environmental filtering and competitive exclusion drive … · 2018-04-24 · 1. understanding the...

Journal of Ecology 20181ndash13 wileyonlinelibrarycomjournaljec emsp|emsp1copy 2018 The Authors Journal of Ecology copy 2018 British Ecological Society

Received22November2017emsp |emsp Accepted15January2018DOI1011111365-274512963

R E S E A R C H A R T I C L E

Environmental filtering and competitive exclusion drive biodiversity- invasibility relationships in shallow lake plant communities

Ranjan Muthukrishnan1 emsp|emspNicole Hansel-Welch2emsp|emspDaniel J Larkin1

1DepartmentofFisheriesWildlifeandConservationBiologyandMinnesotaAquaticInvasiveSpeciesResearchCenterUniversityofMinnesota-TwinCitiesStPaulMNUSA2ShallowLakesProgramMinnesotaDepartmentofNaturalResourcesBrainerdMNUSA

CorrrespondenceRanjanMuthukrishnanEmail mrunjumnedu

Funding informationMinnesotaAquaticInvasiveSpeciesResearchCenterMinnesotaEnvironmentandNaturalResourcesTrustFund

HandlingEditorChristerNilsson

Abstract1 Understandingtheprocessesthatinfluencethediversityofecologicalcommuni-tiesandtheirsusceptibilityto invasionbyexoticspeciesremainsachallenge inecologyInmanysystemsapositiverelationshipbetweentherichnessofnativespecies and exotic species has been observed at larger spatial (eg regional)scaleswhileanegativepatternhasbeenobservedatlocal(egplot)scalesThesepatternsarewidelyattributedto(1)bioticinteractionsparticularlybioticresist-ancelimitinginvasionsinhigh-diversitylocationsproducingnegativelocal-scalerelationshipsand(2)nativeandexoticrichnesscovaryingatlargerspatialscalesasafunctionofenvironmentalconditionsandheterogeneityproducingpositivelarge-scalerelationshipsHoweveralternativeprocessescanproducesimilarpat-ternsandneedtobecriticallyevaluatedtomakesoundinferencesaboutunderly-ingmechanisms

2 Weaggregatedalargedatasetofaquaticvegetationsurveysfrom1102Minnesotashallowlakescollectedover13yearstoquantifyspatialandtemporalpatternsofcommunitycompositionUsingthosedataandadditionalinformationonenviron-mentalconditionsweevaluatedevidenceforfourdistinctmechanismsthatcoulddrivepatternsofnativeandexoticspeciesrichnessbioticresistancecompetitiveexclusionenvironmentalfilteringandenvironmentalheterogeneity

3 Wefoundtheclassicpatternofanegativenative-exoticrichnessrelationshipatlocalscalesandapositiverelationshipatlakescalesHoweverwefoundnoevi-denceforlocal-scalebioticresistanceinsteadcompetitiveexclusionbyinvasivespecies appeared to reduce native species richness after locations became in-vadedEvaluatingtheinfluenceofenvironmentalfilteringandheterogeneitywefoundthatnativeandexoticspeciesoccupiedsomewhatdifferentnichesInvaderswerelesssensitivetoenvironmentalgradientsandmoretolerantofawiderrangeofconditionsThissegregationofhabitatpreferencesalonecouldproduceanega-tivelocalnative-exoticrichnessrelationshipandapositiveregionalpatternwith-outtheinvolvementofbioticinteractions

4 SynthesisOurfindingsconflictwithestablishedexpectationswhichcomefromresearchpredominantlyconductedinterrestrialecosystemsThisillustratestheimportanceofexplicitlyevaluatingunderlyingmechanismsindiversity-invasibility

2emsp |emsp emspenspJournal of Ecology MUTHUKRISHNAN eT Al

1emsp |emspINTRODUC TION

The relationship between the diversity of ecological communitiesandtheirpropensitytobeinvadedbyexoticspecieshasbeenheav-ilydebated(FargioneampTilman2005Kennedyetal2002Levine2000 Levine amp DrsquoAntonio 1999Wardle 2001) Much researchparticularlymodelling and small-scale experiments has supportedanegativerelationshipbetweendiversityandinvasibilityHoweveratlarger(egregional)scalestheoppositepatternisfrequentlyob-servedwithmorediversecommunitieshavingmoreexoticspecies(Cleland etal 2004 Levine amp DrsquoAntonio 1999 Stohlgren etal1999)Thisscale-dependentshiftinthenative-exoticrichnessrela-tionship(NERR)remainsdifficulttoexplainwithmultipleprocessespotentiallyinteractingtoproduceoverallpatternsAtthesametimeinvasive species are a global ecological threat (Bellard Cassey ampBlackburn 2016MillenniumEcosystemAssessment 2005) thusimprovingunderstandingofbiodiversity-invasibilityrelationshipsisimportantforsupportingconservationandmanagement

A common explanation for scale-dependentNERR differencesisthatseparateprocessesdrivelocalandregionalpatterns(LevineampDrsquoAntonio1999Stohlgrenetal1999)Ithasbeenpositedthatat local scales high diversity confers biotic resistance to invasion(FargioneampTilman2005Kennedyetal2002)butthatatbroaderscales incorporation of new habitats that are favourable for na-tiveandinvasivespeciesalikeincreasesdiversityofbothinparallel(LevineampDrsquoAntonio1999Naeemetal 2000)However furtherwork has highlighted other processes that may influence NERRs(Fridleyetal2007)Spatialheterogeneityinenvironmentalcondi-tionsmaysupportpositiveNERRs(Daviesetal2005)byincreasingavenues for coexistence (eg Chesson 2000 Tilman 2004) Thestrengthordirectionofalocal-scaleNERRcanalsoshiftasafunc-tionofproductivitydisturbanceorenvironmentalgradients(BeloteJonesHoodampWender2008DaviesHarrisonSaffordampViers2007)Forexampleinvadersthathavebroaderenvironmentaltoler-ancesorpreferlessproductiveconditionsmayoccuronaverageinlessdiverselocalities(egPaavolaOleninampLeppaumlkoski2005)be-causethoseconditionstendtocorrelatewithlowerdiversityInsuchcasesnegativeNERRsmayarisethroughasamplingeffectwithouttheneedforanyparticularbioticinteractiontobeinvolved

ThemanagementimplicationsofanNERRcandifferdependingonitsunderlyingmechanism(s)ForexampleanegativeNERRresult-ing fromdiversity-drivenbiotic resistancewouldargue foreffortstocreateormaintaindiversitytopre-emptinvasionIncontrast if

suchpatternsarearesultofcompetitiveexclusionbythe invadereffortstoincreasediversitymayofferlittleprotectionagainstinva-sionAttheregionalscaleifapositiveNERRarisesbecauseinvasiveandnativespeciesshareenvironmentalpreferencesthenthemostresource-richenvironmentsmaybeatthegreatestriskofinvasionAlternativelyifheterogeneityisthedrivingmechanismforanNERRthemostvariablelocalesmaybemostvulnerable

EveninasinglesystemNERRsarelikelytoarisefrommultipleprocessesespeciallyacrosslocalandregionalscales(Fridleyetal2007)Howeverthereisagrowingconsensusthatbioticinteractionstendtobekeydriversofcommunitystructureatlocalscaleswhileenvironmental conditionsbecomemore influential as spatial scaleincreases(Fridleyetal2007)ThusamoremechanisticperspectivethatevaluatesmultipleprocessesatmultiplescalesisneededSuchstudiesarelogisticallydifficulttoconductasexperimentsbutlarge-scale long-termmonitoringdatasetsofferanalternativemeanstoaddressthesedynamics

Herewefocusonfourmechanismsthatcouldinfluencenativeorexoticspeciesdiversitythreeofwhichwecouldevaluateatmul-tiplespatialscalesBiotic resistance to invasionhas longbeencon-sideredapotentialbenefitofdiversecommunities(Elton1958)andiswell-supportedbyexperimentalwork(FargioneampTilman2005Kennedyetal2002Levine2000Naeemetal2000StachowiczWhitlatchampOsman1999)thoughtheuniversalityofthismecha-nismhasbeenquestioned(CapersSelskyBugbeeampWhite2007)Invasivespeciescanalsocompetitively excluderesidentspeciesafterestablishment(CasasScrosatiampLuzPiriz2004YurkonisMeinersampWachholder2005)producingapatternofnativeandinvaderrich-nesssimilartobioticresistancebutwithadifferenttemporalsigna-tureielossofnativediversityfollowinginvasionratherthanlowerlikelihoodofsubsequentinvasionindiverselocalesThirdlyenviron-mental filtering influences speciesrsquo abilities toestablishandpersistin particular localities Alignment of preferences between nativesandinvaderscouldproducepositiveregionalNERRswhilecompet-itiveinteractionsdeterminelocal-scaleoutcomes(Cavender-BaresKozakFineampKembel2009Daviesetal2005)Alternativelyifin-vadershavewiderenvironmentaltolerancesthannatives(RichardsBossdorf Muth Gurevitch amp Pigliucci 2006 Vazquez 2006) anegativelocalNERRcouldbeproducedbyinvadersestablishinginmarginalhabitatwithfewnativespeciesLastlyenvironmental het-erogeneity in conditions or habitat types is a keymechanism sup-portingoveralldiversity thatcan increasebothnativeand invaderrichness (Daviesetal2005)Thiseffect is likely tobecomemore

researchandforcomparisonsacrossdifferenttypesofecosystemsIdentificationof different drivers of diversity also has direct implications for decisions aboutmanagementoffreshwaterplantcommunities

K E Y W O R D S

aquaticplantsbiodiversitybioticresistancecompetitiveexclusionenvironmentalfilteringheterogeneityinvasionecologynative-exoticrichnessrelationship

emspensp emsp | emsp3Journal of EcologyMUTHUKRISHNAN eT Al

pronouncedoverlargerspatialscalesasgreatervariabilityisaccrued(Huston1999)

Inthisstudyweusedanexceptionally largedatasetofaquaticvegetation surveys fromMinnesota shallow lakes to characterizeNERRsatlocalandregionalscalesandexamineevidenceforalterna-tivemechanismsUsingdatafromsiteswithrepeatedsamplingovertimewetestedfor(1)nativespeciesrichnessconferringbiotic resis-tancetoinvasionand(2)invaderscompetitively excludingnativespe-ciesafterestablishmentWeusedenvironmentaldatatocorrelatenative and invasive species richnesswith abiotic conditions to (3)evaluateifenvironmental filteringactedsimilarlyonbothgroupsand(4)evaluatehownativeandinvasivespeciesrespondedtoenviron-mental heterogeneityasapotentialdriverofregionalscalediversity

2emsp |emspMATERIAL S AND METHODS

21emsp|emspSurvey data

Vegetation data for the study were aggregated from 1662 grid-based point-intercept surveys conducted by the MinnesotaDepartmentofNaturalResourcesin1102shallowlakesfrom2002to2014Thelakesrepresentabroadrangeofshallowlakesacrossthestatewithvarying levelsandtypesofnearby landusehumanactivityandmanagementSurveyswereconductedwitha thrownrakethatwaspulledalongthebenthicsurfacetocollectvegetationAllmacrophytes(aquaticvascularplantsandmacroalgae)wereiden-tifiedtospeciesorlowestfeasibletaxonForsimplicitywerefertoalltaxaasldquospeciesrdquoieincludingthoseidentifiedonlytogenus(seeTableS1forafull listoftaxa)Thenumberofsurveypointsvariedbetweenlakes(617plusmn379MplusmnSD)scalingwithlakesize

WeusedthesedatatocalculatespeciesrichnessatpointandlakescalesWedistinguishedspeciesconsidered invasive inMinnesotabased on established lists (Milburn BourdaghsampHusveth 2007USDA2016)andsixwerepresentinoursurveysLythrum salicaria (purple loosestrife) Myriophyllum spicatum (Eurasian watermil-foil) Phalaris arundinacea (reed canarygrass) Potamogeton crispus (curly-leaf pondweed) Typha angustifolia (narrow-leaf cattail) and Typha times glauca(hybridcattail)Incaseswhereidentificationwasre-solvedtoataxonomiclevelencompassingbothinvasiveandnativespecies(egTyphasp isambiguouswiththenativeTypha latifolia)weconservativelyassumedthenativeformSimilarlywhileinvasiveEuropeangenotypesofPhragmites australisoccurinMinnesotalin-eageswerenotdiscriminatedinourdatasetThuswetreatedallP australisascomprisingthewidespreadnativesubspeciesP australis sspamericanus Inasmallnumberof lakes invasiveTyphawasre-cordedbothtospeciesandtothegroupedcategoryldquoT angustifolia or times glaucardquoWecountedtheseasrepresentingonlyasingleinvaderspecies

UsingthesedataweevaluatedNERRsatlocal(individualsam-plingpoint)andregional(whole-lake)scalesAllanalyseswereper-formedinrversion312(RCoreTeam2014)Usingpoint-leveldatawe estimated the relationship between native and exotic speciesrichnessToaccountfortheintegernatureoftheresponsevariable

we used aGLMwith a Poisson error distribution (using the ldquoglmrdquofunction from the stats package) and evaluated significance usingtheldquosummaryglmrdquofunction(thisapproachwasusedforallGLMs)Wethencalculatedlake-levelrichnessvaluesandconstructedasep-arateGLMforlake-levelnativeandexoticspeciesrichness

22emsp|emspBiotic interaction mechanisms

Tocalculatethepotentialfornativediversitytoconferbioticresist-ance to invasionand for invasivespecies tocompetitivelyexcludenativespeciesweanalysedtemporalpatternsinlakesthathadbeenrepeatedly sampled overmultiple years Because temporal analy-seswouldbe sensitive to changes in sampling effort or locationsweonlyincludeddatafromlakeswherethesamegridsofsamplingpointswereusedamongyearsthiscomprised179lakeseachwith2ndash9interannualsurveys(M=322)

Toquantifybioticresistancewecomparedtherelationshipbe-tweennativespeciesrichnessandtheprobabilityofasamplingpointbecominginvadedatsubsequentsamplingtimesBecauseinvasivespecies themselves can potentially increase the likelihood of fur-therinvasions(viaaninvasionalmeltdownSimberloffampVonHolle1999) or increase resistance (HenrikssonWardle Trygg Diehl ampEnglund 2016)we focused only on initial invasions excluding alllocationsthatwerealreadyinvadedWhilethepotentialeffectsofinitial invadersonsecondary invasionsareof interest thenumberofsuchrecordswas insufficienttoaddressthis issueAdditionallysomelocationsmayhavebeengenerallyunsuitableforvegetationproducingzerovaluesforrichnessthatcouldartificiallyreduceesti-matesofspeciesrichnessthusweexcludedfromouranalysispointslackingvegetationatanysamplingtimeWealsoexcludedlocationsfromlakesthatdidnotcontainanyinvasivespeciesattheinitialsam-plingpointInvasioninsuchcaseswouldrequirecolonizationfromanotherlakeahighlystochasticprocessthatcouldbiasestimatesWeanalyseddatafromtheremainingsitesusingageneralizedlin-earmixedeffectsmodel(fromthebinomialfamily)Whetherornotanuninvadedpointwassubsequently invadedwasusedasthere-sponsevariablenativespeciesrichnesswastreatedasafixedeffectandlakeidentitywasincludedasarandomeffectThemodelwasfitusingtheldquoglmerrdquofunctionfromthelme4package(BatesMaumlchlerBolkerampWalker2015)andusingtheldquobobyqardquooptimizer(withtheargument control=glmerControl(optimizer=ldquobobyqardquo)) signifi-cancewas evaluated using a parametric bootstrap This approachfirst estimates the full mixed model with the variable of interestincludedthenareducedmodelwiththevariableremovedchangeinfitbetweenmodelswasassessedusingtheldquoPBmodcomprdquofunc-tion(fromthepbkrtestpackagewith1000simulationsHalekohampHoslashjsgaard 2014)We also evaluated biotic resistance at the lakescaleevaluatinghowwhole-lakenativespeciesrichnessinfluencestheprobabilityofbecominginvadedusingaGLMfromthebinomialfamily

Toevaluatewhetherinvaderscompetitivelyexcludednativespe-ciesweestimatedrateofchangeinnativespeciesrichnessforeachsamplingpointbyestimatinga linear regression fornativespecies


richnesswithsamplingyearasthesingleindependentvariableForeachmodelthecoefficientforthetimeparameterprovidesanesti-mateoftheaverageyearlychangeinspeciesnumberwithnegativevaluesindicatingspecieslossDifferencesinaveragecoefficientval-ueswerecomparedbetweensitesthatwereinvadedandthosethatremaineduninvadedthroughallsurveysalsousingalinearmodelWe again excluded locations where no vegetation was recordedduring any surveyanduseda linearmixedeffectmodel (with theldquolmerrdquofunctionfromthelme4package)tocompareratesbetweeninvadedanduninvadedsiteswhileaccountingforlakeasarandomeffect Statistical significancewasagainevaluatedusing the sameparametricbootstrapapproachasaboveCompetitiveexclusionwasalsoevaluatedatthelakescaleusingastandardlinearmodel(withtheldquolmrdquoandldquosummarylmrdquofunctions)tocompareratesofchangeinspeciesrichnessbetweeninvadedanduninvadedlakes

23emsp|emspEnvironmental mechanisms of invasion

ToinvestigatehowenvironmentalconditionsinfluencedpatternsofdiversitywecollecteddataonarangeofenvironmentalparametersatbothpointandlakescalesDuringsurveyspoint-levelmeasuresofbottomdepthandSecchidepthwererecordedWeusedGLMstoestimate influenceofdepthandSecchidepthonnativeand in-vasivespeciesrichnessassumingPoissondistributionsforspeciesrichnessWecalculatedtheserelationshipsatpointandwhole-lakescales(usingmeanvaluesacrosspoints)BecausedepthandSecchidepthwerecorrelatedweusedseparatemodelstoindependentlyevaluatetheirrelationshipswithrichnessratherthanincludingbothparametersinasingleanalysisThetotalpossiblerichnessofinva-sivespecieswasmuchlowerthanthatofnativespeciesthuswealsoconductedanalogousanalysesusinginvaderpresenceasabinomialresponseinGLMstotestforenvironmentalpreferencesofinvasivespecies in general Additionallywe calculated standard deviations(SD)ofdepthandSecchidepthforeachlakeasmeasuresofwithin-lakeheterogeneity andused thesedata to estimateGLMs testingrelationships between lake heterogeneity and native and invasivespeciesrichnessatthelakescaleagainassumingPoissondistribu-tionsforspeciesrichnessWealsoconductedanadditionalanalysisof invader responsewith invaderpresenceasabinomial responseinaGLM

Toestimateadditionalenvironmentalparameters for lakesweaggregateddatafromtwopubliclyavailablesourcesWecollectedmeasurementsoflakeareaandlong-termaverageSecchidepth(m)forc11000lakesderivedfromremotesensingdatabytheUniversityofMinnesotaRemoteSensingandGeospatialAnalysisLaboratory(OlmansonBauerampBrezonik2008OlmansonBrezonikampBauer2014)InadditiontheMinnesotaPollutionControlAgency(MPCA)manages a large dataset of direct lakemeasurements (c 6 million records)collectedbystatelocalandcitizen-basedorganizationsonawidevarietyofenvironmentalparametersWefocusedonfivepa-rameterslikelytoinfluencemacrophytedistributionthatweresam-pledinlargenumbersoflakespHconductance(μS)totalKjeldahlnitrogen (N mgL) total phosphorus (P mgL) and chlorophyll a

concentration (μgL)Datawereheterogeneous in spaceand timeandcollectedbygroupswithdifferingtechnicalproficiencythuswetookseveralstepstoassuredataqualityWelimitedenvironmentalmeasures to only those collected since the year 2000 and duringthegrowingseason(JunendashSeptember)ToremovedatalikelytobeerroneouswecalculatedmeanandSD foreachvariableacrossalllakesandexcludedanysampleswithvaluesgt5SDfromthemeanBecauseSDwas sometimes strongly influencedby extremeoutli-erswethenrecalculatedSDwithoutliersremovedandrepeatedtheprocessasecondtimeThisleftuswith139lakesinthedatasetwithvaluesforallparametersFortheselakesweaggregatedallmeasure-mentsofagivenparameterintoasinglemean

ForsurveyedlakeswithdataforallenvironmentalparametersweusedGLMswithmultiplefixedeffectstoidentifyenvironmentalconditionsassociatedwithnativeorinvasivespeciesrichnessGLMsincludedsixenvironmentalparametersaspotentialpredictors(NPpHconductancechlorophyllaandSecchidepth)Nativeandinva-sivespeciesrichnessandinvasionstatusweremodelledasresponsesinseparateanalysesusingaPoissonerrordistributionforrichnessmeasuresandinvaderpresenceabsenceasabinomialresponse

3emsp |emspRESULTS

31emsp|emspOverall patterns

Vegetationdatacomprised56134samplingpointsfrom1662sur-veys in1102 lakesAcrosssurveys150318 individualvegetationsampleswere identified to 172 taxa (generally species Table S1)Invasivespecieswereidentifiedinnearlyhalfofthelakes(546)andinvaded lakes spanned theentire rangeofnative species richness(Figure1)Theaveragenumberofspeciesatasamplingpointwas269plusmn183(MplusmnSD)andwithinalakewas1013plusmn723Consistentwith the ldquoinvasion paradoxrdquo (Fridley etal 2007) we observed anegativeNERRatthepointscaleandapositiverelationshipatthewhole-lakescale(Table1Figure2)

F IGURE 1emspFrequencyoflakeswithdifferentnativespeciesrichnessDarkgrayportionsofbarsindicatelakesthathadnoinvasivespeciespresentandlightgrayportionsindicatelakeswithatleastoneinvasivespecies

0 10 20 30 40

InvadedUninvaded

Native species richness

Num

ber o

f lak

es0

2040

6080


TABLE 1emspResultsoffixedeffectsfromallstatisticalmodelsGeneralizedlinearmodelswereusedinmostanalysesbutmixedmodelswereusedforpointscaleanalysesofbioticresistanceandcompetitiveexclusiontoaccountforautocorrelationwithinlakesStatisticallysignificantresultsindicatedwithaldquordquo

Analysis Scale Parameter Estimate SE Test statistic p- value Significant

Overall NERR Point Intercept minus2103 0024 minus88076 lt001

Coefficient minus0096 0008 minus11308 lt001

Lake Intercept minus0786 0070 minus11277 lt001

Coefficient 0023 0005 4631 lt001

Bioticinteractions

Bioticresistance Point Intercept minus3921 0286 minus13735

Coefficient 0053 0054 0971 356

Lake Intercept minus0642 0230 minus2798 005

Coefficient 0028 0026 1103 270

Competitiveexclusion Point Intercept 0080 0024 3343


Lake Intercept 0021 0182 0114 910

Coefficient 0239 0221 1080 282

Environmentalanalyses

NativerichnessmdashDepth Point Intercept 1150 0006 208374 lt001


Lake Intercept 2268 0020 114602 lt001

Coefficient 0010 0004 2747 006

InvaderrichnessmdashDepth Point Intercept minus2430 0028 minus87339 lt001



Coefficient minus0003 0016 minus0178 859

NativerichnessmdashSecchidepth

Point Intercept 0857 0005 171688 lt001

Coefficient 0037 0001 25767 lt001


Coefficient 0125 0004 29164 lt001

InvaderrichnessmdashSecchidepth

Point Intercept minus2545 0026 minus96303 lt001



Coefficient 0014 0022 0656 512

NativerichnessmdashEnvironmentalconditions


pH 0087 0043 2006 045

Conductance minus0001 0000 minus6518 lt001

P minus1359 0380 minus3580 lt001

N 0028 0051 0550 582

Chlorophylla minus0006 0001 minus4678 lt001

Secchidepth 0106 0038 2829 005

InvaderrichnessmdashEnvironmentalconditions


pH 0412 0175 2355 019

Conductance 0000 0000 minus1098 272

P 0953 0923 1032 302

N 0050 0140 0360 719

Chlorophylla minus0006 0003 minus1866 062

Secchidepth minus0316 0157 minus2012 044

(Continues)


32emsp|emspBiotic resistance

Atthelocalscaleweobservednosignificantrelationshipbetweenspeciesrichnessandtheprobabilitythatalocationwouldbecomein-vadedinthesubsequentsurvey(Table1Figure3a)ienosupportforlocal-scalebioticresistanceResultsshowedhighvariabilitywithmany lakes showing positive relationships while others displayednegative relationships indicating very noisy data with little pat-ternratherthanaconsistentbutsmalleffectAtthelakescalewealsodidnotseeasignificantrelationshipbetweenspeciesrichnessand invasion though the parameter estimatewas positive (0028Table1)Thuswhilenon-significantthetrendfollowedtheoppositepatternwithhigherspeciesrichnessbeingassociatedwithagreaterpropensityforinvasionHoweverthispatternmaybelargelynoise

33emsp|emspCompetitive exclusion

Ouranalysesdidprovidesupport forcompetitiveexclusionofna-tivespeciesbyinvadersatthelocalscale(Table1)Basedonparam-eterestimatesof the linearmixedeffectsmodel species richnessdecreasedatinvadedsamplingpointsby002speciesperyear(afteraccounting for lake-to-lake differences Figure3b) while at unin-vadedpointsrichnessincreasedby008speciesperyearAtthelakescaletherewasnosignificantdifferenceinratesofrichnesschangebetweeninvadedanduninvadedlakesrichnesstendedtoincreaseinbothovertime(Table1)

34emsp|emspEnvironmental filtering

At the local scale both native and invasive species richness sig-nificantly varied with environmental conditions (Table1 analysesusing binomial GLMs based on invasive species presence gener-ally show the samedirectionality and significance patterns as theanalysesusinginvaderrichnessresultscanbeseeninTableS2andFiguresS1andS2inonlineSupportingInformation)Nativeandinva-sivespecieshadsignificantbutopposingrelationshipswithdepth(Figure4ab) native richness decreasedwith greater depth whileinvasive richness increased though less strongly Both native andinvasiverichnessincreasedwithwaterclarity(Figure4cd)butthis

relationshipwasmuchstrongerfornative(z=4017)thaninvasivespecies (z=3897) suggesting weaker light limitation in invadersAt the lake scale native richness increasedwithmean lake depthandmeanSecchidepth(Figure4eg) Invasiverichnessdidnotsig-nificantlydifferwitheitherparameter(Figure4fh)againsuggestingbroadertolerance

Analysingthelargersetofenvironmentalvariablesweidenti-fiedmanysignificantrelationshipsbetweenlake-levelenvironmen-tal parameters and species richness (Table1) but the significantvariables differed between native and invasive species All envi-ronmentalconditionsexceptNweresignificantpredictorsofnativerichness In contrast only pH and Secchi depthwere significantpredictorsofinvasiverichnessFurthermoredirectionalityofsomestrong predictors of richnesswere reversed between native andinvasive species For example native richness had a strong neg-ative relationshipwith Pwhile the patternwas positive (thoughnotsignificant)forinvasivespeciesTheoppositepatternwasseenforSecchidepth invasiverichnessdecreasedandnativerichnessincreasedwithgreaterclarityConductanceandchlorophylla were significant negative predictors of native richness and negativelycorrelated but not significant for invaders The generallyweakerresponses of invasive richness to environmental conditions sug-gest that invaders had broader environmental tolerances At thelakescalethesepatternsarepotentiallyconfoundedbythegeneralcorrelationofaveragedepthandlakesizeHoweverbothlakesizeandaveragedepth (asopposed todepthataparticular location)arelikelyproxiesforoverallhabitatvariabilitywhichinturndrivesincreasednativespeciesrichnessratherthanadirectinfluenceofaveragedepthorsizeThusthegeneralpatternofstrongerenvi-ronmentalconstraintsonnativespeciesthaninvadersexistsinde-pendentofwhetherlakesizeandaveragedepthareconfounded

35emsp|emspHeterogeneity

Within-lakeheterogeneity indepthandSecchidepthweresignifi-cantpositivepredictorsofnativerichness(Table1Figure5ac)buthadnoinfluenceoninvasiverichness(Table1Figure5bd)Thisfur-thersupportsthecontentionthatinvadershavelowersensitivitytoenvironmentalconditions


Heterogeneityanalyses

NativerichnessmdashDepthheterogeneity


Coefficient 0079 0006 13223 lt001

InvaderrichnessmdashDepthheterogeneity



NativerichnessmdashSecchidepthheterogeneity


Coefficient 0311 0012 26725 lt001

InvaderrichnessmdashSecchidepthheterogeneity


Coefficient 0050 0058 0856 392

TABLE 1emsp (Continued)


4emsp |emspDISCUSSION

Theaquaticplantcommunitieswestudiedshowedastrongnega-tive relationshipbetweennativeand invasivespecies richnessatlocal (point) scales but a positive relationship at regional (lake-wide) scales matching patterns observed in numerous systemsHowever when we evaluated mechanisms that could generatethesepatternswefoundvaryinglevelsofsupportindicatingthatnotallmechanismswereofequalimportanceSimilarlynomecha-nismdominatedandanygivenfactorexplainedonlyasmallamountof thepatternsobserved innativeand invasivespecies richnessIn contrast withmany terrestrial systems (Kennedy etal 2002LevineAdlerampYelenik2004Naeemetal2000)wefoundnoevidenceforlocal-scalebioticresistanceOurresultsalsoindicateastronginfluenceofenvironmentalconstraintsonlocal-scalerich-nesspatternscountertogeneralexpectationsthatenvironmental

filteringbecomesmoreimportantatbroaderspatialscales(Fridleyetal 2007) Our findings illustrate that similar NERR patternscanbeproducedbydifferentunderlyingmechanismsthatcanbedifficult todiscriminateThesealternativemechanismsmayhavevery different implications for conservation andmanagement ofaquatic plant communities underscoring the value of applying amechanistic lens to evaluating patterns of community structureanddiversity

41emsp|emspStrong opposing roles of environmental drivers on native and invasive species

ContrastingpatternsofnegativeNERRsatlocalscalesandpositiveNERRsatregionalscaleshavebeenseeninavarietyofsystemswesawsimilarpatternsinMinnesotaaquaticplantcommunitiesWhileitisrecognizedthatmultipleprocessescaninfluenceNERRsthere

F IGURE 2emspRelationshipbetweenrichnessofnativespeciesandinvasivespeciesidentifiedinindividualsamples(a)oraggregatedtothelakelevel(b)Pointsarejitteredalongthey-axistoincreasevisibilityofoverlappingpointsThesolidlinesindicatetheestimatedvalueanddashedlinesarethe95confidenceintervalfortheestimate

0 5 10 15Pointminuslevel native species richness

Inva

sive

spe

cies

rich

ness

01

23

0 10 20 30 40Lakeminuslevel native species richness

Inva

sive

spe

cies

rich

ness

01

23

(a) (b)

F IGURE 3emspBioticresistance(a)isindicatedbyanestimateoftheprobabilityofinvasionofindividualsamplinglocationsasafunctionofnativespeciesrichnessColouredlinesindicatethetrendsforindividuallakeswithpurplelinesindicatinglakeswhereinvasionriskdecreaseswithgreaternativespeciesrichness(indicatingbioticresistance)andgreenlinesindicatinghigherriskofinvasionThedashedportionsoflinesindicateestimatescalculatedfornativespeciesrichnessbeyondtherangewhereactualdatawereobservedThesolidblacklinesindicatetheoverallestimatesafteraccountingforautocorrelationwithinlakesandthedashedlinesindicatethe95confidenceintervalforthoseestimatesCompetitiveexclusion(b)isevaluatedbyacomparisonoftherateofchangeinnativespeciesrichnessbetweenlocationsthatareuninvadedacrossallsamplingtimepointsandthosewhereaninvaderispresentHeregreenlinesindicatelakeswithhighervaluesatinvadedpointswhilepurplelinesarelakeswithlowervaluesatinvadedsitesandtheblacklinesagainshowtheoverallestimateswitha95confidenceinterval

0 2 4 6 8 10 12

00

02

04

06

08

10


Pro

babi

lity

of in

vasi

on

(a)

Invader presence

Cha

nge

in s

peci

es ri

chne

ss p

er y

ear

minus3minus2

minus1minus

50

51

23

Uninvaded Invaded

(b)


FIGURE 4emspRelationshipsbetweendepth(abef)orSecchidepth(cdgh) andtherichnessofnativespeciesandinvasivespeciesatindividualsamplinglocations(andashd)andaggregatedacrossentirelakes(endashh)Pointsarejitteredalongthey-axisforclarityandsolidanddashedlinesindicatethemeanand95confidenceintervaloftheestimatedvalue

0 5 10 15 20

05

1015

0 5 10 15 20

01

23

0 5 10 15 20

05

1015

0 5 10 15 20

01

23

0 5 10 15

010

2030

40

0 5 10 15

01

23

0 5 10 15

010

2030

40

0 5 10 15

01

23

Nat

ive

spec

ies

richn

ess

(a)

Inva

sive

spe

cies

rich

ness

(b)N

ativ

e sp

ecie

s ric

hnes

s

(c)In

vasi

ve s

peci

es ri

chne

ss(d)

Nat

ive

spec

ies

richn

ess

(e)

Inva

sive

spe

cies

rich

ness

(f)

Nat

ive

spec

ies

richn

ess

(g)

Inva

sive

spe

cies

rich

ness

(h)

Depth Depth

Secchi depth Secchi depth

Lake average depth Lake average depth

Lake average Secchi depth Lake average Secchi depth


is a general expectation that biotic interactions dominate at localscalesbutaresupplantedbyabioticdeterminantsatbroaderscales(Fridleyetal2007)OurdatadonotsupportthispredictionRatherwefoundthatenvironmentalconditionswere relatively importantpredictorsof richnessat regionaland local scaleswhileeffectsofbiotic interactions were relatively weak However there was stillsubstantialunexplainedvariancethatmaybeinfluencedbyenviron-mentalfactorsnotconsideredaspartofthisstudyorbyalternativeecologicalmechanisms

Nativeandinvasivespeciesweresensitivetodifferentenviron-mentalfactorsinsomecasesevenshowingopposingresponsestothesameenvironmentalgradientsForexamplenativerichnesswasassociated with lower water depth and P while invasive richnesswas associatedwithgreaterdepth andPForwater clarity nativeandinvasivespeciesbothshowedpositiverelationshipsatthelocalscale but the relationshipwasweaker for invasive speciesThesedivergentpreferencessuggestthatnativeandinvasivespeciesoccu-piedsomewhatdifferentnichesSuchnichesegregationalonecouldproduceanegativeNERRwithoutbioticinteractionsbeinginvolved

ThepatternsweobservedindicatethatinvasivespeciesgainedanadvantageovernativespeciesundermoreeutrophicconditionsThis is presumably due to these species being better adapted toexploit higher resource availability and tolerate lower light levels(NicholsampShaw1986WooampZedler2002)Alternativelyitisalsopossible thatpoorwaterquality increasedwithgreaterhumanac-tivityandthathumanactivitywastheproximatecauseofgreaterinvasionratesviaincreasedtransmissionopportunities

Furthermorewhilegreaterenvironmentalheterogeneitywasassociatedwith increased richness of native speciesmdashconsistentwith a large body of ecological theory and literature (LarkinBrulandampZedler2016PickettampCadenasso1995)mdashtherewasno such response by invasive species This suggests that nativespecies were more specialized to depth and light niches withinlakes while invasive species occupied broader niches and werethus able to exploitmoremarginal habitatHowever our analy-seswere limited towater depth and Secchi depth it is possiblethat invadersmayhaveexhibitedgreater responsiveness tohet-erogeneity in other environmental factors Greater responsive-nesstoincreasedresourceavailabilityandbroaderenvironmentaltolerances appear to be attributes of successful invasive plantsin general (Davis Grime amp Thompson 2000 Zedler amp Kercher2004) and global drivers of change reinforce these advantages(ThompsonampDavis2011)Innorthernshallowlakesrecentfind-ings point to persistent anthropogenic shifts to more nutrient-rich turbidalternativestates (RamstackHobbsetal2016)Ourfindingssuggestthatthesechangeswillexacerbateaquaticplantinvasions

42emsp|emspInvasive species win biotic interactions Competitive exclusion but not biotic resistance

How new invasions affect native plant communities depends onbiotic interactions between resident native vegetation and invad-ing speciesWe analysed repeated surveys in the same locations

F IGURE 5emspRelationshipsbetweentheheterogeneityofdepthorSecchidepthinalakeandtherichnessofnativespecies(ac)andinvasivespecies(bd)Pointsarejitteredalongthey-axisforclarityandsolidanddashedlinesindicatethemeanand95confidenceintervaloftheestimatedvalue

0 2 4 6 8 10 12

010

2030

40

Lake depth SD

Nat

ive

spec

ies

richn

ess

0 2 4 6 8 10 12

Lake depth SD

Inva

sive

spe

cies

rich

ness

01

23

0 1 2 3 4

010

2030

40

Lake Secchi depth SD

Nat

ive

spec

ies

richn

ess

0 1 2 3 4


Inva

sive

spe

cies

rich

ness

01

23

(a) (b)

(c) (d)


toinvestigatebioticinteractionsandfoundmixedsupportfortheirimportanceAftersampling locationswere invadednativespeciesrichness tended to decrease over timewhile uninvaded locationsgained species This supports the competitive exclusion hypoth-esisiethatinvadersreducelocal-scalediversitybydisplacingna-tive species In contrastwhenweevaluatedbiotic resistancewefoundnoevidencethatmore-diversesiteswerelesslikelytobesub-sequently invadedAcaveat is that invasionsarehighlystochasticprocessespunctuatedbyrelativelyfewinvasionevents(Macketal2000Simberloff2009)Furthermoreitisdifficulttoresurveypre-ciselocationsovermultipleyearsandimperfectdetectionmaycon-foundspeciesrsquopresenceabsencerecords(ChenKeacuteryPlattnerMaampGardner2013)ThesefactorscanresultinnoisydatasetsandassuchthelikelihoodoftypeIIerrors(falsenegatives)maybeparticu-larlyhighandtheabilitytodetectasignallowYetourabilitytostillidentifycompetitiveexclusiondespitesuchnoisesuggeststhatourgeneralapproachisvalidandthatbioticresistanceislikelyweakerorpotentiallyabsentinthissystemthoughitisdifficulttomakeadirectcomparisonofprocessstrengthsThuswhilewefoundevi-denceofinfluentialbioticinteractionsatthelocalscaleasexpected(Fridleyetal2007)wedidnotobservebioticresistancewhichisoftenconsideredtobethekeydriverforanegativeNERR(FargioneampTilman2005Levineetal2004) Insteadwefoundstatisticallysignificant evidence for competitive exclusionwhich is less oftencitedasadriverofnegativeNERRsThoughtheeffectsweobservedwererelativelymodestontheorderofonemorespeciesbeinglostper decade in invaded sites relative to uninvaded sites and therewashighvariabilitywithmany individualsitesand lakesexhibitingtheoppositepattern

Overtimebioticresistanceandcompetitiveexclusioncanpro-duce similar negativeNERR patterns Studies inwhich richness isexamined at only a single timepoint are inherently unable todis-criminate these twoprocessesYet the twomechanismshavedif-ferent implications for conservation and management A systemwithstrongbioticresistancewillberesilienttoinvasions(FargioneampTilman2005Naeemetal2000)andmanagingfordiversitycanminimizeriskButwherebioticresistanceisweakandcompetitiveexclusion likely uninvaded communities are vulnerable and biodi-versitywillnotreduceinvasionrisk

Thecombinationofbroaderenvironmentaltoleranceofinvasivespecies and the potential for competitive displacement of nativespeciesmayprovidean importantpathwayfor invasionBytakingadvantageofmarginal habitat fornative species invaders canes-tablishinnewareaswithoutfacingcompetitionOnceestablishedpropagule pressure can then promote spread into nearby habitatpreferredbynativespecies(LockwoodCasseyampBlackburn2005)Propagulepressurefromnearbysourceswill farexceedthatasso-ciatedwith rare long-distance dispersal events (Simberloff 2009)andcouldswampeffectsofbioticresistance(ThomsenDrsquoAntonioSuttleampSousa2006)This ldquoleapfroggingrdquoof invasiveplants frommarginal to preferred habitat has been demonstrated in invasionof EuropeanPhragmites australis inNorthAmericawhich spreadsacross the landscape via highway corridors and anthropogenic

habitat(LelongLavoieJodoinampBelzile2007TaddeoampDeBlois2012)providingpropagulesthatcantheninvadeintactnaturalwet-landsanddisplacenativespecies(FantPriceampLarkin2016PriceFantampLarkin2014)Theimportanceofenvironmentalconditionsin determining native and invasive species richness suggest thatmanagementofthosefactorsmaybeakeystrategyforlimitingin-vaderestablishment

At the larger spatial scale of whole lakes our findings morecloselymatchexpectationsfromothersystems(Daviesetal2005Fridleyetal2007LevineampDrsquoAntonio1999)Ourlake-scaleanal-yses showed no evidence of biotic resistance or competitive ex-clusion instead native and invasive species richness increased inconcert This is consistentwithNERRs not being driven by bioticinteractions at large spatial scales but instead broader environ-mental historical or biogeographic factors (Cavender-Bares etal2009Fridleyetal2007Ricklefs2004)Native species richnessincreasedwithenvironmentalheterogeneitywhichalignswiththeexpectationthattheinclusionofbroaderenvironmentalconditionsdrivesregional-scalediversitypatterns(Daviesetal2005Fridleyetal2007LevineampDrsquoAntonio1999)thoughwedidnotobservea similar pattern for invasive specieswith the environmental fac-torsweevaluatedNonethelessevenifinvasivespecieshavebroadenvironmentaltolerancesandarenotinfluencedbyheterogeneitystochasticprocessescouldstillleadtoincreasedinvaderrichnessatlargerspatialscalesresultinginapositiveNERR(FridleyBrownampBruno2004)

43emsp|emspIs biotic resistance ldquoall dryrdquo

Whileourresultsregardingtherelativeimportanceofbioticinterac-tions vs abiotic drivers run counter to previous findingsmdashparticu-larlywithrespecttotheabsenceofbioticresistancemdashthecauseofthat inconsistency remainsuncertain Itmaybepartlydue to fewstudies simultaneously investigating multiple alternative mecha-nismsofNERRs (but seeFargioneampTilman 2005) or topatternsbeingattributed tomechanisms thatarepresumed tobecommonbuthavenotbeenexplicitlytested

Itisalsopossiblethatthepreponderanceofdiversity-invasibilityresearch that comes from terrestrial systems biases expectationsStrong (1992) asked whether trophic cascades were ldquoall wetrdquo Isbiotic resistance ldquoall dryrdquo Nearly all evidence for local-scale bi-otic resistance comes from grassland or other terrestrial systems(FargioneampTilman2005Fridleyetal 2007 Levineetal 2004Naeemetal2000butseeStachowiczetal1999)Relativelylittleresearchhasbeenconductedinaquaticplantcommunitiesandsomepast findings have run counter to terrestrial expectations Capersetal(2007)foundnoevidenceofbioticresistanceinlakeplantcom-munitiesinthenortheasternUSInlakesacrosstheUSFlemingDibbleMadsen andWersal (2015) testedDarwinrsquos naturalizationhypothesisthatnichesbeingoccupiedbycloserelativeswouldrepelinvaderstheyfoundnoevidenceofsuchresistanceStroumlmJanssonandNilsson (2014) experimentally demonstrated a local-scale butpositiveNERRinborealwetlands


Why would diversity-invasibility relationships differ betweenland and water There is some evidence that aquatic plant com-munities are more strongly structured by abiotic environmentalconstraints (Heino Soininen Alahuhta Lappalainen amp Virtanen2017 Santamariacutea 2002) Difficult environmental conditions inaquatic communities particularly at higher latitudes may imposesuch a strong filter on the macrophyte habitat species pool thatspeciesinteractionshavelimitedinfluenceoncommunityassembly(Santamariacutea2002)Similarpatternshavebeenobservedinaquaticinvertebratecommunities(MilnerBrittainCastellaampPetts2001PeckarskyHornampStatzner1990) suggesting that thismaybeacommonpatternforfreshwatersystemsIftherelativeimportanceof abiotic andbioticprocesses inNERRs systematically variesbe-tween terrestrial and aquatic systems then the limited researchperformedinthelattercouldbiasourgeneralunderstandingoftheecologicalmechanismscontributingtothesepatterns

44emsp|emspImplications for biodiversity conservation and invasive species management

Invasive species are one of the most important drivers of globalchangeandcandrasticallyrestructureecosystems(TylianakisDidhamBascompteampWardle2008VitousekDrsquoantonioLoopeRejmanekampWestbrooks1997WHMasonBastowWilsonampBSteel2007)Therelationshipbetweendiversity and compositionof native communi-ties and their invasibility has been a fundamental areaof inquiry inecologygoingbacktoElton(1958)andevenDarwin(Daehler2001)Understandingtheconditionsthatallowinvasivespeciestoestablishandthatmediatetheirimpactsremaincriticalissuesforconservationandmanagement(Byersetal2002Macketal2000)Studyingtherelationshipbetweendiversityofnativespeciesandinvasivespeciescanofferimportantinsightsintothesequestionsbyhelpingtoidentifythefactorsthatsupportordeter invasions Inparticular the ideaofbioticresistancesuggestsaldquovirtuouscyclerdquowhereineffortstosupportbiodiversityalsohelprepel invasionsHoweverthepatternsweob-servedsuggestthatwatershedmanagementtosupportwaterqualitymaybeamoreeffectivemeansofmitigatinginvasionsandtheirim-pactsNonethelessitisclearthatdiversity-invasibilitypatternscanbedrivenbymultiplemechanismsand recognizing thecontext-specificimportance of these differentmechanisms can help refinemanage-mentstrategies

Our analysis of alternativemechanisms underlyingNERRs inshallow lakes reveals several concerning trends (1)environmen-tal conditions consistent with broad patterns of anthropogenicchangebenefitinvasivespecies(2)lakeswithhigherbiodiversityvaluearemorelikelytobecomeinvadedand(3)bioticinteractionsrepresentedaldquobadnews-badnewsrdquoscenariowhereinlocal-scalediversitydoesnotconferresistancetoinvasionbutinvasiondoesreduce local-scale diversity via competitive exclusion Howeverour results do support continued effort towards establishedstrategies for invasive speciesmanagement Specifically effortstomaintainor improve lakecondition reducespreadof invasivespecies and restore diverse plant assemblageswhere they have

beenlostareneededtoslowtheerosionofnativeplantdiversityintheseimportantecosystems

ACKNOWLEDG EMENTS

FundingforthisprojectwasprovidedthroughtheMinnesotaAquaticInvasive Species ResearchCenter from theMinnesota Environmentand Natural Resources Trust Fund We thank A Geisen and theShallowLakesProgramstafffortheirextensiveeffortscollectingandorganizing fielddata (whichwassupportedby theMinnesotaGameandFish fundMinnesotaEnvironmentandNaturalResourcesTrustFundandtheOutdoorHeritageFund)andWGlissonMVerhoeven CWagnerandRNewmanforinputonthemanuscriptTheauthorsdeclarenoconflictsofinterest

AUTHORSrsquo CONTRIBUTIONS

NH-W managed data collection RM and DJL designed thestudyandanalysesRManalysedthedataandwrotetheinitialdraftofthemanuscriptAllauthorsparticipatedindatainterpretationandrevisingthemanuscript

DATA ACCE SSIBILIT Y

MacrophytecommunitydataenvironmentaldataandanalysisscriptsforthisstudyareavailablefromtheDryadDigitalRepositoryhttpsdoiorg105061dryad19cf1c2 (Muthukrishnan Hansel-Welch ampLarkin2018)

ORCID

Ranjan Muthukrishnan httporcidorg0000-0002-7001-6249

R E FE R E N C E S

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BellardCCasseyPampBlackburnTM(2016)Alienspeciesasadriverof recent extinctions Biology Letters 12 20150623 httpsdoiorg101098rsbl20150623

BeloteRTJonesRHHoodSMampWenderBW(2008)DiversityndashinvasibilityacrossanexperimentaldisturbancegradientinAppalachianforestsEcology89183ndash192httpsdoiorg10189007-02701

ByersJEReichardSRandallJMParkerIMSmithCSLonsdaleW M hellip Hayes D (2002) Directing research to reduce the im-pactsofnonindigenousspeciesConservation Biology16630ndash640httpsdoiorg101046j1523-1739200201057x

Capers R S Selsky R BugbeeG J ampWhite J C (2007) Aquaticplantcommunityinvasibilityandscale-dependentpatternsinnativeand invasive species richnessEcology88 3135ndash3143 httpsdoiorg10189006-19111

CasasGScrosatiRampLuzPirizM(2004)TheinvasivekelpUndaria pinnatifida (Phaeophyceae Laminariales) reduces native seaweeddiversityinnuevogulf(PatagoniaArgentina)Biological Invasions6411ndash416httpsdoiorg101023BBINV00000415552930541

Cavender-Bares J Kozak K H Fine P V A amp Kembel S W(2009) The merging of community ecology and phylogenetic


biology Ecology Letters 12 693ndash715 httpsdoiorg101111 j1461-0248200901314x

ChenGKeacuteryMPlattnerMMaKampGardnerB(2013)Imperfectdetection is the rule rather than the exception in plant distri-bution studies Journal of Ecology 101 183ndash191 httpsdoiorg1011111365-274512021

Chesson P (2000) General theory of competitive coexistence inspatially-varying environments Theoretical Population Biology 58211ndash237httpsdoiorg101006tpbi20001486

ClelandEESmithMDAndelmanSJBowlesCCarneyKMClaireHorner-DevineMhellipVandermastDB(2004)InvasioninspaceandtimeNon-nativespeciesrichnessandrelativeabundancerespondtointerannualvariationinproductivityanddiversityEcology Letters7947ndash957httpsdoiorg101111j1461-0248200400655x

DaehlerCC (2001)DarwinrsquosnaturalizationhypothesisrevisitedThe American Naturalist158324ndash330httpsdoiorg101086321316

DaviesKFChessonPHarrisonS InouyeBDMelbourneBAampRiceKJ(2005)Spatialheterogeneityexplainsthescaledepen-denceofthenativendashexoticdiversityrelationshipEcology861602ndash1610httpsdoiorg10189004-1196

DaviesKFHarrisonSSaffordHDampViersJH(2007)ProductivityaltersthescaledependenceofthediversityndashinvasibilityrelationshipEcology881940ndash1947httpsdoiorg10189006-19071

DavisMAGrimeJPampThompsonK(2000)FluctuatingresourcesinplantcommunitiesAgeneraltheoryofinvasibilityJournal of Ecology88528ndash534httpsdoiorg101046j1365-2745200000473x

Elton C S (1958) The ecology of invasions by animals and plants Chicago IL University of Chicago Press httpsdoiorg101007 978-1-4899-7214-9

Fant JBPriceA LampLarkinD J (2016)The influenceofhabitatdisturbanceongeneticstructureandreproductivestrategieswithinstandsofnativeandnon-nativePhragmites australis(commonreed)Diversity and Distributions221301ndash1313httpsdoiorg101111ddi12492

FargioneJEampTilmanD(2005)DiversitydecreasesinvasionviabothsamplingandcomplementarityeffectsEcology Letters8604ndash611httpsdoiorg101111j1461-0248200500753x

Fleming J P Dibble E D Madsen J D amp Wersal R M (2015)InvestigationofDarwinrsquosnaturalizationhypothesisininvadedmac-rophyte communities Biological Invasions 17 1519ndash1531 httpsdoiorg101007s10530-014-0812-0

Fridley JDBrownR LampBruno J F (2004)Nullmodels of ex-otic invasion and scale-dependent patterns of native and ex-otic species richness Ecology 85 3215ndash3222 httpsdoiorg10189003-0676

Fridley J D Stachowicz J J Naeem S Sax D F SeabloomE W Smith M D hellip Von Holle B (2007) The invasion par-adox Reconciling pattern and process in species invasionsEcology 88 3ndash17 httpsdoiorg1018900012-9658(2007)88 [3TIPRPA]20CO2

HalekohUampHoslashjsgaardS(2014)AKenward-RogerapproximationandparametricbootstrapmethodsfortestsinlinearmixedmodelsndashTheRPackagepbkrtestJournal of Statistical Software591ndash32

HeinoJSoininenJAlahuhtaJLappalainenJampVirtanenR(2017)MetacommunityecologymeetsbiogeographyEffectsofgeograph-icalregionspatialdynamicsandenvironmentalfilteringoncommu-nitystructureinaquaticorganismsOecologia183121ndash137httpsdoiorg101007s00442-016-3750-y

HenrikssonAWardleDATryggJDiehlSampEnglundG(2016)Strong invaders are strong defenders ndash Implications for the resis-tanceofinvadedcommunitiesEcology Letters19487ndash494httpsdoiorg101111ele12586

HustonMA(1999)LocalprocessesandregionalpatternsAppropriatescalesforunderstandingvariationinthediversityofplantsandani-malsOikos86393ndash401httpsdoiorg1023073546645

Kennedy T A Naeem S Howe KM Knops JM H Tilman DampReich P (2002) Biodiversity as a barrier to ecological invasionNature417636ndash638httpsdoiorg101038nature00776

LarkinDJBrulandGLampZedlerJB(2016)HeterogeneitytheoryandecologicalrestorationInMAPalmerJBZedlerampDAFalk(Eds)Foundations of restoration ecology(pp271ndash300)WashingtonDCIslandPresshttpsdoiorg105822978-1-61091-698-1

LelongBLavoieCJodoinYampBelzileF(2007)Expansionpathwaysoftheexoticcommonreed(Phragmites australis)Ahistoricalandge-netic analysisDiversity and Distributions13 430ndash437 httpsdoiorg101111j1472-4642200700351x

LevineJM(2000)SpeciesdiversityandbiologicalinvasionsRelatinglocalprocesstocommunitypatternScience288852ndash854httpsdoiorg101126science2885467852

LevineJMAdlerPBampYelenikSG(2004)Ameta-analysisofbi-oticresistancetoexoticplantinvasionsEcology Letters7975ndash989httpsdoiorg101111j1461-0248200400657x

LevineJMampDrsquoAntonioCM(1999)EltonrevisitedAreviewofevi-dencelinkingdiversityandinvasibilityOikos8715ndash26httpsdoiorg1023073546992

Lockwood J LCasseyPampBlackburnT (2005)The roleofpropa-gulepressure inexplainingspecies invasionsTrends in Ecology and Evolution20223ndash228httpsdoiorg101016jtree200502004

MackRNSimberloffDLonsdaleWMEvansHCloutMampBazzazF A (2000) Biotic invasions Causes epidemiology global conse-quences and controlEcological Applications10 689ndash710 httpsdoiorg1018901051-0761(2000)010[0689BICEGC]20CO2

Milburn S A BourdaghsM ampHusveth J J (2007)Floristic quality assessment for minnesota wetlandsStPaulMNMinnesotaPollutionControlAgency

Millennium Ecosystem Assessment (2005) Ecosystems and human well-being SynthesisWashingtonDCIslandPress

MilnerAMBrittainJ ECastella EampPettsGE (2001)Trendsofmacroinvertebratecommunitystructureinglacier-fedriversinrelationtoenvironmentalconditionsAsynthesisFreshwater Biology461833ndash1847httpsdoiorg101046j1365-2427200100861x

MuthukrishnanRHansel-WelchNampLarkinDJ(2018)DatafromEnvironmentalfilteringandcompetitiveexclusiondrivebiodiversity-invasibility relationships in shallow lake plant communitiesDryad Digital Repositoryhttpsdoiorg105061dryad19cf1c2

NaeemSKnopsJMHTilmanDHoweKMKennedyTampGaleS(2000)Plantdiversityincreasesresistancetoinvasionintheab-senceofcovaryingextrinsicfactorsOikos9197ndash108httpsdoiorg101034j1600-07062000910108x

NicholsSAampShawBH(1986)Ecologicallifehistoriesofthethreeaquatic nuisance plantsMyriophyllum spicatum Potamogeton cris-pus and Elodea canadensis Hydrobiologia 131 3ndash21 httpsdoiorg101007BF00008319

Olmanson L G Bauer M E amp Brezonik P L (2008) A 20-yearLandsatwater clarity census ofMinnesotarsquos 10000 lakesRemote Sensing of Environment 112 4086ndash4097 httpsdoiorg101016 jrse200712013

OlmansonLGBrezonikPLampBauerME (2014)Geospatialandtemporalanalysisofa20-yearrecordofLandsat-basedwaterclar-ity in Minnesotarsquos 10000 Lakes JAWRA Journal of the American Water Resources Association50 748ndash761 httpsdoiorg101111jawr12138

PaavolaM Olenin S amp Leppaumlkoski E (2005) Are invasive speciesmost successful in habitats of low native species richness acrossEuropeanbrackishwater seasEstuarine Coastal and Shelf Science64738ndash750httpsdoiorg101016jecss200503021

Peckarsky B L Horn S C amp Statzner B (1990) Stonefly preda-tion along a hydraulic gradient A field test of the harshmdashbe-nign hypothesis Freshwater Biology 24 181ndash191 httpsdoiorg101111j1365-24271990tb00317x


PickettSTAampCadenassoML(1995)LandscapeecologySpatialheterogeneityinecologicalsystemsScience269331ndash333httpsdoiorg101126science2695222331

PriceALFantJBampLarkinDJ(2014)Ecologyofnativevsintro-duced Phragmites australis(commonreed)inChicago-areawetlandsWetlands34369ndash377httpsdoiorg101007s13157-013-0504-z

RCoreTeam(2014)R A language and environment for statistical comput-ingViennaAustriaRFoundationforStatisticalComputing

Ramstack Hobbs J M HobbsW O Edlund M B Zimmer K DTheissenKMHoidalNhellipCotnerJB(2016)ThelegacyoflargeregimeshiftsinshallowlakesEcological Applications262662ndash2676httpsdoiorg101002eap1382

RichardsCLBossdorfOMuthNZGurevitch JampPigliucciM(2006)JackofalltradesmasterofsomeOntheroleofphenotypicplasticityinplantinvasionsEcology Letters9981ndash993httpsdoiorg101111j1461-0248200600950x

Ricklefs R E (2004) A comprehensive framework for global pat-terns in biodiversity Ecology Letters 7 1ndash15 httpsdoiorg101046j1461-0248200300554x

SantamariacuteaL(2002)WhyaremostaquaticplantswidelydistributedDispersalclonalgrowthandsmall-scaleheterogeneityinastressfulenvironmentActa Oecologica23137ndash154httpsdoiorg101016S1146-609X(02)01146-3

SimberloffD(2009)Theroleofpropagulepressureinbiologicalinva-sionsAnnual Review of Ecology Evolution and Systematics40 81ndash102httpsdoiorg101146annurevecolsys110308120304

SimberloffDampVonHolleB(1999)Positiveinteractionsofnonindig-enous species InvasionalmeltdownBiological Invasions1 21ndash32httpsdoiorg101023A1010086329619

Stachowicz J JWhitlatch R BampOsman RW (1999) Species di-versityandinvasionresistanceinamarineecosystemScience2861577ndashLP-1579httpsdoiorg101126science28654441577

StohlgrenTJBinkleyDChongGWKalkhanMASchellLDBullKAhellipSonY(1999)ExoticplantspeciesinvadehotspotsofnativeplantdiversityEcological Monographs6925ndash46httpsdoiorg1018900012-9615(1999)069[0025EPSIHS]20CO2

Stroumlm L Jansson R ampNilsson C (2014) Invasibility of borealwet-landplantcommunitiesJournal of Vegetation Science251078ndash1089httpsdoiorg101111jvs12157

StrongDR (1992)Are trophic cascadesallwetDifferentiationanddonor-controlinspecioseecosystemsEcology73747ndash754httpsdoiorg1023071940154

Taddeo S amp De Blois S (2012) Coexistence of introduced and na-tive common reed (Phragmites australis) in freshwater wetlandsEcoscience1999ndash105httpsdoiorg10298019-2-3468

ThompsonKampDavisMA(2011)WhyresearchontraitsofinvasiveplantstellsusverylittleTrends in Ecology amp Evolution26155ndash156httpsdoiorg101016jtree201101007

ThomsenMADrsquoAntonioCMSuttleKBampSousaWP (2006)EcologicalresistanceseeddensityandtheirinteractionsdeterminepatternsofinvasioninaCaliforniacoastalgrasslandEcology Letters9160ndash170httpsdoiorg101111j1461-0248200500857x

Tilman D (2004) Niche tradeoffs neutrality and community struc-ture A stochastic theory of resource competition invasion and

communityassemblyProceedings of the National Academy of Sciences of the United States of America 101 10854ndash10861 httpsdoiorg101073pnas0403458101

Tylianakis J M Didham R K Bascompte J amp Wardle D A(2008) Global change and species interactions in terres-trial ecosystems Ecology Letters 11 1351ndash1363 httpsdoiorg101111j1461-0248200801250x

USDA N (2016) The PLANTS Database Retrived from httpplantsusdagov

VazquezDP(2006)ExploringtherelationshipbetweennichebreadthandinvasionsuccessInMWCadotteSMMcmahonampTFukami(Eds)Conceptual ecology and invasion biology Reciprocal approaches to nature (pp307ndash322)DordrechtNetherlandsSpringerhttpsdoiorg1010071-4020-4925-0

Vitousek P M Drsquoantonio C M Loope L L Rejmanek M ampWestbrooksR(1997)IntroducedspeciesAsignificantcomponentofhuman-causedglobalchangeNew Zealand Journal of Ecology211ndash16

WHMasonNBastowWilsonJampBSteelJ(2007)Arealternativestable states more likely in high stress environments Logic andavailable evidencedonot supportDidhamet al 2005Oikos116353ndash357httpsdoiorg101111j0030-1299200715283x

Wardle D A (2001) Experimental demonstration that plant diver-sity reduces invasibilityndashEvidenceof abiologicalmechanismor aconsequence of sampling effect Oikos 95 161ndash170 httpsdoiorg101034j1600-07062001950119x

Woo I amp Zedler J B (2002) Can nutrients alone shift a sedgemeadow towards dominance by the invasive Typha times glaucaWetlands 22 509ndash521 httpsdoiorg1016720277-5212(2002) 022[0509CNASAS]20CO2

YurkonisKAMeinersSJampWachholderBE(2005)Invasionimpactsdiversity through altered community dynamics Journal of Ecology931053ndash1061httpsdoiorg101111j1365-2745200501029x

Zedler J B amp Kercher S (2004) Causes and consequences of in-vasive plants in wetlands Opportunities opportunists and out-comes Critical Reviews in Plant Sciences 23 431ndash452 httpsdoiorg10108007352680490514673

SUPPORTING INFORMATION

Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle

How to cite this articleMuthukrishnanRHansel-WelchNLarkinDJEnvironmentalfilteringandcompetitiveexclusiondrivebiodiversity-invasibilityrelationshipsinshallowlakeplantcommunitiesJ Ecol 2018001ndash13 httpsdoiorg1011111365-274512963


1emsp |emspINTRODUC TION

The relationship between the diversity of ecological communitiesandtheirpropensitytobeinvadedbyexoticspecieshasbeenheav-ilydebated(FargioneampTilman2005Kennedyetal2002Levine2000 Levine amp DrsquoAntonio 1999Wardle 2001) Much researchparticularlymodelling and small-scale experiments has supportedanegativerelationshipbetweendiversityandinvasibilityHoweveratlarger(egregional)scalestheoppositepatternisfrequentlyob-servedwithmorediversecommunitieshavingmoreexoticspecies(Cleland etal 2004 Levine amp DrsquoAntonio 1999 Stohlgren etal1999)Thisscale-dependentshiftinthenative-exoticrichnessrela-tionship(NERR)remainsdifficulttoexplainwithmultipleprocessespotentiallyinteractingtoproduceoverallpatternsAtthesametimeinvasive species are a global ecological threat (Bellard Cassey ampBlackburn 2016MillenniumEcosystemAssessment 2005) thusimprovingunderstandingofbiodiversity-invasibilityrelationshipsisimportantforsupportingconservationandmanagement

A common explanation for scale-dependentNERR differencesisthatseparateprocessesdrivelocalandregionalpatterns(LevineampDrsquoAntonio1999Stohlgrenetal1999)Ithasbeenpositedthatat local scales high diversity confers biotic resistance to invasion(FargioneampTilman2005Kennedyetal2002)butthatatbroaderscales incorporation of new habitats that are favourable for na-tiveandinvasivespeciesalikeincreasesdiversityofbothinparallel(LevineampDrsquoAntonio1999Naeemetal 2000)However furtherwork has highlighted other processes that may influence NERRs(Fridleyetal2007)Spatialheterogeneityinenvironmentalcondi-tionsmaysupportpositiveNERRs(Daviesetal2005)byincreasingavenues for coexistence (eg Chesson 2000 Tilman 2004) Thestrengthordirectionofalocal-scaleNERRcanalsoshiftasafunc-tionofproductivitydisturbanceorenvironmentalgradients(BeloteJonesHoodampWender2008DaviesHarrisonSaffordampViers2007)Forexampleinvadersthathavebroaderenvironmentaltoler-ancesorpreferlessproductiveconditionsmayoccuronaverageinlessdiverselocalities(egPaavolaOleninampLeppaumlkoski2005)be-causethoseconditionstendtocorrelatewithlowerdiversityInsuchcasesnegativeNERRsmayarisethroughasamplingeffectwithouttheneedforanyparticularbioticinteractiontobeinvolved

ThemanagementimplicationsofanNERRcandifferdependingonitsunderlyingmechanism(s)ForexampleanegativeNERRresult-ing fromdiversity-drivenbiotic resistancewouldargue foreffortstocreateormaintaindiversitytopre-emptinvasionIncontrast if

suchpatternsarearesultofcompetitiveexclusionbythe invadereffortstoincreasediversitymayofferlittleprotectionagainstinva-sionAttheregionalscaleifapositiveNERRarisesbecauseinvasiveandnativespeciesshareenvironmentalpreferencesthenthemostresource-richenvironmentsmaybeatthegreatestriskofinvasionAlternativelyifheterogeneityisthedrivingmechanismforanNERRthemostvariablelocalesmaybemostvulnerable

EveninasinglesystemNERRsarelikelytoarisefrommultipleprocessesespeciallyacrosslocalandregionalscales(Fridleyetal2007)Howeverthereisagrowingconsensusthatbioticinteractionstendtobekeydriversofcommunitystructureatlocalscaleswhileenvironmental conditionsbecomemore influential as spatial scaleincreases(Fridleyetal2007)ThusamoremechanisticperspectivethatevaluatesmultipleprocessesatmultiplescalesisneededSuchstudiesarelogisticallydifficulttoconductasexperimentsbutlarge-scale long-termmonitoringdatasetsofferanalternativemeanstoaddressthesedynamics

Herewefocusonfourmechanismsthatcouldinfluencenativeorexoticspeciesdiversitythreeofwhichwecouldevaluateatmul-tiplespatialscalesBiotic resistance to invasionhas longbeencon-sideredapotentialbenefitofdiversecommunities(Elton1958)andiswell-supportedbyexperimentalwork(FargioneampTilman2005Kennedyetal2002Levine2000Naeemetal2000StachowiczWhitlatchampOsman1999)thoughtheuniversalityofthismecha-nismhasbeenquestioned(CapersSelskyBugbeeampWhite2007)Invasivespeciescanalsocompetitively excluderesidentspeciesafterestablishment(CasasScrosatiampLuzPiriz2004YurkonisMeinersampWachholder2005)producingapatternofnativeandinvaderrich-nesssimilartobioticresistancebutwithadifferenttemporalsigna-tureielossofnativediversityfollowinginvasionratherthanlowerlikelihoodofsubsequentinvasionindiverselocalesThirdlyenviron-mental filtering influences speciesrsquo abilities toestablishandpersistin particular localities Alignment of preferences between nativesandinvaderscouldproducepositiveregionalNERRswhilecompet-itiveinteractionsdeterminelocal-scaleoutcomes(Cavender-BaresKozakFineampKembel2009Daviesetal2005)Alternativelyifin-vadershavewiderenvironmentaltolerancesthannatives(RichardsBossdorf Muth Gurevitch amp Pigliucci 2006 Vazquez 2006) anegativelocalNERRcouldbeproducedbyinvadersestablishinginmarginalhabitatwithfewnativespeciesLastlyenvironmental het-erogeneity in conditions or habitat types is a keymechanism sup-portingoveralldiversity thatcan increasebothnativeand invaderrichness (Daviesetal2005)Thiseffect is likely tobecomemore

researchandforcomparisonsacrossdifferenttypesofecosystemsIdentificationof different drivers of diversity also has direct implications for decisions aboutmanagementoffreshwaterplantcommunities

K E Y W O R D S

aquaticplantsbiodiversitybioticresistancecompetitiveexclusionenvironmentalfilteringheterogeneityinvasionecologynative-exoticrichnessrelationship





















3emsp |emspRESULTS




0 10 20 30 40

InvadedUninvaded


Num

ber o

f lak

es0

2040

6080








Bioticinteractions


Coefficient 0053 0054 0971 356


Coefficient 0028 0026 1103 270



Lake Intercept 0021 0182 0114 910

Coefficient 0239 0221 1080 282





Coefficient 0010 0004 2747 006







Coefficient 0037 0001 25767 lt001


Coefficient 0125 0004 29164 lt001





Coefficient 0014 0022 0656 512



pH 0087 0043 2006 045



N 0028 0051 0550 582


Secchidepth 0106 0038 2829 005



pH 0412 0175 2355 019


P 0953 0923 1032 302

N 0050 0140 0360 719



(Continues)
















Coefficient 0079 0006 13223 lt001






Coefficient 0311 0012 26725 lt001



Coefficient 0050 0058 0856 392










Inva

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(a) (b)


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of in

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Invader presence

Cha

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minus3minus2

minus1minus

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Uninvaded Invaded

(b)



0 5 10 15 20

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ACKNOWLEDG EMENTS






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3emsp |emspRESULTS




0 10 20 30 40

InvadedUninvaded


Num

ber o

f lak

es0

2040

6080








Bioticinteractions


Coefficient 0053 0054 0971 356


Coefficient 0028 0026 1103 270



Lake Intercept 0021 0182 0114 910

Coefficient 0239 0221 1080 282





Coefficient 0010 0004 2747 006







Coefficient 0037 0001 25767 lt001


Coefficient 0125 0004 29164 lt001





Coefficient 0014 0022 0656 512



pH 0087 0043 2006 045



N 0028 0051 0550 582


Secchidepth 0106 0038 2829 005



pH 0412 0175 2355 019


P 0953 0923 1032 302

N 0050 0140 0360 719



(Continues)
















Coefficient 0079 0006 13223 lt001






Coefficient 0311 0012 26725 lt001



Coefficient 0050 0058 0856 392










Inva

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Cha

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minus3minus2

minus1minus

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(b)



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ACKNOWLEDG EMENTS






ORCID


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Bioticinteractions


Coefficient 0053 0054 0971 356


Coefficient 0028 0026 1103 270



Lake Intercept 0021 0182 0114 910

Coefficient 0239 0221 1080 282





Coefficient 0010 0004 2747 006







Coefficient 0037 0001 25767 lt001


Coefficient 0125 0004 29164 lt001





Coefficient 0014 0022 0656 512



pH 0087 0043 2006 045



N 0028 0051 0550 582


Secchidepth 0106 0038 2829 005



pH 0412 0175 2355 019


P 0953 0923 1032 302

N 0050 0140 0360 719



(Continues)
















Coefficient 0079 0006 13223 lt001






Coefficient 0311 0012 26725 lt001



Coefficient 0050 0058 0856 392










Inva

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Cha

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minus3minus2

minus1minus

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(b)



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ACKNOWLEDG EMENTS






ORCID


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Coefficient 0079 0006 13223 lt001






Coefficient 0311 0012 26725 lt001



Coefficient 0050 0058 0856 392










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Cha

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minus3minus2

minus1minus

50

51

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Uninvaded Invaded

(b)



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0 2 4 6 8 10 12

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ACKNOWLEDG EMENTS






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Inva

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0 2 4 6 8 10 12

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of in

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minus3minus2

minus1minus

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(b)



0 5 10 15 20

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0 5 10 15 20

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0 2 4 6 8 10 12

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ACKNOWLEDG EMENTS






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environmental filtering and competitive exclusion drive … · 2018-04-24 · 1. understanding the...

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