Microscopic fungi on cadavers and skeletons from cave and mine environments


previous item | next item

Citation
Microscopic fungi on cadavers and skeletons from cave and mine environments

Material Information

Title:
Microscopic fungi on cadavers and skeletons from cave and mine environments
Series Title:
Czeck Mycology
Creator:
Nováková, Alena
Kubátová, Alena
SklenáÅ™, FrantiÅ¡ek
Hubka, Vít
Publication Date:
Language:
English

Subjects

Genre:
serial ( sobekcm )

Notes

Original Version:
Czeck Mycology, Vol. 70, no. 2 (2018-08-19).

Record Information

Source Institution:
University of South Florida Library
Holding Location:
University of South Florida
Rights Management:
This object is protected by copyright, and is made available here for research and educational purposes. Permission to reuse, publish, or reproduce the object beyond the bounds of Fair Use or other exemptions to copyright law must be obtained from the copyright holder.
Resource Identifier:
K26-00030 ( USFLDC: LOCAL DOI )
k26.30 ( USFLDC: LOCAL Handle )

USFLDC Membership

Aggregations:
University of South Florida
Karst Information Portal

Postcard Information

Format:
serial

Downloads

This item is only available as the following downloads:


Full Text

PAGE 1

Microscopicfungioncadaversandskeletons fromcaveandmineenvironmentsALENANOVÁKOVÁ1*,ALENAKUBÁTOVÁ2,FRANTIŠEKSKLENÁ1,2,VÍTHUBKA1,21LaboratoryofFungalGeneticsandMetabolism,In stituteofMicrobiologyoftheCAS,v.v.i., Vídeská1083,CZ-14220Praha4,CzechRepublic2DepartmentofBotany,FacultyofScience,CharlesUniversity,Benátská2,CZ-12801Praha2, CzechRepublic *correspondingauthor:ANm icrofungi@seznam.czNovákováA.,KubátováA.,SklenáF.,HubkaV.(2018):Microscopicfungionca daversandskeletonsfromcaveandmineenvironments.…CzechMycol.70(2): 101…121.Duringlong-termstudiesofmicroscopicfungiin80Europeancavesandmineenvironments manycadaversandskeletonsofanimalsinhabitingth eseenvironmentsandvariousanimalvisitors werefound,someofthemwithvisiblemicrofungal growth.Directisolation,thedilutionplate methodandvarioustypesofisolationmediawereu sed.Theresultingspectrumofisolatedfungiis presentedandcomparedwithreco rdsabouttheirpreviousisolation. Comparedtoformerstudiesfocusedmainlyonbatmycobiota,thispapercontributestoawider knowledgeoffungalassemblagescolonisingvari ousanimalbodiesinundergroundenvironments. Themostinterestingfindingsincludeascocarpsof Acauliumcaviariforme foundabundantonmammalscadavers,while Botryosporiumlongibrachiatum isolatedfromfrogs, Chaetocladiumjonesiae frombatsand Penicilliumvulpinum fromspidersrepresentthefirstrecordsofthesespeciesfrom cadaversorskeletons. Keywords: Europeancaves,abandonedmines,deadbodies,bones,mammals,frogs,spiders,is opods, micromycetes. Articlehistory: received11May2018,revised17June 2018,accepted20June2018,publishedon line19August2018.NovákováA.,KubátováA.,SklenáF.,HubkaV.(2018):Mikroskopickéhoubyna mrtvýchtlechakostráchživoichvpr ostedíjeskyníadol.…CzechMycol. 70(2):101…121.Vprbhudlouhodobéhostudiamikroskopickýchhubvosmdesátievropskýchpodzemníchpro storách(jeskyn,oputnédoly)bylynalezenyta kémrtvátlaakostryživoichžijícíchvtomto prostedíinahodilýchnávtvník,nkterés viditelnýminárostymikroskopickýchhub.Pímáizo lace,zeovacímetodaarznámédiabylypoužit yproizolacikonkrétníchdruh.Získanéspektrum hubjeprezentovánoasrovnánospedchozíminálezy. Oprotidosavadnímstudiím,zamenýmhlavn nahoubynapadajícínetopýry,jetatopráce píspvkemkirímupoznáníspoleenstevhub,kol onizujícíchtlarznýchživoichvpodzemním prostedí.Mezinejzajímavjínálezylzezaadit Acauliumcaviariforme, jehožplodnicebylyhojn nacházenynamrtvýchtlechsavc,zatímcodruhy Botryosporiumlongibrachiatum (izolované zžab), Chaetocladiumjonesiae (znetopýr)ataké Penicilliumvulpinum (zpavouk)pedstavují prvnínálezytchtodruhnamrvýchtlechnebokostráchživoich.101CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 2

INTRODUCTIONHitherto,themajorityofstudiesintomicrofungalassemblagesinunder groundspaceshavebeenpredominantlyf ocusedoncaveairandsedimentsoron rockandspeleothemsurfaces.Thiss eeminglynutrient-poorecosystemcanhow everalsoincludemanyspotswithorganicmatter,suchasplantmaterial(e.g. seeds,twigs,detritus)washedfromtheenvironmentaboveaswellasvariousde positsofanimalinhabitants,excretionsofcave-inhabitinginvertebratesandver tebrates,batdroppingsandguano. Undergroundenvironmentsincludingcaves areoftenvisitedbyvariousanimals whichseekrefugefromunfavourableweatherconditionsorsearchforfood,and someofthemalsofallintotheunderground(frogs,lizards).Alloftheseanimalsmay dieaftersometimeasaconsequenceofage,foodabsenceorcollapsefromexhaus tion.Cadaversofcave-inhabitinganimals, mainlybats,areutilisedasfoodforcaveinhabitingterrestrialinvertebratessu chasearthworms,isopods,diplopods,spring tails,mitesetc.which,togetherwithcavemicrobiota,graduallydecomposedeador ganicmatter.Cadaversinvariousstageofdecompositionarefoundoncavesedimentorspeleothems,fromfreshdeadbodi estoskeletonsorparticularbones.Given thehighairhumidityandconstantairtemperatureinthecaveenvironment, successionaldecompositionisnotlimitedtodryperiods,asinabove-groundconditions,butgoesoncontinually.Somecadaversarecoveredbyvisiblemyceliaofmicroscopicfungi,otheronesarewit houtvisiblemicrofungalinfection. Duringlong-termstudiesofcavemyc obiotainvariousundergroundenvironments,from2002uptothepresent,mainlyfocusedonmicroscopicfungiincave air,cavesedimentsandbatguano,wefoundanumberofrecentlydeceasedanimalsaswellasskeletonsandseparatebones.Weusedvariousisolationtech niquestoelucidatewhichmicrofungalspeciescolonisethesesubstratesandare responsiblefortheirdecomposition.Thisreportprovidesanoverviewofmicro fungalspecieswhichhavebeenfoundon skeletons/bonesanddeadanimals (withtheexceptionofinsects)inha bitingundergroundenvironments. MATERIALANDMETHODSSamplingsites.Studiesofmicrofungalassemblageshavebeencarried outsince2002,inatotalof80undergroundenvironmentsofseveralEuropean countries,mainlyintheCzechRepublic ,Slovakia,SpainandRomania.Their originalandEnglishnamesandothercharacteristicsaregiveninTab.1.Studied cavesarekarstic,oligotrophicoreutrophic,oneischemoautotrophic(Movile Cave),oneisofmarineorigin(TreasureCave),andtwositesbelongtononkarsticenvironments(NaRozhraníCaveandSimonandJudeMines). 102CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 3

103NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERSTab.1. Overviewofthestudiedcaves.Cavesinwhich cadaversorskeletonswerefoundareinbold. CountryUndergroundsiteOriginalnameUndergroundtypeAirtemperature(°C)* Czech Republic ChýnovCaveChýnovskájeskynKa rsticcave,showcave5.0…9.0 KonprusyCavesKonpruskéjeskynKarsticcave,showcave10.6 BozkovDolomiteCavesBozkovskédolomito véjeskynKarsticcave,showcave7.5…9.0 NaPomezíCavesJeskynNaPomezíKarsticcave,showcave7.0…8.0 Na—piákuCaveJeskynNa—piáku Karsticcave,showcave7.0…9.0 MladeCavesMladeskéjeskynKarsticcave,showcave8.0 JavoíkoCaves JavoískéjeskynKarsti ccave,showcave7.0…8.0 ZbraovAragoniteCavesZbraovskéaragonitové jeskynHydrothermalcave,showcave14.0…16.0 HranickáAbyss…RotundaHranickápropast …RotundaHydrothermalabyss14.3…18.0 NaTurolduCaveJeskynNaTurolduKarsticcave,showcave7.1…9.1 PunkvaCavesPunkevníjeskynKa rsticcave,showcave7.0…8.0 (Catherines)KateinasCaveKateinsk ájeskynKarsticcave,showcave7.0…8.0 BalcarkaCaveJeskynBalcarkaKarsticcave,showcave7.0…8.0 Sloup-—ovkaCaves Sloupsko-ovskéjeskynKa rsticcave,showcave7.0…8.0 VýpustekCaveJeskynVýpustekKarsticcave,showcave7.0…9.0 PustožlebskázazdnáCavePustožlebskázazdná jeskynKarsticcave,closedtothepublic7.0…9.0 NewAmateurCaveNováAmatérskájeskynKarsticcave,closedtothepublic7.0…9.0 BýískálaCaveJeskynBýískálaKar sticcave,closedtothepublic7.0…9.0 HarbeskáCaveHarbeskájeskynKars ticcave,closedtothepublic7.0…9.0 ManželskýSinkholeManželskýzávrtKar sticcave,closedtothepublic7.0…9.0 KrálovaCaveKrálovajeskynKarsticcave,closedtothepublic9.0…10.0 PodkížemCaveJeskynPodkížemKar sticcave,closedtothepublic9.0…10.0 NaRozhraníCaveJeskynNaRozhraníNon-karsticcave,closedtothepublic9.0…10.0 OchozskáCaveOchozskájeskynKarsticcave,closedtothepublic8.0 SlámovaslujCaveJeskynSlámovaslujK arsticcave,closedtothepublic8.0…10.0 SimonandJudeMines Doly—imonaaJudyAbandonedironoremines5.0…10.0

PAGE 4

104CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)CountryUndergroundsiteOriginalnameUndergroundtypeAirtemperature(°C)* Slovakia DomicaCave JaskyaDomicaKarsticcave,showcave10.2…11.4 ertovadieraCaveJaskyaertovadieraK arsticcave,closedtothepublic10.2…11.4 ArdovskáCaveArdovskájaskyaKarsti ccave,closedtothepublic7.9…11.5 GombaseckáCave GombaseckájaskyaKarsticcave,showcave9.0…9.4 KrásnohorskáCave KrásnohorskájaskyaKarsticcave,showcave8.7…8.9 HruovskáCaveHruovskájaskyaKarsticcave,closedtothepublic9.0 JasovskáCaveJasovskájaskyaKa rsticcave,showcave8.8…9.4 —ingliarovaAbyss—ingliarovapriepasKa rsticcave,closedtothepublic9.0…10.0 StaráBrzotínskaCaveStaráBrzotínskajasky aKarsticcave,closedtothepublic9.5…10.4 DrienovskáCaveDrienovskájaskyaKars ticcave,closedtothepublic9.3…11.3 SilickáIceCaveSilickáadovájaskyaKarsticcave,closedtothepublic4.0…10.0(…1.0to…11.0)** OchtinskáAragoniteCaveOchtinskáaragoni továjaskyaKarsticcave,showcave7.6…8.4 DobinskáIceCaveDobinskáadovájaskyaKa rsticcave,showcave…0.4to…1.0(0.8…3.5)** DemänovskáIceCaveDemänovskáadovájas kyaKarsticcave,showcave0(1.3…5.7)** DemänovskáPeaceCave DemänovskájaskyaMieruKarsticcave,closedtothepublic6.5…7.0 DemänovskáCaveofLibertyDemänovskájaskyaSlobodyKarsticcave,showcave6.1…7.0 DeadBatsCave JaskyamtvychnetopierovKarsticcave,showcave3.0…3.5 BobakaCaveJaskyaBobakaKarst iccave,closedtothepublic7.3…9.1 HarmaneckáCave HarmaneckájaskyaKarsticcave,showcave5.8…6.4 ModrovskáCaveModrovskájaskyaKars ticcave,closedtothepublic8.9…9.1 SucháCaveSuchájaskyaKarsticcav e,closedtothepublic3.4…9.5 PružinskáDúpnaCavePružinskáDúpnajas kyaKarsticcave,showcave7.4…8.9 BelianskaCaveBelianskajaskyaKarsticcave,showcave5.0…5.8 MiladaCaveJaskyaMiladaKarsticcave,closedtothepublic9.0…10.0 MichováAbyssMichovápriepasKars ticcave,closedtothepublic8.0…10.0 BrestovskáCaveBrestovskájaskya Karsticcave,showcave4.9…5.4 PerlováCavePerlovájaskyaKarsticcave,closedtothepublic9.0…10.0 SpainAltamiraCaveCuevadeAltamiraKarsticcave,closedtothepublic18.0 ArdalesCaveCuevadeDoaTrinidadKarsticcave,showcave17.6

PAGE 5

105NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERSCountryUndergroundsiteOriginalnameUndergroundtypeAirtemperature(°C)* CastaardeIborCaveCuevadeCastaarKarsticcave,showcave16.9 TreasureCaveCuevadelTesoroCaveo fmarineorigin,showcave17.6…19.2 GrottooftheMarvelsGrutadelasMaravillasKarsticcave,showcave18.1…19.0 NerjaCave CuevadeNerjaKarsticcave,showcave19.5…20.5 RomaniaScrioaraIceCavePeteraghetarulScri oaraKarsticcave,showcave0…1.0(…7.0inwinter) VârtopIceCavePeteraghetarulVârtopKarsticcave,showcave0…3.0 CoibaMareCavePeteraCoibaMareKar sticcave,closedtothepublic9.0…10.0 PoartaluiIoneleCavePeteraPoartaluiI oneleKarsticcave,showcave9.0…10.0 FânaeCave PeteradelaFânaeKarsticca ve,closedtothepublic9.0…10.0 FericeCavePeteradelaFericeKarsticcave,closedtothepublic9.0…10.0 MguraCavePeteraMguraKarsticcave,closedtothepublic11.0…12.0 UrilorCave(BearsCave)PeteraUrilorKarsticcave,showcave9.8 MeziadCavePeteraMeziadKarsticcave,showcave9.0…10.0 LimanuCavePeteraLimanuKarsticcave,closedtothepublic 15.0…18.0 LiliecilordelaGuraDobrogeiCave PeteraLiliecilordelaGuraDobrogeiKarsticcave,closedtothe public 18.0…19.0 MovileCave PeteraMovileChemoautotrophiccave,closedtothepublic 21.5 ZiditaCavePeteraZiditaKarsticcave,closedtothepublic9.0…10.0 DracoaiaCavePeteraDracoaiaKarst iccave,closedtothepublic9.0…10.0 UnguruluiCavePeteraUnguruluiKar sticcave,closedtothepublic9.0…10.0 ColiboaiaCavePeteraColiboaiaKarst iccave,closedtothepublic9.0…10.0 UngureascaCavePeteraUngureasca Karsticcave,showcave9.0…10.0 Hungary BaradlaCave BaradlabarlangKarsticcave,showcave 10.2 CroatiaHrustovaaCaveHrustovaapeina Karsticcave,closedtothepublic10.0…12.0 Slovenia—kocjanCaves—kocjanske jameKarsticcave,showcave12.0 FranceLascauxCaveGrottedeLascauxKarsticcave,closedtothepublic12.7 *Temperaturevaluesweretakenfromofficialwebsitesofthecavesorth eCzechandSlovakCavesAdministration.Temperaturesmeasuredbythe authors(digitalMulti-thermom eter,Guangdong,China)areinbold. **Differentvaluesindicatetemperaturesindiffere ntpartsofthecave(withorwithouticedeposition).

PAGE 6

Allstudiedsitesarecharacterisedbyhighairhumidity(c.98…99%)butair temperaturedifferedaccordingtotheirgeographicallocationaswellastocave type.WhileCzech,Slovak,andsomeRomaniancavesintheApuseniMts.are characterisedbyanairtemperatureof7to11°C,mostofthestudiedSpanish cavesandRomanianonesintheDobrogearegionarewarmercavesystemswith anairtemperatureof16…21°C.Someo fthestudiedcavesareabundantlyinhab itedbybats(e.g.theCzechJavoíkoCavesorNaTurolduCave,theSlovak DomicaCave,DrienovskáCave,DeadBatsCave,JasovskáCave,andArdovská Cave,theRomanianLiliecilordelaGur aDobrogeiCave,MeziadCave,Ferice CaveandFânaeCave),inothersbatsarelesscommon(e.g.theSlovak DemänovskáPeaceCave,DemänovskáCaveofLiberty,GombaseckáCaveand KrásnohorskáCave,theRomanianLimanuCave,theSpanishNerjaCave,the CzechKateinasCaveandSloup-Šovka Caves).Incontrast,batsareabsent fromtheRomanianMovileCave,theSpanishGrottooftheMarvels,Ardales Cave,AltamiraCave,andtheSlovakOchtinskáAragoniteCave.Severalcaves, suchasAltamiraCave,GrottooftheMarvels,andArdalesCave(Spain),areregu larlyvisitedbyvariousspeciesofrodents. Isolationandidentification.Samplesofcadavers…deadbodies… withvisiblemicrofungalgrowthanddegradingorganicmatterwerecollectedusingsterileforcepsintosterilemicrotubesordirectlyonagarisolationmediain Petridishes.Inthelaboratory,isolati onswerecarriedoutbytransferringthecollectedmaterialonagardiscsinPetridishesorpreparingadilutioninsterilewater.DichloranroseBengalchloramphenicolagar(DRBC),Sabouraudsglucose agarandbeerwortagar,bothwithroseBengal(0.1g/l)andchroramphenicol (0.1g/l)(Atlas2010)wereusedasisolationmedia.Cultivationlastedfor7daysat 25°Cinthedark. Microfungalidentificationwasperformedaccordingtothemacro-and micromorphologicalcharactersusingre levanttaxonomicliteraturefocusedon particulargenera(e.g.deHoog2000,Samson&Varga2004,2007,Samson& Houbraken2011,Seifertetal.2011,Samsonetal.2011,2013,Benschetal.2012, Guarroetel.2012,Dijksterhuisetal.2013,Hubkaetal.2016,Sandoval-Deniset al.2016,Chenetal.2016,2017,etc.).Maltextractagar(MEA),Czapekyeast autolysateagar(CYA)andCzapek-Doxagar(CZA)wereusedformicrofungal identification(Atlas2010). Molecularanalysis.Someisolateswerealsoidentifiedwithmolecular methods.DNAwasextractedfrom7-dayoldcolonieswiththeArchivePureDNA yeastandGram2+kit(5PRIMEInc.,Gaithersburg,Maryland,USA)withmodified incubationtimes:lyticenzymesolution(2h,37°C)andcelllysissolution(4h, 64°C).Partial caM geneencodingcalmodulinwasamplifiedusingforwardprim ersCF1MorCF1LandreverseprimerCF4(Peterson2008).ThePCRmixture 106CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 7

(totalvolume25µl)contained0.1µlMyTaqDNApolymerase(BiolineGmbH, Luckenwalde,Germany),5µlMyTaqReactionBuffer,1µlofeachprimer(10µM stockconcentration),and1µl(50ng)genomicDNA.Thestandardthermalcycle profilewas93°Cfor2min;38cyclesof93°Cfor30s,55°Cfor30s,72°Cfor60s, andfinalextension72°Cfor10min.Automatedsequencingwasperformedat MacrogenSequencingService(Amsterdam,TheNetherlands)usingtheforward andreverseprimers.Theobtainedsequenceswereinspectedandassembled withBioEditversion7.1.8(www.mbio.nc su.edu/BioEdit/bioe dit.html)andthen comparedwiththosederivedfromex-typestrainsdepositedintheGenBank databaseinordertoidentifytheisolatesatthespecieslevel. RepresentativestrainsofthesequencedspeciesaredepositedintheCulture CollectionofFungiattheDepartmentofBotany,CharlesUniversityinPrague (CCF).ObtainedDNAsequencesweredepositedintheEuropeanNucleotide Archive(ENA)database(Tab.2).Tab.2. GenBankdatabaseaccessionnumbersofthesequencesobtainedinthisstudy.107NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERSSpeciesLocalityStrainnumber/culturecollectioncode*ITSrDNA caM Aspergillusaureolatus FânaeCaveS193LS974072 Aspergillusbaeticus MovileCaveS349=CCF5046LT558749 Aspergillusbaeticus DemänovskáPeaceCaveCMFISB2181=CCF4231HE615119 Aspergilluscreber DemänovskáPeaceCaveS321LS974073 Aspergillusmovilensis MovileCaveMo10=CCF4410=CMFISB2614= NRRL62819=CBS134395 HG916740 Aspergillusparasiticus HarmaneckáCaveS146LS974074 Aspergillustennesseensis MovileCaveS135LS974075 Aspergillusthesauricus MovileCaveS552=CCF4968LT558753 Aspergillusthesauricus MovileCaveS741LS974076 Botryosporium longibrachiatum Domica-Baradlacave system CCF5732LS974068 *CCF…CultureCollectionofFungi,Prague;CMF…CollectionofMicroscopicFungiISB,eské Budjovice;SandMo…strainsfrom A.Novákovásworkingcollection.RESULTSANDDISCUSSIONFungionbatcadavers Batsbelongtothemostcommonlyknowninhabitantsincavesandotherun dergroundenvironments.Unfortunately,untilrecentlystudieswerefocusedon theoccurrenceofmicrofungionbatfur(Larcheretal.2003,Beguinetal.2005) andlatermainlyon Pseudogymnoascus ( Geomyces ) destructans asaninfection agentofWNS(whitenosesyndrome)(Blehertetal.2008,Gargasetal.2009,

PAGE 8

108CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421) Tab.3. Overviewofmicrofungaltaxaisol atedfromdeadanimalbodiesorbones. Sitesoforigin:1…JavoíkoCaves,2…Sloup-ŠovkaCaves,3…SimonandJudeMines,4…Domica Cave,5…GombaseckáCave,6…DemänovskáPeaceCave,7…DeadBatsCave,8…HarmaneckáCave, 9…KrásnohorskáCave,10…NerjaCave,11…Fâna eCave,12…LiliecilordelaGuraDobrogeiCave, 13…MovileCave,14…BaradlaCave. Deadanimalsmarten dormousebatspider isopod frogCaves65123467810 1 112591313414 Mucoromycota Chaetocladiumjonesiae (Berk.&Broome)Fresen.++ Mortierellahorticola Linnem.+ Mortierellahumilis Linnem.exW.Gams+++ Mortierella sp.++ Mucorhiemalis Wehmerf. hiemalis + Mucorhiemalis f. luteus (Linnem.)Schipper+ Mucorhiemalis f. silvaticus (Hagem)Schipper+ Mucormucedo P.MicheliexSt.-Amans+ Mucorracemosus Fresen.var. racemosus +++ Mucorwosnessenskii Schostak.++ Rhizomucorpusillus (Lindt)Schipper+ Thamnidiumelegans Link+ Ascomycota Acauliumcaviariforme (Malloch&Hubart)SandovalDenis,Guarro&Gené * +++ Aspergillusaureolatus Munt.-Cvetk.&Bata+ Aspergillusbaeticus A.Nováková&Hubka++ Aspergilluscreber Jurjevi,S.W.Peterson&B.W.Horn+ Aspergillusmovilensis Nováková,Hubka,M.Kolaík& S.W.Peterson + Aspergillusparasiticus Speare+ Aspergillustennesseensis Jurjevi,S.W.Peterson&B.W.Horn+ Aspergillusthesauricus Hubka&A.Nováková+ Botryosporiumlongibrachiatum (Oudem.)Maire++ Cephalotrichumstemonitis (Pers.)Nees+ Chrysosporium sp.+ Cladosporiumcladosporioides (Fresen.)G.A.deVries+ Cladosporiumherbarum (Pers.)Link+ Cladosporiumsphaerospermum Penz.+ Cylindrocarponobtusiusculum (Sacc.)U.Braun+ Fusariummerismoides Corda+ Gliomastixchartarum (Corda)S.Hughes+ Oidiodendrongriseum Robak++ Penicilliumaurantiogriseum Dierckx+

PAGE 9

Martínkováetal.2010,Wibbeltetal.2010,Puechmailleetal.2011,Johnsonetal. 2013,Zukaletal.2014,Vanderwolfetal.2016et c.)andmicrofungalcolonisation ofbatcadaverswasneglected. Attheplaceoftheirroostingorhibernationaswellasinplaceswherethey movethrough,theircadaverscanbefoundinvariousstagesofdecomposition andwithprogressivemicrofungalcolonisation.Batcadaverswithwhitecottony overgrowth(mostlyof Myotismyotis, butinsomecaseunidentifiableduetodisintegration)werefoundinsever alcavesduring2005…2011,e.g.DomicaCave, DobinskáIceCaveandDeadBatsCave(Slovakia),NerjaCave(Spain),and LiliecilordelaGuraDobrogeiCave(Romania)(Fig.1a…c).Fromallthesecadavers,non-sporulatingstrainsofthegenus Mortierella wereisolated,whichwere identifiedonthegenuslevelaccordingtotheircharacteristiccolonygrowth(typ icallobatecolonies)andgarlicodour.Ahangingdeadbat( Myotismyotis )with whitemycelialovergrowth(Fig.1d)identifiedaccordingtoitsmacro-and micromorphologicalpropertiesas Mortierellahumilis (Fig.1f…g)wasfoundin Sloup-ŠovkaCaves(MoravianKarst,Cz echRepublic).Thisspecieswasalso isolatedfromfinemyceliumgrowing onbatbones(Fig.1e)ondisplayinthe DeadBatsCave(Slovakia). Aspergillusaureolatus wasisolatedfrombatcadav ersfoundintheentrancecorridoroftheLiliecilordelaGuraDobrogeiCavein Romania.DuringoursamplingingalleriesoftheSimonandJudeMinesnearthe villageofMaláMorávka(northernMoravia,CzechRepublic)inspring2015we foundseveralfreshbatcadavers.Thesebatshadbeenkilledbymarten( Martes foina ),afterwhichtheircadaversinanearlystageofdecompositionwerecolo nisedbypredominantlyzygomycetousfungi(Fig.2),especiallyby Mucor spp. and Chaetocladiumjonesiae.Chaetocladium sp.wasalsofoundonabat cadavercollectedinJavoíkoCaves(C zechRepublic).Speciesofthegenus 109NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERSDeadanimalsmarten dormousebatspider isopod frogCaves65123467810 1 112591313414 Penicilliumchrysogenum Thom+ Penicilliumcorylophilum Dierckx+ Penicilliumolsonii Bainier&Sartory+ Penicilliumvulpinum (Cooke&Massee)Seifert&Samson++ Pseudogymnoascuspannorum complex+ Undeterminedstrains Steriledarkpigmentedmycelium+ Undeterminedyeast+ Undeterminedbasidiomycetes+ *Theidentificationwascarriedoutonlyonmicroscopi cfeaturesofcollectedmaterial,notisolated.

PAGE 10

110CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421) Fig.1. Mortierella spp.ondeadbatbodies. a …DomicaCave(Slovakia); b …NerjaCave(Spain); c …LiliecilordelaGuraDobrogeiCave(Romania); d …growthof Mortierellahumilis ondead Myotis myotis (Sloup-ŠovkaCaves,CzechRepublic); e …exhibitionofbonesinDeadBatsCave (Slovakia); f …14-dayoldcolonyof M.humilis onmaltextractagar; g … M.humilis, sporangiophore withyoungsporangium.Scalebar=20µm.P hotoA.Nováková(a…c,e…g),P.Zajíek(d).

PAGE 11

Chaetocladium mainlybelongtofacultative,gall-formingparasitesonother Mucorales (Benny2005)andstrainsofthisgenuswereearlierisolatedfrommar tendunginArdovskáCaveaswellasfromcavesedimentoftheDomicaCave (Nováková,unpublished). Onthecontrary,olderbatcadaversfoundinDemänovskáPeaceCaveand HarmaneckáCave(Fig.3)aswellasdormousecadaversfoundinGombasecká Cave(SlovakKarst,Slovakia)weref oundtobecoveredbyamassofblackasco carpsof Acauliumcaviariforme. Theisolationofthisspecieswasunsuccessful butitstypicalmorphologyenabledreliabl eidentification.Inthecaseoftwodor mouse( Dryomysnitedula )cadaversfoundinGombaseckáCaveaftersummer floods,wecouldobserveafungalsuccessi onondeadbodies:theoccurrenceof zygomycetousfungi( Mucor spp.and Mortierella spp.inanearlystage)wasfol 111NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS Fig.2. Chaetocladiumjonesiae . a …coloniesondeadbatsinSimonandJudeMines,MaláMorávka (CzechRepublic); b …10-dayoldcolonyonMEA; c,d …branchedfertilehyphaewithunispored sporangiaandsterilespines(c…Nomarskiinterfe rencecontrast,d…SEM).Scalebars=20µm.Photo A.Kubátová.

PAGE 12

lowedbylargenumbersofascocarpsof Acauliumcaviariforme afterseveral months.ThisfunguswasfirstfoundintheCaveofRamioul(Belgium)andde scribedas Microascuscaviariformis (Malloch&Hubart1987)andrecently transferredtothegenus Acaulium (Sandoval-Denisetal.2016).Vanderwolfetal. 112CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421) Fig.3. Acauliumcaviariforme . a …blackascocarpsondeaddormousebody; b …detailofdeaddor mousebodywithblackascocarpsof A.caviariforme andwhite Mortierella sp.growth; c–f …amass ofblackascocarpsonbatskeletonsfromSlovakcaves:GulikováPassageinDemänovskáPeace Cave(c,d),RuinsPassageinDemänovskáPeaceCave(e),StrayDomeinHarmaneckáCave(f). PhotoA.Nováková.

PAGE 13

(2013a)isolatedthisspeciesfromfurofhibernatingbatsinthreeNewBrunswick caves,Canada.Theoccurrenceof A.caviariforme ascomataonbatcarcassesin anadvancedstageofdecomposition,justconsistingofremnantfurandbone, wasobservedintheNewBrunswickhibernacula(Vanderwolfetal.2016a).In spiteofthefactthatthisspecieshasbeenrarelyreportedfromundergrounden vironments,itisprobablyacommonmicrofungalspeciesparticipatinginthe decompositionofdeadanimalsincavesandmines. Usingthedilutionisolationmethod(Garrett1981),severalfilamentousfungi wereisolatedduringoursurveys(Tab.3). Aspergillusbaeticus , Cephalotrichum stemonitis , Cylindrocarponobtusiusculum , Fusariummerismoides , Mucor racemosus var. racemosus , Mucorwosnessenskii , Oidiodendrongriseum and Pseudogymnoascuspannorum s.l.wereisolatedfromdeadbatscollectedinthe DemänovskáPeaceCave. Aspergillusbaeticus (Fig.4)hadalreadybeenisolated fromSpanishTreasureCave,GrottooftheMarvels(Novákováetal.2012)and 113NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS Fig.4. Aspergillusbaeticus . a …batskeletonwithamassofblackmaterialfromwhichthisspecies wasisolated(GulikováPassageinDemänovskáPeaceCave,Slovakia); b …7-dayoldcolonieson CYA(top),MEA(bottomleft)andCZA(bottomright); c …conidiophore; d …Hüllecells; e …conidia. Scalebars=20µm(c,d),10µm(e).PhotoA.Nováková(a,b),A.Kubátová(c…e).

PAGE 14

NerjaCave(Nováková,unpublished)andwaslaterisolatedfromtheRomanian MovileCave(Novákováetal.2018). Aspergillusparasiticus , Gliomastixchar tarum , Mortierellahumilis , M.horticola , Mucorhiemalis var. hiemalis , M.hiema lis var. silvaticus , M.mucedo , M.wosnessenskii , Cladosporiumherbarum s.l., Rhizomucorpusillus andasteriledarkpigmentedfunguswereisolatedfrom adeadbatcollectedinHarmaneckáCaveand Clonostachysrosea f. rosea , Mortierella sp.and Mucormucedo wereisolatedfromdeaddormousebodies foundintheGombaseckáCave. Previouslypublishedrecordsofmicromycetesincludingyeastsisolatedfrom deadbatsinundergroundenvironmentsaregiveninTab.4.Atotalof48fungal specieswereisolatedfrombatcadavers.Twentymicrofungaltaxaarereported inthestudyondeadbatsintheGrottadelPalummarolocatedinsouthernItaly andintheGrottadelleVene,Piedmont,Italy(Voyronetal.2011),while16micro fungalspecieswereisolatedfromdeadbatsinNewBrunswickhibernacula (Vanderwolfetal.2016).AworldreviewofCanadianresearchers(Vanderwolfet al.2013b)reportedasurveyofpublishedrecordsoffungi,yeastsandslime 114CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421) Tab.4. Anoverviewofmicrofungaltaxaisolatedfr omdeadbats,reportedinpreviousstudies. ReferencesCountrySpecies Zeller(1966)Hungary Chrysosporiummerdarium Wibbelt etal.(2010) United Kingdom Penicillium sp. Voyron etal.(2011) Italy Alternaria sp., Aspergillus sp., Candidapalmioleophila,Chrysosporium/Gymnoascus , Chrysosporiummerdarium , Cladosporiumcladosporioides , Fusariumdimerum , Fusarium equiseti , Gymnoascaceae , Lecanicilliumlecanii , Mortierellagamsii , Mortierellapolycephala , Mucorhiemalis f. hiemalis , Mucorplumbeus , Mucorracemosus , Ophiostomataceae , Penicilliumgriseofulvum , Penicillium sp., Thielavia sp., Trichosporonchiropterorum Nováková (2012) Slovakia Mortierellahumilis Vanderwolf etal.(2013b) world Acremoniumimplicatum , Alternaria sp., Arthrodermasilverae , Aspergillusbaeticus , Aspergillus sp., Candidapalmioleophila , Chrysosporiummerdarium , Chrysosporium sp., Cladosporiumcladosporioides , Clonostachysrosea f. catenulata , Fusariumdimerum , Fusariumequiseti , Gliocladiumatrum , Gymnoascus sp., Gymnoascaceae unidentified, Lecanicilliumlecanii , Mortierellagamsii , Mortierellapolycephala ,Mucorhiemalis f. hiemalis , Mucorpiriformis , Mucorplumbeus , Mucorracemosus , Ochroconisconstricta , Ophiostomataceae unidentified, Penicilliumglandicola , Penicilliumrestrictum , Penicillium sp., Scolecobasidiumtenerum , Sporobolomycespruinosum , Thielaviaterricola , Thielavia sp., Trichosporonchiropterorum Vanderwolf etal.(2016) Canada Acauliumcaviariforme , Acremonium spp., Arachniotus sp., Arthrodermasilverae , Cephalotrichumstemonitis , Chrysosporiummerdarium , Chrysosporium sp., Fusarium sp., Leuconeurosporacapsici , Mortierella sp., Mucor sp., Oidiodendrontruncatum , Pseudogymnoascusdestructans , Pseudogymnoascuspannorum s.l., Trichoderma sp., Trichosporondulcitum

PAGE 15

mouldsincavesincluding32microfungalspeciesisolatedfrombatcadavers.On thecontrary,Zeller(1966)andWibbeltetal.(2010)presentedonlyoneisolated species.Themostfrequentlyreportedspeciesfromdeadbatsis Chrysosporium merdarium .Nováková(2009)isolatedaspeciesidentifiedas Mortierellahumilis onlyonce(Nováková2012). Ourrecordsareratherpoorincomparisonwiththeresultsofstudiesby Voyronetal.(2011)andVanderwolfetal.(2016)onlytargetedatmycobiotaof deadbats,becausetheyoriginatefromrandomfindsduringstudiesfocusedon 115NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS Fig.5. Aspergilluscreber . a …martenskeletoninGulikováPassage,DemänovskáPeaceCave (Slovakia)fromwhichthespecieswasisolated; b …7-dayoldcoloniesonCYA(top),MEA(bottom left)andCZA(bottomright); c …conidiophore; d …conidia.Scalebars=20µm(c),10µm(d).Photo A.Nováková(a,b),A.Kubátová(c,d).

PAGE 16

116CZECHMYCOLOGY70(2):101Â…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 17

cavemycobiotaincludingfungaloccurrenceincaveair,sediments,batguano, andanimalexcretions.Nevertheless,someofourrecordsareveryinteresting andincluderarelyisolatedspeciesandfirstreportsfromthissubstrate. 117NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS Fig.7. Spiders. a … Agraecinacristianii ; b …dead A.cristianii withsynnematalmicrofungal growth,cavewall(LakeRoom,MovileCave,Romania); c …collectedsampleonPetridishwith DRBC; d …coloniesof Penicilliumvulpinum ondeadspiderbody( Metamenardi )inentrancecorri dorofKrásnohorskáCave(Slovakia).PhotoA.Nováková. Fig.6. Botryosporiumlongibrachiatum . a,b …frogskeletonswithvisiblewhitegrowth(DomicaBaradlacavesystem,Slovakia); c,d …14-dayoldcoloniesof B.longibrachiatum onMEA; e,f …de tailofcolonymarginwithvisibleconidiophores; g–i …conidiophoredetails:brancheswith conidiogenouscellsandconidia.Scalebars=50 µm(g),20µm(h,i).PhotoA.Nováková(a…f), A.Kubátová(g…i).

PAGE 18

Fungionotheranimals Undergroundenvironmentsarealsovisitedbyotheranimals,e.g.martens ( Martesfoina ),dormice( Dryomysnitedula ),frogs( Pelophylax sp.),andspi ders( Metamenardi inentrancesectionsbutalsosometruecave-inhabitants suchastheendemic Agraecinacristianii inMovileCave).Besidestheabovementioneddormice,martensareveryfrequentvisitorstocavesandabandoned mines.Someofthementerundergroundsitestoprotectthemselvesfrombad weatherconditionsorinordertosearchforfood.Thereforemartencadaversor skeletonswerealsooccasionallyfoundincaves…e.g.awell-preservedmarten skeletonwasfoundintheGulikováPassageoftheDemänovskáPeaceCave (Fig.5).Boneslackedvisiblemicrofungalgrowth,butcultivationyielded Asper gilluscreber (identifiedusingthe caM gene,seeTab.2). Otheranimalssuchasfrogsandlizardsvisitcaveenvironmentsoccasionally aftersummerfloodsorstorms,becauseofdownfallorduringsearchingfor acoldersiteduringahotsummer.Theirlong-termstayintheunderground mostlyendsindeathbecauseofstarvation.Frogskeletonswithvisiblewhite microfungalgrowthidentifiedas Botryosporiumlongibrachiatum werediscoveredintheDomica-Baradlacavesystem(Fig.6).Ourfindisthefirstrecordof thisfungusfromananimalsubstrateaswellasfromacaveenvironment.Thus far,thisspecieshadbeenrecordedpredominantlyfromplantmaterialincluding Curcumarubricaulis leaves(Tribe&Weber2001)andlaterfromawidevariety ofdeadanddecayingplantmaterial(Tribe&Weber2001,Park&Park2013)oras anairbornespecies(Anonymus2016). DuringourstudyofthemycobiotaoftheMovileCave(Romania),weisolated microscopicfungifromdeadinvertebr atebodies.Severalspeciesofthegenus Aspergillus wereisolatedfromadeadendemicspider, Agraecinacristianii ,i.e. Aspergillusbaeticus and A.tennesseensis ,whilst A.movilensis and A.thesau ricus wereisolatedfromadeaddiplopod, Trachelipustroglobius (Novákováet al.2018). Synnematalmicrofungalcolonies(Fig.7b)werefoundonsomecadaversof thespider Agraecinacristianii intheLakeRoomofMovileCavein2013.Itwas impossibletoidentifythisfungusbase donmorphologicalcharactersandisola tionwasunsuccessful.Unfortunately ,similardeadspiderbodieswithsynnema talcolonieswerenotfoundduringsamplinginthefollowingyears.Deadspider bodies( Metamenardi )werealsofoundinGombaseckáCaveandKrásnohorská Cave(SlovakKarst)(Fig.7d)andinbothcases, Penicilliumvulpinum wasiso latedfromthem.Thisspeciesisacoprophilousfungusfrequentlyfoundincaves onvarioussortsofdung. 118CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 19

CONCLUSIONSDuringourstudies,atotalof39fungalta xa(classifiedasspecies,formsoriden tifiedatasupraspecifi clevel)onvariouscadaversandskeletonsfoundinunder groundenvironmentwereidentifiedins everalEuropeancavesandmines.Thirtyeightspecieswereisolatedinpurecul tures…12ofthembelongingtoMucoro mycota,23speciestoAscomycota,while3strainswerenotidentifiedtothespe cieslevel.Speciesofthegenera Mucor and Aspergillus wereisolatedmostabun dantly.TherichestmicrofungalspectrumwasfoundintheDemänovskáPeace CaveandDeadBatsCave,fromwhich14and16microfungalspecieswereiso lated,respectively.Theascomycete Acauliumcaviariforme wasreportedrepeat edlyfromseveralSlovakcaves,butunfortunatelytheisolationofthesestrains failed.However,thisfungusisprobablyacommonfungalspeciesparticipatingin thedecompositionprocessofdeadanim alsinundergroundenvironments. ACKNOWLEDGEMENTSWethankMiladaChudíkováandAlenaGab rielová(InstituteofMicrobiology oftheCAS,Prague)andIvanaBoroviková(DepartmentofBotany,CharlesUniversity,Prague)fortheirinvaluableassistanceinthelaboratory. REFERENCES ANONYMUS(2016): Botryosporiumlongibrachiatum .… http://www.mycobank.org/BioloMICS.aspx?Table=Mycobank&Rec=3319&Fields=All.[accessed May2018] ATLASR.M.(2010):Handbookofmicrobiologicalmedia.…CRCPress,Washington,D.C. BEGUINH.,LARCHERG.,NOLARDN.,CHABASSED.(2005): Chrysosporiumchiropterorum sp.nov., isolatedinFrance,resembling Chrysosporium stateof Ajellomycescapsulatus ( Histoplasma capsulatum ).…MedicalMycology43(2):161…169. BENNYG.L.(2005): Chaetocladium .…http://zygomycetes.org/i ndex.php?id=102.[accessedMay2018] BENSCHK.,BRAUNU.,GROENEWALDJ.Z.,CROUSP.W.(2012):Thegenus Cladosporium . – Studiesin Mycology72:1…401. BLEHERTD.S.,HICKSA.C.,BEHRM.,METEYERC.U.,BERLOWSKI-ZIERB.M.,BUCKLESE.L.,COLEMANJ.T., DARLINGS.R.,GARGASA.,NIVERR.,OKONIEWSKIJ.C.,RUDDR.J.,STONEW.B.(2008):Batwhitenosesyndrome:anemergingfungalpathogen?…Science323(5911):227. CHENA.J.,FRISVADJ.C.,SUNB.D.,VARGAJ.,KOCSUBÉS.,DIJKSTERHUISJ.,KIMD.H.,HONGS.-B., HOUBRAKENJ.,SAMSONR.A.(2016): Aspergillus section Nidulantes (formerly Emericella ): Polyphasictaxonomy,chemistryand biology.…StudiesinMycology84 : 1…118. CHENA.J.,HUBKAV.,FRISVADJ.C.,HOUBRAKENJ.,MEIJERM.,VARGAJ.,DEMIRELR.,JURJEVI™., KUBÁTOVÁA.,SKLENÁF.,ZHOUY.G.,SAMSONR.A.(2017):Polyphasictaxonomyof Aspergillus section Aspergillus (formerly Eurotium ),anditsoccurrenceinindoorenvironmentsandfood. – StudiesinMycology88:37…135.119NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS

PAGE 20

DIJKSTERHUISJ.,WÖSTENH.,eds.(2013):Developmentof Aspergillusniger . – StudiesinMycology 74:1…85. GARGASA.,TRESTM.T.,CHRISTENSENM.,VOLKT.J.,BLEHERTD.S.(2009): Geomycesdestructans sp. nov.associatedwithbatwhite-nosesyndrome.…Mycotaxon108:147…154. GARRETTS.D.(1981):Soilfungiandsoilfertility:anintroductiontosoilmycology,2nded.…Pergamon Press,Oxford. GUARROJ.,GENÉJ.,STCHIGELA.M.,FIGUERASM.J.(2012):AtlasofsoilAscomycetes.…CBSBiodiver sitySeries10,486p.,CentraalbureauvoorSchimmelcultures,Utrecht. DEHOOGG.S.(2000):Atlasofclinicalfungi,2nded. – 1126p.,CentraalbureauvoorSchimmelcultures, Utrecht/UniversitatRoviraiVirgili,Reus. HUBKAV.,NOVÁKOVÁA.,PETERSONS.W.,FRISVADJ.,SKLENÁF.,MATSUZAWAT.,KUBÁTOVÁA., KOLAÍKM.(2016):Areappraisalof Aspergillus section Nidulantes withdescriptionsoftwonew sterigmatocystin-producingspecies.… PlantSystematics andEvolution302:1267…1299. JOHNSONL.J.A.N.,MILLERA.N.,MCCLEERYR.A.,MCCLANAHANR.,KATHJ.A.,LUESCHOWS.,PORRASALFAROA.(2013):Psychrophilicandpsychrotolerantfungionbatsandthepresenceof Geomyces spp.onbatwingspriortothearrivalofwhitenosesyndrome.…AppliedandEnviron mentalMicrobiology79(18):54…65. LARCHERG.,BOUCHARAJ.P.,PAILLEYP.,MONTFORTD.,BÉGUINH.,DEBI VREC.,CHABASSED.(2003): Fungalbiotaassociatedwithbatsinwester nFrance.…JournaldeMycologieMédical13:29…34. LORCHJ.M.,MULLERL.K.,RUSSELLR.F.,OCONNORM.,LINDNERD.L.,BLEHERTD.S.(2013):Distribu tionandenvironmentalpersistenceofthecausativeagentofwhite-nosesyndrome, Geomyces destructans ,inbathibernaculaoftheeasternUnitedStates .– AppliedandEnvironmentalMicrobiology79(4):1293…1301. MALLOCHD.,HUBARTJ.-M.(1987):Anundescribedspeciesof Microascus fromtheCaveofRamioul. …CanadianJournalofBotany65(11):2384…2388. MARTÍNKOVÁN.etal.(2010):Increasingincidenceof Geomycesdestructans fungusinbatsfrom CzechRepublicandSlovakia.…PLOSONE5(11):e13853. NOVÁKOVÁA.(2009):MicroscopicfungifromtheDomicaCavesystem(SlovakKarstNationalPark, Slovakia).Areview.…InternationalJournalofSpeleology38:71…82. NOVÁKOVÁA.(2012):Microscopicfungiassociatedwith bats.…In:Ková.,UhrinM.,uptáikP.,eds.,21stInternationalConferenceonSubterraneanBiology,2nd…7thSeptember2012,Koice, Slovakia.Abstractbook,p.78. NOVÁKOVÁA.,HUBKAV.,SAIZ-JIMENEZC.,KOLAÍKM.(2012): Aspergillusbaeticus sp.nov.and Aspergillusthesauricus sp.nov.,twospeciesinsection Usti fromSpanishcaves.…International JournalofSystematicandEvol utionaryMicrobiology62:2778…2785. NOVÁKOVÁA.,HUBKAV.,VALINOVÁŠ.,KOLAÍKM.,HILLEBRAND-VOICULESCUA.M.(2018):Cultivable microscopicfungifromanundergroundchemosynth esis-basedecosystem:apreliminarystudy.… FoliaMicrobiologica6:1…13. PARKJ.H.,PARKM.J.(2013):Firstreportofblackstemcausedby Botryosporiumlongibrachiatum onsweetbasilinKorea.…PlantDisease97(3):425. PETERSONS.W.(2008):Phylogeneticanalysisof Aspergillus speciesusingDNAsequencesfromfour loci.…Mycologia100:205…226. PUECHMAILLES.J.etal.(2011):Pan-Europeandistributionofwhite-nosesyndromefungus ( Geomycesdestructans )notassociatedwithmassmortality.…PLOSONE6(4):e19167. SAMSONR.A.,COBUSM.,VISAGIEC.M.,HOUBRAKENJ.,eds.(2014):Speciesdiversityin Aspergillus, Penicillium and Talaromyces . – StudiesinMycology78:1…451. SAMSONR.A.,FRISVADJ.C.(2004): Penicillium subgenus Penicillium :newtaxonomicschemesand mycotoxinsandotherextrolit es.…StudiesinMycology49:1…174. SAMSONR.A.,HOUBRAKENJ.(2011):Phylogeneticandta xonomicstudiesonthegenera Penicillium and Talaromyces .…StudiesinMycology70:1…183.120CZECHMYCOLOGY70(2):101…121,AUGUST19,2018(ONLINEVERSION,ISSN1805-1421)

PAGE 21

SAMSONR.A.,VARGAJ.(2007): Aspergillus systematicsinthegenomicera.…StudiesinMycology59: 1…206. SAMSONR.A.,VARGAJ.,FRISVADJ.C.(2011):Taxonomicstudiesonthegenus Aspergillus .…Studiesin Mycology69:1…97. SANDOVAL-DENISM.,GUARROJ.,CANO-LIRAJ.F.,SUTTOND.A.,WIEDERHOLDN.P.,DEHOOGG.S., ABBOTTS.P.,DECOCKC.,SIGLERL.,GENÉJ.(2016):Phylogenyandtaxonomicrevisionof Micro ascaceae withemphasisonsynnematousfungi.…StudiesinMycology83:193…233. SEIFERTK.,MORGAN-JONESG.,GAMSW.,KENDRICKB.(2011):ThegeneraofHyphomycetes. – CBS BiodiversitySeries9,997p.,CentraalbureauvoorSchimmelcultures,Utrecht. TRIBEH.T.,WEBERR.W.S.(2001):Deadbasilstems…apossibleecologicalnicheforthehoar-frost fungus Botryosporiumlongibrachiatum .…Mycologist15(4):158…161. VANDERWOLFK.J.,MCALPINED.F.,MALLOCHD.,FORBESG.J.(2013a):Ectomycotaassociatedwithhi bernatingcavebatsineasternCanadapriortotheemergenceofwhite-nosesyndrome.…North easternNaturalist20(1):115…130. VANDERWOLFK.J.,MALLOCHD.,MCALPINED.F.,FORBESG.J.(2013b):Aworldreviewoffungi,yeasts andslimemoldsincaves.…InternationalJournalofSpeleology42(1):77…96. VANDERWOLFK.J.,MALLOCHD.,MCALPINED.F.(2016):Fungionwhite-noseinfectedbats( Myotis spp.) inEasternCanadashownodeclineindiversityassociatedwith Pseudogymnoascusdestructans (Ascomycota: Pseudeurotiaceae ).…InternationalJournalofSpeleology45(1):43…50. VOYRONS.,LAZZARIA.,RICCUCCIM.,CALVINIM.,VARESEG.C.(2011):Firstmycologicalinvestigation onItalianbats.…Hystrix22:189…197. WIBBELTG.,KURTHA.,HELLMANND.,WEISHAARM.,BARLOWA.,VEITHM.,PRUGERJ.,GORFOLT., GROSCHEL.,BONTADINAF.,ZOPHELU.,SEIDLH.P.,CRYANP.M.,BLEHERTD.S.(2010):Whitenose syndromefungus( Geomycesdestructans )inbats,Europe.…EmergingInfectiousDiseases16: 1237…1243. ZELLERL.(1966):KeratinophilicfungifromtheBaradla caveinAggtelek(Biospel eologicaHungarica, XXII).…AnnalsoftheUniversityofSciencesBudapest,SectionBiology,8:375…388. ZUKALJ.,BANOUCHOVÁH.,BARTONIKAT.,BERKOVÁH.,BRACKV.,BRICHTAJ.,DOLINAYM.,JAROK.S., KOVÁOVÁV.,KOVAÍKM.,MARTÍNKOVÁN.,ONDRÁEKK.,EHÁKZ.,TURNERG.G.,PIKULAJ. (2014):White-nosesyndromefungus:ageneralistpathogenofhibernatingbats.…PLOSONE9: e97224.121NOVÁKOVÁA.,KUBÁTOVÁA.,SKLENÁF.,HUBKAV.:MICROSCOPICFUNGIONCADAVERS


printinsert_linkshareget_appmore_horiz

Download Options

close


  • info Info

    There are only PDFs associated with this resource.

  • link PDF(s)



Cite this item close

APA

Cras ut cursus ante, a fringilla nunc. Mauris lorem nunc, cursus sit amet enim ac, vehicula vestibulum mi. Mauris viverra nisl vel enim faucibus porta. Praesent sit amet ornare diam, non finibus nulla.

MLA

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

CHICAGO

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

WIKIPEDIA

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