40Microbialecologyofbiologicalinvasions

MINI-REVIEWMicrobialecologyofbiologicalinvasionsWimHvanderPutten1,2,JohnNKlironomos3andDavidAWardle4,51DepartmentofMultitrophicInteractions,NetherlandsInstituteofEcology,Heteren,TheNetherlands;2LaboratoryofNematology,WageningenUniversity,Wageningen,TheNetherlands;3DepartmentofIntegrativeBiology,UniversityofGuelph,Guelph,Ontario,Canada;4DepartmentofForestVegetationEcology,SwedishUniversityofAgriculturalSciences,Umea˚,Swedenand5LandcareResearch,Lincoln,NewZealandInvasivemicrobes,plantsandanimalsareamajorthreattothecompositionandfunctioningofecosystems;however,themechanisticbasisofwhyexoticspeciescanbesoabundantanddisruptiveisnotwellunderstood.Moststudieshavefocusedoninvasiveplantsandanimals,althoughfewhaveconsideredtheeffectsofinvasivemicrobes,orinteractionsofinvasiveplantandanimalspecieswithmicrobialcommunities.Here,werevieweffectsofinvasiveplantsonsoilmicrobialcommunitiesanddiscussconsequencesforplantperformance,plantcommunitystructureandecosystemprocesses.Inaddition,webrieflydiscusseffectsofinvasivesoilmicrobesonplantcommunities,whichhasbeenlesswellstudied,andeffectsofinvasiveanimalsonsoildecomposersandecosystemfunctioning.Wedothisbyconsideringeachofthreeimportantfunctionalgroupsofmicrobes,namelysoilmicrobialparasitesandpathogens,mutualisticsymbiontsanddecomposers.Weconcludethatinvasiveplants,pathogenicandsymbioticsoilmicrobeswillhavestrongesteffectsontheabundanceofindividualspecies,communitydiversityandecosystemfunctioning.Invasivedecomposermicrobesprobablyhavelittleimpact,becauseoflimitedspecificityandgreatfunctionalredundancy.However,invasiveplantsandanimalscanhavemajoreffectsonmicrobialdecompositioninsoil.Weproposethatunderstanding,predictingandcounteractingconsequencesofenhancedglobalhomogenizationofnaturalcommunitiesthroughintroducingexoticplants,animalsandmicrobeswillrequirefuturestudiesonhowpathogenic,symbioticanddecomposersoilmicrobesinteract,howtheyareinfluencedbyhighertrophiclevelorganismsandhowtheircombinedeffectsareinfluencingthecompositionandfunctioningofecosystems.TheISMEJournal(2007)1,28–37;doi:10.1038/ismej.2007.9Keywords:plantinvasion;invasivesoilmicrobes;invasiveanimals;naturalenemies;ecosystemprocesses;climatewarmingIntroductionOneofthemajorchallengesofecologyistounder-standwhatcontrolstheabundanceanddiversityofspecies,howtheseareinfluencedbynaturalorhuman-inducedchanges,andwhataretheconse-quencesforecosystemprocessesandproperties.Thedifficultiesthatwehaveinunderstandingandforecastingbiologicalinvasionsshowthattherearemajorquestionstobesolved,especiallybecauseglobalizationandclimatewarmingenhancethemovementofspeciesand,therefore,theincidenceofinvasivespecies.Biologicalinvasionsofexoticspeciesareconsideredtobeamongthemostseriousthreatstolocalbiodiversityandecosystemfunction-inginterrestrialecosystems(MooneyandHobbs,2000).Traditionally,therehasbeenmuchinterestinthevisiblecomponentsofecosystems,suchasinvasiveplantsandabovegroundanimals(Elton,1958;Williamson,1996).However,thesevisiblebiotacanhavemajorimpactsonthemoreinvisible,microbialcomponentsofecosystemsandontheprocessesthatmicrobesdrive.Moreover,thereisincreasingawarenessofinvasivemicrobes,includ-inghuman,animalorplantdiseases,whichcaninsomecaseschangetheappearanceandfunctioningofentireecosystems(Liebholdetal.,1995;Gerlach,2001;Julesetal.,2002;Niwaetal.,2004;WaringandO’Hara,2005).Here,wewillrevieweffectsofinvasiveplantsonsoilmicrobialcommunitiesandnativeplantcom-munitycomposition.Inaddition,wewillbrieflyrevieweffectsofinvasivesoilmicrobesonplantcommunitiesandeffectsofinvasiveanimalsonsoilmicrobialcommunitiesandecosystemprocesses.Ourreviewisnotexhaustive,butitshowsthecurrenttrendsinthisfieldofecology,andourlengthofdiscussionontheseveraltopicsisroughlyinReceived5February2007;revisedandaccepted21February2007Correspondence:ProfessorWHvanderPutten,DepartmentofMultitrophicInteractions,NetherlandsInstituteofEcology,POBox40,Boterhoeksestraat48,6666ZGHeteren,TheNetherlands.E-mail:[e-mail](2007)1,28–37&2007InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/07$30.00(Hooperetal.,2000;Woltersetal.,2000;Scheu,2001;VanderPuttenetal.,2001;Wardleetal.,2004).Biologicalinvasionsinvolveexoticspeciesthathavebeenintroduced,accidentallyorincidentally,fromoneregionintoanotherregionseparatedbygeographicalbarriers,suchasoceansormountainridgesandwhichbecomenon-proportionallyabun-dantintheirnewrange(Williamson,1996).Therearenumerousdocumentedexamplesofbiologicalinvasions,butthenumberofexamplesinvolvingsoilmicrobesarerelativelyrare.Thusfar,researchonbiologicalinvasionshasbeenstronglydominatedbystudiesthatdescribepatterns,whereasonlysome5%ofthepublishedstudieshaveattemptedtoexperimentallyanalysewhatcausesbiologicalinva-si