Patterns and drivers of biodiversity–stability

Journal of Ecology 20171ndash13 wileyonlinelibrarycomjournaljec emsp|emsp1copy 2017 The Authors Journal of Ecology copy 2017 British Ecological Society

Received3May2017emsp |emsp Accepted11October2017DOI1011111365-274512897

E S S A Y R E V I E W

Patterns and drivers of biodiversityndashstability relationships under climate extremes

Hans J De Boeck1 emsp|emspJuliette M G Bloor2emsp|emspJuergen Kreyling3 emsp|emsp Johannes C G Ransijn4emsp|emspIvan Nijs1emsp|emspAnke Jentsch4emsp|emspMichaela Zeiter56

1DepartmentofBiologyCentreofExcellencePLECO(PlantandVegetationEcology)UniversiteitAntwerpenWilrijkBelgium2INRAVetAgro-SupUREPClermont-FerrandFrance3ExperimentalPlantEcologyErnst-Moritz-ArndtUniversityGreifswaldGreifswaldGermany4DisturbanceEcologyBayreuthCentreofEcologyandEnvironmentalResearch(BayCEER)UniversityofBayreuthBayreuthGermany5InstituteofPlantSciencesUniversityofBernBernSwitzerlandand6SchoolofAgriculturalForestampFoodSciencesBernUniversityofAppliedSciencesZollikofenSwitzerland

CorrespondenceHansJDeBoeckEmailhansdeboeckuantwerpbe

Funding informationERA-NetBiodivERsABelgianFederalSciencePolicyOfficeGermanFederalMinistryofEducationandResearchMinistegraveredelrsquoEacutecologieduDeacuteveloppementdurableetdelrsquoEacutenergieSwissNationalScienceFoundation

HandlingEditorDavidWardle

Abstract1 Interactionsbetweenbiodiversitylossandclimatechangepresentsignificantchal-lengesforresearchpolicyandmanagementofecosystemsEvidencesuggeststhathighspeciesdiversitytendstoincreaseplantcommunitystabilityunderinterannualclimatefluctuationsandmilddryandweteventsbuttheoverallpatternofdiver-sityndashstabilityrelationshipsunderclimateextremesisunclear

2 WecomprehensivelyreviewresultsfromobservationalandexperimentalstudiestoassesstheimportanceofdiversityeffectsforecosystemfunctionunderclimateextremesBoththebroadliteraturereviewandameta-analysisfocusedontheef-fectsofextremeprecipitationeventsonabove-groundbiomassrevealnosignifi-cantinteractionbetweenspeciesrichnessandclimateextremes

3 CausesforvariationindiversityeffectsunderclimateextremesareexploredfromstressthresholdstobioticinteractionsandcommunityassemblyandweconsiderhowthesemaymodulatetheoutcomesofbiodiversityndashstabilityrelationshipsWealsoexaminehowspecificcharacteristicsofclimateextremesandtimingofmeas-urementsmayinteractwithmechanismsofdiversityndashstabilityrelationships

4 SynthesisHypothesestailoredtothecomplexityofdiversityeffectstheimplemen-tationofstandardisedexperimentsandtheuseoftrait-basedbiodiversitymeas-ures rather than species richness should lead to better causal understanding ofwhether and how biodiversitymay protect ecosystems from adverse effects ofclimateextremes

K E Y W O R D S

climatechangeecosystemfunctioninginsurancehypothesisplantcommunityplantndashclimateinteractionsresilienceresistancespeciesrichness

1emsp |emspINTRODUCTION

Assessing the consequences of human-induced changes to theenvironmentisakeychallengeforresearchpolicyandmanagement(BarnardampThuiller2008)Rapidratesofecosystemdegradationand

simplificationhaveraisedconcernsabouthowbiodiversity lossmayaffectthefunctioningofecosystemsandtheircontributiontohumanwell-being via ecosystem services (Cardinale etal 2012 Hooperetal2005) Inadditionecosystemsarefacedwithongoingclimatechangeandassociatedalterationsinthefrequencyintensityduration

2emsp |emsp emspenspJournal of Ecology DE BOECK Et al

andtimingofextremeweatherevents(FisherampKnutti2014IPCC2013)Extremeeventssuchasseveredroughtandperiodsofheavyrainfallhavethepotentialtocausedramaticchangesinplantphysiol-ogypopulationdynamicsandecosystemstructurewithcascadingef-fectsonbiogeochemicalcycling(Franketal2015Reyeretal2013Smith2011)However themechanismsdeterminingecosystem re-sponseandrecoverytoclimateextremesremainunclearmakingvul-nerabilityassessmentsuncertain(Kayleretal2015)

Overthelastdecadeanincreasingnumberofstudieshaveinvesti-gatedtheimpactsofextremeeventsinparticularonherbaceousplantcommunitiesAvailabledataindicatehighvariationinthemagnitudeof ecosystem responses to climate extremes ranging fromminimalimpacts on ecosystem structure and function (Jentsch etal 2011)tomajoreffects in theshortandor long term (BredaHucGranierampDreyer 2006DeBoeckBassinVerlindenZeiterampHiltbrunner2016HooverKnappampSmith2014)Suchcontrastingresultsamongstudieshavebeenattributedtodifferencesinthenatureoftheclimateextremes or the ecosystems in question (Frank etal 2015 Smith2011)Inparticularlevelsofbiodiversitywithinecosystemsmayplayanimportantroleindeterminingecosystemresponsestoclimateex-tremes(Isbelletal2015)Considerableevidencefromtheoreticalandexperimentalstudiessuggeststhathighspeciesdiversitywithineco-systemstendstoincreaseplantcommunitystabilityoftenmeasuredas decreased temporal variability in community biomass (Cardinaleetal 2012McCann2000TilmanWedinampKnops 1996) If bio-diversityplaysastabilisingroleforecosystemssubjectedtoclimaticextremesthennotonlywilldiversitylossimpairecosystemfunctionbutitmayalsoreduceitscapacitytobuffersevereenvironmentalfluc-tuations(LoreauampdeMazancourt2013)

Although interest in diversityndashstability relationships has a longhistory(egMacArthur1955McNaughton1977)theexactmech-anismsunderlyingdiversityndashstability relationships remaina subjectofdebate (GrmanLauSchoolmasterampGross2010Gross2016Loreau amp de Mazancourt 2013) Positive effects of diversity oncommunityfunctioningareoftenlinkedtodifferencesinsensitivityto fluctuations in environmental factors More diverse communi-tiesaregenerallyconsideredtohaveawiderrangeofsensitivitiesEventhoughspeciesresponsesvarycommunityfunctioningismorestable under a rangeof conditions due to species asynchrony andcompensatory responses (cf the ldquoInsurance Hypothesisrdquo Grossetal 2014 Yachi amp Loreau 1999) However most of the theoryondiversityndashstabilityrelationshipsinplantcommunitiesfocusesonyear-to-yearstabilityandormoderatefluctuationsinenvironmentalconditions (Dodd SilvertownMcConway PottsampCrawley 1994Gross etal 2014 RomanukVogt amp Kolasa 2006Tilman Reichamp Knops 2006Valone ampHoffman 2003) It is only relatively re-centlythatstudieshavealsostartedapplyingthistheorytoextremeevents(BloorampBardgett2012Isbelletal2015KahmenPernerampBuchmann2005Kreylingetal2008)Herewereviewtheliter-atureandsynthesiseexperimentalandobservationalstudieswhichexaminetheroleofbiodiversityforecosystemresponsesspecificallyinthecontextofclimateextremesNextweexplorethefactorsun-derlyingvariationinbiodiversityndashstabilityrelationshipsunderclimate

extremesFinallywediscuss future researchdirections thatshouldimprovemechanisticunderstandingofbiodiversityndashstabilityeffectsinachangingenvironment

2emsp |emspLOOKING FOR EVIDENCE DOES BIODIVERSITY PROMOTE STABILITY UNDER CLIMATE EXTREMES

Ecosystemstabilityistypicallyconsideredintermsofresistance(ldquothe instantaneous impact of exogenous disturbance on system staterdquo)andor recovery (ldquothe endogenous processes that pull the disturbed system back towards an equilibriumrdquo)(HodgsonMcDonaldampHosken2015)InthemostcomprehensivestudytodateIsbelletal(2015)showedthatplant species richness increasesbiomass resistancebutnot re-silienceofgrasslandsundernaturalprecipitation regimesofvaryingextremityMoreovertheresultsfromIsbelletal(2015)suggestthatspecies richnessmaybemore important for stability undermoder-ateratherthanextremeeventsHowevertoourknowledgenore-view has explicitly addressed diversityndashstability relationships underextreme climatic eventsHerewe consider extreme climatic eventsintermsoftheirprobabilityofoccurrencedefinedstatisticallyasthe10thpercentileorlessofthedistributionfromalong-termreferencetime-period(Knappetal2015)

Anextensive literaturesearchwasconducted forpeer-reviewedstudies addressing the relationship between biodiversity and eco-systemstabilityforecosystemsexposedtovariousclimateextremes(droughts wet spells and heat waves see Table S1)We used thesearch engines ISIregWeb of Science andGoogle Scholar aswell ascross-referencing to find studies published beforeAugust 2016 re-porting on the effects of extreme climatic events onplant commu-nitiesofdifferentdiversityStudiesthatfocusedontheperformanceofsingleindividualsinaneighbourhoodvaryingindiversity(egMetzetal2016)werenotretainedThefollowingsearchtermswereused(stabilityorresistanceorresilience)(diversityorspeciesrichness)(ex-tremeorsevere) (droughtordryorwaterorwetorprecipitationorsoilmoistureorheatorcoldorwarmortemperatureorclimate)and(grassorplantcommunity)Theliteraturesearchandsubsequentse-lectionreturned43papersthemajorityofwhichaddressedgrasslandsystems(33articles)witharangeofapproachesfromopportunisticobservationalexaminationofnaturalextremesin(semi-)naturaleco-systems to experimentally imposed events in artificially assembledsystems Based on the authorsrsquo own interpretation of results thesupport forpositivediversityndashstabilityeffectswasmixedasneutralandnegativeeffectsofdiversityonecosystemstabilityunderextremeeventswerefrequentlyreported(TableS1)

Whiletheliteraturesearchprovidedamixedqualitativepictureofbiodiversityndashstability relationshipsduring andafter extremeswealsosought amore formal quantitative conclusion throughmeta-analysis(seeSupportingInformation)Inbriefwefocusedourstatisticalanaly-sisonstudiesinvestigatingtheeffectsofextremelydryorwetclimaticevents effects on above-ground biomass as other combinations ofclimaticdriverandor responsevariablewere representedby too few

emspensp emsp | emsp3Journal of EcologyDE BOECK Et al

studiesWeretainedstudieswhere(1)theclimaticeventhadareturntimeofonein10yearsormoreextreme(2)climaticallyextremeyearswereprecededbyanon-extremeyearand(3)atruecontrolornormalreferenceyearwasavailableasabaselineTheanalysisfocusedmainlyon resistanceandonhighand lowspecies richness levels In studiesperformedwithmorethantwolevelsofspeciesrichnesstheanalysiswasrestrictedtothetwomostextremespeciesrichnesslevelsIncaseofnaturalspeciesrichnessgradientsrepresentedbyasingleplotattheendsof thegradients thegradientwas restricted to species richnesslevelswithmultiplereplicatesBiomassdataweretakenfromharvestsattheendoftheextremeevent(resistance)andfromthefirstbiomassmeasureavailableaftertheendoftheextremeevent(recovery)Incaseofsequentialexperimentalextremeeventsweonly includedbiomassresponsestothefirstextremeeventinordertoexcludecarry-overef-fectsofrepeateddroughts

The natural logarithm of the response ratio (LRR=ln[treatmentmeancontrol mean]) was used as a metric of treatment effect size(HedgesGurevitchampCurtis1999KorichevaGurevitchampMengersen2013)onabove-groundbiomassreflectingtherelativechangeinbio-massduetotreatmentsControlswereassignedas lowdiversityandcontrolplotsinmanipulationstudies(andreferenceyearsinobserva-tional studies)whereas ldquotreatmentsrdquowereassignedashighdiversityandtheextremeeventForallstudiesweusedtheaveragebiomassofhighdiversitywithoutextremeeventhighdiversitywithextremeeventlowdiversitywithoutextremeeventandlowdiversitywithex-treme event treatment combinations to calculate themain effect ofspeciesrichnessthemaineffectoftheextremeeventandtheinterac-tioneffectsizeaccordingtoGruneretal(2008)Asignificantinterac-tionindicatesthattheeffectsofthetwofactorsarenotindependentapositiveinteractiontermoccurswhenthecombinedeffectoftreat-mentsisgreaterthantheproductofthetwomainfactors(synergisticinteraction)whereasanegativeinteractiontermreflectsalower-than-expected effect of treatments in combination (antagonistic interac-tion)Inthepresentstudyapositivediversityndashstabilityrelationshipisindicatedwhenthedeviationinbiomassduetotheextremeeventislowerinhigh-comparedtolow-diversitycommunitiesNonparametricbias-corrected95confidenceintervalswerecalculatedbybootstrapsamplingfromeffectsizepoolswith10000iterationsTheLRRissta-tisticallysignificantwhentheboot-strapped95confidence intervaldoesnotoverlapzeroMoredetailsonthemethodologyofthemeta-analysiscanbefoundintheSupportingInformation

Intotalouranalysiscompriseddatafrom28studiespublishedin17articlesthemajorityofwhichaddressedeffectsinEuropeangrasslands Nineteen studies considered extremely dry climaticevents in grasslands (n=17) or forests (n=2)while nine studiesreportedoneffectsofextremelywetclimaticeventsingrasslandsAll wet event studies and the majority of the dry event studieswereperformedwithcommunitiesofrandomspeciescomposition(n=23)meaningthatspeciesarenotmorelikelytobepresentataspecificdiversitylevelIrrespectiveofthetypeofclimaticextreme(dryvswet)speciesrichnesshadapositiveeffectonbiomasspro-ductionTheextremelydryclimaticeventshadanegativeeffectonbiomass production while extremely wet climatic events had no

net effect on productivityHowever ecosystems containingmoreplantspeciesdidnotshowgreaterresistancetoclimateextremesintermsofabove-groundbiomassacrossstudiesMoreoverwefoundno significant interaction between diversity and climate extremesforboththeextremelydryandextremelywetevents(Figure1)Thisresultwas robust ie the same lackofbiodiversityndashresistance re-lationshipwasfoundwithwithoutthe inclusionofexperiments inforestswithwithout the inclusion of studies that experimentallymanipulatedclimateextremesandwithwithoutmonocultures(seeSupportingInformation)Itshouldalsobenotedthatthemeansoftheinteractionsareveryclosetozeroandtheconfidenceintervalsarenarrowfurtherreinforcingtherobustnessoftheconclusionofnon-significantdiversityeffectson resistanceFor theother com-ponentofstabilityrecoveryfewerstudieswereavailableformeta-analysis(n=8)Theresultsrevealanon-significantinteractionbutshouldbetreatedwithcautionduetothepaucityofdata(FigureS1)Takentogetherourresultssuggestanetneutraleffectofdiversityonstabilityreflectingthevariedconclusionsinliterature(TableS1)

Ourqualitativeandquantitativeassessmentofstudiesonbiodi-versityndashstability relationshipsandextremeeventsbothdemonstratethattherearenumerousandnon-trivialexceptionstothepurportedgeneralrulethatbiodiversityincreasesstabilityThisraisestheques-tionofwhetherexistingconceptsofbiodiversityndashstabilityderivedinthe context ofmild climate fluctuations are readily transposable toextremeevents

F IGURE 1emspAverageeffectsize(naturallogresponseratioLRR)ofclimateextremesbiodiversityandtheirinteractiononabove-groundbiomassfordry(n=19studies)andwet(n=9)climateextremesandforallextremestogether(n=28studies)Theeffectsizeofdiversityisbasedonthecomparisonofhighandlowspeciesrichnesslevels(meanspeciesrichnessof117vs19species)Climateextremeshaveareturntimeofonein10years(ormoreextreme)Effectsizesarestatisticallysignificantwhentheboot-strapped95confidenceintervaldoesnotoverlapthezerolineandasignificantinteractionindicatesthateffectsofthetwofactorsarenotindependent

ndash5

ndash4

ndash3

ndash2

ndash1

0

1

2

ExtremeBiodiversityBiodiversity times extreme

LRR

of a

bove

-gro

und

biom

ass

Resistance Recovery


3emsp |emspCAUSES FOR VARIATION IN BIODIVERSITYndashSTABILITY RELATIONSHIPS UNDER CLIMATE EXTREMES

31emsp|emspDifferences between climate extremes

Inconsistentbiodiversityeffectsonstability inthefaceofclimateextremes (Table S1) may in part reflect differences between ex-tremes (typesorproperties)whichgeneratedifferent impacts fora given probability of occurrence (return time) For example themoststudiedtypeofextremedroughtcanbeshortterm(mostlyweeksormonths)with (almost)noprecipitation (pulseeventegLanta Dolezal Zemkova amp Leps 2012) or long term (monthsto years) with prolonged precipitation deficits (press event egEvansByrne LauenrothampBurke2011)Recentmodellingworkhas shown thatpulse andpressdroughtsof the samemagnitudeaffectprimaryproductionandcarbonstoragedifferently (HooverampRogers2016)Thechronicnatureofpressevents implies thatadverse conditions are long-lastingwith only brief periods of re-covery while the ldquoacuterdquo nature of pulse events implies distinctperiods of (intense) stress and stress alleviation (Figure2) Thetemporaldynamicsofextremeeventsalsohavesignificantimplica-tions for resistance and recoveryResistance is likely tobemoreimportant during press events as chronic exposure to stressfulconditions gives time to trigger potential acclimation responses(Zhou Medlyn amp Prentice 2016) and species reordering (Evansetal2011)Pulsedroughtsareshorttermandforagivenreturntime more likely to exceed extreme soil water stress thresholds(Figure2)becausewatersavinginsuchcasesoftenlacksefficiencyasdroughtdefencemechanismsareoverwhelmedandacclimationis limited (Larcher 2003) Alleviation of stress following a pulsedrought is usually more pronounced than after press droughtspromotingfastrecoveryviaaflushofavailablenutrients(DreesenDeBoeckJanssensampNijs2014)Potentialinteractionsbetweenproperties of climate extremes and the different components ofstability like those described here are relevant to diversityndashsta-bilityoutcomesasresistanceandrecoverycanbeaffecteddiffer-entlybybiodiversity(Kreylingetal2017VanRuijvenampBerendse2010seeSection33)

Apartfromtheseverityandspeedofonsetofclimateextremesitisalsopossiblethatthenatureoftheextremeitself(egextremedroughtvsextremeprecipitation)triggersdifferentorevencontrastingdiversity-mediated responses A key aspect here is how plant functional traitsand their associated physiological and phenological processes inter-actwitheachtypeofextremeevent (Reyeretal2013)Forexamplediversity-inducedincreasesinleafarea(SpehnJoshiSchmidDiemerampKoumlrner 2000) or transpiration rates (Kunert SchwendenmannPotvinampHoumllscher2012)maybeadisadvantageunderdrought (Juckeretal2014VanPeerNijsReheulampDeCauwer2004Yangetal2016)butcouldyieldbeneficialeffectsunderconditionswithhightemperaturesasmoreofthetotal leafsurface isat leastpartiallyshadedandorhighertranspiration cools leaves preventing overheating (cfMoro PugnaireHaaseampPuigdefabregas1997)Likewiseadensercanopygenerallyof-fersbetterprotectionagainstsoilerosionduringextremeprecipitationevents(HartantoPrabhuWidayatampAsdak2003)

Extremes such as drought and hot temperatures are usually as-sociatedwithreductionsofabove-groundproductionbutnoteveryextreme event affects ecosystem functioning negatively Some canevenevokegrowth increasessuchasverywetweather inausuallydryregion(HarpolePottsampSuding2007)Inarecentmeta-analysisofgrasslandexperimentsIsbelletal(2015)reportedbothhigherpro-ductivity inwetconditionsandhigherresistancetowetextremesinhigh diversity treatmentsUnlike positive diversity effects observedindryextremeshighdiversityappearstobuffercommunitiesagainstproductivitygains inwetextremes (Isbelletal2015)This isasur-prisingandcounter-intuitiveresultasthemechanismsassociatedwithbiodiversityincreases ieresourcepartitioningandtheselectionef-fectareexpectedtostimulategrowthratherthanreduce itSuchalackofdivergenceinpatternsofresistancetodryandwetextremesemphasises thatmechanismsofdiversityndashstability relationshipsmaybeconfoundedbyaldquoone-size-fits-allrdquoapproachandthathypothesesshouldbetailoredtothesystemandtheextremeinquestion

32emsp|emspDifferences in ecosystem sensitivity to stress

Theorystatingthatdiversitystabilisesecosystemfunctioningintimeis largely derived from observations in systems exposed to mildly

F IGURE 2emspConceptualdepictionofapressdrought(extendedperiodwithsparseprecipitation)andapulsedrought(shortperiodwithnosignificantprecipitation)identicalinreturntime(extremity)Stress(hypotheticalthresholdsforspeciestimesindicated)reacheslessextremelevelsduringpressdroughtsbutlastslongerandfeaturesonlyshortperiodswhen(limited)recoveryispossiblePrecipitationeventsaredepictedbyarrowswithalengththatscaleswithprecipitationamount0 50 100 150 200 250 300 350 50 100 150 200 250 300 350

Mortality thresholdSoi

l wat

er c

onte

nt

Time (days)

Stress threshold

Press drought Pulse drought


fluctuatingenvironmentalconditions(Cardinaleetal2012McCann2000Tilmanetal1996)Directlyextrapolating this toclimateex-tremes assumes little or no interaction of biodiversity effectswiththereturntimeoftheeventinquestionSuchascenarioisdepictedinFigure3awherethemorediverseecosystemreachesathresholdforreducedfunctioningfurtheralongtheextremityaxisthanthelessdiverseecosystemThisresults inpositiveeffectsofbiodiversityonstabilityacrosstheextremitygradientasstress-induceddecreasesinfunctioning are relatively less at higher diversity (but note that thedifferencebetweenlow-andhigh-diversitysystemsdecreasesagainathigherlevelsofextremity)HowevertherearereasonstobelievethisassumptiondoesnotholdformanyecosystemsTherecentmeta-analysis on artificially assembled grassland systems by Isbell etal(2015)showsthatpositivediversityeffectsonresistance to rainfallvariationweresignificantlyreducedinextreme(gt10-yearreturntime)comparedtomoderate (4- to10-year returntime)events Itshouldbenotedthatthelargemajorityofextremesfeaturedintheiranalysishadareturntimebelow50yearsandnonehadareturntimeabove75years (calculatedviaSPEI z-scoresBegueriaVicente-SerranoampAngulo-Martiacutenez2010)meaningthattheanalysisexploredonlypartof the extremity gradient Moreover what is currently consideredrareisexpectedtobecommoninthenearfutureForexamplethe2003heatanddroughtinpartsofEuropeiscalculatedtohaveacur-rentreturntimeofc100yearsbutisprojectedtobeacommonoc-currencebymid-century(ChristidisJonesampStott2015)Inassessingbiodiversityndashstability relationshipsunderclimateextremes thecon-textofongoingclimatechangemakesit imperativetoalsoconsidereventswhicharecurrentlyveryrare

Our literaturesearchfeaturesabroadersetofstudies includingthose on (semi-) natural ecosystems and with imposed extremeswhichthoughdifficulttoquantifyexactlyoftenreportreturntimesexceeding50years(egBloorampBardgett2012Jentschetal2011)Acrossthedatasetwefoundvariedoutcomesoftheconnectionbe-tweendiversityandstabilityGiventheevidenceregardingthevariable

strengthofthediversityndashstabilityrelationshippresentedinbothIsbelletal(2015)andthecurrentstudywesuggestthatthedifferenceinresponsesbetweenecosystems thatare richervspoorer in speciesmaynotbeconstantwithchangingextremityByadaptingFigure3asothattherateofecosystemfunctioningdeclineisnolongerequiva-lentbetweenmoreandlessdiversesystemspositiveneutralorneg-ative diversityndashstability relationships are possible depending on theextremityoftheevent(Figure3b)Thismayhelpexplainwhystudiesfocusingoninterannualvariationormilddryorweteventstendtofindpositivediversityndashstabilityeffectswhilestudiesexplicitlyfocusingonextremeeventsofvariablereturntimereportdiverseoutcomes(TableS1)Insumconclusionsregardingtheeffectofdiversityonthestabil-ityofecosystemfunctioningmaydifferfundamentallyalongagradientofextremity

33emsp|emspTiming of biomass harvests and interacting effects of recovery

Someauthorshavesuggestedthatdiversityhasstabilisingeffectsonecosystemprocesses onlywhen time-scales are sufficient to incor-poratetheaverageneteffectsofdiversityonbothresistancetoandrecoveryfromclimaticstress(Tilmanetal2006)Duringboththeseconstituentphasesofresilience(asdefinedbyHodgsonetal2015)therelationshipwithdiversitymaydiffersignificantlySeveralstudieshavereportedneutralorevennegativebiodiversityeffectsonplantbiomassresistancetoseveredroughtbutpositivediversityeffectsonrecoveryandorresilience(whichcombinesresistanceandrecovery)(VanRuijvenampBerendse2010VogelScherer-LorenzenampWeigelt2012)InarecentstudythatspanneddifferentclimatezonesKreylingetal(2017)foundthatonlyrecoveryandnotresistancewasstimu-lated by species richness in grasslandmesocosms Studies that dif-ferentially incorporate resistanceandrecoverymay therefore reachdifferent conclusions contributing to variation in diversityndashstabilityrelationshipsandcomplicatingdirectcomparisons

F IGURE 3emspEcosystemscandifferintheirresponse(relativetoacontroliebetween0and1)tochangesinenvironmentalconditionsbecauseofdifferencesin(a)thepositionofthestressthreshold(stresslevelwhereresponsesbecomesubstantial)or(b)thesteepnessoftheresponsecurveSituation(a)wouldpromotepositiveeffectsofbiodiversityonstabilityofecosystemfunctioningindependentoftheextremityoftheevent(fromcommontoextreme)whilesituation(b)wouldgiverisetopositive(A)neutral(B)ornegative(C)outcomesforthebiodiversityndashstabilityrelationshipdependingonextremity

0

Sta

bilit

y

Rel

ativ

e re

spon

se (e

g p

rodu

ctiv

ity)

Extremity

(a)

Low biodiversityHigh biodiversity

+Biodiv

1

(b)

+ 0 ndash

A B C


Whenbiomassdataarecollected immediatelyaftertheextremeeventonlyresistance istaken intoaccount (egPfistererampSchmid2002VanPeeretal2004)whileinlong-termbiodiversityndashstabilitystudiesabove-groundproductivityisusuallycollectedatfixedpointsintimeoftenincludingend-of-growingseasonbiomassorevenbio-massproducedintheyearfollowingtheperturbationThisapproachyieldsameasureofstabilitythatveryrarelyonlyreflectsresistanceandalsoshort-andorlong-termrecoverymakingdirectcomparisonsacrossstudies lessstraightforwardandcontributingtotheobservedvariabilityinbiodiversityndashstabilityrelationshipsChangesintheinflu-enceofbioticinteractionsonresistanceandbiodiversityeffectscouldthushelpexplainwhypositivediversityeffectsobservedundermildclimaticvariationmay turnneutralorevennegativewith increasingextremityofenvironmentalconditions

DeClerckBarbourandSawyer(2006)haveproposedthatresis-tanceisprimarilydrivenbycompetitionforasinglelimitingresource(suchaswaterinthecaseofdrought)whereasrecoveryisdrivenbythecapacityofcommunitiestopartitionresourcesintheabsenceofasinglelimitingresourceafterstressreliefThisimpliesthatbiodiversityismorelikelytohaveapositiveeffectonrecoveryasgreaternumbersofcoexistingspeciesarelesslikelytobeequallylimitedbythesameresource (nutrientswater light etc) In the caseof resistance it ishighly probable that the same resource limits the functioning of allspecies so that resource partitioning is diminished and negative in-teractions (ie competition) become dominant Such negative inter-actionswouldbemore likelytodevelopastheresource inquestionbecomesscarcerieastheextremityincreases(rightsideoftheX-axisinFigure3)inlinewithfindingsofMetzandTielboumlrger(2016)whodemonstratedanincreaseincompetitiveeffectsinashrublandduringdryyearsMaestreandCortina (2004) suggesteda shift from facili-tationtocompetitionwhenenvironmentalstressbecomesextremelysevereUndermilderconditionscompetitionforthelimitingresourcewouldbe less intenseandfacilitationandotherbiodiversity-relatedmechanisms such as themore extensiveportfolio of sensitivities athigherdiversitywouldbemoreprominent(Michaletetal2006)in-creasingtheprobabilityoffindingneutralorpositiveeffectsofbiodi-versityonstabilityattheleftsideofFigure3b

Ofcoursediversityeffectsonthestabilityofabove-groundpro-ductivity may not only simply reflect ldquoplant-onlyrdquo mechanisms butalsoplantndashsoil interactionsSeveralstudiessuggestthatplantstabil-itytodroughtmayoccurattheexpenseofmicrobialstability (BloorampBardgett 2012OrwinampWardle2005) likelydrivenby shifts inplantndashmicrobial resourcepartitioningConfoundingeffectsofplantndashsoil interactions may arise if microbial communities differ in theirsensitivity to extremeeventsdependingonplantdiversity (GordonHaygarthampBardgett2008SchimelBalserampWallenstein2007)al-teringpatternsofnutrientreleasebothduringandaftertheclimaticextreme Disentangling the relative role of plantndashplant and plantndashsoil competition for ecosystem responses to environmental changeremains a considerable challenge for ecologists In conclusion theconstituentelementsofstability(resistanceandrecovery)maybedif-ferentlyaffectedbybiodiversitywhileinteractionswiththeextremityoftheeventarelikely

34emsp|emspInteracting effects of plant community assembly

Diversityndashstabilityrelationshipsmaybemediatedbymechanismsofcommunityassembly(ietheprocessesthatshapecommunitycompo-sition)whichinteractwithresistanceandrecoveryfurtherincreasingthe range of potential biodiversityndashstability outcomesMechanismsunderlyingcommunityassemblybothinnaturaandinartificialassem-blagesplayafundamentalroleindeterminingpatternsofproductiv-ityandtraitabundanceatdifferentdiversitylevelsAbioticandbioticdriversbothconstrainspeciesestablishment(McGillEnquistWeiherampWestoby 2006) and determine species loss (Vitousek MooneyLubchencoampMelillo 1997)with nutrient enrichment in particularreducing species diversity via increases in productivity competitiveexclusionandreductionofspeciesrecruitment(FosterampGross1998Grime1973)Speciesthatprofitmostfromnutrientenrichmentareoftenthosespecieswithhighgrowthrateswhileslow-growingspe-cies lose out (cf Hautier Niklaus amp Hector 2009) Consequentlythese low-diversitycommunitiesaremore likely tocontainahigherproportionoffast-growingspeciesthatareoften(butnotalwaysseeGrmanetal 2010WilseyDaneshgarHofmockelampPolley2014)alsomoresusceptibletodroughtandotherextremeevents(Huston1997OueacutedraogoMortierGourlet-FleuryampPicard2013) Incon-trastcommunitieswithhigherspeciesrichnessare likelytocontainahigherproportionofsubordinateslow-growingspeciesandthesemayhelptobuffertheecosystemfunctionfollowingextremeevents(LepšOsbornova-KosinovaampRejmanek1982Mariotteetal2013)Eutrophication-driven diversity losses resulting in highly productivebutspecies-poorplantcommunitiesareofglobalrelevance(Salaetal2000)especiallywith regard topotentialdeclining stabilityof suchimpoverishedecosystems

Unlike studiesbasedonnaturaldiversitygradientsor communi-tiesshapedbydeterministicmechanismsalargenumberofextremeeventstudiesfeaturingmultiplebiodiversitylevelsuseartificialassem-blages (28articles inTableS1)where communitiesdiffering in spe-ciesrichnessarecreated inanon-deterministicmannerThismeansthatthelow-diversity levels includespeciesalsopresentatallotherlevelsorfeaturespeciesthathavebeenpickedrandomlyandnotonthebasisoftheircompetitiveabilityAsaresultlow-diversityexper-imental treatments tend to have a greater probability of containingslow-growingspeciescomparedwithlow-diversityplantcommunitiesinnature(Lepš2004)Thisinturnimpliesthatartificiallyassembledspecies-poorldquoexperimentalcommunitiesrdquomaygenerallybelesssensi-tivetoextremeeventsthanldquoinnaturacommunitiesrdquoimpoverishedinanon-randommanner(egthrougheutrophicationorinvasivespecies)becausetheformerarelesslikelytobedominatedbyfast-growingyetsensitivespecies

Asahypotheticalexampleof thepossibleeffectsofcommunityassemblyondiversityndashstabilityrelationshipssupposethatplantcom-munitieswitheitherartificialorinnaturaassemblypatternsarecom-prisedoftwotypesofspecieswithcontrastingproductivity(Figure4)In linewith the ideasoutlinedaboveweassume that (1) relativelymore productive species are found in lower diversity communities


undernon-randomvs randomassembly (2) there isa trade-offbe-tweenproductivityandresistancetoextremeevents(cfOueacutedraogoetal2013) (3)productivespecies recover fasterafter theextreme(cfLepšetal1982)and (4)positiveeffectsofbiodiversityareas-sumedtodecreaseduringtheresistancephaseand increaseduringtherecoveryphase(cfDeClercketal2006)Outcomesofdiversityvarydependingonboththepatternsofcommunityassemblyandthetimingofbiomassmeasurementsaftertheextreme(Figure4)

While non-random community assembly does not always leadto selection of fast growers in impoverished communities (drivers

such as reduced precipitation may even lead to opposite results cfHarrisonGornishampCopeland2015)itisclearthatoutcomesofdiversityndashstabilitystudiescanvaryifplantgrowthratesorothertraitsthat modulate responses to extreme events are not equally repre-sentedat thesamebiodiversity levelbetweenstudiesFundamentaldiversity-mediated processes may explain further differences be-tweenexperimentaland(semi-)naturalcommunitiesWell-establishedtheorystatesthatathigherdiversitylevelsmoreofthetotalavailableamountofresources(nutrientslightwater)canbeusedbythecom-munityallowingspecies-richcommunitiestoldquooveryieldrdquocomparedtothemonoculturesofthecomposingspecies(LoreauampHector2001)Thisoveryieldingphenomenon(oftenconsideredintermsofbiomassproduction)mayinteractwithclimateextremesaffectingtheoutcomeofbiodiversityndashstabilityrelationshipsForexampletheclearpositiverelationshipbetweenspecies richnessandproductivityobservedbyVanPeeretal(2004)wasreversedduringadroughtwithincreasedmortalityobservedinspecies-richcommunitiesregardlessofspeciesidentityTheauthorsattributedthenegativebiodiversityndashstabilityre-lationshiptoincreasedwateruseinthemoreproductivespecies-richcommunities (cfGrossiordGranierGesslerJuckerampBonal2014)which caused them to reach damaging drought levels earlierThuspositivediversityeffects(increasedresourcepartitioning)underambi-entormildlyfluctuatingclimaticconditionsmayoccurattheexpenseofecosystemstabilityastheevent(egdrought)getsmoreextremeIn conclusion traits of the community thatdifferbetweendiversitylevels shaped by patterns of community assembly or fundamentaldiversity-mediatedprocessescanimproveunderstandingofbiodiver-sityndashstabilityrelationships

4emsp |emspEXPERIMENTAL APPROACHES TO IMPROVE DIVERSITYndashSTABILITY UNDERSTANDING

Throughout this reviewwe have discussed howbiotic (communityassemblybiodiversityeffectsoncommunitytraitspriortotheevent)andabioticfactors(thenatureandreturntimeofclimateeventsun-derlying resource availability) can modulate possible stabilising ef-fectsofbiodiversityunderclimateextremesVariationinthedriversofdiversity effects and the componentsof stability considered cancombinetogiverisetoaplethoraofpossibleoutcomesofbiodiver-sityndashstabilityrelationshipsWearguethatassessmentsoftheroleofbiodiversity instabilisingecosystemfunctioningwouldbenefit fromclear comparisons between studieswhich account for confoundingfactors andprovideexplicit details on the return timeof theevent(seealsoSmith2011)Somestandardisationispossibleforexamplebysystematicallyusingreturntimesofonein10yearsormore(Knappetal2015)andbyusingindiceswhichareclearlycoupledtoreturntimessuchasSPEIinthecaseofdryorwetextremes(Begueriaetal2010)Valuable insightscanalsobegainedbycollectingdataalonganextremitygradient(iemultiplelevelsofreturntime)Changesinbiodiversityndashstability relations along gradients of stress intensity assuggested in Figure3b could be revealed by gradient approaches

F IGURE 4emspAhypotheticalexampleillustratingpotentialinteractionsbetweenbiodiversityndashstabilityrelationshipsandpatternsofcommunityassemblyTwotypesofspecies(XandO)withcontrastinglevelsofproductivityarepresentX-typespeciesaretwiceasproductiveasO-typespeciesundernormalconditionsBiomassproductionrelativetoeachspeciesrsquotypeinherentproductionisrepresentedbyfontsizeandrelativechangesincommunitybiomassareindicatedRandomassemblyimpliesthatbothspeciestypesareequallyrepresentedatalldiversitylevelswhilenon-randomassemblyresultsinahigherproportionofproductivespeciesinlow-diversitycommunities(whichwouldbeexpectedundernutrientenrichmentseetext)LessproductivespeciesareassumedtobemoreresistantbuttohaveslowrecoveryTheeffectsofbiodiversityonstabilityduringandaftertheextremeeventsareshownassumingalimitedrecoveryperiodResilienceintegratesbothresistanceandrecoveryInthisexamplepositiveeffectsofbiodiversity(pre-extremeincludesoveryielding)areassumedtodecreaseduringtheresistancephaseandincreaseduringtherecoveryphase(cfDeClercketal2006VanRuijvenampBerendse2010)DetailsofthecalculationscanbefoundinTableS3FigureS2depictsresultswithoutdifferentdiversityeffectsduringresistanceandrecovery

Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo

Pre-extreme Resistance Resilience

x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110


TABLE 1emspOverviewofstudiesincludedinthemeta-analyses(multipledatasetsderivedfromsinglestudiesareindicatedwhereapplicable)Timingdurationandnatureofextremeevents

(naturalorexperimentallyimposed)areindicatedThetimewindowused(egSPEI-1=1-monthwindow)wasbasedontheeventlengthindicatedinthestudyIfonlyadryorwetyearwas

mentioned(withoutfurtherspecification)thewindowwassettoSPEI-12Inthecaseofexperimentaldroughtno

z-valuesfromtheSPEIdatabasecouldbederivedandeventdurationand

precipitationamountswereusedtoassesswhethertheeventqualifiedasextremeCommunitieswereeitherartificiallyassembled(a)orselectedinnatura(n)Studiespredominantlyfocusedon

grasslands(asteriskindicateswhenthiswasnotthecase)

Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)

SouthAfrica(KrugerNP)

1Drynatural

01rsquo91ndash12rsquo93

36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)

CzechRepublic(Benešov)

1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)

CzechRepublic(Srbsko)

1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)

Switzerland(LaFreacutetaz)

1Dryexperiment


8weeks

na

na

Fiel

dn

813

PfistererandSchmid(2002)

Switzerland(Lupsingen)

1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816

StClairSudderthCastanha

TornandAckerly(2009)

USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17

VanRuijvenandBerendse

(2010)

Netherlands(Wageningen)

1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19

CaldeiraHectorLoreau

PereiraandEriksson(2005)

Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814

GuoSchafferandBuhl(2006)

USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest


using increasingly severe climatic disturbances (ie longer returntimes)wherepossiblethresholdsortippingpointsmaybeidentified(KreylingJentschampBeier2014)Furthermorestudiesshouldmakethedistinctionbetweenresistanceandrecoverybycollectingdataatadequatetime intervalsas focusingontheconstituentelementsofstability offers added value for the interpretation of responses andmechanismsinvolved(seeVanRuijvenampBerendse2010)Finallyre-sultsobtainedinartificiallyassembledcommunitiesshouldbetestedinnaturatotakedifferencespropagatedbycommunityassemblyintoaccountandtoverifywhethertheresultscanbedirectlytranslatedtoreal-worldsystems(Wardle2016)Hereitisespeciallyimportanttoconsiderenvironmentaldriversthatcanaffectbothdiversityandstability (Ives amp Carpenter 2007)We earlier discussed the impor-tanceofnutrientenrichmentand implications fordiversityndashstabilityrelationships and also adaptations to local climate canbe relevantForexampleinthestudyofLloretetal(2007)thenatureofrelation-shipsbetweenspeciesrichnessanddroughtresistancedependedonthetypeofforest(TableS1)whichinturndependedonclimateandhistoricalselectivepressuresTobeabletofullyexplainrelationshipsbetween diversity and stability hypotheses need to be adjusted toincludethemultitudeofcontributingfactors(IvesampCarpenter2007)

Another issue thathinders comparisonsandextrapolation indi-versityndashstabilityresearchinvolvesthedifferentdefinitionsofdiversityacrossstudiesAlthoughmoststudiesinourliteraturesearchquanti-fiedbiodiversitythroughspeciesrichnessdiversityconstitutesmorethanmerelyspeciesnumbersIndeedtheuseofplanttraitvariationand functionaldiversitymetricsmaybemoreappropriate for inves-tigatingdiversityndashstabilityrelationshipsIncreasingevidencesuggeststhat thevaluesandorvarianceofplant traits inagivencommunity(functionaldiversitysensuDiazetal2007)playakeyroleinmodulat-ingecosystemresponsestoenvironmentalchange(Jungetal2014PolleyIsbellampWilsey2013Sudingetal2008)Somestudiesthatreportedanabsenceofpositivediversityeffectsbasedonspeciesrich-nesshavehypothesisedthatthisreflectedalackoffunctionalortraitdiversitywithin the community (egCarterampBlair 2012KennedyBiggsampZambatis2003LuumlbbeSchuldtConersampLeuschner2016)leadingtospeciesrespondingsimilarlytoanextremeeventLimitedtraitdiversitymayconstrainpossiblestabilisingeffectsofasynchrony(DeClercketal2006)orleadtoaccessingresourcesonsimilarspa-tialandtemporalscalesminimisingpotentialcomplementaryeffectsEvenness effects can add further complexity species asynchronyis expected to bemore important in communitieswith a relativelyevendistributionofbiomassamongtheconstituentspecieswhereasthe traitsof thedominant species are likely tobecritical for stabil-ity in communitieswith anunevenbiomassdistribution (HillebrandBennettampCadotte2008Wilseyetal2014)Explicitlyconsideringevennessandtraitvariationinbiodiversityornotmaythereforeleadtodifferentconclusionsregardingtheroleofdiversityinthestabilityofecosystemfunctioning

Wesuggest that trait-basedapproachesmaypavethewayto-wardsamorefundamentalunderstandingoftheroleofldquodiversityrdquoon the stability of ecosystem functioningTrait-based approachesareexpectedtobeparticularlyusefulwhenplantcommunitiesare

dominated by a few species of the same functional group (Polleyetal2013)orforresponsestoshort-termeventssuchasextremedroughtswhichinducerapidfunctionalresponsesviashiftsinspe-ciesabundance(Jungetal2014)orplantplasticityWithinasin-gle species functionaldiversityexpressedbygenotypeshasbeenshowntoimproverecoveryafterclimaticextremes(ReuschEhlersHaumlmmerliampWorm2005)and intraspecificvariation instress re-sponse can actually reach similar levels to interspecific variation(BeierkuhnleinThielJentschWillnerampKreyling2011Malyshevetal2016but seePrietoetal2015)Varyingpatternsof func-tional diversity could thushelpexplaindiscrepanciesbetween re-sultsofbiodiversityndashstabilitystudiestodate

5emsp |emspCONCLUSIONS

Ourreviewindicatesthatmorediverseecosystemsdonotsystemat-icallybuffertheimpactsofclimateextremesonecosystemfunction-ingbetterthanlessdiverseecosystemsWehighlightseveralfactorsthat can modulate or confound diversityndashstability relationshipsunderextremeeventsandmayexplainmixedresultsacrossstud-iestodateInordertobetterassessifandwhenhigherbiodiversitycan buffer climate extreme impactswhich is highly relevant bothforthefunctioningof(semi-)naturalecosystemsandtheenhance-ment of food security in a climate change context (Altieri Funes-Monzote amp Petersen 2012) the broad paradigms in traditionaldiversityndashstabilityliteratureneedtobere-evaluatedWeencouragefurtherresearchinthisareaandtheimplementationofstudiesthat(1) apply climatic extremes in a standardisedmanner (2) compareresponses in artificially assembled and (semi-) natural ecosystemsexplicitlyconsideringcommunityassembly(3)quantifydifferencesin biodiversity using trait-basedmetrics and (4) explicitly separateresistanceandrecoveryRobustexperimentsandclearhypothesesadjustedtothespecificsystemandextremeinquestionwillenhanceourmechanisticunderstandingofbiodiversityndashstabilityeffects

ACKNOWLEDGEMENTS

ThisworkispartoftheprojectSIGNALwhichismainlyfundedbytheERA-NetBiodivERsA (httpwwwbiodiversaorg)with thenationalfunders Belgian Federal Science Policy Office (BELSPO) GermanFederalMinistryofEducationandResearch(BMBF)andMinistegraveredelrsquoEacutecologieduDeacuteveloppementdurableetdelrsquoEacutenergie(France)aspartofthe2011ndash2012BiodivERsAcallforresearchproposalsAdditionalsupport was provided by the Swiss National Science Foundation(projectnumber149862)

AUTHORSrsquo CONTRIBUTIONS

HJDBJMGBandMZdesignedthestudyandperformedthelit-erature searchMZ analysed thedataHJDB JMGB andMZwrotethefirstdraftallauthorscontributedsubstantiallytorevisionsandgavefinalapprovalforpublication


DATA ACCESSIBILITY

Data available from the Dryad Digital Repository httpsdoiorg105061dryad6g8n1 (De Boeck 2017) Data for the meta-analyseswereretrievedfrompublishedstudies(seeTable1)

ORCID

Hans J De Boeck httporcidorg0000-0003-2180-8837

Juergen Kreyling httporcidorg0000-0001-8489-7289

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Barnard P amp ThuillerW (2008) Introduction Global change and bio-diversity Future challenges Biology Letters 4 553ndash555 httpsdoiorg101098rsbl20080374

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Breda N Huc R Granier A amp Dreyer E (2006) Temperate foresttrees and stands under severe droughtA reviewof ecophysiolog-ical responses adaptation processes and long-term consequencesAnnals of Forest Science 63 625ndash644 httpsdoiorg101051forest2006042

CaldeiraMCHectorALoreauMPereiraJSampErikssonO(2005)Species richness temporalvariability and resistanceof biomasspro-ductioninaMediterraneangrasslandOikos110115ndash123httpsdoiorg101111j0030-1299200513873x

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Christidis N Jones G S amp Stott PA (2015)Dramatically increasingchance of extremely hot summers since the 2003 European heat-wave Nature Climate Change 5 46ndash50 httpsdoiorg101038nclimate2468

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De Boeck H J Bassin S Verlinden M Zeiter M amp Hiltbrunner E(2016)Simulatedheatwavesaffectedalpinegrasslandonly incom-bination with drought New Phytologist 209 531ndash541 httpsdoiorg101111nph13601

DeClerckFAJBarbourMGampSawyerJO(2006)Speciesrichnessand stand stability in conifer forests of the Sierra Nevada Ecology87 2787ndash2799 httpsdoiorg1018900012-9658(2006)87[2787 SRASSI]20CO2

DiazSLavorelSdeBelloFQueacutetierFGrigulisKampRobsonTM(2007) Incorporating plant functional diversity effects in ecosystemservice assessmentsProceedings of the National Academy of Sciences of the United States of America 104 20684ndash20689 httpsdoiorg101073pnas0704716104

DoddMESilvertownJMcConwayKPottsJampCrawleyM(1994)Stability intheplantcommunitiesoftheParkGrassExperimentTherelationshipsbetweenspeciesrichnesssoilpHandbiomassvariabilityPhilosophical Transactions of the Royal Society B Biological Sciences346185ndash193httpsdoiorg101098rstb19940140

DreesenFEDeBoeckHJJanssens IAampNijs I (2014)Dosuc-cessiveclimateextremesweakentheresistanceofplantcommunitiesAn experimental study using plant assemblages Biogeosciences 11109ndash121httpsdoiorg105194bg-11-109-2014

EvansSEByrneKMLauenrothWKampBurkeIC(2011)Definingthe limit to resistance in a drought-tolerant grassland Long-termsevere drought significantly reduces the dominant species and in-creases ruderals Journal of Ecology 99 1500ndash1507 httpsdoiorg101111j1365-2745201101864x

FisherEMampKnuttiR(2014)Detectionofspatiallyaggregatedchangesin temperature and precipitation extremes Geophysical Research Letters41547ndash554httpsdoiorg1010022013GL058499

FosterBLampGrossKL(1998)SpeciesrichnessinasuccessionalgrasslandEffectsofnitrogenenrichmentandplantlitterEcology792593ndash2602httpsdoiorg1018900012-9658(1998)079[2593SRIASG]20CO2

Frank D ReichsteinM BahnM Thonicke K Frank DMahechaM D hellip Zscheischler J (2015) Effects of climate extremes onthe terrestrial carbon cycleConcepts processes andpotential fu-ture impacts Global Change Biology 21 2861ndash2880 httpsdoiorg101111gcb12916

GordonHHaygarthPMampBardgettRD(2008)DryingandrewettingeffectsonsoilmicrobialcommunitycompositionandnutrientleachingSoil Biology and Biochemistry 40 302ndash311 httpsdoiorg101016 jsoilbio200708008

GrimeJP(1973)CompetitiveexclusioninherbaceousvegetationNature242344ndash347httpsdoiorg101038242344a0

Grman E Lau J A Schoolmaster D R Jr amp Gross K L (2010)MechanismscontributingtostabilityinecosystemfunctiondependontheenvironmentalcontextEcology Letters131400ndash1410httpsdoiorg101111j1461-0248201001533x

GrossK(2016)EcologyBiodiversityandproductivityentwinedNature529293ndash294httpsdoiorg101038nature16867

GrossKLCardinaleBJFoxJWGonzalezALoreauMPolleyHWhellipvanRuijvenJ (2014)Species richnessand the temporalstabilityofbiomassproductionAnewanalysisof recentbiodiver-sity experiments The American Naturalist 183 1ndash12 httpsdoiorg101086673915

GrossiordCGranierAGesslerAJuckerTampBonalD(2014)Doesdrought influence the relationship betweenbiodiversity and ecosys-tem functioning in boreal forestsEcosystems17 394ndash404 httpsdoiorg101007s10021-013-9729-1

Gruner D S Smith J E Seabloom E W Sandin S A Ngai JT Hillebrand H hellip Bolker B M (2008) A cross-system syn-thesis of consumer and nutrient resource control on pro-ducer biomass Ecology Letters 11 740ndash755 httpsdoiorg101111j1461-0248200801192x

Guo Q Schaffer T amp Buhl T (2006) Community maturity speciessaturation and the variant diversityndashproductivity relationships ingrasslands Ecology Letters 9 1284ndash1292 httpsdoiorg101111 j1461-0248200600980x


Harpole W S Potts D L amp Suding K N (2007) Ecosystem re-sponses to water and nitrogen amendment in a Californiagrassland Global Change Biology 13 2341ndash2348 httpsdoiorg101111j1365-2486200701447x

HarrisonSPGornishESampCopelandS(2015)Climate-drivendiver-sitylossinagrasslandcommunityProceedings of the National Academy of Sciences of the United States of America1128672ndash8677httpsdoiorg101073pnas1502074112

Hartanto H Prabhu R Widayat A S E amp Asdak C (2003)Factors affecting runoff and soil erosion Plot-level soil lossmon-itoring for assessing sustainability of forest management Forest Ecology and Management 180 361ndash374 httpsdoiorg101016S0378-1127(02)00656-4

HautierYNiklausPAampHectorA(2009)Competitionforlightcausesplant biodiversity loss after eutrophication Science 324 636ndash638httpsdoiorg101126science1169640

HedgesLVGurevitchJampCurtisPS(1999)Themeta-analysisofre-sponseratiosinexperimentalecologyEcology801150ndash1156httpsdoiorg1018900012-9658(1999)080[1150TMAORR]20CO2

HillebrandH BennettDMampCadotteMW (2008) Consequencesof dominance A review of evenness effects on local and re-gional ecosystem processes Ecology 89 1510ndash1520 httpsdoiorg10189007-10531

HodgsonDMcDonaldJLampHoskenDJ(2015)Whatdoyoumeanlsquoresilientrsquo Trends in Ecology and Evolution 30 503ndash506 httpsdoiorg101016jtree201506010

HooperDUChapinFSIIIEwelJJHectorAInchaustiPLavorelShellipWardleDA(2005)Effectsofbiodiversityonecosystemfunc-tioningAconsensusofcurrentknowledgeEcological Monographs753ndash35httpsdoiorg10189004-0922

HooverDLKnappAKampSmithMD(2014)ResistanceandresilienceofagrasslandecosystemtoclimateextremesEcology952646ndash2656httpsdoiorg10189013-21861

HooverDLampRogersBM(2016)NotalldroughtsarecreatedequalTheimpactsof interannualdroughtpatternandmagnitudeongrass-landcarboncyclingGlobal Change Biology221809ndash1820httpsdoiorg101111gcb13161

HustonMA (1997)Hidden treatments in ecological experiments Re-evaluating the ecosystem function of biodiversity Oecologia 110449ndash460httpsdoiorg101007s004420050180

IPCC (2013) Climate change 2013 The physical science basis In T FStockerDQinG-KPlattnerMTignorSKAllenJBoschunghellipPMMidgley(Eds)Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate changeCambridgeUKCambridgeUniversityPress

Isbell F CravenD Connolly J LoreauM Schmid B BeierkuhnleinC hellip Eisenhauer N (2015) Biodiversity increases the resistance ofecosystem productivity to climate extremesNature 526 574ndash577httpsdoiorg101038nature15374

IvesARampCarpenterSR(2007)StabilityanddiversityofecosystemsScience31758ndash62httpsdoiorg101126science1133258

Jentsch A Kreyling J Elmer M Gellesch E Glaser B Grant Khellip Beierkuhnlein C (2011) Climate extremes initiate ecosystem-regulatingfunctionswhilemaintainingproductivityJournal of Ecology99689ndash702httpsdoiorg101111j1365-2745201101817x

JuckerTBouriaudOAvacariteiDDanilaIDudumanGValladaresF amp Coomes D A (2014) Competition for light and water playcontrasting roles in driving diversityndashproductivity relationships inIberian forests Journal of Ecology 102 1202ndash1213 httpsdoiorg1011111365-274512276

Jung V Albert C H Violle C Kunstler G Loucougaray G ampSpiegelbergerT(2014)Intraspecifictraitvariabilitymediatesthere-sponseofsubalpinegrasslandcommunitiestoextremedroughteventsJournal of Ecology10245ndash53httpsdoiorg1011111365-2745 12177

KahmenAPernerJampBuchmannN(2005)Diversity-dependentpro-ductivity in semi-natural grasslands following climate perturbationsFunctional Ecology19594ndash601httpsdoiorg101111j1365-2435 200501001x

KaylerZEDeBoeckHJFatichiSGruumlnzweigJMMerboldLBeierChellipDukesJS (2015)Experimentstoconfronttheenvironmentalextremesof climatechangeFrontiers in Ecology and the Environment13219ndash225httpsdoiorg101890140174

KennedyA D Biggs H amp Zambatis N (2003) Relationship betweengrass species richness and ecosystem stability in Kruger NationalParkSouthAfricaAfrican Journal of Ecology41131ndash140httpsdoiorg101046j1365-2028200300391x

KirwanLConnollyJBrophyCBaadshaugOBelanderGBlackAhellipFinnJ(2014)TheAgrodiversityExperimentThreeyearsofdatafromamultisitestudyinintensivelymanagedgrasslandsEcology952680httpsdoiorg10189014-01701

KnappAKHooverDLWilcoxKRAvolioMLKoernerSELaPierreKJhellipSmithMD(2015)Characterizingdifferencesinprecip-itationregimesofextremewetanddryyearsImplicationsforclimatechange experimentsGlobal Change Biology21 2624ndash2633 httpsdoiorg101111gcb12888

KorichevaJGurevitchJampMengersenK(2013)Handbook of meta-anal-ysis in ecology and evolutionPrincetonNJPrincetonUniversityPresshttpsdoiorg1015159781400846184

KreylingJBeierkuhnleinCElmerMPritschKRadovskiMSchloterMhellipJentschA(2008)Soilbioticprocessesremainremarkablysta-bleafter100-yearextremeweathereventsinexperimentalgrasslandand heath Plant and Soil 308 175ndash188 httpsdoiorg101007s11104-008-9617-1

KreylingJDenglerJWalterJVelevNUgurluESopotlievaDhellipJentschA(2017)Speciesrichnesseffectsongrasslandrecoveryfromdroughtdependoncommunityproductivityinamulti-siteexperimentEcology Lettershttpsdoiorg101111ele12848

KreylingJJentschAampBeierC(2014)Beyondrealisminclimatechangeexperiments Gradient approaches identify thresholds and tippingpointsEcology Letters17125ndashe1httpsdoiorg101111ele12193

Kunert N Schwendenmann L Potvin C amp Houmllscher D (2012)Tree diversity enhances tree transpiration in a Panamanian for-est plantation Journal of Applied Ecology 49 135ndash144 httpsdoiorg101111j1365-2664201102065x

LantaVDolezalJZemkovaLampLepsJ(2012)CommunitiesofdifferentplantdiversityrespondsimilarlytodroughtstressExperimentalevidencefromfieldnon-weededandgreenhouseconditionsNaturwissenschaften99473ndash482httpsdoiorg101007s00114-012-0922-4

LarcherW(2003)Physiological plant ecology (4thedn)BerlinSpringer-Verlaghttpsdoiorg101007978-3-662-05214-3

LepšJ (2004)Whatdo thebiodiversityexperiments tellusaboutcon-sequences of plant species loss in the realworldBasic and Applied Ecology5529ndash534

LepšJOsbornova-KosinovaJampRejmanekM(1982)Communitystabil-itycomplexityandspecieslifehistorystrategiesVegetatio5053ndash63

LloretFLoboAEstevanHMaisongrandePVeyredaJampTerradasJ(2007)WoodyplantrichnessandNDVIresponsetodroughteventsin Catalonian (northeastern Spain) forests Ecology 88 2270ndash2279httpsdoiorg10189006-11951

LoreauMampdeMazancourtC (2013)Biodiversityandecosystemsta-bilityAsynthesisofunderlyingmechanismsEcology Letters16106ndash115httpsdoiorg101111ele12073

LoreauM ampHectorA (2001) Partitioning selection and complemen-tarity in biodiversity experiments Nature 412 72ndash76 httpsdoiorg10103835083573

LuumlbbeTSchuldtBConersHampLeuschnerC (2016)Speciesdiver-sityandidentityeffectsonthewaterconsumptionoftreesaplingas-semblagesunderampleandlimitedwatersupplyOikos12586ndash97httpsdoiorg101111oik02367


MacArthur R (1955) Fluctuations of animal populations and a mea-sure of community stability Ecology 36 533ndash536 httpsdoiorg1023071929601

MaestreFTampCortinaJ(2004)DopositiveinteractionsincreasewithabioticstressAtestfromasemi-aridsteppeProceedings of the Royal Society of London Series B271S331ndashS333httpsdoiorg101098rsbl20040181

MalyshevAVArfinKhanMASBeierkuhnleinCSteinbauerMJHenryHALJentschAhellipKreylingJ (2016)Plant responses toclimaticextremesWithin-speciesvariationequalsamong-speciesvari-ationGlobal Change Biology 22 449ndash464 httpsdoiorg101111gcb13114

Mariotte PVandenberghe C Kardol P Hagedorn F ButtlerA ampSchwinning S (2013) Subordinateplant species enhance commu-nity resistance against drought in semi-natural grasslands Journal of Ecology 101 763ndash773 httpsdoiorg1011111365-2745 12064

McCann K S (2000)The diversityndashstability debateNature405 228ndash233httpsdoiorg10103835012234

McGillBJEnquistBJWeiherEampWestobyM (2006)Rebuildingcommunity ecology from functional traits Trends in Ecology and Evolution21178ndash185httpsdoiorg101016jtree200602002

McNaughtonSJ (1977)Diversityandstabilityofecological communi-tiesA comment on the role of empiricism in ecologyThe American Naturalist111515ndash525httpsdoiorg101086283181

MetzJAnnighoumlferPSchallPZimmermannJKahlTSchulzeE-DampAmmerC(2016)Siteadaptedadmixedtreespeciesreducedroughtsusceptibility of mature European beechGlobal Change Biology 22903ndash920httpsdoiorg101111gcb13113

MetzJampTielboumlrgerK(2016)Spatialandtemporalariditygradientspro-videpoor proxies for plantndashplant interactions under climate changeA large-scale experiment Functional Ecology 30 20ndash29 httpsdoiorg1011111365-243512599

Michalet R Brooker R W Cavieres L A Kikvidze Z Lortie CJ Pugnaire F I Callaway R M (2006) Do biotic interactionsshape both sides of the humped-back model of species richnessin plant communities Ecology Letters 9 767ndash773 httpsdoiorg101111j1461-0248200600935x

MoroMJPugnaireF IHaasePampPuigdefabregasJ (1997)Effectof thecanopyofRetamasphaerocarpaon itsunderstorey inasemi-arid environment Functional Ecology 11 425ndash431 httpsdoiorg101046j1365-2435199700106x

Orwin KH ampWardleDA (2005) Plant species composition effectson belowground properties and the resistance and resilience of thesoilmicrofloratoadryingdisturbancePlant and Soil278205ndash221httpsdoiorg101007s11104-005-8424-1

Oueacutedraogo D-Y Mortier F Gourlet-Fleury S amp Picard N (2013)Slow-growing species cope bestwith drought Evidence from long-term measurements in a tropical semi-deciduous moist forest ofCentral Africa Journal of Ecology 101 1459ndash1470 httpsdoiorg1011111365-274512165

PfistererABampSchmidB(2002)Diversity-dependentproductioncandecrease thestabilityofecosystemfunctioningNature41684ndash86httpsdoiorg101038416084a

PolleyHWIsbellFIampWilseyBJ(2013)Plantfunctionaltraitsimprovediversity-basedpredictionsoftemporalstabilityofgrasslandproduc-tivityOikos122 1275ndash1282 httpsdoiorg101111j1600-0706 201300338x

Prieto IViolle C Barre P Durand J L GhesquiereM amp Litrico I(2015) Complementary effects of species and genetic diversity onproductivityandstabilityofsowngrasslandsNature Plants115033httpsdoiorg101038nplants201533

ReuschTBHEhlersAHaumlmmerliAampWormB (2005)Ecosystemrecovery after climatic extremes enhanced by genotypic diversityProceedings of the National Academy of Sciences of the United States

of America 102 2826ndash2831 httpsdoiorg101073pnas0500 008102

Reyer C P Leuzinger S Rammig A Wolf A Bartholomeus R PBonfanteA hellipMonicaMartins G (2013)A plantrsquos perspective ofextremesTerrestrial plant responses to changing climaticvariabilityGlobal Change Biology1975ndash89httpsdoiorg101111gcb12023

RomanukTNVogtRJampKolasaJ(2006)Nutrientenrichmentweak-ens the stabilizing effect of species richnessOikos 114 291ndash302httpsdoiorg101111j20060030-129914739x

SalaOEChapinFSIIIArmestoJJBerlowEBloomfieldJDirzoRhellipWallDH(2000)Globalbiodiversityscenariosfortheyear2100Nature2871770ndash1774

SchimelJBalserTCampWallensteinM(2007)Microbialstress-responsephysiology and its implications for ecosystem function Ecology 881386ndash1394httpsdoiorg10189006-0219

SmithMD(2011)TheecologicalroleofclimateextremesCurrentun-derstanding and future prospects Journal of Ecology 99 651ndash655httpsdoiorg101111j1365-2745201101833x

SpehnEMHectorAJoshiJScherer-LorenzenMSchmidBBazely-WhiteEampLawtonJH(2005)Ecosystemeffectsofbiodiversityma-nipulationsinEuropeangrasslandsEcological Monographs7537ndash63httpsdoiorg10189003-4101

SpehnEMJoshiJSchmidBDiemerMampKoumlrnerC(2000)Above-ground resourceuse increaseswithplant species richness inexperi-mentalgrasslandecosystemsFunctional Ecology14326ndash337httpsdoiorg101046j1365-2435200000437x

StClairSBSudderthEACastanhaCTornMSampAckerlyDD(2009)PlantresponsivenesstovariationinprecipitationandnitrogenisconsistentacrossthecompositionaldiversityofaCaliforniaannualgrassland Journal of Vegetation Science 20 860ndash870 httpsdoiorg101111j1654-1103200901089x

SudingKNLavorelSChapinFSCornelissenJHCDiazSGarnierE hellip Navas M L (2008) Scaling environmental change throughthe community level A trait-based response-and-effect frame-work for plants Global Change Biology 14 1125ndash1140 httpsdoiorg101111j1365-2486200801557x

TilmanD Reich P B ampKnops JMH (2006) Biodiversity and eco-systemstability in adecade-longgrasslandexperimentNature441629ndash631httpsdoiorg101038nature04742

TilmanDWedinDampKnopsJ (1996)ProductivityandsustainabilityinfluencedbybiodiversityingrasslandecosystemsNature379718ndash720httpsdoiorg101038379718a0

ValoneTJampHoffmanCD(2003)PopulationstabilityishigherinmorediverseannualplantcommunitiesEcology Letters690ndash95httpsdoiorg101046j1461-0248200300406x

VanPeerLNijsIReheulDampDeCauwerB(2004)Speciesrichnessandsusceptibilitytoheatanddroughtextremesinsynthesizedgrass-landecosystemsCompositionalvsphysiological effectsFunctional Ecology 18 769ndash778 httpsdoiorg101111j0269-84632004 00901x

VanRuijvenJampBerendseF (2010)Diversityenhancescommunityre-coverybutnotresistanceafterdroughtJournal of Ecology9881ndash86httpsdoiorg101111j1365-2745200901603x

Vitousek P M Mooney H A Lubchenco J amp Melillo J M (1997)Human domination of Earthrsquos ecosystems Science 277 494ndash499httpsdoiorg101126science2775325494

VogelAScherer-LorenzenMampWeigeltA(2012)Grasslandresistanceand resilience after drought depends on management intensity andspeciesrichnessPLoS ONE7e36992httpsdoiorg101371jour-nalpone0036992

WangYYuSampWangJ (2007)Biomass-dependent susceptibility todrought in experimental grassland communities Ecology Letters 10401ndash410httpsdoiorg101111j1461-0248200701031x

WardleDA(2016)Doexperimentsexploringplantdiversityndashecosystemfunctioningrelationshipsinformhowbiodiversitylossimpactsnatural


ecosystems Journal of Vegetation Science 27 646ndash653 httpsdoiorg101111jvs12399

WilseyBJDaneshgarPPHofmockelKampPolleyHW(2014)Invadedgrasslandcommunitieshavealteredstability-maintenancemechanismsbutequalstabilitycomparedtonativecommunitiesEcology Letters1792ndash100httpsdoiorg101111ele12213

WrightAEbelingADeKroonHRoscherCWeigeltAampBuchmanN (2015) Flooding disturbances increase resource availability andproductivitybutreducestabilityindiverseplantcommunitiesNature Communications66062httpsdoiorg101038ncomms7092

YachiSampLoreauM(1999)BiodiversityandecosystemproductivityinafluctuatingenvironmentTheinsurancehypothesisProceedings of the National Academy of Sciences of the United States of America961463ndash1468httpsdoiorg101073pnas9641463

YangZ Jiang L Su F ZhangQXia JampWan S (2016)Nighttimewarmingenhancesdroughtresistanceofplantcommunitiesinatem-perate steppe Scientific Reports 6 23267 httpsdoiorg101038srep23267

ZhouSXMedlynBEampPrenticeC (2016)Long-termwaterstressleads to acclimation of drought sensitivity of photosynthetic capac-ityinxericbutnotriparianEucalyptusspeciesAnnals of Botany117133ndash144httpsdoiorg101093aobmcv161

SUPPORTING INFORMATION

Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle

How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897


andtimingofextremeweatherevents(FisherampKnutti2014IPCC2013)Extremeeventssuchasseveredroughtandperiodsofheavyrainfallhavethepotentialtocausedramaticchangesinplantphysiol-ogypopulationdynamicsandecosystemstructurewithcascadingef-fectsonbiogeochemicalcycling(Franketal2015Reyeretal2013Smith2011)However themechanismsdeterminingecosystem re-sponseandrecoverytoclimateextremesremainunclearmakingvul-nerabilityassessmentsuncertain(Kayleretal2015)

Overthelastdecadeanincreasingnumberofstudieshaveinvesti-gatedtheimpactsofextremeeventsinparticularonherbaceousplantcommunitiesAvailabledataindicatehighvariationinthemagnitudeof ecosystem responses to climate extremes ranging fromminimalimpacts on ecosystem structure and function (Jentsch etal 2011)tomajoreffects in theshortandor long term (BredaHucGranierampDreyer 2006DeBoeckBassinVerlindenZeiterampHiltbrunner2016HooverKnappampSmith2014)Suchcontrastingresultsamongstudieshavebeenattributedtodifferencesinthenatureoftheclimateextremes or the ecosystems in question (Frank etal 2015 Smith2011)Inparticularlevelsofbiodiversitywithinecosystemsmayplayanimportantroleindeterminingecosystemresponsestoclimateex-tremes(Isbelletal2015)Considerableevidencefromtheoreticalandexperimentalstudiessuggeststhathighspeciesdiversitywithineco-systemstendstoincreaseplantcommunitystabilityoftenmeasuredas decreased temporal variability in community biomass (Cardinaleetal 2012McCann2000TilmanWedinampKnops 1996) If bio-diversityplaysastabilisingroleforecosystemssubjectedtoclimaticextremesthennotonlywilldiversitylossimpairecosystemfunctionbutitmayalsoreduceitscapacitytobuffersevereenvironmentalfluc-tuations(LoreauampdeMazancourt2013)

Although interest in diversityndashstability relationships has a longhistory(egMacArthur1955McNaughton1977)theexactmech-anismsunderlyingdiversityndashstability relationships remaina subjectofdebate (GrmanLauSchoolmasterampGross2010Gross2016Loreau amp de Mazancourt 2013) Positive effects of diversity oncommunityfunctioningareoftenlinkedtodifferencesinsensitivityto fluctuations in environmental factors More diverse communi-tiesaregenerallyconsideredtohaveawiderrangeofsensitivitiesEventhoughspeciesresponsesvarycommunityfunctioningismorestable under a rangeof conditions due to species asynchrony andcompensatory responses (cf the ldquoInsurance Hypothesisrdquo Grossetal 2014 Yachi amp Loreau 1999) However most of the theoryondiversityndashstabilityrelationshipsinplantcommunitiesfocusesonyear-to-yearstabilityandormoderatefluctuationsinenvironmentalconditions (Dodd SilvertownMcConway PottsampCrawley 1994Gross etal 2014 RomanukVogt amp Kolasa 2006Tilman Reichamp Knops 2006Valone ampHoffman 2003) It is only relatively re-centlythatstudieshavealsostartedapplyingthistheorytoextremeevents(BloorampBardgett2012Isbelletal2015KahmenPernerampBuchmann2005Kreylingetal2008)Herewereviewtheliter-atureandsynthesiseexperimentalandobservationalstudieswhichexaminetheroleofbiodiversityforecosystemresponsesspecificallyinthecontextofclimateextremesNextweexplorethefactorsun-derlyingvariationinbiodiversityndashstabilityrelationshipsunderclimate

extremesFinallywediscuss future researchdirections thatshouldimprovemechanisticunderstandingofbiodiversityndashstabilityeffectsinachangingenvironment

2emsp |emspLOOKING FOR EVIDENCE DOES BIODIVERSITY PROMOTE STABILITY UNDER CLIMATE EXTREMES

Ecosystemstabilityistypicallyconsideredintermsofresistance(ldquothe instantaneous impact of exogenous disturbance on system staterdquo)andor recovery (ldquothe endogenous processes that pull the disturbed system back towards an equilibriumrdquo)(HodgsonMcDonaldampHosken2015)InthemostcomprehensivestudytodateIsbelletal(2015)showedthatplant species richness increasesbiomass resistancebutnot re-silienceofgrasslandsundernaturalprecipitation regimesofvaryingextremityMoreovertheresultsfromIsbelletal(2015)suggestthatspecies richnessmaybemore important for stability undermoder-ateratherthanextremeeventsHowevertoourknowledgenore-view has explicitly addressed diversityndashstability relationships underextreme climatic eventsHerewe consider extreme climatic eventsintermsoftheirprobabilityofoccurrencedefinedstatisticallyasthe10thpercentileorlessofthedistributionfromalong-termreferencetime-period(Knappetal2015)

Anextensive literaturesearchwasconducted forpeer-reviewedstudies addressing the relationship between biodiversity and eco-systemstabilityforecosystemsexposedtovariousclimateextremes(droughts wet spells and heat waves see Table S1)We used thesearch engines ISIregWeb of Science andGoogle Scholar aswell ascross-referencing to find studies published beforeAugust 2016 re-porting on the effects of extreme climatic events onplant commu-nitiesofdifferentdiversityStudiesthatfocusedontheperformanceofsingleindividualsinaneighbourhoodvaryingindiversity(egMetzetal2016)werenotretainedThefollowingsearchtermswereused(stabilityorresistanceorresilience)(diversityorspeciesrichness)(ex-tremeorsevere) (droughtordryorwaterorwetorprecipitationorsoilmoistureorheatorcoldorwarmortemperatureorclimate)and(grassorplantcommunity)Theliteraturesearchandsubsequentse-lectionreturned43papersthemajorityofwhichaddressedgrasslandsystems(33articles)witharangeofapproachesfromopportunisticobservationalexaminationofnaturalextremesin(semi-)naturaleco-systems to experimentally imposed events in artificially assembledsystems Based on the authorsrsquo own interpretation of results thesupport forpositivediversityndashstabilityeffectswasmixedasneutralandnegativeeffectsofdiversityonecosystemstabilityunderextremeeventswerefrequentlyreported(TableS1)

Whiletheliteraturesearchprovidedamixedqualitativepictureofbiodiversityndashstability relationshipsduring andafter extremeswealsosought amore formal quantitative conclusion throughmeta-analysis(seeSupportingInformation)Inbriefwefocusedourstatisticalanaly-sisonstudiesinvestigatingtheeffectsofextremelydryorwetclimaticevents effects on above-ground biomass as other combinations ofclimaticdriverandor responsevariablewere representedby too few








ndash5

ndash4

ndash3

ndash2

ndash1

0

1

2


LRR

of a

bove

-gro

und

biom

ass

Resistance Recovery











l wat

er c

onte

nt

Time (days)

Stress threshold









0

Sta

bilit

y

Rel

ativ

e re

spon

se (e

g p

rodu

ctiv

ity)

Extremity

(a)


+Biodiv

1

(b)

+ 0 ndash

A B C
















Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES























































































































ndash5

ndash4

ndash3

ndash2

ndash1

0

1

2


LRR

of a

bove

-gro

und

biom

ass

Resistance Recovery











l wat

er c

onte

nt

Time (days)

Stress threshold









0

Sta

bilit

y

Rel

ativ

e re

spon

se (e

g p

rodu

ctiv

ity)

Extremity

(a)


+Biodiv

1

(b)

+ 0 ndash

A B C
















Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES


























































































































l wat

er c

onte

nt

Time (days)

Stress threshold









0

Sta

bilit

y

Rel

ativ

e re

spon

se (e

g p

rodu

ctiv

ity)

Extremity

(a)


+Biodiv

1

(b)

+ 0 ndash

A B C
















Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES























































































































0

Sta

bilit

y

Rel

ativ

e re

spon

se (e

g p

rodu

ctiv

ity)

Extremity

(a)


+Biodiv

1

(b)

+ 0 ndash

A B C
















Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES































































































































Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES























































































































Rand

om a

ssem

bly

xx

xoo

o

xxxooo

xx

xxo

x

o xoooo

x

x

xoo

o

x

x

xx

ox

ox

oo

oo

xx

xoo

o

xx

xxo

x

ox

oooo


x

x

xoo

ox

x

xoo

oBi

odiv

ersit

y

Non

-ran

dom

ass

embl

y

Low

High

0 0+ +

+ ndash 0+

Biod

iver

sity

Low

High

Biodiversity (log)

Biom

ass

Biom

ass

Biodiversity (Log)

Stab

ility

Stab

ility

Stab

ility

Stab

ility

ndash50

ndash65

+80

+180

ndash65

ndash55

+135

+110








Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES























































































































Refe

renc

eLo

catio

nD

atas

ets

Extr

eme

Perio

dD

urat

ion

SPEI

z- va

lue

Sett

ing

Com

posi

tion

Spec

ies r

ichn

ess

DeClercketal(2006)

USA(CA)

1Drynatural

1940ndash2004

Drysummers

SPEI-9

ltminus154

Field

n1ndash4

Juckeretal(2014)

Spain(AltoTajo)

1Drynatural

2005

Dry

yea

rSPEI-12

minus171

Field

n1234

Kennedyetal(2003)


1Drynatural


36months

SPEI-36

minus168

Fiel

dn

3ndash13

Lantaetal(2012)


1Dryexperiment


4months

na

na

Fiel

da

13612

Lantaetal(2012)


1Dryexperiment

na

30days

na

na

Mesocosm

a136

Lepšetal(1982)


1Drynatural


3months

SPEI-3

minus128

Fiel

dn

1318

Mariotteetal(2013)


1Dryexperiment


8weeks

na

na

Fiel

dn

813



1Dryexperiment


8weeks

na

na

Fiel

da

124822

Spehnetal(2005)

Germany(Bayreuth)

1Drynatural


Dry

yea

rSPEI-12

minus180

Fiel

da

124816



USA(Richmond)

2Dryexperiment


6months

na

na

Mesocosm

a17


(2010)


1Drynatural


2months

SPEI-2

minus241

Fiel

da

1248

Vogeletal(2012)

Germany(Jena)

4Dryexperiment


6weeks

na

na

Fiel

da

12481660

WangYuandWang(2007)

China(Heishiding)

1Dryexperiment


4months

na

na

Fiel

da

1ndash40

Wilseyetal(2014)

USA(TX)

2Drynatural


Dry

yea

rSPEI-12

minus205

Fiel

da

19



Portugal(Lezirias)

1Wetnatural


Wetgr

season

SPEI-9

145

Fiel

da

124814


USA(DevilsLake)

1Wetnatural


Wetyear

SPEI-12

135

Fiel

da

1816

Kirwanetal(2014)

Canada(Leacutevis)

1Wetnatural


Wetyear

SPEI-12

215

Fiel

da

14

Kirwanetal(2014)

Norway(Holt)

1Wetnatural


Wetyear

SPEI-12

184

Fiel

da

14

Spehnetal(2005)

Greece(Mytilini)

1Wetnatural


Wetyear

SPEI-12

173

Fiel

da

124818

Spehnetal(2005)

Sweden(Umearing)

1Wetnatural


Wetyear

SPEI-12

192

Fiel

da

1234812

StClairetal(2009)

USA(Richmond)

2Wetexperiment


6months

na

na

Mesocosm

a17

Wrightetal(2015)

Germany(Jena)

1Wetnatural


2months

SPEI-2

225

Fiel

da

1481216

Forest








ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES























































































































ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES

















































































































DATA ACCESSIBILITY


ORCID



REFERENCES




























































































































































































































































Documents

Patterns and drivers of biodiversity–stability