Patterns and drivers of biodiversity–stability ...
Transcript of 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
4emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp5Journal of EcologyDE BOECK Et al
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
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
Begueria S Vicente-Serrano S M amp Angulo-Martiacutenez M (2010) Amultiscalar global drought dataset The Speibase a new griddedproduct for the analysis of drought variability and impacts Bulletin of the American Meteorological Society 91 1351ndash1354 httpsdoiorg1011752010BAMS29881
BeierkuhnleinCThielDJentschAWillnerEampKreylingJ (2011)Ecotypes of European grass species respond differently towarmingand extreme drought Journal of Ecology 99 703ndash713 httpsdoiorg101111j1365-2745201101809x
Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
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
4emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp5Journal of EcologyDE BOECK Et al
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
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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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SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897
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
4emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp5Journal of EcologyDE BOECK Et al
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
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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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Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
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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
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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
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HooverDLKnappAKampSmithMD(2014)ResistanceandresilienceofagrasslandecosystemtoclimateextremesEcology952646ndash2656httpsdoiorg10189013-21861
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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
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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
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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
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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
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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
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RomanukTNVogtRJampKolasaJ(2006)Nutrientenrichmentweak-ens the stabilizing effect of species richnessOikos 114 291ndash302httpsdoiorg101111j20060030-129914739x
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SmithMD(2011)TheecologicalroleofclimateextremesCurrentun-derstanding and future prospects Journal of Ecology 99 651ndash655httpsdoiorg101111j1365-2745201101833x
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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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
4emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp5Journal of EcologyDE BOECK Et al
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
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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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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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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
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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
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Guo Q Schaffer T amp Buhl T (2006) Community maturity speciessaturation and the variant diversityndashproductivity relationships ingrasslands Ecology Letters 9 1284ndash1292 httpsdoiorg101111 j1461-0248200600980x
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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
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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
emspensp emsp | emsp5Journal of EcologyDE BOECK Et al
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
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
REFERENCES
AltieriMAFunes-MonzoteFRampPetersenP(2012)Agroecologicallyefficient agricultural systems for smallholder farmers ContributionstofoodsovereigntyAgronomy for Sustainable Development321ndash13httpsdoiorg101007s13593-011-0065-6
Barnard P amp ThuillerW (2008) Introduction Global change and bio-diversity Future challenges Biology Letters 4 553ndash555 httpsdoiorg101098rsbl20080374
Begueria S Vicente-Serrano S M amp Angulo-Martiacutenez M (2010) Amultiscalar global drought dataset The Speibase a new griddedproduct for the analysis of drought variability and impacts Bulletin of the American Meteorological Society 91 1351ndash1354 httpsdoiorg1011752010BAMS29881
BeierkuhnleinCThielDJentschAWillnerEampKreylingJ (2011)Ecotypes of European grass species respond differently towarmingand extreme drought Journal of Ecology 99 703ndash713 httpsdoiorg101111j1365-2745201101809x
Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
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HooverDLKnappAKampSmithMD(2014)ResistanceandresilienceofagrasslandecosystemtoclimateextremesEcology952646ndash2656httpsdoiorg10189013-21861
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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
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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
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LloretFLoboAEstevanHMaisongrandePVeyredaJampTerradasJ(2007)WoodyplantrichnessandNDVIresponsetodroughteventsin Catalonian (northeastern Spain) forests Ecology 88 2270ndash2279httpsdoiorg10189006-11951
LoreauMampdeMazancourtC (2013)Biodiversityandecosystemsta-bilityAsynthesisofunderlyingmechanismsEcology Letters16106ndash115httpsdoiorg101111ele12073
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LuumlbbeTSchuldtBConersHampLeuschnerC (2016)Speciesdiver-sityandidentityeffectsonthewaterconsumptionoftreesaplingas-semblagesunderampleandlimitedwatersupplyOikos12586ndash97httpsdoiorg101111oik02367
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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
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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
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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
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ValoneTJampHoffmanCD(2003)PopulationstabilityishigherinmorediverseannualplantcommunitiesEcology Letters690ndash95httpsdoiorg101046j1461-0248200300406x
VanPeerLNijsIReheulDampDeCauwerB(2004)Speciesrichnessandsusceptibilitytoheatanddroughtextremesinsynthesizedgrass-landecosystemsCompositionalvsphysiological effectsFunctional Ecology 18 769ndash778 httpsdoiorg101111j0269-84632004 00901x
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SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897
6emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
Begueria S Vicente-Serrano S M amp Angulo-Martiacutenez M (2010) Amultiscalar global drought dataset The Speibase a new griddedproduct for the analysis of drought variability and impacts Bulletin of the American Meteorological Society 91 1351ndash1354 httpsdoiorg1011752010BAMS29881
BeierkuhnleinCThielDJentschAWillnerEampKreylingJ (2011)Ecotypes of European grass species respond differently towarmingand extreme drought Journal of Ecology 99 703ndash713 httpsdoiorg101111j1365-2745201101809x
Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
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VogelAScherer-LorenzenMampWeigeltA(2012)Grasslandresistanceand resilience after drought depends on management intensity andspeciesrichnessPLoS ONE7e36992httpsdoiorg101371jour-nalpone0036992
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emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
ecosystems Journal of Vegetation Science 27 646ndash653 httpsdoiorg101111jvs12399
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WrightAEbelingADeKroonHRoscherCWeigeltAampBuchmanN (2015) Flooding disturbances increase resource availability andproductivitybutreducestabilityindiverseplantcommunitiesNature Communications66062httpsdoiorg101038ncomms7092
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YangZ Jiang L Su F ZhangQXia JampWan S (2016)Nighttimewarmingenhancesdroughtresistanceofplantcommunitiesinatem-perate steppe Scientific Reports 6 23267 httpsdoiorg101038srep23267
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SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897
emspensp emsp | emsp7Journal of EcologyDE BOECK Et al
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
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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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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
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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
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Guo Q Schaffer T amp Buhl T (2006) Community maturity speciessaturation and the variant diversityndashproductivity relationships ingrasslands Ecology Letters 9 1284ndash1292 httpsdoiorg101111 j1461-0248200600980x
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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
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SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897
8emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
05rsquo03ndash09rsquo03
4months
na
na
Fiel
da
13612
Lantaetal(2012)
CzechRepublic(Benešov)
1Dryexperiment
na
30days
na
na
Mesocosm
a136
Lepšetal(1982)
CzechRepublic(Srbsko)
1Drynatural
04rsquo76ndash06rsquo76
3months
SPEI-3
minus128
Fiel
dn
1318
Mariotteetal(2013)
Switzerland(LaFreacutetaz)
1Dryexperiment
07rsquo10ndash09rsquo10
8weeks
na
na
Fiel
dn
813
PfistererandSchmid(2002)
Switzerland(Lupsingen)
1Dryexperiment
07rsquo98ndash09rsquo98
8weeks
na
na
Fiel
da
124822
Spehnetal(2005)
Germany(Bayreuth)
1Drynatural
09rsquo97ndash08rsquo98
Dry
yea
rSPEI-12
minus180
Fiel
da
124816
StClairSudderthCastanha
TornandAckerly(2009)
USA(Richmond)
2Dryexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
VanRuijvenandBerendse
(2010)
Netherlands(Wageningen)
1Drynatural
06rsquo06ndash07rsquo06
2months
SPEI-2
minus241
Fiel
da
1248
Vogeletal(2012)
Germany(Jena)
4Dryexperiment
07rsquo08ndash09rsquo08
6weeks
na
na
Fiel
da
12481660
WangYuandWang(2007)
China(Heishiding)
1Dryexperiment
06rsquo05ndash10rsquo05
4months
na
na
Fiel
da
1ndash40
Wilseyetal(2014)
USA(TX)
2Drynatural
10rsquo10ndash09rsquo11
Dry
yea
rSPEI-12
minus205
Fiel
da
19
CaldeiraHectorLoreau
PereiraandEriksson(2005)
Portugal(Lezirias)
1Wetnatural
10rsquo97ndash06rsquo98
Wetgr
season
SPEI-9
145
Fiel
da
124814
GuoSchafferandBuhl(2006)
USA(DevilsLake)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
135
Fiel
da
1816
Kirwanetal(2014)
Canada(Leacutevis)
1Wetnatural
08rsquo05ndash07rsquo06
Wetyear
SPEI-12
215
Fiel
da
14
Kirwanetal(2014)
Norway(Holt)
1Wetnatural
09rsquo04ndash08rsquo05
Wetyear
SPEI-12
184
Fiel
da
14
Spehnetal(2005)
Greece(Mytilini)
1Wetnatural
06rsquo98ndash05rsquo99
Wetyear
SPEI-12
173
Fiel
da
124818
Spehnetal(2005)
Sweden(Umearing)
1Wetnatural
09rsquo97ndash08rsquo98
Wetyear
SPEI-12
192
Fiel
da
1234812
StClairetal(2009)
USA(Richmond)
2Wetexperiment
11rsquo05ndash05rsquo07
6months
na
na
Mesocosm
a17
Wrightetal(2015)
Germany(Jena)
1Wetnatural
05rsquo13ndash06rsquo13
2months
SPEI-2
225
Fiel
da
1481216
Forest
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
REFERENCES
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Barnard P amp ThuillerW (2008) Introduction Global change and bio-diversity Future challenges Biology Letters 4 553ndash555 httpsdoiorg101098rsbl20080374
Begueria S Vicente-Serrano S M amp Angulo-Martiacutenez M (2010) Amultiscalar global drought dataset The Speibase a new griddedproduct for the analysis of drought variability and impacts Bulletin of the American Meteorological Society 91 1351ndash1354 httpsdoiorg1011752010BAMS29881
BeierkuhnleinCThielDJentschAWillnerEampKreylingJ (2011)Ecotypes of European grass species respond differently towarmingand extreme drought Journal of Ecology 99 703ndash713 httpsdoiorg101111j1365-2745201101809x
Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
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emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897
emspensp emsp | emsp9Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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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McCann K S (2000)The diversityndashstability debateNature405 228ndash233httpsdoiorg10103835012234
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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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
10emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
REFERENCES
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Barnard P amp ThuillerW (2008) Introduction Global change and bio-diversity Future challenges Biology Letters 4 553ndash555 httpsdoiorg101098rsbl20080374
Begueria S Vicente-Serrano S M amp Angulo-Martiacutenez M (2010) Amultiscalar global drought dataset The Speibase a new griddedproduct for the analysis of drought variability and impacts Bulletin of the American Meteorological Society 91 1351ndash1354 httpsdoiorg1011752010BAMS29881
BeierkuhnleinCThielDJentschAWillnerEampKreylingJ (2011)Ecotypes of European grass species respond differently towarmingand extreme drought Journal of Ecology 99 703ndash713 httpsdoiorg101111j1365-2745201101809x
Bloor JM G amp Bardgett R D (2012) Stability of above-ground andbelow-groundprocessestoextremedroughtinmodelgrasslandeco-systems Interactions with plant species diversity and soil nitrogenavailabilityPerspectives in Plant Ecology Evolution and Systematics14193ndash204httpsdoiorg101016jppees201112001
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
CardinaleBJDuffyJEGonzalezAHooperDUPerringsCVenailPhellipNaeemS (2012)Biodiversity lossand its impactonhumanityNature48659ndash67httpsdoiorg101038nature11148
CarterD LampBlairJM (2012)High richness anddense seedingen-hance grassland restoration establishment but have little effect ondroughtresponseEcological Applications221308ndash1319httpsdoiorg10189011-19701
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
DeBoeckH J (2017)Data from Patterns and drivers of biodiversity-stabilityrelationshipsunderclimateextremesDryad Digital Repositoryhttpsdoiorg105061dryad6g8n1
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
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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
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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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
emspensp emsp | emsp11Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
12emsp |emsp emspenspJournal of Ecology DE BOECK Et al
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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
emspensp emsp | emsp13Journal of EcologyDE BOECK Et al
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
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How to cite this articleDeBoeckHJBloorJMGKreylingJetalPatternsanddriversofbiodiversityndashstabilityrelationshipsunderclimateextremesJ Ecol 2017001ndash13 httpsdoiorg1011111365-274512897