Ecologicalnicheandspeciestraits:keydrivers ofregional plant invader assemblages

Wilfried Thuiller • Nu´riaGasso´ • Joan Pino•

MontserratVila`

Abstract Linkingspeciestraitstonichepropertiesis fundamentaltounderstand thespatialstructureof invasivespeciesassemblagesandtheinvasionprocess itself.Usinginformation on74invasivespeciesin Spain, theaimsofthispaperareto(1)testwhether invasiveplantspeciesassemblages followanested patternattheregionalscale,(2)inspecttherelationship betweenrangesizeandnicheproperties(positionand breadth)ofinvasivespeciesto testwhetherthe nested patternisaproductofspeciesnicheoverlap;andfinally (3)examinehowspeciestraitsofinvadersarerelatedto theirnicheproperties.Weshowthatregionalinvasive plantspeciesassemblagesinSpainareorganizedin nestedsubsets.Invasivespecieswithrestrictedrange

W.Thuiller()

Laboratoired’EcologieAlpine,CNRS-UMR5553, Universite´JosephFourier,BP53,38041

GrenobleCedex9,France

e-mail:

N.Gasso´ J.Pino

CREAF(CentreforEcologicalResearchandForestry

Applications),UniversitatAuto`nomadeBarcelona,

08193Bellaterra,Catalonia,Spain e-mail:

J.Pino

e-mail:

M.Vila`

Estacio´nBiolo´gicadeDon˜ana-CentroSuperiorde

InvestigacionesCient´ıficas(EBD-CSIC),Avda.Ame´rico

Vespucios/n,IsladelaCartuja,41092Sevilla,Spain e-mail:

occurinareasinvadedbywidespreadinvaders.By relatingnestednessmetricstospecies’nicheproperties frommultivariateanalyses,wefound thatthese restrictedinvaders arelesstolerantofbroadclimatic andlandscapeconditionsthanwidespreadinvaders. Finally, regarding theassociationbetween niche properties andspeciestraits,wefoundthatspecies withlargeenvironmental nichebreadthcommonly exhibitnonN-fixing strategy,short-lifespan,and clonalgrowth, whilethosewithnichepositionin anthropogeniccoastalareaswereperennialandclonal speciesofunintentionalandagriculturalorigin.Using anintegrativeapproach linkingtheregionalspatial structureof invasiveplantassemblages,speciesniche properties andspeciestraits,wewereabletounder- standthepotentialcausesofinvasivespeciesdistribu- tioninSpain.Theapproachdevelopedinthisresearch couldbeeasilyappliedtootherareastodisentanglethe mechanismsdrivinginvasivespeciesdistributions.

KeywordsAlienplants Clonalgrowth Disturbance Invasiveness Inference-basedmodel Life-historytraits Nestedness Nicheposition Nichebreadth Rangesize

Introduction

Lesseningtheecologicalandsocio-economicimpactsof invasivespeciesrequiresacomprehensiveunderstanding

ofthe factorsdrivinginvasions(Mack1996;Pysˇek etal.2010).Invasionecologyhasmainlyfocusedon thefactorsthatmakeeitheraspecies aninvader (Hamiltonetal.2005;Rejma´nek1995)orahabitat pronetoinvasion(Pauchardetal.2004;Pysˇek2004; Stohlgren etal.2005).However, thesetwoapproaches havebeenkeptseparateuntilrecently,when such species havebeguntobeconsidered ashavingasetof intrinsic and extrinsic traits that result invasiveness (i.e.potentialtoinvade) incertainenvironmental conditions (Jiangetal.2010;SaxandBrown2000; SheaandChesson 2002;Thuilleretal.2010b).This integrated approachisfundamentalto understanding thecomposition ofinvasivespeciesassemblages, becausebothspeciesproperties andrecipienthabitat characteristicsareknown todeterminethelevelof invasioninhabitatsandregions.

Fromabiogeographic perspective,onemight wonderwhether certaininvadershaveverygeneral requirements explainingtheirlargedistributional rangesandoverlaps, orwhethertheyneedspecific environmentalconditions.Thisquestionhasseldom beenexplored.Inageneralcontext,afirststepwould betoinvestigateifspeciesassemblages arenestedat theregional scale.Inotherwords, arespecies present inspecies-poor sitesonlysubsetsofthespeciesfrom species-richsites?Inthiscase,assemblageswithfew species tendtobemadeupofthemostfrequently occurringspecies,whiletheleastfrequentlyoccurring speciesarenotrestrictedtospecificsitesbutoccurin species richareas.Thispatternhasbeenmostly investigatedfornativeanimalcommunities(Wright etal.1998),andwhether such anestedpatternisalso foundininvasiveplantspeciesassemblages is unknown.

In the caseofinvasiveplants,speciesdistribu- tion could be the outcome of a combination of factors such as minimum residence time (Ahern etal.2010; Gasso´etal.2010; Phillips etal.2010; Wilsonetal.2007),propagulepressure(Lockwood et al. 2005; Pysˇek et al. 2010) and species ecologicalrequirements asrepresentedbytheir realizedecological niche(Thuilleret al. 2005; Va´zquez2006;Jime´nez-Valverde etal.2011). Althoughseveralstudieshaveappliednichetheory toinvasion biology(Fitzpatrick andWeltzin2005; Gallagheret al. 2010;Roura-Pascualet al. 2009), little effort has been made to establish a link between the physiological, morphological and

reproductive attributesofspeciesandtheirniche propertieslikenicheposition(e.g.averageposition on a given gradient) and niche breadth (e.g. standarddeviationaroundthe averagepositionon a given gradient) (but see Ku¨hn et al. 2006; Niinemets 2001;Thuilleretal.2010a).Theinves- tigationofthistopicwillenlargeourunderstanding ontherelationshipbetweeninvaderrangesize(i.e. thesizeofthedistribution area)andspeciestraits (Gasso´etal.2009;Lloretetal.2005).

Weargueherethattherangesizeofaninvader is relatedtoitsniche(Brown1995;Gaston andBlack- burn2000).Abroaderniche,forinstance, might enablethespeciestobecomemoresuccessful andto reachlargerangesizes(Va´zquez2006). Ourhypoth- esisisthatanested patternofspecies assemblages couldbetheresultofanicheoverlap among rareand widespreadinvasivespecies(GastonandBlackburn

2000),anddifferencesamongnichesmightbe,inturn, aconsequenceofdifferencesbetweenspeciestraits (Albertetal. 2010;Thuiller et al.2004;Va´zquez

2006).

Weexaminedthesizeofinvader plantspecies’ rangesacrossmainlandSpain, theirtraitsandthe environmental characteristicsofinvadedareasin orderto(1)testwhetherinvasive plantspecies assemblages attheregionalscalefollowanested pattern,(2)inspecttherelationshipbetweenrangesize andnichepositionandbreadthtotestwhether the nestedpatternisaproduct ofspeciesnicheoverlap; andfinally(3)examineifcertainspeciestraitsare relatedtonicheposition ornichebreadth,and therefore,arerelatedtoaspecies’ potentialof becomingwidespread.

Methods

Studyregion

SpainislocatedintheSWofEuropeandoccupies

493,486km2.Theregionhasalonghistoryofplant speciesintroductions,enoughformanyspeciestobe

distributed acrossawiderangeofenvironmental conditions(Sanz-Elorzaetal.2004). Duetoits geographic,topographic,climaticandgeologicheter- ogeneity,Spainhasahighlandscape andhabitat diversity (Ninyerola et al. 2000; Valladareset al.

2005),includingarid,Mediterranean,temperateand alpineecosystems,providingabroadenvironmental rangeforplantinvasions(Gasso´etal.2009).

Table1 Intrinsic and extrinsic species traits taken into accounttoexplaininvasive plantspeciesnicheposition and breadthinSpain

Dataset

Intrinsictraits

CategoryCode

Invasivespeciesandtraits

Dataonthedistribution ofinvasiveneophytes(i.e. established aliensintroducedafter1500)were extractedfromtheAtlasofInvasive PlantSpecies in Spain(Sanz-Elorzaetal.2004).Invasive speciesare definedfollowingPysˇeketal.(2004):alienspecies withself-sustainablepopulations withoutdirect humaninterventionthatproducesoffspringatconsid- erabledistancesfromtheparentplants,and thushave thepotentialtospread overlargeareas.TheAtlas containspresence recordsforover100species ata resolution of 10km UTM (Universal Transverse Mercator)grid,butwerestrictedtheanalysesto74 speciesfoundatleastin10UTMgridcellsinmainland Spain.Thiswasmadetoavoidsporadicspecies with relativelyunknowndistributionsand tomakesure we hadenoughinformation relatedtoenvironmental descriptors. Duetothepotentialheterogeneityof samplingeffortacrossthecountryandtheconsequent difficulty ofdistinguishingbetweentheabsenceof invasive speciesandmissingdata,theanalyseswere alsolimitedtoUTM cellswithatleastoneinvasive speciesrecorded. Inordertohavecomparablepixels withsimilarlandsurface, wealsoexcludedcoastal UTMcellswithalandproportionlowerthan60 %. Thefinal numberofUTMcellsincludedinthe analyseswas2401.

Foreachspecieswecalculateditsrangesizeas the numberofoccupiedUTMcells(Gasso´etal.2010)and exploredalistofintrinsic (i.e.seedsize,clonal growth,longevity,life-form,dispersalandpollination syndromes,andnitrogenfixingcapacity)andextrinsic traits(i.e.regionoforiginandpathway ofintroduc- tion)thatarecommonly associatedtoinvasiveness (PysˇekandRichardson 2007;Thuilleretal.2006) (Table1).

Residencetimewasestimatedastheyearoffirst bibliographicorherbariumrecordinSpain.Allthe aboveinformationwastakenfromCastroviejo etal. (1986–2000),Casasayas(1990),Bolo´setal.(1993) andSanz-Elorzaetal.(2004).SeeTable6inAppendix forthetraitvaluesofall74species.

SeedsizeVerylarge([10mm)5

Large(5–10mm)4

Medium(2–5mm)3

Small(1–2mm)2

Verysmall(\1mm)1

N-fixingYesYes

NoNo

ClonalgrowthYesYes

NoNo

LongevityAnnualAnnual BiennialBiennial PerennialPerennial

Life-formChamaephyte Ch GeophyteGe HemicryptophyteHe MacrophanerophyteMc Mesophanerophyte Ms Nanophanerophyte Nn Therophyte Th Vine Vi

DispersalsyndromeAnemochoryWind ZoochoryAnimal HydrochoryWater

PollinationtypeAnemophilyWind

ZoophilyAnimal

Extrinsictraits

RegionoforiginAmericaAM SouthAmericaSM NorthAmericaNM AsiaA EuropeE AfricaSF Oceania O

Pathwayofintroduction Agriculture A GardeningG SilvicultureS WeedW UnintentionalU

Thedifferentcategoriesforeachtraitandthecodeusedin

Fig.4andTable6inAppendixareshown

Environmentaldata

Modelsforinvaderspecies’realizednicheswerebased oninformation fromasetofnineteenenvironmental predictors groupedunderland cover,topographicand climaticvariables(Table2)gatheredfromdifferent sources andaveraged at10kmUTMgridresolution. Theproportion ofmainlandcovercategories(i.e. built-up areas,agriculturalareas,forests, scruband herbaceous vegetation,openspaces,wetlandsand waterbodies)werecalculatedfromtheCORINELand CoverMapofSpain( coverdiversityperUTMcellwasestimatedbycalcu- latingtheShannonindexoftheabove-mentionedland covercategories(Shannon1948).

Roadlength(m)andrailway length(m)were calculated from maps obtained from the official serveroftheSpanishMinistry( Weconsidered thesehumansettlementvariablesasa measureofhumanfootprint(Sandersonetal.2002) andassurrogates forpropagulepressure (Pysˇek etal.

2002).Mean altitude(m)andaltituderange(m)were calculatedfromthenationalDigitalElevationsModel (DEM) at 100m resolution ( uab.es). Meandistancetothecoastline(m)wascal- culatedusingMiraMon distance algorithms.

Finally,sixclimaticvariableswerecalculatedfrom theDigitalClimaticAtlasofSpain(Ninyerolaetal.

2005; agridsetof200m9200mpixelsizegeneratedby modellingfromtheSpanishnetwork ofmeteorologi- calstations.Wecalculatedthemeanvaluespersiteof annualtemperature(°C), minimumwintertempera- ture(°C),temperaturerange(i.e.difference between maximum temperatureinJulyandminimaltempera- tureinJanuary),annualrainfall(mm),summerrainfall (sumoftherainfallinJune,JulyandAugust) and annualsolarradiation(KJm-2 day-1 lm-1).

Nestednessinspeciesassemblages

Weusedanestednessindextoestimatethedegreeof associationamonginvasivespecies’occurrences in UTMcells.Thisprocedure aimedatevaluating whetherspeciescomposition inagivensitewas random(lownestedness)orspecies-poorsiteswere madeupbythemostfrequent invadersfromthe regionalpool(highnestedness). Theminimum requirementfornestednessisthatsitesdifferintheir

suitability, andspeciesdifferintheirabilitiesto colonizeandpersistinthem(RytiandGilpin1987).

Tovalidatetheexistenceofanested structure amongspeciesandsites,weestimatedthenestedness index (N)as N=(100-T)/100,where T is the so-called ‘Temperature’index,whichmeasures the site-occurrence matrixdisorderwithvaluesranging from0°to100°(AtmarandPatterson1993).Because wewereinterestedinemphasizingorderednestedness ratherthandisordered, wecalculatedthelevelofN, withvaluesrangingfrom0(minimumN) to1 (maximumN).Nwascalculatedusingthe Nestedness CalculatorSoftware(AtmarandPatterson 1993; Wrightetal.1998),whichreorders therowsand columns ofthematrixtominimizetheunexpected occurrences,andpackthematrixintoastateofmax- imalnestedness (i.e.sitesindescending orderof species richness and species in decreasing order ofrangeextension).Then,Tiscalculatedasthesum ofsquareddeviations fromtheisoclineofperfect nestedness ofunexpectedpresencesandabsences, dividedbythemaximumvaluepossibleforthematrix, multipliedby100.ToassessthesignificanceofTwe comparedtheobservedvalueofTwithabenchmarkof

500randommatricesprovided byanullmodelin whicheachcellinthematrix hasthesameprobability ofbeingoccupied(GastonandBlackburn2000).This isanefficient waytotestiftheobservednestedness differedfromarandompattern(Wright etal.1998).

Species’nicheproperties

Toseparate invaderspeciesnichesbasedonspecies distribution andtheenvironmentalvariablesselected (Table2),weusedtheoutlying meanindex analysis (OMI,hereafter),amethodproposedbyDole´decetal. (2000) andimplementedintheade4library(Chessel etal.2004)inR(RDevelopment CoreTeam2012). TheOMImakesnoassumption abouttheshapeof curvesofspeciesresponsetotheenvironment,and givesequalweighttospecies-rich andspecies-poor sites.Thismethod determinesnichepositionasthe meanlocationofthespecies intheenvironmental space.Therefore,itmeasuresthepropensity ofthe speciestoselectamarginalenvironment (asopposed toaverageorcommonenvironment wherethemean position iscloseto0).Nichebreadthiscalculatedas thevariability(SD)oftheenvironment usedbyeach species along the main axes calculated from the

Table2 Environmental

VariablesDatasource

predictorsanddatasources

usedtomodelinvasive

plantspeciesnicheposition andbreadthinSpain

Landscape

Percentageofbuilt-upareasCORINELandCoverMapofSpain

Percentageofagriculturalareas

Percentageofforests

Percentageofscrubandherbaceousassociations

Percentageofopenspaces Percentageofwetlands Percentageofwaterbodies

Landcoverdiversity(Shannonindex)

(

Roadslength(m)OfficialserveroftheSpanishMinistry

Railwaylength(m)

Topography

(

Meanaltitude(m)DigitalElevationModel(DEM)

Altituderange(maximum-minimum;m) Meandistancetothecoastline(m) Climate

(

Meanannualtemperature(°C)DigitalClimaticAtlasofSpain

Temperaturerange(maxJuly–minJanuary;°C) Minimumwintertemperature(°C)

Annualrainfall(mm) Summerrainfall(mm)

Meanannualradiation(KJ/m2 daylm)

(

index.htm)

environmentalvariablesincludedintheOMI(Thuiller etal.2004).

Species’nichepropertiesasapredictorofrangesize

The nicheconceptstatesathree dimensionalrelation- shipbetweennicheposition,nichebreadthandspecies abundanceorrangesizeinanassemblage(Shugart andPatten1972).Wemodelledrangesize(i.e.number ofUTM where eachspecies ispresent,logtrans- formed) asafunctionofnichepositionandniche breadthonthetwomaingradients selectedbythe OMI.

Becausespeciesarelinkedbyphylogeny (Harvey andPagel1991),usingspeciesasindependentdata pointsmayinflatethedegreesoffreedom(Blomberg etal.2003;Felsenstein1985)andincreasetheType-I error.Wethusbuiltaphylogenetic treeforour74 species.Thetopologyofthesupertreewasconstructed withphylomatic ( phylomatic/phylomatic.html, Webb et al. 2008).

Branchlengthsweresetbyassigning anagetostem familynodesbasedonWikstro¨metal.(2001),and interpolatingtheremainingbranchlengthsoftheother nodesusingthebranchlengthadjustment (bladj) algorithminPhylocom(Webbetal.2008).

Totesthowspecies rangemightbeexplainedby nicheproperties andminimumresidencetime,we usedgeneralizedleastsquaresmodels (GLS) control- lingforthepotentialcorrelationbetween species associated withphylogenetichistory. Thevariance explainedbytheGLSmodel wasestimatedby extractedtheR2 valuefromtheregressionbetween observedspeciesrangeandpredictedonesfromthe GLSmodel.Weused theglsfunctionwithinpackage nlmeinR(RDevelopmentCoreTeam2012).

Speciestraitsexplainingspeciesnicheproperties

Werelatedspecies’nicheproperties (position and breadth) onthetwomainnicheaxestospeciestraits withthesameapproachthanabove;i.e.generalized

leastsquares model(GLS) controlledbyphylogeny. Tomeasuretheactualpowerofeachspeciestraitover nichepositionandnichebreadth, weusedamulti- modelinferenceapproach(BurnhamandAnderson

2002;LinkandBarker 2006)onselectingall-subsets oftheGLSusingtheAICc(Akaike information criterion,Akaike1974)measure. Theweightof evidence(wpi)ofeachspecies traitasapredictorof nicheposition andnichebreadth canbesimply estimatedasthesumofthemodelAICweights over allmodelsinwhichtheselectedpredictorappeared (BrookandBradshaw 2006;Carbonietal.2010; Thuilleretal.2007).Thepredictorwiththehighestwpi (theclosestto1)getsthehighest weightofevidence (i.e.hasthehighestrelativeimportance)toexplainthe response variable.Thisapproachbasedonasetof multiplemodels isfarmorerobustthaninferring variableimportance basedonasinglestepwise selectedmodel(BurnhamandAnderson2002;Link andBarker2006).Weusedthedredgefunctionwithin thepackage MuMIn inRtorunthisoverallanalysis.

Results

Nestednessinspeciesassemblages

Site-occurrencematrixtemperaturewas4.85°,which gavealevelofnestedness(N) of0.952.After comparingthisvaluewithabenchmarkof500random matrices,withanaveragedTof29.9°±0.24(i.e.a meannestednessof 0.70),we foundthattheprobabil- ityofarandomreplicatebeingequallyormorenested thanourstudymatrixwaslessthan0.0001.Therewas thusahighlevelofnestedness inthesite-occurrence matrix,indicatingthatthespeciespresentinsiteswith lowinvasiveplantrichness wereasubsetofspecies alsooccurringinrichersites.

Speciesnichesproperties

ThefirsttwoaxesoftheOMIsuccessfullyexplained

45and32%respectivelyofthe totalvariability when separatinginvasivespeciesniches(Fig. 1).Thefirst axis(anthropizationhereafter)summarisedagradient ofhumantransformation. Thisgradientopposed highlybuilt-upareasinflatlands (i.e.dense coverage ofroadsandrailways) tohighaltitudeareasfarfrom thecoastandwitharelativelylowurbanpressure.The

second axis(climate-landscapehereafter)opposed forested tocroplandareas.Forestedareaswere associated withcoldandhumidmountainranges withinrelativelydiverselandscapes, whilecroplands wereconcentratedinlowlands withwarmanddry climaticconditions. Speciesnichepositionsofinva- sivespecieswerewidelydistributed ontheenviron- mental ordinationdiagram(Fig.1), mostlyon the lowland areaswithahighdegreeofanthropization.

Thespecies withahigherlevelofspecialization (i.e.nichepositioninmarginalenvironmentsinthe studyareaandnarrownichebreadth)had,ingeneral,a nestednicheinside theniche ofmoregeneralist species(seeFig.2foranexample).

Speciesnichepropertiesasapredictorofrange size

Thegeneralized leastsquare model ofrange sizeasa function ofnichepositionand breadthwhile account- ingforphylogeneticrelationships explainedalmost half of the variation in range size (R2=0.43, p\0.0001)(Table3).Inthismodel,rangesizewas negativelyrelatedtopositionandbreadth onaxis1. Thespecieswithnichepositions closetotheaverage environmentalconditionsshowingsmalltomedium nichebreadth,suchasSorghumhalepense,Robinia pseudoacacia orAmaranthusretroflexus,werealso thespecieswiththe largestrangesize(Fig.3,Table 5 inAppendix).Thosespeciesdonotneedtohavea largenichebreadthtohavelargerangesizegiventhey occupythemostwidespreadenvironmental condi- tions. Specieswithrestricteddistributionrangeswere foundinhighlyhuman-disturbed placeswitharela- tivelywidetoleranceovertheanthropizationgradient (Fig.3).Incontrast, rangesizewaspositivelyrelated withnichebreadth onaxis2:largerangesizespecies were,onaverage, moretolerantofbroadclimateand landscapeconditionsrepresentedbyaxis2(Table3). Interestingly, minimum residence timehadnoinflu- enceonspeciesrangeinrespecttonicheproperties (Table3).

Speciestraitsexplainingspeciesnicheproperties

Modelsaccountingforbothnichepositionandbreadth onaxis1explainedslightlymorevariancethanmodels foraxis2ontheOMIordination(Table4).

Fig.1 Representationof

theexplicativevariablesand nichepositionof74invasive plantspeciesinSpaininthe firsttwoaxesoftheOMI ordinationanalysis.Thefirst axisdenotes agradient of anthropization.Thesecond axisis agradientofclimatic andlandscapegradientfrom mountainousforestedareas

RANGE.TEMP

AGRICULTUR

MEAN.TEMP

RADIATION

MIN.TEMP

tolowland croplands.See Table2foracomplete descriptionofvariables and Table5inAppendixfor species acronyms

DIST.COAST

SCRUB.HERB

OPEN.SPWACATEEWRE.BTOLADNIDS

ROAD.LENGT RAILWAY.LE

BUILD.UP

Axis1

MEAN.ALTIT

RANGE.ALTI

LAND.DIVER

FOREST

ANNUAL.RAI

SUMMER.RAI

Hel_curas

Zyg_fabag

Opu_dille

Bid_pilos

NOixca__gplaruecsS.col_bonar

Aca_cyano

Euc_camal Opu_ficus

Ipo_sagit

Dat_Aimnnao_xvirid

Chl_gayan

Sor_halepAga_aAmuesr_iAsumbau_lmuric

Sop_japon

Ela_angus

Gle_trAAiabcu_theop

IpLLoi_pi_nfdilifc

Gom_frutiEle_indic

Bid_aurea

Ara_sericArc_calen

Ama_bAlistot_squam

Con_bonCaoMrnPi_ar_ssuj__ampplaapstpa

Bid_CCsuabr_aelduli

Axis1

Ama_albusXan_strum

Bro_willd

Ach_Xfailinp_spino

Ail_altisIpo_purpu

Cot_coron

Dat_stram

Ama_hybri

Ama_retro

Con_canad

Ace_negun

Bid_frond

Lon_japon

Pas_dilat

Pas_vagin

Ste_secun

Hel_tuAbret_rverlo

Fal_balds

Ama_powel

Oen_glazi

Sebn__pinsaeeuqd

Tra_flumi

Cor_sello

Spa_paten

Oen_bienn

Aca_dealb

Euc_globu

Sen_mikan

Bud_david

Aca_melan

Bac_halim

Tro_majus

Rey_japon

a

bc

Axis1

d

e

Fig.2 Graphicalrepresentationofthenicheoffourinvasive plantspecieswith restricteddistributionranges:(b)Eucalyptus camaldulensis, range size=75 UTM 10km; (c) Opuntia dillenii17UTM;(d)Fallopia baldschuanica, 86UTMand (e)Acaciamelanoxylon,71UTMnestedinsidethenicheof (a)Conyza canadensis,505UTM,aspecieswithawide distributionrange.Thefirst axisdenotesagradientof anthropization.Thesecondaxisisagradientofclimaticand landscapegradientfrommountainousforestedareastolowland croplands.Nichepositionis the centreof eachspeciesellipsoid andnichebreathisthewidthoftheellipsoidasafunctionofthe maximaldeviationofsiteconditionsfromnicheposition

Table3 Phylogeneticgeneralized linear modelsaccounting forvariationinthedistribution rangesizeofinvasiveplant speciesinSpain,asafunction oftheirnicheposition and breadthonthemaintwoaxesoftheOMIordination and minimumresidencetime

(Table4). Perennial, N-fixingand clonal invasive speciesoccur generallymoreinhighly human- disturbedplacesclosetothecoast(Fig.4).

Nichebreadth overaxis1wasmainlyrelatedto pathway, N-fixing and longevity traits (Table4). Specieswithwidernichebreadth overthenaturalto human-disturbed gradientwerepredominantlyintro- ducedforgardeningandagriculturalpurposes,arenon N-fixingandbiennialspecies.Reversely,smallniche breadth species overaxis1werepredominantly speciesintroducedforsilviculture(Fig.4).

Nichepositionoveraxis2representing agradient fromforestedtocroplandareaswasmainlyrelatedto N-fixing speciesandlongevityintrinsictraitsand pathwayof introduction (Table4). Unintentionally introducedspecies,agriculturalweeds,andcropplants werethose presentinthewarmest,driest,agricultural areas.Speciesoccurring insuchhabitats wereperen- nial,nonN-fixingspecies(Fig.4).

Finally, speciesnichebreadth overaxis2was mainlyaffectedbylongevity, clonalgrowthand pathwayofintroduction(Table4).Short-lived clonal species(i.e.annualsandbiennials)introducedthrough agriculture(i.e.cropsandweeds) hadgenerallya widertolerancetodifferent climaticandlandscape conditionsthantheotherspecies(Fig.4).

Discussion

Nested patternandspeciesniches

Attheregionalscale,invasiveplantspeciesassem- blages in Spain are organized in nested subsets:

Value / SE / tvalue / pvaluespecieswithrestricteddistributionrangesoccurin
siteswithhighinvasiveplantrichness,whereassites
\0.0001withfewspeciesaregenerallypopulatedbywide-
\0.0001spreadinvaders.Oneofourinitialhypotheseswasthat
Intercept / 5.66 / 0.47 / 11.95
Axis1position / -0.60 / 0.11 / -5.68
Axis1breadth / -0.30 / 0.10 / -3.12 / \0.01 / such a nested pattern could reflect species niche
Axis2position / 0.03 / 0.09 / 0.32 / 0.75 / overlap.Hereweshowthatrangesizeisindeedrelated
Axis2breadth / 0.24 / 0.08 / 3.13 / \0.01 / tonichepositionandbreadthofinvaders,suggestinga
Residencetime / 0.00 / 0.00 / 1.02 / 0.31 / nicheoverlapamonginvasiveplantspecies.However,

Themodelexplainedalmosthalfofthevariationinrangesize

(R2=0.43,p\0.0001)

Ingeneral,species nicheposition overaxis1 representing agradientofanthropizationwasmainly conditionedbylongevity,N-fixingandclonalgrowth

there are several alternative explanations for this

nestedpattern.Nestedness mightbegeneratedby factorssuchaspassivesamplingeffect,patchareaand isolation,andhabitatdistribution(Wrightetal.1998), ormaysimply beanartefactofparticularspecies’ distributions (GastonandBlackburn2000).Inour database,therecouldbeapassivesamplingeffect

01234

NichepositiononOMIaxis1

234567

NichebreadthonOMIaxis1

0123456

NichebreadthonOMIaxis2

Fig.3 Relationships between range size of invasive plant speciesinSpainandnicheproperties.Onlythevariableshaving asignificanteffectonrangesizeareplotted(nichepositionon OMI axis 1,nichebreadthon OMI axes 1and2).Thefirstaxis denotesagradientofhuman-pressure.Thesecondaxisisa

gradientofclimaticandlandscape gradientfrommountainous forestedareastolowlandcroplands. Thestraightlinecorre- spondstotheestimatedresponse ofrangesizetoniche propertiesbytheGLSmodels

Table4Relativeimportanceofthenine selectedtraitsfor explaining invasiveplantspeciesnicheproperties overaxes1 and2oftheOMIordination

withthehighestcolonizationabilitywillbeableto reachthemostremotesites(Conroy etal.1999; Kadmon1995).Finally,thenestedpattern ofinvasive

reportedthatthefloraofurbanizedareasandtheir

R2 0.20 0.27 0.13 0.23

Thethreetraitswiththehighestrelativeimportanceoneach nicheproperty areshown inbold.Thelastrowshowsthe varianceexplainedbythemodels(allsignificant,p\0.0001)

becausethecartographicinformationoftheAtlasof

InvasivePlantSpeciesinSpain(Sanz-Elorzaetal.

2004)havebeengeneratedthrough5 yearsofwork compilingbibliographicandherbariumrecords.How- ever, weminimizedthiseffectbyanalysing onlythe cellswithatleastoneinvasivespeciesandbyselecting onlyspeciesrecorded atleastin10UTMcells. Although webasedtheanalysisinagridcellof constantsize(i.e.UTM10910km),habitatisola- tioncouldalso causenestednessbecause onlyspecies

aggregatedinhighlyanthropogenic areas,while widespreadspecieshavetheirnichepositionscloser totheaverageprevailingenvironmental conditions. Coastal areas in Spain have a mild climate and intensehumanpressures, concentratingtourism, tradingandtransport centresand,inturn,they accumulatemostofthefirst recordsofalienspecies (Gasso´etal.2009).

Thelackofassociation between rangesizeand nicheposition ontheclimate-landscapegradient(2nd OMIaxis)reinforcestheideathatinvasive speciesin Spainarenotparticularlyconstrainedbyenvironmen- talconditions.Nevertheless,rangesizewaspositively relatedtonichebreadth alongthisgradient, which impliesthatbroader niches inclimateandlandscape enable a species to become more widespread, as

Longevity

N-fixing

Clonality

AnnualBiennial Perennial

NoYes

NoYes

Pathway

N-fixing

Longevity

AGSUW

NoYes

AnnualBiennial Perennial

N-fixing

Longevity

Pathway

NoYes

Longevity

AnnualBiennial Perennial

Pathway

AGSUW

Clonality

AnnualBiennial Perennial

AGSUW

NoYes

Fig.4 PredictedmeannichevaluefromtheGLSmodelsfor invasiveplantspeciestraits.Onlythethreemostimportanttraits explainingnichepropertiesareplotted(byorderofimportance

fromlefttoright).SeeTable1fortraitcodeandTable4fortrait importance(boldnumbers)

suggestedbyotherstudies(Brown1995;Brownetal.

1995;Va´zquez2006).Interestingly, widespreadspe- ciesarenotnecessarilymoretoleranttoawiderange ofanthropogenic conditions thanrestrictedspecies, andtheirmeannichepositionsarelocatedinsiteswith moderatehuman-dominated landscapes.Thispro- vides evidence that the intermediate disturbance

hypothesisalso holds for invader species richness

(HobbsandHuenneke 1992;McKinney2002). Speciesnichesandtraits

An overview of the relationship between species niches and traits revealed that some intrinsic

(longevity,N-fixing capacity,clonalgrowth)and extrinsic(pathway)traitsarerelatedtonicheposition andnichebreadth.Nitrogen-fixingcapacityiscom- monlyrelatedtoinvasion successbecauseofthe competitiveadvantagethatitrepresentsinnitrogen poorsoils(PysˇekandRichardson2007;Thuiller et al.

2006).However,theabilitytofix Nisusuallyatthe costofbeingspecialisedtoNpoorsoils(Fitter1996). Thistrade-offexplainswhyN-fixing speciesmostly occurincoastal areas withhighhuman pressure, whereN-rich habitats(i.e. croplands)arescarcerthan inland, and exhibit relativelysmaller nichebreadthin comparisontononN-fixingspeciesthatcanoccur moreorlesseverywhere.

Short-livedinvasivespeciesoccurredinthemost widespreadenvironmental conditions andthey showedthehighest tolerancetoclimate-landscape variation.Short-livedspecieshavebeensuggested to bebetterinvadersthanlong-livedtypes(Cadotte and Lovett-Doust2001;Pysˇek etal.1995;Pysˇek and Richardson2007)duetotheiryearlyreproduction or theirsurvival asdormant seedsinadverseconditions (Crawley 1997).Inourdataset,clonalspeciesare indeedfoundinmanydifferenttypes ofecosystems (i.e.coastal,human-disturbed,hotanddryplaces)and havelargenichebreadthonthesecondenvironmental gradientsrevealedbytheOMI.

Extrinsictraitshaverecentlybeenconsidered as predictors ofinvasionsuccess(PysˇekandRichardson

2007;Thuilleretal.2006). Tooursurprise,the pathway ofintroduction,acomponent directlyasso- ciatedtohumanactivityisrelatedtonichepositionon theclimate-landscapegradientratherthantoniche

climate-landscapegradientthanthoseintroduced by othermeans.

Conclusions

Wedemonstrate herethatlinkingnichepositionand breadthwithnestednessofspeciesdistributionsand invaderrangesizecanbringinsightfullessons.Our analysis revealsthatattheregionalscaleinvasive specieswithrestricteddistributiondonothavespecific topo-climaticrequirements,butratheroccurinhuman disturbed areasalsoinvadedbygeneralistandwide- spreadinvasivespecies.Theinvaderswitharestricted distribution rangearelesstolerantofbroadclimate- landscapeconditionsthanwidespread invaders.With regardtowidespreadinvaders,thesearethespecies invadingtheaverageenvironmental conditionsin Spainbutnotclimaticallyextremesorheavilyhuman- disturbedsites.Thoseinvasionpatternsare,inturn, modulatedbywithspecific life-historytraitssuchas longevity,N-fixingcapabilityandclonalgrowth.

Acknowledgments WethankI.Bartomeus,B.Sa´nchez,D.Sol, M.Vall-lloseraandtwoanonymousrefereesforcommentson earlierversionsofthemanuscriptandC.Roquetfortheconstruction ofthephylogeny.Thisstudyhasbeenpartiallyfinanced bythe ALARM(GOCE-CT-2003-506675)andDAISIE(SSPI-CT-2003-

511202)projectswithinthe6thFrameworkProgramme ofthe EuropeanCommission;theMinisteriodeCienciaeInnovacio´n projectsRIXFUTUR(CGL2009-07515) andMONTES (CSD2008-00040). WTacknowledgessupportfromtheANR SCIONproject(ANR-08-PEXT-03).Thispapercontributestothe forthcoming VirtualLabonBiologicalInvasions withinthe LIFEWATCHframework.

positionontheanthropizationgradient.Speciesboth
introduced byagriculture(i.e.cropsandweeds)and unintentionallyaremostlyfoundinwarm,dryagri- culturalareas; andexhibitlargernichebreadthonthe
Table5 Listof74plantinvaderspeciesmodelled
FamilySpeciesSpecies acronym / Appendix1
SeeTable5.
Rangesize
(no.ofUTM) / Axis1 position / Axis1 breadth / Axis2 position / Axis2 breadth
Malvaceae / Abutilontheophrasti / Abu_theop / 111 / 0.76 / 2.56 / 0.73 / 2.58
Fabaceae / Acaciacyanophylla / Aca_cyano / 21 / 2.79 / 3.65 / 1.85 / 1.27
Fabaceae / Acaciadealbata / Aca_dealb / 210 / 1.50 / 2.63 / -1.85 / 1.61
Fabaceae / Acaciamelanoxylon / Aca_melan / 71 / 2.60 / 1.45 / -2.30 / 0.50
Table5continued
Family / Species / Species / Rangesize / Axis1 / Axis1 / Axis2 / Axis2
acronym / (no.ofUTM) / position / breadth / position / breadth
Aceraceae / Acernegundo / Ace_negun / 66 / 1.29 / 6.54 / -0.39 / 2.27
Asteraceae / Achilleafilipendulina / Ach_filip / 18 / -0.21 / 7.00 / -0.15 / 2.58
Agavaceae / Agaveamericana / Aga_ameri / 231 / 0.93 / 3.23 / 1.15 / 1.80
Simaroubaceae / Ailanthusaltissima / Ail_altis / 230 / 0.61 / 4.12 / -0.09 / 3.01
Amaranthaceae / Amaranthusalbus / Ama_albus / 467 / 0.14 / 3.43 / 0.02 / 2.50
Amaranthaceae / Amaranthusblitoides / Ama_blito / 483 / 0.55 / 2.91 / 0.34 / 2.51
Amaranthaceae / Amaranthushybridus / Ama_hybri / 402 / 0.49 / 3.53 / -0.46 / 4.24
Amaranthaceae / Amaranthusmuricatus / Ama_muric / 207 / 1.49 / 3.06 / 1.14 / 1.84
Amaranthaceae / Amaranthuspowellii / Ama_powel / 90 / 0.19 / 4.16 / -1.16 / 5.56
Amaranthaceae / A.retroflexus / Ama_retro / 608 / 0.08 / 3.19 / -0.59 / 4.20
Amaranthaceae / Amaranthusviridis / Ama_virid / 116 / 1.58 / 3.41 / 1.27 / 1.76
Asclepiadaceae / Araujiasericifera / Ara_seric / 93 / 2.15 / 2.99 / 0.39 / 1.67
Asteraceae / Arctothecacalendula / Arc_calen / 24 / 3.26 / 2.65 / 0.41 / 6.15
Asteraceae / Artemisiaverlotiorum / Art_verlo / 167 / 1.11 / 4.02 / -0.87 / 4.24
Asteraceae / Astersquamatus / Ast_squam / 350 / 0.92 / 2.87 / 0.29 / 2.60
Cactaceae / Austrocylindropuntiasubulata / Aus_subul / 51 / 1.22 / 1.59 / 1.12 / 1.31
Asteraceae / Baccharishalimifolia / Bac_halim / 14 / 3.98 / 1.73 / -2.32 / 0.32
Asteraceae / Bidens aurea / Bid_aurea / 75 / 1.33 / 5.50 / 0.46 / 2.89
Asteraceae / Bidens frondosa / Bid_frond / 89 / 1.13 / 2.90 / -0.72 / 4.04
Asteraceae / Bidens pilosa / Bid_pilos / 25 / 1.97 / 2.89 / 1.75 / 0.93
Asteraceae / Bidens subalternans / Bid_subal / 134 / 1.79 / 2.60 / 0.22 / 1.82
Poaceae / Bromuswilldenowii / Bro_willd / 155 / 1.42 / 4.94 / -0.01 / 4.90
Buddlejaceae / Buddlejadavidii / Bud_david / 102 / 1.04 / 5.09 / -2.31 / 3.98
Aizoaceae / Carpobrotusedulis / Car_eduli / 105 / 1.98 / 3.46 / 0.27 / 2.64
Poaceae / Chlorisgayana / Chl_gayan / 24 / 2.59 / 2.84 / 1.45 / 0.75
Asteraceae / Conyzabonariensis / Con_bonar / 389 / 0.66 / 3.44 / 0.22 / 2.79
Asteraceae / Conyzacanadensis / Con_canad / 505 / 0.15 / 3.60 / -0.75 / 4.04
Asteraceae / Conyzasumatrensis / Con_sumat / 289 / 1.08 / 3.00 / 0.17 / 2.58
Poaceae / Cortaderia selloana / Cor_sello / 62 / 3.06 / 4.42 / -1.37 / 2.45
Asteraceae / Cotulacoronopifolia / Cot_coron / 43 / 2.81 / 2.92 / -0.26 / 5.93
Solanaceae / Daturainnoxia / Dat_innox / 71 / 1.41 / 3.19 / 1.25 / 1.63
Solanaceae / Daturastramonium / Dat_stram / 421 / 0.35 / 3.89 / -0.34 / 4.57
Elaeagnaceae / Elaeagnusangustifolia / Ela_angus / 63 / 0.46 / 5.45 / 0.82 / 1.35
Poaceae / Eleusineindica / Ele_indic / 43 / 2.50 / 4.25 / 0.66 / 3.60
Myrtaceae / Eucalyptuscamaldulensis / Euc_camal / 75 / 0.05 / 1.85 / 1.32 / 1.60
Myrtaceae / Eucalyptusglobulus / Euc_globu / 209 / 2.12 / 2.60 / -2.03 / 1.42
Polygonaceae / Fallopiabaldschuanica / Fal_balds / 86 / -0.76 / 2.47 / -1.23 / 3.31
Caesalpiniaceae / Gleditsiatriacanthos / Gle_triac / 54 / 0.42 / 4.53 / 0.76 / 1.05
Asclepiadaceae / Gomphocarpusfruticosus / Gom_fruti / 55 / 1.96 / 2.00 / 0.63 / 2.75
Boraginaceae / Heliotropiumcurassavicum / Hel_curas / 42 / 2.84 / 2.61 / 2.21 / 0.50
Asteraceae / Helianthustuberosus / Hel_tuber / 184 / 0.82 / 4.26 / -0.92 / 4.55
Convolvulaceae / Ipomoeaindica / Ipo_indic / 150 / 1.71 / 3.17 / 0.86 / 1.44
Convolvulaceae / Ipomoeapurpurea / Ipo_purpu / 129 / 1.01 / 4.45 / -0.08 / 3.53
Convolvulaceae / Ipomoeasagittata / Ipo_sagit / 38 / 1.84 / 2.14 / 1.48 / 0.87
Table5continued
Family / Species / Species / Rangesize / Axis1 / Axis1 / Axis2 / Axis2
acronym / (no.ofUTM) / position / breadth / position / breadth
Verbenaceae / Lippiafiliformis / Lip_filif / 50 / 1.76 / 3.89 / 0.86 / 3.60
Caprifoliaceae / Lonicerajaponica / Lon_japon / 78 / 2.09 / 5.02 / -0.38 / 3.55
Nyctaginaceae / Mirabilisjalapa / Mir_jalap / 242 / 1.12 / 3.32 / 0.18 / 2.36
Solanaceae / Nicotianaglauca / Nic_glauc / 127 / 1.72 / 2.50 / 1.64 / 1.30
Onagraceae / Oenotherabiennis / Oen_bienn / 112 / 0.80 / 4.87 / -1.67 / 4.04
Onagraceae / Oenotheraglazioviana / Oen_glazi / 54 / 1.04 / 4.19 / -1.26 / 2.52
Cactaceae / Opuntiadillenii / Opu_dille / 17 / 1.81 / 1.88 / 1.81 / 0.60
Cactaceae / Opuntiaficus-indica / Opu_ficus / 434 / 0.66 / 2.15 / 1.32 / 2.42
Oxalidaceae / Oxalispes-caprae / Oxa_pes.c / 213 / 1.78 / 2.55 / 1.67 / 1.36
Poaceae / Paspalumdilatatum / Pas_dilat / 190 / 2.14 / 2.89 / -0.77 / 3.67
Poaceae / Paspalumpaspalodes / Pas_paspa / 231 / 1.22 / 3.49 / 0.18 / 2.77
Poaceae / Paspalumvaginatum / Pas_vagin / 40 / 2.97 / 3.91 / -0.32 / 5.24
Polygonaceae / Reynoutriajaponica / Rey_japon / 14 / 2.71 / 4.00 / -3.46 / 2.14
Fabaceae / R.pseudoacacia / Rob_pseud / 594 / 0.94 / 3.79 / -1.33 / 3.97
Asteraceae / Senecioinaequidens / Sen_inaeq / 14 / 0.95 / 5.20 / -1.37 / 1.99
Asteraceae / Seneciomikanioides / Sen_mikan / 20 / 3.19 / 3.29 / -1.73 / 1.11
Solanaceae / Solanumbonariense / Sol_bonar / 48 / 2.21 / 3.97 / 1.66 / 2.00
Fabaceae / Sophorajaponica / Sop_japon / 11 / -0.51 / 4.35 / 0.60 / 1.43
Poaceae / S.halepense / Sor_halep / 743 / 0.46 / 2.47 / 1.19 / 2.63
Poaceae / Spartinapatens / Spa_paten / 32 / 2.91 / 1.29 / -1.41 / 3.97
Poaceae / Stenotaphrumsecundatum / Ste_secun / 28 / 3.51 / 2.32 / -0.59 / 4.23
Commelinaceae / Tradescantiafluminensis / Tra_flumi / 19 / 2.78 / 5.90 / -1.21 / 4.39
Tropaeolaceae / Tropaeolummajus / Tro_majus / 9 / 2.58 / 3.44 / -3.35 / 0.12
Asteraceae / Xanthiumspinosum / Xan_spino / 411 / 0.02 / 3.66 / -0.09 / 3.28
Asteraceae / Xanthiumstrumarium / Xan_strum / 275 / 0.72 / 3.76 / 0.01 / 3.25
Zygophyllaceae / Zygophyllumfabago / Zyg_fabag / 64 / 1.12 / 2.55 / 1.83 / 1.29

DistributionrangesizewasmeasuredasthenumberofUTM10910kmwherethespecieswasobserved,andnichepositionand breadthwereextractedfromthe2mainaxesoftheOMIordination

Appendix2

SeeTable6.

Table6 Extrinsicandintrinsicspeciestraitsfor74plantinvaderspeciesinSpain

Seed size / Longevity / Clonality / Dispersal / Pollination / N-fixing / Llifeform / Pathway / Origin / Origin code
Abutilontheophrasti / 3 / 1 / 0 / Animal / Animal / 0 / Therophyte / Agriculture / Europe / E
Acaciacyanophylla / 4 / 3 / 1 / Animal / Animal / 1 / Phanerophyte / Gardening / Oceania / O
Acaciadealbata / 3 / 3 / 0 / Animal / Animal / 1 / Phanerophyte / Gardening / Oceania / O
Acaciamelanoxylon / 3 / 3 / 1 / Animal / Animal / 1 / Phanerophyte / Silviculture / Oceania / O
Acernegundo / 5 / 3 / 0 / Wind / Wind / 0 / Phanerophyte / Gardening / NAmerica / NM
Achilleafilipendulina / 2 / 3 / 1 / Wind / Animal / 0 / Geocryptophyte / Gardening / Europe / E
Agaveamericana / 3 / 3 / 1 / Animal / Animal / 0 / Chamaephyte / Gardening / NAmerica / NM
Ailanthusaltissima / 5 / 3 / 1 / Wind / Animal / 0 / Phanerophyte / Gardening / Asia / A
Amaranthusalbus / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / NAmerica / NM
Amaranthusblitoides / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / NAmerica / NM
Amaranthushybridus / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / America / AM
Amaranthusmuricatus / 2 / 3 / 0 / Wind / Wind / 0 / Hemicryptophyte / Unintentionally / SAmerica / SM
Amaranthuspowellii / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / NAmerica / NM
A.retroflexus / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / NAmerica / NM
Amaranthusviridis / 2 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / Africa / A
Araujiasericifera / 4 / 3 / 1 / Wind / Animal / 1 / Vine / Gardening / SAmerica / SM
Arctothecacalendula / 3 / 1 / 1 / Wind / Animal / 0 / Therophyte / Unintentionally / Africa / AF
Artemisiaverlotiorum / 1 / 3 / 1 / Wind / Wind / 0 / Geocryptophyte / Unintentionally / Asia / A
Astersquamatus / 2 / 2 / 0 / Wind / Animal / 0 / Therophyte / Unintentionally / America / AM
Austrocylindropuntiasubulata / 3 / 3 / 1 / Animal / Animal / 0 / Phanerophyte / Gardening / SAmerica / SM
Baccharishalimifolia / 1 / 3 / 1 / Wind / Wind / 0 / Phanerophyte / Gardening / NAmerica / NM
Bidens aurea / 2 / 3 / 1 / Animal / Animal / 0 / Hemicryptophyte / Unintentionally / America / AM
Bidens frondosa / 4 / 1 / 0 / Animal / Animal / 0 / Therophyte / Unintentionally / NAmerica / NM
Bidens pilosa / 2 / 1 / 0 / Animal / Animal / 0 / Therophyte / Unintentionally / America / AM
Bidens subalternans / 2 / 1 / 0 / Animal / Animal / 0 / Therophyte / Unintentionally / America / AM
Bromuswilldenowii / 3 / 2 / 0 / Animal / Wind / 0 / Hemicryptophyte / Weed / SAmerica / SM
Buddlejadavidii / 1 / 3 / 1 / Wind / Animal / 0 / Phanerophyte / Gardening / Asia / A
Carpobrotusedulis / 2 / 3 / 1 / Animal / Animal / 0 / Chamaephyte / Gardening / Africa / AF
Chlorisgayana / 3 / 3 / 1 / Wind / Wind / 0 / Hemicryptophyte / Gardening / Africa / AF
Conyzabonariensis / 2 / 1 / 0 / Wind / Animal / 0 / Therophyte / Unintentionally / America / AM
Conyzacanadensis / 1 / 1 / 0 / Wind / Animal / 0 / Therophyte / Unintentionally / NAmerica / NM
Table6continued
Seed size / Longevity / Clonality / Dispersal / Pollination / N-fixing / Llifeform / Pathway / Origin / Origin code
Conyzasumatrensis / 2 / 1 / 0 / Wind / Animal / 0 / Therophyte / Unintentionally / SAmerica / SM
Cortaderia selloana / 3 / 3 / 0 / Wind / Wind / 0 / Chamaephyte / Gardening / SAmerica / SM
Cotulacoronopifolia / 2 / 1 / 0 / Wind / Animal / 0 / Therophyte / Weed / Africa / AF
Daturainnoxia / 3 / 1 / 0 / Animal / Animal / 0 / Therophyte / Unintentionally / SAmerica / SM
Daturastramonium / 3 / 1 / 0 / Animal / Animal / 0 / Therophyte / Unintentionally / America / AM
Elaeagnusangustifolia / 3 / 3 / 1 / Animal / Animal / 0 / Phanerophyte / Gardening / Africa / AF
Eleusineindica / 3 / 1 / 0 / Wind / Wind / 0 / Therophyte / Weed / Asia / A
Eucalyptuscamaldulensis / 2 / 3 / 0 / Wind / Animal / 0 / Phanerophyte / Silviculture / Oceania / O
Eucalyptusglobulus / 3 / 3 / 0 / Wind / Animal / 0 / Phanerophyte / Silviculture / Oceania / O
Fallopiabaldschuanica / 1 / 3 / 1 / Animal / Animal / 0 / Vine / Gardening / EAsia / A
Gleditsiatriacanthos / 4 / 3 / 1 / Animal / Wind / 1 / Phanerophyte / Gardening / NAmerica / NM
Gomphocarpusfruticosus / 4 / 3 / 0 / Wind / Animal / 1 / Phanerophyte / Gardening / Africa / AF
Heliotropiumcurassavicum / 3 / 3 / 1 / Wind / Animal / 0 / Geocryptophyte / Unintentionally / America / AM
Helianthustuberosus / 4 / 3 / 1 / Animal / Animal / 0 / Geocryptophyte / Agriculture / NAmerica / NM
Ipomoeaindica / 3 / 3 / 1 / Animal / Animal / 0 / Vine / Gardening / America / AM
Ipomoeapurpurea / 4 / 1 / 1 / Animal / Animal / 0 / Vine / Gardening / America / AM
Ipomoeasagittata / 4 / 3 / 1 / Animal / Animal / 0 / Vine / Unintentionally / America / AM
Lippiafiliformis / 1 / 3 / 1 / Water / Animal / 0 / Chamaephyte / Gardening / SAmerica / SM
Lonicerajaponica / 3 / 3 / 1 / Animal / Animal / 0 / Vine / Gardening / Asia / A
Mirabilisjalapa / 4 / 3 / 0 / Wind / Animal / 0 / Hemicryptophyte / Gardening / America / AM
Nicotianaglauca / 5 / 3 / 1 / Wind / Animal / 0 / Phanerophyte / Gardening / SAmerica / SM
Oenotherabiennis / 2 / 2 / 0 / Animal / Animal / 0 / Hemicryptophyte / Gardening / NAmerica / NM
Oenotheraglazioviana / 2 / 2 / 0 / Animal / Animal / 0 / Hemicryptophyte / Gardening / Europe / E
Opuntiadillenii / 3 / 3 / 1 / Animal / Animal / 0 / Phanerophyte / Gardening / America / AM
Opuntiaficus-indica / 3 / 3 / 1 / Animal / Animal / 0 / Phanerophyte / Gardening / America / AM
Oxalispes-caprae / 1 / 3 / 1 / Animal / Animal / 0 / Geocryptophyte / Weed / Africa / AF
Paspalumdilatatum / 2 / 3 / 1 / Wind / Wind / 0 / Hemicryptophyte / Weed / America / AM
Paspalumpaspalodes / 2 / 3 / 1 / Animal / Wind / 0 / Hemicryptophyte / Unintentionally / America / AM
Paspalumvaginatum / 2 / 3 / 1 / Animal / Wind / 0 / Hemicryptophyte / Unintentionally / America / AM
Reynoutriajaponica / 3 / 3 / 1 / Animal / Animal / 0 / Geocryptophyte / Gardening / Asia / A
R.pseudoacacia / 3 / 3 / 1 / Animal / Animal / 1 / Phanerophyte / Gardening / NAmerica / NM