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PlantSignalBehav.2009Jun4(6):554556.

PMCID:PMC2688311

doi:10.4161/psb.4.6.8733

Antplantmutualismsshouldbeviewedassymbioticcommunities
RumsasBlatrix, 1SalahBouamer, 2SergeMorand, 3andMarcAndrSelosse1
1
Centred'EcologieFonctionnelleetEvolutiveMontpellier,France
2
CentredeBiologieetdeGestiondesPopulationsMontferriersurLez,France
3
InstitutdesSciencesdel'EvolutiondeMontpellierMontpellier,France
Correspondingauthor.
Correspondenceto:RumsasBlatrixCentred'EcologieFonctionnelleetEvolutiveUMR5175CNRS1919routedeMendeMontpelliercedex534093
FranceEmail:blatrix@cefe.cnrs.fr
Received2009Apr14Accepted2009Apr15.
Copyright2009LandesBioscience

Seethearticle"Antplantsandfungi:anewthreewaysymbiosis."inNewPhytol,volume182onpage942.
ThisarticlehasbeencitedbyotherarticlesinPMC.

Abstract

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Antplantsprovidefoodandnestingspace(domatia)forantsthatprotectthemagainstherbivores.These
mutualismsareoftenveryspecificandareusuallyconsideredasbipartite,ortripartitewhenantsusehemipteransas
trophobionts.However,fungigrowinginsidedomatiahavebeenrecordedbyafewauthors.Herewereporton
theiroccurrenceonadditionalantplantsfromAfrica,AsiaandSouthAmerica.Wedemonstratedthesymbiotic
natureoftherelationshipbetweentheplant,theantandthefungusinthemodelplantLeonardoxaafricana
africanaanditsmutualisticantPetalomyrmexphylax.Moreover,datasuggesttheantfungusrelationshipis
mutualistic.Herewediscussthemostprobableroleofthefungusandthepotentialimplicationsonthe
understandingofnutritionalecologyofantplantsymbioses.Thefungusisalsoassociatedwiththepresenceof
nematodesandbacteria.Manyantplantsymbiosespreviouslyconsideredtobebipartitewillsoonlikelyproveto
bemultipartitesymbioticcommunities.
Keywords:symbiosis,mutualism,antplant,fungi,communityecology,Leonardoxa,coevolution,nematodes
Intropicalforests,someplantsknownasantplants,ormyrmecophytes,areengagedwithantsintight,often
obligatoryrelationships.Theseplantshavespecialisedhollowstructures,calleddomatia,tohostantcolonies.Such
structuresinvolvestems,thorns,stipules,petiolesorleaves,dependingonthespecies.Moreover,theseplants
produceextrafloralnectarand/orfoodbodiestosustaintheirantcolony.Inmutualisticinteractions,antscontribute
toprotectingtheplantagainstherbivores,1fungalpathogens2andcompetingplants.3Thesemutualismshave
focusedtheattentionfordecadesbecauseofthespectacularnatureofcoevolvedtraits.Atthebeginningofthe20th
century,afewauthorsreportedthepresenceoffungiwithinantplantsbelongingtoatotalof11genera.47Within
thelastfourdecades,publicationsonantplantshaveincreasedatanexponentialrate,butveryfewauthorshave
takenfungiintoaccount.8,9Recently,wedescribednewcasesoffungigrowinginantplantsand,forthefirsttime,
investigatedthenatureoftherelationship.10
TheantplantLeonardoxaafricanaafricana(Fabaceae)isendemictoanarrowstripofcoastallowlandrainforest
insouthernCameroon.11EachplantisoccupiedbyasinglecolonyofthemutualisticantPetalomyrmexphylax.12
However,themutualisticcolonyissometimesreplacedbyCataulacusmckeyi,anantconsideredasaparasiteof
themutualismbecauseittakesadvantageofnestingspaceandfoliarnectarwithoutprotectingtheplant.13Wenow
havedissectedmorethan1,200domatiafrommorethan150plantsoccupiedbyP.phylax.Morethan95%ofthe
domatiawiththemutualisticantshavefungus.Ontheotherhand,unopeneddomatiaanddomatiafromunoccupied

plantsorplantsoccupiedbyC.mckeyibearnofungus.Thus,theoccurrenceofthefungusisstrictlytiedtothe
presenceofthemutualisticant.Moreover,inyoungdomatiathathavebeenonlyveryrecentlyopenedand
occupiedbytheants,thefungalpatchisnotdistinguishablebyvisualinspection,butapileofverysmallpiecesof
rubbleordetritusispresent.Asdomatiabecomeolderaverysmallpatchoffungusisseentobeassociatedwith
thepileofrubble.Thus,mutualisticantsmayactivelypropagatethefungus.Recordingantbehaviourinsidethe
domatiawithanendoscoperevealedanotherspecificantbehaviour:onafewoccasionsantswereseenchewingthe
fungalmatandcuttingoffapieceofit.Thiscouldexplaintheregularandhighlylocalizedsizeoffungalpatches,a
veryunusualfeaturetoanymycologist'seye.
Sequencinginternaltranscribedspacer(ITS)ofribosomalDNAofthefungifromfourindividualsofL.a.africana
showedthesamespeciesacrosssamples.Inthissystem,theplantantfungusassociationseemsspecific.This
fungus,aswellasthoseidentifiedfromtwootherantplants(Barteriafistulosa[Passifloraceae]andKeetiahispida
[Rubiaceae]),belongtotheAscomycotaorderChaetothyriales.Antmediatedpropagationofthefungus,specific
antbehaviourtowardthefungusandspeciesspecificityoftheassociationclearlydemonstratethesymbioticnature
ofthisplantantfungusassociation.AlltheP.phylaxcoloniesweinvestigated(morethan150,alloverthe
distributionarea)hadfungusintheirhostplant.Theantfungusassociationisthusconstant.Moreover,domatiathat
wedisturbedinthecourseofourexperiments(byrepeatedlydrillingandmanipulatingthem)wereeventually
desertedbytheantsandthefungus,suggestingthattheantshadremoveditwhentheyfled.Suchbehaviourtoward
aparasiteisratherunlikely.Thus,datafromourstudymodelsuggestthattheantandthefungushaverathera
mutualisticrelationship.Butstill,themutualisticnatureoftherelationshipremainstobedemonstrated.Otherant
plantsystemshavetobeinvestigatedtofullyunderstandevolutionarydiversificationoftheseantplantfungal
symbioses.
Whetherthefungusismutualisticcanbeestablishedbyelucidatingitsroleinthethreewaysystem.Fungiareused
bytheantsAllomerusdecemarticulatusandLasius,respectivelytobuildatrapfacilitatingthecaptureoflarge
prey14andtoreinforcenestwalls(occasionallyinvolvingChaetothyriales).15IneachdomatiumofL.a.africana,
thefungusappearsintheformofathindiscoidpatch,usuallylessthan1cmindiameter,ofhyphae.Astructural
roleofthefungusisthusveryunlikely.Infact,onlytwohypothesesappearplausible.First,thefungalpatchcould
serveasanutrientrecycler,allowingalltherefuseproducedbythecolonytobetransformedintonutrientforms
availabletotheplant,oreventotheants.Second,thefunguscouldbeafoodsourcefortheants,asisthecasefor
Attineants16andforEuprenolepisprocera,whichreliesentirelyonnaturallygrowingmushrooms.17Thesetwo
hypothesesarenotmutuallyexclusive.Indeed,almosteveryfungalpatchisassociatedwiththerefusepileofthe
colonycontainingfragmentsofinsectcuticleinwhichwerecognisedpartsofthemutualistants,amongother
unidentifiabledebris.Bycontrast,domatiaoccupiedbytheparasiticantC.mckeyi,whichdonothavefungus,do
notcontainarefusepile.Moreover,antswereseendefecatingonthefungalpatch.Theseobservationsarguein
favourofthefirsthypothesis.Butthechewingofthefungusinastereotypedmannerisreminiscentofpruning
behaviourbytheNewWorldfungusgrowingants(Attini),whichgrowfungusasastaplefood.
Nutrientbalanceinplantantsisconsiderednitrogenlimitedbecauseplantexudatesandhoneydewconstitute
supposedlythemostimportantpartoftheirdiet.1820Symbioticbacteriahavebeenidentifiedinthegutofseveral
antspecies.21,22Suchsymbiontsinplantantscouldprovideessentialaminoacidsorhelpfixingnitrogen.Ifthe
fungigrownbyplantantsprovetobeafoodsource,itwouldcertainlyrevolutionizeourunderstandingofthe
nutritionalecologyofantplantsymbioses.
Ourearlystageinvestigationofantplant/ant/fungirelationshipsledustorealisethatmoreorganismsmaybe
involvedindomatiafunctioning.First,nematodesabundinfungalpatchesofalmostallspecies.Theywerealready
noticedinsomeoftheearlydescriptionsofthefungi.Theycanbeseenunderthebinocularandtheirmovements
canevenbedetectedbythenakedeye,especiallyinthelargefungalpatchesinB.fistulosaoccupiedbyT.
aethiops.ThoseweidentifiedfromcoloniesoftheplantantsT.aethiopsandP.phylaxbelongtothegenus
Pelodera,nematodegrazersfeedingonbacteria.23Second,transmissionelectronmicroscopyonthefungalpatches
revealedaworldofmicroorganismsincludingnumerousbacteria.Moreover,manyplantantsareknowntorear
hemipteransforfoodwithindomatia.24Thepresenceofhemipteransandfungiisnotexclusivebecauseseveral
plantants,suchasAphomomyrmexafer(inL.a.letouzeyi),T.aethiops(inB.fistulosa)andCrematogaster(inK.
hispida),haveboth.Eveniftherolesofthenewlyidentifiedpartnersinantplantsymbiosesarenotyetfully

understood,thepotentialfordiscoveringnewsymbiontsisgreat.Itisnoteworthythatthefirstorganismstobe
identifiedintheantplantsymbiosesweretheplant,theantandthehemipterans,allthreebigenoughtobeobvious
tothenakedeye.Then,thelessevidentfungiandnematodescameonstage.Andtheinvisiblemicroorganismswill
probablydosointhenearfuture.Thisdiscoverysequenceiscertainlyduetotechnologicallimitationsandraising
interestfortheinvisiblebiodiversity.Itishighlyreminiscentofthestoryoffungusgrowingantresearch.Despite
theecologicalandeconomicimportanceofsomeattines(Attaisapestofagricultureintheneotropics),their
symbioticrelationshipwithfungiwasevidencedonlyattheendof19thcentury.Attinefungussymbiosisstartedto
beconsideredasasymbioticcommunityonly20yearsago,whenantswerediscoveredtohostspecialised
antibioticproducingbacteriatoprotecttheirmutualisticfungusagainstafungalparasite.25,26Onlyrecentadvances
inmoleculartechnologyallowtheidentificationofnewsymbiontsandelucidationoftheirroles.27Wearethus
confidentthatsimilartoolsappliedtoantplantassociatedcommunitieswillrevealacomplexsymbioticcommunity.
Inadditiontothe11antplantgenerareportedtohostfungiatthebeginningofthe20thcentury,ourown
investigations(includingveryrecentfindings)showedfungiinsixmoregenera:Leonardoxa,Calpocalyx
(Fabaceae),Keetia(Rubiaceae)andVitex(Lamiaceae)fromCameroon,10Tachigali(Fabaceae)fromFrench
Guiana,andDrypetes(Euphorbiaceae)fromBorneo(kindlyprovidedbyJoachimMoog).Thepreliminary
dissectionofafewleafpouchesofTococa(Melastomataceae)andhollowstemsofCecropia(Cecropiaceae)from
FrenchGuianadidnotshowanyvisiblefungalpatch.Nevertheless,fungioccurintropicalantplantssymbioses
onallcontinents.Thisisthusaverycommonandwidespreadphenomenon,whichhasbeenoverlooked.Thesmall
windowopenedonthesesymbioticcommunitieshashighlightedmanypromisingresearchdirections.
Acknowledgements

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WethankDoyleMcKeyforcommentingandproofreadingthemanuscript.Theresearchleadingtotheseresults
hasreceivedfundingfromtwograntsfromtheFrenchAgenceNationaledelaRecherche:onefromtheYoung
scientistsprogramme(researchagreementno.ANR06CC0127)andonefromtheBiodiversityprogramme
(IFORAproject).
Notes

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Addendumto:DefossezE,SelosseMA,DuboisMP,MondolotL,FaccioA,DjietoLordonC,etal.Antplants
andfungi:anewthreewaysymbiosisNewPhytol2009Inpressdoi:10.1111/j.14698137.2009.02793.x.
Footnotes

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PreviouslypublishedonlineasaPlantSignaling&BehaviorEpublication:
http://www.landesbioscience.com/journals/psb/article/8733

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