Functional Trait Changes, Productivity Shifts and Vegetation Stability in Mountain Grasslands

17 Pages·2015·1.18 MB·English

RESEARCHARTICLE
Functional Trait Changes, Productivity Shifts
and Vegetation Stability in Mountain
Grasslands during a Short-Term Warming
HaifaDebouk1,2*,FrancescodeBello3,4,Maria-TeresaSebastià1,2
1 Laboratoryoffunctionalecologyandglobalchange(ECOFUN),ForestSciencesCentreofCatalonia
(CTFC),Solsona,Spain,2 GroupGAMESanddepartmentofHorticulture,BotanyandGardening,Schoolof
AgrifoodandForestryScienceandEngineering,UniversityofLleida,Lleida,Spain,3 DepartmentofBotany,
FacultyofSciences,UniversityofSouthBohemia,ČeskéBudějovice,CzechRepublic,4 InstituteofBotany,
CzechAcademyofSciences,Třeboň,CzechRepublic
a11111
*[email protected]
Abstract
Plantfunctionaltraitsunderlievegetationresponsestoenvironmentalchangessuchas
OPENACCESS
globalwarming,andconsequentlyinfluenceecosystemprocesses.Whilemostoftheexist-
Citation:DeboukH,deBelloF,SebastiàM-T(2015) ingstudiesfocusontheeffectofwarmingonlyonspeciesdiversityandproductivity,wefur-
FunctionalTraitChanges,ProductivityShiftsand
therinvestigated(i)howthestructureofcommunityplantfunctionaltraitsintemperate
VegetationStabilityinMountainGrasslandsduringa
grasslandsrespondtoexperimentalwarming,and(ii)whetherspeciesandfunctionaldiver-
Short-TermWarming.PLoSONE10(10):e0141899.
doi:10.1371/journal.pone.0141899 sitycontributetoagreaterstabilityofgrasslands,intermsofvegetationcompositionand
productivity.Intactvegetationturveswereextractedfromtemperatesubalpinegrassland
Editor:ChristianRixen,WSLInstituteforSnowand
AvalancheResearchSLF,SWITZERLAND (highland)intheEasternPyreneesandtransplantedintoawarmcontinental,experimental
siteinLleida,inWesternCatalonia(lowland).Theimpactsofsimulatedwarmingonplant
Received:May1,2015
productionanddiversity,functionaltraitstructure,andvegetationcompositionalstability
Accepted:October14,2015
wereassessed.Weobservedanincreaseinbiomassandareductioninspeciesandfunc-
Published:October29,2015
tionaldiversityundershort-termwarming.Thefunctionalstructureofthegrasslandcommu-
Copyright:©2015Debouketal.Thisisanopen nitieschangedsignificantly,intermsoffunctionaldiversityandcommunity-weightedmeans
accessarticledistributedunderthetermsofthe
(CWM)forseveraltraits.Acquisitiveandfast-growingspecieswithhigherSLA,earlyflower-
CreativeCommonsAttributionLicense,whichpermits
ing,erectgrowthhabit,andrhizomatousstrategybecamedominantinthelowland.Produc-
unrestricteduse,distribution,andreproductioninany
medium,providedtheoriginalauthorandsourceare tivitywassignificantlypositivelyrelatedtospecies,andtoalowerextent,functional
credited. diversity,butproductivityandstabilityafterwarmingweremoredependentontraitcomposi-
DataAvailabilityStatement:Allrelevantdataare tion(CWM)thanondiversity.Theturveswithmoreacquisitivespeciesbeforewarming
withinthepaperanditsSupportingInformationfiles. changedlessincompositionafterwarming.Resultssuggestthat(i)theshort-termwarming
Funding:SpanishScienceFoundationfundedthe canleadtothedominanceofacquisitivefastgrowingspeciesoverconservativespecies,
projectCAPAS(CGL2010-22378-C03-01),http:// thusreducingspeciesrichness,and(ii)thefunctionaltraitsstructureingrasslandcommuni-
www.fecyt.es/:MTS.SpanishScienceFoundation
tieshadagreaterinfluenceontheproductivityandstabilityofthecommunityundershort-
fundedtheprojectBIOGEI(CGL2013-49142-C2-1-
termwarming,comparedtodiversityeffects.Insummary,short-termclimatewarmingcan
R),http://www.fecyt.es/:MTS.SpanishMinistryof
EconomyandCompetitivenessfundedtheFPIshort- greatlyaltervegetationfunctionalstructureanditsrelationtoproductivity.
termvisittotheCzechAcademyofSciences(BES-
2011-047009):HD.Thefundershadnoroleinstudy
design,datacollectionandanalysis,decisionto
publish,orpreparationofthemanuscript.
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 1/17
FunctionalChangesinMountainGrasslandsunderWarming
CompetingInterests:Theauthorshavedeclared Introduction
thatnocompetinginterestsexist.
Highmountainecosystemsareconsideredtobeparticularlyvulnerabletoglobalwarming
[1,2].Underclimatechangeconditions,floristicbiodiversityinEuropeansemi-natural,spe-
cies-richandsubalpinegrasslandsisexpectedtobehighlyaffected[3–5].Anumberofstudies
haveobservedthatwarmingenhancesproductivity[6–10],altersspeciescompositionand
reducesspeciesdiversity[10,11],atleastinashortterm.Theincreaseinbiomassproductivity
hasbeenattributedtotheenhancedplantgrowthasatransientresultofincreasedsoilorganic
mattermineralization[12,13]andnutrientavailabilitywithwarming[6,8].Theseresource
enrichedenvironmentalconditionsareconsideredfavorabletospeciescharacterizedbyfast
growthandhighreturnsonresourcesinvestment[14,15].Thismeansthatconservativespe-
cies,withslowernutrientacquisitionandslowergrowth(asopposedtoacquisitivespecies,
Diazetal.[16])couldbeout-competedasaresultofnutrientdepletionbyfast-growingspecies
[17]orcoulddisappearasaresultoflowadaptationabilitytothenewconditions.Increased
productivitycan,therefore,eitherincreaseorreducediversitydependingontherelationship
betweenproductivityanddiversity[18,19].
Theimpactofwarmingshouldalsodependontheresistanceandresilience,altogether
definingstability,ofplantcommunities.Inmanystudies,thestabilityofthecommunityhas
beenrelatedtodiversity—withanaprioriknownasthe“diversitybegetsstability”hypothesis.
Thetheorysuggestsapositivestability-diversityrelationshipbecausethesystemcouldbemore
stablewhenmorespeciesareavailable,thusprovidingasortofinsurancetowardsdifferent
environmentalchanges[20–23].However,otherstudiesquestionthishypothesis[24–26]
becauseecosystemstabilitycouldsimplydependonthetypeofdominantspeciesinthesystem.
Thesestudiesadvocatethatthepositivecorrelationbetweenstabilityanddiversitycanbe
explainedbythefactthathigherdiversitysimplyincreasestheprobabilityofincludingspecies
withtraitsbetteradaptedtothenewenvironmentalconditions[27–29].Theyalsoarguethat
lookingonlyatspeciescompositionanddiversitydoesnotgiveamechanisticviewontheeco-
systemanddoesnotallowgeneralizationsbeyondspecificsites.
Whileseveralstudieshaveassessedtheeffectofglobalwarmingonspeciesdiversity[3–
5,30,31],theresponseofthecommunityplantfunctionaltraitstoincreasingtemperaturesand
theirroleinthevegetationstabilityhavebeengenerallyoverlooked.Theimportanceofplant
functionaltraits(anycharacteristicsoforganismswhichimpactitsfitness)liesinthefactthat
theyconsistentlyrevealcommunityresponsestoenvironmentalchangesacrossregionsand
controlecosystemprocesses(vegetativegrowth,photosynthesis,decomposition,etc.[32]).Spe-
cieswithdistinctfunctionaltraitsareexpectedtoresponddifferentlytoenvironmentalcondi-
tions,andhenceinfluenceecosystemprocessesaccordingly[33].Inwarmingexperiments,it
remainsunclearhowdiversityandplantfunctionaltraitsinfluencethecommunityresistance
andtowhichextenttheycontributetoitsresilienceunderwarming.Itisalsounclearhoweco-
systemprocessessuchasproductivityandstabilitywillbeaffectedbychangesinvegetation
structureandwhattypeofspecieswillbecomemoredominant.Therefore,weexpectthatthe
studyoffunctionaltraitscanimproveourunderstandingofthemechanismsrelatedtothesta-
bilityoftheecosystem,underwarming.
Inthisstudy,weinvestigatedtheeffectofwarmingonproductivity,planttraitscomposition
andfunctionaldiversityduringonegrowingseasonthroughtransplantinggrasslandturves
fromthehighland(humidandcold)tothelowland(dryandwarm)areas.Wefocusonsemi-
naturalsubalpinegrasslandsintheEasternPyrenees,whichareconsideredtobevulnerableto
climatechangeduetotheirpositionatthesouth-westernedgeofthesemi-naturalgrassland
biomeinEurope[8].Additionally,climatechangescenariosintheregionpredictanincrease
inmeanannualtemperatureof0.5°Candadecreaseinmeanannualprecipitationof10%[34].
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 2/17
FunctionalChangesinMountainGrasslandsunderWarming
ParticularlyintheSpanishPyrenees,effectsofwarmingarebelievedtobeparticularlypro-
nounced[35,36].Manystudiessuggestthatbiodiversityenhancesecosystemfunction[37,38]
andisindispensableforthestabilityofplantcommunitiesintermsofproductivityandvegeta-
tioncomposition[20–22].Howeverstabilitydoesnotonlydependonspeciesrichnessbutalso
onthefunctionaltraitsofthespeciesandonthegrowth-relatedtraits[25,26].Therefore,we
hypothesizethatcommunitytraitsassociatedtoresourceacquisitionandcompetitiveness(spe-
cificleafarea,leafdrymattercontent,startoffirstflowering,plantheight,growthhabit,rhi-
zome-formation,etc.),togetherwithspeciesrichness,willcontributetothestabilityofthe
communityinthefaceofwarming,intermsofvegetationcomposition.Wealsohypothesize
thattheincreasedproductivityinthelowlandisnotexclusivelytheresultoftheinitialspecies
richness,butalsoofthefunctionaltraitchangesunderwarmingconditions.Inourstudy,we
analyze(1)theresistanceofthegrasslandcommunitytowarming,(2)theeffectofdiversity
andfunctionaltraitsonbiomassproduction,(3)andtheeffectofspeciesandfunctionaldiver-
sityandfunctionaltraitscompositiononcommunitystabilityintermsofvegetation
composition.
MaterialsandMethods
Transplanting
Ashort-term(onegrowingseason)climatechangeexperimentwascarriedoutthroughtrans-
plantinggrasslandturvesfromhighland(moistandcold)tolowland(dryandwarm)areas.
Thehighlandstudysystemconsistedoftwocoldtemperatesemi-naturalsubalpinegrassland
sites(p1andp2)ataround2000ma.s.l.withadistanceofapproximately1kmfromone
anotheratthePladeRusinCadí-MoixeròNaturalPark(1(cid:1)993°E,42(cid:1)276°N).Thesesubalpine
grasslandsarecharacterizedbycoldtemperateclimate(meanannualtemperatureis5.3°Cand
meanannualprecipitationis1183.4mm;AtlasClimàticDigitaldeCatalunyahttp://www.
opengis.uab.cat/acdc/,accessedinJuly2013).Thevegetationwasdominated,inbothsites,by
subalpineperennialmesicgrasslandsonlimestonedominatedbyFestucanigrescensLam.,in
additiontoCarexcaryophylleaLatourr.,AnthoxanthumodoratumL.,Potentillaneumanniana
Reichenb.,GaliumverumL.,ThymuspulegioidesL.,andKoeleriamacrantha(Ledeb.)Schultes
(seeSebastiáetal.[7]formoredetailsonoriginalvegetationandenvironment).
Theexperimentaddressedmostlyatemperatureandwaterchangescenario(seebelow)dur-
ingthevegetativeperiodoftheplants,representinganextremewarmingevent.Ateachofthe
twohighlandsites,60turveswereextractedandeachturfwasputinplastictraysof40cmx40
cmx20cm(depth).Halfoftheturvesfromeachsitewereselectedrandomlyandplacedback
inthegrassland(‘highland’treatment).Theotherhalfwasplacedinexperimentalfieldsofthe
SchoolofAgrifoodandForestryScienceandEngineeringoftheUniversityofLleida(‘low-
land’).ThelowlandsitehasacontinentalMediterraneanclimate(meanannualtemperatureis
14.5°Candmeanannualprecipitationis442mm).Sincethelowlandsite(Lleida)isexposedto
verydryandwarmconditionsduringsummer,waterwasaddedweeklytoapproximatehalfof
thenaturalrainfrequencyatthesubalpinesiteandtopreventthemortalityoftheplantsdueto
thehighdiscrepancyinprecipitationbetweenthehighlandandthelowland.Theshort-term
durationoftheexperimentimpliesthatnewcolonizersdidnothavetimetocolonizetheturves,
andthusobservedresponsescorrespondonlytointernalresponsesoftheoriginalsystem.It
shouldbenotedthathighertemperatureandreducedwateravailabilitywerethemainstressors
inthelowlandcomparedtothehighland.However,otherfactorscouldalsodifferbetweenthe
highlandandthelowland.Sincewedidnotobserveanyobviousdifferenceinpestsandpara-
sitesbetweenhighlandandlowland,wecansafelyattributetheobservedchangestoincreased
temperature(seepublishedworkonthisdataforamoredetaileddiscussion;[8,11]).As
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 3/17
FunctionalChangesinMountainGrasslandsunderWarming
revealedbythiswork,changesinmineralizationcouldexplainsomeofthepatternsobserved,
butagainthesechangesweretriggeredbytheincreaseintemperature.Theturveswereran-
domlydistributedwithinthelowland,butkeptseparatedbetweentwositesasinthehighland.
A20cmx20cmquadratwasfixedinthecentreofthe60turves.Thisquadratwasdividedinto
agridof100subquadratsof2cmx2cmeach.Allthespeciespresentineachquadratwere
recordedeverytwoweeks.Frequencyrecordsandspeciescountsweretakenseventimes
throughoutthegrowingseasoninthehighlandandeighttimesinthelowland(formore
detailedinformationabouttheexperimentandvegetationcompositionchangesseeSebastià
2007;Sebastiàetal.2008).Wedidonlysevenmeasurementsatthehighlandsitebecausethe
seventhmeasurementhadalreadycoveredtheendofthegrowingseasoninthesubalpine
grassland.
Attheendoftheexperiment,17weeksafterthestart,above-groundbiomasswasestimated
byharvestingvegetationona20x20cmquadratplacedinthemiddleofasubsetof28outof
the60turvesusedforspeciesfrequency.Apreviousharvestwascarriedoutin28different
turves10weeksafterthestartoftheexperiment.Thebiomassdataatthetwodateswereused
toanalyzethediversity-productivityrelationship.
Ethicsstatement. Thisstudydidnotinvolveprotectedorendangeredspeciesanditwas
notnecessarytoobtainspecificpermissiontosampleatanyofthesamplingsites.
Communityfunctionaltraitstructure
Weconsideredvariousrelevantfunctionaltraitsthatarelinkedtodifferentspeciesresponses
tobioticandabioticfactors.Thesewere:specificleafarea(SLA,leafareaperunitdrymass),
leafdrymattercontent(LDMC,theratioofleafdrymasstofreshmass),vegetativereproduc-
tion(presenceofrhizomesorstolons),plantgrowthhabit(erectvs.prostrate),meanplant
height(H ),andstartoffirstflowering(month).Traitvaluesofthespeciespresentwere
mean
obtainedfromtwotraitbases,i.e.theLEDAtraitbase[39],andtheCLO-PLAtraitbase[40]and
complementedbyspecificstandardizedmeasurementsforSLA[41]inthefield.Onlyfewtrait
valueswereacquiredfromdeBelloetal.[42].Oneimportantfactorintheresponseofspecies
towarmingcouldbetraitplasticity[43]whichisconsideredoneofthemajormeansbywhich
speciescancopewithnewenvironmentalconditions[44].Unfortunately,wecouldnotmea-
surethetraitsdirectlyinthefield.Assuch,ouranalysesmightonlypartiallycapturethefull
extentofplantcommunityresponsetowarming.
Twoindiceswereconsideredtorevealthemajorcharacteristicsofthecommunityfunc-
tionaltraitstructure[45].Thefirstoneisthecommunityweightedmeansofthetraits(CWM).
TheCWMforeachtraitiscalculatedasthemeanofthetraitvaluesinthecommunity,
weightedbytherelativeabundanceofeachspecies[46].Forcategoricaltraits,thiscorresponds
totherelativeabundanceofspeciesbearingacertaintypeoftraits.Thesecondindexisacom-
monlyusedmeasureoffunctionaldiversityexpressedwiththeRaoquadraticentropy[45].
TheRaoindexexpressesthesumoftraitdissimilaritybetweeneachpairofspeciesinaturfand
itisweightedbyspeciesrelativeabundance.Thisindexismostlyindependentfromthenumber
ofspecies.Itwasexpressedasequivalentnumbers[47]andforalltraitscombined.Thenum-
bersequivalentofadiversityindexindicatestheeffectivediversity,i.e.howmanyeffectively
differentspeciesintermsofabundanceand,incaseoftraits,functionaldifference[48],thus
providingamoreintuitiveconceptofdiversitycomparabletospeciesrichness.UsingRaonot
inequivalentnumbersproducedstronglyrelatedresults(astheyarestronglyrelatedmathe-
matically).Twoadditionalindicesofspeciesdiversitywerecalculated:speciesrichnessand
Simpson’sdiversity,alsoexpressedintermsofequivalentnumbers[47].
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 4/17
FunctionalChangesinMountainGrasslandsunderWarming
Dataanalysis
Theeffectsoftheshort-termclimatechangeontheCWMofthetraits(SLA,%ofrhizomes,%
ofprostrate,startoffirstflowering,LDMC,andmeanplantheight)andthediversityindices
(speciesrichness,Simpson,andRao)wereanalyzedusingrepeatedmeasuresANOVA;where
transplant(highlandandlowland),extractionsite(p1andp2inhighland)andtime(asquanti-
tativevalue,1to7or8)arethefixedfactors.ResultsbySebastià[8]suggestedanincreasein
above-groundbiomassinthelowlandincomparisontothehighland.Therefore,weconducted
multipleregressionmodelstoexaminetheeffectofeachofthediversityindicesandCWMon
above-groundbiomassinthetwositesinboththehighlandandthelowland.Inallthemultiple
regressionanalyses,weselectedthebestmodelbasedontheAkaikeinformationcriterion[49]
usingstepwiseregressions.Correlationtestsbetweenthetraitsandthediversityindiceswere
carriedoutpriortoincludingthemintheregressionmodelstominimizecollinearityproblems
(S1andS2Tables).ThestrongercorrelationwasbetweenspeciesrichnessandSimpson’sdiver-
sityindex(R=0.864,S2Table)butwedecidedtokeepbothvariablesbecausetheycoverdiffer-
entecologicalimplications.
Changesinvegetationcompositionbetweenturvesofthetwotreatments(thehighlandand
thelowland)werealreadyobservedbySebastiàetal.[11],andahigherdissimilarityinspecies
compositionwasdetectedamongthehighlandsamplesincomparisontothelowland,suggest-
ingachangeinthevegetationcompositionwithwarming.Todeterminethedynamicsof
changeinvegetationcompositionwithintheturvesasaresultofthetransplant,wecalculated
theBray-Curtisdissimilarity[50]atthefirstandthesecondharvest(endofexperiment)within
eachturve,usingtheCRANpackage“vegan”inRsoftware[51].Multipleregressionmodels
werecarriedouttotesttheeffectofeachoftheinitialdiversityindicesandtheinitialCWMof
traitsonthechangeinvegetationcomposition(Bray-Curtis)inboththehighlandandthelow-
land(explanatoryvariables).Wemadeadditionallyastepwiseregressionmodelincludingall
thevariablesofdiversityandCWMtraitswiththeBray-Curtisdissimilarity.Allstatisticalanal-
yseswerecarriedoutusingRsoftware[52].
Results
Functionalstructure
Afterthetransplant,thefunctionalstructureofthegrasslandcommunitieschangedconsider-
ably(Table1;Figs1and2).Fewweeksafterthetransplant,thecommunityweightedmean
(CWM)ofSLA,startoffirstfloweringandproportionofrhizomatousandprostratespecies
startedtodivergefromthelowlandtothehighland.Thefunctionalstructureinthehighland
remainedrelativelyunchangedalongthegrowingseason(Fig1).Communitiesinthelowland
appearedtobeprogressivelymoredominatedbyspecieswithhigherSLA,earlierflowering,
erectgrowthhabitandwithrhizomes(Table1;Fig1).Howeverleafdrymattercontent
(LDMC)didnotrespondtotheshort-termwarming(Table1).Allthoseresponsesoccurred
basedontheoriginalspeciescompositionineachturf(weobservednonewcomerappearingin
theturves).Suchanincreaseinabundancebyacertaintypeofspecieswasaccompaniedbythe
disappearanceofotherspecies(lowerspeciesrichnessandSimpsondiversity)inthelowland
(Fig2).Thesetwodiversitycomponents,inadditiontofunctionaldiversity,decreasedsignifi-
cantlyinmagnitudeafterthetransplant(Fig2;Table1).
Wetestedthechangeinvegetationcompositionwithinturvesinboththehighlandandthe
lowlandwithmultipleregressionmodelsandfoundthatneithertheinitialdiversitynortheini-
tialfunctionaltraitsdiversity,hadaninfluenceonthechangeinvegetationcomposition
(Table2andS3Table).OnthecontrarythecommunitieswithinitiallylowCWMofSLA
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FunctionalChangesinMountainGrasslandsunderWarming
Table1. ResultsofrepeatedmeasuresANOVAtoassesstheeffectofthetransplantondiversityindicesandCWMtraitswithtransplant(highland
andlowland),site(p1andp2inthehighland)andtime. SeeFigs1&2foragraphicalrepresentation.
Transplant Site Time Transp.xTime SitexTime Transp.xSitex
Time
F P F P F P F P F P F P
Diversity
Speciesrichness 25.502 <0.001 0.791 0.3776 156.37 <0.001 126.002 <0.001 5.613 0.0183 6.455 0.0115
Simpson 14.113 <0.001 0.041 0.8396 60.595 <0.001 134.248 <0.001 0.462 0.4971 18.931 <0.001
Rao 22.137 <0.001 0.119 0.7312 87.449 <0.001 55.558 <0.001a 2.159 0.1426 1.473 0.2256
CWMtraits
SLA 32.091 <0.001 0.014 0.906 142.03 <0.001 52.828 <0.001 1.483 0.224 0.031 0.859
%Rhizomes 27.521 <0.001 7.630 0.008 60.605 <0.001 53.480 <0.001 0.014 0.907 1.570 0.211
%Prostrate 1.426 0.238 1.264 0.266 47.863 <0.001 27.925 <0.001 8.599 0.004 4.681 0.031
Startoffirstflowering 17.462 <0.001 2.464 0.122 132.52 <0.001 80.168 <0.001 3.52 0.061 0.659 0.417
LDMC 1.079 0.303 0.005 0.942 4.211 0.041 3.428 0.065 0.42 0.517 0.033 0.856
MeanHeight 0.03 0.863 0.901 0.347 4.648 0.032 1.134 0.288 1.069 0.302 9.826 0.002
aP-valuesinboldindicatesignificantrelationships.
doi:10.1371/journal.pone.0141899.t001
witnessedasignificantgreaterchangeinvegetationcompositionafterthetransplant(Fig3;S3
andS5Tables).Ourresultsshowthat,inthelowland,turvesoriginallydominatedbyspecies
withhigherSLAweremorestableastheydidnotchangeconsiderablyintermsofvegetation
compositionunderwarming.Ontheotherhand,inplotsoriginallydominatedbyspecieswith
lowerSLA,speciescharacterizedwithhighSLAreplacedthosewithlowSLAasaresultof
warming(Fig3).
Productivity
Weobservedthattheproductivityinthegrasslandcommunityunderwarmingincreasedwith
diversity(Fig4;Table2),particularlyinthelastharvest.Theresultsofthebestmultipleregres-
sionmodelshowedasignificantpositiveeffectofdiversityonbiomass,exceptforSimpson’s
diversityindex(Table2).
Plantfunctionaltraitcomposition(CWM)alsoseemstoaffectproductivity,eithernega-
tivelyorpositively(Table3).Particularly,inthelowland,biomassproductionincreasedin
communitieswithtallerandlessrhizomatousspecies(estimate=44.85forheight,estimate=
-1091.43forrhizomatouspropagation,S4Table).Whereasinthehighland,biomassincreased
withmorerhizomatousspecies(estimate=136.38,S4Table).Othertraits,suchasSLAand
prostrategrowthpresentedasignificantpositiverelationshipwithbiomass,inboththehigh-
landandthelowland(estimate=71.6,P<0.001forSLAandestimate=405.66,P<0.05for
prostrategrowthform,Table3).OurstepwiseregressionresultsalsoshowedthattheCWM
traits,particularlytheheightandtheproportionofrhizomes,haveagreatereffectonabove-
groundbiomassthandiversity(S4Table).
Discussion
Wefoundthatshort-termclimatewarmingcanhaveagreatimpactonthefunctionalstructure
ofgrasslandcommunities,bothintermsofCWMoftraits(Fig1;Table1)andfunctional
diversity(Fig2;Table1).Nomajorchangesinthehighlandwereobservedalongthegrowing
seasonintermsofCWMoftraitsanddiversity,suggestingthatchangesinthelowlandare
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FunctionalChangesinMountainGrasslandsunderWarming
Fig1.EffectofthetransplantexperimentontheCWMoftraits.EffectofthetransplantexperimentontheCommunityweightedmeans(CWM)ofSLA
(upperleft),%ofrhizomatousspecies(upperright),startoffirstflowering(lowerleft),and%ofprostrateplants(lowerright)alongtime.Theblackpoints
correspondtothelowland,andthewhitepointscorrespondtothehighland.Thewhiskersrefertostandarddeviation.Thexaxisindicatesthedatesofthe
repeatedsamplings(frequency)withineachturf.ThefirstsamplingwasdoneinmidMayandthelastoneinthelowlandatthebeginningofSeptember.For
thecorrespondingstatisticaltestsseeTable1.
doi:10.1371/journal.pone.0141899.g001
relatedtoclimaticstressandnotseasonality.Thesignificantinteraction“transplantxsitex
time”suggestsindeedthatthepatternovertimeisdifferentdependingonwhichhighlandsite
thesamplecamefrom.Whileinsomecasesthisinteractionwassignificant,theestimatesin
Table1wereoftennotveryhighandfromvisualinspectiontheseeffectswerenotstrong.We
thereforeconcludedthattheseeffects,althoughexistingwerenotverymarked.Diversityvari-
ablesandcommunitytraitsshoweddifferentresistanceinfrontofthenewenvironmentalcon-
ditionsinthelowland(Figs1and2).CWMofSLAandstartoffirstfloweringstartedshifting
alreadyafteronlytwoweekswhereasmostoftheothervariableswereresistantforaroundsix
weeks(Figs1and2).Particularly,theproportionofprostratespeciesmanifestedaconsiderable
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FunctionalChangesinMountainGrasslandsunderWarming
Fig2.Effectofthetransplantonthediversityindices.Effectofthetransplantexperimentondiversityindices:Speciesrichness(left),Simpson’s
reciprocaldiversityindexwithequivalentnumbers(centre),andFunctionaldiversity’sindexRaowithequivalentnumbers(left)alongtime.Theblackpoints
correspondtothelowland,andthewhitepointscorrespondtothehighland.Thewhiskersrefertostandarddeviation.SeeFig1formoreinformationon
samplingdatesandTable1forthecorrespondingstatisticaltests.
doi:10.1371/journal.pone.0141899.g002
resistanceuntiltheeighthweekoftheexperimentbeforedeclining(Fig1).Ourresultsalso
showedthattraitswhichprovideopportunisticuseofincreasedresourceavailability(inour
casespecieswithhigherSLA,earlyflowering,erectgrowthhabit,andrhizomatousstrategy)
becamedominantasaresultoftheshort-termclimatechange,whileconservativespecies
becamelessabundantordisappearedfromthesystem(Fig1;Table1).Specieswithhigher
Table2. Resultsofmultipleregressionmodelstoassesstheeffectofthediversityindices(speciesrichnessSR,Simpson’sdiversityindex,func-
tionaldiversityFD)onabove-groundbiomass(finalharvest)andchangesinvegetationcomposition(Bray-Curtis),withtransplant(highlandand
lowland)andsite(p1andp2sitesinthehighland). SeeFig4foragraphicalrepresentationofthebiomassmodels.
Above-groundbiomass Bray-Curtis
Model R2 P Model R2 P
adj. adj.
***a 0.810 *** 0.538
Site 0.741 0.568
Transplant 0.989 0.102
SR 0.144 0.932
SR*transplant 0.008b 0.852
*** 0.690 *** 0.543
Site 0.829 0.325
Transplant 0.803 0.406
Simpson 0.636 0.414
Simpson*transplant 0.405 0.570
*** 0.800 *** 0.540
Site 0.390 0.441
Transplant 0.328 0.592
FD 0.067 0.682
FD*transplant 0.008 0.685
a***P<0.001
bP-valuesinboldindicatesignificantrelationships.
doi:10.1371/journal.pone.0141899.t002
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FunctionalChangesinMountainGrasslandsunderWarming
Fig3.RelationshipbetweentheinitialCWMSLAandthechangeinvegetationcomposition.RelationshipbetweentheinitialCWMSLAandthe
changeinvegetationcomposition(Bray-Curtisdissimilarity)betweenbeginningandendofexperiment,inboththehighlandandthelowland.Theblack
pointscorrespondtothelowland,andthewhitepointscorrespondtothehighland.Solidlinearregressionlinereflectssignificantrelationship(p<0.05)inthe
lowland;andnolinerepresentsnosignificance.
doi:10.1371/journal.pone.0141899.g003
SLA,butnotdiversitycomponents(speciesandfunctionaldiversity),contributedtothestabil-
ityofthegrasslandcommunityunderwarmingconditions(Fig3;Table2andS3Table).In
boththehighlandandthelowland,therewasapositiverelationshipbetweenspeciesrichness
andproductivity.However,inthelowlandthevegetationwasmoreproductiveandlessdiverse
(asfoundbySebastiàetal.[11]).Overalltheresultssuggestthatplantfunctionaltraits,in
termsofCWM,arethemaindriverstotheincreasedproductivityinthelowland.Wediscuss
thesehypothesesandthepatternsdetectedinthefollowingsections.
Communitychanges
Ourresultssuggestthatthewarminginthelowlandfavoredopportunisticerectspecieswith
higherSLA,anticipatedfloweringperiod,andmorerhizomes(Fig1).Itiswidelyacknowledged
thatspeciesfromnutrient-richhabitatshaveagreaterrelativegrowthrate,hencegreaterSLA,
manifestedbyfastresourcecaptureandfastturnoveroforgans[53–55].Mountainareasare
characterizedbylownutrientavailability,wheremineralizationisoftenlimitedbycoldtemper-
atures[56,57].Removingthetemperaturelimitationinthelowlandcausedanincreaseinfast
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 9/17
FunctionalChangesinMountainGrasslandsunderWarming
Fig4.Relationbetweenabove-groundbiomassanddiversityindices.Relationbetweenabove-groundbiomassanddiversityindices:Speciesrichness
(left),Simpson’sdiversityindexwithequivalentnumbers(centre),andFunctionaldiversity’sindexRaowithequivalentnumbers(right)inboththehighland
andthelowland.Theblackpointscorrespondtothelowland,andthewhitepointscorrespondtothehighland.Solidlinearregressionlinereflectssignificant
relationship(p<0.05)betweenthevariablesinthelowland;dashedlinereferstoamarginalsignificantcorrelation(p<0.1)inthehighland;andnoline
representsnosignificance.
doi:10.1371/journal.pone.0141899.g004
growthandresourceacquisitionspecies(e.g.higherSLAandearlierflowering).Earlierflower-
ingoftheplantsasaresponsetowarmingwasalreadyobservedinpreviousstudies[58–60].
DespiteincreasesofSLAasaresponsetoshort-termwarming,itseemstobeunresponsiveto
long-termclimatewarming[61].Thedominanceofspecieswithrhizomesunderwarming
Table3. Resultsofmultipleregressionmodelstoassesstheeffectoftheplantfunctionaltraits(SLA,LDMC,height,startoffirstflowering,%pros-
trate,%rhizomes)onabove-groundbiomass,withtransplant(highlandandlowland)andsite(p1andp2sitesinthehighland).
Above-groundbiomass
Model R2 Estimate Std.Error tvalue P
adj.
Site ***a 0.984 -181.98 28.54 -6.38 <0.001b
Transplant -1683.23 426.60 -3.95 0.001
LDMC 1.49 0.88 1.69 0.111
SLA 71.60 13.48 5.31 <0.001
Prostrate 405.66 181.42 2.24 0.040
Rhizomes 2653.65 265.88 9.98 <0.001
Height -16.46 10.87 -1.51 0.150
Startoffirstflowering -995.52 193.78 -5.14 <0.001
Transplant*rhizomes -2156.80 175.02 -12.32 <0.001
Transplant*height 21.37 9.34 2.29 0.036
Transplant*startoffirstflowering 693.08 137.38 5.05 <0.001
a***P<0.001
bP-valuesinboldindicatesignificantrelationships(P-values<0.05)
doi:10.1371/journal.pone.0141899.t003
PLOSONE|DOI:10.1371/journal.pone.0141899 October29,2015 10/17