Shifts in plant functional composition following long‐term...

Journal of Ecology 20191072133ndash2148 wileyonlinelibrarycomjournaljec emsp|emsp2133copy 2019 The Authors Journal of Ecology copy 2019 British Ecological Society

Received28January2019emsp |emsp Accepted17April2019DOI 1011111365-274513252

I S P H Y L O G E N E T I C A N D F U N C T I O N A L T R A I T D I V E R S I T Y A D R I V E R O R C O N S E Q U E N C E O F G R A S S L A N D C O M M U N I T Y A S S E M B LY

Shifts in plant functional composition following long‐term drought in grasslands

Robert J Griffin‐Nolan1 emsp| Dana M Blumenthal2emsp| Scott L Collins3emsp| Timothy E Farkas3emsp| Ava M Hoffman1 emsp| Kevin E Mueller4emsp| Troy W Ocheltree5emsp| Melinda D Smith1 emsp| Kenneth D Whitney3 emsp| Alan K Knapp1

1GraduateDegreePrograminEcologyandDepartmentofBiologyColoradoStateUniversityFortCollinsColorado2RangelandResourcesandSystemResearchUnitUSDAAgriculturalResearchServiceFortCollinsColorado3DepartmentofBiologyUniversityofNewMexicoAlbuquerqueNMUSA4DepartmentofBiologicalGeologicalandEnvironmentalSciencesClevelandStateUniversityClevelandOhio5DepartmentofForestandRangelandStewardshipColoradoStateUniversityFortCollinsColorado

CorrespondenceRobertJGriffin‐NolanEmailrgriffi2colostateedu

Funding informationNSFMacrosystemsBiologyProgramGrantAwardNumberDEB‐11373781137363and 1137342

HandlingEditorHollyJones

Abstract1 PlanttraitscanprovideuniqueinsightsintoplantperformanceatthecommunityscaleFunctionalcompositiondefinedbybothfunctionaldiversityandcommunity‐weightedtraitmeans(CWMs)canaffectthestabilityofabove‐groundnetprimaryproduction (ANPP) in response to climate extremes Further complexity ariseshoweverwhenfunctionalcomposition itself respondstoenvironmentalchangeThedurationofclimateextremessuchasdrought isexpectedto increasewithrisingglobaltemperaturesthusunderstandingtheimpactsoflong‐termdroughton functional composition and the corresponding effect that has on ecosystemfunctioncouldimprovepredictionsofecosystemsensitivitytoclimatechange

2 Weexperimentallyreducedgrowingseasonprecipitationby66acrosssixtem-perategrasslandsfor4yearsandmeasuredchangesinthreeindicesoffunctionaldiversity (functional dispersion richness and evenness) community‐weightedtraitmeansandphylogeneticdiversity(PD)Specificleafarea(SLA)leafnitrogencontent(LNC)and(atmostsites)leafturgorlosspoint(πTLP)weremeasuredforspeciescumulativelyrepresenting~90plantcoverateachsite

3 Long‐term drought led to increased community functional dispersion in threesiteswithnegligibleeffectsontheremainingsitesSpeciesre‐orderingfollowingthemortalitysenescenceofdominantspecieswasthemaindriverof increasedfunctionaldispersionTheresponseoffunctionaldiversitywasnotconsistentlymatchedbychanges inphylogeneticdiversityCommunity‐leveldroughtstrate-gies(assessedasCWMs)largelyshiftedfromdroughttolerancetodroughtavoid-anceandorescapestrategiesasevidencedbyhighercommunity‐weightedπTLPSLA and LNC Lastly ecosystem drought sensitivity (ie relative reduction inANPPindroughtplots)waspositivelycorrelatedwithcommunity‐weightedSLAandnegativelycorrelatedwithfunctionaldiversity

4 SynthesisIncreasedfunctionaldiversityfollowinglong‐termdroughtmaystabilizeecosystemfunctioninginresponsetofuturedroughtHowevershiftsincommu-nity‐scaledroughtstrategiesmayincreaseecosystemdroughtsensitivitydepend-ingonthenatureandtimingofdroughtThusourresultshighlighttheimportance

2134emsp |emsp emspenspJournal of Ecology GRIFFIN‐NOLAN et AL

1emsp |emspINTRODUC TION

Ecosystemfunctionislargelydeterminedbythefunctionalattributesof residentplant speciesPlant traitsareuseful forunderstandinghow resources are acquired by plants (Reich 2014Wright et al2004)andconsequentlytransferredtoorstoredinvariousecosys-tempools suchasplantbiomassorsoilorganicmatter (LavorelampGarnier 2002) Plant community functional composition definedbycommunity‐weightedtraitmeans (CWMs)andfunctionaldiver-sity(iethedistributionoftraitswithinacommunity)respondstoenvironmentalchangeandcanaffectecosystemprocessessuchasabove‐groundnetprimaryproduction(ANPP)nutrientcyclinganddecomposition(DiacuteazampCabido2001)Atrait‐basedresponse‐and‐effectframeworkhasbeenproposed(Sudingetal2008)wherebycertainplant traits indicatehowspecieswill shift inabundance inresponse to environmental change (eg conservative leaf watereconomictraitsimprovespeciestolerancetodroughtandwarmingAnderegg et al 2016 Soudzilovskaia et al 2013)whereasothertraits(orthesametraits)arelinkedtospecificecosystemfunctions(eg leaf nitrogen content [LNC] is correlated with variability inANPPGarnieretal2004Reich2012)Theimportanceofclimatein governing functional composition iswell supportedby commu-nityscalesurveysofplanttraitsonbroadspatialandtemporalscales(Newbold Butchart Şekercioǧlu Purves amp Scharlemann 2012ReichampOleksyn2004Šiacutemovaacuteetal2018Wieczynskietal2019Wright et al 2005) Few studies however have assessed the re-sponseofbothfunctionaldiversityandCWMstoclimateextremeswhich are rare by definition (Smith 2011) and the correspondingeffectonecosystemfunctioningacrossspaceandtime

Risingglobaltemperaturesincreaseratesofevapotranspirationand thus the intensity and duration of climate extremes such asdrought(Trenberth2011)withimmediateandlong‐lastingnegativeimpactsonEarthsvegetation (Breshearsetal2005)Themagni-tudeofvegetationresponsestodroughtvariesamongecosystemswith xeric ecosystems generally being more sensitive than mesicones(Huxmanetal2004Knappetal2015)Ecosystemresistanceandresiliencetodroughthavebeenlinkedtospeciesdiversityandfunctionaldiversityinparticular(DiacuteazampCabido2001Isbelletal2015TilmanampDowning1994Tilmanetal1997)Plantcommu-nities with high functional diversity are buffered against declinesinecosystemfunctionssuchasANPPduetofunctionalinsurance(Andereggetal2018DeLaRivaetal2017Grime1998Peacuterez‐Ramosetal2017)Inotherwordsagreaterdiversityofspecies(and

traits)increasestheoddsofoneormorespeciessurvivingadroughtandcompensatingfordrought‐inducedsenescenceormortalityofotherspeciesBeyonddiversitythemeancompositionoftraits(asmeasuredbyCWMs)canconferecosystemresistanceandresiliencetodroughtespeciallyifspecieswithtraitslinkedtodroughtsurvival(McDowelletal2008)andordroughtavoidanceescapestrategies(Kooyers2015Noy‐Meir1973)areinhighabundance

Increasing complexity arises howeverwhen functional com-positionitselfisalteredbydroughtAnextremeclimateeventcanact as an environmental filter allowing only certain species (andtrait values) to persist potentially leading to trait convergenceandor decreased functional and genetic diversity (Diacuteaz CabidoZakMartiacutenezCarreteroampAraniacutebar1999Grime2006Whitneyet al 2019) however an array of biotic interactions influencingcompetitioncoexistenceandnichedifferentiationcanactsimulta-neouslytostructurecommunitiesinanoppositemanner(CadotteampTucker2017Kraftetal2015)Thusgivenuncertainandcoun-teractingrolesofenvironmentalfilteringandnichedifferentiationtheneteffectsofdroughtoncommunity functionalcompositionare currently unpredictable Indeed the impact of drought andariditymorebroadlyonfunctionaldiversityishighlyvariablewithpositive (Cantarel Bloor amp Soussana 2013) negative (Qi et al2015)andneutral(Copelandetal2016HallettSteinampSuding2017)responsesobservedTheseinconsistenciesarelikelyduetodifferencesintheselectionoftraitsandfunctionaldiversityindi-cestheextremityofdroughtandorthespatialtemporalcontextinwhich aridity is being examined Thus coordinated long‐termandmulti‐siteexperimentsareneededtoassesstheimpactofex-tremedroughtonfunctionalcompositionandecosystemfunction

The lsquoExtreme Drought in Grasslands Experimentrsquo (EDGE) wasestablishedin2012toassessthedroughtsensitivityofANPPinsixNorthAmerican grasslands ranging fromdesert grassland to tall-grass prairie (Figure 1 Table 1) Grasslands are ideal ecosystemsforassessingdroughtsensitivityasANPPinthesesystemsishighlyresponsive toprecipitationvariability (HsuPowellampAdler2012Knappamp Smith 2001) and their short stature allows for easy in-stallationof experimental drought infrastructure (YahdjianampSala2002) We surveyed plant traits of the most common species ateachEDGE site (cumulatively representing~90plant cover) andtracked changes in three indicesof functional diversity (eg func-tionaldispersionrichnessandevenness)andabundance‐weightedtraitsinresponsetoa4‐yearexperimentaldroughtOurtraitsurveyincludedleafturgorlosspoint(πTLP)specificleafarea(SLA)andLNC

ofconsideringbothfunctionaldiversityandabundance‐weightedtraitsmeansofplantcommunitiesastheircollectiveeffectmayeitherstabilizeorenhanceeco-systemsensitivitytodrought

K E Y W O R D S

ANPPclimatechangecommunity‐weightedtraitsdroughtfunctionaldiversityplantfunctionaltraits

emspensp emsp | emsp2135Journal of EcologyGRIFFIN‐NOLAN et AL

LeafeconomictraitssuchasSLAandLNChavebeenassociatedwithplantecologicalstrategies(egfastvsslowresourceeconomiesanddroughttolerancevsavoidanceFrenette‐DussaultShipleyLeacutegerMezianeampHingrat2012Reich2014)andaredescriptiveofANPPdynamics (Garnier et al 2004 Reich 2012 Suding et al 2008)Hydraulic traits such as πTLP are informative of leaf‐level droughttoleranceandareexpected tobepredictiveofplant responses toaridity (Bartlett Scoffoniamp Sack 2012Griffin‐NolanBushey etal2018Reich2014)Additionallywemeasuredplot‐levelphyloge-neticdiversitytoassesswhetherfunctionalandphylogeneticdiver-sityarecoupledintheirresponsetodrought(iewhetherdecreasedfunctionaldiversityisdrivenbydecreasedgeneticdissimilarity)

Droughtresistanceismultidimensional(ieavarietyoftraitscanbestoworhinderdrought resistanceviaavarietyofmechanisms)thusthereareseveralplausibleshiftsintraitdiversityandweighted‐means in response to drought Herewe test the hypothesis thathighfunctionaldiversityandahighabundanceofconservativeleafeconomictraitsconfergreaterresistanceofANPPtodroughtandask how drought influences functional composition over time Astrongroleofenvironmentalfilteringshouldbereflectedinreduced

functional diversity and altered community‐weighted trait meanswith the direction of the mean trait shift dependent on the roleof various traits in shaping drought resistance within and acrossecosystems

2emsp |emspMATERIAL S AND METHODS

21emsp|emspSite descriptions

The impact of long‐term drought on community functional di-versityandabundance‐weightedtraitswasassessedinsixnativegrasslandsitesspanninga620mmgradient inmeanannualpre-cipitation(MAP)anda55degCgradientinmeanannualtemperature(Table1Knappetal2015)Thesesixsitesencompassthefourmajor grassland types of North America including desert grass-land shortgrass prairiemixed grass prairie and tallgrass prairieExperimentalplotswereestablished inuplandpasturesthathadnotbeengrazedforover10yearsapartfromthetwomixedgrassprairiesites(HPGandHYS)whichwerelastgrazed3yearspriorto this study The tallgrass prairie site (KNZ) is burned annually

F I G U R E 1 emsp (a)LargerainfallexclusionshelterswereestablishedinsixNorthAmericangrasslandsitesaspartoftheExtremeDroughtinGrasslandsExperiment(EDGEhttpedgebiologycolostateedu)(b)Theseshelterspassivelyremove66ofincomingprecipitationduringthegrowingseasonleadingtoa~40reductioninannualprecipitationfor4years(errorbarsrepresentSEofmeanprecipitationduringthe4years)Droughttreatmentshadnegativeeffectsonabove‐groundnetprimaryproductioninallsitesrangingfromtheSevilletadesertgrassland(SBK)inNewMexico(cphotocreditScottCollins)totheKonzatallgrassprairie(KNZ)ineasternKansas(dphotocreditAlanKnapp)SeeTable1forsiteabbreviations[Colourfigurecanbeviewedatwileyonlinelibrarycom]


followingregionalmanagementregimes(KnappBriggsHartnettampCollins1998)whereasothersitesareunburnedSoiltexturesvaryacrosssitesfromsandytoclay‐loam(Burkeetal19911989Kieftetal1998)

22emsp|emspExperimental drought treatments

Droughtwasexperimentallyimposedateachsitefor4yearsusinglarge rainfall exclusion shelters (Figure1aYahdjianampSala2002)At each site twenty 36‐m2 plotswere established across a topo-graphically uniform area and hydrologically isolated from the sur-rounding soil matrix using aluminium flashing and 6‐mil plasticbarriersinstalledtoadepthofatleast20cmPlotsweresplitinto4subplotseach25times25mwitha05mbufferoneachsideTwoofthesesubplotsweredesignatedfordestructivemeasurementsofplantbiomassonewasdesignated fornon‐destructive surveysofspeciescompositionandthefinalsubplotwasleftforresearchondecompositionandmicrobialcommunities (Fernandesetal2018Ochoa‐Huesoetal2018)

Droughtwasimposedintenplotspersitebyinstallinglargeshel-ters(10times10m2)whichpassivelyblocked66ofincomingrainfallduring each growing seasonmdashthis is roughly equivalent to a 40reductioninannualprecipitationgiventhat60ndash75ofMAPfallsduringthegrowingseasonintheseecosystems(April‐SeptemberforSGSHPGHYSandKNZApril‐OctoberforSBKandSBL)Rainfallexclusionsheltersutilizetransparentpolyethylenepanelsarrayedatadensitytoreduceeachrainfalleventby66therebymaintainingthenatural precipitationpatternof each site (Knappet al 2017)Theremainingtenplotspersitewere trenchedandhydrologicallyisolatedyetreceivedambientrainfall(ienoshelterswerepresent)Treatment infrastructure was installed in the spring of 2012 yetdroughttreatmentsdidnotbeginuntilApril2013attheNewMexicosites(SBKandSBL)and2014atthenorthernsites(SGSHPGHYSandKNZ)

Raingaugeswereestablished in a subsetof control and treat-mentplotsRainfallexclusionsheltersreducedannualprecipitationby~40relativetoambientamountacrossallsixsites(Figure1b)arelativereductioncomparabletotheextremedroughtthataffectedthis region in 2012 (the 4th largest drought in the past centuryKnapp et al 2015) However the experimental drought imposedherelasted4yearsratherthanone

23emsp|emspSpecies composition

Species composition was assessed at each site during spring andfall of each year starting one year before treatments were im-posedAbsoluteaerialcoverofeachspecieswasestimatedvisuallywithin four quadrats (1 m2) placed within the subplot designatedfornon‐destructivemeasurementsForeachplotandspeciesab-solutecoverwasconvertedtoaveragepercentrelativecoverwiththehighercovervalueineachyear(springorfall)usedinthefinalanalysis(KoernerampCollins2014)Attheendofeachgrowingsea-son in the four northern sites all above‐groundbiomasswashar-vestedinthreequadrats(01m2)whichwereplacedrandomlyinoneoftwosubplotsdesignatedfordestructivemeasurements(alteringbetweenyears)Biomasswassortedtoremovethepreviousyearsgrowthdriedfor48hrat60degCandweighedtoestimatetotalANPPAtthetwoSevilletasites(SBKandSBL)above‐groundbiomasswasestimated in springand fallusinganon‐destructiveallometricap-proach(Muldavinetal2008)foreachspeciesoccurringineachofthespeciescompositionsubplots

24emsp|emspPlant traits

Traitsofthemostabundantplantspeciespersiteweremeasuredinanareaadjacenttoexperimentalplotstoavoiddestructivemeasure-mentswithin plots Thus all traitsweremeasured under ambientrainfallconditionsPlanttraitsweremeasuredatdifferenttimesof

TA B L E 1 emspCharacteristicsofsixgrasslandsitesincludedinthelsquoExtremeDroughtinGrasslandsExperimentrsquo(EDGE)Five‐yearaveragesofShannonsdiversityindexandspeciesrichnessareshownforambientplotsateachsiteMeanannualprecipitation(MAP)andtemperature(MAT)weretakenfromGriffin‐NolanCarrolletal(2018)

Sitea Grassland typeMAP (mm)

MAT (degC)

Shannon Diversity

Species Richness

SevilletaBlackGrama(SBK) Desert 244 134 204 10

SevilletaBlueGrama(SBL) Shortgrass 257 134 339 12

ShortgrassSteppe(SGS) Shortgrass 366 95 579 17

HighPlainsGrassland(HPG) Mixed-Grass 415 79 825 23

HaysAgriculturalResearchCenter(HYS) Mixed-Grass 581 123 752 23

KonzaPrairie(KNZ) Tallgrass 864 130 614 16

aSitesincludeadesertgrassland[SevilletaNationalWildlifeRefugedominatedbyblackgramaBouteloua eriopoda(C4)mdashSBK]andasouthernShortgrassSteppe[SevilletaNationalWildlifeRefugedominatedbybluegrama(Bouteloua gracilis(C4))ndashSBL]bothinNewMexicoanorthernShortgrassSteppe[CentralPlainsExperimentalRangedominatedbyB gracilismdashSGS]inColoradoanorthernmixed‐grassprairie[HighPlainsGrasslandResearchCenterco‐dominatedbyPascopyron smithii(C3)andB gracilismdashHPG]inWyomingaswellasasouthernmixed‐grassprairie[HaysAgriculturalResearchCenterco‐dominatedbyP smithiiBouteloua curtipendula(C4)andSporobolus asper(C4)mdashHYS]andatallgrassprairie[KonzaPrairieBiologicalStationdominatedbyAndropogon gerardii(C4)andSorghastrum nutans(C4)mdashKNZ]bothinKansas


thegrowingseasontocapturepeakgrowthandhydratedsoilmois-tureconditionsForSBKandSBLtraitsweremeasuredatthebe-ginningofthe2017monsoonseason(earlyAugust)toensurefullyemerged green leaveswere sampled For SGS andHPG all traitsweremeasured in lateMayandearlyJuneof2015tocapturethehighabundanceofC3speciesatthesesitesForHYSandKNZtraitsweremeasuredinmid‐July2015duringpeakbiomass

Tenindividualswereselectedalongatransectthelengthoftheexperimental infrastructure and two recently emerged fully ex-pandedleaveswereclippedatthebaseofthepetioleandplacedinplasticbagscontainingamoistpapertowelLeaves(n=20perspe-cies)wererehydratedinthelabscannedandleafareawasestimatedusingImageJsoftware(httpsimagejnihgovij)Eachleafwasthenoven‐driedfor48hrat60degCandweighedSpecificleafarea(SLA)wascalculatedasleafarealeafdrymass(m2kg)DriedleafsampleswerethengroundtoafinepowderfortissuenutrientanalysesLNCwasestimatedonamassbasisusingaLECOTru‐SpecCNanalyser(LecoCorp)

Leafturgorlosspoint(πTLP)wasestimatedforeachspeciesusingavapourpressureosmometer(BartlettScoffoniArdyetal2012Griffin‐Nolan Blumenthal et al 2019) Briefly a single tiller (forgraminoids)orwholeindividual(forforbsandshrubs)wasunearthedtoincluderoottissueandplacedinareservoirofwaterWholeplantsamples(n=6species)wererelocatedtothelabandcoveredinadarkplasticbag for~12hr toallowforcomplete leaf rehydrationLeaftissuewasthensampledfrom5ndash8leavesspeciesusingabiopsypunchTheleafsamplewaswrappedintinfoilandsubmergedinliq-uidnitrogenfor60storupturecellwallsEachdiscwasthenpunc-tured~15timesusingforcepstoensurecelllysisandquicklyplacedin a vapour pressure osmometer chamberwithin 30 s of freezing(VAPRO5520Wescor) Sampleswere left in the closed chamberfor~10mintoallowequilibrationMeasurementswerethenmadeeverytwominutesuntilosmolarityreachedequilibrium(lt5mmolkgchangeinosmolaritybetweenmeasurements)Osmolaritywasthenconverted to leaf osmotic potential at full turgor (πo) (πo = osmo-laritytimesminus239581000)andfurtherconvertedtoπTLPusingalinearmodeldevelopedspecificallyforherbaceousspecies(Griffin‐NolanOcheltreeetal2019)πTLP = 080πominus0845

Estimatesoffunctionaldiversityarehighlysensitivetomissingtraitdata(Pakeman2014)Oursurveyofplanttraitsfailedtocap-ture species that increased in abundance inotheryearsordue totreatmenteffectsThuswefilledinmissingtraitdatausingavarietyofsourcesincludingpublishedmanuscriptsorcontributeddatasetsSampling year differed depending on data sources but samplingmethodologiesfollowedthesameorsimilarstandardizedprotocols(BartlettScoffoniArdyetal2012Griffin‐NolanOcheltreeetal2019Perez‐Harguindeguyetal2016)andtraitswereoftenmea-suredduringthesameseasonandfromplotsadjacenttoornearbytheEDGEplots(seeAppendixS1insupportinginformationformoredetails)DataforπTLPwerelackingfordesertspeciescommonintheSevilletagrassland (SBKandSBL) thusouranalysesat thesesiteswasconstrainedtoSLAandLNCForthenorthernsites(SGSHPG

HYSandKNZ)sufficientπTLPdatawereavailableandwereincludedin all analyses

The final trait dataset included trait values for species cumu-latively representing an average of 90 plant cover in each plotObservationswithlessthan75relativecoverrepresentedbytraitdatawereremovedfromallanalyses(21of600plot‐yearcombina-tionswere removed final range75ndash100plant coverplot) Forthiscoresetof579observationsthenumberofspeciesusedtoes-timateindicesoffunctionalcompositionrangedfrom11to37withameanof28speciesCovariationbetweentraitswastestedacrosssitesusinglog‐transformeddata(lsquocorrsquofunctioninbaseR)Asignifi-cantcorrelationwasobservedbetweenLNCandπTLP(r=292)butnotbetweenSLAandπTLP(r=014)orSLAandLNC(r=minus117)

25emsp|emspFunctional composition

Functionaldiversityisdescribedbyseveralindiceseachofwhichdescribedifferentaspectsof traitdistributionswithinacommu-nity (Mason De Bello Mouillot Pavoine amp Dray 2013) Givenuncertainty as towhich index ismost sensitive to drought andor informativeofecosystemresponses todrought (Botta‐Dukaacutet2005CarmonaBelloMasonampLepš2016LaliberteampLegendre2010Masonet al 2013MasonMacGillivray SteelampWilson2003PetcheyampGaston2002VilleacutegerMasonampMouillot2008)wecalculatedthreeseparateindicesoffunctionaldiversityusingthe dbFD function in the lsquoFDrsquo R‐package (Laliberteacute amp Legendre2010LaliberteacuteLegendreShipleyampLaliberteacute2014)Usingaflex-ible distance‐based framework and principle components analy-ses the dbFD function estimates functional richness (FRic thetotal volume of x‐dimensional functional space occupied by thecommunity) functionalevenness (FEvetheregularityofspacingbetween species within multivariate trait space) and functionaldispersion (FDis the multivariate equivalent of mean absolutedeviation in trait space) (Laliberteamp Legendre 2010Villeacuteger etal2008)FDisdescribesthespreadofspecieswithinmultivariatespaceandiscalculatedasthemean‐weighteddistanceofaspeciesto the community‐weighted centroid ofmultivariate trait spaceTo control for any bias caused by the lack of πTLP data for twosites(SBKandSBL)wealsocalculatedFRicFEveandFDisusingjusttwotraits(SLAandLNC)acrosssites(ietwo‐dimensionaldi-versity)Multivariate functional diversity indices can potentiallymask community assembly processes occurring on a single traitaxis (SpasojevicampSuding2012)thusFRicFEveandFDiswerealsoestimatedseparatelyforeachofthethreetraitssurveyedinthisstudy

SpeciesrichnessiswellcorrelatedwithbothFRicandFDisandcanhaveastrongeffectontheestimationsoftheseparametersespeciallyincommunitieswithlowspeciesrichness(Masonetal2013) To control for this effectwe compared our estimates ofFRic andFDis to those estimated from randomly generatednullcommunities and calculated standardized effect sizes (SES) foreachplot


where themean and standard deviation of expected FDis (or FRic)were calculated from 999 randomly generated null communityma-tricesusingalsquoname‐swaprsquoandlsquoindependent‐swaprsquoalgorithmforFDisandFRicrespectively(RcodemodifiedfromSwenson2014)Thesenullmodelalgorithmsrandomizethetraitdatamatrixwhilemaintain-ingspeciesrichnessandoccupancywithineachplotThelsquoname‐swaprsquomethodalsomaintainsrelativeabundancewithineachplotthuspro-vidinginsightintoprocessesstructuringplantcommunities(SpasojevicampSuding2012)ObservedFEve is independentof species richnessandthuswasnotcomparedtonullcommunities(Masonetal2013)

We also calculated community‐weighted means (CWMs) foreach trait (weightedbyspecies relativeabundance)which furthercharacterizes the functional composition of the community Eachindex of functional diversity and CWMs was measured for eachplot‐year combination using the fixed trait dataset (ie traits col-lectedin20152017pluscontributeddata)andcoverdatafromeach year Thus the responses ofCWMsand functional diversitytodroughtrepresentspeciesturnoverandinterspecifictraitdiffer-encesIntraspecifictraitvariabilityandtraitplasticitywerenotas-sessedinthisstudybutthesetypicallycontributesubstantiallylesstototaltraitvariationthaninterspecifictraitvariabilityevenwhensamplingacrossbroadspatialscalesandstrongenvironmentalgra-dients(Siefertetal2015)

26emsp|emspPhylogenetic diversity

Wequantified phylogenetic distinctiveness at the plot level usingFaithsphylogeneticdiversity(PD)index(Faith1992)Amixtureofnineproteincodingandnon‐codinggenesequenceswereacquiredfromNCBIGenBankforeachspeciesFollowingsequencealignmentand trimming maximum likelihood trees were constructed usingRAxML(1000bootstrapiterationswithPhyscomitrella patensastreeoutgroup)(version8210)(Stamakis2014)Followingtreeconstruc-tionPDwascalculatedusingthepIcantepackageinR(Kembeletal2010)Tocontrolfortheeffectofspeciesrichnessthestandardizedeffectsize(SES)ofPD(PDses)wascalculatedusingthelsquoindependentswaprsquonullmodelinthepIcantepackage

27emsp|emspData analysis

We tested for interactive effects of treatment year and site onfunctionalphylogenetic composition using repeated measuresmixed effectsmodels (lsquolme4rsquo packageBatesMaumlchler BolkerampWalker2014)Sitetreatmentandyearwereincludedasfixedef-fects andplotwas included as a randomeffect Trait datawerelog‐transformedwhennecessarytomeetassumptionsofnormal-ity Separate models were run for multivariate and single traitfunctional richness and dispersion (FDisses and FRicses) FEvephylogeneticdiversity(PDses)aswellaseachCWM(ieSLALNC

and πTLP)Pairwisecomparisonsweremadebetweendroughtandcontrol plotswithineachyear and for each site (Tukey‐adjustedp‐values are presented) With the exception of xeric sites (egSevilleta) ambient temporal changes in species composition areoftengreaterthantreatmenteffectsinglobalchangeexperiments(Langleyetal2018) therefore functional andphylogenetic re-sponsestodroughtarepresentedhereaseitherlogresponseratios(ln(droughtcontrol))forFEveandCWMsortreatmentdifferences(iedroughtmdashcontrol)forPDsesFDissesandFRicsesCalculatinglogresponseratiosofSESvalueswasnotappropriateasSESisoftennegativeNegativelogresponseratiosareshownforcommunity‐weightedπTLPasthistrait ismeasuredinnegativepressureunits(MPa)All analyseswere repeated for two‐dimensional diversityindices(iethoseincludingjustSLAandLNC)

ThesensitivityofANPPtodroughtwascalculatedasthere-ductioninANPPindroughtplotsforeachsiteandforeachyearasfollows

whereANPPisthemeanvalueacrossallplotsofthattreatmentin a given year Drought sensitivity is presented as an absolutevalue(abs)suchthatlargepositivevaluesindicategreatersensitiv-ity(iegreaterrelativereductioninANPP)Correlationsbetweenannualdroughtsensitivity(n=24sixsitesand4years)andeithercurrent‐year (cy) or previous‐year (py) functionalphylogeneticcomposition indices (eg PDses CWMs for each trait aswell assingletraitandmultivariateFDissesFRicsesandFEve)wereinves-tigatedusingthecor function inbaseRwithp‐valuescomparedtoaBenjaminndashHochbergcorrectedsignificancelevelofα = 0047 for 32 comparisons Variables that were significantly correlatedwithdroughtsensitivityatthislevelwereincludedasfixedeffectsinseparategenerallinearmixedeffectsmodelswithsiteincludedas a random effect To avoid pseudo‐replication mixed effectsmodelswerethencomparedtonullmodels(usingAIC)wherenullmodelsincludedonlytherandomeffectofsiteBothmarginalandconditionalR2values(NakagawaampSchielzeth2013)werecalcu-latedforeachmixedeffectmodelusingthelsquorsquaredrsquofunctioninthe lsquopiecewiseSEMrsquo package (Lefcheck 2016) All analyseswererunusingRversion352

3emsp |emspRESULTS

The experimental drought treatments significantly altered com-munity functional and phylogenetic composition with significantthree‐way interactions inmixed effectsmodels for each diversityindex except FRicses and each abundance‐weighted trait (treat-menttimessitetimesyearTable2)Thesixgrasslandsitesvariedextensivelyin themagnitude and directionality of their response to droughtvariationthatwasassociatedwithdiversityindextraitidentityand

SES=observed FDisminusmean of expected FDis

standard deviation of expected FDis

Drought sensitivity=abs

(

100timesANPPdroughtminusANPPcontrol

ANPPcontrol

)


drought duration The most responsive functional diversity indexacross sites was functional dispersion (FDisses) with significantdroughtresponsesobservedinallbuttwosites

Four years of experimental drought led to significantly highermultivariateFDissesinhalfofthesites(SBKSGSandHYS)withonlyaslightdeclineinFDissesobservedatSBLinyear3ofthedrought(Figure2a)TherewerenoobservabletreatmenteffectsonFDisses at thewettest site (KNZ) or at the coolest site (HPG) Single traitFDisses did not consistently mirror multivariate FDisses especiallyatthethreedriestsites (Figure2bndashd)For instancethe increase inFDisses at SBK was largely driven by increased functional disper-sionofLNC(Figure2c)asFDissesofSLAdidnotdiffersignificantlybetween drought and control plots For SBL multivariate FDisses masked the opposing responses of single trait FDisses In the firsttwoyearsofdroughtoppositeresponsesofFDissesofSLAandLNCcanceledeachotheroutleadingtonochangeinmultivariateFDisses Itwasnotuntilyear3thatFDissesofbothSLAandLNCdeclinedatSBLleadingtoasignificantresponseinmultivariateFDissesForSGSFDisses of SLA increased in drought plots relative to control plotsand remained significantly higher for the remainder of the exper-iment (Figure2b)however this relative increase inFDissesofSLAwasnotcapturedinmultivariatemeasuresofFDissesduetoalackofresponseofFDissesofLNCandπTLPuntilthefinalyearsofdrought(Figure 2cd)On the contrary single trait FDisses largelymirroredmultivariate FDisses for the three wettest sites with positive re-sponsesofFDissesforeachtraitatHYSandnosignificantresponsesobserved atHPG andKNZ (Figure 2)Other indices of functionaldiversity(ieFRicsesandFEve)weremoderatelyaffectedbydroughttreatments depending on site with treatment effects not consis-tent acrossyears (seeAppendixS2FiguresS1andS2)Estimatesoffunctionaldiversityintwo‐dimensionaltraitspace(ieexcludingπTLPfromestimatesofFDissesFRicsesandFEveacrosssites)didnotdiffer drastically from estimates in three‐dimensional trait space(AppendixS2andFigureS3)

Experimentaldrought ledtoasignificantshift incommunity‐weightedtraitmeansacrosssiteslargelyawayfromconservative

resource‐use strategies (Figure3)Community‐weighted specificleafarea(SLAcw)initiallydecreasedinresponsetodroughtfortwosites (SBK and SBL) however long‐term drought eventually ledto significant increases in SLAcw at all six sites relative to ambi-entplots(Figure3a)ThepositiveeffectofdroughtonSLAcw was notpersistentinitssignificanceormagnitudethroughthefourthyear of the experiment for all the sites Community‐weightedLNC (LNCcw) was unchanged until the final years of drought atwhich point elevated LNCcwwas observed for all sites but KNZ(Figure 3b) Lastly drought effects on community‐weighted leafturgorlosspoint(πTLP‐cw)werevariableamongsiteswithasignif-icant decline in πTLP‐cw (iemore negative) atHPG a significantincrease in πTLP‐cwatSGSamoderatelysignificantincreaseatHYS(p=06)andnochangeobservedatKNZ(Figure3c)

Phylogeneticdiversity (PDses)wasmostsensitivetodroughtatthe twodriest sites SBKandSBLwith variableeffectsobservedatthewettestsiteKNZ(Figure4)DroughtledtoincreasedPDses atSBKinyear3anddecreasedPDsesatSBLinyear4(Figure4)AtKNZ PDses alternated between drought‐induced declines in PDses and no difference between control and drought plots howeverPDsesofdroughtplotswassignificantlylowerthancontrolplotsbythefourthyearofdroughtPDsesdidnotrespondtodroughttreat-mentsatSGSHPGorHYS

Acrossall32linearmodelsruntheonlysignificantpredictorsof ANPP sensitivity (following a BenjaminndashHochberg correctionformultiplecomparisons)were(a)SLAcwofthepreviousyear(b)FEveofSLAof thecurrentyearand (c)multivariateFEveof thecurrent year (TableS2)Thesepredictorswere includedas fixedeffectsinseparatemixedeffectsmodelseachwithsiteasaran-domeffect Followingnullmodel comparison (seemethods)weobserved a statistically significant positive relationshipbetweendroughtsensitivityandpreviousyearSLAcw (Figure5a) InotherwordsgrasslandcommunitieswithlowSLAcw inagivenyearex-perienced less drought‐induced declines in ANPP the followingyear Significant negative correlations were observed betweencurrentyearFEve(bothmultivariateandFEveofSLA)anddrought

TA B L E 2 emspANOVAtableformixedeffectsmodelsforthestandardizedeffectsize(SES)ofmultivariatefunctionaldiversitycommunity‐weightedtraitmeansandSESofphylogeneticdiversity

Effect

SES of functional and phylogenetic diversity Community‐weighted trait means

FDis FRic FEve PD SLA LNC πTLP

Trt 368 00001 364 0075 2732 699 0002

Site 1531 019 1291 5122 33974 61562 28613

Year 1102 326 144 1118 3344 5806 12219

TrttimesSite 243 211 051 172 348 026 630

TrttimesYear 1198 047 152 351 1502 2829 234

SitetimesYear 3034 253 307 866 2672 3270 6254

TrttimesSitetimesYear 721 089 217 176 913 712 352

Note F‐valuesareshownforfixedeffectsandallinteractionsStatisticalsignificanceisrepresentedbyasterisksplt05plt01plt001AbbreviationsFDisfunctionaldispersionFEvefunctionalevennessFRicfunctionalrichnessLNCleafnitrogencontentPDphylogeneticdiver-sitySLAspecificleafareaπTLPleafturgorlosspoint


sensitivityhowevernullmodelcomparisons rejected themodelwithmultivariateFEveandacceptedthemodelwithFEveofSLA(Figure5bTableS2)

4emsp |emspDISCUSSION

41emsp|emspFunctional diversity

Weassessedtheimpactof long‐termdroughtonfunctionaldiver-sityofsixNorthAmericangrasslandcommunities(Table1)Removalof ~40of annual rainfall for 4 years negatively impactedANPP(Figures1and5)Incontrastweobservedpositiveeffectsofdroughtonfunctionaldispersion(ascomparedtonullcommunitiesFDisses)in half of the grasslands surveyedherewith anegative responseobservedinonlyonesite(Figure2)Whileseveralindicesoffunc-tionaldiversityweremeasured inthisstudyFDisseswasthemostresponsivetodrought (Figure2andTable2) Increasedfunctional

diversityfollowingdroughthaspreviouslybeenattributedtomech-anisms of niche differentiation and species coexistence (Grime2006)whereasdeclinesindiversityareattributedtodroughtactingasanenvironmental filter (DiazCabidoampCasanoves1998Diacuteazetal1999Whitneyetal2019)Ingrasslandsseveral indicesoffunctional diversity respond strongly to interannual variability inprecipitation (GherardiampSala2015)Dryyearsoften lead to lowfunctionaldiversityas thedominantdrought‐tolerantgrassesper-sistwhereasrarespeciesexhibitdroughtavoidance(egincreasedwater‐useefficiencyandslowergrowth)orescapestrategies (egearlyflowering)(GherardiampSala2015Kooyers2015)Wetyearshowevercanleadtohighdiversityduetonegativelegaciesofdryyearsactingondominantgrassesandthefastgrowthrateofdroughtavoiderswhichtakeadvantageoflargeraineventsthatpenetratedeepersoilprofiles (GherardiampSala2015)While traits linked todrought tolerancemay allow a species to persist during transientdry periods long‐term intense droughts can lead to mortality of

F I G U R E 2 emspTheeffectof4yearsofdroughtonthestandardizedeffectsize(SES)offunctionaldispersion(FDis)estimatedinmultivariatetraitspace(a)aswellasforeachtraitindividually(bndashd)DroughteffectsareshownasthedifferenceinSESofFDisbetweendroughtandcontrolplotsforeachyearincludingthepre‐treatmentyearYearswithstatisticallysignificanttreatmenteffects(plt05)arerepresentedbyfilledinsymbolswiththecolourrepresentingapositive( )ornegative( )effectofdroughtOpencirclesrepresentalackofsignificantdifferencebetweencontrolanddroughtplotswithlsquonsrsquodenotingalackofsignificanceacrossallyearsNotethatmultivariateFDisofSBKandSBLarecalculatedusingonlytwotraits(SLAandLNC)whileallthreetraitsareincludedinthecalculationofmultivariateFDisforeveryothersiteSite abbreviations HPGHighplainsgrasslandHYSHaysagriculturalresearchstationKNZKonzatallgrassprairieSBKSevilletablackgramaSBLSevilletabluegramaSGSShortgrasssteppe[Colourfigurecanbeviewedatwileyonlinelibrarycom]


species exhibiting such strategies (McDowell et al 2008) HerethevariableeffectsofdroughtonFDisses canbeexplainedby (a)mortalitysenescenceandreorderingofdominantdrought‐tolerantspecies(SmithKnappampCollins2009)and(b)increasesintherela-tiveabundanceofrareorsubordinatedroughtescaping(oravoiding)species(Frenette‐Dussaultetal2012Kooyers2015)Speciesareconsidereddominanthere if theyhavehighabundancerelativetootherspeciesinthecommunityandhaveproportionateeffectsonecosystemfunction(Avolioetal2019)

TheincreaseinFDisses inthefinalyearofdroughtwithinthedesert grassland site (SBK) corresponded with gt95 mortalityof the dominant grass species Bouteloua eriopoda This species

generallycontributes~80oftotalplantcoverinambientplotsThe removal of the competitive influence of this dominant spe-ciesallowedasuiteofspeciescharacterizedbyawiderrangeoftrait values to colonize this desert community Indeed overalltrait space occupied by the community (ie FRicses) significantlyincreased in the final year of drought (Figure S1) Mortality ofB eriopoda led to a community composedentirelyof ephemeralspeciesdeep‐rooted shrubsand fast‐growing forbs (iedroughtavoidersescapers) It isworthnotingthatphylogeneticdiversity(PDses)increasedintheyearpriortoincreasedFDissesandFRicses (Figure 4)which suggests phylogenetic and functional diversityarecoupledatthissite

F I G U R E 3 emspLogresponseratios(lnRR)forcommunity‐weightedtraitmeans(CWM)inresponsetothedroughttreatment(lnRR=ln(droughtcontrol)Focaltraitsinclude(a)specificleafarea(SLA)(b)leafnitrogencontent(LNC)and(c)leafturgorlosspoint(πTLP)Yearswithstatisticallysignificanttreatmenteffects(plt05)arerepresentedbyfilledinsymbolswiththecolourrepresentingapositive( )ornegative( )effectofdroughtOpencirclesrepresentalackofsignificantdifferencebetweencontrolanddroughtplotswithlsquonsrsquodenotingalackofsignificanceacrossallyearsSymbolcolouralsoreflectsconservative( )versusacquisitive( )resource‐usestrategiesatthecommunity‐scaleashighvaluesofSLALNCandπTLPallreflectacquisitivestrategiesNotethatHYSexperiencedamoderatelysignificantincrease in πTLP(p=06)inyear3ofdroughtAxisscalingisnotconsistentacrossallpanelsNegativelnRRisshownforπTLPsuchthatpositivevaluesindicatelessnegativeleafwaterpotentialSite abbreviationsHPGHighplainsgrasslandHYSHaysagriculturalresearchstationKNZKonzatallgrassprairieSBKSevilletablackgramaSBLSevilletabluegramaSGSShortgrasssteppe[Colourfigurecanbeviewedatwileyonlinelibrarycom]


The southern shortgrass prairie site inNewMexico (SBL)wastheonlysitetoexperiencedecreasedFDissesinresponsetodrought(Figure2)ThisissurprisingconsideringSBKandSBLarewithinsev-eral kilometres of one another (bothwithin the SevilletaNationalWildlifeRefuge)andexperienceasimilarmeanclimateThisregionischaracterizedbyasharpecotonehoweverresultingindifferentplantcommunitiesatSBKandSBLsuch thatSBL isco‐dominated

by B eriopoda and Bouteloua gracilis a closely relatedC4 grassB gracilisischaracterizedbygreaterleaf‐leveldroughttolerancethanB eriopoda(πTLP=minus159andminus186MPaforB eriopoda and B grac‐ilisrespectively)whichallowsittopersistduringdroughtWhileB eriopoda and B gracilisbothexperienceddrought‐inducedmortality(Bauretalinprep)thegreaterpersistenceofB gracilisledtosta-bilityincommunitystructurewithonlymoderatedeclinesinFDisses

F I G U R E 4 emspDroughteffectsonstandardizedeffectsize(SES)ofphylogeneticdiversity(PD)Theeffectofdrought(iedroughtmdashcontrol)wascalculatedforthepre‐treatmentyearandeachyearofthedroughttreatmentYearswithstatisticallysignificanttreatmenteffects(plt05)arerepresentedbyfilledinsymbolswiththecolourrepresentingapositive( )ornegative( )effectofdroughtOpencirclesrepresentalackofsignificantdifferencebetweencontrolanddroughtplotswithlsquonsrsquodenotingalackofsignificanceacrossallyearsSite abbreviationsHPGHighplainsgrasslandHYSHaysagriculturalresearchstationKNZKonzatallgrassprairieSBKSevilletablackgramaSBLSevilletabluegramaSGSShortgrasssteppe[Colourfigurecanbeviewedatwileyonlinelibrarycom]

F I G U R E 5 emspDroughtsensitivityis(a)positivelycorrelatedwithcommunity‐weighted(log‐transformed)specificleafareaofthepreviousyear(SLApy)and(b)negativelycorrelatedwithcurrentyearfunctionalevennessofspecificleafarea(FEve‐SLAcy)Droughtsensitivitywascalculatedastheabsolutevalueofpercentchangeinabove‐groundnetprimaryproduction(ANPP)indroughtplotsrelativetocontrolplotsinagivenyearTheplottedregressionlinesarefromtheoutputoftwogenerallinearmixedeffectmodels(GLMM)includingsiteasarandomeffectandthefixedeffectofeitherSLApy(aSensitivity=9255timesSLApyminus20544)orFEve‐SLAcy(bSensitivity=minus2248timesFEve‐SLAcy+13242)Boththemarginal(m)andconditional(c)R

2valuesfortheGLMMareshownSite abbreviationsHPGHighplainsgrasslandHYSHaysagriculturalresearchstationKNZKonzatallgrassprairieSBKSevilletablackgramaSBLSevilletabluegramaSGSShortgrasssteppe


inthethirdyearofdroughtTransientdeclines inFDissesmayrep-resent environmental filtering acting on subordinate species withtraitsmuchdifferent from thoseof thedominantgrasses IndeeddecreasedFDissesatSBLwasaccompaniedbyincreasedfunctionalevenness(FEve)(FigureS2)anddecreasedPDses(Figure4)Thusthefunctionalchangesobservedinthiscommunityweredrivenbybothgeneticallyandfunctionallysimilarspecies

At the northern shortgrass prairie site (SGS) the response ofFDissestodroughtwaslikelyduetore‐orderingofdominantspeciesTheearlyseasonplantcommunityatSGSisdominatedbyC3grassesandforbswhereasB gracilisrepresents~90oftotalplantcoverinmid‐tolatesummer(OesterheldLoretiSemmartinampSala2001)Thenatureofourdroughttreatments(ieremovalofsummerrain-fall) favouredthesubordinateC3plantcommunityat thissiteWeobservedashiftinspeciesdominancefromB gracilistoVulpia octo‐floraanearlyseasonC3grassbeginninginyear2ofdrought(Bauretalinprep)Theinitialco‐dominanceofB gracilis and V octoflora increasedFDissesofSLA(Figure2b)asthesetwodominantspeciesexhibitdivergent leafcarbonallocationstrategies (SLA=125and192kgm2forB gracilis and V octoflorarespectively)Thisempha-sizes the importance of investigating single trait diversity indices(Spasojevic amp Suding 2012) as this community functional changewas masked by multivariate measures of FDisses (Figure 2a) TheeventualmortalityofB gracilisinthefourthyearofdroughtledtosignificantlyhighermultivariateFDisses(Figure2)asthislateseasonnichewasfilledbyspecieswithadiversityofleafcarbonandnitro-geneconomies(LNCandSLA)Indeeddroughtledtoa55increaseinShannonsdiversityindexatSGS(Bauretalinprep)

Functional diversity of the northernmixed grass prairie (HPG)was unresponsive to drought (Figure 2) This site has the lowestmeanannualtemperatureofthesixsites(Table1)andislargelydom-inatedbyC3specieswhichexhibitspringtimephenologylargelyde-terminedbytheavailabilityofsnowmelt(Knappetal2015)Thusthenatureofourdrought treatment (ie removalof summer rain-fall)hadnoeffectonfunctionalorphylogeneticdiversityatthissite(Figures2and4)OnthecontraryweobservedincreasedFDissesatthesouthernmixedgrassprairie(HYS)inresponsetoexperimentaldrought(Figure2a)AgaindroughttreatmentsledtoincreasedcoverofdominantC3grassesanddecreasedcoverofC4grasses(Bauretalinprep)HereincreasedmultivariateFDisseswaslargelymirroredby single trait FDisses (Figure 2bndashd) The three co‐dominant grassspecies at this site (Pascopyrum smithii [C3]Bouteloua curtipendula [C4]andSporobolus asper[C4])arecharacterizedbyremarkablysimi-lar πTLP(rangingfromminus232tominus230MPa)ThissimilarityminimizesFDissesofπTLPastheweighteddistancetothecommunity‐weightedtrait centroid is minimized (see calculation of FDis in Laliberte ampLegendre2010) IndeedHYShas the lowestFDisofπTLP relativeto other sites (5‐year ambient average SGS = 067 HPG = 093HYS=036KNZ=037)Inthefinalyearsofdroughtplotsprevi-ouslyinhabitedbydominantC4grasseswereinvadedbyBromus ja‐ponicusaC3grasswithhigherπTLP(πTLP=minus16)aswellasperennialforbsafunctionaltypepreviouslyshowntohavehigherπTLP com-paredtograsses(Griffin‐NolanBlumenthaletal2019)Increased

abundanceofthedominantC3grassP smithiimaintainedthecom-munity‐weighted trait centroidnear theoriginalmean (minus23MPa)whereastheinvasionofsubordinateC3speciesledtoincreaseddis-similarityinπTLP(LaliberteampLegendre2010)AdditionallyP smithii is characterized by low SLA relative to other species at this site(SLA=573kgm2forP smithiivstheSLAcw=123kgm

2)ThusincreasedabundanceofP smithiicontributedtothespikeinFDisses ofSLAinyear3ofthedrought(Figure2b)

Nochangeincommunitycompositionwasobservedatthetall-grassprairie site (KNZ) andconsequentlyweobservednochangein FDis (Figure2)Drought did cause variable negative effects onPDsesatKNZ(Figure4)howevertheresponsewasnotconsistentandthuswarrantsfurtherinvestigationIt isworthnotingthatthedroughtresponseofPDsesdidnotmatchFDissesresponsesineitherSGSHYSorKNZ (Figure4) It is therefore important tomeasurebothfunctionalandphylogeneticdiversityascloselyrelatedspeciesmaydifferintheirfunctionalattributes(Forresteletal2017LiuampOsborne2015)

42emsp|emspCommunity‐weighted traits

Functionalcompositionofplantcommunities isdescribedbyboththe diversity of traits aswell as community‐weighted traitmeans(CWMs) with the latter also having important consequences forecosystem function (Garnier et al 2004Vile ShipleyampGarnier2006)Wethereforeassessedthe impactofexperimentaldroughton community‐weighted trait means of several plant traits linkedto leafcarbonnitrogenandwatereconomyLeafeconomictraitssuchasSLAandLNCdescribeaspeciesstrategyofresourceallo-cationusealongacontinuumofconservativetoacquisitive(Reich2014)Empiricallyandtheoreticallyconservativespecieswith lowSLAandorLNCaremorelikelytopersistduringtimesofresource‐limitation such as drought (Ackerly 2004 Reich 2014 WrightReich ampWestoby 2001) and community‐weighted SLA tends todeclineinresponsetodroughtduetotraitplasticity(Wellsteinetal2017)AlternativelyhighSLAandLNChavebeenlinkedtostrate-giesofdroughtescapeoravoidance(Frenette‐Dussaultetal2012Kooyers2015)HereweobservedincreasedSLAcwandLNCcwwithlong‐termdroughtinallsixsites(Figure3a)suggestingashiftawayfromspecieswithconservativeresource‐usestrategies(iedroughttolerance) and towards a community with greater prevalence ofdrought avoidance and escape strategiesWe likely overestimatethesetraitvaluesgiventhatwedonotaccountfortraitplasticityandtheabilityofspeciestoadjustcarbonandnutrientallocationduringstressfulconditions(Wellsteinetal2017)howeverourresultsdoindicatespeciesre‐orderingtowardsaplantcommunitywithinher-entlyhigherSLAandLNCfollowinglong‐termdroughtThisislikelyduetotheobservedincreaseinrelativeabundanceofearly‐seasonannualspecies(iedroughtescapers)andshrubs(iedroughtavoid-ers)speciesthatarecharacterizedbyhighSLAandLNCacrossmostsites (Bauretal inprep)Forbsandshrubstendtoaccessdeepersourcesofsoilwaterthangrasses(NippertampKnapp2007)achar-acteristicthathasallowedthemtopersistduringhistoricaldroughts


(iedroughtescapeWeaver1958)andmayhaveallowedthemtopersistduringourexperimentaldroughtThisfurthersupportstheconclusionofacommunityshifttowardsdroughtescapestrategiesand emphasizes the importance of measuring rooting depth androottraitsmorebroadlywhichare infrequentlymeasured incom-munity‐scale surveys of plant traits (Bardgett Mommer amp Vries2014Griffin‐NolanBusheyetal2018)

While leaf economic traits such as SLA and LNC are usefulfor defining syndromes of plant form and function at both theindividual (Diacuteaz et al 2016) and community‐scale (Bruelheideet al 2018) they are often unreliable indices of plant droughttolerance (eg leafeconomic traitsmightnotbecorrelatedwithdroughttolerancewithinsomecommunitieseven ifcorrelationsexist at larger scales) (Brodribb 2017 Griffin‐Nolan Bushey etal2018RosadoDiasampMattos2013)Weestimatedcommu-nity‐weightedπTLPortheleafwaterpotentialatwhichcellturgorislostwhichisconsideredastrongindexofplantdroughttoler-ance(BartlettScoffoniampSack2012)Theoryandexperimentalevidencesuggests thatdryconditions favourspecieswith lowerπTLP (Bartlett Scoffoni amp Sack 2012 Zhu et al 2018) Whilethismaybe trueof individual speciesdistributions ranging fromgrasslands to forests (Griffin‐NolanOcheltreeet al2019Zhuetal2018) thishasnotbeentestedat thecommunityscaleorwithinasinglecommunityrespondingtolong‐termdroughtHereweshowthatcommunity‐scaleπTLPrespondsvariablytodroughtwithnegative (HPG)positive (SGSandHYS)andneutraleffects(KNZ) (Figure3c)WhilespeciescanadjustπTLPthroughosmoticadjustmentandorchangestomembranecharacteristics(MeinzerWoodruffMariasMccullohampSevanto2014)thistraitplasticityrarelyaffectshowspeciesrankintermsofleaf‐leveldroughttol-erance(Bartlettetal2014)Thustheseresultssuggestthatcom-munity‐scale leaf‐level drought tolerance decreased (ie higherπTLP)inresponsetodroughtinhalfofthesitesinwhichπTLP was measured The opposing effects of drought on community πTLP for SGS and HPG is striking (Figure 3c) especially consideringthesesitesare~50kmapartandhavesimilarspeciescompositionIncreased grass dominance at HPG (BergerndashParker dominanceindexBauretal inprep) resulted indecreasedπTLP (iegreaterdrought tolerance) whereas at SGS the community shifted to-wards a greater abundance of drought avoidersescapers ForbsandshrubsinthesegrasslandstendtohavehigherπTLPcomparedtobothC3andC4grasses(Griffin‐NolanBlumenthaletal2019)whichexplainsthisincreaseincommunity‐weightedπTLPNotablythe plant community at HPG is devoid of a true shrub specieswhichcouldfurtherexplaintheuniqueeffectsofdroughtontheabundance‐weightedπTLPofthisgrassland

43emsp|emspDrought sensitivity of ANPP

Biodiversity and functional diversity more specifically is wellrecognized as an important driver of ecosystem resistance toextreme climate events (Anderegg et al 2018 De La Riva etal 2017 Peacuterez‐Ramos et al 2017)We tested this hypothesis

acrosssixgrasslandsbyinvestigatingrelationshipsbetweensev-eral functional diversity indices and the sensitivity of ANPP todrought(iedroughtsensitivity)Weobservedasignificantnega-tivecorrelationbetweenfunctionalevennessofSLAanddroughtsensitivityprovidingsomesupportforthishypothesis(Figure5b)while alsoemphasizing the importanceofmeasuring single traitfunctionaldiversityindices(SpasojevicampSuding2012)Thesig-nificantnegativecorrelationbetweenFEveofSLAcyanddroughtsensitivitysuggeststhatcommunitieswithevenlydistributedleafeconomictraitsarelesssensitivetodroughtWhileotherindicesoffunctionaldiversitywereweaklycorrelatedwithdroughtsen-sitivity(TableS2)allcorrelationswerenegativeimplyinggreaterdroughtsensitivityinplotssiteswithlowercommunityfunctionaldiversity

Thestrongestpredictorofdroughtsensitivitywascommunity‐weightedSLAofthepreviousyear(TableS2)Thesignificantpos-itive relationshipobserved in this study (Figure5a) suggests thatplantcommunitieswithagreaterabundanceofspecieswithhighSLA(ie resourceacquisitivestrategies)aremore likelytoexperi-encegreaterrelativereductionsinANPPduringdroughtinthefol-lowingyearFurthermoreSLAcwincreasedinresponsetolong‐termdroughtacrosssites (Figure3)whichmay result ingreatersensi-tivity of these communities to future drought depending on thetimingandnatureofdroughtThe lackof a relationshipbetweenπTLPanddroughtsensitivitywassurprisinggiventhatπTLP is widely considered an important metric of leaf level drought tolerance(BartlettScoffoniampSack2012)WhileπTLPisdescriptiveofindi-vidualplantstrategiesforcopingwithdroughtitmaynotscaleuptoecosystemlevelprocessessuchasANPPWerecognizethatthelackofπTLPdatafromthetwomostsensitivesites (SBKandSBL)limitsourabilitytoaccuratelytesttherelationshipbetweencom-munity‐weightedπTLPanddroughtsensitivityofANPPOurresultsclearlydemonstratehoweverthatleafeconomictraitssuchasSLAare informativeofANPPdynamicsduringdrought (Garnieret al2004Reich2012)

ItisimportanttonotethatthisanalysisequatesspacefortimewithregardstofunctionalcompositionanddroughtsensitivityThedriversofthetemporalpatternsinfunctionalcompositionobservedhere(iespeciesre‐ordering)arelikelynotthesamedriversofspa-tialpatternsinfunctionalcompositionandmayhaveseparatecon-sequences for ecosystem drought sensitivity Nonetheless thesealterationstofunctionalcompositionwilllikelyimpactdroughtleg-acy effects (ie lagged effects of drought on ecosystem functionfollowingthereturnofaverageprecipitationconditions)Thisises-peciallylikelyforthesesixgrasslandsgiventhattheyexhibitstronglegacyeffectsevenaftershort‐termdrought(Griffin‐NolanCarrolletal2018)

5emsp |emspCONCLUSIONS

Grasslandsprovideawealthofecosystemservicessuchascarbonstorageforageproductionandsoilstabilization(Knappetal1998


SchlesingerampBernhardt2013)Thesensitivityoftheseservicestoextremeclimateeventsisdriveninpartbythefunctionalcomposi-tionofplantcommunities(DeLaRivaetal2017NaeemampWright2003 Peacuterez‐Ramos et al 2017 TilmanWedin amp Knops 1996)Functionalcompositionrespondsvariablytodrought(Cantareletal2013Copelandetal2016Qietal2015)withlong‐termdroughtslargelyunderstudiedatbroadspatialscales

Weimposeda4‐yearexperimentaldroughtwhichsignificantlyaltered community functional composition of six North Americangrasslands with potential consequences for ecosystem functionLong‐term drought led to increased community functional disper-sioninthreesitesandashiftincommunity‐leveldroughtstrategies(assessedasabundance‐weightedtraits)fromdroughttolerancetodrought avoidance and escape strategies Species re‐ordering fol-lowingdominantspeciesmortalitysenescencewasthemaindriverof these shifts in functional composition Drought sensitivity ofANPP(ierelativereductioninANPP)waslinkedtobothfunctionaldiversityandcommunity‐weightedtraitmeansSpecificallydroughtsensitivitywasnegatively correlatedwith community evennessofSLAandpositivelycorrelatedwithcommunity‐weightedSLAofthepreviousyear

These findingshighlight thevalueof long‐termclimatechangeexperimentsasmanyofthechangesinfunctionalcompositionwerenotobserveduntilthefinalyearsofdroughtAdditionallyourresultsemphasize the importance ofmeasuring both functional diversityandcommunity‐weightedplanttraitsIncreasedfunctionaldiversityfollowinglong‐termdroughtmaystabilizeecosystemfunctioninginresponsetofuturedroughtHoweverashiftfromcommunity‐leveldroughttolerancetowardsdroughtavoidancemayincreaseecosys-temdroughtsensitivitydependingonthetimingandnatureoffu-turedroughtsThecollectiveresponseandeffectofbothfunctionaldiversityandtraitmeansmayeitherstabilizeorenhanceecosystemresponsestoclimateextremes

ACKNOWLEDG EMENTS

We thank the scientists and technicians at the Konza PrairieShortgrassSteppeandSevilletaLTERsitesaswell as thoseat theUSDA High Plains research facility for collecting managing andsharingdataPrimary support for thisproject came from theNSFMacrosystems Biology Program (DEB‐1137378 1137363 and1137342) with additional research support from grants from theNSFtoColoradoStateUniversityKansasStateUniversityandtheUniversityofNewMexicoforlong‐termecologicalresearchWealsothankVictoriaKlimkowskiJulieKrayJulieBusheyNathanGehresJohn Dietrich Lauren Baur Madeline Shields Melissa JohnstonAndrewFeltonandNateLemoineforhelpwithdatacollectionpro-cessingandoranalysis

AUTHORSrsquo CONTRIBUTIONS

RJG‐N SLC MDS and AKK conceived the experimentRJG‐N DMB TEF AMF KEM TWO and KDW

collectedandorcontributeddataRJG‐NanalysedthedataandwrotethemanuscriptAllauthorsprovidedcommentsonthefinalmanuscript

DATA AVAIL ABILIT Y S TATEMENT

Traitdataavailable fromtheDryadDigitalRepositoryhttpsdoiorg105061dryadk4v262p (Griffin‐Nolan Blumenthal et al2019) See also data associated with the EDGE project followingpublicationofothermanuscriptsutilizingthesamedata(httpedgebiologycolostateedu)

ORCID

Robert J Griffin‐Nolan httpsorcidorg0000‐0002‐9411‐3588

Ava M Hoffman httpsorcidorg0000‐0002‐1833‐4397

Melinda D Smith httpsorcidorg0000‐0003‐4920‐6985

Kenneth D Whitney httpsorcidorg0000‐0002‐2523‐5469

R E FE R E N C E S

AckerlyD(2004)FunctionalstrategiesofchaparralshrubsinrelationtoseasonalwaterdeficitanddisturbanceEcological Monographs74(1)25ndash44httpsdoiorg10189003‐4022

AndereggWR LKleinTBartlettM Sack L PellegriniA FAChoat B amp Jansen S (2016)Meta‐analysis reveals that hydrau-lic traits explain cross‐species patterns of drought‐induced treemortality across theglobePNAS113(18)5024ndash5029httpsdoiorg101073pnas1525678113

AndereggWRLKoningsAGTrugmanATYuKBowlingDRGabbitasRhellipZenesN (2018)Hydraulic diversity of forestsregulates ecosystem resilience during droughtNature 561(7724)538ndash541httpsdoiorg101038s41586‐018‐0539‐7

AvolioM L Forrestel E JChangCC LaPierreK J BurghardtK T amp SmithMD (2019)Demystifying dominant speciesNew Phytologist2231106ndash1126httpsdoiorg101111nph15789

Bardgett R D Mommer L amp De Vries F T (2014) Going under-ground Root traits as drivers of ecosystem processes Trends in Ecology amp Evolution 29(12) 692ndash699 httpsdoiorg101016jtree201410006

Bartlett M K Scoffoni C Ardy R Zhang Y Sun S Cao K ampSack L (2012) Rapid determination of comparative drought tol-erance traits Using an osmometer to predict turgor loss pointMethods in Ecology and Evolution 3(5) 880ndash888 httpsdoiorg101111j2041‐210X201200230x

BartlettMKScoffoniCampSackL(2012)ThedeterminantsofleafturgorlosspointandpredictionofdroughttoleranceofspeciesandbiomesAglobalmeta‐analysisEcology Letters15(5)393ndash405httpsdoiorg101111j1461‐0248201201751x

BartlettMKZhangYKreidlerNSunSArdyRCaoKampSackL (2014) Global analysis of plasticity in turgor loss point a keydroughttolerancetraitEcology Letters17(12)1580ndash1590httpsdoiorg101111ele12374

Bates D Maumlchler M Bolker B amp Walker S (2014) Fitting linearmixed‐effectsmodelsusinglme4arXivpreprintarXiv14065823

Botta‐DukaacutetZ (2005)Raorsquosquadraticentropyasameasureof func-tionaldiversitybasedonmultipletraitsJournal of Vegetation Science16(5) 533ndash540 httpsdoiorg101111j1654‐11032005tb02393x


BreshearsDDCobbNSRichPMPriceKPAllenCDBaliceRGhellipMeyerCW(2005)Regionalvegetationdie‐offinresponsetoglobal‐change‐typedroughtPNAS102(42)15144ndash15148httpsdoiorg101073pnas0505734102

BrodribbTJ(2017)ProgressingfromlsquofunctionalrsquotomechanistictraitsNew Phytologist215(1)9ndash11httpsdoiorg101111nph14620

BruelheideHDengler J PurschkeO Lenoir J Jimeacutenez‐AlfaroBHennekensSMhellipJandtU (2018)Globaltraitndashenvironmentre-lationshipsofplant communitiesNature Ecology amp Evolution2(12)1906ndash1917httpsdoiorg101038s41559‐018‐0699‐8

BurkeICKittelTGFLauenrothWKSnookPYonkerCMampPartonW J (1991) Regional analysis of the centralGreat PlainsBioScience41(10)685ndash692httpsdoiorg1023071311763

Burke ICYonkerCMPartonW JColeCV SchimelDSampFlach K (1989) Texture climate and cultivation effects on soilorganic matter content in US grassland soils Soil Science Society of America Journal 53(3) 800ndash805 httpsdoiorg102136sssaj198903615 99500 53000 30029x

CadotteMWampTuckerCM(2017)Shouldenvironmentalfilteringbeabandoned Trends in Ecology and Evolution32(6)429ndash437httpsdoiorg101016jtree201703004

Cantarel A A M Bloor J M G amp Soussana J F (2013) Fouryears of simulated climate change reduces above‐ground pro-ductivity and alters functional diversity in a grassland ecosys-tem Journal of Vegetation Science 24(1) 113ndash126 httpsdoiorg101111j1654‐1103201201452x

CarmonaCPdeBelloFMasonNWHampLepš J (2016)TraitswithoutbordersIntegratingfunctionaldiversityacrossscalesTrends in Ecology amp Evolution 31(5) 382ndash394 httpsdoiorg101016jtree201602003

CopelandSMHarrisonSPLatimerAMDamschenEIEskelinenAMFernandez‐GoingBhellipThorneJH(2016)Ecologicaleffectsof extremedrought onCalifornian herbaceous plant communitiesEcological Monographs 86(3) 295ndash311 httpsdoiorg101002ecm1218

DeLaRivaEGLloretFPeacuterez‐RamosIMMarantildeoacutenTSaura‐MasSDiacuteaz‐DelgadoRampVillarR(2017)Theimportanceoffunctionaldiversity in the stability ofMediterranean shrubland communitiesaftertheimpactofextremeclimaticeventsJournal of Plant Ecology10(2)281ndash293

DiacuteazSampCabidoM(2001)ViveladifferencePlantfunctionaldiver-sitymatters toecosystemprocessesTrends in Ecology amp Evolution16(11)646ndash655httpsdoiorg101016s0169‐5347(01)02283‐2

DiazSCabidoMampCasanovesF (1998)PlantfunctionaltraitsandenvironmentalfiltersataregionalscaleJournal of Vegetation Science9(1)113ndash122httpsdoiorg1023073237229

DiacuteazSCabidoMZakMMartiacutenezCarreteroEampAraniacutebarJ(1999)Plantfunctionaltraitsecosystemstructureandland‐usehistoryalongaclimaticgradientincentral‐westernArgentinaJournal of Vegetation Science10(5)651ndash660httpsdoiorg1023073237080

DiacuteazSKattgeJCornelissenJHCWright I JLavorelSDrayS hellip Gorneacute L D (2016) The global spectrum of plant form andfunctionNature529(7585)167ndash171httpsdoiorg101038nature16489

FaithDP (1992)ConservationevaluationandphylogeneticdiversityBiological Conservation 61(1) 1ndash10 httpsdoiorg1010160006‐ 3207(92)91201‐3

FernandesVMMachadodeLimaNMRoushDRudgersJCollinsSLampGarcia‐PichelF(2018)Exposuretopredictedprecipitationpatterns decreases population size and alters community struc-tureofcyanobacteria inbiologicalsoilcrustsfromtheChihuahuanDesert Environmental Microbiology 20(1) 259ndash269 httpsdoiorg1011111462‐292013983

Forrestel E J Donoghue M J Edwards E J Jetz W du Toit JC amp SmithMD (2017)Different clades and traits yield similar

grasslandfunctionalresponsesPNAS114(4)705ndash710httpsdoiorg101073pnas1612909114

Frenette‐Dussault C Shipley B Leacuteger J F Meziane D ampHingrat Y (2012) Functional structure of an arid steppeplant community reveals similarities with Grimersquos C‐S‐R the-ory Journal of Vegetation Science 23(2) 208ndash222 httpsdoiorg101111j1654‐1103201101350x

GarnierECortezJBillegravesGNavasM‐LRoumetCDebusscheMhellipToussaintJ‐P(2004)PlantfunctionalmarkerscaptureecosystempropertiesduringsecondarysuccessionEcology85(9)2630ndash2637httpsdoiorg10189003‐0799

GherardiLAampSalaOE(2015)Enhancedinterannualprecipitationvariability increases plant functional diversity that in turn amelio-ratesnegativeimpactonproductivityEcology Letters18(12)1293ndash1300httpsdoiorg101111ele12523

Griffin‐Nolan R J Blumenthal D M Collins S L Farkas T EHoffmanAMMueller K EhellipKnappA K (2019)Data fromShiftsinplantfunctionalcompositionfollowinglong‐termdroughtingrasslandsDryad Digital Repository httpsdoiorg105061dryadk4v262p

Griffin‐NolanRJBusheyJACarrollCJWChallisAChieppaJGarbowskiMhellipKnappAK(2018)Traitselectionandcommunityweightingarekeytounderstandingecosystemresponsestochang-ingprecipitationregimesFunctional Ecology32(7)1746ndash1756httpsdoiorg1011111365‐243513135

Griffin‐NolanRCarrollCJWDentonEMJohnstonMKCollinsSLSmithMDampKnappAK(2018)Legacyeffectsofaregionaldrought on aboveground net primary production in six centralUSgrasslandsPlant Ecology219(5)505ndash515httpsdoiorg101007s11258-018-0813-7

Griffin‐Nolan R Ocheltree TWMueller K E Blumenthal DMKrayJAampKnappAK(2019)Extendingtheosmometermethodfor assessing drought tolerance in herbaceous speciesOecologia189(2)353ndash363httpsdoiorg101007s00442‐019‐04336‐w

GrimeJP(1998)BenefitsofplantdiversitytoecosystemsImmediatefilterandfoundereffectsJournal of Ecology86(6)902ndash910httpsdoiorg101046j1365‐2745199800306x

Grime J P (2006) Trait convergence and trait divergence in her-baceous plant communities Mechanisms and consequencesJournal of Vegetation Science 17(2) 255ndash260 httpsdoiorg101111j1654‐11032006tb02444x

HallettLMSteinCampSudingKN (2017)Functionaldiversity in-creasesecologicalstability inagrazedgrasslandOecologia183(3)831ndash840httpsdoiorg101007s00442‐016‐3802‐3

Hsu J S Powell J ampAdler P B (2012) Sensitivity ofmean annualprimary production to precipitation Global Change Biology 18(7)2246ndash2255httpsdoiorg101111j1365‐2486201202687x

HuxmanTESmithMDFayPAKnappAKShawMRLoikMEhellipWilliamsDG (2004)Convergenceacrossbiomestoacom-mon rain‐use efficiency Nature 429(6992) 651ndash654 httpsdoiorg101038nature02561

IsbellFCravenDConnollyJLoreauMSchmidBBeierkuhnleinC Eisenhauer N (2015) Biodiversity increases the resistance ofecosystem productivity to climate extremes Nature 526(7574)574ndash577

KembelSWCowanPDHelmusMRCornwellWKMorlonHAckerlyDDhellipWebbCO(2010)PicanteRtoolsforintegratingphylogeniesandecologyBioinformatics26(11)1463ndash1464httpsdoiorg101093bioinformaticsbtq166

KieftTLWhiteCSLoftinSRAguilarRCraigJAampSkaarDA(1998)TemporaldynamicsinsoilcarbonandnitrogenresourcesatagrasslandndashshrublandecotoneEcology79(2)671ndash683httpsdoiorg1018900012‐9658(1998)079[0671tdisca]20co2

KnappAKAvolioMLBeierCCarrollCJWCollinsSLDukesJShellipSmithMD (2017)Pushingprecipitation to theextremes


in distributed experiments Recommendations for simulating wetand dry years Global Change Biology23(5)1774ndash1782httpsdoiorg101111gcb13504

Knapp A K Briggs J M Hartnett D C amp Collins S L (1998)Grassland dynamics Long‐Term ecological research in Tallgrass Prairie Long‐term ecological research network series (Vol1)NewYorkNYOxfordUniversityPress

KnappACarrollCJWDentonEMLaPierreKJCollinsSLampSmithMD(2015)Differentialsensitivitytoregional‐scaledroughtinsixcentralUSgrasslandsOecologia177(4)949ndash957httpsdoiorg101007s00442‐015‐3233‐6

KnappAKampSmithMD(2001)Variationamongbiomesintemporaldynamics of aboveground primary production Science291(5503)481ndash484httpsdoiorg101126science2915503481

Koerner S E amp Collins S L (2014) Interactive effects of grazingdroughtandfireongrasslandplantcommunitiesinNorthAmericaandSouthAfricaEcology95(1)98ndash109httpsdoiorg10189013‐ 05261

KooyersNJ(2015)TheevolutionofdroughtescapeandavoidanceinnaturalherbaceouspopulationsPlant Science234155ndash162httpsdoiorg101016jplantsci201502012

KraftNJBAdlerPBGodoyOJamesECFullerSampLevineJM(2015)Communityassemblycoexistenceandtheenvironmentalfiltering metaphor Functional Ecology 29(5) 592ndash599 httpsdoiorg1011111365‐243512345

Laliberteacute E amp Legendre P (2010) A distance‐based framework formeasuring functional diversity from multiple traits Ecology 91(1)299ndash305httpsdoiorg10189008‐22441

LaliberteacuteELegendrePShipleyBampLaliberteacuteME(2014)PackagelsquoFDrsquoMeasuring functionaldiversity frommultiple traitsandothertoolsforfunctionalecology

LangleyJAChapmanSKLaPierreKJAvolioMBowmanWD Johnson D S hellip Tilman D (2018) Ambient changes exceedtreatmenteffectsonplantspeciesabundance inglobalchangeex-periments Global Change Biology 24(12) 5668ndash5679 httpsdoiorg101111gcb14442

LavorelSampGarnierE(2002)Predictingchangesincommunitycom-position and ecosystem functioning from plant traits Revisitingthe Holy Grail Functional Ecology 16 545ndash556 httpsdoiorg101046j1365‐2435200200664x

Lefcheck J S (2016) piecewiseSEM Piecewise structural equa-tion modelling in R for ecology evolution and systematicsMethods in Ecology and Evolution 7(5) 573ndash579 httpsdoiorg1011112041‐210x12512

LiuHampOsborneCP(2015)WaterrelationstraitsofC4grassesde-pendonphylogeneticlineagephotosyntheticpathwayandhabitatwater availability Journal of Experimental Botany 66(3) 761ndash773httpsdoiorg101093jxberu430

Mason N W H De Bello F Mouillot D Pavoine S amp Dray S(2013) A guide for using functional diversity indices to revealchanges in assembly processes along ecological gradients Journal of Vegetation Science 24(5) 794ndash806 httpsdoiorg101111jvs 12013

MasonNWHMacGillivrayKSteelJBampWilsonJB(2003)AnindexoffunctionaldiversityJournal of Vegetation Science14(4)571ndash578httpsdoiorg101111j1654‐11032003tb02184x

McDowellNPockmanWTAllenCDBreshearsDDCobbNKolb T hellip Yepez E A (2008)Mechanisms of plant survival andmortalityduringdroughtWhydosomeplantssurvivewhileotherssuccumb todroughtNew Phytologist178(4)719ndash739httpsdoiorg101111j1469‐8137200802436x

MeinzerFCWoodruffDRMariasDEMccullohKAampSevantoS(2014)Dynamicsofleafwaterrelationscomponentsinco‐occur-ringiso‐andanisohydricconiferspeciesPlant Cell and Environment37(11)2577ndash2586httpsdoiorg101111pce12327

MuldavinEHMooreDICollinsSLWetherillKRampLightfootDC(2008)Abovegroundnetprimaryproductiondynamicsinanorth-ernChihuahuanDesertecosystemOecologia155123ndash132

Naeem S amp Wright J P (2003) Disentangling biodiversity effectson ecosystem functioning Deriving solutions to a seemingly in-surmountable problem Ecology Letters 6(6) 567ndash579 httpsdoiorg101046j1461‐0248200300471x

Nakagawa S amp Schielzeth H (2013) A general and simple methodfor obtaining R2 from generalized linear mixed‐effects mod-els Methods in Ecology and Evolution 4(2) 133ndash142 httpsdoiorg101111j2041‐210x201200261x

Newbold T Butchart S H M Şekercioǧlu Ccedil H Purves DW ampScharlemannJPW(2012)MappingfunctionaltraitsComparingabundance and presence‐absence estimates at large spatialscales PLoS ONE 7(8) e44019 httpsdoiorg101371journalpone0044019

NippertJBampKnappAK(2007)SoilwaterpartitioningcontributestospeciescoexistenceintallgrassprairieOikos116(6)1017ndash1029httpsdoiorg101111j0030‐1299200715630x

Noy‐Meir I (1973) Desert ecosystems Environment and producersAnnual Review of Ecology and Systematics 4(1) 25ndash51 httpsdoiorg101146annureves04110173000325

Ochoa‐Hueso R Collins S L Delgado‐Baquerizo M Hamonts KPockmanWT SinsabaughR LhellipPower SA (2018)Droughtconsistentlyaltersthecompositionofsoilfungalandbacterialcom-munities ingrasslands from twocontinentsGlobal Change Biology24(7)2818ndash2827httpsdoiorg101111gcb14113

OesterheldMLoretiJSemmartinMampSalaOE(2001)Inter‐an-nualvariationinprimaryproductionofasemi‐aridgrasslandrelatedto previous‐year production Journal of Vegetation Science 12(1)137ndash142httpsdoiorg1023073236681

PakemanRJ(2014)Functionaltraitmetricsaresensitivetothecom-pletenessofthespeciesrsquotraitdataMethods in Ecology and Evolution5(1)9ndash15httpsdoiorg1011112041‐210X12136

Peacuterez‐Harguindeguy N Diacuteaz S Garnier E Lavorel S Poorter HJaureguiberry P hellip Cornelissen J H C (2016) Corrigendum toNew handbook for standardisedmeasurement of plant functionaltraitsworldwideAustralian Journal of Botany64(8)715httpsdoiorg101071BT12225_CO

Peacuterez‐RamosIMDiacuteaz‐DelgadoRdelaRivaEGVillarRLloretFampMarantildeoacutenT(2017)ClimatevariabilityandcommunitystabilityinMediterranean shrublands The role of functional diversity andsoilenvironmentJournal of Ecology105(5)1335ndash1346httpsdoiorg1011111365‐274512747

PetcheyOLampGastonKJ(2002)Functionaldiversity(FD)speciesrichnessandcommunitycompositionEcology Letters5(3)402ndash411httpsdoiorg101046j1461‐0248200200339x

Qi W Zhou X Ma M Knops J M H Li W amp Du G (2015)Elevation moisture and shade drive the functional and phylo-genetic meadow communitiesrsquo assembly in the northeasternTibetan Plateau Community Ecology 16(1) 66ndash75 httpsdoiorg10155616820151618

ReichP(2012)KeycanopytraitsdriveforestproductivityProceedings of the Royal Society B Biological Sciences 279(1736) 2128ndash2134httpsdoiorg101098rspb20112270

ReichP(2014)Theworld‐wideldquofast‐slowrdquoplanteconomicsspectrumA traitsmanifesto Journal of Ecology102(2)275ndash301httpsdoiorg1011111365‐274512211

ReichPampOleksynJ (2004)GlobalpatternsofplantleafNandPinrelationtotemperatureandlatitudePNAS101(30)11001ndash11006httpsdoiorg101073pnas0403588101

RosadoBHPDiasATCampdeMattosEA(2013)GoingbacktobasicsImportanceofecophysiologywhenchoosingfunctionaltraitsforstudyingcommunitiesandecosystemsNatureza amp Conservaccedilatildeo11(1)15ndash22httpsdoiorg104322natcon2013002


SchlesingerWHampBernhardtES(2013)Biogeochemistry An analysis of global changeCambridgeMAAcademicpress

SiefertAViolleCChalmandrierLAlbertCHTaudiereAFajardoA hellipWardle D A (2015) A global meta‐analysis of the relativeextentof intraspecific traitvariation inplantcommunitiesEcology Letters18(12)1406ndash1419httpsdoiorg101111ele12508

Šiacutemovaacute IViolleC Svenning J‐CKattge J EngemannK SandelBhellipEnquistBJ(2018)Spatialpatternsandclimaterelationshipsofmajorplant traits in theNewWorlddifferbetweenwoodyandherbaceousspeciesJournal of Biogeography45(4)895ndash916httpsdoiorg101111jbi13171

SmithMD(2011)TheecologicalroleofclimateextremesCurrentun-derstandingandfutureprospectsJournal of Ecology99(3)651ndash655httpsdoiorg101111j1365‐2745201101833x

SmithMDKnappAKampCollinsSL(2009)Aframeworkforassess-ingecosystemdynamicsinresponsetochronicresourcealterationsinduced by global changeEcology90(12) 3279ndash3289 httpsdoiorg10189008‐18151

SoudzilovskaiaNA Elumeeva TGOnipchenkoVG Shidakov IISalpagarovaFSKhubievABhellipCornelissenJHC (2013)Functionaltraitspredictrelationshipbetweenplantabundancedy-namicandlong‐termclimatewarmingPNAS110(45)18180ndash18184httpsdoiorg101073pnas1310700110

SpasojevicM J amp Suding KN (2012) Inferring community assem-blymechanismsfromfunctionaldiversitypatternsTheimportanceofmultipleassemblyprocessesJournal of Ecology100(3)652ndash661httpsdoiorg101111j1365‐2745201101945x

StamakisA (2014)RAxMLversion8Atoolforphylogeneticanalysisand post‐analysis of large phylogenies Bioinformatics 30 1312ndash1313httpsdoiorg101093bioinformaticsbtu033

SudingKNLavorelSChapinFSCornelissenJHCDiacuteazSGarnierE hellip Navas M‐L (2008) Scaling environmental change throughthe community‐level A trait‐based response‐and‐effect frame-work for plantsGlobal Change Biology 14(5) 1125ndash1140 https doiorg101111j1365‐2486200801557x

Swenson N G (2014) Functional and phylogenetic ecology in R NewYorkNYSpringer

TilmanDampDowningJA(1994)BiodiversityandstabilityingrasslandsNature367(6461)363ndash365httpsdoiorg101038367363a0

Tilman D Knops JWedin D Reich P RitchieM amp Siemann E(1997) The influence of functional diversity and composition onecosystem processes Science 277(5330) 1300ndash1302 httpsdoiorg101126science27753301300

Tilman D Wedin D amp Knops J (1996) Productivity and sustain-ability influenced by biodiversity in grassland ecosystemsNature379(6567)718ndash720httpsdoiorg101038379718a0

Trenberth K E (2011) Changes in precipitation with climate changeClimate Research47(1ndash2)123ndash138httpsdoiorg103354cr00953

Vile D Shipley B amp Garnier E (2006) Ecosystem productivitycan be predicted from potential relative growth rate and spe-cies abundance Ecology Letters 9(9) 1061ndash1067 httpsdoiorg101111j1461‐0248200600958x

Villeacuteger S Mason N W amp Mouillot D (2008) New multidi-mensional functional diversity indices for a multifaceted

frameworkinfunctionalecologyEcology89(8)2290ndash2301httpsdoiorg10189007‐12061

WeaverJE(1958)Classificationofrootsystemsofforbsofgrasslandand a consideration of their significance Ecology39(3) 393ndash401httpsdoiorg1023071931749

WellsteinCPoschlodPGohlkeAChelliSCampetellaGRosbakhShellipBeierkuhnleinC (2017)Effectsofextremedroughtonspe-cificleafareaofgrasslandspeciesAmeta‐analysisofexperimentalstudiesintemperateandsub‐MediterraneansystemsGlobal Change Biology23(6)2473ndash2481httpsdoiorg101111gcb13662

WhitneyKDMudgeJNatvigDOSundararajanAPockmanWT Bell J hellip Rudgers J A (2019) Experimental drought reducesgenetic diversity in the grassland foundation species Boutelouaeriopoda Oecologia 189(4) 1107ndash1120 httpsdoiorg101007s00442-019-04371-7

WieczynskiDJBoyleBBuzzardVDuranSMHendersonANHulshof CM hellip Savage VM (2019) Climate shapes and shiftsfunctionalbiodiversityinforestsworldwidePNAS116(2)587ndash592httpsdoiorg101073pnas1813723116

WrightIJReichPBCornelissenJHCFalsterDSHikosakaKLamontBBLeeWOleksynJOsadaNPoorterHVillarRWartonDIampWestobyM(2005)AssessingthegeneralityofleaftraitofglobalrelationshipsNew Phytologist166(2)485ndash496httpsdoi101111j1469-8137200501349x

WrightIJReichPBampWestobyM(2001)Strategyshiftsinleafphys-iologystructureandnutrientcontentbetweenspeciesofhigh‐andlow‐rainfallandhigh‐andlow‐nutrienthabitatsFunctional Ecology15(4)423ndash434httpsdoiorg101046j0269‐8463200100542x

WrightIJReichPBWestobyMAckerlyDDBaruchZBongersF hellip Villar R (2004) The worldwide leaf economics spectrumNature428(6985)821ndash827

YahdjianLampSalaOE(2002)ArainoutshelterdesignforinterceptingdifferentamountsofrainfallOecologia133(2)95ndash101httpsdoiorg101007s00442‐002‐1024‐3

Zhu S‐D Chen Y‐J YeQHe P‐C LiuH Li R‐HhellipCaoK‐F(2018) Leaf turgor loss point is correlatedwith drought toleranceand leaf carbon economics traitsTree Physiology38(5) 658ndash663httpsdoiorg101093treephystpy013

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGriffin‐NolanRJBlumenthalDMCollinsSLetalShiftsinplantfunctionalcompositionfollowinglong‐termdroughtingrasslandsJ Ecol 2019107 2133ndash2148 httpsdoiorg1011111365‐274513252


1emsp |emspINTRODUC TION

Ecosystemfunctionislargelydeterminedbythefunctionalattributesof residentplant speciesPlant traitsareuseful forunderstandinghow resources are acquired by plants (Reich 2014Wright et al2004)andconsequentlytransferredtoorstoredinvariousecosys-tempools suchasplantbiomassorsoilorganicmatter (LavorelampGarnier 2002) Plant community functional composition definedbycommunity‐weightedtraitmeans (CWMs)andfunctionaldiver-sity(iethedistributionoftraitswithinacommunity)respondstoenvironmentalchangeandcanaffectecosystemprocessessuchasabove‐groundnetprimaryproduction(ANPP)nutrientcyclinganddecomposition(DiacuteazampCabido2001)Atrait‐basedresponse‐and‐effectframeworkhasbeenproposed(Sudingetal2008)wherebycertainplant traits indicatehowspecieswill shift inabundance inresponse to environmental change (eg conservative leaf watereconomictraitsimprovespeciestolerancetodroughtandwarmingAnderegg et al 2016 Soudzilovskaia et al 2013)whereasothertraits(orthesametraits)arelinkedtospecificecosystemfunctions(eg leaf nitrogen content [LNC] is correlated with variability inANPPGarnieretal2004Reich2012)Theimportanceofclimatein governing functional composition iswell supportedby commu-nityscalesurveysofplanttraitsonbroadspatialandtemporalscales(Newbold Butchart Şekercioǧlu Purves amp Scharlemann 2012ReichampOleksyn2004Šiacutemovaacuteetal2018Wieczynskietal2019Wright et al 2005) Few studies however have assessed the re-sponseofbothfunctionaldiversityandCWMstoclimateextremeswhich are rare by definition (Smith 2011) and the correspondingeffectonecosystemfunctioningacrossspaceandtime

Risingglobaltemperaturesincreaseratesofevapotranspirationand thus the intensity and duration of climate extremes such asdrought(Trenberth2011)withimmediateandlong‐lastingnegativeimpactsonEarthsvegetation (Breshearsetal2005)Themagni-tudeofvegetationresponsestodroughtvariesamongecosystemswith xeric ecosystems generally being more sensitive than mesicones(Huxmanetal2004Knappetal2015)Ecosystemresistanceandresiliencetodroughthavebeenlinkedtospeciesdiversityandfunctionaldiversityinparticular(DiacuteazampCabido2001Isbelletal2015TilmanampDowning1994Tilmanetal1997)Plantcommu-nities with high functional diversity are buffered against declinesinecosystemfunctionssuchasANPPduetofunctionalinsurance(Andereggetal2018DeLaRivaetal2017Grime1998Peacuterez‐Ramosetal2017)Inotherwordsagreaterdiversityofspecies(and

traits)increasestheoddsofoneormorespeciessurvivingadroughtandcompensatingfordrought‐inducedsenescenceormortalityofotherspeciesBeyonddiversitythemeancompositionoftraits(asmeasuredbyCWMs)canconferecosystemresistanceandresiliencetodroughtespeciallyifspecieswithtraitslinkedtodroughtsurvival(McDowelletal2008)andordroughtavoidanceescapestrategies(Kooyers2015Noy‐Meir1973)areinhighabundance

Increasing complexity arises howeverwhen functional com-positionitselfisalteredbydroughtAnextremeclimateeventcanact as an environmental filter allowing only certain species (andtrait values) to persist potentially leading to trait convergenceandor decreased functional and genetic diversity (Diacuteaz CabidoZakMartiacutenezCarreteroampAraniacutebar1999Grime2006Whitneyet al 2019) however an array of biotic interactions influencingcompetitioncoexistenceandnichedifferentiationcanactsimulta-neouslytostructurecommunitiesinanoppositemanner(CadotteampTucker2017Kraftetal2015)Thusgivenuncertainandcoun-teractingrolesofenvironmentalfilteringandnichedifferentiationtheneteffectsofdroughtoncommunity functionalcompositionare currently unpredictable Indeed the impact of drought andariditymorebroadlyonfunctionaldiversityishighlyvariablewithpositive (Cantarel Bloor amp Soussana 2013) negative (Qi et al2015)andneutral(Copelandetal2016HallettSteinampSuding2017)responsesobservedTheseinconsistenciesarelikelyduetodifferencesintheselectionoftraitsandfunctionaldiversityindi-cestheextremityofdroughtandorthespatialtemporalcontextinwhich aridity is being examined Thus coordinated long‐termandmulti‐siteexperimentsareneededtoassesstheimpactofex-tremedroughtonfunctionalcompositionandecosystemfunction

The lsquoExtreme Drought in Grasslands Experimentrsquo (EDGE) wasestablishedin2012toassessthedroughtsensitivityofANPPinsixNorthAmerican grasslands ranging fromdesert grassland to tall-grass prairie (Figure 1 Table 1) Grasslands are ideal ecosystemsforassessingdroughtsensitivityasANPPinthesesystemsishighlyresponsive toprecipitationvariability (HsuPowellampAdler2012Knappamp Smith 2001) and their short stature allows for easy in-stallationof experimental drought infrastructure (YahdjianampSala2002) We surveyed plant traits of the most common species ateachEDGE site (cumulatively representing~90plant cover) andtracked changes in three indicesof functional diversity (eg func-tionaldispersionrichnessandevenness)andabundance‐weightedtraitsinresponsetoa4‐yearexperimentaldroughtOurtraitsurveyincludedleafturgorlosspoint(πTLP)specificleafarea(SLA)andLNC

ofconsideringbothfunctionaldiversityandabundance‐weightedtraitsmeansofplantcommunitiesastheircollectiveeffectmayeitherstabilizeorenhanceeco-systemsensitivitytodrought

K E Y W O R D S

ANPPclimatechangecommunity‐weightedtraitsdroughtfunctionaldiversityplantfunctionaltraits





















MAT (degC)

Shannon Diversity

Species Richness




























3emsp |emspRESULTS





(


ANPPcontrol

)









Effect



Trt 368 00001 364 0075 2732 699 0002

Site 1531 019 1291 5122 33974 61562 28613

Year 1102 326 144 1118 3344 5806 12219

TrttimesSite 243 211 051 172 348 026 630

TrttimesYear 1198 047 152 351 1502 2829 234

SitetimesYear 3034 253 307 866 2672 3270 6254












































ACKNOWLEDG EMENTS







ORCID





R E FE R E N C E S



































































































































MAT (degC)

Shannon Diversity

Species Richness




























3emsp |emspRESULTS





(


ANPPcontrol

)









Effect



Trt 368 00001 364 0075 2732 699 0002

Site 1531 019 1291 5122 33974 61562 28613

Year 1102 326 144 1118 3344 5806 12219

TrttimesSite 243 211 051 172 348 026 630

TrttimesYear 1198 047 152 351 1502 2829 234

SitetimesYear 3034 253 307 866 2672 3270 6254












































ACKNOWLEDG EMENTS







ORCID





R E FE R E N C E S



































































































































3emsp |emspRESULTS





(


ANPPcontrol

)









Effect



Trt 368 00001 364 0075 2732 699 0002

Site 1531 019 1291 5122 33974 61562 28613

Year 1102 326 144 1118 3344 5806 12219

TrttimesSite 243 211 051 172 348 026 630

TrttimesYear 1198 047 152 351 1502 2829 234

SitetimesYear 3034 253 307 866 2672 3270 6254












































ACKNOWLEDG EMENTS







ORCID





R E FE R E N C E S























































































































Effect



Trt 368 00001 364 0075 2732 699 0002

Site 1531 019 1291 5122 33974 61562 28613

Year 1102 326 144 1118 3344 5806 12219

TrttimesSite 243 211 051 172 348 026 630

TrttimesYear 1198 047 152 351 1502 2829 234

SitetimesYear 3034 253 307 866 2672 3270 6254












































ACKNOWLEDG EMENTS







ORCID





R E FE R E N C E S
























































































































































ACKNOWLEDG EMENTS







ORCID





R E FE R E N C E S















































































































Shifts in plant functional composition following long‐term...

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