Impacts of warming and changes in precipitation frequency on the regeneration of two Acer species

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Contents lists available atScienceDirect

Flora

j o u r n a l h o m e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / f l o r a

Impacts

of

warming

and

changes

in

precipitation

frequency

on

the

regeneration

of

two

Acer

species

M.M.

Carón

a,∗

_,

_P.

_De

_Frenne

a

_,

_O.

_Chabrerie

b

_,

_S.A.O.

_Cousins

c

_,

_L.

_De

_Backer

d

_,

_G.

_Decocq

b

_,

M. Diekmann

e

_,

_T.

_Heinken

f

_,

_A.

_Kolb

e

_,

_T.

_Naaf

g

_,

_J.

_Plue

c

_,

_F.

_Selvi

h

_,

_G.R.

_Strimbeck

i

_,

M. Wulf

g

_,

_K.

_Verheyen

a

a_Forest_&_Nature_Lab,_Ghent_University,_{Gontrode-Melle,}_Belgium

b_Jules_Verne_University_of_Picardie,_UR_Ecologie_et_Dynamique_des_Systèmes_Anthropisés_(EDYSAN,_FRE₃₄₉₈_CNRS-UPJV),₁_rue_des_Louvels,_F-80037

AmiensCedex1,France

c_Department_of_Physical_Geography_and_Quaternary_Geology,_Stockholm_University,_Stockholm,_Sweden d_Sylva_nurseries_BVBA,_Waarschoot,_Belgium

e_Vegetation_Ecology_and_Conservation_Biology,_Institute_of_Ecology,_FB2,_University_of_Bremen,_Bremen,_Germany f_Biodiversity_and_Systematic_Botany,_Institute_of_Biochemistry_and_Biology,_University_of_Potsdam,_Potsdam,_Germany g_Institute_of_Land_Use_Systems,_{Leibniz-Centre}_for_Agricultural_Landscape_Research_(ZALF)_Müncheberg,_Germany

h_Department_of_Agrifood_Production_and_{Environmental}_Sciences,_Section_of_Soil_and_Plant_Sciences_University_of_Florence,_Firenze,_Italy i_Department_of_Biology,_Norwegian_University_of_Science_and_Technology,_Trondheim,_Norway

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received16September2014 Receivedinrevisedform20May2015 Accepted21May2015

Availableonline22May2015

Keywords: Seedprovenance Germination Climatechange Interactiveeffects

a

b

s

t

r

a

c

t

Climateprojectionsindicatethattemperatureswillincreasebyupto4.5◦_C_in_Europe_by_the_end_of

thiscentury,andthatmoreextremerainfalleventsandlongerinterveningdryperiodswilltakeplace. Climatechangewilllikelyaffectallphasesofthelifecycleofplants,butplantreproductionhasbeen suggestedtobeespeciallysensitive.Here,usingacombinationofapproaches(soilheatersanddifferent provenancesalongalatitudinalgradient),weanalyzedtheregenerationfromseedsofAcerplatanoides andA.pseudoplatanus,twotreespeciesconsidered,fromamanagementpointofview,ofsecondary rel-evance.Westudiedgermination,seedlingsurvivalandgrowthinafull-factorialexperimentincluding warmingandchangesinwateringfrequency.Bothspeciesrespondedtowarming,wateringfrequency andseedprovenance,withstronger(negative)effectsofwarmingandprovenancethanofwatering frequency.Ingeneral,thecentralprovenancesperformedbetterthanthenorthernmostand southern-mostprovenances.Wealsodetectedinteractiveeffectsbetweenwarming,wateringfrequencyand/or seedprovenance.Basedontheseresults,bothspeciesareexpectedtoshowdissimilarresponsestothe changesinthestudiedclimaticfactors,butalsotheimpactsofclimatechangeonthedifferentphases ofplantregenerationmaydifferindirectionandmagnitude.Ingeneralincreasesintheprecipitation, frequencywillstimulategerminationwhilewarmingwillreducesurvivalandgrowth.Moreover,the frequentdivergentresponsesofseedlingsalongthelatitudinalgradientsuggestthatclimatechangewill likelyhaveheterogeneousimpactsacrossEurope,withstrongerimpactsinthenorthernandsouthern partsofthespecies’distributionranges.

1. Introduction

Depending on the concentration-driven scenario considered (suiteofgreenhousegases,aerosolsandchemicallyactivegases),a futureincreaseoftheaverageannualtemperaturebetween0.6◦C

∗ Correspondingauthor.Tel.:+3292649036·

E-mailaddresses:MariaMercedes.Caron@UGent.be,mechicaron@gmail.com (M.M.Carón).

and4.5◦CisexpectedinEuropebytheendofthiscentury(IPCC, 2013).Theprojectionspredictthatthewintermeantemperature will risemore in NorthernEurope than in Central Europe and theMediterraneanareawhilethesummerwarmingwilllikelybe moreintenseintheMediterraneanareaandCentralEuropethan inNorthernEurope(Christensenetal.,2013).Extremeeventsof warmingarealsoexpected;thelength,frequency,and/or inten-sityofwarmperiodsareexpectedtoincrease(IPCC,2013).Asa consequenceofglobalwarming,thewatercycleisalsoexpected tochangenon-uniformly.Precipitationfrequencieswillbelikely http://dx.doi.org/10.1016/j.ﬂora.2015.05.005

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modiﬁed,withmoreextremerainfalleventsandlongerdry inter-vals(Chaoyangetal.,2012;IPCC,2012,2013).However,notonly thechangesinindividualfactorswillbeimportantinthefuture.The interactionbetweendifferentclimaticfactorscanproducedifferent impactsonterrestrialecosystemscomparedtotheeffectsof indi-vidualfactors;forexample,thecombinationofdrought,extreme heatand/orlowhumiditywillclearlyhavestrongerimpactsthan anyfactoralone(IPCC,2012,2013).Additionally,changesin cli-maticfactorscaninducechangesinotherabioticenvironmental factors.Forinstance,soilmoistureistheresultofacombination ofdifferentabioticfactorssuchasprecipitation,temperature,air humidity,soiltextureandorganicmattercontent(Wang,2005; Chaoyangetal.,2012;Schneideretal.,2014).

Eventhoughthechangesinclimaticdriversandotherrelated abioticaspectsareexpectedtobelargerattheendofthecentury, theeffectsofcurrentglobalwarmingarealreadyvisibleinseveral ecosystems(Hedhlyetal.,2008;VanMantgemetal.,2009)and affecttheecologyofmanyspecies,includingtheirgeographical dis-tribution,phenology,bioticinteractionsandextinctionrisks(fora reviewseePe ˜nuelasetal.,2013).Temperaturehasbeenshownto inﬂuenceseedproduction(Walcketal.,2011;Carónetal.,2014a), germination,establishment(Lewisetal.,1999;Jensen,2001)and growthofplants(Rappetal.,2012).Rainfallamountorsoilmoisture contentmayaffectplantdistributions(Northetal.,2005),seed ger-mination(Fay&Schultz,2009,b;Carónetal.,2014a,b),growth(Fay andSchultz,2009;Dreesenetal.,2012),phenology(Seghierietal., 2009),andmortality(Andereggetal.,2013).However,changesof differentclimaticfactorshavenotreceivedthesamelevelof atten-tion.Forinstance,theimpactsofchangesinprecipitationfrequency arerarelyassessed(butseee.g.Fayetal.,2003;Chaoyangetal., 2012;Schneideretal.,2014).Precipitationfrequencymaychange separatelyfromrainfalltotalswhenthetotalamountofrainfall overacertainperiodremainsconstant,butthenumberof rain-falleventsdecreasesandtheprecipitationamountineachrainfall eventincreases.Someofthefewavailablestudiesonplantshave shownthatreducedrainfallfrequenciescanincreaseproductivity, decreaseroot-to-shootratiosoraffectleaf senescencein grass-landspecies(Fayetal.,2003,2002;Schneideretal.,2014).Yet, moreresearchisurgentlyneededtobetterunderstandtheeffectof changesinprecipitationfrequencyonotherplantgrowth parame-ters,functionalgroups,andecosystems(Schneideretal.,2014).

Even though climate change will likely affect all plant life cyclephases,plantreproductionhasbeensuggestedtobe espe-ciallysensitive(Hedhlyetal.,2008;Walcketal.,2011).Inmany cases,warminghasbeenshowntopositivelyinﬂuenceseed ger-mination (Milbau et al., 2009; McCarragher et al., 2011) or to enhanceseedlingsurvivalandgrowth(Piperetal.,2013).In con-trast,reducedsoilmoisturecontentstendtonegativelyaffectseed germinationandseedlingsurvivalandgrowth(FayandSchultz, 2009;Shevtsovaetal.,2009).Informationabouttheimpactsof cli-matechangeonregenerationfromseedsisessentialfortreespecies becauseitisthemostcommonnaturalwaythroughwhichforests regeneratearoundtheglobe.Inpractice,themajorityoftreespecies usedforafforestationorreforestationinEuropearegrownfrom seeds(DenOudenetal.,2010).ThroughoutEurope,youngtreesthat areusedforreforestationandafforestationgenerallycomefroma poolofrecommendedand/orautochthonousprovenances(cf.the EUDirective1999/105/EConthemarketingofforestreproductive material).However,onlyverylimitedinformationisavailableon howtheserecommendedprovenanceswillperformunderfuture climaticconditions.

Here,weanalyzetheeffectsofwarmingandchangedwatering frequencyonregenerationfromseedsoftwoimportant,currently secondarytreespeciesinforestmanagement,namelyA.platanoides andA.pseudoplatanus.Bothspeciesmightbecomemoreabundant inthecontextofclimatechangeduetotheprojected

composi-tionalchangeinEuropeanforestsasaconsequenceofthedecline inﬁtnessandabundanceofcurrentlyprimaryspeciessuchasPicea abiesand Fagus sylvatica(Hanewinkelet al.,2012).We analyze theimpactsofwarmingandchanges inprecipitationfrequency (assimulatedbyvariouswateringintervals)ongerminationand earlyestablishmentofthesetwoAcerspeciesfromdifferent Euro-peanprovenances.Avarietyoftechniquesareavailabletostudy theeffectsofclimatechangeonplantspeciesincludingsoilheating cables,opentopchambers,growthchambers,andnaturalclimatic gradientssuchasthoseacrosslatitudesorelevations(Carónetal., 2015;DeFrenneetal.,2013;Deinesetal.,2007;DunnettandGrime, 1999).Thetechniqueselectedineachcasedependsonseveral fac-torsincludingthelifecyclephasethatisbeinginvestigated.Here, wecombinetheuseofsoilheatingmats(Carónetal.,2014a)with seedcollectionalongalatitudinalgradient(FukamiandWardle, 2005;De Frenneetal.,2013).Thecombinationof various tech-niquesconstitutesaninterestingstepfurther,relativetotheuse ofonlyonetechniquebecauseitallowstoilluminatetheimpacts ofclimatechangeondifferentaspectsofplantpopulationssuchas differentphasesofplantreproduction(DeFrenneetal.,2013).

We speciﬁcallyaddress(i)Howdo warmingand changesin wateringfrequencyaffectseedgermination,seedlingsurvivaland growth?(ii)Isthereaninteractingeffectofwarmingandwatering frequencyontreespecies’regeneration?(iii)Isthereavariation intheseedandseedlingsresponsetochangesintemperatureand wateringfrequencyaccordingtotheprovenanceoftheseeds?We hypothesizethattheseedsandseedlingsfrommothertreesfrom southernprovenanceswillbeabletobettercopewithinteractive warmingandlessfrequentwateringthantheseedsandseedlings from mother trees growingunder colder and wetter northerly conditions. Additionally, we expect that warming willenhance seedlingsurvivalandgrowthandthatmorefrequentwateringwill stimulategermination.

2. Materialandmethods 2.1. Studyspecies

AcerplatanoidesL.andA.pseudoplatanusL.aretwosecondary foresttreespeciesthatcurrentlycover≤3%ofthetotalforestcover in Europein purestands(Spieckeretal.,2009).However,both speciesarelikely tobecomemoreabundantandimportantdue toaclimatechange-drivendecreaseinﬁtnessandabundanceof currentlyprimaryforesttreespecies(Hanewinkeletal.,2012).

BothspecieshavearelativewidedistributioninEuropeand sim-ilarsoilrequirements.Bothspeciescangrowonloamyandclayey soilsaslongasthesearerichinnutrients.Additionally,thestudy species showphenologicaland morphologicalsimilarities: They ﬂowerinApril,areinsectpollinated,andthewind-dispersedseeds ripeninSeptember–October(ForestEcology&ForestManagement Group,2005).

Acerpseudoplatanusisnaturallydistributedacrosswestern, cen-tralandsouthern Europe(ForestEcology &ForestManagement Group,2005).Thisspecieshasmoderatesiterequirements(Krabel andWolf,2013)ismediumshadetolerantandmediumdrought tolerant.Thisspecieshasa wideecologicalamplitudeand high reproductivecapacity(KrabelandWolf,2013).Itswide ecologi-calamplitudeandhighreproductivecapacityexplainthepotential expansiontosomeEuropeanareassuchasSwedenandNorway (WeidemaandBuchwald,2010;KrabelandWolf,2013).

A.platanoidesisanativespeciesinnorthernandcentralEurope, intheKaukasusandTurkey(ForestEcology&ForestManagement Group,2005).Thisspeciesisconsideredmoreshadetolerantthan A.pseudoplatanus.SomeauthorsindicatethatA.platanoidesand A.pseudoplatanusaresimilarlydroughttolerant(ForestEcology&

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Fig.1.Locationofthecountries/regionsofseedcollectionofAcerplatanoidesandA. pseudoplatanusalongalatitudinalgradient.

ForestManagementGroup,2005), while othersconsiderA. pla-tanoidesmore droughttolerantthan A.pseudoplatanus (Hemery etal.,2009).Itsrobustgrowthandhighshadetolerancemakethis speciesanimportantinvasivespecies,especiallyinNorthAmerica (Martin,1999).

Withongoing climate change,both species are expected to movetheirdistributionrangenorthwardsandtohigherelevations (Hemeryetal.,2009).Moreover,itislikelythatthesusceptibilityto pathogenswillincreasewithstressbyintensewarmanddry con-ditions(Hemeryetal.,2009).Takingintoaccountthatthespecies mightbedifferentlysusceptibletodrought,divergentresponsesto theprojecteddryersummerconditionsmaybeexpected,including topshootdiebackandprematuremortality(Hemeryetal.,2009). Moreover,itisknownthatbothAcerspeciesdonotshow identi-calgrowthandwatereconomy.GrowthofstemandleavesofA. platanoidesisfasterthaninA.pseudoplatanus,andA.platanoides consumeslesswaterperunitofleafareathanA.pseudoplatanus (Braun,1977).Itisthusverylikelythatthesespecieswillbeaffected differentlybyclimatechange.Changesinthesoilmoisturecontent mightalsodifferentlyaffecttheseedsbecausetheseedsofA. pla-tanoidesareconsideredorthodox(desiccation-tolerant),whileA. pseudoplatanus’seedsarerecalcitrant(desiccationsensitive)(Hong andEllis,1990).Alsodormancybreak mightbeaffectedby cli-matechange,aswarmingmayreducethenumberofcolddays.A. platanoidesrequiresapproximately105daysofcoldstratiﬁcation, whileA.pseudoplatanusonlyneeds49–63days(BaskinandBaskin, 1998).Finally,A.platanoidesshowsaninhibitionofgermination attemperaturesabove10–15◦C, butcangerminateaftera sec-ondchillingperiod(Jensen,2001),whileA.pseudoplatanusshows verygoodgerminationathightemperaturessuchas25◦C(Jinks etal.,2006).Thisdissimilarbehaviourunderlinestherelevanceof studyingtheresponsetoclimatechangeofcloselyrelatedspecies, avoidingimproperconclusionsforthegenuslevel.

2.2. Experimentaldesign

SeedsofA.platanoidesandA.pseudoplatanuswerecollectedin 2012fromfourandﬁveregions,respectively.Theregionsselected forthisstudywerelocatedalonga2200kmlonglatitudinal gra-dient,fromItalythroughHungary,Poland,DenmarkandSweden toNorway (Fig. 1). Seeds were either (i) bought from a

nurs-erywhich couldprovide exactprovenanceinformation (Poland, DenmarkandHungary),or(ii)collectedfromthreeforestpatches inanareaof40km×40km(Italy,CentralSwedenandNorway). Inthelattercase,oneseed-bearinghealthymothertreewasused forseedcollectionineachforestpatchandtheseedswerepicked fromtheforestﬂoorimmediatelyafterseeddispersal(Italy, Cen-tralSwedenandNorway).Theselocationswereselectedduethe relativelyhighviabilityoftheseedsproducedintheseregionsin 2011:Italy(40.0_±35.3S.E.%viableseedspertree),CentralSweden (40.0±12.0)andNorway(55.6±10.7)(Carónetal.,2014a).

We performed a full factorial experiment with soil heating andwateringfrequencymanipulation,tosimulateatotalofnine climatechangescenarios. Webasedourexperimentonthe dif-ferentrepresentativeconcentrationpathway-scenariosproposed bytheIntergovernmentalPanelonClimateChange(IPCC,2013). InEurope,anincreaseoftheairtemperaturebetween0.6◦Cand 4.5◦Cisprojected,whichinturnwillresultinanincreaseofthe soiltemperatureduetotherelationshipbetweenthesefactors,but thewarmingoftheairandsoilisexpectednottobeequaldue tothenatural variationbetweenthesefactors(seeCarónetal., 2015).Themeanannualprecipitationisalsoprojectedtochange, andis expectedtoincrease innorthernandcentralEuropeand decreaseintheMediterraneanarea(IPCC,2013).Moreover, con-sidering the possible changes in precipitation frequency, three wateringfrequencytreatmentswereapplied.Theamountofwater wasexpressedassoilmoisturecontentratherthanmillimetresof rainfallsince(i)thisisastrongerpredictoroftheimpactonplant establishmentthanprecipitation(Walcketal.,2011),(ii) germina-tionandotherearlyestablishmentvariablesarehighlydependent onavailablesoilmoisture(KosandPoschlod,2008),and(iii)itis easiertocomparetheresultswithpreviousstudiesthatusedthis variable(Viccaetal.,2012;Carónetal.,2014b).

Allseedswerecoldstratifieduntildormancybreak.Theseeds were soaked in water until the desired level of moisture was reached(i.e.48%and38%forA.pseudoplatanusandA.platanoides, respectively),afterwhichtheseedswereplacedundercontrolled coldconditions(0–1◦Cand90–95%humidity)untilgermination started. Because the stratification time is highly dependent on speciesandprovenance,andtoensurethattheseedsfromallthe provenanceswereatthesamedevelopmentalstageatthestartof theexperiment, seedlotsthatstartedtogerminatewerestored inafreezerat−2◦_C_until_the_start_of_the_experiment₍₅₂_days_of differencebetweenthefirstandthelastseedlotgermination).

Fourseedsofeachspeciesandregionwererandomlysownin eachof12plasticpots(112cm3_,₇_cm_deep)₍₄_×₁₂₌₄₈_seeds)_per treatment,ﬁlledwithstandardpottingsoil(meanpH6,nutrient contentratioNPK15:10:11 at1kg/m3_,_organic_matter _20%_and waterholdingcapacityof80%).Themanipulationsofthesoil tem-peraturewere:(1)Controlatambienttemperature(theaverage forthewholeperiodwas19.2±3.2◦C(mean±SD)measuredevery minute,andaveragedandloggedevery15minusingDecagondata loggers Em50ECH2OLogger inside thesoilof thepotsat 4cm depth);(2)warmingwith+2.8◦C(22.0±2.9◦C),and(3)extreme warmingwith +7.0◦C (26.2±4.6◦C). Additionally, the watering frequencywasmanipulatedbyaddingthesametotalamountof wateroneachoccasion,butindifferentintervals(one,twoorthree timesperweek).Thenecessaryamountofwatertobeaddedevery weekwascalculatedbyweighingthreerandomlychosenpotsper warmingtreatmentandcalculatingthenecessaryamountofwater toreachﬁeldcapacity.Thenthenecessaryamountofwaterwas dividedbythewateringintervalassuringthatallthetreatments receivedexactlythesameamountofwaterperweekbutin differ-entintervals.Theaverageweeklyamountofwateraddedtoeach potduringtheexperimentundereachtreatmentwas:+0◦C:24ml (control),+2.8◦C:25ml,and+7.0◦C:29ml.

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Table1

Establishmentandgrowthvariablesasafunctionofthecountryofprovenanceoftheseedsandtheexperimentalconditions:warming(temperatureincreasedby2.8◦_C_or

7.0◦Ccomparedtothecontrol)andwateringfrequency(one,twoorthreetimesperweek).

Acerplatanoides Acerpseudoplatanus

Establishmentvariables Predictor LRT Predictor LRT

Germination Wateringfrequency ↑6.38* _Watering_frequency _↑4.49*

Seedprovenance 183.69*** _Seed_provenance _545.79***

Warming ↓10.46**

Survival Warming ↓84.11*** _Warming_×_seed_provenance _13.24*

Warming×wateringfrequency×seedprovenance 11.68*

Growth Predictor Scaleddev Predictor Scaleddev

Totalbiomass Warming ↓99.38*** _Warming _↓49.42***

Warming×seedprovenance 114.61*** _Warming_×_Watering_frequency _31.40***

Abovegroundbiomass Warming ↓88.86*** _Warming _↓43.87***

Warming×seedprovenance 103.22*** _Warming_×_Watering_frequency _25.00***

Belowgroundbiomass Warming ↓92.98*** _Warming _↓35.54***

Warming×seedprovenance 106.17***

Wateringfrequency×seedprovenance 32.53***

Root:shootratio Warming ↓24.33*** _Warming _↓10.76**

Height Warming ↓64.69*** _Warming _↓139.72***

Warming×seedprovenance 89.69***

LRT:likelihoodratiotest;scaleddev:scaleddeviance.Thedirectionoftheeffectisindicatedbyarrows:↑and↓correspondtoanincreaseanddecreaseofthevariables analyzed,respectively.

*_P_<_0.05. **_P_<_0.01. ***_P_<_0.001.

Warmingwasachievedthroughevenlyspreadsoilheatingmats (ACDheatingmatsHMT-A,OberweidbachGermany).The experi-mentwasinstalledfacingwestattheedgeofadeciduousforest in Gontrode,Belgium (50◦58N,3◦48E), withF.sylvatica, Fraxi-nusexcelsior,Quercus roburand Acerpseudoplatanusdominating thecanopy.Thelocationoftheexperimentwasclosetotheforest edge(<10m)butnotdirectlyundertheforestcanopyassuringthat thewholeexperimentalareareceiveddirectmid-daylightwithout interferenceoftheforestcanopy.Thepotswereplacedontopof thesoilheatingmats,onwoodentablesunderplasticroofs(70cm abovethepots)toexcludethenaturalprecipitationandallowfree airexchange.Duringtheexperiment,thepotswerecontinuously randomlyrelocated.

Attheendoftheexperiment(ca.3monthsaftersowing),we assessed the regeneration in terms of germination (number of emerged seedlings),survival (number ofliving seedlings atthe endoftheexperiment)andseedlinggrowth(height,aboveground andbelowground biomassandtotalbiomass).Germinationwas recordedonceperweek.Attheendoftheexperiment,theseedlings werecarefullyremovedfromthesoil,theabovegroundand below-groundpartsseparated,driedat60◦Cfor24handweighed.

2.3. Dataanalysis

Generalized linear models (GLM) in Rversion 3.1.0 (R Core Team, 2013)were applied.For thebinomial data (germination andsurvival)andcontinuousdata(aboveground,belowgroundand totalbiomass,root:shootratioandheight),weusedbinomialand Gaussianerrorsstructures,respectively.Tofulﬁltherequirements ofnormalityandhomoscedasticity,for bothspecies,the above-ground,belowgroundandtotalbiomasswerelogtransformedand root:shoot ratiowas square root-transformed.Additionally, the heightofA.platanoideswaslog-transformedpriortoanalyses.The

temperature treatments(+0◦C, +2.8◦C and +7◦C), thewatering frequencytreatments(one,twoandthreetimesweekly)andthe countryofseedprovenance(Poland,Denmark,Sweden,Norway, Italy andHungary)wereusedasfixedeffects. Theaprioridata explorationshowedthattheseeds’origin(i.e.collectedbyusvs. purchasedfromtreenurseries)didnotaffecttheresults,therefore, thisfactorwasnotincludedintheanalyses.Foreachvariable ana-lysed,firstthefullmodelwasfitted(allthefixedeffectsandtheir interactions),afterwhichmodelsweresimplifiedbydroppingfirst theleastsignificantinteractionandthentheleastsignificant indi-vidualvariableateachstep.Thecomparisonbetweenmodelswas basedonthelikelihoodratiotestorthescaleddevianceforthe binomialandGaussiandata,respectively,untilalltheremaining termsweresignificant(Zuuretal.,2009).

3. Results

3.1. Establishmentvariables

Both species germination and seedlings’ performance responded to temperature, watering frequency and the coun-tryoforigin,withstrongereffectsoftemperatureandthecountry oforiginthanofwateringfrequency(Table1).Seedprovenance signiﬁcantly affected germination in both species; the highest germinationofbothspecies wasrecorded approximatelyin the centre ofthedistribution range(Table1 and Fig.2).Moreover, germinationwas19and12%(A.platanoides)and16and12%(A. pseudoplatanus)higherwhenthewateringtreatmentwasapplied twoandthreetimesperweek,respectively,comparedtotheleast frequentwatering(Table1,Fig.2andElectronicAppendixTables A1andA2).Additionally,forA.pseudoplatanus,thetemperature increase reduced germination, being 17.3% lower with 2.8◦C

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Fig.2.GerminationofAcerplatanoidesandA.pseudoplatanusasafunctionofwateringfrequency(one,twoandthreetimesperweek)andseedprovenance.Thesigniﬁcance ofthefactorsthataredisplayedisindicated.Theerrorbarsindicatestandarderrorsacross12replicatesoffourseedsperprovenanceandtreatment(totaln=3888).

warmingthanunder controlconditions (Table1 and Electronic AppendixTableA2).

Signiﬁcantdifferenceswereobservedbetweenthespeciesin termsofseedlingsurvival.A.platanoides’survivaldecreasedwith warming,andwas,onaverageacrossthecountries,49.9%lower underwarmestcondition(+7.0◦C)thanundercontrolcondition (Table 1, Fig. 3 and Electronic Appendix TableA1). Survival of A. pseudoplatanus, on the other hand, responded differently to increasesintemperaturedependingonthecountryof originof theseeds(signiﬁcantwarming×provenanceinteraction,Table1 andFig.3).SurvivalofseedlingsofseedsfromHungaryand Cen-tralSwedenincreasedunderthewarmestcondition(+7.0◦C),while survivalofseedlingsofseedsfromDenmarkandNorwaydeclined withwarming(+2.8◦Cand +7.0◦C)(Fig.3).Thejoint manipula-tionoftemperatureandwatering frequencydifferentlyaffected seedlingsurvivaldependingontheseeds’provenance(Table1). Forexample,seedlings fromItalianseedsshowedahigher sur-vivalwithwarmingwhen watered onceper week,butshowed reducedsurvivalunderwarmingwhenwateredmoreoften(3times perweek).TheCentralSwedishprovenanceexhibitedaconstant increaseofsurvivalwithwarmingacrossallthewatering frequen-ciestreatments.

3.2. Growthvariables

Regardingthebiomassvariables,bothspeciesshowedsimilar responsestothemanipulatedfactors(Table1), despitethatthe seedlingsofA.platanoidesweremuchbiggerthantheseedlingsof A.pseudoplatanus(Figs.4and5).

Warmingnegatively affectedtheaboveground, belowground and consequently the total biomass of both species. The total biomasswas53.5%(A.platanoides)and37.9%(A.pseudoplatanus) lowerinseedlingsgrowingunderthewarmestcondition(+7.0◦C) thanunderthecontroltemperaturetreatment(+0◦C)(Fig.5and ElectronicAppendixTablesA1andA2).Furthermore,the prove-nanceoftheseedsinﬂuencedtheaboveground,belowgroundand thetotalbiomass,whichgenerallyincreasedtothenorth,butthe highestvalueswererecordedinCentralSweden(A.platanoides)and Denmark(A.pseudoplatanus).Inaddition,analysesrevealed inter-activeeffectsaffectingbothspecies(Table1).Theaboveground, belowgroundandtotalseedlingbiomassofA.platanoidesgenerally decreasedwithwarming,butseedlingsgrownfromseedsofmiddle latitudes(PolandandCentralSweden)weresmallerundera mod-eratewarming(+2.8◦C)thanunderextremewarming(signiﬁcant warming×provenanceinteraction,Table1,Fig.4andElectronic

Fig.3. SurvivalofAcerplatanoidesandA.pseudoplatanusasafunctionoftemperature(ambienttemperatureandincreasesof2.8◦_C_and₇◦_C)_and_the_seed_provenance._The

signiﬁcanceofthefactorsandinteractionsthataredisplayedisindicated.Theerrorbarsindicatestandarderrorsacross12replicatesoffourseedsperprovenanceand treatment(A.platanoidestotaln=1080,A.pseudoplatanustotaln=992).

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Fig.4.Totalbiomassandbiomassallocation(rootvs.shoot)ofAcerplatanoidesandA.pseudoplatanusunderthedifferenttemperaturetreatmentsandinrelationtoseed provenance.Thesigniﬁcanceofthefactorsandinteractionsthataredisplayedisindicated.Errorbarsindicatestandarderrorsacross12replicatesoffourseeds(A.platanoides totaln=536,A.pseudoplatanustotaln=514).

AppendixTableA1).InA.pseudoplatanus,theabovegroundbiomass andtotalbiomassshowedareductionof38and48%,respectively, whengrowingunderthewarmestconditionandthemostfrequent wateringtreatment(7.0◦Candwateredthreetimesperweek) com-paredwiththelessfrequentlywateringandunwarmedconditions (controltemperatureandwateredonetimeperweek)(Table1and ElectronicAppendixTableA2).

The root:shoot ratio of both species depended onthe seed provenanceandwasaffectedbyexperimentalwarming(Table1). Root:shootratioswerehighestinCentralSweden(A.platanoides) andDenmark(A.pseudoplatanus)(Fig.4andElectronicAppendix TablesA1andA2).Warmingdecreasedtheroot:shootratioinboth species(Table1,Figs.4and5andElectronicAppendixTablesA1 andA2).

Fig.5.Totalbiomassandbiomassallocation(rootandshoot)ofAcerplatanoidesandA.pseudoplatanusasafunctionofthewarmingandwateringfrequencytreatments.The signiﬁcanceofthefactorsandinteractionsthataredisplayedisindicated.Errorbarsindicatestandarderrorsacross12replicatesoffourseeds(A.platanoidestotaln=536, A.pseudoplatanustotaln=514).

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Finally, the height of both species was negatively affected by warming. The seedlings of A. platanoides and A. pseudopla-tanus were 18.3% and 24.2% shorter when growing under the warmestconditionscomparedtothecontrol(Table1andElectronic AppendixTablesA1andA2).Inaddition,seedlingheightappeared tobeprovenance-speciﬁc;seedlingsgrownfromseedscollectedin Poland(A.platanoides)orCentralSweden(A.pseudoplatanus)were thetallest.Moreover,theseedlingsofA.platanoidesfromthe south-ernandnorthernprovenances(HungaryandNorway)showeda strongheightgrowthreductionundersimulatedwarming(2.8◦C and7.0◦C),whilethatwasnotthecaseforthecentralprovenances (Table1andElectronicAppendixTableA1).

4. Discussion

Differentresponsestowarmingandwateringfrequencywere observedinbothspeciesandamongthelifephasesanalysed(i.e. germination,seedlingsurvivalandgrowth).Germinationofboth specieswasstronglyinﬂuencedbythewateringfrequencyandthe countryoforiginoftheseeds,whilewarmingwasthemainfactor affectingseedlinggrowth.Overall,temperatureand thecountry oforiginoftheseedsappearedtobethemostimportantfactors affectinggerminationandseedlingsurvivalandgrowthofthese species.Theinteractiveeffects betweenwarming,watering fre-quencyand/orseedprovenancewerelessimportantthaninitially expected.

Thefrequency ofwateringaffectedseedgerminationofboth species.Precipitationfrequencyhasbeenshowntoaffectsoil mois-turevariability(FayandSchultz,2009),whichinturnmayinfluence germinationpatterns(Shevtsovaetal.,2009;Carónetal.,2014b). Our results, consistent with the observations of Fay & Schultz (2009),showthatcyclesofhydrationanddehydration(i.e.lower amountsof water, but morefrequent watering events) tendto enhancegermination.Bothspeciesshoweddifferentgermination percentagesaccordingtoseedprovenance.Germinationgenerally appearedtobehigherinseedsfrommorenortherlyprovenances, probablyduetohighernortherlyseedmass(Carónetal.,2014a), likelycaused by aslowerseed ripening atlower temperatures, slowerseed fillingprocessand thereforeagreater total assimi-lation(FennerandThompson,2005).However,contradictingour hypothesis,seedprovenancedidnotinfluenceseedgermination inresponsetothetreatmentsapplied(warmingand changesin watering frequency), which indicates that climate change will affectgerminationof thesespecies similarly in Europe,despite thevariablegerminationratesobservedalong theirdistribution range.Ontheotherhand,warmingonlyaffectedgerminationof oneofthespecies,A.pseudoplatanus,withgermination decreas-ingatincreasedtemperatures.Itispossiblethattheexperimental warmingreachedalevelclosetothethresholdtemperaturesfor thespecies’germination(Chmuraetal.,2011)andthatasimilar futurewarmingwillaffectthisspecies’recruitmentbyreducing germinationprobability.Thedecreaseingerminationdueto warm-ingobservedhere wasnotcaused bya correspondingnegative effectofwarmingondormancybreakbecausethestratification processwascompletedbeforethebeginningoftheexperiment. Eventhoughdormancybreakwasnotevaluatedhere,itislikely thatbothspecies’dormancywillbedifferentlyimpactedby cli-matechange.ConsideringthatA.platanoidesrequiresmoredaysof coldstratificationforsuccessfuldormancybreakthanA. pseudopla-tanus(BaskinandBaskin,1998),itislikelythatA.platanoideswillbe impactedmorethanA.pseudoplatanusbythepredictedreduction oftheamountofchillingdaysinwintercausedbyglobalwarming. Treatmenteffectsonseedlingsurvivaldifferedmorebetween thetwospeciesthantheireffectsongermination,apartfromthe effectsofwarmingonseedgerminationthatwereclearly

species-specific.SeedlingsurvivalofA.platanoidesdecreasedunderwarmer conditions.Itisknownthatwarmerconditionstendtoenhance physiological processes, thereby also increasing thechances of survival (Chmuraet al.,2011).Warmertemperatures at north-ernlatitudesmayenhancephotosynthesisinborealandtemperate treesduetoanincreaseinthecontentofphotosyntheticpigments, light-saturatedphotosyntheticrateandquantumyield(Saxeetal., 2001).Effectsonphotoinhibitionandphotorespirationaremore difficulttogeneralizebecausetheydependonthespeciesand gen-eralclimaticconditionsoftheareabut,overall,slightlywarmer conditions(ca.2◦C)areexpectedtopromotephotoinhibitionand photorespiration(Saxe etal.,2001).However,thesoil moisture contentis alsoimportantand mightbeeven morerelevant for photosynthesisthantemperatureperse(Saxeetal.,2001;Chmura etal.,2011).Moreover,itisknownthatwarmingnotonlyaffects abovegroundprocesses butalsocanaffectsoil respiration(root andmicrobialrespiration),nutrientavailabilityandroot dynam-icswhichareallimportantaspectsforseedlings’survival(Baietal., 2010;Zhouetal.,2012).Warmingintherangeof0.3–6.0◦Ccan indeedincrease soilrespirationratesby 20%,netN mineraliza-tionrates by46%,and plantproductivityby19% (Rustad etal., 2001).Theresponseofsoilrespirationandmineralizationratesto warmingnotonlydependsonthetemperaturechange,butalso onotherfactorssuchasthesoilsubstrate,theorganicmatterand soilmoisturecontent(Rustad etal.,2001;Saxe etal.,2001).In termsofrootdynamics,warmingcanreducerootbiomasswhile increases in precipitationcan increase root biomass(Baiet al., 2010).It ispossiblethat theobservednegativeeffectof warm-ingonA.platanoidessurvivaliscausedbyanexcessivewarming appliedinthisexperiment.Consideringthepreviousconcepts,itis likelythatthedirectionoftheimpactofclimatechangeonseedling survivalwilldependonthelevelofwarmingexperiencedbythe seedlingsbutalsoofmanyinteractingfactorsasobservedforA. pseudoplatanus.ThesurvivalofA.pseudoplatanuswasinfluenced byacomplexinteractionofwarming,seedprovenanceand water-ingfrequency.Underextremewarming(+7.0◦C),morefrequent wateringenhancedsurvival.Extremelywarmconditionsintensify evapotranspiration, and, consequently, more frequent watering tendstoresultinhighersoilmoistureintheupperlayersofthesoil duetothemoreintenseheatatthebottomofthepotswhichisin directcontactwiththesoilheaters.Moreover,asmentionedbefore, manyphysiologicalprocessesnotonlydependonthetemperature butalsothesoilmoisturecontentandthiscanbethecausebehind thesignificanceofthisinteraction.Thisresultnotonlyhighlights therelevanceofmultipleinteractingfactors(Shaveretal.,2000), butalsopointstosomeofthepossibleproblems(i.e.possible not-uniformwarmingofthesoilcolumninthepot)associatedwith themethodsutilizedforstudyingtheeffectsofclimatechangeon plants.However,becausethepotsusedinthisexperimentwere relativelysmall(112cm3_),_it_is_likely_that_no_significant_differences inwarmingexistedalongthesoilcolumnorthatthehighspecific heatofwaterplayedaroleinthesignificanceofthisinteraction regardingseedlingsurvival.Finally,itisimportanttoconsiderthat underfutureclimaticconditions,warmingoftheairwillbe accom-paniedbypotentiallynon-uniformwarmingofthesoil.Toclarify therelevanceandroleofalltheseaspectsandtounraveltheeffectof temperatureandwateringfrequency,moreexperimentsusing dif-ferentmethodscanbeperformedemploying,forexample,growth chambers(e.g.Deinesetal.,2007;DeFrenneetal.,2012).In addi-tion,A.pseudoplatanusalsoshowedprovenance-specificresponses toincreasesintemperature.Thesurvivalofseedlingsgrownfrom seedscollectedin Hungaryand Central Sweden wasin general higherunderwarmerconditions,whilesurvivalofseedlingsgrown fromseedscollectedinDenmarkandNorwayshowedan oppo-siteresponse(i.e.lowersurvivalunderwarmerconditions).This islikelyrelatedtotheenvironmentalconditionsexperiencedby

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themothertreeduringseedproduction(Johnsenetal.,2005a,b; Skrøppaetal.,2010;Carónetal.,2014a).Whilewelackdetailed informationonenvironmentalconditionsexperiencedbyallthe mothertrees,previousstudiessuggestthattheobservedpattern (differentsurvivalaccordingtotheseedprovenanceunder chang-ingenvironmentalconditions)islikelyrelatedtothetemperature experiencedduringseedproduction(Johnsenetal.,2005a,b;Carón etal.,2014a,b).Nevertheless,ourresultsclearlypointoutthe inﬂu-enceofseedprovenanceonseedlingresponsestoclimatechange (Atzmonetal.,2004;Thieletal.,2014).Additionally,thepossibility ofthepresenceoflocaladaptationsshouldbeanalysed(Kawecki andEbert,2004)throughtheuseof,forinstance,transplant exper-iments(DeFrenneetal.,2011;HilleRisLambersetal.,2013;Ibá ˜nez andMcCarthy-Neumann,2014).

Regardingseedlinggrowth,thetotalbiomasswasmuchmore affectedbywarmingthanbythechangesinwateringfrequency. Theabsenceofeffectsofwateringfrequency(individualfactor)is surprisinggiventhatpreviousexperimentsdemonstratedeffects of precipitationamount(e.g. Dreesenet al.,2012; Carónet al., 2014a)andofsoilmoisturevariability(e.g.Fayetal.,2002,2012) on growth.However, it is possible that the high organic mat-ter content (20%) of the potting soil used in this experiment inducedahighwaterretentioncapacity,therefore,irrespectiveof thetreatments applied,theseedlings never experienced strong droughtstressrelated tothedifferences inwatering frequency. Conversely,warmingnegativelyaffectedseedlinggrowthinboth species despite that under warmer conditions, the physiologi-calprocessesofplantsincludingphotosynthesisandrespiration increaseaslongasthewatercontentisadequate(Chmuraetal., 2011).However, theincrease ofphotosynthesis andrespiration mightnotbeequalandcan,insomecases,negativelyaffectspecies growth ifthe fraction of gross photosyntheticproduction con-sumedbyrespirationbecomestoohigh(Saxeetal.,2001).Growth of A. platanoides was strongly reduced in both warming treat-ments(+2.8◦Cand+7.0◦C),whilegrowthofA.pseudoplatanusalso declinedunderwarmerconditionsbutnotasabruptlyasinA. pla-tanoides.Inapreviousstudy,similarresultswereobtained,with bothspeciesnotshowingapositivegrowthresponsetowarming (Carónetal.,2014b).Warmingreducedbelowgroundand above-groundbiomass.However,thestrongernegativeeffectofwarming onbelowgroundbiomassresultedinareductionoftheroot:shoot ratiounderwarmerconditions.Itwasobservedbeforethat warm-ingcandecreaseannualrootproduction(Baietal.,2010)andfine rootbiomass(Wanetal.,2004)butalsocandecreaseroot mor-tality(Baietal.,2010).However,otherstudiessuggestthatthe evapotranspirationcaused bywarmingdecreasesthesoil mois-turecontentandcanincreasetheproportionalallocationtowards rootsinordertofacilitateplantwateruptake.Thiseffect,however, mightalsosuppressoverallrootgrowth(Rustadetal.,2001;Zhou etal.,2012).Moreover,thereductionoftheroot:shootratiomight alsobelinkedtoanimbalancebetweenphotosynthesisand res-piration.Therelevanceofinteractingfactorswasespeciallyclear forA.pseudoplatanus’growth.Theinteractionbetweenfactorshas beenhighlightedaskeywhenpredictingspeciesresponsesto cli-matechange(Baietal.,2010).Theresultsreportedherecorroborate therelevance ofstudying interactingfactorsof climatechange. Regardingtheinfluenceof theprovenanceonseedling’s perfor-mance,itisinterestingtonotethatA.pseudoplatanusdidnotshow provenance-specificgrowthresponsestothetreatmentsapplied. Thisindicatesthat,independentoftheprovenanceofA. pseudopla-tanusseeds,theseedlingsareequallyaffectedintermsofgrowth. However,A.platanoidesshowedprovenance-specificresponsesin biomassgrowthasobservedearlierforothertreespeciessuchas F.sylvaticawherethemarginalprovenancesshowedamorestable performanceunderdroughtbutapparentlytherewasatrade-off betweendroughttoleranceandgrowth(Thieletal.,2014).

Consideringtheresultsofthisstudy,itispossibletosuggest thatbothspecieswillbeaffectedbychangesinsomeclimatic fac-tors(warmingandprecipitationfrequency).Divergenteffectsof changes inclimaticfactorscanbeexpectedondifferentphases of plant recruitment,and theirimpacts may differ in direction and magnitude.Stronger effects of warmingwereobserved for bothspecies,whilewateringfrequencyappearedtobeless impor-tant.Furtherresearchshouldfocusonmorerealisticsimulationsof changesinprecipitationfrequencywithpossiblylonger interme-diatedryperiods(see,forinstance,Dreesenetal.,2012)tomore clearlyshowtherelevanceofthisfactoronthesespecies’ recruit-ment.Moreover,duetothefrequentdivergentresponsesofseeds andseedlingsalongthegradientanalysed,itislikelythattheimpact will not be homogenous across Europe. In general, more cen-tralEuropeanprovenancesperformedbetterirrespectivewhether seedswerecollectedfromtreesgrowinginnaturalforestsorwere purchasedfromnurseries.Theseresultspoint outtherelevance ofperformingmoreexperimentswheredifferentprovenancesare testedundersimulatedfutureclimaticconditions,including trans-plantexperimentstoanalysethepresenceoflocaladaptationandto deliverurgently-neededinformationforthedevelopmentof strate-giesofforestadaptationinthecontextofclimatechange(Pereira etal.,2010;Bellardetal.,2012).

Acknowledgments

WethanktheResearchFoundation-Flanders(FWO)for fund-ingtheScientiﬁcResearchNetwork‘FLEUR’(www.ﬂeur.ugent.be) allowingtheseedcollection.Theexperimentwasperformedand thispaperwaswrittenwhileMMCheldaPhDfellowshipfromthe ErasmusMundusfundingthroughtheEuroTangoprojectandPDF heldapostdoctoralfellowshipfromtheFWO.

AppendixA. Supplementarydata

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