveandKarstStudies, v.69, no.1,p.94–102. 94 N JournalofCaveandKarstStudies, April2007

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(Fig.1).Thelargenumberoftracesoverlongdistances withrapidflowclearlyindicatethatextensivenetworksof interconnectedconduitsonascaleofmanykilometersare common. Therehavebeenanumberofstudiesfromdolinesor fromthesurfacetodrippointsincaves10–100mbelow thesurface(FriederichandSmart,1981;Bottrelland Atkinson,1992;Kogovs ek,1997).Tracerarrivaltimesare typicallyminutestohours,butthereiscommonlyhigh dispersionsothatmeanresidencetimesaremuchgreater. Therehavealsobeenanumberoftracertestsbetweenwells andthesetypicallygivetravelarrivalvelocitiesoftensto hundredsofmetersperday.Theexistenceofvelocities 100md 1 fromsinktospring,surfacetoconduitand fromwelltowelltracertestsclearlyshowthatthereare manypathwaysincarbonateaquiferswherethereisrapid flow. Awiderangeofenvironmentaltracershavebeenused todetermineresidencetimes,includingwatertemperature, chemicalvariablessuchastotalhardnessandbothstable andradioactiveisotopes.Samplinginshallowconduitshas shownthataverageresidencetimesinthevadosezoneare typicallymonthsorlonger(Pitty,1968;Yongeetal.,1985). Thesetimesaremuchlongerthanthetracerarrivaltimes frominjectedtracersanddemonstratethelargevariancein residencetime.Similarly,therehavebeenmanytritium measurementsatspringsthathavedemonstratedmean residencetimesofyearswhileinthesameaquiferstracers haveshownflow-throughtimesofdays,andanumberof thesestudieswillbedescribedbelow. Thebroadconclusiontobemadefromallthetracer studiesisthatenvironmentaltracerstendtogivemuch greateraquiferresidencetimesthaninjectedtracers.This apparentanomalycanberesolvedbyaccountingforthe multipleporosityelementsinacarbonateaquifer. C ALCULATIONOF R ESIDENCE T IMESIN C ARBONATE A QUIFERS Asimpleandusefulwaytoconsidercarbonateaquifers isintermsofflowandstorageinone-,two-andthreedimensionalelementsoftheaquifer(Worthington,1999). Theonedimensionalelementshavegenericallybeencalled channels(WorthingtonandFord,1995).Channelswith diameterslessthanafewcentimeterscommonlyprovide mostoftheinflowtoboreholesduringpumpingtests,and incavesarebestseenasthevadoseflowsanddripsthat formstalactitesandstalagmites.Largerchannelsarecalled conduitswhenflowbecomesturbulent,whichiscommonly atathresholddiameterofabout1cm(White,1988,p. 290–293).Cavesarelargeconduitsthatapersoncanenter. Thetwodimensionalelementsincarbonateaquifersare jointsandfaults.Thethreedimensionalelementsarethe matrixblocksthatliebetweenthefractures. Thecalculationofresidencetimesinporous-medium aquifersisstraightforward.Insuchaquifersflowlinesare parallelandparticletrackingnumericalmodelssuchasthe U.S.GeologicalSurveyprogramFLOWPATHcangive estimatesoftravelbetweentwopointsinanaquiferand thereforeofresidencetime.Thecalculationofresidence timesincarbonateaquifersisonlystraightforwardintwo simplesituations.Oneiswherealltheflowisalong aconduitfromasinkingstreamtoaspring.Inthese situationsthereisnomixingbetweenwaterparticlesof differentagesandthusasimplepiston-flowmodelof advectiveflowfromsinktospringprovidesanaccurate model.Thesecondsimplesituationmayoccurwhere rechargeisthroughathickporousmediumoverburden suchassand.Soilisunlikelytobehaveasaporousmedium becauseofpreferentialflowviachannelscausedbyroot casts,animalburrowsordessicationshrinkageofclays.In adowngradientdirectionincarbonateaquifersthereis increasingmixingbetweenwatersthathavefollowed differentflowpathsandthushavearangeofages. Consequently,thevarianceoftheagewillgenerally increaseinadowngradientdirection. R ESIDENCE T IMESFROM E NVIRONMENTALAND I NJECTED T RACERS Therehavebeenanumberofstudieswhereboth environmentalandinjectedtracershavebeenused(Table1).Eachofthesestudiesinvolvedanalysisofanumber oftritiumsamplesaswellasmultipletracesfromsinking streamstosprings. Theeast-flowingDanubeRiverlosesflowatsinkpoints initsbedinsouthernGermany.Tracertestingin1877 usingsaltandthefluorescentdyeuranineshowedthatthe flowcrossestheEuropeancontinentaldivideandresurges 12kmtothesouthatAachSpring,whichisonatributary ofthewest-flowingRhineRiver.Thisspringisthelargest inGermanywithanaveragedischargeof8.5m 3 s 1 ,and Figure1.Ground-watervelocitiesandtraceddistancesfor 2,877sinktospringtracertests. S.R.H.W ORTHINGTON JournalofCaveandKarstStudies, April2007 N 95

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lossesfromtheDanubeaccountforamajorfractionofthe flow(Batscheetal.,1970;Ka ¨ss,1998).Tracingfromthese sinkstoAachSpringgavetraveltimesof2.5to13d,with thetraveltimebeinginverselyrelatedtodischargeatthe spring.However,tritiumanalysesgaveameanresidence timeof6to14yr.Theageofwaterattwomajorsinkson theDanubeis2to6yrand6to14yr,respectively(Batsche etal.,1970),sotheactualresidencetimeintheaquiferof theoldcomponentofflowisuncertain. TheAreuseSpringintheSwissJuraMountainshas ameanflowof4.7m 3 s 1 .Tracertestsfromfivesinking streamstothisspringhelpeddelineatethecatchmentarea andgiveconduitvelocities.Tritiumanddischargemeasurementsshowedthattherapidcomponentofflowwas 20%oftotaldischarge,withtheremaining80%of dischargehavingameanresidencetimeof9monthsto 2yr(Mu ¨llerandZo ¨tl,1980). InthePeloponnesepeninsulainGreecethereareaseries ofenclosedbasinswithlargesinkingstreams,surrounded bymountainsthatriseupseveralhundredmeters.The meanresidencetimeofmorethan80springsinthisarea wasdeterminedfromtritiumsamples,withmostsprings havingresidencetimesintherangeof2to10yr(Morfis andZojer,1986).Someofthelargerspringswereselected forintensivetritiumsampling.Forinstance,monthly sampleswerecollectedatKiveriSpringforaperiodof threeyearsandafurther14sampleswerecollectedduring athreemonthperiodwhiletracertestswerebeingcarried out.KiveriSpringisacoastalspringandisoneofthe largestspringsinGreece.Sixinjectedtracerswererecoveredatthisspring,withflowpathsof3–42kmand muchfastergroundwatervelocitiesthanthetritium indicated(Table1).Therewassimilarintensivesampling atspringsatStymfalia,Ladon,andKefalariwhichyielded groundwateragesof5yr,4.5yr,and4yr,respectively. Injectedtracersrecoveredatthesethreespringsdaysto weeksafterinjectiongavesimilarresultstoKiveri,with mosttracersgivingvelocities 1000md 1 (Morfisand Zojer,1986). TheVaucluseSpringisthelargestspringinFranceand hasagroundwatercatchmentofabout1,100km 2 .The springhasbeenexploredtoadepthof 308mbyaremoteoperatedsubmersiblevehicle(MudryandPuig,1991). Tritiummeasurementsatthespringhaveshownthatthere isamixtureofwaterofdifferentages;athighflowsrecent precipitationpredominates,whileatlowflowthereis alargecomponentofwaterwitharesidencetimeofmore than30yr.Similarlylongresidencetimeshavealsobeen measuredinboreholesinthecatchmentarea(Puig,1990). Theshortresidencetimecomponenthasbeendemonstratedbyseventracertestsoverdistancesof23–46km,where tracerresidencetimeshavevariedfrom2weekstoseveral months(CouturaudandPuig,1992). Ho ¨llochisthelongestcaveinWesternEurope,with amappedlengthof190km.Therehavebeenextensive studiesofthecaveanditshydrology(Bo ¨gliandHarum, Table1.Groundwatervelocitiesfrominjectedandenvironmentaltracers Location No.of 3 H samples Meanflowpath length(km) Residencetime 3 H(years) Velocityfrom 3 H(md 1 ) Traced distance(km) Velocityfrom injectedtracer (md 1 )Reference Aach,Germany109102.512–181000–4800Batscheetal.,1970 Areuse,Switzerland2360.75–28–226–14350–4800Mu ¨llerandZo ¨tl,1980 Kiveri,Greece40152203–42160–4300MorfisandZojer,1986 Vaucluse,France573010823–46200–2300Puig,1990;MudryandPuig,1991; CouturaudandPuig,1992 Ho ¨lloch,Switzerland2450.5–1.7 a 80.4–11600–5300Bo ¨gliandHarum,1981;Jeannin etal.,1995 a Fromboth 2 Hand 3 H G ROUND-WATERRESIDENCETIMESINUNCONFINEDCARBONATEAQUIFERS 96 N JournalofCaveandKarstStudies, April2007

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1981;Jeanninetal.,1995;Jeannin,2001).Measurements withdeuteriumandtritiumgaveestimatedmeanresidence timesof1.6yrand1.7yr,respectively,forthelong residence-timecomponentwhichaccountedforaminimum of30%oftotaldischarge.Deuteriumgaveamean residencetimeof6monthsforthetotalspringflow,and tracertestsgaveresidencetimesof10htoaweek. Theresidencetimesandvelocitiesoftheabove fivestudiesaresummarizedinTable1.Thetritium analysesgaveanageforthegroundwaterthatyielded anaveragevelocityof2–22md 1 whereastheinjected tracersgavevelocitiesthatwereaboutonehundredtimes faster. RecentstudiesatWakullaSpring(Florida)havegiven anevenlargercontrastbetweentheresultsofthetwo techniques.Environmentaltracersgaveagroundwater residencetimeageof39yearsfrom 3 H/ 3 Heanalysis,and Katz(2001)suggestedthatsuch 3 H/ 3 Hedating‘‘provides arealisticassessmentofthesusceptibilityoftheUFA [UpperFloridanAquifer]tocontaminationbyapproximatingthetraveltimeforcontaminantstoreachaparticularzoneintheaquifer.’’Thisinterpretationisbasedon theassumptionthattheaquiferbehavesasaporous medium.However,recenttracertestingwithfluorescent dyesfromthesinkingstreamsofMunsonSlough,Fisher CreekandBlackCreekhasgivengroundwateragesof justdaystoweeks(Loperetal.,2005).Thisconfirmsthat theaquiferbehavesasadoubleortripleporosityaquifer ratherthanasingleporosityporousmediumaquifer. Additionallytherehasbeenextensivecaveexploration upstreamfromWakullaSprings,whichhaveamean dischargeof11m 3 s 1 (Wisenbaker,2006).Thecombinationofthemassivedischargefromasinglelocationandthe caveexplorationgivesfurtherinformationontheconduit fractionofflow. Theverylargedifferencesbetweengroundwaterages frominjectedtracersandenvironmentaltracersinallthe abovestudiesarecomplementaryratherthancontradictory becausetheymeasuredifferentaspectsoftheporosity.The tracersinjectedintosinkingstreamsandrecoveredat springsgivevelocitiesandresidencetimesofconduitflow, thefastestcomponentofflowthroughtheaquifer.The environmentaltracersgiveanaverageageofthegroundwater,includingnotonlytherapidflowcomponent throughconduits,butalsotheslowflowcomponent throughthematrixandfracturesinthebedrockaswell asthesoilandepikarst. Thecombinationofenvironmentalandinjectedtracers intheabovestudiesclearlyshowsthattherearemultiple residencetimesincarbonateaquifersandthatresidence timeisafunctionoftheparameterbeingmeasured.There havebeenanumberofstudiesthathaveconsideredthe volumesandresidencetimesofthedifferentporosity componentsincarbonateaquifers,andonesingle-porosity, threedouble-porosity,andtwodouble-porositymodelsare discussedbelow. R ESIDENCE T IMESAND S TORAGE V OLUMESIN S INGLE-AND D OUBLE -P OROSITY M ODELS JordtullaCaveisanalmoststraight580mlong submergedconduitinPaleozoicmarblethatdrains GlomdalLakeinNorwayandprovidesanexampleof asimplesinktospringconduit.Thecavesurveyshowed theconduitvolumesis1.35 3 10 4 m 3 andcontinuous dischargemeasurementsoveraperiodof20monthsgave ameandischargeof2.5 3 ms 1 (Lauritzenetal.,1985; Lauritzen,1986).Themeanresidencetimeoftheflow throughtheconduitisthus13,500/2.5sor90min.This calculationignoresthegainalongtheconduitfrom autogenicrechargefrommatrix,fractureorconduitflow. Theautogeniccatchmentis2.6%ofthetotalcatchment andtheproportionsofflowthroughtherockmatrix, fractures,orchannelshavenotbeenmeasuredor calculated.Thematrixflowislikelytobeextremelylow inthislow-porositymarble,soitislikelythatalmostall autogenicrechargeflowsrapidlythroughfracturesand channelsandconsequentlymayalsohaveashortresidence time.Residencetimeintheconduitisinverselyproportionaltodischarge,whichvariessubstantiallyinthis mountainoussubarcticenvironment.Theresidencetime hasbeenmeasuredbymorethanfortytracesatflows between1m 3 s 1 and10m 3 s 1 (Lauritzen,1986;Smart andLauritzen,1992).Atextremeflowsof0.1m 3 s 1 and 50m 3 s 1 thecalculatedresidencetimeis38hand4.5min, respectively. TheCheddarSpringshaveameandischargeof 0.73m 3 s 1 anddrainanestimated39km 2 oftheMendip HillsinEngland,andbothconduitandnon-conduit fractionsofflowandstoragewerecalculatedbyAtkinson (1977).Thelagbetweenthearrivalofafloodpulseandthe arrivaloflow-conductivitysinkingstreamwaterwasused toestimateaconduitvolumeof1.1 3 10 5 m 3 .Integration ofthedischargerecessioncurvegaveabaseflowstorageof 3.3 3 10 6 m 3 ,showingthatconduitsonlyaccountfor3%of totalstorage.Anon-conduittransmissivityof0.031m 3 s 1 wascalculatedfromthebaseflowrecessionandfromthe storagecoefficient,whichenabledthefractionofnonconduitflowof30%tobeestimated,withtheremaining 70%offlowbeingthroughconduits(Atkinson,1977). Theresidencetimefornon-conduitflowcanbecalculatedbydividingthenon-conduitvolumebythedischarge of0.22m 3 s 1 ,givinganaverageresidencetimeof170d. Similarly,theaverageresidencetimesforconduitflowcan becalculatedbydividingtheconduitvolumebythe conduitdischargeof0.51m 3 s 1 ,givingaresidencetimeof 2.5d.Thegroundwatercatchmentis10kminlengthso thistimewouldrepresentanaveragevelocityof2kmd 1 overanaverageflowpathlengthof5km.Smart(1981) carriedoutrepeattracingalongtheLongwoodSwalletto CheddarSpringsflowpathandfoundthatconduitvelocity wasdirectlyproportionaltodischargeandrangedfrom 110md 1 to6400md 1 ,with13ofthetracesexceeding S.R.H.W ORTHINGTON JournalofCaveandKarstStudies, April2007 N 97

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2kmd 1 and11tracesbeinglessthan2kmd 1 .Thusthe repeattracinglendscredencetotheestimateofconduit volumebyAtkinson(1977). TheHo ¨llengebirgeintheNorthernLimestoneAlpsof Austriaareahighmountainrangewithautogenicrecharge.Seasonaldischarge, 18 Ovariationsandlow-flow tritiumconcentrationswereusedtocalculatestorage volumesandresidencetimesforconduitandnon-conduit flowandstorage(Benischkeetal.,1988).Resultsshowed thatconcentratedrechargeandrapidflowthrough conduitsaccountedfor72%offlow,butthisonly accountedfor4%ofaquiferstorage. TheCentralStyrianKarstinAustriahasamajor sinkingstream,theLurbach,aswellasalimestoneplateau withautogenicrecharge.Thesinkingstreamaccounts for64%ofthespringdischargeof0.29m 3 s 1 .Conduit volumewascalculatedfromthespringdischargebetween tracerinjectionandrecoverytimesduring17repeattracer tests,andnon-conduitstoragewascalculatedfrom29 tritiummeasurementsfromsamplescollectedoveraperiod oftwoyears(Behrensetal.,1992). Theresultsfromthefourareasdescribedaboveare summarizedinFigure2.Thethreedouble-porositymodels givebroadlysimilarresults,with4%orlessofstorage beinginconduits,butmostoftheflowbeinginthem. Therearealsosomesubstantialdifferences.Thesmall conduitvolumeintheStyriankarstisbecausethe calculationisonlyofthemainconduitfromtheLurbach sinkingstreamanddoesnotincludeconduitsinthe autogenicfractionofthecatchment.Thelargedifferences inmatrix/fractureresidencetimesareprobablyatleast partlyduetothedifferencesinthemethodofcalculation, withthetwoAustrianexamplesusingtritiumandCheddar usingbaseflowrecession.However,allthreedoubleporositymodelsshowthatconduitresidencetimesare ordersofmagnitudelessthannon-conduitresidencetimes. R ESIDENCE T IMESAND S TORAGE V OLUMESIN T RIPLEP OROSITY M ODELS Triple-porositymodelscanpotentiallygiveamore accuratepicturethandouble-porositymodelsofgroundwaterresidencetimesincarbonateaquifers,andtwo examplesareshowninFigure3,theManavgatRiver basininTurkeyandtheTurnholeSpringbasinin Kentucky. TheManavgatRiverbasindrainsatopographicbasin of928km 2 andinadditionseveralclosedbasins,givingan estimatedtotaldrainageareaof9,100km 2 (Yurtseverand Payne,1986).Thisareahasboththelongestgroundwater tracesandoneofthelargestspringsintheworld (Bakalowicz,1973;Chabert,1977;KaranjacandGunay, 1980).Atotalof41tritiumsampleswerecollectedbetween 1963and1980attheOymapnargaugingstation,where long-termdischargerecordsareavailable.Tritiumconcentrationswerefoundtovarybymorethananorderof magnitude,withthemaximumof684tritiumunitsbeing measuredinasamplecollectedinApril1963.Partofthe variationovertimewasduetodecreasingatmospheric concentrationsfollowingthecessationofatmospheric nuclearweaponstesting,buttherewasalsoafactorof fourvariationinconcentrationbetweenhigh-flowandlowflowperiods.Fromrecessioncurveanalysis,Yurtseverand Payne(1986)inferredthatthereweretwostorageelements intheaquiferwithaverageresidencetimesofabout3 monthsand9months,respectively,plusabaseflow componentwithalongerresidencetimeandadischarge of29m 3 s 1 .Best-fitanalysistomatchmodeledandmeasuredtritiumvaluesgavemeanresidencetimesof2 months,9monthsand12yrforthethreecomponentsof Figure2.Oneandtwo-boxmodelsforcarbonateaquifers, withfractionofstorage(inpercentage)andresidencetimein eachboxandflowin(m 3 s 1 )betweenboxes.Seetext fordetails. G ROUND-WATERRESIDENCETIMESINUNCONFINEDCARBONATEAQUIFERS 98 N JournalofCaveandKarstStudies, April2007

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flow,with86%ofstoragebeinginthelongresidencetime component(Figure3). TheTurnholeSpringbasindrainsanareaof217km 2 includingpartofMammothCave(QuinlanandEwers, 1989).Worthingtonetal.(2000)calculatedmatrix,fracture andchannelfractionsofflowandstorage.Matrixporosity andhydraulicconductivityweremeasurefromcoreand handsamples.Fracturehydraulicconductivitywasdeterminedbypumpandslugtestsinboreholes,andfracture porositywascalculatedfromestimatedfractureapertures. Channelporositywasdeterminedfromthelagbetweenthe arrivalofafloodpulseandthearrivaloflow-conductivity sinking-streamwaterandfromtracer-testvelocities. Channelflowwasdeterminedfromrunoffcalculations. Finally,theeffectiveaquiferthicknesswasestimatedfrom theloopingofcavepassagesinMammothCave,whichare upto23mbelowthecontemporaneouswatertable. Resultsgave96–97%ofstorageinthematrixoftherock (Worthingtonetal.,2000).However,thestudyonly consideredbedrockstorageandflow,andsoilandepikarst propertieswerenotincluded.Gunn(1986a,b)showedthat suchstoragecanbeaconsiderablefractionoftotalstorage wherethereisthicksoiloroverburdenaboveacarbonate aquifer.Thedepthofsoilandmoisturecontentinthe TurnholeSpringscatchmenthavenotbeenmeasured,but anestimated300mmofstoragewouldhaveamean residencetimeof6monthsandwouldthenaccountfor 35%oftotalstorageinthegroundwaterbasin(Fig.3). R ESIDENCE T IME D ISTRIBUTIONSOF F LOWAND S TORAGE Fromtheabovestudiesitispossibletoestimate residencetimedistributionsfortherespectiveaquifers. However,therearetwoverydifferentdefinitionsof residencetimedistribution(Worthingtonetal.,2000). Theseare T r T m R m T f R f T c R c 1 T s T m S m T f S f T c S c 2 where T isresidencetime, R isrechargetotheaquifer, S is thestorageintheaquifer,thesubscripts m,f ,and c referto matrix,fractureandchannel,respectively; T r isthe residencetimeofwaterrechargingtheaquifer,and T s is theresidencetimeofthewaterwithintheaquifer.Thethree componentsof R and S aredimensionlessfractions,the sumofwhicharebothunity. JordtullaCaveandtheTurnholeSpringbasinarethe simplestandmostcomplicatedmodels,respectively,ofthe examplesthatareshowninFigures2and3.Residence timedistributionsforthemwerecalculatedusingEquations1and2andassumingthattheresidencetimeofeach flowcomponentinthebedrockhasalog-normaldistribution.Examplesoflog-normaldistributionsincludethe tracervelocitydistributioninFigure1,whichhasastandarddeviationof0.54logunits.Similarly,hydraulic conductivitydataalsohavealog-normaldistribution,with thestandarddeviationusuallybeingbetween0.5and1.5 logunits(FreezeandCherry,1979,p.31).Forinstance,the slugtestdatafromnineboreholesintheTurnholeSpring basinhaveageometricmeanof6 3 10 6 ms 1 ,with astandarddeviationof0.94logunits. Incalculatingtheresidencetimedistributions,the residencetimesforJordtullaCavearebasedontheflow durationdata(Lauritzenetal.,1986).Forconduitflowat TurnholeSpring,residencetimesarebasedonamean groundwaterpathwayof11kmandonthehistogramof tracer-velocitydistributioninWorthingtonetal.(2000); thesedataareshowninFigure1.Formatrixflowand fractureflowitisassumedthattheresidencetime distributionsarelog-normalwithastandarddeviationof 2.0logunits.Thislargestandarddeviationreflectsnotonly thevariationinhydraulicconductivity,butalsothelarge variationindistanceflowed.Forthesoil/matrixastandard deviationof1.0isusedbecauseflowthroughsoilislikely tobeapproximatedbypistonflowandthesubstantial differencesinresidencetimemaybelargelydueto differencesinsoilthickness. ResultsareshowninFigure4.JordtullaCaveis modeledasasingle-porosityaquifer,sotheresidence timedistributionsfromEquations1and2areidentical (Fig.4a).However,thetwodistributionsforTurnhole Springareverydifferent.Intermsofrechargetothe Figure3.Multiple-boxmodelsforcarbonateaquifers,with fractionofstorage(inpercentage)andresidencetimeineach boxandflowin(m 3 s 1 )betweenboxes.Seetextfordetails. S.R.H.W ORTHINGTON JournalofCaveandKarstStudies, April2007 N 99

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aquifer(ordischargefromtheaquifer),mostofthewater passesquicklythroughitandthemodeis0.01–0.1yr,or 4–37d(Fig.4b).Thisreflectsthelargeproportionof concentratedrechargeatsinkingstreamsordolineswhich hasbeenshownbytracingtoquicklytraveltoTurnhole Spring.Theresidencetimeofstorageisbimodalandis dominatedbysoilsandepikarststorage,witharesidence timeofmonths,andbymatrixstorage,whichhasavery longresidencetime(Fig.4c).FromEquation1,themean residencetimeofrechargetotheaquiferis4years.The meanresidencetimeofstorageintheaquiferisgivenby T s T m S m T f S f T c S c T e S e 3 wheretermsforresidencetime( T e )andstoragefraction ( S e )inthesoilandepikarstareaddedtothevariablesin Equation2.Equation3givesameanstorageresidence timeof19,000years;thisisdominatedbythelarge fractionoftotalstoragethatisinthematrixandbyits longstoragetime.Theestimatedresidencetimesareonly firstapproximationsastheyarebasedonverylimited data. D ISCUSSIONAND C ONCLUSIONS ThemodelsinFigures2and3areallsimplificationsof thecarbonateaquifersdiscussed.Therangeinresidence timesmaybemoreofacontinuumratherthanthediscrete agesthatthesefiguresimplybecausethereisacontinuum ofaperturesizes.Theserangefromporethroatslessthan 1 minwidthtofractures,manyofwhichhaveapertures inthe10–100 mrange,tochannels.Thesmallest channels,suchasthosefeedingslow-drippingstalactites, havecalculatedaperturesinthe0.05–1mmrange (Worthington,1999).Thelargestchannels,suchasthose closetohigh-dischargesprings,haveaperturesgreaterthan 10m. Thereareanumberoffactorsinfluencingtheestimated residencetimesofthedifferentaquifersdiscussed,includingtheuseofdifferenttracersanddifferentmethodologiestocalculateresidencetimesaswellasdifferencesin theaquifersthemselves. Theaquifersdiscussedinthispaperareallunconfined. Insomeconfinedcarbonateaquifers,suchasdeep Figure4.ResidencetimesforbothflowandstorageinJordtullaCave(topl eft),flowintheTurnholeSpringbasin(topright), andstorageintheTurnholeSpringbasin(bottomleft). G ROUND-WATERRESIDENCETIMESINUNCONFINEDCARBONATEAQUIFERS 100 N JournalofCaveandKarstStudies, April2007

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synclinalbasins,extremelyhightotaldissolvedsolids (TDS)concentrationsshowthatflowissluggish,andin thesesituationstheremayhavebeenlittlekarstification unlessitoccursatanearlypre-burialstage.However,in otherconfinedaquiferssuchastheEdwardsAquiferin Texas,therearelargespringswithlowTDSandtheaquifer iswell-karstified(Lindgrenetal.,2004). Detailedconsiderationofadvectiveflowandof diffusionhaveshownthatfracturedrocksareunlikelyto behaveasporousmedia(Pankowetal.,1986).Furthermore,theself-organizationduetothepositivefeedback loopbetweenflowanddissolutionmeansthatcarbonate aquifersarelesslikelythanotherfracturedrockstobehave asporousmedia.Theuseofbothinjectedandenvironmentaltracersisanexcellentwayofdemonstratingthe multipleporositiesandlargerangeinresidencetimesin carbonateaquifers.Therehavebeenanumberof conceptualmodelsthathavesuggestedthatcarbonate aquifersrangefromconduit-flowtodiffuse-flowtypes. However,thepresentstudybettersupportstheconclusions ofWorthingtonetal.(2000)thatunconfinedcarbonate aquifersallhavegreatsimilarities,withallhavingtriple porositywithcontrastingflowandstoragepropertiesinthe matrix,fracturesandchannels. A CKNOWLEDGEMENTS IthankGearySchindelandIraSasowskyforhelpful commentsthatimprovedthemanuscript. R EFERENCES Atkinson,T.C.,1977,Diffuseflowandconduitflowinlimestoneterrain intheMendipHills,Somerset(GreatBritain):JournalofHydrology, v.35,p.93–110. Atkinson,T.C.,andSmart,P.L.,1981,Artificialtracersinhydrogeolog y, in AsurveyofBritishhydrogeology1980:London,RoyalSociety, p.173–190. Bakalowicz,M.,1973,Lesgrandesmanifestationshydrologiquesdes karstsdanslemonde:Spelunca,no.2,p.38–40. Batsche,H.,Bauer,F.,Behrens,H.,Buchtela,K.,Dombrowski,H.J., Geisler,R.,Geyh,M.A.,Ho ¨tzl,H.,Hribar,F.,Ka ¨ss,W.,Mairhofer, J.,Maurin,V.,Moser,H.,Neumaier,F.,Schnitzer,W.A.,Schreiner, A.,Vogg,H.,andZo ¨tl,J.,1970,KombinierteKarstwasseruntersuchungenimGebietderDonauversickerung(Baden-Wu ¨rttenberg)in denJahren1967–1969:SteierischeBeitra ¨gezurHydrogeologie,v.22, p.5–165. Behrens,H.,Benischke,R.,Bricelj,M.,Harum,T.,Ka ¨ss,W.,Kosi,G., Leditzky,H.P.,Leibundgut,C.h.,Maloszewski,P.,Maurin,N., Rajner,V.,Rank,D.,Reichart,B.,Stadler,H.,Stichler,W., Trimborn,P.,Zojer,H.,andZupan,M.,1992,Investigationswith naturalandartificialtracersinthekarstaquiferoftheLurbachsystem (Peggau-Tanneben-Semriach,Austria):SteierischeBeitra ¨gezurHydrogeologie,v.43,p.9–158. Benischke,R.,Zojer,H.,Fritz,P.,Maloszewski,P.,andStichler,W., 1988,EnvironmentalandartificialtracerstudiesinanAlpinekarst massif(Austria), in Yuan,Daoxian,andXie,Chaofan,eds.,Karst hydrogeologyandkarstenvironmentprotection(ProceedingsIAH 21stCongress):Beijing,GeologicalPublishingHouse,p.938–947. Bo ¨gli,A.,andHarum,T.,1981,HydrogeologisischeUntersuchungenim KarstdeshinterenMuotatales(Schweiz):SteirischeBeitra ¨gezur Hydrogeologie,v.33,p.125–264. Bottrell,S.H.,andAtkinson,T.C.,1992,Tracerstudyofflowandstorage intheunsaturatedzoneofakarsticlimestoneaquifer, in Ho ¨tzl,H., andWerner,A.,eds.,Tracerhydrology:Rotterdam,Balkema, p.207–211. Chabert,C.,1977,Surtroissyste `meskarstiquesdegrandeampleur:Eynif, KembosetDumanli(TaurusOccidental), in Ford,T.D.,ed., Proceedingsofthe7thInternationalCongressofSpeleology, Sheffield,1977:Westonzoyland,Somerset,BritishCaveResearch Association,p.105–108. Couturaud,A.,andPuig,J.-M.,1992,Trac agesenborduredusyste `me karstiquedeVaucluse:Karstologia,no.20,p.23–36. Freeze,R.A.,andCherry,J.A.,1979,Groundwater:EnglewoodCliffs, NJ,PrenticeHall,604p. Friederich,H.,andSmart,P.L.,1981,Dyetracestudiesofthe unsaturated-zonerechargeoftheCarboniferousLimestoneaquifer oftheMendipHills,England, in Beck,B.F.,ed.,Proceedingsofthe 8thInternationalCongressofSpeleology,BowlingGreen:Huntsville, Alabama,NationalSpeleologicalSociety,p.283–286. Gunn,J.,1986a,Aconceptualmodelforconduitflowdominatedkarst aquifers, in Gunay,G.,andJohnson,A.I.,eds.,Karstwaterresources: IAHSPublicationNo.161,p.587–596. Gunn,J.,1986b,Soluteprocessesandkarstlandforms, in Trudgill,S.,ed., SoluteProcesses:Chichester,JohnWileyandSons,p.363–437. Jeannin,P-Y.,2001,Modelingflowinphreaticandepiphreatickarst conduitsintheHo ¨llochCave(Muotatal,Switzerland):Water ResourcesResearch,v.37,p.191–200. Jeannin,P-Y.,Wildberger,A.,andRossi,P.,1995,MultitracingVersuch e 1992und1993imKarstgebietderSilberen(MuotatalundKlo ¨ntal, Zentralschweiz):Beitra ¨gezurHydrogeologie,v.46,p.43–88. Karanjac,J.,andGunay,G.,1980,DumanliSpring,Turkey—thelargest springintheworld?:JournalofHydrology,v.45,p.219–231. Ka ¨ss,W.,1998,Tracertechniqueingeohydrology:Rotterdam,Balkema, 581p. Katz,B.G.,2001,Amultitracerapproachforassessingthesusceptibilit y ofgroundwatercontaminationintheWoodvilleKarstPlain, NorthernFlorida, in Kuniansky,ed.,U.S.GeologicalSurveyKarst InterestGroupProceedings:Water-ResourcesInvestigationsReport 01-4011,p.167–176. Kogovs ek,J.,1997,Watertracingtestsinvadosezone, in Kranj,A.,ed., Tracerhydrology97:Rotterdam,Balkema,p.167–172. Lauritzen,S.-E.,1986,Hydraulicsanddissolutionkineticsofaphreati c conduit, in OrganizingCommissionoftheIXInternationalCongress ofSpeleology,ed.,ProceedingsoftheNinthInternationalCongressof Speleology:Barcelona,CatalanFederationofSpeleology,v.1, p.20–22. Lauritzen,S.-E.,Abbott,J.,Arnesen,R.,Crossley,G.,Grepperud,D., Ive,A.,andJohnson,S.,1985,Morphologyandhydraulicsofan activephreaticconduit:CaveScience,v.12,p.139–146. Lindgren,R.J.,Dutton,A.R.,Hovorka,S.D.,Worthington,S.R.H.,and Painter,S.,2004,ConceptualizationandsimulationoftheEdwards Aquifer,SanAntonioRegion,Texas,U.S.GeologicalSurvey, ScientificInvestigationsReport2004–5277. Loper,D.E.,Werner,C.L.,Chicken,E.,Gavies,G.,andKinkaid,T., 2005,Carbonatecoastalaquifersensitivitytotides:Eos,v.86, p.353–357. Morfis,A.,andZojer,H.,1986,Karsthydrologyofthecentraland easternPeleponnesus,Greece:SteirischeBeitra ¨gezurHydrogeologie, v.37/38,p.1–301. Mudry,J.,andPuig,J.-M.,1991,LekarstdelaFontainedeVaucluse: Karstologia,no.18,p.29–38. Mu ¨ller,I.,andZo ¨tl,J.,1980,KarsthydrologischeUntersuchungenmit natu ¨rlischeandku ¨nstlicheTracernimNeuenburgerJura(Schweiz): SteirischeBeitra ¨gezurHydrogeologie,v.32,p.5–100. Pankow,J.F.,Johnson,R.L.,Hewetson,J.P.,andCherry,J.A.,1986,An evaluationofcontaminantmigrationpatternsattwowastedisposal sitesinfracturedporousmediaintermsoftheequivalentporous medium(EPM)model:JournalofContaminantHydrology,v.1, p.65–76. Pitty,A.F.,1968,Calciumcarbonatecontentofkarstwaterinrelationto flow-throughtime:Nature,v.217,p.939–940. Puig,J.M.,1990,Lesyste `mekarstiquedelaFontainedeVaucluse: DocumentduBRGMNo.180,208p. Quinlan,J.F.,1986,Groundwatertracers:Discussion:GroundWater, v.24,p.396–399. Quinlan,J.F.,andEwers,R.O.,1989,Subsurfacedrainageinthe MammothCavearea, in White,W.B.,andWhite,E.L.,eds.,Karst S.R.H.W ORTHINGTON JournalofCaveandKarstStudies, April2007 N 101

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hydrology:conceptsfromtheMammothCavearea:NewYork,Van NostrandReinhold,p.65–103. Quinlan,J.F.,Smart,P.L.,Schindel,G.M.,Alexander,Jr.,E.C.,Edward s, A.J.,andSmith,A.R.,1992,Recommendedadministrative/regulatory definitionofcarbonateaquifers,principlesforclassificationof carbonateaquifers,practicalevaluationofvulnerabilityofkarst aquifers,anddeterminationofoptimumsamplingfrequencyat springs, in Proceedingsofthethirdconferenceonhydrogeology, ecology,monitoring,andmanagementofgroundwaterinkarst terrains:Dublin,Ohio,WaterWellJournalPublishingCompany, p.573–635. Smart,P.L.,1981,Variationofconduitflowvelocitieswithdischargein theLongwoodtoCheddarRisingsystem,MendipHills, in Beck,B.F., ed.,ProceedingsoftheEighthInternationalCongressofSpeleology, BowlingGreen:Huntsville,Alabama,NationalSpeleologicalSociety, p.333–335. Smart,P.L.,andHobbs,S.L.,1986,Characterisationofcarbonate aquifers:aconceptualbase, in Environmentalproblemsinkarst terranesandtheirsolutionsconference(1st,BowlingGreen, Kentucky):Dublin,Ohio,NationalWaterWellAssociation,p.1–14. Smart,C.C.,andLauritzen,S.-E.,1992,Continuous-flowfluorometryin groundwatertracing, in Quinlan,J.F.,ed.,ProceedingsoftheThird ConferenceonHydrogeology,Ecology,Monitoring,andManagementofGroundWaterinKarstTerranes:Dublin,Ohio,WaterWell PublishingCompany,p.231–241. White,W.B.,1969,Conceptualmodelsforcarbonateaquifers:GroundWater,v.7,p.15–21. White,W.B.,1988,Geomorphologyandhydrologyofkarstterrains:New York,OxfordUniversityPress,464p. White,W.B.,andSchmidt,V.A.,1966,HydrologyofakarstareaineastcentralWestVirginia:WaterResourcesResearch,v.2,p.549–560. Wisenbaker,M.,2006,AhistoryofexplorationinAmerica’slongest underwatercave(PartI):NSSNews,v.64(6),p.4–11. Worthington,S.R.H.,1999,Acomprehensivestrategyforunderstanding flowincarbonateaquifers, in Palmer,A.N.,Palmer,M.V.,and Sasowsky,I.D.,eds.,Karstmodeling:CharlesTown,W.Va.,Karst WatersInstitute,SpecialPublicationNo.5,p.30–37. Worthington,S.R.H.,andFord,D.C.,1995,Boreholetestsformegascale channelingincarbonateaquifers.Proceedings,XXVICongressofthe InternationalAssociationofHydrogeologists,Edmonton,Alberta, June5th–9th1995. Worthington,S.R.H.,Davies,G.J.,andFord,D.C.,2000,Matrix, fractureandchannelcomponentsofstorageandflowinaPaleozoic limestoneaquifer, in Wicks,C.M.,andSasowsky,I.D.,eds., Groundwaterflowandcontaminanttransportincarbonateaquifers: Rotterdam,Balkema,p.113–128. Yonge,C.,Ford,D.C.,Gray,J.,andSchwarcz,H.P.,1985,Stableisotope studiesofcaveseepagewater:ChemicalGeology(IsotopeGeoscience section),v.58,p.97–105. Yurtsever,Y.,andPayne,B.R.,1986,Time-variantlinearcompartment modelapproachtostudyflowdynamicsofakarsticgroundwater systembyaidofenvironmentaltritium(acasestudyofsouth-eastern karstareainTurkey), in Gunay,G.,andJohnson,A.I.,eds.,Karst waterresources:IAHSPublicationNo.161,p.545–561. G ROUND-WATERRESIDENCETIMESINUNCONFINEDCARBONATEAQUIFERS 102 N JournalofCaveandKarstStudies, April2007



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CONTENTSEditorial 1Sixty Five and Still Going Strong Journal of Cave and Karst Studies Malcolm S. FieldArticle 3Cave Geology and Speleogenesis Over the Past 65 Years: Role of the National Speleological Society in Advancing the Science Arthur N. PalmerArticle 13A Brief History of Karst Hydrogeology: Contributions of the NSS William B. WhiteArticle 27Cave Archaeology and the NSS: 1941–2006 George Crothers, P. Willey, and Patty Jo WatsonArticle 35Cave Mineralogy and the NSS: Past, Present, Future Carol A. Hill and Paolo FortiArticle 46The Importance of Cave Exploration to Scienti c Research Patricia KambesisArticle 59Development of the Carbonate Island Karst Model Joan R. Mylroie and John E. MylroieArticle 76Cave Sediments and Paleoclimate William B. WhiteArticle 94Ground-Water Residence Times in Uncon ned Carbonate Aquifers Stephen R.H. WorthingtonArticle 103Pseudokarst in the 21st Century William R. HallidayArticle 114The Biology and Ecology of North American Cave Crickets Kathleen H. Lavoie, Kurt L. Helf, and Thomas L. PoulsonArticle 135Zoogeography and Biodiversity of Missouri Caves and Karst William R. ElliottArticle 163Geomicrobiology in Cave Environments: Past, Current and Future Perspectives Hazel A. Barton and Diana E. NorthupArticle 179Subterranean Biogeography: What Have We Learned From Molecular Techniques? Megan L. PorterArticle 187Observations on the Biodiversity of Sul dic Karst Habitats Annette Summers EngelArticle 207 Risks to Cavers and Cave Workers From Exposures to Low-Level Ionizing Radiation From 222Rn Decay in Caves Malcolm S. FieldArticle 229The Re ection of Karst in the Online Mirror: A Survey Within Scienti c Databases, 1960–2005 Lee J. Florea, Beth Fratesi, and Todd ChavezJournal of Cave and Karst StudiesVolume 69 Number 1 April 2007 JOURNAL OF CAVE AND KARST STUDIESApril 2007 Volume 69, Number 1 ISSN 1090-6924 A Publication of the National Speleological Society 1 9 4 1 2 0 0 6 1941-2006 Journal of Cave and Karst Studies Volume 69 Number 1 April 2007

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GUIDE TO AUTHORS The Journal of Cave and Karst Studies is a multidisciplinary journal devoted to cave and karst research. The Journal is seeking original, unpublished manuscripts concerning the scienti c study of caves or other karst features. Authors do not need to be members of the National Speleological Society but preference is given to manuscripts of importance to North American speleology. LANGUAGES: The Journal of Cave and Karst Studies uses American-style English as its standard language and spelling style, with the exception of allowing a second abstract in another language when room allows. In the case of proper names, the Journal tries to accommodate other spellings and punctuation styles. In cases where the Editor-in-Chief nds it appropriate to use non-English words outside of proper names (generally where no equivalent English word exists), the Journal italicizes them. However, the common abbreviations i.e., e.g., et al., and etc. should appear in roman text. Authors are encouraged to write for our combined professional and amateur readerships. CONTENT: Each paper will contain a title with the authors’ names and addresses, an abstract, and the text of the paper, including a summary or conclusions section. Acknowledgments and references follow the text. ABSTRACTS: An abstract stating the essential points and results must accompany all articles. An abstract is a summary, not a promise of what topics are covered in the paper. STYLE: The Journal consults The Chicago Manual of Style on most general style issues. REFERENCES: In the text, references to previously published work should be followed by the relevant author’s name and date (and page number, when appropriate) in brackets. All cited references are alphabetical at the end of the manuscript with senior author’s last name rst, followed by date of publication, title, publisher, volume, and page numbers. 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At your rst visit, you will be prompted to establish a login and password, after which you will enter information about your manuscript ( e.g., authors and addresses, manuscript title, abstract, etc.). You will then enter your manuscript, tables, and gure les separately or all together as part of the manuscript. Manuscript les can be uploaded as DOC, WPD, RTF, TXT, or LaTeX. A DOC template with additional manuscript speci cations may be downloaded. (Note: LaTeX les should not use any unusual style les; a LaTeX template and BiBTeX le for the Journal may be downloaded or obtained from the Editor-inChief.) Table les can be uploaded as DOC, WPD, RTF, TXT, or LaTeX les and gure les can be uploaded as TIFF, EPS, AI, or CDR les. Alternatively, authors may submit manuscripts as PDF or HTML les, but if the manuscript is accepted for publication, the manuscript will need to be submitted as one of the accepted le types listed above. Manuscripts must be typed, double spaced, and single-sided. 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Illustrations must be a minimum of 300 dpi for acceptance.The Journal of Cave and Karst Studies (ISSN 1090-6924, CPM Number #40065056) is a multi-disciplinary, refereed journal published three times a year by the National Speleological Society, 2813 Cave Avenue, Huntsville, Alabama 35810-4431 USA; Phone (256) 852-1300; Fax (256) 851-9241, email: n ss@caves.org; World Wide Web: http://www.caves.org/pub/journal/. The annual subscription fee is $23 US, $44 US for 2 years, and $65 US for 3 years. Check th e Journal website for international rates. Back issues and cumulative indices are available from the NSS of ce. POSTMASTER: send address changes to the Journal of Cave and Karst Studies 2813 Cave Avenue, Huntsville, Alabama 35810-4431 USA. The Journal of Cave and Karst Studies is covered by the following ISI Thomson Services Science Citation Index Expanded, ISI Alerting Services, and Current Contents/ Physical, Chemical, and Earth Sciences. Copyright 2007 by the National Speleological Society, Inc. Front cover: Photograph by John Mylroie of Sunshaft Room in Hamilton Cave, Bahamas.Published By The National Speleological SocietyEditor-in-Chief Malcolm S. FieldNational Center of Environmental Assessment (8623D) Of ce of Research and Development U.S. Environmental Protection Agency 1200 Pennsylvania Avenue NW Washington, DC 20460-0001 202-564-3279 Voice 202-565-0079 Fax eld.malcolm@epa.govProduction EditorScott A. EngelCH2M HILL 304 Laurel Street, Suite 2A Baton Rouge, LA 70801-1815 225-381-8454 scott.engel@ch2m.comJournal ProofreaderDonald G. Davis441 S. Kearney St Denver, CO 80224 303-355-5283 dgdavis@nyx.netJOURNAL ADVISORY BOARD E. Calvin Alexander, Jr. Hazel A. Barton Garth Davies Harvey DuChene Barbara am Ende Annette Summers Engel John Mylroie Megan Porter Stephen Worthington BOARD OF EDITORSAnthropology Patty Jo Watson Department of AnthropologyWashington University St. Louis, MO 63130 pjwatson@artsci.wustl.eduConservation-Life Sciences Julian J. Lewis & Salisa L. LewisLewis & Associates, LLC. Cave, Karst & Groundwater Biological Consulting 17903 State Road 60  Borden, IN 47106-8608 812-283-6120  lewisbioconsult@aol.comEarth Sciences-Journal Index Ira D. SasowskyDepartment of Geology and Environmental Science Univesity of Akron  Akron, OH 44325-4101 330-972-5389  ids@uakron.eduExploration Paul BurgerCave Resources Of ce 3225 National Parks Highway  Carlsbad, NM 88220 505-785-3106  paul_burger@nps.govHuman and Medical Sciences Stephen R. Mosberg, M.D.#5 Foxboro Drive  Vienna, WV 26105-1939 304-295-5949  cavedoc@suddenlink.netMicrobiology Kathleen H. LavoieDepartment of Biology State University of New York Plattsburgh, NY 12901 518-564-3150  lavoiekh@plattsburgh.eduPaleontology Greg McDonaldPark Museum Management Program National Park Service 1201 Oakridge Dr. Suite 150 Fort Collins, CO 80525 970-267-2167  greg_mcdonald@nps.govSocial Sciences Joseph C. DouglasHistory Department Volunteer State Community College 1480 Nashville Pike  Gallatin, TN 37066 615-230-3241  joe.douglas@volstate.eduBook Reviews Arthur N. Palmer & Margaret V PalmerDepartment of Earth Sciences State University of New York Oneonta, NY 13820-4015 607-432-6024  palmeran@oneonta.edu