Differential influence of four invasive plant species on soil physicochemical properties in a pot experiment

JSoilsSediments(2018)18:1409–1423 https://doi.org/10.1007/s11368-017-1873-3

SOILS,SEC1•SOILORGANICMATTERDYNAMICSANDNUTRIENTCYCLING•RESEARCHARTICLE

Differentialinfluenceoffourinvasiveplantspeciesonsoilphy sicochemicalpropertiesinapotexperiment

AnnaM . S tefanowicz^1&M artaL . M ajewska^2&M ałgorzataStanek^1&M arcinNobis^2&

SzymonZubek²

Received:27July2017/Accepted:8November2017/Publishedonline:16November2017

#TheAuthor(s)2017.Thisarticleisanopenaccesspublication

Abstract

PurposeTh isstudycomparedtheeffectsoffourinvasivepla nts,namelyImpatiensglandulifera,Reynoutriajaponica,Rud beckialaciniata,andSolidagogigantea,aswellastwonatives p e c ies—

Artemisiav u l g a ris,P h alarisa r u n d inacea,andtheirmixtur eonsoilphysicochemicalpropertiesinapotexperiment.

MaterialsandmethodsP l ant s wereplantedinpotsintwo loamysandsoils.Thesoilswerecollectedfromfallowslocat- edoutside(fallowsoil)andwithinrivervalley(valleysoil)und ernativeplantcommunities.Abovegroundplantbiomass,cove r,andsoilphysicochemicalpropertiessuchasnutrientconcent rations,pH,andwaterholdingcapacity(WHC)weremeasureda ftertwogrowingseasons.Discriminantanalysis(DA)wasuse dtoidentifysoilvariablesresponsibleforthediscriminationbe tweenplanttreatments.Identifiedvariableswerefurthercomp aredbetweentreatmentsusingone-

wayANOVAfollowedbyTukey’sHSDtest.

ResultsanddiscussionPlantbiomass,cover,andsoilparam- etersdependedonspeciesandsoiltype.DAeffectivelysepa- ratedsoilsunderdifferentplantspecies.DAonfallowsoildat aseparatedR.laciniatafromallothertreatments,

Responsibleeditor:ZucongCai

ElectronicsupplementarymaterialTheonlineversionofthisarticle(http s://doi.org/10.1007/s11368-017-1873-

3)containssupplementarymaterial,whichisavailabletoauthorizedusers .

*AnnaM.Stefanowicza.st efanowicz@botany.pl

1 W.SzaferInstituteofBotany,PolishAcademyofSciences,Lubicz46, 31–512Kraków,Poland

2 InstituteofBotany,FacultyofBiologyandEarthSciences,Jagiell onianUniversity,Kopernika27,31–501Kraków,Poland

especiallyI.glandulifera,nativespeciesandbaresoil,alongaxis 1(relatedmainlytoexchangeableK,N-NH4,totalP,N-

NO3,andWHC).Largedifferenceswerefoundbetween R.laciniataandS.giganteaasindicatedbyaxis2(S-SO4, exchangeableMg,totalP,exchangeableCa,andtotalMg).DA onvalleysoildataseparatedR.japonicafromallothertreatment s,particularlyS.gigantea,R.laciniata,andnativemixture,alon gaxis1(N-NO3,totalN,S-SO4,totalP,pH).Alongaxis2 (N- NO3,N-

NH4,OlsenP,exchangeableK,WHC),l argedifferencesw ereobservedbetwee n

I.glanduliferaandallotherinvaders.

ConclusionsPlantinfluenceonsoildifferedbothamongin- vasivespeciesandbetweeninvasiveandnativespecies.Impati ensglanduliferahadarelativelyweakeffectanditssoilwassimi lartobothnativeandbaresoils.Multidirectionaleffects ofdifferentinvadersresultedinaconsiderablediver-

genceinsoilcharacteristics.Invasion-

drivenchangesinthesoilenvironmentmaytriggerfeedbacksth atstabilizeoraccel-erateinvasionandhinderre-

colonizationbynativevegetation,whichhasimplicationsforth erestorationofinvadedhabitats.

KeywordsI mpatiensglandulifera.Plantinvasion.Reyno utriajaponica.Rudbeckialaciniata.Soilnutrientconcentr ations.Solidagogigantea

1 Introduction

Biologicalinvasionsareanimportanthuman-inducedprob- lemataglobalscalealongwithanincreaseinatmosphericCO2, pollution,andland-usechange.Invaderscanreducebi- ologicaldiversityandpromoteextinctions,actasavectorofdise ases,andgenerateeconomiclosses.Therateofinvasionisexpect

2 JSoilsSediments(2018)18:1409–1423

edtoincreaseincomingdecades,forexample,duetotheexpan sionofglobaltrade(Liaoetal.2008).Invasive

plantschangetheabundance,diversity,andstructureofplantan danimalcommunities(Hejdaetal.2009;Lendaetal.2013),and oftenconsiderablymodifyphysicochemicalandbiologicalpr opertiesofthesoilenvironment,therebypoten-

tiallyaffectingkeyecosystemprocesses(Vilàetal.2011;Cas tro-

Díezetal.2014;Majewskaetal.2015;Stefanowiczetal.2016;Z ubeketal.2016;Broadbentetal.2017;Castro-

DíezandAlonso2017;Lavoie2017;Rodríguez- Caballeroetal.2017).

Studiesbasedonmeta-analysisindicatedthatplantinva- sionsgenerallyincreasenutrient(C,N,P)poolsandalsoen- hancetherateofsoilprocessessuchaslitterdecompositionand mineralization,possiblyacceleratingnutrientcycling(Liaoet al.2008;Vilàetal.2011;Castro-

Díezetal.2014).Thisisbecauseinvasivespecieshavesignifica ntlyhigher,incomparisontonon-

invasiveones,valuesofperformance- relatedtraitssuchasphysiology,leaf-

areaallocation,shootallocation,growthrate,sizeandfitnes s,whicharedrivingfactorsinregulatingCandNcycles(Liao etal.2008;VanKleunenetal.2010).However,therearealsowor ksindicatingthattheeffectsofinvasiononsoilqualityandproce ssesarenotconsistentanddependoninvasiveplantspecies,reci pientsoil,lengthofinvasionhistory,season,precipitation,andt heinteractionsofthesefactors(Dassonvilleet al.2008;Li aoetal.2008;Tharayiletal.2013;Stefanowiczetal.2016).

Changesinthesoilpropertiesbroughtaboutbyplantinvasionare problematicastheymayleadtopositivefeedbacksthatstabiliz eoraccelerateinvasion.Thechangesmaypersistaftertheremov alofaninvasiveplantandlimitrecolonizationbynativeplantco mmunities.Thisphenomenon,knownasinva-

siveplantlegacy,hasimplicationsforrestorationofinvadedsite s(CorbinandD’Antonio2012;Broadbentetal.2017).

Impatiensglandulifera,Reynoutriajaponica,Rudbeckia laciniata,andSolidagogiganteaareamongthemostfrequentan daggressiveinvasivealienplantsinnatural,extensivelyman aged,andman-madehabitatsincentralEurope(Tokarska- Guziketal.2010;Zelnik2012).Allthesespeciesareconsideredt ransformersthatchangeBthecharacter,condi-

tion,formornatureofecosystemsoverasubstantialarea^dueto,f orexample,excessiveorlimiteduseofresources,promo- tionoferosionorstabilizationofsoil,oraccumulationoflitter(Ri chardsonetal.2000;Tokarska-

Guziketal.2010).However,somedataindicatedthattheinflue nceofinvasiononecosystemsmayconsiderablyvaryamongtra nsformerin-

vasivespecies.Forexample,I.glanduliferainvasionhadamar ginaleffectonvegetationandsoilproperties,whichmakesthissp eciesdifferentfromothermajorinvasivealiensincen-

tralEuropesuchasReynoutriaspp.orHeracleummantega zzianum(HejdaandPyšek2006;Hejdaetal.2009;Čudaetal.20 17).Asplantsaffectsoilmainlythroughtherootsystem(rootexu dates,nutrientuptake)andlitterdeposition,thedistincteffectof

I.glanduliferaonsoilinrelationtootherinvadersmayresultfromi tsannuallifeform,shallower

rootingdepth,and/orhighertissuequality(BeerlingandPerri ns1993;Westonetal.2005;Dassonvilleetal.2008;Scha rfyetal.2011).Similarly,speciesbelongingtovariousfunctio nalgroupsmayaffectecosystemsdifferentlyduetothefactthat theydifferfromeachotherinmanytraitsrelatedto,forexample ,biomassquantityandquality(Scharfyetal.2011).

Mostpreviousst udiesontheeffectsofI.glandulifera, R.japonica,and/orS.giganteaincludedonlyasingleinvasives pecies,asingleorfewstudysitesandtheresultsobtainedwere inconsistent,indicatingincreases,decreases,ornochangein soilpropertiesunderaparticularinvaderincompar-

isontouninvadedsoil(Chapuis-

Lardyetal.2006;Vanderhoevenetal.2006;Dassonvilleeta l.2007;Scharfyetal.2009;Aguileraetal.2010;Tharayiletal.

2013;Minchevaetal.2014;Quistetal.2014;Rucklietal.2014 b;Stefanowiczetal.2017).Toourknowledge,informationont heeffectofR.laciniataonsoilphysicochemicalpropertiesissca rce(Stefanowiczetal.2017).Moreover,overwhelmingma jorityofstudieswasconductedinthefield,makingpairwisec omparisonsofsoilsunderpatchesofinvasivespe-

cieswiththoseunderneighboringnativevegetation(Chapuis- Lardyetal.2006;Vanderhoevenetal.2006;Dassonvilleetal.2 007;Aguileraetal.2010;Tharayiletal.2013;Minchevaetal.

2014;Quistetal.2014;Rucklietal.2014b;Stefanowiczeta l.2017).Althoughsuchspace-for-timesub-

stitutionapproachprovidesavaluablewealthofinformation,it suffersfromdrawbackssuchasthepossibilitythatpotentialdif ferencesbetweeninvadedandnativestandsexistedpriortothei nvasion.Takingintoaccountthelimitationsoffieldstud- ies,itisadvantageoustocomplementresearchwithexperi- mentsthatincludeplantcultivationinstandardizedsoil.Insu chexperiments,soilparameterscanbedirectlycomparednot onlybetweeninvasiveandnativespecies,butalsobe- tweendifferentinvaders.Suchacomparisoncanbeproblem- aticinthefieldasnear-monoculturepatchesofvariousin- vadersrarelygrowclosetoeachother.Short-termpotexper- imentsbasedonplantcultivationdonotideallymimicthefi eldsituationduetotheirshortduration,lowerplantbiomassand litterdeposition,and/orrestrictedrootingdepth.However,the ycansimulateaprimarystageofaninvasion—theen- croachmentofalienplantsontodisturbed(plantbiomassre- moval,sieving,mixing)soil,temporarilydevoidofveget ation.

Todate,onlyfewexperimentalstudieshavetestedtheim- pactofI.glandulifera,R.japonica,R.laciniata,orS.giganteaons oil(Scharfyetal.2010,2011;Bardonetal.2014,2016).Scharfy etal.(2010)performedamesocosmexperimentsim-

ulatingtheinvasionofasinglespecies—

S.giganteaintothreewetlandplantcommunitiesandfoundnoi nvasioneffectonNandPavailabilityinsoil.Inanotherexperim ent,sixinvasiveforbs,includingI.glandulifera,R.japonica,an dS.gigantea,werecomparedwiththegroupsofnativeforb sand

JSoilsSediments(2018)18:1409–1423 1411

graminoidsinrespectoftheireffectsonsoilproperties,sug- gestingnosignificantdifferencesinsolublephenolics,nitrate,a mmonium,orphosphateconcentrationsbetweenthespeciesgr oups(Scharfyetal.2011).Otherexperimentsprovedthatextrac tsfromtherootsandrhizomesofR.japonicainhibitdenitrifica tion(Bardonetal.2014,2016).Comparisonoftheeffectsofthea bove-

mentionedinvadersonthepropertiesofstandardizedsoilwould contributetoourknowledgeontheinvasionimpactonecosyste ms.

Theaimofthisstudywastocomparetheeffectofthe growthoffourplantspeciesthatareinvasiveinEurope,name- lyImpatiensglandulifera,Reynoutriajaponica,Rudbeckia laciniata,andSolidagogigantea,aswellastwonativespe-cies

—

Artemisiavulgaris,P h alarisa rundinacea,andt h eirmixtureo nphysicochemicalpropertiessuchastotalandavail-

ablenutrientconcentrations,waterholdingcapacity,andpHoft wosoilsinapotexperiment.Wehypothesizedthatsoilproperti eswoulddifferbothamonginvadersaswellasbe-

tweeninvasiveandnativespecies.Theweakesteffectonsoilwas expectedinthecaseofI.glandulifera.Moreover,theinflu enceofthetwonativespecies—A.vulgarisand

P.arundinacea—

onsoilwoulddifferfromeachotherasthesespeciesbelongtodist inctfunctionalgroups—

graminoidsandforbs.Finally,planteffectonsoilwoulddepend onsoiltype.

2 Materialsandmethods

2.1 Plantspecies

FourspeciesthataresuccessfulinvadersinEuropewereusedint heexperiment,namelyImpatiensglanduliferaRoyle[=Impat iensroyleiWalpers]

(Balsaminaceae),ReynoutriajaponicaHoutt.

[= Fallopiaj aponica( Houtt.)RonseD ecr.,

=PolygonumcuspidatumSieb.&Zucc.]

(Polygonaceae),RudbeckialaciniataL.

(Asteraceae),andSolidagogiganteaAiton[=S.serotinaAito n]

(Asteraceae).Impatiensglanduliferaiswidespreadinmany partsofEuropeandNorthAmerica.ItwasfirstintroducedtoE uropefromtheHimalayasinthefirsthalfofthenineteenthcen tury(1839)andusedasanornamentalandnectar-

producingplant.ItisthetallestannualspeciesinEurope,reachi ngupto2.5m (BeerlingandPerrins1993;PyšekandPrach1 995).Reynoutriajaponicaisaperennialrhizomatousforbnat ivetoJapan,Korea,Taiwan,andnorthernChina,beingapioneer speciesonvolcanicslopes.ItwasintroducedinEuropein182 5andinNorthAmericaabout1870forornamentalpur-

pose(Barney2006;Barneyetal.2006).Reynoutriajaponicaprod uceshugeamountsofbiomass;itsbamboo-

likestemscanbeupto5mhigh,rhizomescanextendmorethan2 mindepth,15–

20minlength,andevenburrowthroughasphalt(Barney2006;W estonetal.2005).

6 JSoilsSediments(2018)18:1409–1423

RudbeckialaciniataandS.giganteaarebothtall(upto3m)rh izomatousperennialforbsnativetoNorthAmericathatwereintr oducedinEuropeasornamentalsatthebeginningofthe17thandi nthemiddleofeighteenthcentury(1758),respec-

tively.TheyarealsoproblematicinvasivespeciesinAsia(

Weber1998;Akasakaetal.2015;CABI2017).Impatiensgla ndulifera,R.japonica,R.laciniata,andS.giganteainvadearang eofhabitatssuchasriparianzonesaroundstandingwa-

tersorstreams,floodplainwoods,forestclearings,swamps,w astelands,grasslands,cultivatedfieldmargins,fallows,road- sides,and/orareasalongrailroadtracks(Zelnik2012).

TwocommonrhizomatousperennialsnativeinEuro pe,belongingtodifferentfamiliesandfunctionalgroups

—theforbArtemisiavulgarisL.

(Asteraceae)andthegrassPhalarisa rundinaceaL . ( Poaceae)w erealsos electedf ortheexperiment.Bothplants aretallandreach0.5–

2.5minheight.ArtemisiavulgarisandP.arundinaceaarecons ideredinvadersinNorthAmerica,infestingroadsides,wastea reas,agronomicsettings,and/orwetlands(Westonetal.2005;

Jacintheetal.2010).

2.2 Experimentalsetupandsampling

SoilsfortheexperimentwerecollectedinApril2014fromfall owslocatedwithinrivervalley(theSkawariverinZator,49^°59′5 9″N,19^°26′40.5″E,265ma.s.l.;hereafterreferredtoasvalleysoi l)andoutsidevalley(Kraków,49^°59′49.5″N,19^°52′13.6″E,260 ma.s.l.;hereafterreferredtoasfallowsoil)insouthernPolandund ernativeplantcommunities(Artemisieteavulgaris).Thisarealie sinthetransitionalclimatezonebetweenatemperateoceaniccli mateinthewestandatemperateconti-

nentalclimateintheeast.Meanannualtemperaturefluctuatesb etween7 and9 °Candprecipitationbetween700and900mm.

Thevegetationseason(dayswithanaveragetemper-

ature>5°C)spansaperiodbetween210and230days.Ateachsit e,soilwastakenfromoneplot(approx.4m²)toadepthofapprox.

30cm.Thefollowingplantspecieswererecordedattheplots:A chilleamillefolium,Equisetumarvense,Lysimachiavulgaris ,P.arundinacea,Poapratensis,Rubuscaesius,Tanacetumvu lgare(Zator)andCalamagrostisepigejos,Cirsiumarvense,H ypericumperforatum,Lathyruspratensis,Lysimachiavulga ris,Lythrumsalicaria,Phragmitescommunis,Rubuscaesi us,Sanguisorbaofficinalis,Selinumcarvifolia,Tanacetumvu lgare(Kraków).Collectedsoilswerehomogenizedbysieving(

15-

mmmesh)andmixing,andthenplacedinpots(10Lvolume,25 cmwide×30cmhigh).Theseedsoffivestudiedspeciesandther hizomesofR.japonicaweregatheredinOctober2013andinApri l2014,respectively,fromthesameareaassoils.Theseedswerest oredat4°C.Therhizomeswereusedtosetuptheexperimentdirec tlyaftertheircollection.AllspecieswiththeexceptionofR.japon ica,thereproductionofwhichinEuropeismainlyvegetativ e(Dassonvilleetal.2007),weresowed(ca.30seedsperpot)

andrhizomesofR.japonica(onerhizomeperpot)wereplantedin April2014directlyintheexperimentalpots.Theseedswerehomo genouslyscatteredonthesoilsurfaceandcoatedwith

0.5cmofsoillayer.InthecaseofannualI.glandulifera,30seedspe rpotwerealsosowedinthesecondyear.Thefollowingplanttreat mentswereestablishedineachsoilinsixreplicates

(1)baresoil,(2)nativeA.vulgaris,(3)nativeP.arundinacea, (4)nativeA.vulgaris+ P.arundinacea,(5)invasive I.glandulifera,(6)invasiveR.japonica,(7)invasive R.laciniata,and(8)invasiveS.gigantea,givingatotalof96pots.T hepotswerearrangedinarandommannerandkeptundernatura latmosphericandlightconditionsintheBotanicalGardenofth eJagiellonianUniversity(50^°3′57.8N,19^°57′19.0E)fortwogrow ingseasons(since12thApril2014to25thAugust2015).Theplan tswerewateredinspringandsummerwiththesamevolumeoftap water(1Lperpot)whenprecipitationwasinsufficient.Meanvalu esofselectedpropertiesoftapwaterwereasfollows:pH—

7.7,nitrites—

<0.02mg/L,nitrates—10.5mg/L,Ca—73.4mg/L,andMg—

8.2mg/L(MPWiK2015,2016).Allemergingweedswereremo vedbyhand.Inwinter,thepotswerewrappedwithabubblewrapto preventplantsfromfreezing.

Attheendoftheexperiment,plantcoverineachpotwasrecor dedandthenabovegroundplantbiomasswasharvested.Awhol evolumeofsoilwaspulledoutfromeachpotandanoutersoillaye r(upto3cm)wasdiscarded.Thenthesoilfromeachpotwasthoro ughlymixedandsubsamplesforphysico-

chemicalanalyseswerecollected.Additionally,sixreplicateso feachsoilusedtoestablishtheexperiment(initialsoil)wereanal yzedalongwithpotsoils,givingatotalof108samples.

2.3Laboratorywork

Plantbiomasswasdriedat80°Cfor48handweighted.Twe ntyphysicochemicalparametersweremeasuredinallsoilsampl es.ThesewerepH,maximumwaterholdingcapacity(WHC),t hecontentsoforganicmatter,organicC,totalC,Ca,Fe,K,Mg,N, Na,P,S,exchangeableCa,K,Mg,OlsenP,N-NH4,N-

NO3,andS-

SO4.Textureoftwoinitialsoilsthathadbeenusedtoestablishth eexperimentwasalsodetermined.Soilsamplesweresieved(2- mmmesh),driedatroomtem-

peratureorat105°C,dependingonanalysis.Soiltexturewasdeter minedthroughacombinationofsievingandsedimenta- tion(ISO112771998)andWHCaccordingtoÖhlinger(1996) withmodifications.SoilpHwasmeasuredin1:5(w:v)watersus pensionswithaHachHQ40Dmeter.Organicmatter,total,ando rganicCweredeterminedwithaLecoRC-

612,andtotalSwithaLecoSC-

144DRdrycombustionanalyzeringroundsoil.TotalNwasm easuredusingtheKjeldahlmethod;groundsoilwasdigested inH2SO4withKjeltabs(K2SO4+CuSO4·5H2O;FossTecatorDi gestorAuto)followedbydistillationonaFossTecatorKjeltec 2300AnalyzerUnit.TheavailableP(OlsenP)wasmeasured

withanionchromatograph(DionexICS-

1100)followingsoilextractionwith0.5MNaHCO3(1:10,w:v) .ToanalyzeN-NH4,N-NO3,andS-

SO4,soilwasshakeninwaterfor1h(1:10,w:v),andN- NO3andS-SO4intheextractsweredeter-

minedwithDionexICS-1100,whileN-NH4withDionexDX- 100.TotalCa,Fe,K,Mg,Na,P,andexchangeableCa,K,and Mgwereextractedbydigestionofgroundsoilinhotconcen- tratedHClO4(FossTecatorDigestorAuto)orshakingsoilin 0.1MBaCl2(ISO112601996),respectively.Extractedele- mentswereanalyzedwithflameatomicabsorptionspectrom- etry(VarianAA280FS),withtheexceptionoftotalP,whichwas measuredcolorimetrically(Hach-

LangeDR3800).Twocertifiedreferencematerials,namelyCR M048-050(RTC;to-tal)andISE-

912(WEPAL;exchangeable)wereusedtoesti-

matethequalityofmetalanalysesinsoil.Therecoveryvaluesfort otalmetalsrangedfrom95(Na)to99%

(Fe,K)andforexchangeablemetalsfrom87(Ca)to99%(K).

2.4S tatisticala nalysis

Priortostatisticalanalysis,allvariablesweretransformedwitha logarithmicorexponentialfunctiontoobtainanormaloratleasts ymmetricaldistribution.Thevariableswerethenstan- dardizedtogetvaluesrangingfrom0to1.Two-

wayANOVAwasperformedtotesttheeffectofplantspecies,soi ltype,andtheirinteractionsonplantbiomassandcover.Ifplants pecies

×soiltypeinteractionsweresignificant(p<0.05)ormargin- allysignificant(p<0.1),plantspecieseffectsonplantbio- massandcoverwereassessedseparatelyforeachsoiltypeusin gone-wayANOVAfollowedbypost-

hocTukey’sHSDtest.Reynoutriajaponicawasexcludedfroms tatisticalanaly-

sesinvolvingplantbiomassandcoverasitwasplantedfromrhizo mes,andthus,ishardlycomparablewithotherspecies.

Clusteranalysis(singlelinkage,Euclidean distance) onphysicochemicalvariableswasusedtoexplorethegroupingof soilsamples.Initialfallowandvalleysoilswerecomparedinterm sofphysicochemicalpropertiesusingStudent’sttest.Discriminan tanalysis(DA)wasperformedseparatelyonfallowandvalleydata toidentifythecombinationsofphysicochemicalvariablesdiscri minatingsoilsunderdifferentplantspeciesthemosteffectively.V ariableswiththehighestcontributiontodis-

criminatingaxeswereidentifiedonthebasisoftheirloadingvalue s.Thesevariableswerefurthercomparedbetweenplantspeciesu singone-wayANOVAfollowedbypost-

hocTukey’sHSDtest.Pearson’scorrelationsbetweenplantbiom assandsoilpropertieswereassessed.Statisticalanalysisempl oyedSTATISTICA12andPAST3.14(Hammeretal.2001).

3 Resul ts

Abovegroundplantbiomassinexperimentalpotswasaffected byspecies(F5,60=16.1,p<0.001),soiltype(F1,60=37.9,

Table1Abovegroundplantbiomass(gdryweight)andcover(%)inexperimentalpots(meansandstandarddeviations,N=6) SoiltypeNativespeciesInvasivespecies ArtemisiavulgarisPhalarisarundinaceaA.vulgaris+P.arundinaceaImpatiensglanduliferaReynoutriajaponica

JSoilsSediments(2018)18:1409–1423 141

3

RudbeckialaciniataSolidagogigantea Biomass4.79±1.06bc 3.06±0.81ab 3.17±0.48bc 6.46±2.84c 4.28±1.00c 2.09±0.76a 1.26±0.22a 35.63±3.00* 22.26±6.27* 5.76±0.73c 3.43±1.00bc 6.02±1.06c 2.93±0.84bc FallowValley 53.3±9.8b 56.7±10.8c 68.3±23.2b 47.5±16.4abc 25.0±8.9a 23.3±6.1a 12.5±2.7* 8.3±4.1* 75.8±16.9b 59.2±15.0c 55.8±8.6b 30.0±11.4ab FallowValley Meansmarkedwithdifferentletterswithinarowaresignificantly(p<0.05)differentaccordingtoTukey’sHSDtest*R .japonicawasexcludedfromanalysisasitwas,incontrasttootherspecies,plantedfromrhizomes

p<0.001),andspecies×soiltypeinteraction(F5,60=2.75,p=0.0 27).Plantbiomassofmostspecieswashigheronfallowt hanon valleys oil(Table1).R eynoutriajaponicawasdistinguishedby thehighestbiomassasitwasplantedfromrhizomes.Amongsp eciesplantedfromseeds,thelowestbiomasswasobservedinthe caseofI.glanduliferaandthehighestinaspeciesmixture(A.v ulgaris+P.arundinacea)growinginbothsoiltypes(Table1).Pl antcoverinexperi-

mentalpotswassignificantlyaffectedbyspecies(F5,60=13.5,p<

0.001)andsoiltype(F1,60=10.0,p=0.002).Theeffectofspecies×

soiltypeinteractiononplantcoverwasmarginallysignificant(F

5,60=2.17,p=0.07).Plantcoverwas eithersimilaronthetw osoiltypesorhigheronfallowsoil(Table1).Reynoutriajapon icawascharacterizedbythelow-

estcover.Amongspeciesplantedfromseeds,thelowestcoverw asobservedinI.glanduliferaandthehighestinR.laciniatainboth soils(Table1).

Bothsoiltypesusedintheexperimentwereclassifiedasloa mysand.Fallowandvalleysoilscontained84and87%sand,7a nd4%silt,and9%clay,respectively.Despitethesimilarityint exture,initialfallowandvalleysoilsdifferedsignificantly(p

<0.05)intermsofnearlyallsoilphysico-

chemicalproperties.InitialfallowsoilhadhigherWHC,or- ganicmatterandorganicCcontent,totalCandN,exchange- ableMgandOlsenPconcentrations,butlowerconcentrationsof totalCa,Fe,K,Mg,andNa,exchangeableCaandK,N-

NH4,andpHthaninitialvalleysoil(TablesS1andS2,Electroni cSupplementaryMaterial).Clusteranalysisalsoshowedthatfa llowandvalleysoilsgroupedintoclearlydis-

tinguishableclusters(Fig.1).Asverylargedifferencesbe- tweensoiltypescanaffectmultivariateanalysisand/orhinderth edetectionofmoresubtledifferences(i.e.,thosebetweenplant species),DAwasperformedseparatelyforeachsoiltype.

Discriminantanalysisonbothfallowandvalleysoildatasho wedthatplantspeciestreatmentswereseparatedeffective- ly.Thelargestdiscriminationwasobservedamonginvasivespe cies(Figs.2and3).Invasiveplants,withtheexceptionof I.glandulifera,alsodifferedconsiderablyfromnativespecies(F igs.2and3).TheconcentrationsofN-NO3,N-NH4,S-

SO4,exchangeableK, totalP,andWHCwereamongthemosti mportantvariablesforthediscriminationofplantspeciestrea tmentsinbothsoiltypes(Table2).ThefirsttwoDAaxesexplaine djointly76.8%ofvarianceinfallowsoildata(Table2).Exchan geableK,N-NH4,totalP,N-

NO3,andWHChadthehighestloadingsonthefirstandS- SO4,ex-

changeableMg,totalP,exchangeableCa,andtotalMgonthes econdaxis(Table2).Rudbeckialaciniatastoodawayfromall otherspecies(Fig.2).Thelargestdistancealongthefirstaxeswas foundbetweeninvasiveR.laciniata(rightsideofthediagram)a ndinvasiveI.glandulifera,nativespecies,andbaresoil(leftside )(Fig.2).Overall,theformerhadrela-

tivelylowconcentrationsofexchangeableK(Fig.4a),N-NH4

Axis2Distance E-FRl-FAv-F 0.5

1.0

1.5

2.0

Fig.1Resultsofclusteranalysisonsoilphysicochemicalproperties.Plan tspecies:E—emptypot(baresoil);Native:Av—A.vulgaris,Pa—

P.a r u ndinacea,AvPa—am i xtureo f A . v ulgarisa ndP.a r u ndinacea;

Invasive:Ig—I.glandulifera,Rj—R.japonica,Rl—R.laciniata,Sg—

S.gigantea.Soiltype:F—fallow,V—valley

(Fig.4b)andN-

NO3(Fig.4c),andhighconcentrationoftotalP(Fig.4d)incompa risontothelatter(thoughtherealsoweresomeexceptions).Allin vasivespecies,withtheexceptionof

I.glandulifera,werelocatedontherightsideofthediagram

(Fig.2),probablyduetoverylowN-

NH4concentrationinsoil(Fig.4b).AccordingtoDA(Table2,Fig .2),soilWHCalsocontributedtothediscriminationbetweenspe cies—

thelowestvalueswerefoundunderinvasiveS.gi g anteaandnat ive

S-SO4 10.0

MgEX 7.5

KT MgT PT

5.0 CaEX ST POL

C2a.5T pH

FeT

CORGNT NaT N-NO3

-7.5 -5.0 -2.5 2.5 5.0 7.5 10.0 12.5

KEX

-2.5

N-NH4

WHC -5.0

-7.5 Axis1

Fig.2Two-

dimensionalploto ft hediscriminantanalysisbasedonphysicochemical

propertiesoffallowsoil.Blacksymbolsindicateinvasivespecies(blackd ots—I.glandulifera,blacksquares—

R. japonica,blacktriangles—R.laciniata,blackdiamonds—

S. gigantea),emptysymbolsindicatenativespecies(triangles—

A.vulgaris,invertedtriangles—P.arundinacea,andsquares—

amixtureofA. v u lg a r i s an d P.arun din ace a),an d × in d ica tesb a r e s o i l . E X —exchangeable,OL—Olsen,ORG—organic,T—total

Axis2

8

6

PT 4 WHC

MgEX 2

S-SO4

-8 -6 -4 -2

MgT FeT CaEXNaTS T

2 4 pH 6 8 10

NT -2

CORG KT

-4 CaT

KEX -6

N-NH4-8 POL

-10 Axis1

Fig.3Two-

dimensionalploto ft hediscriminantanalysisbasedonphysicochemical propertiesofvalleysoil.Blacksymbolsindicateinvasivespecies(black dots—I.glandulifera,blacksquares—

R. japonica,blacktriangles—R.laciniata,blackdiamonds—

N-NO3

S. gigantea),emptysymbolsindicatenativespecies(triangles—

A.vulgaris,invertedtriangles—P.arundinacea,andsquares—

amixtureofA.vulgarisandP.arundinacea)and×—baresoil.EX—

exchangeable,OL—Olsen,ORG—organic,T—total

speciesmixtureandthehighestinbaresoil,undernative A.vulgarisandinvasiveI.glandulifera(Fig.4e).Twoin- vaders,namelyR.laciniataandS.gigantea,differedconsid- erablybetweeneachotherasindicatedbytheirpositionsonthed iagram—

theformerwaslocatedatthebottomandthelatteratitsopposites ide(Fig.2).Ingeneral,R.laciniatahadlowerconcentrationsofS -

SO4( Fig.4f),exchangeableMg(Fig.4g),andCa(Fig.4h).Tot alMgdifferedsignificantly(p<0.05)onlybetweenbaresoil(l owconcentrations)andnativespeciesmixture(highconcentr ations)(TableS1,ElectronicSupplementaryMaterial).

ThepatternobtainedbyDAonvalleysoildatawassomewhat similartothatforfallowsoilfortworeasons—

invasiveI . g landuliferas toodc losert o b ares oila ndm ostnati vetreatmentsthantootherinvaders,andanotherinvader(R.japo nicainthiscase)stoodoutfromallothertreatments(Fig.3).Thef irsttwoDAaxesexplainedjointly64.9%ofvarianceinthedata (Table2).TheconcentrationsofN-

NO3insoilcontributedhighlytobothDAaxes,followedbytotal N,S-SO4,totalP,andpH(axis1)andN-

NH4,OlsenP,andexchangeableK ( axis2 )

( Table2).I n vasives peciesw ereseparatedalongboththefirst andthesecondaxes(Fig.3).Rudbeckial a ciniataa n d S . g i ga nteac l usteredo n t h e l e ftsidet ogetherw ithnatives peciesm ixture,a ndR . j aponicaontherightsideofthediagram.Ingener al,R.japonicasoilhadh igherN -

NO3( Fig.5a)a ndp H ( F ig.5b),b utl o wertotalN(Fig.5c),P(Fi g.5d),andS-SO4(Fig.5e)concen-

trationsi n c o mparisont o R . l aciniataa n d/orS . g i gantea.

Impatiensg landuliferal iedi n t heb o ttomo f t hed iagram,i ncontrasttothreeotherinvaders(Fig.3).Ithadstrikinglyhigh c oncentrationso f N -NO3(Fig.5a),N -

NH4(Fig.5f),andOlsenP(Fig.5g)whencomparedtoallother invadersandsomenativetreatments.SoilunderR.japonicah adtheloweste x c h a n geableK ( F i g .5h)a m o n g a l l s p e c i e s.S o i l WHCdifferedsignificantly(p< 0.05)betweenn ative

P.arundinacea,invasiveI.glandulifera(low),and R. laciniata(high)

(TableS2,ElectronicSupplementaryMaterial).Meanvalues andstandarddeviationsofphysico-

chemicalproperties,includingthosethatcontributedlessord idnotcontributetothediscriminationofplantspeciestreat- mentsinDA(Table2),arepresentedinTablesS1andS2(Ele ctronicSupplementaryMaterial).

Plantabovegroundbiomasswassignificantlycorrelat edwithsomesoilparameters,indicatingthatspeciesinfluenc eonsoilmaydependonitsbiomass.Positiverelationshipsbe- tweenplantbiomassandparametersoffallowsoilwerefoundf ortotalFe(r=0.40,p=0.015),Na(r=0.42,p=0.010),Mg (r=0.37,p=0.028),Ca(r=0.35,p=0.038),P(r=0.52, p=0.0013),andnegativeforWHC(r=−0.48,p=0.0029),exch angeableK(r=−0.33,p=0.048),N-

NO3(r=−0.37,p=0.028),andN- NH4(p=−0.41,p=0.012).Positiverela-

tionshipsbetweenplantbiomassandvalleysoilparametersw erefoundforWHC(r=0.33,p=0.047),totalP(r=0.38,p=0.02 1), andnegativeforexchangeableK (r=−0.42,p= 0 . 010),O lsenP (r= − 0.60,p < 0.001),andN -

NO3(r=−0.64,p<0.001;Fig.6).

Table2Resultso fd i scriminantan alysisperformedseparatelyforfallow andvalleysoils

Fallowsoil Valleysoil

Axis1 Axis2 Axis1 Axis2

Eigenvalues 29.4 17.8 24.1

17.5

Varianceexplained(%) 47.9 28.9 37.6 27.3 Loadings

pH 0.003 0.021 0.022 −0.002

WHC −0.020 −0.020 0.005

0.023

CORG 0.009 0.011 −0.010 −0.012

CaT −0.002 0.010 0.010 −0.021

CaEX 0.010 0.023 −0.002

0.000

FeT 0.004 0.019 −0.003

0.003

KT −0.005 0.022 −0.001 −0.015

KEX −0.030 −0.002 −0.011 −0.026

MgT 0.002 0.023 −0.007 −0.002

MgEX −0.009 0.032 0.010

0.015

NT 0.012 0.013 −0.035 −0.008

N-NH4 −0.030 −0.018 −0.007 −0.039

N-NO3 −0.020 0.002 0.049 −0.049

NaT 0.009 0.008 −0.001 −0.001

PT 0.022 0.026 −0.026

0.021

POL −0.002 0.018 0.005 −0.039

ST −0.016 0.017 0.002

0.002

S-SO4 −0.005 0.045 −0.028

0.002 Initialsoilwasexcludedfromanalysis

VariableswiththehighestloadingsoneachaxisaregiveninitalicsEXe xchangeable,OLOlsen,ORGorganic,Ttotal

4 Discussio n

Ourstudycomparedtheeffectsofthegrowthoffourinvasivespe cies—I.glandulifera,R.japonica,R.laciniata,and S. gigantea—

onthephysicochemicalpropertiesoftwosoilsinatwo- yearpotexperiment.Itshowedthattheseinvasiveplantssignifi cantlyinfluencedmostsoilproperties.Theinflu-

encedifferedintermsofmagnitudeanddirectionbothbe- tweeninvasiveandnativespeciesandamonginvasivespe- cies.Themultidirectionaleffectsofdifferentinvadersresultedi naconsiderabledivergenceinsoilcharacteristics.Overall,tota landavailableformsofN(N-NO3,N-NH4)andP(Olsen),S-

SO4,exchangeableK,andMgcontributedthemosttothediscrimina tionofsoilsunderdifferentplantspecies.

TheinfluenceofinvasiveI.glandulifera,R.japonica,and S.giganteaonsoilhasbeenestimatedearlierinnumerousfieldstu dies(Chapuis-

Lardyetal.2006;Vanderhoevenetal.2006;Dassonvilleetal.2008

;Scharfyetal.2009;Maureletal.2010;Tharayiletal.2013;Qu istetal.2014;Rucklietal.2013,2014b;Stefanowiczetal.2017),b utexperiments

Fig.4Physicochemicalpropertiesoffallowsoil(meansandstandard

„

ors).Onlyvariableshighlycontributingtothediscriminationofplantspeci estreatmentsarepresented.Meansbearingdifferentlettersdiffersignifi cantly(p<0.05)accordingtoTukey’sHSDtest.Plantspecies:

E—emptyp ot(bares oil);N ative:Av—A.vulgaris,P a—

P.a r u ndinacea,AvPa—

am i xtureo f A . v ulgarisa ndP.a r u ndinacea;Invasive:Ig—

I.glandulifera,Rj—R.japonica,Rl—R.laciniata,Sg—

S.giga ntea

concerningthisproblemarerare(Scharfyetal.2010,2011;

Bardonetal.2014,2016).Previousstudiesfocusedmainlyo ninvasion-

inducedchangesindifferentformsofNandPinsoilandfound thatthesepropertiesrespondedvariablytothepres-

enceofI.glandulifera,R.japonica,orS.gigantea,andsodids omeexchangeablecations,forexampleKandMg(Chapuis- Lardyetal.2006;HejdaandPyšek2006;Vanderhoevenetal .2006;Dassonvilleetal.2007;Scharfyetal.2009,2010,2011

;Tharayiletal.2013;Rucklietal.2014b;Stefanowiczetal.

2017).Specifically,ourfieldstudyindicatedthatNandPwe retheonlysoilphysicochemicalvariablesthatreactedtoinv a-

sion;totalPdecreasedsignificantlyunderinvasivespecies

—

R. japonica,R . l a c i n i a t a ,a n d S . g i g a n t e a,a n d N - N O3in-

creasedunderR.japonicaincomparisontonativevegetation (Stefanowiczetal.2017).Anotherstudyrevealedthat S. giganteainvasionsignificantlyincreasedavailablePan ddecreasedN-

NO3concentration,butdidnotinduceanychangesinmanyot hersoilvariables,includingexchangeablecations,incomp arisontonativeplants(Vanderhoevenetal.2006).Anincrea seinsoilavailablePwasalsodetectedunder

S.giganteaandI.glanduliferaincomparisontouninvaded sites(Chapuis-

Lardyetal.2006;Rucklietal.2014b).Ontheotherhand,nodif ferencesinsoilCandNwerefoundbetweenpatchesofR.jap onicaandadjacentareas(Aguileraetal.2010).Similarly, soiltotalphenolics,N,andPdidnotdifferbetwee nthegro upsofinvasiveforbs,including

I.g landulifera,R . j aponica,a ndS.gigantea,nativeforbs andnativegraminoids(Scharfyetal.2011).Overall,itseems thatincreasesornochangesinsoilnutrientconcentrationsdu etotheinvasionofthesespeciesprevailoverdecreases(G üsewelletal.2005;Vanderhoevenetal.2005,2006;Chapu is-

Lardyetal.2006;Dassonvilleetal.2007;Aguileraetal.2010

;Minchevaetal.2014;Rucklietal.2014a;Scharfyetal.2009 ,2010,2011;Stefanowiczetal.2017).

Physicochemicalsoilpropertiesmaybeaffectedbyplant sbothdirectlyandindirectly—

throughmodificationoftheac-

tivity,biomass,ormicrobialcommunitystructure,whichi nturnresultsinchangesinorganicmatterdecompositionan

dothersoilprocesses,andthus,inconcentrationsoftotalandava ilablenutrientsinsoil.Afewexperimentalandfieldworkshavec onsistentlyreportedtheabilityofR.japonicatomodifyNturnov er(HiroseandTateno1984;Tharayiletal.2013;Bardonetal.

2014,2016;Stefanowiczetal.2016).Thisspe-

ciesincreases,atleastseasonally,theconcentrationofN- NO3insoilincomparisontonativevegetation,presumablydueto

N-NO3(mgkg-1)ExchangeableK(mgkg-1)WHC(gHOg-1dw) N-NH4(mgkg-1)TotalP(gkg-1)

(a)

44

40 cd

F7,40=8.1,p<0.001 d

(b)

15

12

d F7,40=22.0,p<0.001

bcd

28

20 a b c b c d

bcd

b a

bc 3 ab

0

cd cd

a a

a

(c)

14

E Av PaAvPaIg

RjRl Sg

(d )

2

E Av PaAvPaI g Rj Rl Sg

b 12 b ab

F

=3.6 ,p=0 .004

a b a b

2.

0

c

F7,4 0=1 2.0 ,p<

0.0 01 c

c 10

a b a b

1.8 bc

bc

8 1.6

a

ab

ab a

6 1.4

4

(e)

E Av

PaAvPaIg Rj RlSg

(f)

1.

2 E Av

PaAvPaIg Rj Rl Sg

0.60b b

0 . 5

6

ab F

=5.4, p<0.

b001

10 F7,4 0=1 2.4,p<

0.001

ExchangeableMg(mgkg-1) -1 S-SO4(mgkg)

2 ExchangeableCa(mgkg-1)

50 600

E Av PaAvPaIg Rj Rl Sg E Av PaAvPaIg Rj Rl Sg

8 bcd d

c d

bc d

0 .

0.48 a b

ab ab

a a a

abc a

0.44

(g)

110 E Av

PaAv PaIg Rj Rl Sg

F7,40=6.3,p<

0.001

( h )

2

1 4 0 0

E Av

PaAvPaI g Rj

Rl Sg

F

100

90

80

70

60 c

ba c

a b c ab

a 120

0

100 0

800 a ab

ab c

b c

a bc

c

a b c a b

themodificationofdenitrificationandNmineralizationpro- cessesviasecondarymetabolites(HiroseandTateno1984;Th arayiletal.2013;Bardonetal.2016;Stefanowiczetal.2017).

However,theeffectofR.japonicaonN-NO3concen-

trationwasnotevidentinourexperiment.TheconcentrationofN -

NO3invalleysoilwasactuallyhigherunderR.japonicathanund ersomenativeandinvasivespecies,butnosuchdifferenc eswerefoundinthecaseoffallowsoil.

Thevariabilityinthesoilresponsetoplantinvasionre- vealedbydifferentstudiesmaybecausedbyanumberofreas ons,amongwhichthemostimportantarefunctionaltraitsofinva sivespeciesandnativevegetation,propertiesofrecip-

ientsoil,season,andlengthofinvasionhistory(Dassonvilleetal .2008;Liaoetal.2008;Scharfyetal.2011;Tharayiletal.2013).Pl antsaffectthesoilenvironmentthroughdepositionoflitter,exu dationofchemicalcompoundsviaroots,ortheirleachingfrompl antsbyrain,aswellasthroughnutrientup-

take(Hobbie1992;Orwinetal.2010;Haicharetal.2014;Ruc klietal.2014a).Itisknownthatinvasiveplantspeciesoftenpro ducehugeamountsofbiomasswhichdiffersconsid-

erablyfromthatofnativevegetationinchemicalquality,forexa mpleligninandelementcontent,C/Nandlignin/Nratios,and/or secondarymetaboliteconcentrations(Dassonvilleetal.2007,2 008;Tharayiletal.2013;Minchevaetal.2014).Largequantities ofsenescentplantbiomassreachthesoilsurfaceduringlitterfa llandundecomposedlitterfragmentsmayaccu-

mulateintheformofathicklayerifthelitterquality,andhence ,itsdecompositionratearelow.Suchaphenomenonwasobser vedinR.japonica,contributingtochangesinbothsoilpropertie sandplantcommunities(Maureletal.2010;Stefanowiczet al.2016;Stefanowiczetal.2017).Thequalityandquantityofp lantbiomassdifferconsiderablyamonginvasivespecies.Dass onvilleetal.

(2008)foundthattheamountofbiomassofR.japonicawasmuch higherthanthatofI.glanduliferaandS.gigantea,andthetissues of

I.glanduliferacontainedmorenutrientsthatthetwoothers pecies.

Itshouldbenoted,however,thatlitterdepositionbyplantsgro winginapotexperimenthardlymimicsthatbywell-

establishedstandsofvegetationinnaturalconditions.Litter fallwasconsiderablyrestrictedinthisexperimentduetoitsshor tdurationandlowplantbiomass.OnlyR.japonica,thebiomasso fwhichwasanorderofmagnitudehigherthanthebiomassofothe rspecies,depositednoticeableamountofleaflitterinoneseasona ndcouldhaveameasurableeffectonsoilpropertiesthroughleac hingofelementsorphenolicsfromthatlitter(BergandMcClaug herty2008;Tharayiletal.2013).Therefore,itmaybesupposedth atthestrongandmultidirec-

tionalsoilresponsetothepresenceofinvasivespeciesinourexpe rimentwasmainlytriggeredbynutrientuptakeandexu- dationofspecies-

specificchemicalcompoundsviaplantroots,thoughplantgro

wthwassuggestedtoexertaweakereffectonsoilthanplantdetritali nputs(Dornbush2007).Plant

Fig.5Physicochemicalpropertiesofvalleysoil(meansandstandard

„

ors).Onlyvariableshighlycontributingtothediscriminationofplantspeci estreatmentsarepresented.Meansbearingdifferentlettersdiffersignifi cantly(p<0.05)accordingtoTukey’sHSDtest.Plantspecies:

E—emptyp ot(bares oil);N ative:Av—A.vulgaris,P a—

P.a r u ndinacea,AvPa—

am i xtureo f A . v ulgarisa ndP.a r u ndinacea;Invasive:Ig—

I.glandulifera,Rj—R.japonica,Rl—R.laciniata,Sg—

S.giga ntea

rootsexudeanumberofcompounds,amongothers,sugars, organicacids,aminoacids,proteins,enzymes,phenolics,a ndinorganicions,whichactasnutrientsource,chemoattract antsignals,chelatorsofmineralnutrients,plantdefendersor mod-

ifiersofplant,andmicrobialgrowth(Haicharetal.2014).

Rhizodepositionisinfluencedbymanybioticandabioticfac -

torssuchasplantspecies,developmentalstatus,evapotrans -

piration,rootage,rootingdepth,mycorrhiza,soiltype,nutri -

entdeficiency,temperature,moisture,andmanymore(Jone setal.2004).Rootexudationofsecondarymetabolitesma yplayaparticularlyimportantroleinthecaseofinvasiveplan tasthesecompoundspotentiallycontributetotheinvasionsu c-cessofsomespecies—

aphenomenoncallednovelweaponshypothesis(Callaway andRidenour2004).Theycanactnotonlyasallelopathicag entsbutalsoasmediatorsinplant-

soilmicrobialinteractions,therebypotentiallyalteringther ateofsoilprocessesandnutrientconcentrationsinsoil(Call awayandRidenour2004).

Inourexperiment,plantrootswereverylongandpresenti nthewholevolumeofsoilunderallspeciesexcept I.glandulifera.Inthecaseofthelatterspecies,therootswere muchshorterandgrewonlyinthesurfacesoil.Infact,thero otingdepthofI.glanduliferaisshallower(10–

15cm)incomparisontosomeotherinvaders,forexampleR.

japonica(2m)

(BeerlingandPerrins1993;Westonetal.2005).Thediffere ncesintherootingdepthbetweenI.glanduliferaandothers peciesobservedinexperimentalpotsmayhavecontrib- utedtosomeextenttodifferentialinfluenceofthisspecieson soil.Lowbelowgroundandabovegroundbiomassof I.glanduliferamayhaveresultedinaweakinfluenceofthiss peciesonsoil,andthus,inarelativesimilarityofitssoiltobot hnativeandbaresoils.

WhilethetissuesorlitterofI.glandulifera,R.japonica, R.laciniata,andS.giganteahavebeenassessedinrespectofe lementand/orsecondarymetaboliteconcentrationsandso meauthorstriedtolinktheirtissuequalitywiththesoilenviro n-

ment(Kalembaetal.2001;Dassonvilleetal.2008;Fanetal.2 009;Aguileraetal.2010;Tharayiletal.2013;Bardonetal.20

14;Rucklietal.2014a;Stefanowiczetal.2017),muchlessiskno wnonthequalityofrootexudatesofthesespeciesortheireffects onphysicochemicalandbiologicalsoilproperties(Scharfyetal.

2010;Rucklietal.2014a).Rucklietal.

(2014a)foundthatI.glanduliferaisabletoinhibitmyceliumgro wthbynaphthoquinones—

phenolicsreleasedfromrootsorleachedfromleavesbyrain.On theotherhand,3-yeargrowth

TotalN(gkg)N-NO3(mgkg-1)-1 TotalP(gkg-1)pH

(a)

6

5

4 cd

3

c

F7,40=63.6,p<0.001 d

bc

(b)

8.32

8.28

8.24

8.20 b

ab ab

ab ab

F7,40=3.9,p=0.002 b

ab 2 b

1 a a a 0 a

8.16

8.12

(c )

.5 E Av

PaAvPaI g Rj Rl Sg

(d)

1. 8

E Av PaAvPa Ig Rj

RlSg

0.4

0.3

0.2 b

b

a b

a b a b

F

7, 4 0= 4. 8 ,p

<0 .0 01

ab

a 1.

6

1.

4

1.

2 a bb

a

F7,4 0=1 3.2, p<0 .00 1

c b

ab

(e )

E Av

PaA vPaI g Rj Rl Sg

( f )

1 . 0

8

E Av

PaAvPaI g Rj

RlSg

-1-1 N-NH4(mgkg-1)

S-SO4(mgkg)OlsenP(mgkg) -1ExchangeableK(mgkg)

0 68

E Av PaAvPaIg Rj Rl Sg E Av PaAvPaIg Rj Rl Sg

10

bcd8 cd bcd

F7,40

=11.

7,p<

0.00 1 d

6

4

cF .001

c c b c

a b

b c 6

a 2 a ab 4 aa

a

2

(g)

16 E Av

PaAv PaIg Rj Rl Sg

0

(h )

92

E Av

PaAvPaIg Rj Rl Sg

dF c c

F,p<0.001

88 12bc

84 b bc

c ab

8 80 a

b

c

4 a b b c

ab a bc

a

N-NO3(standardizedvalues)

1420 JSoilsSediments(2018)18:1409–1423

1.0

0.8

0.6

0.4

0.2

0.0

0.0 0.2 0.4 0.6 0.8 1.0

Plantbiomass(standardizedvalues)

Fig.6RelationshipbetweenplantbiomassandN-

NO3concentrationinvalleysoil.Blacksymbolsindicateinvasivespecies(

blackdots—

I.glandulifera,blacktriangles—R.laciniata,blackdiamonds—

S.gigantea),emptysymbolsindicatenativespecies(triangles—

A.vulgaris,invertedtriangles—P.arundinaceaandsquares—

amixtureofA.vulgarisandP.arundinacea).Pearson’sr=−0.64,p<0.001

ofS.giganteainexperimentalwetlandplantcommuniti esinfluencedneitherNnorPavailabilityinsoil(Scharfyetal.20 10).

Therearesomedataindicatingthatinvasiveplantspeciesdiff erfromnativeonesintermsofnutrientuptake.Solidagogigante atookupabouttwiceasmuchPperunitareaasnativeplants,possi blyduetoitshigherproductivity,deeperrootingsystem,ormore effectiveexploitationofmycorrhizalsymbi-osis(Chapuis- Lardyetal.2006).Actually,Majewskaetal.

(2017)reportedthatthegrowthofS.giganteaand

R.laciniataandPcontentintheirtissueswereenhancedbyarbu scularmycorrhizalfungi.Dassonvilleetal.

(2007)stressedtheimportanceofhighproductivityandnutrient upliftfromdeepsoilhorizonsasmechanismsdrivingchanges intopsoilchemicalcompositioninducedbytheinvasionof R.japonica.However,thelattermechanismdoesnotplayarolei nrelativelyshallowexperimentalpots.

Thedifferencesbetweenthetwonativespeciesintheir effectsonsoilwereratherminorwhencomparedtothose amonginvasivespecies.SoilsunderA.vulgarisand P.a r u n d inacead i fferedi n N - H N4,N -

N O3,a n d / o r t o t a l P,

whichmostlywerehigherunderthelatterspecies.Thesena- tiveswereexpectedtoaffectsoildifferentlyastheybelongtodisti nctfunctionalgroups—forbsandgraminoids,whichdif- ferfromeachotherinmanytraits,forexample,tissuedensity,lea fthickness,leaflifespan,andlitterdecomposability(Scharfy etal.2011).Itshouldbekeptinmindthat

A.vulgarisandP.arundinaceaarenativeexpansivespecies

JSoilsSediments(2018)18:1409–1423 1421

inEurope,butnoxiousinvadersinsomeotherpartsofthewo rld,forexample,NorthAmerica(Westonetal.2005;Jacinthe etal.2010).Inthiscontext,dataontheireffectsonsoilgatheredi nthisstudyseemparticularlyvaluable.

Inourexperiment,theeffectsofplantinvasionvariedamon gthetwosoils,probablybecausethesoilsdifferedinnearlyall physicochemicalproperties,i.e.,totaland/oravail-

ableconcentrationsofmostelements,organicmattercontent, WHC,andpH.Otherstudiesalsosuggestedthattheeffectsofin vasionmaydependonthepropertiesofrecipientsoil(Dasso nvilleetal.2008;Scharfyetal.2009).Dassonvilleetal.

(2008)observedapositiveimpactofplantinvasiononnutrientc oncentrationsinsoilswithinitiallylownutrientlevelsandanegat iveimpactundertheoppositeconditions.Inturn,Scharfyetal.

(2009)foundthattheeffectsofinvasiononsomesoilphysicoch emicalpropertiesdependedonPavailability,beingmoreevid entatP-richsites.Inourexperiment,plant-

soilfeedbackwasobservedasmorefertile(intermsoforganicm atterandNcontent)fallowsoilgenerallymaintainedplantschara cterizedbyhigherbiomassthanplantsonpoorervalleysoil.The differencesinplantbiomassbetweenthesoiltypesmayhavecont ributedfurthertodifferencesininvasioneffectsonthesesoils.A smentionedearlier,onlyrestrictedresponseofsoilphysicoche micalcharacteristicstotheinvasionof

R.japonica,R.laciniata,andS.giganteawasobservedinourpre viousfieldresearch,whichusedmanystudysitesinordertosear chforgeneralpatternsofinvasioneffectsonsoil(Stefanowi czetal.2017).Anexplanationfortheweakoverall

soilresponsecouldbethatthesoilsactuallychangedduetotheinv asionbutthedirectionofthechangesvariedamongsoils.Therefo re,nosignificantinvasioninfluencecouldbefoundwhenanaly zingthedataacrossallsites.Thisexperimentseemstosupportthe explanationasinvasivespeciesgrowinginpotsdidinduceconsi derablealterationsinsoil,butthechangesusuallydifferedbet weensoilsinmagnitudeanddirection.

5 Conclusions

Althoughshort-termpotexperimentsbasedonplantcultiva- tiondonotideallymimicthefieldsituationduetotheirshortdurat ion,lowerplantbiomassandlitterdeposition,and/orrest rictedrootingdepth,theycanbeconsideredavaluablecompl ementofspace-for-timesubstitutionfieldstudies,sim-

ulatingaprimarystageoftheencroachmentofalienplantsonto disturbedbaresoil.Ourexperimentshowedthatthegrowthofin vasiveplantssignificantlyinfluencedmostsoilphysicochemi calproperties.Theinfluencedifferedbothbe-

tweeninvasiveandnativespeciesaswellasamonginvasivespec ies.Themultidirectionaleffectsofdifferentinvadersre- sultedinaconsiderabledivergenceinsoilcharacteristics,mai nlyintotalandavailableformsofNandP,S-SO4,ex-

changeableK,andMg,aswellaspH.Asbiomassproducedbypla ntsgrowinginpotswasgenerallylowandlitterdepo-

sitionnegligible,itmaybesupposedthattheplantsinfluencedsoi lthroughtheexudationofchemicalcompoundsviarootsandnut rientuptake.Suchinvasion-

drivenchangesinthesoilenvironmentmaytriggerfeedbacksth atstabilizeoraccelerateinvasionandhinderre-

colonizationbynativevegetation,whichhasimplicationsforth erestorationofinvadedhabitats.

AcknowledgementsT heauthorsthankAngelikaBanaśandElżbietaChrz anowskafortheirhelpwiththelaboratorywork.

FundingTher e s earchw asf undedb y th e N ationalS cienceC entre,Pola nd,undertheprojectDEC–2011/03/B/NZ8/00008(2012–

16).ItalsoreceivedfinancialsupportfromtheInstituteofBotanyattheJagiel lonianUniversity(K/ZDS/005399,K/ZDS/006305)andtheW.SzaferInst ituteofBotany,PolishAcademyofSciences.

OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCo m mo nsAt tribu t ion4. 0In t ernat iona lLicen se(ht tp://creativecommo ns.org/licenses/by/4.0/),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedyougiveappropriatecredittotheori ginalauthor(s)andthesource,providealinktotheCreativeCommonslicens e,andindicateifchangesweremade.

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