EcologicalandevolutionaryconsequencesofbiotichomogenizationJulianD.Old - PDF document

EcologicalandevolutionaryconsequencesofbiotichomogenizationJulianD.Olden,N.LeRoyPoff,MarlisR.Douglas,MichaelE.DouglasKurtD.FauschDepartmentofBiology,ColoradoStateUniversity,FortCollins,CO80523,USAGraduateDegreePrograminEcology,ColoradoStateUniversity,FortCollins,CO80523,USADepartmentofFisheryandWildlifeBiology,ColoradoStateUniversity,FortCollins,CO80523,USABiotichomogenization,thegradualreplacementofnativebiotasbylocallyexpandingnon-natives,isaglobalprocessthatdiminishesßoralandfaunaldistinc- Correspondingauthor:JulianD.Olden(olden@lamar.colostate.edu). TRENDSinEcologyandEvolutionVol.19No.1January20040169-5347/$-seefrontmatter2003ElsevierLtd.Allrightsreserved.doi:10.1016/j.tree.2003.09.010 mechanisms:(i)intentionaltranslocationofpopulationsfromonepartoftherangetoanother;(ii)intentionalintroductionsofspeciesoutsideoftheirnormalranges;and(iii)extirpationoflocalorregionalfaunas.Genetichomogenizationisaseriousbutoftenlessrecognizedthreattotheintegrityofendemicgenepools,andcanhaveseveralimportantimplications.Translocationofpopulation(s)wouldenhancethepotentialforintraspeciÞchybridization,withtheendresultbeingtheassimilationofpreviouslydifferentiatedgenepoolspools.Introductionsofspeciesoutsideoftheiroriginalrange(s)couldresultinafoundereffectandyieldreducedlevelsofgeneticvariability,aswellassettingthestageforinterspeciÞchybridizationhybridization.AndÞnally,ifextirpationswereacauseforfaunalhomogenization,thenoneconsequencemightbebottleneck(s)inlocalpopu-lationsoftheimpactedspecies,alongwithloweredeffectivepopulationsize(s)size(s).Thiswouldoccurdirectlyviaremovalofindividualsfromsourcepopulations,orindirectlybyhabitatmodiÞcations.Here,weexplaintheseconsiderationsingreaterdetail.IntraspeciÞchybridizationIntraspeciÞchybridizationcanhomogenizetheuniquecharacteristicsofgeographicallydistinctpopulationspopulations,aswellascompromisetheÞtnessofindividualsbydisruptinglocaladaptationsadaptations.IntentionalintraspeciÞcintroductions(eithertoreplaceortosupplementdecliningorextirpatedpopulations)oftenresultinanovertlossofgeneticvariabilityvariability,resultingfromfoundereffects,bottlenecksandtheresultinglowgeneticvariabilitythattheyengender(e.g.(e.g.).Forexample,globalstockingofcutthroattroutOncorhynchusclarkifromasinglesourceregionhasyieldedsubstantialgenetichomogenizationand,inatleastoneinstance,hasplayedaprimaryroleinthelossofageneticallydistinctsubspeciessubspecies.Asabove,widespreadaquaculturepracticesareoftenthecatalystforsuchhomogenizationinmanyÞshspecies,yetramiÞca-tionsareonlynowbeingunraveledunraveled.Genetichomogenizationofpopulationscanalsoinßu-encethecapacityofaspeciestoexpanditsdistribution.Mixingoflocallyadaptedpopulations(e.g.peripheralwithcentral)canimpedespeciesexpansion,becausepheno-typesfavoredincentralareasmightbemaladaptedforconditionsencounteredatthedistributionalperipheryry.Similarly,intraspeciÞchybridizationandsub-sequentbreakdownofregionaldistinctivenesscanalsoincreasevulnerabilitytoinvasionand,conversely,mightenhancethesuccessofhybridcompetitorscompetitors.Itmightevenpromotetheexpansionandultimatesuccessoftheinvadingspecies.AninterestingexampleofthelatterinvolvestheArgentineantLinepithemahumile.Here,spatialsegregationofnestsisdeterminedgeneticallybyinnateaggressionagainstnon-nestmatesnon-nestmates.However,recentlyinvadingpopulationsinCaliforniaexperiencedageneticbottleneckowingtofoundereffectsthatresultedinwidespreadgeneticsimilarityamongpopulations.This,inturn,reducedintraspeciÞcaggressionandpromotedtheformationofaggressivesupercoloniesthatsigniÞcantlyimpactedcommunity-andecosystem-levelprocessesprocesses.Developmentofsingle,largecoloniesmightbeunstableoverthelongtermterm,yetamoreimmediatesolutionwassoughttoenhancetherecoveryofinvadedecosystems.Onesolutionwastointroducenewallelesintotheinvasivepopulationssoastoreducegenetichomogeneityandeliminatewidespreaddevelopmentofsupercoloniessupercolonies.Clearly,geneticconsequencesofhomogenization,particu-larlywithregardtoinvaderandresident,areonlynowbeginningtobeunderstood.Thisisasmuchafunctionoftechnologicaldevelopments(suchasapplicationofsinglenucleotidepolymorphismstopopulation-levelproblemsproblems)asitisoftheoreticaldevelopment.InterspeciÞchybridizationHybridizationbetweengeneticallydistinctspeciescancreatenewadaptivesystemsand,thus,newecologicalecological.Thisisparticularlyevidentinaquaticecosystems,wherehuman-mediateddispersalhas Box1.Measuringgenetic,taxonomicandfunctionalBiotichomogenization,whetherreferringtogenetic,taxonomicorfunctionalhomogenization,isdeÞnedasanincreaseinthespatialsimilarityofaparticularbiologicalvariableovertime,andisusuallyevaluatedbycomparingtheaveragepairwisesimilarityofthevariablecalculatedattwodiscretetimes.GenetichomogenizationcanbequantiÞedusingavarietyofgeneticcharacteristics,suchasthealleliccompositionofaparticularlocusorsetofloci(i.e.identityofgenotypes),theirfrequencies(i.e.relativeabundanceofgenotypes),orbyoneofmanymetricsderivedfromtheaboveparameters,suchaspercentpolymorphicloci,meannumberofallelesperlocusandmeanheterozygosity.Inaddition,levelsofpopulationdivergencecanalsobeassessedbyindicesofgeneticsimilaritysuchasorusingavarietyofclusteranalyses(e.g.Bayesianinference).Thesemeasuresofgeneticdiversityareusuallyassessedinacomparativespatialframework(i.e.introducedversussourcepopulation,ordisturbedversusnondisturbedpopulations),buttheyarerarelyexaminedinatemporalframework(i.e.pre-andpostdisturbance),simplybecausenogeneticbaselinedatawerecollectedbeforethehomogenizationevent.Itisinthistemporalcontextwhereresearchisneededtoelucidategeneticconsequencesofhomogenization.Furthermore,thechoiceofgeneticmarkers(i.e.levelofresolution)iscrucialtodetectthepotentialsubtlegeneticdifferencesinherenttohomogenization.Taxonomichomogenizationiscalculatedusingspeciespresenceorabsencedatatoexaminethedegreeofsimilarityincommunitycomposition,andcanbequantiÞedusinganyoneofasuiteofsimilarityindices,diversityindices,clusteranalysesorordinationapproaches.Ofthemanysimilarityindicesusedinecologyforquantifyingcommunitysimilarity,JaccardÕscoefÞcient(basedonspeciesoccurrencedata)isemployedalmostexclusivelyinhom-ogenizationstudies.Otherapproachesincludeusingdiversitytoquantifyspatialturnoverofspecies,comparisonofspeciessimilaritybasedonclustermembershipofcommunities,andtheexaminationofpositionanddistancebetweencommunitiesinreduced,species-ordinationspace.FunctionalhomogenizationcanbecalculatedinasimilarfashionbyÞrstcalculatingthesite-by-traitmatrix(inthesimplestcase,calculatedastheproductofthespecies-by-sitematrixandthetrait-by-speciesmatrix)andthenexaminingcommunitysimilarityusingoneofthesameapproachesfortaxonomichomogenization.Communitysimilarityinfunctionalcharacteristicscouldbeassessedbasedonthepresenceorabsenceofspeciestraitsorthefrequencydistributionoftraitsinthecommunity.Whetherthespeciestraitsarediscrete(binaryormulti-state)orcontinuouswilldictatethechoiceofsimilaritycoefÞcientormultivariatestatisticalapproach. TRENDSinEcologyandEvolutionVol.19No.1January2004 promotednumerousanddramatichybridizationeventsevents.Fishprovidethebestexamples,owingsimplytotheirexternalmodeoffertilizationcoupledwithweaklydevel-opedreproductiveisolatingmechanismsmechanisms.Thesitu-ationbecomesexacerbatedwhentheintroducedÞshhasevolvedallopatrically,yetiscloselyrelatedtotheindigenousone.TheposterchildforthisphenomenonareindigenoussalmonidÞshesofNorthAmericaAmerica.Wepositthatmechanismsdrivinggenetichomogeniz-ationareactuallysynergisticandthathumaninterven-tions(asabove)simplyamplifythepotentialforhybridizationwithinagivensystem.Human-mediated,long-distancedispersalandcolonizationevents,forexample,elevatetheprobabilitythatpairwiseinteractionsbetweenspecieswillyieldhybrids,whilsthuman-pro-vokedenvironmentaldisturbanceswilllikewiseprovidehabitatsthataresuitableforhybridprogenyprogeny.ThishumandimensionsaspectenhancestheprobabilitythatÔhybridswarmsÕwillgeneticallyextirpatenativetaxataxa.Althoughsucheventsarethoughttooccurovermanyyears,evendecades(aswithtrout),examplesdoexistwheregeneticswampinghasoccurredwithinabbreviatedtimeframes.Forexample,withinafour-yearperiodfollowingitsintroduction,theexoticpupÞshwasinvolvedinalarge-scaleintrogressivehybridizationeventwiththeendemicC.pecosensis430kmofthePecosRiverinNewMexicoMexico.Geneticswampingcanoccurrelativelyrapidlyandoverextendeddistances,andtheseriousnessofthisphenomenoncannotbeunderestimatedsimplybecauseitseffectsaredeemedslowerthan,say,overtpredation.Insummary,inspiteofalimitednumberofstudies,itisapparentthatmuchuncertaintyremainsregardingtheecologicalconsequencesofgenetichomogenization.Thistopicclearlydeservesfurtherinvestigation.Indeed,genetichomogenizationmightgaingreaterattentioninthefuturegiventheemergenceoftheÞeldoflandscapelandscapeandtheimportanceofpopulationdiversityforecosystemservicesservices.CausesandconsequencesoftaxonomicandfunctionalhomogenizationforcommunitiesandecosystemsTodate,scientiÞcresearchonhomogenizationhasbeenpursuedlargelyfromaphylogeneticperspectiveperspective,wherethetermÔtaxonomichomogenizationÕisusedtodescribeanincreaseinthecompositionalsimilarityamongcommunitiesowingtothesuccessfulinvasionofÔwinningÕspeciesandtheextirpationofÔlosingÕspeciesspecies(Box1Accountingfortaxonomicchangeincommunitiesisimportantandachievedrelativelyeasilyeasily;however,ecologicallyprofoundfunctionalchangesmightoccurinhomogenizedcommunitiesthatarelargelyindependentoftaxonomicidentity.Thus,amoresubtleecologicalexam-inationofhomogenizationisrequired.Speciescontributeindividuallyandcollectivelytothefunctionalstabilityofcommunitiesandecosystems.Winnersandlosersinthehomogenizationlotteryarenotrandomlydistributedtaxonomically;rather,invasionsuccessandextirpationvulnerabilityareprimarilydeÞnedbytheinteractionbetweenintrinsicspeciestraitsandextrinsicenvironmentalcharacteristicscharacteristics.EcologicalimplicationsofbiotichomogenizationmightbemoreproÞtablyexaminedbyconsideringÔfunctionaldiversityÕ(i.e.thecompositionofandvariationincommunitytraits,anditsspatialdistributionacrosslandscapes)(Box1Modifyingthefunctionaldiversityofacommunitymightresultinfunctionalhomogenizationinvolvingthereplace-mentofecologicalspecialistsbythesamewidespreadgeneralists.Althoughfunctionaldiversityisrecognizedasadeterminantofecosystemprocessesprocesses,theimportanceoffunctionalhomogenizationhasreceivedinadequateWepresentaconceptualmodeltoassessthemannerinwhichspeciesintroductionsand/orextirpationscanleadtofunctionalhomogenizationwithsubsequentchangesinoverallcommunityfunctionandareductioninecosystemresilience(Box2).ModiÞcationstowithin-andbetween-communitytraitcompositionswillprobablyimpingeuponcommunityandecosystemfunction,andresistancetoenvironmentalchange.Adecreaseinfunctionaldiversitymightreduceoverallcommunityandecosystemfunction-function-,stabilitystabilityandresistancetoenvironmentalchangebysimplynarrowingtheavailablerangeofspecies-speciÞcresponsesresponses.Consideraseveredrought(thedisturbanceoval;Box2,FigureIb)thatstronglyaffectsasubsetofspeciesinacommunitythathas(orlacks)aparticularsuiteoffunctionaltraits.Historicalcommu-nities,withmuchgreaterbreadthinfunctionalspace,shouldexhibithigherresistanceorresiliencewhencomparedwithhomogenizedcommunities.Thefunctionalhomogenizationofalllocalcommunitieswithinaregion(i.e.metacommunities)canincreasevulnerabilitytolarge-scaleenvironmentaleventsbysynchronizinglocalbiologicalresponsesacrossindividualcommunities.This,inturn,wouldreducevariabilityamongcommunitiesintheirresponsetodisturbanceandwouldcompromisethepotentialforlandscape-andregional-levelbuffering.BecausecommunitycompositiondeÞnestherangeoffunctionaltraitsthatinßuenceecosystemfunctions(suchasnutrientretentionorenergyßow;e.g.e.g.),biotichomogenizationmightjeopardizeecosystemfunctionbylimitingthepoolofspeciesthatcancompensateforlocalextinctions(i.e.reducespatialpatternsinfunctionalredundancy).Homogenizedcom-munitiesmightthereforeexhibitadecreasedresiliencetoenvironmentaldisturbance,becauseelevatedsimilaritiesamongcommunitiesmightdampenoreliminatepotentialrecolonizationsbyspecieswithlocallyextirpatedtrait(s).Susceptibilityofhomogenizedcommunitiestoenviron-mentalalterationmightbeparticularlyhighinareas,suchasurbanecosystems,thatexperiencemorefrequentandseveredisturbanceeventsevents.AlthoughourmodelforfunctionalhomogenizationBox2)ishypothetical,itoffersamethodologicalframe-workforfuturestudies.Knowledgeofthefunctionalcharacteristicsofspatiallydistinctbiologicalcommunitiescouldbeusedwithobservationalandexperimentaldatatoexplorethefunctionalimplicationsofcommunitychangesintraittypesandfrequenciesthatresultfromhomogen-ization.Anexplorationofcommunitysimilaritiesinmultidimensionalfunctionalspaceshouldadvanceourunderstandingofbiotichomogenizationanditslong-term TRENDSinEcologyandEvolutionVol.19No.1January2004 ecologicalconsequences,includingthepotentialeffectsofhomogenizationonfood-webstructureandcommunitysusceptibilitytospeciesinvasions(Box3EvolutionaryconsequencesofbiotichomogenizationAnevolutionarydimensiontothecurrentbioticcrisiswasperhapsbestexpressedbySouleSoulewhostated:Ôdeathisonething,anendtobirthissomethingelseÕ.Webelievethepotentialevolutionaryimpactsassociatedwithspeciesspeciesandendemicextirpationsextirpationsareausefulframeworkwithinwhichtheevolutionaryimplicationsofbiotichomogenizationcanbeaddressed.Speciationisaresultofnumerousecologicalandevolutionaryprocesses,whicharguablyactonthesamebiologicaltemplate:thespecies.RosenzweigRosenzweigrecentlysuggestedthatthefutureofspeciationisintricatelylinkedwiththefutureofspeciesdiversity.Althoughweagree,wefurtherexpectbiotichomogenizationtoprovideacriticalcontextwithinwhichspeciationcanoccur,becausefuturespatialvariabilityinspeciesdiversityandcompositionislikelytobereducedgreatly.Acommoncomponentofmostproposedmechanismsofspeciationisthatgeographicalisolationofsisterpopulations(co-adaptedgenecomplexes)isrequiredforallopatricspeciation,theputativesourceof Box2.Aconceptual,trait-basedframeworkforassessingthepotentialecologicalconsequencesoffunctionalhomogenizationTheoccurrenceandrelativeabundanceoffunctionaltraitscontributedbyconstituentspeciesdeterminesthefunctionaldiversityofabiologicalcommunity.FigureIpresentsaconceptualframeworkwhereeachfunctionaltraitisrepresentedbyasingleaxis,andthecollectionoffunctionaltraitscontributedbyallspeciesofthecommunitydenesthe-dimensionalhypervolumeinfunctionalspaceoccupiedbythecommunity(analogoustothespecies-specicfunctionalnicheofRosenfeld[56]extendedtotheentirecommunity).Foreachsinglefunctionaltrait,speciesoccupysometolerancerangealongtheenvironmentalaxisdenedrelativetothattrait.Thecumulativedistributionofthetraitstatesofallspeciesrepresentstheaggregateenvironmentaltoleranceforthecommunity;therefore,analterationofspeciescomposition(e.g.byinvasionorextinction)canmodifytheoverallcommunitytolerancetotheenvironmentalcondition.FigureIaillustratestheeffectsofhomogenizationonadistributionofasinglefunctionaltrait(i.e.one-dimensionaltraitspace)forthreehypotheticalcommunities.Thereplacementofspecieswithuniquetraitstates(e.g.viatheextirpationofrarespecies)byspecieswithsimilartraitstates(e.g.viatheintroductionofgeneralistspecies)duringthehomogeniz-ationprocesswilltruncatethetailsofthetraitdistributionandcompresstheoveralltraitrangeforthecommunity.Consequently,historicaldifferencesinthetraitdistributionamongthethreecommunitiesmightbelost,causingthemtobecomehomogenizedinfunctionalspace(i.e.currenttraitdistributionsconvergetowardsomecommoncentraltendency).InFigureIb,thisconceptualframeworkisextendedtoasuiteofspeciestraitsrepresentedinmulti-dimensionalfunctionalspaceforthesamethreehypotheticalcommunities.Itshowshowthereplacementofnativespecieswithuniquetraitstatesbyintro-ducedspecieswithcommontraitstatesresultsinreducedbreadth(i.e.traitvariation)ofthecurrentorhomogenizedcommunitiesinfunctionalspacecomparedtothehistoricalcommunities.Further-more,thelocationsofthecommunitiesinfunctionalspaceareshiftedtowardacommoncentraltendency,asindicatedbygreateroverlapinthethreecommunitytraitpolygons(FigureIb),anindicationoffunctionalhomogenization.Notethat,becausethewinnersinbiotichomogenizationareoftengeneralistspecies[1],theintroductionofnon-nativespecieswillresultinreducedwithin-communityfunctionaldiversity.However,ifspecialistnon-nativespeciesareintroduced(i.e.specieswithtraitcombinationsthatdonotexistintherecipientcommunities),thewithin-communityfunctionaldiversityisexpectedtoincrease;however,greaterbetween-communitytraitsimilarityisstillexpectedtooccurbecausethesamespecies(andthereforetraits)areintroducedtothecommunities.FigureI.Aconceptualmodeloffunctionalhomogenization.Theeffectsofhomogenizationonadistributionofasinglefunctionaltrait(i.e.one-dimen-sionaltraitspace)forthreehypotheticalcommunities(AC),whereTraitstatecanrefertothevalueofacontinuoustraitorthecategoryofadiscretetrait,andFrequencycanrefertothefrequencyofspeciesorindividualsinthecommu-nitythathaveparticulartraitvaluesorcategories.historicalandcurrentrepresentthemeantraitstatesforthehistorical(dashedline)andcurrentorhomogenized(solidline)communities,respectively.(b)Theeffectsofhomogenizationonasetofspeciestraitsthatarerepresentedinmulti-dimensionalfunctionalspace(shownintwo-dimensionsforsimplicitybutcanbereadilyextendedto-dimensions)forcommunities(AC).Upper-caselettersanddashedtraitpoly-gonsrepresenthistoricalcommunities,andlower-caselettersandsolidtraitpolygonsrepresentcurrentorhomogenizedcommunities.Theshadedarearep-resentsahypotheticalenvironmentaldisturbancethataffectsalimitedsetofspeciesinacommunitythathas(orlack)aparticularsuiteoffunctionaltraits(indicatedbythedegreeofoverlapbetweenthecommunitypolygonsandthedisturbanceovalinfunctionalspace),andshowstherelativeresilienceofthehomogenizedcommunitiestofuturedisturbances. Community ACommunity BCommunity C FrequencyFrequencyFrequencyTrait stateTrait stateTrait state BAcba Species trait 1Species trait 2 historical (a)(b)X historical historical TRENDSinEcologyandEvolutionVol.19No.1January2004 mostnewspecies.Humanfacilitationofpopulationdispersalacrossnaturalbiogeographicalbarriershasdiminishedgeographicalisolatesthatarenecessaryforeventualallopatricspeciation,therebylimitingfuturepotentialspeciesdiversity.Furthermore,thesourceoffuturebiodiversitymightalsoberestrictedthroughthefusionofincipientevolutionarylineagesviahybridizationandintrogressionintrogression.Alternatively,thereissomepossibilitythatbiotichomogenizationwillpromotetheoriginanddiversiÞcationofnewspecies,asinvasivespeciesevolveinnewenvironments,orasgreaterhybridizationopportunitiescreatenewspeciesspecies.SpeciesdiversiÞcationmightindeedbelikely,giventhemanyexamplesofcontemporaryevolution(i.e.evolutionarychangesobservableoverlessthanafewhundredyears)involvinginvasivespeciesspecies.ThequestionofwhetherhomogenizationwillactuallypromotediversiÞcationvianovelgeneticconvergencesinnewenvironmentsrequiresadditionalstudies,perhapsusingÔhomeandawayÕcomparisonsofinvasivespecieswithrespecttoenergeticsandlife-cycledynamicsdynamics),behaviourandpopulationgenetics(e.g.(e.g.)andhabitatandresourceuse(e.g.(e.g.).ThewidespreaduseofcaptiveandgeneticallymodiÞedstockstosupplementdwindlingwildpopulationswillcontinuetocausemixingofformerlyisolatedpopulations.Immediateconsequencesoftheseeventswouldbeacompromiseindiseaseorparasiteresistanceforthehybridpopulation,andadisruptionofitscapacityforlocaladaptation.Localadaptationanddriftcontributetothegeneticvariabilityofisolatedpopulationsthathelpsensurethatspeciesrespondevolutionarilytoenvironmen-talchange.Long-termconsequencesthusdependonthecapacityforadaptationtoenvironmentalchangechange,whichisafunctionofgeneticbackground.Accordingly,homogenizedgeneticand/orfunctionalvariationmightjeopardizethefutureresilienceofbiologicalcommunitiesbyincreasingthechancesofspeciesextirpationsviareducedadaptivecapacity.Indeed,paleontologicalevi-dencesuggeststhatmassextinctionshaveneverentirelyresettheevolutionaryclockbecauseenoughtaxa(andtherefore,functionaldiversity)survivedtoseedtherecoveryprocesswithouttheoriginofnewphylaphyla.However,theextenttowhichextensivehomogenizationmightconstraingeneticorfunctionaldiversityandlimitrecoveryinthefaceoffutureextinctioneventsisInaddition,theintroductionofnewspeciesintonewregionswillresultinmultiplefoundereffectsandcouldleadtonovelselectionpressuresthathavenotpreviouslybeenobservedobserved.Thishasthepotentialtoalterevolutionarytrajectories,irrespectiveoftheextirpationofnativespecies.Interestingly,althoughhomogenizationmightfacilitatenovelspeciesinteractions,thenumberandbreadthoftheseinteractionsarelikelytobelimited,owingtothetaxonomicandfunctionalsimpliÞcationofthecommunitiesviacommonspeciesinvasionsandextirpa-tions.ThesesimpliÞcationsinbioticinteractionscouldleadtoweakerselectionpressuresinthehomogenizedcommunities,andbioticmixingcouldthereforeevenendangerthelong-termsuccessofspeciesthatareseeminglytheÔwinnersÕinthehomogenizationprocess.Homogenizationisnowconsideredonethemostpromi-nentformsofbioticimpoverishmentworldwide.Todate,wehavebeguntounderstandpatternsinbiotichomogen-izationinbothaquaticandterrestrialecosystems;however,westillcannotpredicttheconsequencesoftheseevents,particularlyfortheprovisioningofenviron-mentalgoodsandservices.Webelievethatelucidatingthe Box3.Effectsofhomogenizationonfood-webstructureandfuturespeciesinvasionscationoffood-webstructureGiventhatspeciesinvasionsandextirpationsareactinginconcertatalltrophiclevels,biotichomogenizationcouldaffectanyofthemanyprocessesincommunitiesthatvaryinspaceandtime,suchasspatialsubsidiesandfood-webdynamics,andtherebyhavecascadingeffectselsewhereonthelandscape.Forexample,increasedspatialsimilarityinthespeciesidentityofpredatorsandcompetitorscouldhavedirectandindirecteffectsonspeciesatlowerandhighertrophiclevelsbyincreasingextirpationratesviaintensiedspecies-speciinteractions(i.e.functionallysimilarspeciesmightutilizethesameresources).Inarecentstudy,Beisneretal.[57]showedthattheinvasionofrainbowsmeltOsmerusmordaxintotwonorthtemperatelakesresultedinshcommunityhomogenizationthroughthespreadofinvaders,aswellasthehomogenizationofzooplanktoncommunitystructureviadirectpredationeffectsofsmeltandindirecteffectsactingthroughcompetitiveinteractionsamongzooplankton.There-fore,positivefeedbackmechanismsofhomogenizationmightexistwherethesimplicationofonetrophiclevelleadstoincreasedsimplicationofotherinterconnectedtrophiclevels(()Investigationsofbiotichomogenizationacrossmultipletrophiclevelswillthereforebecomeincreasinglyimportantforunder-standingtherelationshipbetweenbioticmixingandfood-webstructureanddynamics.Webelievethatresearchexamininghowfood-webdynamicsareinuencedbyinvasivespeciesintroductions(e.g.[59]),invasivespeciesremoval(e.g.[60]),keystonenativespecies(e.g.[61])andrarespecies(e.g.[62]),andhowchangesinfood-webstructureinuenceecosystemprocesses(e.g.[63])couldprovideimportantinsightintoourunderstandingofthefood-webconsequencesofbiotichomogenization.IncreasedsusceptibilityofcommunitiestospeciesinvasionsSimplicationviahomogenizationmightalsoplayasignicantroleininuencingtherateofspeciesspreadandcommunityresistancetofutureinvasions.GarcandRodr[26]foundthatthespeedofspeciesinvasionincreasedwithenvironmentalhomogen-ization,whichpointstotheimportanceofspatialheterogeneityinreducingpopulationexpansionofinvasivespecies.Furthermore,uctuatingresourcetheory[64]describeshowspeciesdeletionsareaccompaniedbyresourcerelease,whichmightmakeacommunitysusceptibletofurtherinvasions.Thelossofrarespeciesfromsystems(apatterncommonlyassociatedwithhomogenization;e.g.[39])mightsubstantiallyfacilitatefuturespeciesinvasionsandtheirassociatedecologicalimpacts(e.g.[62]).Inadditiontoindividualrarespecies,thesimplicationofthetaxonomicandfunctionalcompo-sitionofentirecommunitiescouldhaveimportantimplicationsforfutureinvasionsandtheirecologicalimpacts.Forexample,grass-landcommunitieswithlowfunctionaldiversityexhibitdecreasedresistancetospeciesinvasions[65].Communitieswithlowfunc-tionaldiversityarealsomorelikelytoexhibitsimilaritiesintemporalpatternsofresourceuse,whichultimatelytranslateintosynchro-nizeddynamicsinspeciesabundances.Temporalsynchronyinpopulationdynamicsandthelackofcomplementaryuseofresourcesintimecouldincreasetheprobabilitythatresourcesareavailabletofacilitatespeciesinvasions(e.g.[44]). TRENDSinEcologyandEvolutionVol.19No.1January2004 futureecologicalandevolutionarythreatsofbioticmixingrequiresexpandingourfocusbeyondisolatedcasesofspeciesinvasionsandextinctionstotheaccumulationofmultipleeventsthatcollectivelyoccuracrosstheentirelandscapeovertime.Becausethebiotichomogenizationprocessoperatesatlargerspatialandtemporalscales,wemustincorporatethisbroadercontextintoourthinkingifwewanttoquantifyandunderstandtherisksofgenetic,taxonomicandfunctionalhomogenizationtovariouslevelsofbiologicalorganization.Moreover,thereisanincreasingneedtoexpandthedimensionsofbiotichomogenization,toincludetheabioticcontextofglobalenvironmentalhomogenization,whichpromotesbioticsimpliÞcation.Itisintheseareasthatresearchwillmosteffectivelycontributenewknowledgeabouttheecologicalandevolutionaryimplicationsofbiotichomogenization.Thiswillbeachallengegiventhatcontinuedgrowthandexpansionofthehumanpopulationwillresultinlarge-scaleenvironmentalupheavalandsubsequentpressuresonregionalbiotas.However,wemustplaceapremiumonthisresearch,andontheadaptivemanagementscenariosthatitwillproduce,toensurethattheecosystemsonEarthretaintheirresilienceandsustainabilityinthefaceofthisanthropogenicblender.AcknowledgementsWethankJulieLockwood,MichaelMcKinney,TomRooney,JordanRosenfeldandananonymousreviewerforconstructivecomments,andBryanNeffforhisperspectivesontheevolutionaryimplicationsofbiotichomogenization.FundingforJ.D.O.wasprovidedbyagraduatescholar-shipfromtheNaturalSciencesandEngineeringResearchCouncilofCanada,forN.L.P.partiallybytheUSNationalScienceFoundation(#DEB-0075352)andtheUSEnvironmentalProtectionAgency(SPOBS0056363),andforK.D.F.bytheUSNationalScienceFoundation(#DEB-0108222).1McKinney,M.L.andLockwood,J.L.(1999)Biotichomogenization:afewwinnersreplacingmanylosersinthenextmassextinction.TrendsEcol.Evol.14,450Ð4532Vermeij,G.J.(1991)Whenbiotasmeet:understandingbioticinter-Science253,1099Ð11043Elton,C.S.(1958)TheEcologyofInvasionsbyAnimalsandPlantsUniversityofChicagoPress4Rooney,T.P.,etal.Bioticimpoverishmentandhomogenizationinunfragmentedforestunderstorycommunities.Conserv.Biol.(inpress)5Lockwood,J.L.etal.(2000)TaxonomichomogenizationofglobalAnim.Conserv.3,27Ð356Wilson,K.J.(1997)ExtinctandintroducedvertebratespeciesinNewZealand:alossofbiodistinctivenessandgaininbiodiversity.Conserv.Biol.3,301Ð3057Blair,R.B.(2001)BirdsandbutterßiesalongurbangradientsintwoecoregionsoftheUnitedStates:isurbanizationcreatingahomogeneousfauna?InBioticHomogenization(Lockwood,J.L.andMcKinney,M.L.,eds),pp.33Ð56,KluwerAcademic/PlenumPublishers8Rahel,F.J.(2000)HomogenizationofÞshfaunasacrosstheUnited288,854Ð8569Duncan,J.R.andLockwood,J.L.(2001)SpatialhomogenizationofaquaticfaunaofTennessee:extinctionandinvasionfollowinglandusechangeandhabitatalteration.InBioticHomogenizationJ.L.andMcKinney,M.L.,eds),pp.245Ð258,KluwerAcademic/PlenumPublishers10Carlton,J.T.(1996)Pattern,process,andpredictioninmarineinvasionecology.Biol.Conserv.78,97Ð10611Cowie,R.H.(2001)DeclineandhomogenizationofPaciÞcfaunas:thelandsnailsofAmericanSamoa.Biol.Conserv.99,207Ð22212Rosenzweig,M.L.(2001)Thefourquestions:whatdoestheintroduc-tionofexoticspeciesdotodiversity?Evol.Ecol.Res.3,361Ð36713Lockwood,J.L.,McKinney,M.L.eds(2001)BioticHomogenizationKluwerAcademic/PlenumPublishers14Kinzig,A.P.,etal.eds(2002)TheFunctionalConsequencesofBiodiversity:EmpiricalProgressandTheoreticalExtensionstonUniversityPress15Moritz,C.(2002)Strategiestoprotectbiologicaldiversityandtheevolutionaryprocessesthatsustainit.Syst.Biol.51,238Ð25416Ehrlich,P.R.andEhrlich,A.H.(1992)Thevalueofbiodiversity.Ambio21,219Ð22617Collins,M.D.etal.(2002)Species-areacurves,homogenizationandthelossofglobaldiversity.Evol.Ecol.Res.4,457Ð46418Stockwell,C.A.etal.(1996)Translocationsandthepreservationofallelicdiversity.Conserv.Biol.10,1133Ð114119Storfer,A.(1999)Geneßowandendangeredspeciestranslocations:atopicrevisited.Biol.Conserv.87,173Ð18020Rhymer,J.M.andSimberloff,D.S.(1996)Extinctionbyhybridizationandintrogression.Annu.Rev.Ecol.Syst.27,83Ð10921Lee,C.E.(2002)Evolutionarygeneticsofinvasivespecies.TrendsEcol.17,386Ð39122Daehler,C.C.andCarino,D.A.(2001)Hybridizationbetweennativeandalienplantsanditsconsequences.InBioticHomogenization(Lockwood,J.L.andMcKinney,M.L.,eds),pp.81Ð102,KluwerAcademic/PlenumPublishers23Quattro,J.M.etal.(2002)Geneticissuesinaquaticspeciesmanage-ment:theshortnosesturgeon(Acipenserbrevirostrum)inthesouth-easternUnitedStates.Conserv.Genet.3,155Ð16624Behnke,R.J.(1992)NativeTroutofWesternNorthAmericaAmericanFisheriesSocietyMonograph6,AmericanFisheriesSociety25Douglas,M.R.andBrunner,P.C.(2002)BiodiversityofCentralAlpine(Salmoniformes):impactofone-hundredyearsofmanage-Ecol.Appl.12,154Ð17226Garcõa-Ramos,G.andRodrõguez,D.(2002)Evolutionaryspeedofspeciesinvasions.Evolution56,661Ð66827Lenormand,T.etal.(1999)TrackingtheevolutionofinsecticideresistanceinthemosquitoCulexpipiens400,861Ð86428Tsutsui,N.D.etal.(2000)Reducedgeneticvariationandthesuccessofaninvasivespecies.Proc.Natl.Acad.Sci.U.S.A.97,5948Ð595329Holway,D.A.etal.(2002)ThecausesandconsequencesofantAnnu.Rev.Ecol.Syst.33,181Ð23330Tsutsui,N.D.andCase,T.J.(2001)PopulationgeneticsandcolonystructureoftheArgentineant(Linepithemahumile)initsnativeandintroducedranges.Evolution55,976Ð98531BrumÞeld,R.T.etal.(2003)Theutilityofsinglenucleotidepolymorphismsininferencesofpopulationhistory.TrendsEcol.18,249Ð25632Anderson,E.andStebbins,G.L.(1954)Hybridizationasanevolution-arystimulus.Evolution8,378Ð38833Perry,W.L.etal.(2002)Importanceofhybridizationbetweenindigenousandnonindigenousfreshwaterspecies:anoverlookedthreattoNorthAmericanbiodiversity.Syst.Biol.51,255Ð27534Hubbs,C.L.(1955)HybridizationbetweenÞshspeciesinnature.4,1Ð2035Ellstrand,N.C.andSchierenbeck,K.A.(2000)Hybridizationasastimulusfortheevolutionofinvasivenessinplants?Proc.Natl.Acad.Sci.U.S.A.97,7043Ð705036Echelle,A.A.andConnor,P.J.(1989)Rapid,geographicallyextensivegeneticintrogressionaftersecondarycontactbetweentwopupÞshspecies(Cyprinodon,Cyprinodontidae).Evolution43,717Ð72737Manel,S.etal.(2003)Landscapegenetics:combininglandscapeecologyandpopulationgenetics.TrendsEcol.Evol.18,189Ð19738Luck,G.W.etal.(2003)Populationdiversityandecosystemservices.TrendsEcol.Evol.18,331Ð33639Rahel,F.J.(2002)Homogenizationoffreshwaterfaunas.Annu.Rev.Ecol.Syst.33,291Ð31540Olden,J.D.andPoff,N.L.Towardamechanisticunderstandingandpredictionofbiotichomogenization.Am.Nat.(inpress)41Dõaz,S.andCabido,M.(2001)Viveladifference:plantfunctionaldiversitymatterstoecosystemprocesses.TrendsEcol.Evol.646Ð65542Tilman,D.etal.(1997)Theinßuenceoffunctionaldiversityandcompositiononecosystemprocesses.Science277,1300Ð130243Sankaran,M.andMcNaughton,S.J.(1999)Determinantsof TRENDSinEcologyandEvolutionVol.19No.1January2004 biodiversityregulatecompositionalstabilityofcommunities.401,691Ð69344Stachowicz,J.J.etal.(2002)Biodiversity,invasionresistance,andmarineecosystemfunction:reconcilingpatternandprocess.Ecology83,2575Ð259045McGrady-Steed,J.etal.(1997)Biodiversityregulatesecosystempredictability.390,162Ð16546Rebele,F.(1994)Urbanecologyandspecialfeaturesofurbanecosystems.Glob.Ecol.Biogeogr.Lett.4,173Ð18747Soule,M.E.(1980)Thresholdsforsurvival:maintainingÞtnessandevolutionarypotential.InConservationBiology:AnEvolutionary-EcologicalPerspective(Soule,M.E.andWilcox,B.A.,eds),pp.151Ð170,Sinauer48Mooney,H.A.andCleland,E.E.(2001)Theevolutionaryimpactofinvasivespecies.Proc.Natl.Acad.Sci.U.S.A.98,5446Ð545149Rosenzweig,M.L.(2001)Lossofspeciationratewillimpoverishfuturediversity.Proc.Natl.Acad.Sci.U.S.A.98,5404Ð541050Abbott,R.J.(1992)Plantinvasions,interspeciÞchybridizationandtheevolutionofnewplanttaxa.TrendsEcol.Evol.7,401Ð40551Stockwell,C.A.etal.(2003)Contemporaryevolutionmeetsconserva-tionbiology.TrendsEcol.Evol.18,94Ð10152Chess,D.W.andStanford,J.A.(1998)Comparativeenergeticsandlifecycleoftheopossumshrimp(Mysisrelicta)innativeandnon-nativeenvironments.Freshw.Biol.40,783Ð79453Lohrer,A.M.etal.(2000)Homeandaway:comparisonsofresourceutilizationbyamarinespeciesinnativeandinvadedhabitat.Biol.Inv.2,41Ð5754Levins,R.(1968)EvolutioninChangingEnvironments,PrincetonUniversityPress55Erwin,D.H.etal.(1987)Acomparative-studyofdiversiÞcationeventsÐtheearlyPaleozoicversustheMesozoic.41,1177Ð118656Rosenfeld,J.S.(2002)Functionalredundancyinecologyandcon-98,156Ð16257Beisner,B.E.etal.(2003)TheeffectsofanexoticÞshinvasiononthepreycommunitiesoftwolakes.J.Anim.Ecol.72,331Ð34258Fausch,K.D.etal.(2002)Linkagesbetweenstreamandforestfoodwebs:ShigeruNakanoÕslegacyforecologyinJapan.TrendsEcol.Evol.17,429Ð43459Woodward,G.andHildrew,A.G.(2001)Invasionofastreamfoodwebbyanewtoppredator.J.Anim.Ecol.70,273Ð28860Zavaleta,E.S.etal.(2001)Viewinginvasivespeciesremovalinawhole-ecosystemcontext.TrendsEcol.Evol.16,454Ð45961Power,M.E.etal.(1996)Challengesinthequestforkeystones:identifyingkeystonespeciesisdifÞcult-butessentialtounderstandinghowlossofspecieswillaffectecosystems.46,609Ð62062Lyons,K.G.andSchwartz,M.W.(2001)RarespecieslossaltersecosystemfunctionÐinvasionresistance.Ecol.Lett.4,358Ð36563Seta,H.(2002)Sensitivityofecosystemfunctioningtochangesintrophicstructure,functionalgroupcompositionandspeciesdiversityinbelowgroundfoodwebs.Ecol.Res.17,207Ð21564Davis,M.A.etal.(2000)Fluctuatingresourcesinplantcommunities:ageneraltheoryofinvasibility.J.Ecol.88,528Ð53465Dukes,J.S.(2002)Speciescompositionanddiversityaffectgrasslandsusceptibilityandresponsetoinvasion.Ecol.Appl.12,602Ð617 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