geomicrobiology 2009 ics proceedingsdigital.csic.es/bitstream/10261/81329/1/what...

Geomicrobiology 384 2009 ICS Proceedings

WHAT CAN MOLECULAR MICROBIOLOGY TELL US ABOUT LASCAUX CAVE?

V.¡URADO', F BASTlAN', C. ALABOUVETTE', and C. SAIZ jIMENEZ'

' Instituto de Recursos Naturales y Agrobiologia, CSIC, Apartado 1052, 41080 Sevilla, Spain

' UMR INllA-Université de Bourgogne, Microbiologie du Sol el de l'Environment, BP 865 I O, 21065 Dijon Cedex, Frallct

Lascaux Cave comains paintings from che Upper Paleolichic periodo Shorcly ancr discovery in 1940. che

cave was se riously disturbed duc ro major desrructive imerventions (e.g. excavarions , aie conditioning,

anificial lighr insrallation, ete.). In 1963, che cave \Vas closed duc ce algal growth on che wa lls. In 2000 che ait conditioning sysrcm \Vas replaced. In 2001, (a few momhs aner rhat replacemem), che vaulc, walIs,

scdimclUs and soil \Vece colonized by Fusarium solani. Later, black sra ins aiso appeared ae che encrance,

which extended in 2007 to che test of che cave. Betwcen 200 1 and 2004, and again in 2008, thc cave was

treated wich benzalkonium chloride. Recently, \Ve have srudied che microbial communitie in Lascaux

Cave using molecular cools. We condude thac the índigenous bacterial cornmunity was replaced by

microbia l populations selecred for by biocide application and other majo r desrructive intc rvenrions. In

additioo tO che m icrobial populacio ns, enromopathogcnic fungí play an imponanr role in rhe cave and

arrhropods conrríbute to che dispersion of spores and fl.1n gal development.

1. lntroduction 1he conservaríon of Paleolirh ic paintings in caves is o f

grcar interesr because rhey represenc a priceless cultural

herirage of all humankind. Among che Paleolich ic pa incings,

rhose ar C hauvcr and Lascaux. France, and ac Alcamira in

Spain , show remarkable soph isricarion. ln recenr rimes,

some of che mosr imporcant caves are suffering episodes of

biological concam inaríon char mighr damage rhe paintings

(SCH ABEREITER-GU RTNER e[ al., 2002; DUPONT

e[ al., 2007)

The Cave of Lascaux was d iscovered in 1940. lhe

imporrance of irs paintings was recognized shortly afrer ¡es

discovery and chey are cOl1sidered ro be among the finesr

rock arr painrings. As soon as ir \Vas open ro rhe pl.1blic

rhe cave anracred many visirors, which amounted up ro

1,800 every day in [he 1960's (S IRE, 2006). This seriously

d isrurbed che cave microclimare and had a scrong impace o n

rhe who le cave.

Rock art rour islll srarred ar che beginning of rhe pasr

cencury. Ac rhat rime. no sc iencific knowledge on

conservaríon problems exísred, rherefore managemenc

decisions adoprcd o feen resu lred in grear harm fo r che

furure of many caves. In rhe Cave of Lascaux, che condüio ns

for visi" berween 1945 and 1948 and in 1958 (and che

impact of rnassíve rourism rhereafrer) were nvo of rhe maín

problcms. In fact.lighting which began in 1960 caused rhe

growrh of a grecn biofi lm o n the wall painrings. inirially

identified as produced by CUorobot,.ys, a Xanthophy[.

alga. Years lace r, che observaríon of zoospore fo rmarion

in one of rhe alga! isolaces, nor previously derecred , led ro

¡rs proper spec ific determinarion as Bracteacocms minor, a

member of [he C hlocophy,a (LEFÉVRE, 1974). This green

biofilm, considered as "'la maladie ve rre", was rhe firsr o ne of

rhe di fie renr contaminaríon episodes suffered by rhe cave

lcading ro ies closure in 1963 due ro the damage p rod uced

by visirors, Iighcing, and algal growrh on che painrings.

SIRE (2006). in an excellenr hisrorical repo re on Lascaux

management, sra red that rhe rrearments for defearing "' la

malad ie verte" included a combined spray applic:trion of

srreptomycin and penicillin fo r bacteria and a subsequenr

rrearmenr with formaldehyde foc aIgae. These applicarions

were effecrive tlncU 1969 when it was necessary ro starr again

and a programme of periodic maintenance and cleaning was

adop[ed.

Bcrwecn JlIly and Seprember 2001 che firsr evidence

of a fungal ourbreak appeared alo ng with an assoc iaced

bac terium Pseudomonas fiuorescens (ALLEMAN D,

2003; ORIAL AND MERTZ, 2006). In Augllsr 2001,

rrcarmenr of che ourbreak began bU[ irs rapid expansion

led ro a more intensive crearmenr in Sepeember lIsing

aH""Y1 dimerhylbenzylammon ium chlo ride soluríons plus

srrep romycin and polymyxin. The soils were creared with

qu ick1 ime (SI RE, 2006). In 2004 benzalkonium chloride

treacments were replaced by mechanical c1eaningand air

exrracríon and recovery of c1eaning debris. Ar presenr there

is srricr control o n access ro rhe cave, and al! inrervencions

are reco rded and discussed ar rhe "Com iré Scienrifique

Internacional de la Grone de Lascal.1x': creared in 2002 by

15th International Congress of Speleology

Geomicrobiology

che French Minisrcr foc Culture and Communication.

In 2007, black srains (Fig. 1) IVere found in the vault and passagc banks. Ahhough rheir origin is unknowll,

dematiaceous hyphornyccrcs, producing olive~green ro black

coJonies, \Vere isolarcd from (he srains (BASTIAN AND

ALABOUVETTE,2009).

Figure 1: Black stains in the vault 01 the Passage.june 2008. Picture protected by copyright: Ministere de la Culture et de la Communication, DRAe d:Aquitaine and

Centre National de la Préhistoire.

In me tase year a debate was initiatcd in European and u.s. media on Lascaux black srains (e.g. DE ROUX, 2007, SIMONS, 2007, FOX, 2008). In addition ro a hisrorical description on [he works carried out in che cave since che

discovery, commems on me problem from difrecenr expcns

\Vere summarized and [he appearance ofblack smins noüccd.

2. Cave Ecology Why has Lascaux Cave suffered slIccesive biological invasions since ¡es d iscovery? 1he problem derives from

che public imcrest and pressure of rock arr rourism and

che crroneolls concepcion that aU rock are should be

exposed [ O public comcmplarion. llis concepe is in general

opposirio n [O cffecrive conservation of che rock arto This

is because opcning a cave irnmediately resules in a sudden

change of microdimare wim accompanying dcrcrioration of

speleorhcms and rack art p:ünrings.

Opening a cave also impaC[s cave biology. Bacteria, fungi,

and arthropods, all have constructed delicare and balanced


385 2009 ICS Proceedings

rrophic relationships between predaror and prey and che strength ofinreracrions berween species can be imcrruprcd

by rourism and cave prepararíon for rourism whích ¡nelude

cxcavarions and major dcsrruc(Ívc intcrvcneions.

Thc situarion in Lascaux is particularly worrying beca use

the cave has had two different fungal invasions ín síx years.

In 2001 rhe presence of members of the Fltsarimn so/ani

species cOlllplex (DUPONT et al., 2007) was reponed. In addítion, represematives of six fungal genera were fOllnd

in the cave: Chrysosporium, Gliocladium, Gliornastix, Paecilomyces, Trichoderma and Verticillium. Whi le no species

idemihcation was provided, the data reponed by these

allmOrS sllggest a strong correlarion between cave fungi

and arthropods because rhese fungal genera COntaLn many

entol11opathogenic (insect infeccing) species (SAMSON

ee al., 1988). Species of Chrysosporium, G/¡oc!adium,

Paeci/omyces, and Verticillium havc beco isolated from larval

and adult cadavers ofcave cricketS (GUNDE-CIMERMAN ct al., 1998), and rhe association between fungi and insecrs

in caves was recendy reponed by KUBÁTOVÁ ANO

DVORÁK (2005). These studies indicated the necd for

a detailed molecular smdy ro decipher rhe origin of rhe

microbial c0l11l1111ni ries rhriving in rhe cave.

3. Molecular Ecology We collecred eleven samples berween April 2006 and

)anllary 2007 in differenr halls and galleries of Lascaux

Cave. The Painted Gallery, Grea, Hall of Bulls, Chamber

of Felines and Shaft of rhe Dead Man were sclected co

represent rhe diffe renr cave microenviromentS. The samples

inelllded areas wim whire colonizarion, black srains. areas

nor apparendy colonized (and rherefore considered as

references) and an area cleaned with biocides in 2004,

wirhour apparent colonizarion. Bacterial DNA was

extracred from cach sampling using a merhod adaprcd co

smaU soil qllantiries as described previously (BASTIAN cr

al. ,2009).

From chc eleven samples, 696 clones were rerrieved.

Rarefacrion analysis showed 90% clone coverage indicating

thar the majoriry of the bacterial diversiry was derecred.

A considerable majo riry of rhe clone sequences rerrieved

could be assigned ro dehned Caxa, from which rhe 10 mosr

nllmerically dominam covered 533 clones or 76.6% of

che coral number of dones examined (Table 1) The (\Vo

most abundam Caxa were Ralstonia and Pseudomonas. The

cwo most abllndanc phylotypes in the cave \Vere Rtllstonia

mannitoliLytictl and Ralstonia pickettii. which cogether

represem 17.8% of rhe total clones. Ir is noceworrhy thar

only 5 sequen ces of PseudomoJlas jluorescens, a species wh ich

Geomicrobiology

\Vas reportcd ca be abundam in che cave (O RIAL AND

MERTZ, 2006) \Vere recorded. In concrase, 77 and 47

sequences cor responding respectively [Q R. mamzitoligtica

and R. pickettii \Vece dcrcctcd. 'TIlcre is unfocwnarely

no informarion on rhe bacteria present in Lascaux Cave

before benzalkon ium chloride trcatments and thercfore a

comparison of chese resules ro rhe pre-rourism microbial

coml11unities cannor be perfo rmed. However. rhe data

suggest thar yeaes ofbenzalkonium chloride trcamlCntS

in Lascaux Cave may have se!ectcd a mixed population of

RaLstonia and Pseudomonas, horh high ly resistant [O rhe

b iocide.

Tu. Total No. of clones (%)

Rlllslonüz 207 (29.7)

PsellllQ1l/onas 167 (24.0)

Escberichia 28(4.0)

Acbromobacur 25 (3 .6)

Jlfip;n 22 (3.2)

Oc"robactrum 20 (2.9)

Legio11l!/ltz 19 (2.7)

AlcaJigmes 15 (2.2)

Slmolrophomonas 15 (2.2)

To gauge the fungal diversity in Lascaux Cave. \Ve similarly

produced and analyzed a clone library offungal 18S rDNA

sequences. Six hundred and seven clones were panially

sequenced (750 bp) and sorted ioto phylorypes. The 10

most ahundam phylotypes represenced 59.2% of the clones

(Table 2). Only r\Vo our of rhese ren phylotypes are soil

fungi: Tricholoma saponaceum and Kraurogynmocllrpa l1'Ochieospora. while the others are emomophilous fungi.

including the well-known encomopathogens Isaria jizrinosa.

Engyodontium a/bum. Geosmithia putterilliiJ ctc. This

indicates that encomopathogcnic fungi play an importam

role in the cave and arthropods comrihuce ro the dispersion

of spotes.

Phylorype,

Penicillillm namyslolUskii

Isaria forinosll

Aspcrgillus versícolor

Tolypocladiu1IJ cylindrospomm

Tricholom(l sllponauu1Jl

Geomyces pllU1l0mm

GeosmitlJia ptttleríllii

Ellgyotlonlium a/bum

Kmurogynmocarpa lrocbleospom

C/Il/Jicipitacme sp.

Total No. of clones (%)

79 (13.0)

53 (8.7)

37 (6. 1)

32 (5.3)

30 (4 .9)

28 (4.6)

28 (4.6)

28 (4.6)

28 (4.6)

17 (2.8)


4. Arthropod Ecology

In the lase year. among other cavern icole anhropodsJ the

springrail Folsomia candida (Collembola. Isoromidae) was

found in Lascaux. Th is is a cosmopoli ran opporruniscic

croglophile (facultaeive cavern icole. frequenrly complecing

ies whole ti fe cycle in caves. buc nor confined ro rhis habi tar)

recorded from caves all over the \Vorld (PALAC IOS

VARGAS, 2002). Ir is generally accepred rhat this

springra it is found in cave sites wh ich are nor occupied by

cave-adapred species and in discurhed and artific ial areas.

This fics we ll wirh me hisrory ofLascaux as an example

of ecologicaUy disrurbed site where F. candida likcly was

attracted from the rop soil litcer ro the cave by che food

source thar represenred the fungal ourbreak.

Collembola are largely mycophagous and abundanr F.

candida specimens and were observed feeding on black

sra ins (Fig. 2). F. candida prefer feeding on melanised

fungal species (SC H EU AND SIMMERLING, 2004)

over hyaline fungi. but chey also feed on Fusarium hyphae

(SABATIN I AND INNOCENTI, 2000), several

Pseudomonas spp., including P. jluorescms (TH IMM er al.,

1998) and nematodes (LEE AND WIDDEN, 1996).

Table 2: Most abundant fungal phylotypes in

Lascaux Cave.

Folsonlia candida is a known vector fo r microorganisms.

DROMPH (2003) reporred that collembola can carry

enromopathogenic fungi, and GREIF AND CURRAH

(2007) isolatcd species of rhe fungal generaAcremoniumJ

Bearweria, C/adosporiumJ CryptendoxyiaJ GeomycesJ

GliocfadiunlJ HormiactisJ LeptograpbiumJ OidiodendronJ

Peniciffium J and Verticiffium from collembola. The

h igh density of coUembola rhat come in contan wirh

banerial cel ls, mycelial fragmenrs and spores suggest (hat

rhese arrhropods can help disperse bacteria (SCHEU


Geomicrobiology

ANO SIMMERLING, 2004) and fungi (THIMM et

al., 1998) rhrougho ur :ln environment. In addirion. che

gm of F. cllnd¡dll is a selecrive hab itar and a vec tor for

mieroorganisl11s (THIMM er al., 1998).

SABATIN I er al. (2004) showed rhar some eo llembola

preferred Fusllrium as foad and chat a few colon ies of

Fusarium developed from meir fecal pellets. We have observed chat when F. cand¡da is feedingon Lascaux black

srains. and on peat debris in che labofarory. chey have

produeed blaek fecal pellees. Also SAWAHATA (2006)

has ohserved che production of black fecal pcllers when

collembolans consumed che hymenial area of agaric fruje

bodies. Such fecal pellets can comain fu ngal spores that

ge rminare once deposircd on [he \Ver rack surface. Wh ile

che ahility of spores [O germinare may be reduced by gut

passage. ir is nor unccmman fo r almosr al! fecal peUecs

produced by archropods co concajn some germinable spores

(THIMM er al., 1998: WILLIAMS er al., 1998). Therefore,

i[ could be possible rhar collembolans concrihure co [he

sudden appearance of black srains everywhere in Lascaux

Cave, alrhough chis hypothesis needs tO be confirmed.

The presence ofF. candida in Lascaux Cave afte r rhe firsr

fungal ouebreak may be explained by ¡rs feeding preferences.

Fungi produce volarilc compounds rhar are potemially

amaerive ro eollembola (BENGTSSON er al, 1988).

Grazingon che black srains migh[ be a consequence of rhe

presence of melanised fungi in me black srains. lndeed rhese

are aIso rhe most paI.rabIe fungi for mires (SCHNEIDER

AND MARAVN, 2005) wh ieh suggest (har .su[vey for

rhis group of arrnropods should be carried Out in rhe cave.

lmeresringly. members o f rhe fam ily Campodeidae (Diplura)

were observed in rhe black srains (Figure 2). Mosr Diplura

are predacors and rhe ir dicr includes collemho la and mires.

They may also survive on vegerable debris and fungal mycelia.

S. Condusions This srudy raises imriguing quesrions about rhe pase.

present and fumre managemenr of show caves. In fucr.

microorganisms in Lascaux Cave grow as biofilms which

consise o f assembbgcs comaining many specics ofbacrcria.

fungi. prorozoa. erc. O ur research suggestS ehar as 3 resule

of yea rs ofhiocide rrearments, rhe indigenous microbial

communiries of Lascaux Cave have been replaced by

microbial populaeions selecred for by biocide applic3rion.

Ir appears rhar armropods conrribure co rhe dispers ion of

fungal spores inside rhe cave, likely by conraC r wirh rheir

bodies, disseminarion of rheir fecal pellers and growrh on

rheir cadavers. lhc composition of rhe funga l communiry



is largely inAuenced by arehropod colonizarion and acriv iry,

wirh rhe coUembola of primary significance. Colcopn: ra

likely playa role in fungal communiry srfUcture. however,

furrher srudies are needed co verify rhis and rhe degree of

associarion of Geosmitbia species with cave beedes.

The black srains in Lascaux Cave seem ro be related co rhe

presence and grazing effecrs oE rhe cavernicole popularion.

A earefuI study of rhe armropods, me fungal ecoIogy and

rhe dispersion patre rns is needed in o rder co complete OUt

undersrand ing of rhe food wcb and ro help connrm rhe

suggesred origin ofblack stains in rhe cave.

Acknowledgements We rhank rhe Spanish projeer CGL2006-07424/BOS for

support, rhe research projecr .. Microbiology.Microclimare",

from rhe Minisrry ofCulrure and Communication. France.

and facilities ar DRAC Aquiraine. Ms. M-A. Sire and

A. Moskalik-Deralle are aeknowIedgcd for rheir helpfuI

comments. FoLsomia cand¡da specimens, and picrures. Prof.

R.Jordana confirmed rhe collembola identification. This is a

TCP CSD2007-00058 papero

References ALLEMAND, L. (2003) Qt!.i sauvera Laseaux? La

Recherche 363, 26-33.

BASTIAN, E and C. ALABOVVETTE (2009) Lights

and shadows o n che conservarion of a rock are cave:

lhe case ofLascaux Cave. InternationaLjollrnal of

Speleology 38, 55-60

BENGTSSON, G., A. ERLANDSSON, and S.

RVNDGREN (1988) FungaI odour .maees so il

CoIlcmboIa. Soil Biology and Biochemistry 20, 25-30.

DE ROVX, E. (2007) Les fresques de Laseaux menaeées par

des lllois issures. L e /v/ondeo 26 November 2007.

DROMPH, K.M. Collembolans as vcerors of

entomoparhogenie fungi. Pedobiologia 47, 245-256

(2003).

DVPONT,j., C.)ACQYET, B. DENNETIERE,

s. LACOSTE, E BOVSTA, G. ORIAL,

C. CRVAVD. A. COVLOVX and M-E

ROQYEBERT (2007) Invasion of me Freneh

Paleolirhic painted cave ofLascaux by members cf

rhe Fusarium solani species complex. Mycologifl 99.

526-533

Geomicrobiology

AND SIMMERLING, 2004) and 'llngi (THIMM er

aI.~ 1998) rhroughour an environmcm. ln addirion. che

gur ofF cand¡da is a selecrive habitar and a vector for

microorganisms (THIMM ce aJ., 1998).

SABATlN I cr al. (2004) showed rhar sorne eollembola

preferred Fusarium as foad and rhat a few caJonies of Fusarium developed from rheir fecal pellers. We have

observed rhat when F. cand¡da is feedingon Lascaux black

nains, and on pear debris in rhe laborawry. rhey have

prodlleed blaek 'eeal pellees. Also SA\'ifAHATA (2006) has observed che production ofblack fecal pellers when coUembo lans consumed che hymenial afca of agaric fruir

bodies. Such fecal pellets can conrain fungal spores rhar germinare once deposired on rhe \Ver rack surface. While che abiliey of spores to germinare may be reduced by gm

passage, ir is IlQr uncommon for almosr a11 fecal peJlers

produced by arrhropods ro contain so me germinable spores

(THIMM er al., 1998; \'iflLLlAMS er al., 1998). Thedore, ir could be possible rhat collembolans conrribute ro the

sudden appearance ofblack stains everywhere in Lascaux

Cave, alrhough rhis hyporhesis needs ro be confirmed.

The presence ofF. candida in Lascaux Cave afrer rhe firsr

fungal outbreak may be explained by írs feeding preferenccs.

Fungi produce volarile compounds rhar are poremially

arrractive ro eollembola (BENGTSSON er al, 1988). Grazing on rhe black srains might be a consequence of the

presence of melanised fungí in rhe black srains. lndeed rhese

are . Iso rhe Illosr palarable limgi 'or mires (SCHNEIDER AND MARAUN, 2005) whieh suggesr rhar a survey for this group of arrhropods should be carried Out in rhe cave.

lnreresringly, members af rhe family Campodeidae (Diplura)

were observed in rhe black srains (Figure 2). Mase Diplura

are predarors and rhe ir dier ineludes collembola and mires.

They may also survive on vegerable debris and fWlgaI mycelia.

S. Conclusions This srudy raises inrriguing quesrions abour rhe pasr.

presenr and furure managemem of show caves. ln facr,

microorganisl11s in Lascaux Cave grow as biofilms which

consise of assemblages comain ing many species ofbaceeria,

fungí, prorozoa, erc. Our research suggesrs rhar as a resul r

ofyears ofbiocíde rrearmcnts, rhe ind igenous microbial

communicies ofLascaux Cave have been replaced by

microbial popularíons selecred for by biocide applicarion.

Ir appears rhar arrhropods contribure ro che dispersion of

fungal spares inside rhe cave.likely by contact wieh rheir

bodies. disscminarion of rheir fecal pelle ts and growrh on

cheir cadavcrs. The composirion of rhe fungal communiry

lSth International Congress of Speleology


is largcly inAuenced by arrhropod colonizar ion and acriviry,

wirh che collembola of primary significance. Coleopcera

likely playa role in fungal coml11uniry srrtlcrure, however,

furrher srudies are needed ro verify rhis :lI1d rhe degree of

assoc iatiol1 of Geosmithia species wich cave beedes.

The black sra ins in Lascaux Cave seem ro be relared ro [he

presence and grazing effects of che cavernicole popularion.

A eareful srudy o, rhe arrnropods, rhe fungal eeology and rhe dispersion parrerns is needed in o rder ro complece our

underseanding of rhe food web and ro help confirm rhe

suggesced origín ofblack sca ins in rhe cave.

Acknowledgemcnts \'ife rhank rhe Spanish projeer CG L2006-07424/ BOS 'or supporr. rhe research projece "Microbiology-Microdimare".

from chc Mínisrry ofCulrure and Commun ícarion, France,

and fac ilities ar DRAC Aquiraine. Ms. M-A. Sire and

A. Moskalik-Derallc are aeknowlcdged for rheir help'ul commenrs, Folsomia candida specimcns. and picrures. Prof.

R. Jordana confirmed rhe collembola identificarion. This is a

TCP CSD2007-00058 papero

References ALLEMAND, L. (2003) ~ sauvera Laseaux? La

Recberche 363, 26-33.

BASTIAN, E and C. ALABOUVETTE (2009) Lighrs and shado\Vs 011 che conservarían of a rock are cave:

11lC case of Lascaux Cave. InternlltionaLjouYnIlL of Speleology 38, 55-60

BENGTSSON, G., A. ERLANDSSON, and S. RUNDGREN (1988) Fungal odour amactssoil

Collembola. Soil Biology dnd Biochemistry 20, 25-30.

DE ROUX, E. (2007) Les 'resques de Laseaux menaeées par des l11 oisissures. Le Jv[onde, 26 Novcmber 2007.

DROMPH, K.M. Collembolans as veerors o,

enromoparhogenie 'ungi. Pedobiologia 47, 245-256 (2003).

DUPONT,j., C.)ACCCUET, B. DENNETIERE, S. LACOSTE, E BOUSTA, G. ORIAL,

C. C RUAUD, A. COULOUX and M-E RO~EBERT (2007) Invasion of rhe Freneh Paleolithic painced cave ofLascaux by members of

che Fusarium softllli species complex. Nfycofogia 99,

526-533

Geomicrobiology

FOX.].L. (2008) So me say Laseaux Cave paintings are in

microbial "crisis" mode. Miaobe 3, 110- 112.

GREIF. M.D. and R.S. CURRAH (2007) Patrerns in

che occurrence of saprophytic fungi carried by anhropods caught in traps baited w jrh roned wood

and dung. M)'cologia 99. 7-19.

GUNDE-CIMERMAN. N .• P. ZALAR. and S. JERAM.

(1998) MyeoAora of cave erieker Troglophilu, neglectus eadavers. Mycopathologia 141. 111 - 114.

KUBÁTOVÁ. A. and L. DVORÁK (2005) Emomopachogenic fungi associated w ith ¡nsece

hibernat ing in underground shelters. Czech Mycology 57.221-237.

LEE. Q and P. WlDDEN (1996) Folsomia candida. a "fungivorous" co llembolan. feeds preferencially on

nematodes racher man so il fungi . Soil Biology tlnd Biochemistry 28. 689-690.

LEFÉVRE. M. (1974) La maladie verte de Laseaux. Studies in Conservation 19, 126- 156.

ORIAL. G. andJ-D. MERTZ (2006) Eeudeer suivi des

phénomenes microbiologiques.lvlonumenta! 2 ,

76-86.

PALAC IOS-VARGAS.].G. (2002) La disrriblleión

geográfica de los Collembola en el mundo

subterráneo. Boletin de la Sociedad Venezolana de

Espeleologia 36.1-5.

SABATIN I. M.A. and G. INNOCENTI (2000) Soil

borne plant pathogenic fungi in relation to some

collembolan species under laborarory conditions.

MycologyResearch 104. 1197-1201.

SABATlN I. M.A .. M. VENTURA. and G. INNOCENTI

(2004) Do Collembola affecc rhe comperitive

relationships among so il-borne plant parhogenic

fungi? Pedobiologia 48. 603-608.


SAMSON. R.A .. J-P. LATGE. and H.e. EVANS (1988) Atlas ofEntomopathogenic Fungi. Springer Verlag,

Berlin.

SAWAHATA. T. (2006) Hymenial area of agarie ffUir

bodies consumed by Collembo la. Mycoscience 47,

91-93.

SCHABEREITER-GU RTNER. e.. e. SAIZ-JIMENEZ.

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