Effect of cold stratification on seed germination in Solidago × niederederi (Asteraceae) and its parental species

(1)

Biologia(2018)73:945–950

https://doi.org/10.2478/s11756-018-0113-7 SHORTCOMMUNICATION

Effectofcoldstratificationonseedgermination

inSolidago×niederederi(Asteraceae)anditsparentalspecies

ArturPliszko¹^&KingaK ostrakiewicz-Gierałt²

Received:27March2018/Accepted:17August2018/Publishedonline:3September2018

#TheAuthor(s)2018

Abstract

Inthisstudy,weinvestigatedtheinfluenceofcoldstratificationonseedgerminationinS.×niederederi,ahybridbetweentheNorthAm ericanS.canadensisandtheEuropeanS.virgaurea,usingfruitsamplescollectedin2016inPoland.Weaimedtotestthehypothesisthatt helowtemperatureexposuredecreasesthefinalpercentageandspeedofseedgerminationinthehybridanditsparentalspecies.Foreac hspecies,setsof100achenesinthreereplicationsweremixedwithdrysandandstoredinPetridishesindarknessfor12weeks,at−18°C and+4°C,and+25°C.Theseedswereincubatedfor21datroomtemperature(+25°C),underthe12hphotoperiod(630lx).Weshoweda lackofsignificantdifferencesin:(i)thefinalpercentageofgerminatedseedsofstudiedspeciesstoredatthesameconditions,

(ii)thefinalpercentageofgerminatedseedsbetweentheappliedstratificationconditionsinthehybridanditsparentalspecies,and(iii)t hemeanvaluesofTimson’sindex,meangerminationtime,andcoefficientofvelocityofgerminationbetweenthestratificationconditi onsineachspecies.Thestatisticallysignificantinter-

specificdifferencesinthemeangerminationtimeparameterafterthe+25°CtreatmentsuggestthattheseedsofS. ×niederederiareabl etogerminatefasterthantheseedsofitsparentalspecies.However,toimproveourknowledgeofnaturalizationandinvasio nabilitiesofS.

×niederederibysexualreproduction,theseedgerminationandseedlingsurvivalofthehybridshouldbetestedinthefield.

KeywordsAlienspecies.Hybrid.Seeddormancy.Timson’sindex

Introduction

Productionofviableseedsisoneofthemostimportantfactorsfac ilitatingthenaturalizationandinvasionsuccessofalienplan tspecies,especiallywhenvegetativereproductiondoesnotexis tinthewildorishighlyrestricted(Pyšeketal.2004;Richardsona ndPyšek2012;BuffordandDaehler2014).Takingintoaccoun tthenaturalhybridsbetweenalienandna-

tiveplantspecies,whicharetreatedasalienspecies(Pyšeketal.

2004),thenaturalizationbysexualreproductionisusuallylimite dbytheirtypicallowpollenviability(DaehlerandCarino2001;

Staceetal.2015).ThegenusSolidagoL.

(Asteraceae)includesmanyinterspecifichybridsthatoccur

innativerangesoftheirparentalspecies(Nesom1994).Neverth eless,therearetwospontaneoushybridsbetweenalienandnative SolidagospeciesrecordedinEurope,namelyS.×niederederiKh ek,a hybridbetweentheNorthAmerican

S.canadensisL.andtheEuropeanS.virgaureaL.

(Nilsson1976;Pliszko2015;PliszkoandZalewska-

Gałosz2016),andS.×snarskisiiGudžinskas&Žalneravičius,a hybridbetweentheNorthAmericanS.giganteaAit.andtheEur opean

S.virgaurea(GudžinskasandŽalneravičius2016).Thenatura lizationofbothhybridsisinsufficientlyrecog-

nizedandsexualreproductionwasconfirmedonlyinS.

×niederederi(GudžinskasandŽalneravičius2016;Pliszkoan dKostrakiewicz-Gierałt2017a,b).Testingseedgermina- tionofhybridsbetweenalienandnativeplantspeciesunder

laboratoryconditionsisimportantforbetterrecognitionof

*ArturPliszko

artur.pliszko@uj.edu.pl

1 DepartmentofTaxonomy,PhytogeographyandPalaeobotany,I nstituteofBotany,JagiellonianUniversity,Gronostajowa3,30- 387Kraków,Poland

2 DepartmentofPlantEcology,InstituteofBotany,JagiellonianUniversit y,Gronostajowa3,30-387Kraków,Poland

(2)

942 Biologia(2018)73:945–950

theirbiologyandmayfindapplicationindevelopingmet hodsoftheircontrol.

Solidago×niederederihasbeenreportedfromsever alcountriesinEurope,includingAustria,Italy,theUnit edKingdom,Sweden,Denmark,Norway,Germany,Po land,Lithuania,Latvia,andRussia(Jaźwaetal.2018andl iteraturecitedtherein).Itisusuallyfoundamongitsparent alspecies,in

(3)

anthropogenichabitatssuchasabandonedfields,disusedquarr ies,roadsideverges,railwayembankments,treeplanta-

tions,andarablefieldswithgrass-

legumemixtures(Nilsson1976;Burton1980;Sunding1989;

Staceetal.2015;GudžinskasandŽalneravičius2016;Pliszkoa ndJaźwa2017;PliszkoandKostrakiewicz-

Gierałt2017a).Itisabletospreadgenerativelybywind-

dispersedachenes;however,itsfruitsetislimitedduetoreducedp ollenviability(Migdałeketal.2014;KarpavičienėandRadušie nė2016)anddependsontheabun-

danceofmatingpartners(includingtheparentalspecies)andpolli nators(Pagitz2016).Furthermore,S.×niederederishowsmostly self-

incompatibilityandthereforeitcanposeathreattonativeS.virgau reasinceitspollinationbiologypromotescross-

hybridizationandintrogression(Pagitz2016).

Interestingly,someauthorssuggestedthatS.canadensisan ditscloselyrelatedcongenersneedtoreceiveacoldstrat- ificationtobreaktheirseeddormancy,whileotherspointedoutt hatthecoldtemperatureexposureisnotrequiredtotrig-

gerseedgermination(Werneretal.1980;Walcketal.1997;Web er2000).Moreover,Milbauetal.(2009)foundnosignif- icanteffectofcoldstratificationonseedgerminationinS.vir gaurea.AccordingtoPliszkoandKostrakiewicz-

Gierałt(2017a,b),seedsofS.×niederedericanreachahighperce nt-

ageofgermination(morethan90%)withnocoldstratificationtre atmentinvolved.However,sincethehybridisanalienspe- ciesandcanposeathreattonativeS.virgaureabycompeti- tionandintrogression,itsseedgerminationbiologyshouldbeid entifiedinmanyrespects.Inthisstudy,therefore,weaimedtoinv estigatetheinfluenceofcoldstratificationonseedger-

minationinS.×niederederianditsparentalspeciesbytestingthe hypothesisthatthelow-

temperatureexposuredecreasesthefinalpercentageandspeed ofseedgermination.

Materialsandmethods

Fruitsamplingandstorage

FruitsamplesofSolidago×niederederi,S.canadensis,andS.virg aureawerecollectedfromnaturalpopulations(onepopu- lationperspecies)occurringonanabandonedfieldinWarsaw,ce ntralPoland(GPScoordinates:52°06.946′N/20°59.534′E;alti tude:104ma.s.l.),onOctober2,2016.Foreachspecies,10panicle s(synflorescences)withmatureacheneswereran-

domlysampled,placedinpaperbags,andtransportedtothelabor atory.Thepaniclesoftheparentalspecieswerecollectedfromthe plantsformingtheclumpslocatedquitefarfromeachother(100m ),incontrasttothepaniclesofthehybridwhichwerecollectedfro mplantslocatedclosetotheparentalspecies(1–

5m).Inthelaboratory,thecollectedpanicleswereleftinadry,airy

place,atroomtemperaturefor7days.Next,thepan-

icleswerethreshedmanuallytoobtainamixtureofachenesforfurthe rinvestigation.Foreachspecies,setsof100achenesin

(4)

threereplicationswererandomlyselectedfromthesamplesvi suallyidentifiedaswell-developedfruits(withnoabnormal- itiesanddamage),usingaPZOWarszawa18,890stereoscopic microscope.Duringanafter-

ripeningperiod,setsof100achenesinthreereplicationswere mixedwith80gofdrysandasasubstrateandstoredin9cmdiame terpolystyrenePetridishesfor12weeksindarkness,underthree temperaturere-gimes,namely−18°C(inafreezer),

+4°C(inafridge),and+25°C(inaroom).

Seedgerminationtes t

AchenesmixedwiththesandandplacedinPetridishes(aspre paredforthestorage)werewettedwith10mlofsterilewater.

Thesubstratewasdistributeduniformlytocreatealayerthickn essofabout0.5cmanditspHvaluewasabout7.0.Theachenesin Petridisheswereincubatedfor21datroomtem-

perature(+25°C),under12hphotoperiod(630lx).Thesub- stratewascomplementedwith1mlofsterilewatereveryotherd ay.Theseedwasdeterminedasgerminatedwhentheperi- carpoftheachenewasbrokenshowingradicle,hypocotylorco tyledons.Duringthegerminationtest,theacheneswere checkedwith1dintervals.

Germinationparamete rs

Thespeedofseedgerminationwasestimatedbasedonthreepar ameters,namelytheTimson’sindex(Timson1965),meanger minationtime(Orchard1977)andcoefficientofvelocityofge rmination(BaskinandBaskin2014),whicharecom- monlyusedintheseedgerminationstudies(Al-

Mudaris1998;BaskinandBaskin2014).Formulasanddescri ptionsoftheseparametersarepresentedinTable1.Ahighvalue oftheTimson’sindexindicatesafastseedgermination,ahighv alueofthemeangerminationtimeindicatesaslowseed germination,andahighvalueofthecoefficientofvelocityof germinationindicatesa rapidseedgermination.TheTimso n’sindexandmeangerminationtimewerecalculatedfora10d seedgerminationtestperiod,whereasthecoefficientofvelocit yofgerminationwascalculatedforatotaltimeofseedgermina tiontestperiod(21d).

Statisticala nalysi s

Thenon-parametricKruskal-WallisHtestwithmultiplecom- parisonswasappliedtocheckiftherearesignificant:(i)inter- speciesdifferencesinthemeanpercentageofgerminatedseed sbet ween Sol idago×ni ede rederi,S.canaden sis,and S.virgaureasubjectedtothesamefruitstoragetreatm ent,

(ii) differencesinthemeanpercentageofgerminatedseedso feachspeciesbetweendifferentfruitstoragetreatments,

(iii) inter-speciesdifferencesinthemeanvaluesofTimson’s index,meangerminationtimeandcoefficientofvelocityof

(5)

Biologia(2018)73:945–950 947

Table1 Detailsofseedgerminationparametersusedinthestudy

Parameter Formulaforcalculation Description

Timson’sindex Σn n–cumulativedailygerminationpercentageforeachdayofthetest

Meangerminationtime Σ(ni×dⁱ)/N ni–numberofseedsgerminatedatdaydⁱ,N–

totalnumberofseedsgerminatedinthetest Coefficientofvelocity

ofgermination 100(A1+A²+…+A^x)/

(A1T1+A²T2+…+A^xTx)

A1+A²+…+A^x–

numberofseedsgerminatedonthefirst,secondandfinaldays thatseedlingsappeared,T1,T2and

Tx–

numberofdaysbetweensowingandfirst,secondandfinaltimesthat seedlingswererecorded

germinationcalculatedforseedssubjectedtothesamefruitstor agetreatment,and(iv)differencesinthemeanvaluesofgermina tionparametersineachspeciesbetweendifferentfruitstoragetr eatments.StatisticalanalysiswasperformedusingaSTATISTI CA13softwarepackage.

Result s

SeedsofSolidago×niederederianditsparentalspeciesstartedtog erminateinthe2ndor3rddayfromthesowingandthenumberofg erminatedseedswasthegreatestwithinthefirstweekofthegermi nationtestperiod,regardlessofstratification

conditions(Fig.1).Thelowestvaluesofthefinalpercentageofger minationwereachievedbyseedsofS.virgaurea,aftereachstratifi cationtreatment.Additionally,itshouldbepointedoutthatthesee dsofS.×niederederiafterthe−18°Ccoldstratifi-

cationpresentedthegreatestgerminationrate(81.3%onaver- age).However,theinter-specificdifferencesinthemeanper- centageofgerminatedseedsstoredinthesameconditionsweresta tisticallyinsignificant,followingtheKruskal-

WallisHtest(Table2).Moreover,thedifferencesinthemeanperc entageofgerminatedseedsbetweentheappliedfruitstoragecond itionswerestatisticallyinsignificantinthehybrid(H=0.8,P=0.6) anditsparentalspecies(H=0.8,P =0.6forS.canadensisandH =1 .7,P =0.4forS.virgaurea).

(6)

946 Biologia(2018)73:945–950 Fig.1Cumulativenumberandpercentageofgerminatedseeds(greycircles)andminimalandmaximalvalues(whiskers)inSolidago×niederederianditsparentals pecies,following−18°C(A),+4°C(B),and+25°C(C)stratificationtreatments,basedonthreereplications

(7)

Table2

Thestatisticalsignificanceofdifferencesinthemeanpercentage(range)ofgerminatedbetweenSolidago×niederederianditsparentalspeciessubjectedtothreestr atificationtreatments,b asedon threereplications

Temperatureofstratifi

cationt reatment Taxon Meanpercentageofgerminatedseeds Thelevelofstatisticalsignificance

−18°C Solidago×niederederi 81.3(74–87) 3.5;P=0.2

Solidagocanadensis 74.3(50–94) Solidagovirgaurea 56.7(37–69)

+4°C Solidago×niederederi 76.0(68–83) 2.3;P=0.3

+25°C Solidago×niederederi 80.7(74–89) 3.5;P=0.2

ThehighestmeanvaluesofTimson’sindex(535.0)andcoef ficientofvelocityofgermination(23.4)werenoticedin

S.×niederederisubjectedtothe+4°Ccoolstratification, whereasthehighestmeanvalueofthemeangerminationtimewas noticedinS.virgaureasubjectedtothe−18°Cand+25°Cstoraget reatments(Table3).However,thedifferencesinthemeanvalues ofgerminationparametersbetweentheappliedfruitstoragecon ditionswerestatisticallyinsignificantineachspecies,accordingt otheKruskal-WallisHtest(Table3).Ontheotherhand,theinter- specificdifferencesinthemeanvalueofTimson’sindex,meanger minationtime,andcoefficientofvelocityofgerminationinpartic ulartypesoffruitstoragecon-

ditionswerestatisticallyinsignificant,exceptthemeangermi- nationtimeafterthe+25°Cstratificationtreatment(Table3).

Discussion

Consideringtheresultsobtainedinthisstudy,wemustrejectour hypothesisthatthecoldstratificationdecreasesthefinal

percentageandspeedofgerminationinSolidago× niedere derianditsparentalspecies.Nonetheless,alackofinfluenceo fcoldstratificationonfinalpercentageofseedgerminati oninS.canandensiscorrespondswiththefindingsprovidedby Werneretal.

(1980).Moreover,theoutcomesoftheperformedstudiessuppo rttheobservationsmadebyMilbauetal.

(2009)whonoticedthatthecoldstratificationhasnoeffectonth efinalpercentageofgerminatedseedsinS.virgaurea.Additional ly,Bocheneketal.

(2016)showedthatthehighseedvigorinS.giganteaAit.,aspecie scloselyrelat-

edtoS.canadensis,wasmaintainedafterthestorageinawideran geoftemperatures,inbothdryandmoistconditions.Inlightof aforementionedstudies,itmightbestatedthatthespecies, whoseseedsgerminateeasily(regardlessofstorageconditions ),possessthecompetitiveadvantageoverthespe-

ciesrequiringspecificconditionstobreaktheirseeddorman- cy.SuchabilityseemstobeanattributeofS. ×niederederiandmay facilitateitsnaturalizationbysexualreproductioninnewareas.

Ontheotherhand,itshouldbementionedthatthereareseveralstu diesprovingthatthecoldstratificationbreaks

Table3 Themean(range)valuesofseedgerminationparametersinSolidago×niederederianditsparentalspeciesafterthreestratificationtreatments SeedgerminationparameterTaxon Temperatureofstratificationtreatment

Thelevelofstatisticals ignificance

−18°C +4°C +25°C

Timson’sindex Solidago×niederederi 535.0(467–600) 430.6(401–490) 518.7(437–617) H=3.31^ns Solidagocanadensis 481.7(213–663) 406.3(174–553) 393.3(181–500) H=1.7^ns Solidagovirgaurea 341.7(135–453) 300.0(198–438) 241.3(114–315) H=0.8^ns Thelevelofstatisticalsignificance H=3.3^ns H=1.7^ns H=4.4^ns

Meangerminationtime Solidago×niederederi 4.0(3.4–4.5) 4.3(3.8–4.7) 4.2(4.0–4.3)^a H=0.6^ns Solidagocanadensis 3.9(3.6–4.5) 5.2(4.4–6.5) 5.3(4.9–5.8)^b H=4.6^ns Solidagovirgaurea 4.7(4.1–5.7) 5.6(5.2–6.0) 5.6(5.0–6.2)^b H=1.7^ns Thelevelofstatisticalsignificance H=3.5^ns H=1.4^ns H=5.7*

(8)

Coefficientofvelocity Solidago×niederederi 23.4(16.6–28.0) 18.1(14.7–20.8) 21.4(19.0–24.1) H=2.5^ns ofgermination Solidagocanadensis 21.1(12.6–25.6) 16.3(11.0–20.3) 17.2(13.5–19.2) H=1.1^ns Solidagovirgaurea 21.5(14.5–28.1) 16.7(15.4–17.7) 16.8(14.5–18.5) H=0.9^ns Thelevelofstatisticalsignificance H=0.7^ns H=0.4^ns H=4.6^ns

(9)

Biologia(2018)73:945–950 949

dormancyandimprovestheseedgerminationinS.altissimaL., S.nemoralisAit.(Walcketal.1997,2000),S.petiolarisAit.

(Bratcheretal.1993),S.sempervirensL.

(Lonardetal.2015)andS.shortiiTorr.&Gray(Bucheleetal.199 1;Walcketal.1997,2000).Furthermore,theimportanceofcold strat-

ificationwasconfirmedinmanyspeciesoftheAsteraceae.For example,thecoldstratificationbreaksseeddormancyinEchina ceaangustifoliaDC.

(Baskinetal.1992),PolymniacanadensisL.

(Ben deret al .2003),Gui zotiasca bra(Vis.)Chiov.,Parthe niumhysterophorusL.,Verbesinaencelioides(Cav.)Benth.&

Hook.f.exA.Gray(Karlssonetal.2008),aswellasTripleurosper mummaritimum(L.)W.D.J.Koch(Bocheneketal.2010),whil eamoderatethermalstratificationhasapositiveinfluenceonse edgerminationinCirsiumarvense(L.)Scop.

(Bocheneketal.2009).

Interestingly,ourresultssuggestthatS.×niederedericanrea chmuchhighervaluesofthefinalpercentageofseedger- minationthanevidencedbyPagitz(2016)andcorrespond withthepreviouslypublisheddata(PliszkoandKostraki ewicz-Gierałt2017a,b).Moreover,thefinalpercent-

ageofgerminatedseedsinS.canadensiswasalsohigherthanevi dencedbyotherauthors(Huangetal.2007)andalowfinalpercent ageofseedgerminationinS.virgaureacorrespondswiththeres ultsprovidedbyGiménez-Benavidesetal.

(2005).Atthesametime,itshouldbepointedoutthatthehighper -

centageofgerminatedseedsmaynotresultinaconsiderableabu ndanceofadultindividuals.GoldbergandWerner(1983)showe dthatinthecloselyrelatedS.altissimatheseedlinggrowthan dtheirprobabilityofsurvivalincreasedwiththediameterof theopeninginthevegetation.Basedonlaboratoryobservatio ns,Houetal.(2014)evidencedthecon-

siderablemortalityofseedlingsinmanyinvasivespeciesfromth eAsteraceaefamily(e.g.,EupatoriumcatariumVeldkamp,Age ratumconyzoidesL.,TridaxprocumbensL.,Mikaniamicrant haKunth,andSynedrellanodiflora(L.)Gaertn.)ineffectoflo wtemperatures.Findingsofnumerousauthorsshowedthatthe unfavorableweatherconditionsmayleadtoalossofseedlingsin thewild.Forexample,thesowingex-

perimentsconductedbyPolletal.

(2008)inthefieldshowedtheslightsurvivalofseedlingsofS.ca nadensis,Conyzacanadensis(L.)C ronquist,andMatricariadi scoideaDC.Furthermore,thesuppressionofseedlingestablish mentinef-

fectofseveredroughtorstronglatefrostwasnoticedininva- siveF al l op i a j aponi ca (H ou t t .) R o n s e D ec r.

(Engl er e t a l .2011;Funkenbergetal.2012;FormanandKess eli2003).

IncomparisontoWalcketal.(1997),whoevidencedthatin S.altissima,S.nemoralis,andS.shortii,theeffectofstratifi- cationtreatmentonTimson’sindexwasspecies-

specific,wefoundnosignificantdifferenceintheTimson’sind

exvaluebetweenS.×niederederianditsparentalspecies(Table 3).However,regardingthestatisticallysignificantinter- specificdifferencesinthemeangerminationtimeparameterafter the

+25°Ctreatment(Table3),itshouldbestatedthattheseedsof

(10)

Biologia(2018)73:945–950 950

S.×niederederiareabletogerminatefasterthantheseedsofitsp arentalspecies.Ontheotherhand,similarlyto

S.altissima,S.nemoralis,andS.shortii(Walcketal.1997),the greatestnumberofgerminatedseedsinthehybridanditsparent alspecieswasnoticedinthefirstweekofincubation(Fig.1).T obemorecriticalofourresults,werealizethatinthewild,thefina lpercentageofgerminatedseedsandspeedofseedgerminatio ninS.×niederederimaybeverydifferentfromthoseobserve dinthelaboratory,therefore,itshouldbetestedinthefieldaspoi ntedoutbyGioriaandPyšek(2017).Finally,manyotheraspect sofseedecologyofthehybridsuchastolerancetodrought,persi stenceinthesoilseedbank,andinteractionswiththesoilmicro organismsseemtobeinterest-

ingtopicsforfurtherinvestigationonitsnaturalizationandin vasionabilities.

AcknowledgementsWewouldliketothanktheReviewersforvaluable commentsandsuggestionsonourmanuscript.Theresultspresentedinthi spaperwereobtainedwithfinancialsupportfromtheInstituteo fBotanyoftheJagiellonianUniversityinKraków(K/ZDS/006305).

Compliancew ithe thicalstandards

Conflictof interestTheauthorsdeclaret hattheyh aven o conflictofinterest .

OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCo mmo nsAt tribu t ion4. 0In t ernat iona lLicen se(ht tp://creativeco mmons.org/licenses/by/4.0/),whichpermitsunrestricteduse,distributi on,andreproductioninanymedium,providedyougiveappro-

priatecredittotheoriginalauthor(s)andthesource,providealinktotheCre ativeCommonslicense,andindicateifchangesweremade.

Reference s

Al-

MudarisMA(1998)Notesonvariousparametersrecordingthespee dofseedgermination.DerTropenlandwirtBeiträgezurtropischen LandwirtschaftundVeterinärmedizin99:147–154

BaskinCC,BaskinJM,HoffmanGR(1992)Seeddormancyintheprairief orbEchinaceaangustifoliavar.angustifolia(Asteraceae):after ripeningpatternduringcoldstratification.IntJPlantSci153(2):239 –243.h ttps://doi.org/10.1086/297027

BaskinCC,BaskinJM(2014)Seeds:ecology,biogeographyandevolu- tionofdormancyandgermination.Ed.2,AcademicPress/Elsevier,S anDiego

BenderMH,BaskinJM,BaskinCC(2003)SeedgerminationecologyofP olymniacanadensis(Asteraceae),amonocarpicspeciesof thenorthAmericantemperatedeciduousforest.PlantEcol168:22 1–253.https://doi.org/10.1023/A:1024437510330

BochenekA,GołaszewskiJ,Piotrowicz-

CieślakAI,GóreckiRJ(2009)Theeffectsoftemperatureonthedo rmancyandgerminationofCirsiumarvenseseeds.ActaSocBotPo l78:105–114.https://doi.org/10.5586/asbp.2009.014

BochenekA,GołaszewskiJ,GiełwanowskaI(2010)Ahydrotimemodela nalysiso f M a t r icariam a r itimas u b s p.i n o d oras ee d d o r m anc y.PlantSpecBiol25:136–148

BochenekA,SynowiecA,KondratB,SzymczakM,LahutaLB,Gołasz ewskiJ(2016)DotheseedsofSolidagogiganteaAitonhave

(11)

physiologicaldeterminantsofinvasiveness?

ActaPhysiolPlant38(159).https://doi.org/10.1007/s11738-016- 2179-6

BratcherCB,DoleJM,ColeJC(1993)Stratificationimprovesseedger- minationoffivenativewildflowerspecies.HortScience28:899–

901BucheleDE,BaskinJM,BaskinCC(1991)Ecologyoftheendangereds peciesSolidagoshortii.III.Seedgerminationecology.BullTorrey BotClub118:288–291

BuffordJL,DaehlerCC(2014)Sterilityandlackofpollinatorservicesexpl ainreproductivefailureinnon-

invasiveornamentalplants.DiversDistrib20:975–

985.https://doi.org/10.1111/ddi.12224

BurtonR(1980)Solidago×niederederiKhekinBritain.Watsonia13:123 –124

DaehlerCC,CarinoDA(2001)Hybridizationbetweennativeandalienplan tsanditsconsequences.In:LockwoodJL,McKinneyML(eds)Biotic homogenization.Kluweracademic/plenum.Publishers,NewYork, pp81–102

EnglerJ,AbtK,BuhkC(2011)Seedcharacteristicsandgerminationlimit ationsinthehighlyinvasiveFallopiajaponicas.l.

(Polygonaceae).EcolRes26:555–

562.https://doi.org/10.1007/s11284-011-0813-8

FormanJ,KesseliRV(2003)SexualreproductionintheinvasivespeciesFal lopiajaponica(Polygonaceae).AmJBot90:586–

592.https://doi.org/10.3732/ajb.90.4.586

FunkenbergT,RoderusD,BuhkC(2012)EffectsofclimaticfactorsonFallo piajaponicas.l.Seedlingestablishment:evidencefromlabo- ratoryexperiments.PlantSpecBiol27(3):218–

225.https://doi.org/10.1111/j.1442-1984.2011.00349.x Giménez-BenavidesL,EscuderoA,Pérez-GarcíaF(2005)Seedgermi-

nationofhighmountainMediterraneanspecies:altitudinal,inter- populationandinterannualvariability.EcolRes20:433–

444.https://doi.org/10.1007/s11284-005-0059-4

GioriaM,PyšekP(2017)Earlybirdcatchestheworm:germinationasacriti calstepinplantinvasion.BiolInvasions19:1055–

1080.https://doi.org/10.1007/s10530-016-1349-1

GoldbergDE,WernerPA(1983)Theeffectsofsizeofopeninginvege- tationandlittercoveronseedlingestablishmentofgoldenrods(Soli dagospp.).Oecologia60:149–155

GudžinskasZ,ŽalneravičiusE(2016)Solidago×snarskisiinothosp.nov.

(Asteraceae)fromLithuaniaanditspositionintheinfragenericclas- sificationofthegenus.Phytotaxa253:147–

155.h ttps://doi.org/10.11646/phytotaxa.253.2.4 HouQ-Q,ChenB-M,PengS-L,ChenL-

Y(2014)Effectsofextremetemperatureonseedlingestablishmentof nonnativeinvasiveplants.BiolInvasions16:2049–

2061.https://doi.org/10.1007/s10530-014-0647-8

HuangH,GuoSL,ChenGQ(2007)Reproductivebiologyinaninvasiveplan tSolidagocanadensis.FrontBiolChina2:196–

204.https://doi.org/10.1007/s11515-007-0030-6

JaźwaM,JędrzejczakE,KlichowskaE,PliszkoA(2018)Predictingthepot entialdistributionareaofSolidago×niederederi(Asteraceae).TurkJ Bot42:51–56.https://doi.org/10.3906/bot-1703-17

KarlssonL,TamadoT,MilbergP(2008)Interspeciescomparisonofseeddo rmancyandgerminationofsixannualAsteraceaeweedsinanecolog icalcontext.SeedSciRes18:35–

45.https://doi.org/10.1017/S0960258508888496

KarpavičienėB,RadušienėJ(2016)Morphologicalandanatomicalchar- acterizationofSolidago×niederederiandothersympatricSolidagosp ecies.WeedSci64:61–70.https://doi.org/10.1614/WS-D-15- 00066.1

LonardRI,JuddFW,StalterR(2015)Thebiologicalfloraofcoastaldune sandwetlands:SolidagosempervirensL.andSolidagosempervire nsL.subsp.mexicana(L.)Semple.JCoastRes31:1512–

1520.h ttps://doi.org/10.2112/JCOASTRES-D-14-00261.1

MigdałekG,KolczykJ,PliszkoA,Kościńska-

PająkM,SłomkaA(2014)Reducedpollenviabilityandachenedevelo pmentinSolidago

(12)

×niederederiKhekfromPoland.ActaSocBotPol83:251–255.

https://doi.org/10.5586/asbp.2014.0 25

MilbauA,GraaeBJ,ShevtsovaA,NijsI(2009)Effectsofawarmerclim ateonseedgerminationinthesubarctic.AnnBot104:287–

296.https://doi.org/10.1093/aob/mcp11 7

NesomG(1994)HybridizationinthetribeAstereae(Asteraceae).

Phytologia77:298–

307

NilssonA (1976)Spontanagullrishybrider(Solidagocanadensis×

virgaurea)iSverigeochDanmark.SvenBotTidskr70:7–

16OrchardT(1977)Estimatingtheparametersofplantseedlingemergen ce.

SeedSciTechnol5:61–

69

PagitzK(2016)Solidago×niederederi(S.canadensis×S.virgaureassp.v irgaurea)intheEasternAlps.In:RiesC,KrippelY(eds)BiolInva sions:interactionswithenvironmentalchange.Bookofab- stracts.NEOBIOTA2016–

9^thInt

ernationalConferenceonBiologicalInvasions.Vianden,Lu xembourg,pp.194

PliszkoA(2015)NeotypificationofSolidago×niederederi(Asteraceae).

Phytotaxa230:297–

298.https://doi.org/10.11646/phytotaxa.230.3.

1 0

PliszkoA,JaźwaM(2017)Floristiccompositionofvegetationinhabitatss uitableforErigeron×huelsenii(Asteraceae).ActaBotCroat76:9–

14.https://doi.org/10.1515/botcro-2016-0040

PliszkoA,Kostrakiewicz-GierałtK(2017a)Resolvingthenaturalization strategyofSolidago×niederederi(Asteraceae)bytheproductionofs exualrametsandseedlings.PlantEcol218:1243–

1253.https://doi.org/10.1007/s11258-017-0762-6 PliszkoA,Kostrakiewicz-GierałtK (2017b)Seedgerminationin

Solidago×niederederi(Asteraceae)anditsparentalspeciesaftert wodifferentfruitstorageperiods.BiodivResConserv48.https://doi .org/10.1515/biorc-2017-0013

PliszkoA,Zalewska-GałoszJ(2016)Molecularevidenceforhybridiza- tionbetweeninvasiveSolidagocanadensisandnativeS.virgaurea.

BiolInvasions18:3103–3108.https://doi.org/10.1007/s10530- 016-1213-3

PollM,NaylorBJ,AlexanderJM,EdwardsPJ,DietzH(2008)Seedlingest ablishmentofAsteraceaeforbsalongaltitudinalgradients:acom- parisonoftransplantexperimentsinthenativeandintroducedrang es.DiversityDistrib15:254–265.10.1111/j.1472- 4642.2008.00540.x

PyšekP,RichardsonDM,RejmánekM,WebsterGL,WilliamsonM, KirschnerJ(2004)Alienplantsinchecklistsandfloras:towardsbe ttercommunicationbetweentaxonomistsandecologists.Taxon53 :131–143

RichardsonDM,PyšekP(2012)Naturalizationofintroducedplants:

ecologicaldriversofbiogeographicalpatterns.NewPhytol196:

383–396.h ttps://doi.org/10.1111/j.1469-8137.2012.04292.x StaceCA,PrestonCD,PearmanDA(2015)HybridfloraoftheBritish

Isles.BotanicalSocietyofBritainandIreland,Bristol SundingP(1989)NaturaliserteSolidago-

(gullris-)arteriNorge.Blyttia47:23–27

TimsonJ(1965)Newmethodofrecordinggerminationdata.Nature207:

216–

217.https://doi.org/10.1038/207216a0

WalckJL,BaskinJM,BaskinCC(1997)Acomparativestudyoftheseedg erminationbiologyofanarrowendemicandtwogeographically- widespreadspeciesofSolidago(Asteraceae).1.Germinationphe- nologyandeffectofcoldstratificationongermination.SeedSciRes7 :47–58.https://doi.org/10.1017/S0960258500003366

WalckJL,BaskinJM,BaskinCC(2000)Increasedsensitivitytogreenlig htduringtransitionfromconditionaldormancytonondormancyins

eedsofthreespeciesofSolidago(Asteraceae).SeedSciRes10:495–

499.https://doi.org/10.1017/S0960258500000532

WeberE(2000)BiologicalfloraofCentralEurope:SolidagoaltissimaL.

Flora195:123–

134

WernerPA,GrossRS,BradburyIK(1980)ThebiologyofCanadianwee ds:45.SolidagocanadensisL.CanJPlantSci60:1393–

1409.https://doi.org/10.4141/cjps80-194