J Appl Ecol 20181ndash11 wileyonlinelibrarycomjournaljpe emsp|emsp1copy 2018 The Authors Journal of Applied Ecology copy 2018 British Ecological Society

Received27July2017emsp |emsp Accepted24April2018DOI1011111365-266413179

R E S E A R C H A R T I C L E

A framework for identifying and characterising coral reef ldquooasesrdquo against a backdrop of degradation

James R Guest1 emsp|emspPeter J Edmunds2emsp|emspRuth D Gates1emsp|emspIlsa B Kuffner3 emsp|emsp Andreas J Andersson4emsp|emspBrian B Barnes5emsp|emspIliana Chollett6emsp|emspTravis A Courtney4emsp|emsp Robin Elahi7emsp|emspKevin Gross8emsp|emspElizabeth A Lenz1emsp|emspSatoshi Mitarai9emsp|emsp Peter J Mumby10emsp|emspHannah R Nelson2emsp|emspBritt A Parker11emsp|emspHollie M Putnam12 emsp|emsp Caroline S Rogers13emsp|emspLauren T Toth3

1HawairsquoiInstituteofMarineBiologyUniversityofHawairsquoiKāneʻoheHawaii2DepartmentofBiologyCaliforniaStateUniversityNorthridgeCalifornia3USGeologicalSurveyStPetersburgCoastalampMarineScienceCenterStPetersburgFlorida4ScrippsInstitutionofOceanographyUniversityofCaliforniaSanDiegoLaJollaCalifornia5CollegeofMarineScienceUniversityofSouthFloridaStPetersburgFlorida6SmithsonianMarineStationSmithsonianInstitutionFortPierceFlorida7HopkinsMarineStationStanfordUniversityPacificGroveCalifornia8BiomathematicsGraduateProgramNorthCarolinaStateUniversityRaleighNorthCarolina9OkinawaInstituteofScienceandTechnologyGraduateUniversityOkinawaJapan10MarineSpatialEcologyLabSchoolofBiologicalSciencesandARCCentreofExcellenceforReefStudiesUniversityofQueenslandStLuciaQldAustralia11TheBaldwinGroupInconContractattheNOAACoralReefConservationProgramSilverSpringMaryland12DepartmentofBiologicalSciencesUniversityofRhodeIslandKingstonRhodeIsland and 13USGeologicalSurveyWetlandandAquaticResearchCenterStJohnVirginIslands

CorrespondenceJamesRGuestHawairsquoiInstituteofMarineBiologyUniversityofHawairsquoiKāneʻoheHI96744Emailjrguestgmailcom

Present addresses JamesRGuestSchoolofNaturalandEnvironmentalSciencesNewcastleUniversityNewcastleUponTyneNE17RUUK

BrittAParkerCooperativeInstituteforResearchinEnvironmentalSciencesUniversityofColoradoBoulderBoulderColorado

Funding informationUSGeologicalSurveyJohnWesleyPowellCenterforAnalysisandSynthesisNationalScienceFoundation

HandlingEditorJuliaBlanchard

Abstract1 Humanactivitieshaveledtowidespreadecologicaldeclinehowevertheseverityofdegradationisspatiallyheterogeneousduetosomelocationsresistingescap-ingorreboundingfromdisturbances

2 Wedevelopedaframeworkforidentifyingoaseswithincoralreefregionsusinglong-termmonitoringdataWecalculatedstandardisedestimatesofcoralcover(z-scores) todistinguish sites thatdeviatedpositively from regionalmeansWealsousedthecoefficientofvariation(CV)ofcoralcovertoquantifyhowoasesvariedtemporallyandtodistinguishamongtypesofoasesWeestimatedldquocoralcalcificationcapacityrdquo(CCC)ameasureofthecoralcommunityrsquosabilitytopro-duce calcium carbonate structures and tested for an association between thismetricandz-scoresofcoralcover

3 Weillustratedourz-scoreapproachwithinamodellingframeworkbyextract-ingz-scoresandCVsfromsimulateddatabasedonfourgeneralizedtrajectoriesof coral coverWe then applied the approach to time-seriesdata from long-termreefmonitoringprogrammesinfourfocalregionsinthePacific(themainHawaiian Islands and Morsquoorea French Polynesia) and western Atlantic (theFloridaKeysandStJohnUSVirginIslands)Amongthe123sitesanalysed38hadpositivez-scoresformediancoralcoverandwerecategorisedasoases

4 Synthesis and applicationsOur frameworkprovidesecosystemmanagerswithavaluable tool forconservationby identifying ldquooasesrdquowithindegradedareasBy

ThisarticlehasbeencontributedtobyUSGovernmentemployeesandtheirworkisinthepublicdomainintheUSA

2emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

1emsp |emspINTRODUC TION

Humanactivitiesare impactingecosystemsbymodifyingenviron-mental conditions and natural disturbance regimes over multiplespatial scales (Haberl etal 2007 Halpern etal 2008) As a re-sultecosystemshaveexperienceddeclinesinspeciesabundanceschanges in diversity and compromised ecological function (Doneyetal2012HansenStehmanampPotapov2010)Marineecosystemsare no exception For example coral cover has declined at threequartersofthereefsmonitoredintheCaribbean(JacksonDonovanCrameramp Lam 2014) and an estimatedone-third of globalman-groveandseagrasshabitathasbeen lost (RichardsampFriess2016Waycottetal2009)Nonethelesstheseverityofecosystemdeg-radation is not spatially homogeneous and it is common to findlocationsthatremaininorreturntorelativelygoodconditionde-spiteongoingdisturbances(DavisPavlovaThompsonampSunnucks2013TurnerampCorlett1996)Identifyingcasesinwhichindividualsorcommunitiesperformbetterthantheirneighboursdespitebeingat equal risk is common in public health andmedical fields (egHilborn2007SterninSterninampMarsh1997)Similarapproacheshavebecomepopularinecologyastheymayidentifyareasthatcanbeprioritised for conservation and canprovide insights intoeco-system characteristics that confer resilience (Cinner etal 2016OrsquoLearyetal2017)

Mosttropicalcoralreefsareincreasinglyunderthreatfromlocal-(egoverfishingcoastaldevelopment)orglobal-scale(egclimatechange)disturbances(Hughesetal2017) Inmanycases impactsarereportedaschanges inaveragecoralcoversummarisedacrossmultiplesitestimeperiodsandspatialscales(ie100sndash1000skm2 egDersquoathFabriciusSweatmanampPuotinen2012Jacksonetal2014)Althoughmostregionswithcoralreefshaverecentlyexperi-enceddeclines incoralcover (Hughesetal2017)manyregional-scalestudiesreveal individualsitesthathavenotdeclined incoralcover or those where cover has recovered rapidly (eg Gilmour

Smith Heyward Baird amp Pratchett 2013 Graham JenningsMacNeilMouillotampWilson2015Guestetal2016 Idjadietal2006Roffetal2014)Reefsthatavoidthedeclinesincoralcoverexperiencedby their neighbourshavebeen referred to as ldquooasesrdquo(Lirmanetal2011)andmayrepresentareasofconsiderablecon-servationinterest

The total coverof living corals is themostwidelyusedmetricof coral-reef condition and long-term descriptions of this statevariable are available from numerous locations worldwide (egAdamBurkepileRuttenbergampPaddack2015Dersquoathetal2012RodgersJokielBrownHauampSparks2015Ruzickaetal2013)Largedecreasesincoralcoverleadtodecreasedhabitatcomplexityandcalciumcarbonateproductionandconsequentlyareefrsquos func-tionalabilitytoprovidehabitatandshorelineprotection(Perryetal2015)Ascoralcoverisadynamicstatevariablethatcanfluctuateconsiderablyovertime(egAdametal2015Gilmouretal2013)methodstoidentifyecologicallymeaningfulspatialvariationinreefconditionandfunctionarelikelytobeimprovedbyincorporatingameasureoftemporalvariability

Herewe develop amethodological framework for identifyingecosystemoasesusingcoralreefsasanexamplebasedonspatio-temporalvariabilityincoralcoverWeusethetermldquooasisrdquotodescribereefsitesthatstandoutduetotheirabilitytoescaperesistorre-boundfromdisturbancesFirstweillustratethismethodusingsimu-lateddataparameterisedtorepresentfourtrajectoriesrepresentingcommonpatternsoftemporalchangeincoralcoverobservedoverthe last threedecades (egAdametal2015Dersquoathetal2012Guestetal2016 Idjadietal2006Jacksonetal2014Ruzickaetal2013)We thenexplore theutilityofourmethodby identi-fyingpotential oasis sitesusing thepercentage coverof live coralmeasuredat123reefsitesfromfourfocalregionsoverdecadaltimescalesWetestthehypothesisthatreefoases(asdefinedabove)havefunctionalsignificancefortheproductionandmaintenanceofreefstructurebyevaluatingtherelationshipbetweenstandardisedcoral

evaluatingtrajectoriesofchangeinstate(egcoralcover)amongoasesourap-proachmayhelpinidentifyingthemechanismsresponsibleforspatialvariabilityinecosystem condition Increased mechanistic understanding can guide whethermanagementofaparticular locationshouldemphasiseprotectionmitigationorrestorationAnalysisoftheempiricaldatasuggestthatthemajorityofourcoralreefoasesoriginatedbyeitherescapingorresistingdisturbancesalthoughsomesitesshowedahighcapacityforrecoverywhileotherswerecandidatesforresto-rationFinallyourmeasureofreefcondition(iemedianz-scoresofcoralcover)correlatedpositivelywithcoralcalcificationcapacitysuggestingthatourapproachidentifiedoasesthatarealsoexceptionalforonecriticalcomponentofecologicalfunction

K E Y W O R D S

climatechangecoralreefdeclinedisturbanceoasesrecoveryresiliencespatialvariability

emspensp emsp | emsp3Journal of Applied EcologyGUEST ET al

coverandcoralcalcificationcapacity(CCC)Finallyweevaluatethetrajectoriesofchangeexhibitedbyoasesandspeculateabout themechanismsunderpinningtheirabilitytopersistwhileneighbouringsitesbecomedegradedOurgoalistoprovideaframeworkthatwillassistecosystemmanagersandconservationbiologists to identifythemost(andleast)promisingsiteswithinecosystemswherelong-termdataareavailable

2emsp |emspMATERIAL S AND METHODS

21emsp|emspDefining quantifying and identifying oases

WeconceptualisedanoasisasasitethathasexhibitedconsistentlyhighercoralcoverrelativetositeswithinadefinedfocalregionAsiteisdefinedhereasafixedlocationat10ndash100m2scalewithinareefhabitat depth range or areaof shoreline thathasbeen sur-veyedoveratleastadecadeldquoConsistentlyrdquo(asdefinedhere)referstotheproportionofoccasionsoverwhichcoralcoverateachsiteremained above its regionalmean valuewith region referring toadjacentreefsonascaleof10ndash100sofkmToexaminevariationincoralcoveramongsitesandidentifyoaseswithinfocalregionscoralcoverwasstandardizedonaz-scorescalerelativetothemeancoralcoverofallsitessurveyedwithinagivenyearwithinfocalregionsZ-scoresareusedinavarietyofbiologicalapplicationstoidentifyhowfar and inwhatdirection (positivevsnegative) ameasuredvaluedeviatesfromthepopulationmeanandtheyareexpressedinunitsofstandarddeviation(SD)(WangampChen2012)Z-scoresforapopulationhaveameanofzeroandaSDofoneandaredimension-lessbeingobtainedbydividingthedifferencebetweenindividualvalue (x)andthepopulationmean(μ)bythepopulationSD (σ)

wherexijt=meancoralcoverofsiteiinregionjatyeartμjt = mean coralcoverinregionjatyeartaveragedacrosssitesinthatfocalre-gionandσjt=theSDofcoralcoverinregionjatyearttakenacrosssites in that regionNote that thecalculationofz-scoresdoesnotrequireanyassumptionabouttheshapeoftheunderlyingdistribu-tionofcoralcover

Z-scoreswerefirstcalculatedforeachyearateachsiterelativetoall sites in theregion in thatsameyearThemedianz-scoreforeachsitewasthencalculatedacrossallyearsMedianz-scoreratherthanmeanz-scorewasusedtomeasureasitersquosperformancebe-causemediansarelesssensitivetoanomalousyearsinwhichlargechanges in coral cover occurUsing this approach a site can onlyobtainahighmedianz-scorebyhavingconsistentlyhighcoralcoverrelativetoothersitesinthesameregion

Weusedthecoefficientofvariation(CV)ofcoralcovertoquan-tify temporal variation in coral cover within each site and acrossyears

whereσ istheSDforcoralcoverforeachsiteacrossyearsandμ is themean coral cover for each site across yearsAmeasureoftemporalvariabilitywasincludedbecauseavarietyofcoralcovertrajectories(egdeclinefollowedbyrecoveryphaseshiftwithnorecoveryetc)canpotentiallyproducepositivez-scoresExaminingCVaswellasz-scoresthereforeprovidesamethodtodistinguishbetween sites that exhibit relatively stable coral coverover timefrom sites that oscillate or undergo shifts betweenhigh and lowcoral cover

22emsp|emspNumerical simulations of coral- cover dynamics

Simulationswerecarriedouttoevaluateawiderangeofempiricalpossibilitiesand tocapture thebehaviourofcoral-coverdynamicsbased on four predetermined model scenarios These were con-sidered as representative of trajectories observed from long-termmonitoringofreefsandincluded(a)lineartrends(iewherecoralcover declines or increases linearly over time eg Dersquoath etal2012 Jackson etal 2014) (b) nonlinear oscillations (ie wherecoralcoverundergoescyclesofdeclinefollowedbyrecoveryegGilmouretal2013Idjadietal2006)(c)phaseshifts(iewherecoralcoverdeclinessuddenlyandremains lowegHughesetal2017)and(d)long-termstability(iewherecoralcovervariesfromyear to year but does not increase or decrease significantly overtimeRodgersetal2015Ruzickaetal2013)

Foreachscenariowegenerated30randomvaluesforcoralcoverfora30-yeartimeseriesThemodelparameterswerechosentoreturnvaluesofcoralcoverbetween0and65withanormaldistributionand range that are representativeof contemporarycoral coverdatafrom theCaribbean and Indo-WestPacific (egDersquoath etal 2012Gilmour etal 2013 Guest etal 2016 Idjadi etal 2006 Jacksonetal2014Rodgersetal2015)Anormaldistributioncangeneratevaluesthatareoutsidethedomainoftheresponsevariable(iecoralcovervaluesbetween0and100)thereforewhencoralcoversim-ulationsreturnednegativevaluestheywerereplacedwithzero(coralcovervaluesneverexceeded100inoursimulations)Detailedde-scriptionsofthesimulationstepsalongwiththeparametervaluesandstatisticaldistributionsusedtoinitializetherandomnumbergenera-tionareprovided in theSupporting InformationAppendixS1Aftersimulating100timeseriesforeachscenariowecalculatedthemedianz-scoreandtemporalvariability(CV)ofcoralcoverforeachsimulationandexamined the resultsgraphically (Figure1)Photographicexam-ples inFigure1a illustrateandcomparea typicaldegradedsite (leftphoto)withanoasissite(rightphoto)EachsimulationinFigure1bisanalogoustoaldquositerdquo(asdefinedabove)inasinglelargerfocalregionInFigure1beachpointrepresentsthemedianz- score (x-axis)andCV(y-axis)forasinglesimulatedtimeseriesColoursidentifythefourtra-jectoriesofchangethatwereusedtodefine thesimulationsToaidcomparisonbetweenasinglepointinFigure1btoitscorrespondingtimeseriesinFigure1ctheplotisdividedintocellsrepresentingeightpossibilities(1ndash8)forreefcondition(medianz-scoreofcoralcoverx- axis)andtemporalstability(CVy-axis)Cells1ndash4representthemosttemporallyvariablesimulatedsites(CVge50)andcells5ndash8represent

zijt=(xijtminusjt)

jt

CV = (∕) times 100

4emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

emspensp emsp | emsp5Journal of Applied EcologyGUEST ET al

theleasttemporallyvariablesimulatedsites(CVle51)InFigure1ccoralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshowninFigure1bTheobjectiveofthisplotistoshowthetrajectoriesofcoralcoverthatcouldproducethedistributionofscoresinFigure1b

23emsp|emspExamination of empirical coral- cover data from four focal regions

To apply our approach to empirical data we used public domainlong-termcoralcoverdatafromfourfocalregionsinthePacific(mainHawaiianIslandsandMorsquooreaFrenchPolynesia)andwesternAtlantic(FloridaKeysandStJohnUSVirginIslands)representingspatialscalesranging from ~80 to 17000km2 (Supporting Information Table S1Guestetal2018)Wechosefocalregionswithdifferentdisturbanceregimesbecausetheyprovidedawiderangeofbenthicchangetrajec-toriesuponwhichtotestourframeworkSurveyswerecarriedoutatfixedsitesbetween1992and2015Surveydurationsdifferedamongfocal regions and ranged from11years atMorsquoorea to24years at StJohnMultiplefixedsites(definedhereasdistinctareasofreefsurveyedwithinadefined reefhabitat depth rangeor areaof shoreline)weresurveyedrepeatedly(annuallyoreveryfewyears)ineachfocalregionTocaptureavarietyofdisturbanceevents (egElNintildeoeventsmajorstormsetc)onlysiteswithsurveysextendingoveradecadeormoreandwithatleastthreesurveysduringthatperiodwereusedEachfocalregionhasexperienceddisturbancesincludingoverfishingdiseaseout-breaks thermal stress pollution invasive species predator outbreaksandmajorstorms(Adametal2015Edmunds2002JokielampBrown2004Ruzickaetal2013seeSupportingInformationAppendixS2fordetaileddescriptionofdisturbancehistoriesforeachfocalregion)

For each site mean coral cover was calculated across all sur-veyed transects quadratsor stations (dependenton the samplingdesign for each project) within each year The locations of fixedquadrats transectsorstationswithinsiteswererandomlyorhap-hazardly selected except for two sites in St John (Tektite 1 andYawzi1)whichwereselectedbasedontheirhighcoralcoverin1987(SeeSupportingInformationAppendixS3fordescriptionsofbenthicsurveymethodsforeachfocallocation)

Thresholdsfordeterminingwhetheramedianz-scoreissignificantlygreater than zerowill depend on the particular spatial and temporaldistribution of coral coverwithin the focal region therefore median

z-scoressuggesthowunusualthecoralcoverisatagivensiterelativetotheothersiteswithinthesamefocalregionWeidentifiedallsiteswithpositivemedianz-scores(andthusabove-averagecoralcover inmorethanhalfofthesampledyears)aspotentialoasesAsanadditionalfilterifasitehadbeensurveyedonlythreetimeswithinthemonitoringperiodandifthatsitehaddeclinedincoralcoverbytheendofthestudyitwasnotcountedasanoasiseveniftheoverallmedianz-scorewaspositive

24emsp|emspExamination of the relationship between z- scores for coral cover and CCC

WecalculatedascalarestimateofCCCfor121ofthestudysites(twosites from St Johnwere omitted because data on coral communitystructurewerenotavailable)toevaluatewhetherthismetricofecologi-calfunctionassociatedwithmedianz-scoresofcoralcoverTocalculateCCCforeachsitecalcificationratesofreefscleractinianandhydrozoan(Millepora) taxawere estimated as the product of published skeletallinear-extensionratescoraldensitiesandagrowthformadjustmentfactor (sensuMorganampKench 2012)The growth form adjustmentfactoraccountsfortheemptyspacecreatedbybranchingdigitateorcolumnar morphologies versus massive or encrusting morphologies(MorganampKench2012SupportingInformationTableS2ndashS4)Directmeasuresofthethree-dimensionalsurfacearea(ierugosity)werenotavailableforthesitesusedinthepresentstudythereforecoralcalci-ficationratesweremultipliedbytheplanarpercentagecoverforeachcoraltaxonandforeachyearofstudyfollowingPerryetal(2012)AsaresulttheCCCapproachusedhereassumesthereefisaflatplanarsurfaceandthuswillunderestimateactualcalcificationcapacityWeexaminedtherelationshipbetweenmedianz-scoresforcoralcover(in-dependentvariable) andmedianCCC (kgCaCO3 mminus2 yminus1 dependentvariable)withineachregionusingModelIlinearregressionsaftertest-ingthatresidualsinthelinearmodelwerenormallydistributed

3emsp |emspRESULTS

31emsp|emspNumerical simulations of coral- cover dynamics

Thescatterplotofmedianz- score (x-axis)andCV (y-axis)ofcoralcoverforthe400simulatedsites(Figure1b)showedthatthestablecoral-coverscenarioonlyoccurredinthelowerrowoftheplot(cells5ndash8)whereCVscoreswerelt50Simulatedsiteswithoscillatingor

F IGURE 1emspResultsofsimulationsshowingoutcomesformodelscenariosoflong-termchangeinpercentcoralcover(a)TwophotographsfromEAShinnrsquosphotographictimeseriesatGrecianRocksreefintheFloridaKeys(USGSDataReleasehttpsdoiorg105066F7S46QWR)illustratingdegradedandoasisreefsidentifiedin(b)and(c)In(b)eachpointrepresentsthemedianz- score (x-axis)andcoefficientofvariation(y-axis)forasinglesimulatedtime-serieswithcoloursrepresentingfourscenariosofdifferingchangesincoralcovercorrespondingtolinearchangesoscillatingchangesphaseshiftsfromhigh-tolow-coverandstablecover(colourswithsamecodinginbandc)Theplotisdividedarbitrarilyintocellsrepresentingeightpossibilities(1ndash8)forreefconditionalongaspectrumfromdegradedtooasisstatusthatincorporatesrelativestandardisedcoralcover(z-score)andtemporalstabilityTheplotcontains100simulationsforeachscenarioTimeseriesplotsandfrequencydistributionsofz-scoresofallsimulationsareinSupportingInformationFiguresS1andS2inAppendixS1In(c)coralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshownin(b)ThedashedlineineachplotistheoverallmeancoralcoverforallsimulatedsitesacrosstimeSeemethodsandSupportingInformationAppendixS1foradetaileddescriptionofhowthisfigurewasderived

emspensp emsp | emsp3Journal of Applied EcologyGUEST ET al

coverandcoralcalcificationcapacity(CCC)Finallyweevaluatethetrajectoriesofchangeexhibitedbyoasesandspeculateabout themechanismsunderpinningtheirabilitytopersistwhileneighbouringsitesbecomedegradedOurgoalistoprovideaframeworkthatwillassistecosystemmanagersandconservationbiologists to identifythemost(andleast)promisingsiteswithinecosystemswherelong-termdataareavailable

2emsp |emspMATERIAL S AND METHODS

21emsp|emspDefining quantifying and identifying oases

WeconceptualisedanoasisasasitethathasexhibitedconsistentlyhighercoralcoverrelativetositeswithinadefinedfocalregionAsiteisdefinedhereasafixedlocationat10ndash100m2scalewithinareefhabitat depth range or areaof shoreline thathasbeen sur-veyedoveratleastadecadeldquoConsistentlyrdquo(asdefinedhere)referstotheproportionofoccasionsoverwhichcoralcoverateachsiteremained above its regionalmean valuewith region referring toadjacentreefsonascaleof10ndash100sofkmToexaminevariationincoralcoveramongsitesandidentifyoaseswithinfocalregionscoralcoverwasstandardizedonaz-scorescalerelativetothemeancoralcoverofallsitessurveyedwithinagivenyearwithinfocalregionsZ-scoresareusedinavarietyofbiologicalapplicationstoidentifyhowfar and inwhatdirection (positivevsnegative) ameasuredvaluedeviatesfromthepopulationmeanandtheyareexpressedinunitsofstandarddeviation(SD)(WangampChen2012)Z-scoresforapopulationhaveameanofzeroandaSDofoneandaredimension-lessbeingobtainedbydividingthedifferencebetweenindividualvalue (x)andthepopulationmean(μ)bythepopulationSD (σ)

wherexijt=meancoralcoverofsiteiinregionjatyeartμjt = mean coralcoverinregionjatyeartaveragedacrosssitesinthatfocalre-gionandσjt=theSDofcoralcoverinregionjatyearttakenacrosssites in that regionNote that thecalculationofz-scoresdoesnotrequireanyassumptionabouttheshapeoftheunderlyingdistribu-tionofcoralcover

Z-scoreswerefirstcalculatedforeachyearateachsiterelativetoall sites in theregion in thatsameyearThemedianz-scoreforeachsitewasthencalculatedacrossallyearsMedianz-scoreratherthanmeanz-scorewasusedtomeasureasitersquosperformancebe-causemediansarelesssensitivetoanomalousyearsinwhichlargechanges in coral cover occurUsing this approach a site can onlyobtainahighmedianz-scorebyhavingconsistentlyhighcoralcoverrelativetoothersitesinthesameregion

Weusedthecoefficientofvariation(CV)ofcoralcovertoquan-tify temporal variation in coral cover within each site and acrossyears

whereσ istheSDforcoralcoverforeachsiteacrossyearsandμ is themean coral cover for each site across yearsAmeasureoftemporalvariabilitywasincludedbecauseavarietyofcoralcovertrajectories(egdeclinefollowedbyrecoveryphaseshiftwithnorecoveryetc)canpotentiallyproducepositivez-scoresExaminingCVaswellasz-scoresthereforeprovidesamethodtodistinguishbetween sites that exhibit relatively stable coral coverover timefrom sites that oscillate or undergo shifts betweenhigh and lowcoral cover

22emsp|emspNumerical simulations of coral- cover dynamics

Simulationswerecarriedouttoevaluateawiderangeofempiricalpossibilitiesand tocapture thebehaviourofcoral-coverdynamicsbased on four predetermined model scenarios These were con-sidered as representative of trajectories observed from long-termmonitoringofreefsandincluded(a)lineartrends(iewherecoralcover declines or increases linearly over time eg Dersquoath etal2012 Jackson etal 2014) (b) nonlinear oscillations (ie wherecoralcoverundergoescyclesofdeclinefollowedbyrecoveryegGilmouretal2013Idjadietal2006)(c)phaseshifts(iewherecoralcoverdeclinessuddenlyandremains lowegHughesetal2017)and(d)long-termstability(iewherecoralcovervariesfromyear to year but does not increase or decrease significantly overtimeRodgersetal2015Ruzickaetal2013)

Foreachscenariowegenerated30randomvaluesforcoralcoverfora30-yeartimeseriesThemodelparameterswerechosentoreturnvaluesofcoralcoverbetween0and65withanormaldistributionand range that are representativeof contemporarycoral coverdatafrom theCaribbean and Indo-WestPacific (egDersquoath etal 2012Gilmour etal 2013 Guest etal 2016 Idjadi etal 2006 Jacksonetal2014Rodgersetal2015)Anormaldistributioncangeneratevaluesthatareoutsidethedomainoftheresponsevariable(iecoralcovervaluesbetween0and100)thereforewhencoralcoversim-ulationsreturnednegativevaluestheywerereplacedwithzero(coralcovervaluesneverexceeded100inoursimulations)Detailedde-scriptionsofthesimulationstepsalongwiththeparametervaluesandstatisticaldistributionsusedtoinitializetherandomnumbergenera-tionareprovided in theSupporting InformationAppendixS1Aftersimulating100timeseriesforeachscenariowecalculatedthemedianz-scoreandtemporalvariability(CV)ofcoralcoverforeachsimulationandexamined the resultsgraphically (Figure1)Photographicexam-ples inFigure1a illustrateandcomparea typicaldegradedsite (leftphoto)withanoasissite(rightphoto)EachsimulationinFigure1bisanalogoustoaldquositerdquo(asdefinedabove)inasinglelargerfocalregionInFigure1beachpointrepresentsthemedianz- score (x-axis)andCV(y-axis)forasinglesimulatedtimeseriesColoursidentifythefourtra-jectoriesofchangethatwereusedtodefine thesimulationsToaidcomparisonbetweenasinglepointinFigure1btoitscorrespondingtimeseriesinFigure1ctheplotisdividedintocellsrepresentingeightpossibilities(1ndash8)forreefcondition(medianz-scoreofcoralcoverx- axis)andtemporalstability(CVy-axis)Cells1ndash4representthemosttemporallyvariablesimulatedsites(CVge50)andcells5ndash8represent

zijt=(xijtminusjt)

jt

CV = (∕) times 100

4emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

emspensp emsp | emsp5Journal of Applied EcologyGUEST ET al

theleasttemporallyvariablesimulatedsites(CVle51)InFigure1ccoralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshowninFigure1bTheobjectiveofthisplotistoshowthetrajectoriesofcoralcoverthatcouldproducethedistributionofscoresinFigure1b

23emsp|emspExamination of empirical coral- cover data from four focal regions

To apply our approach to empirical data we used public domainlong-termcoralcoverdatafromfourfocalregionsinthePacific(mainHawaiianIslandsandMorsquooreaFrenchPolynesia)andwesternAtlantic(FloridaKeysandStJohnUSVirginIslands)representingspatialscalesranging from ~80 to 17000km2 (Supporting Information Table S1Guestetal2018)Wechosefocalregionswithdifferentdisturbanceregimesbecausetheyprovidedawiderangeofbenthicchangetrajec-toriesuponwhichtotestourframeworkSurveyswerecarriedoutatfixedsitesbetween1992and2015Surveydurationsdifferedamongfocal regions and ranged from11years atMorsquoorea to24years at StJohnMultiplefixedsites(definedhereasdistinctareasofreefsurveyedwithinadefined reefhabitat depth rangeor areaof shoreline)weresurveyedrepeatedly(annuallyoreveryfewyears)ineachfocalregionTocaptureavarietyofdisturbanceevents (egElNintildeoeventsmajorstormsetc)onlysiteswithsurveysextendingoveradecadeormoreandwithatleastthreesurveysduringthatperiodwereusedEachfocalregionhasexperienceddisturbancesincludingoverfishingdiseaseout-breaks thermal stress pollution invasive species predator outbreaksandmajorstorms(Adametal2015Edmunds2002JokielampBrown2004Ruzickaetal2013seeSupportingInformationAppendixS2fordetaileddescriptionofdisturbancehistoriesforeachfocalregion)

For each site mean coral cover was calculated across all sur-veyed transects quadratsor stations (dependenton the samplingdesign for each project) within each year The locations of fixedquadrats transectsorstationswithinsiteswererandomlyorhap-hazardly selected except for two sites in St John (Tektite 1 andYawzi1)whichwereselectedbasedontheirhighcoralcoverin1987(SeeSupportingInformationAppendixS3fordescriptionsofbenthicsurveymethodsforeachfocallocation)

Thresholdsfordeterminingwhetheramedianz-scoreissignificantlygreater than zerowill depend on the particular spatial and temporaldistribution of coral coverwithin the focal region therefore median

z-scoressuggesthowunusualthecoralcoverisatagivensiterelativetotheothersiteswithinthesamefocalregionWeidentifiedallsiteswithpositivemedianz-scores(andthusabove-averagecoralcover inmorethanhalfofthesampledyears)aspotentialoasesAsanadditionalfilterifasitehadbeensurveyedonlythreetimeswithinthemonitoringperiodandifthatsitehaddeclinedincoralcoverbytheendofthestudyitwasnotcountedasanoasiseveniftheoverallmedianz-scorewaspositive

24emsp|emspExamination of the relationship between z- scores for coral cover and CCC

WecalculatedascalarestimateofCCCfor121ofthestudysites(twosites from St Johnwere omitted because data on coral communitystructurewerenotavailable)toevaluatewhetherthismetricofecologi-calfunctionassociatedwithmedianz-scoresofcoralcoverTocalculateCCCforeachsitecalcificationratesofreefscleractinianandhydrozoan(Millepora) taxawere estimated as the product of published skeletallinear-extensionratescoraldensitiesandagrowthformadjustmentfactor (sensuMorganampKench 2012)The growth form adjustmentfactoraccountsfortheemptyspacecreatedbybranchingdigitateorcolumnar morphologies versus massive or encrusting morphologies(MorganampKench2012SupportingInformationTableS2ndashS4)Directmeasuresofthethree-dimensionalsurfacearea(ierugosity)werenotavailableforthesitesusedinthepresentstudythereforecoralcalci-ficationratesweremultipliedbytheplanarpercentagecoverforeachcoraltaxonandforeachyearofstudyfollowingPerryetal(2012)AsaresulttheCCCapproachusedhereassumesthereefisaflatplanarsurfaceandthuswillunderestimateactualcalcificationcapacityWeexaminedtherelationshipbetweenmedianz-scoresforcoralcover(in-dependentvariable) andmedianCCC (kgCaCO3 mminus2 yminus1 dependentvariable)withineachregionusingModelIlinearregressionsaftertest-ingthatresidualsinthelinearmodelwerenormallydistributed

3emsp |emspRESULTS

31emsp|emspNumerical simulations of coral- cover dynamics

Thescatterplotofmedianz- score (x-axis)andCV (y-axis)ofcoralcoverforthe400simulatedsites(Figure1b)showedthatthestablecoral-coverscenarioonlyoccurredinthelowerrowoftheplot(cells5ndash8)whereCVscoreswerelt50Simulatedsiteswithoscillatingor

F IGURE 1emspResultsofsimulationsshowingoutcomesformodelscenariosoflong-termchangeinpercentcoralcover(a)TwophotographsfromEAShinnrsquosphotographictimeseriesatGrecianRocksreefintheFloridaKeys(USGSDataReleasehttpsdoiorg105066F7S46QWR)illustratingdegradedandoasisreefsidentifiedin(b)and(c)In(b)eachpointrepresentsthemedianz- score (x-axis)andcoefficientofvariation(y-axis)forasinglesimulatedtime-serieswithcoloursrepresentingfourscenariosofdifferingchangesincoralcovercorrespondingtolinearchangesoscillatingchangesphaseshiftsfromhigh-tolow-coverandstablecover(colourswithsamecodinginbandc)Theplotisdividedarbitrarilyintocellsrepresentingeightpossibilities(1ndash8)forreefconditionalongaspectrumfromdegradedtooasisstatusthatincorporatesrelativestandardisedcoralcover(z-score)andtemporalstabilityTheplotcontains100simulationsforeachscenarioTimeseriesplotsandfrequencydistributionsofz-scoresofallsimulationsareinSupportingInformationFiguresS1andS2inAppendixS1In(c)coralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshownin(b)ThedashedlineineachplotistheoverallmeancoralcoverforallsimulatedsitesacrosstimeSeemethodsandSupportingInformationAppendixS1foradetaileddescriptionofhowthisfigurewasderived

4emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

emspensp emsp | emsp5Journal of Applied EcologyGUEST ET al

theleasttemporallyvariablesimulatedsites(CVle51)InFigure1ccoralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshowninFigure1bTheobjectiveofthisplotistoshowthetrajectoriesofcoralcoverthatcouldproducethedistributionofscoresinFigure1b

23emsp|emspExamination of empirical coral- cover data from four focal regions

To apply our approach to empirical data we used public domainlong-termcoralcoverdatafromfourfocalregionsinthePacific(mainHawaiianIslandsandMorsquooreaFrenchPolynesia)andwesternAtlantic(FloridaKeysandStJohnUSVirginIslands)representingspatialscalesranging from ~80 to 17000km2 (Supporting Information Table S1Guestetal2018)Wechosefocalregionswithdifferentdisturbanceregimesbecausetheyprovidedawiderangeofbenthicchangetrajec-toriesuponwhichtotestourframeworkSurveyswerecarriedoutatfixedsitesbetween1992and2015Surveydurationsdifferedamongfocal regions and ranged from11years atMorsquoorea to24years at StJohnMultiplefixedsites(definedhereasdistinctareasofreefsurveyedwithinadefined reefhabitat depth rangeor areaof shoreline)weresurveyedrepeatedly(annuallyoreveryfewyears)ineachfocalregionTocaptureavarietyofdisturbanceevents (egElNintildeoeventsmajorstormsetc)onlysiteswithsurveysextendingoveradecadeormoreandwithatleastthreesurveysduringthatperiodwereusedEachfocalregionhasexperienceddisturbancesincludingoverfishingdiseaseout-breaks thermal stress pollution invasive species predator outbreaksandmajorstorms(Adametal2015Edmunds2002JokielampBrown2004Ruzickaetal2013seeSupportingInformationAppendixS2fordetaileddescriptionofdisturbancehistoriesforeachfocalregion)

For each site mean coral cover was calculated across all sur-veyed transects quadratsor stations (dependenton the samplingdesign for each project) within each year The locations of fixedquadrats transectsorstationswithinsiteswererandomlyorhap-hazardly selected except for two sites in St John (Tektite 1 andYawzi1)whichwereselectedbasedontheirhighcoralcoverin1987(SeeSupportingInformationAppendixS3fordescriptionsofbenthicsurveymethodsforeachfocallocation)

Thresholdsfordeterminingwhetheramedianz-scoreissignificantlygreater than zerowill depend on the particular spatial and temporaldistribution of coral coverwithin the focal region therefore median

z-scoressuggesthowunusualthecoralcoverisatagivensiterelativetotheothersiteswithinthesamefocalregionWeidentifiedallsiteswithpositivemedianz-scores(andthusabove-averagecoralcover inmorethanhalfofthesampledyears)aspotentialoasesAsanadditionalfilterifasitehadbeensurveyedonlythreetimeswithinthemonitoringperiodandifthatsitehaddeclinedincoralcoverbytheendofthestudyitwasnotcountedasanoasiseveniftheoverallmedianz-scorewaspositive

24emsp|emspExamination of the relationship between z- scores for coral cover and CCC

WecalculatedascalarestimateofCCCfor121ofthestudysites(twosites from St Johnwere omitted because data on coral communitystructurewerenotavailable)toevaluatewhetherthismetricofecologi-calfunctionassociatedwithmedianz-scoresofcoralcoverTocalculateCCCforeachsitecalcificationratesofreefscleractinianandhydrozoan(Millepora) taxawere estimated as the product of published skeletallinear-extensionratescoraldensitiesandagrowthformadjustmentfactor (sensuMorganampKench 2012)The growth form adjustmentfactoraccountsfortheemptyspacecreatedbybranchingdigitateorcolumnar morphologies versus massive or encrusting morphologies(MorganampKench2012SupportingInformationTableS2ndashS4)Directmeasuresofthethree-dimensionalsurfacearea(ierugosity)werenotavailableforthesitesusedinthepresentstudythereforecoralcalci-ficationratesweremultipliedbytheplanarpercentagecoverforeachcoraltaxonandforeachyearofstudyfollowingPerryetal(2012)AsaresulttheCCCapproachusedhereassumesthereefisaflatplanarsurfaceandthuswillunderestimateactualcalcificationcapacityWeexaminedtherelationshipbetweenmedianz-scoresforcoralcover(in-dependentvariable) andmedianCCC (kgCaCO3 mminus2 yminus1 dependentvariable)withineachregionusingModelIlinearregressionsaftertest-ingthatresidualsinthelinearmodelwerenormallydistributed

3emsp |emspRESULTS

31emsp|emspNumerical simulations of coral- cover dynamics

Thescatterplotofmedianz- score (x-axis)andCV (y-axis)ofcoralcoverforthe400simulatedsites(Figure1b)showedthatthestablecoral-coverscenarioonlyoccurredinthelowerrowoftheplot(cells5ndash8)whereCVscoreswerelt50Simulatedsiteswithoscillatingor

F IGURE 1emspResultsofsimulationsshowingoutcomesformodelscenariosoflong-termchangeinpercentcoralcover(a)TwophotographsfromEAShinnrsquosphotographictimeseriesatGrecianRocksreefintheFloridaKeys(USGSDataReleasehttpsdoiorg105066F7S46QWR)illustratingdegradedandoasisreefsidentifiedin(b)and(c)In(b)eachpointrepresentsthemedianz- score (x-axis)andcoefficientofvariation(y-axis)forasinglesimulatedtime-serieswithcoloursrepresentingfourscenariosofdifferingchangesincoralcovercorrespondingtolinearchangesoscillatingchangesphaseshiftsfromhigh-tolow-coverandstablecover(colourswithsamecodinginbandc)Theplotisdividedarbitrarilyintocellsrepresentingeightpossibilities(1ndash8)forreefconditionalongaspectrumfromdegradedtooasisstatusthatincorporatesrelativestandardisedcoralcover(z-score)andtemporalstabilityTheplotcontains100simulationsforeachscenarioTimeseriesplotsandfrequencydistributionsofz-scoresofallsimulationsareinSupportingInformationFiguresS1andS2inAppendixS1In(c)coralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshownin(b)ThedashedlineineachplotistheoverallmeancoralcoverforallsimulatedsitesacrosstimeSeemethodsandSupportingInformationAppendixS1foradetaileddescriptionofhowthisfigurewasderived

emspensp emsp | emsp5Journal of Applied EcologyGUEST ET al

theleasttemporallyvariablesimulatedsites(CVle51)InFigure1ccoralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshowninFigure1bTheobjectiveofthisplotistoshowthetrajectoriesofcoralcoverthatcouldproducethedistributionofscoresinFigure1b

23emsp|emspExamination of empirical coral- cover data from four focal regions

To apply our approach to empirical data we used public domainlong-termcoralcoverdatafromfourfocalregionsinthePacific(mainHawaiianIslandsandMorsquooreaFrenchPolynesia)andwesternAtlantic(FloridaKeysandStJohnUSVirginIslands)representingspatialscalesranging from ~80 to 17000km2 (Supporting Information Table S1Guestetal2018)Wechosefocalregionswithdifferentdisturbanceregimesbecausetheyprovidedawiderangeofbenthicchangetrajec-toriesuponwhichtotestourframeworkSurveyswerecarriedoutatfixedsitesbetween1992and2015Surveydurationsdifferedamongfocal regions and ranged from11years atMorsquoorea to24years at StJohnMultiplefixedsites(definedhereasdistinctareasofreefsurveyedwithinadefined reefhabitat depth rangeor areaof shoreline)weresurveyedrepeatedly(annuallyoreveryfewyears)ineachfocalregionTocaptureavarietyofdisturbanceevents (egElNintildeoeventsmajorstormsetc)onlysiteswithsurveysextendingoveradecadeormoreandwithatleastthreesurveysduringthatperiodwereusedEachfocalregionhasexperienceddisturbancesincludingoverfishingdiseaseout-breaks thermal stress pollution invasive species predator outbreaksandmajorstorms(Adametal2015Edmunds2002JokielampBrown2004Ruzickaetal2013seeSupportingInformationAppendixS2fordetaileddescriptionofdisturbancehistoriesforeachfocalregion)

For each site mean coral cover was calculated across all sur-veyed transects quadratsor stations (dependenton the samplingdesign for each project) within each year The locations of fixedquadrats transectsorstationswithinsiteswererandomlyorhap-hazardly selected except for two sites in St John (Tektite 1 andYawzi1)whichwereselectedbasedontheirhighcoralcoverin1987(SeeSupportingInformationAppendixS3fordescriptionsofbenthicsurveymethodsforeachfocallocation)

Thresholdsfordeterminingwhetheramedianz-scoreissignificantlygreater than zerowill depend on the particular spatial and temporaldistribution of coral coverwithin the focal region therefore median

z-scoressuggesthowunusualthecoralcoverisatagivensiterelativetotheothersiteswithinthesamefocalregionWeidentifiedallsiteswithpositivemedianz-scores(andthusabove-averagecoralcover inmorethanhalfofthesampledyears)aspotentialoasesAsanadditionalfilterifasitehadbeensurveyedonlythreetimeswithinthemonitoringperiodandifthatsitehaddeclinedincoralcoverbytheendofthestudyitwasnotcountedasanoasiseveniftheoverallmedianz-scorewaspositive

24emsp|emspExamination of the relationship between z- scores for coral cover and CCC

WecalculatedascalarestimateofCCCfor121ofthestudysites(twosites from St Johnwere omitted because data on coral communitystructurewerenotavailable)toevaluatewhetherthismetricofecologi-calfunctionassociatedwithmedianz-scoresofcoralcoverTocalculateCCCforeachsitecalcificationratesofreefscleractinianandhydrozoan(Millepora) taxawere estimated as the product of published skeletallinear-extensionratescoraldensitiesandagrowthformadjustmentfactor (sensuMorganampKench 2012)The growth form adjustmentfactoraccountsfortheemptyspacecreatedbybranchingdigitateorcolumnar morphologies versus massive or encrusting morphologies(MorganampKench2012SupportingInformationTableS2ndashS4)Directmeasuresofthethree-dimensionalsurfacearea(ierugosity)werenotavailableforthesitesusedinthepresentstudythereforecoralcalci-ficationratesweremultipliedbytheplanarpercentagecoverforeachcoraltaxonandforeachyearofstudyfollowingPerryetal(2012)AsaresulttheCCCapproachusedhereassumesthereefisaflatplanarsurfaceandthuswillunderestimateactualcalcificationcapacityWeexaminedtherelationshipbetweenmedianz-scoresforcoralcover(in-dependentvariable) andmedianCCC (kgCaCO3 mminus2 yminus1 dependentvariable)withineachregionusingModelIlinearregressionsaftertest-ingthatresidualsinthelinearmodelwerenormallydistributed

3emsp |emspRESULTS

31emsp|emspNumerical simulations of coral- cover dynamics

Thescatterplotofmedianz- score (x-axis)andCV (y-axis)ofcoralcoverforthe400simulatedsites(Figure1b)showedthatthestablecoral-coverscenarioonlyoccurredinthelowerrowoftheplot(cells5ndash8)whereCVscoreswerelt50Simulatedsiteswithoscillatingor

F IGURE 1emspResultsofsimulationsshowingoutcomesformodelscenariosoflong-termchangeinpercentcoralcover(a)TwophotographsfromEAShinnrsquosphotographictimeseriesatGrecianRocksreefintheFloridaKeys(USGSDataReleasehttpsdoiorg105066F7S46QWR)illustratingdegradedandoasisreefsidentifiedin(b)and(c)In(b)eachpointrepresentsthemedianz- score (x-axis)andcoefficientofvariation(y-axis)forasinglesimulatedtime-serieswithcoloursrepresentingfourscenariosofdifferingchangesincoralcovercorrespondingtolinearchangesoscillatingchangesphaseshiftsfromhigh-tolow-coverandstablecover(colourswithsamecodinginbandc)Theplotisdividedarbitrarilyintocellsrepresentingeightpossibilities(1ndash8)forreefconditionalongaspectrumfromdegradedtooasisstatusthatincorporatesrelativestandardisedcoralcover(z-score)andtemporalstabilityTheplotcontains100simulationsforeachscenarioTimeseriesplotsandfrequencydistributionsofz-scoresofallsimulationsareinSupportingInformationFiguresS1andS2inAppendixS1In(c)coralcoverfromasinglehaphazardlyselectedsimulationfromeachscenarioisplottedagainsttimewithineachoftheeightcellsshownin(b)ThedashedlineineachplotistheoverallmeancoralcoverforallsimulatedsitesacrosstimeSeemethodsandSupportingInformationAppendixS1foradetaileddescriptionofhowthisfigurewasderived

6emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

phase-shiftedcoralcoveralsooccurredinthecellsrepresentinglowtemporalvariability (ie cells5ndash8)when theoscillationswere lessextremeorwhenaphaseshiftfromhightolowcoralcoveroccurredlaterinthesimulationperiod(egseeFigure1bcells7and8)Withthe input parameters of our simulation we observed no pointswithintheupperrightquadrantofourplotindicatingthatitwasnotpossibleforasitetobebothhighlyvariableandtomaintainahighz-scoreSimulatedoases(iesiteswithpositivemedianz-scoresforcoralcover)werefoundincells47and8(Figure1bc)butthema-jorityhadlowCVs(lt50Figure1bccells7and8)HoweverthereweresomeoasesthathadhighCVs(gt50)indicativeofoscillatingandphase-shiftedscenarios(Figure1bccell4)

32emsp|emspExamination of coral- cover data from four focal regions

Mean coral cover (averaged across sites and within years plusmnSE) in-creasedfrom172plusmn21in1999to272plusmn58in2014inthemainHawaiianIslandsbutitdeclinedfrom126plusmn16in1996to68plusmn09in2015intheFloridaKeysfrom115plusmn51in1992to80plusmn20in2015inStJohnandfrom345plusmn23in2005to185plusmn33in2015in Morsquoorea (Figure2 Supporting Information Appendix S4) Withineachfocalregionmeanannualcoralcover(plusmnSD)variedamongsites(Figure2)andrangedfrom26plusmn10to840plusmn54inthemainsevenHawaiian Islands from 87plusmn61 to 407plusmn49 in Morsquoorea from10plusmn05to265plusmn27intheFloridaKeysandfrom14plusmn06to370plusmn69 inSt JohnMedianz-scoresofcoral cover ranged fromminus108 to +242 for the main Hawaiian Islands minus082 to +187 forMorsquooreaminus096to+250fortheFloridaKeysandfromminus081to+263forStJohn(Figures3and4)

Among our 123 study sites 38 (31)were identified as oasesbased on positive median z-scores of coral cover (ranging from

+002to+263Figures3and4)Oaseshadcoralcoverrangingfrom~11to~84(SupportingInformationTableS1FiguresS3ndashS10inAppendixS4)Ingeneraltheempiricallydefinedoasesexhibitedpat-ternsof temporal change in coral cover consistentwith the simula-tionsForexamplethreeofthefourfocalregions(themainHawaiianIslandstheFloridaKeysandStJohn)hadahighproportion(ge80)ofoaseswithlowtemporalvariability(CVle50)withMorsquooreabeingtheexceptionwherethemajorityofoases(63)hadhightemporalvari-ability(CVge50Figure4a)TheoasissiteswithlowCVweretypicalofthestableandlinear-changescenariosdescribedbythesimulationsExamplesofstableoasissitesfromtheempiricaldataincludeMolokini13 inMauiWestWasherWomenintheFloridaKeysandTektite1in StJohn (Figure4b)Overall only13ofoaseshadhigh tempo-ralvariability (ieCVscoresge50)withmeancoralcovervaluesatthesesitesrangingfrom~15to31(SupportingInformationTableS1FiguresS3ndashS10 inAppendixS4)Thesesiteswerecharacterisedbyperiodsoftimewithcoralcoverbothaboveandbelowtheaveragefor the region In some cases temporallyvariable oases underwentdeclinesfollowedbyamarkedrecoveryforexamplesiteLTER1Outer10inMorsquooreaandMokuoLoʻe2inOʻahutherebyexhibitingtheos-cillatingscenariointhesimulations(Figure4bSupportingInformationFiguresS6andS7inAppendixS4)Inothercasesoasissiteshadrel-ativelyhighcoralcoverforlongperiodsoftimefollowedbyrapidde-clinewithoutrecoveryforexampleAdmiralReefintheFloridaKeys(Figure4bSupportingInformationFiguresS4andS5inAppendixS4)similartothephase-shiftscenariointhesimulations

33emsp|emspExamination of the relationship between coral- cover z- scores and CCC

Median CCC (pooled across years) ranged among sites from ~02to ~228 kg CaCO3 mminus2 yminus1 for the main Hawaiian Islands ~04

F IGURE 2emspLong-termchangesincoralcoverandwithinregion-amongsitevariationin(a)themainHawaiianIslands (n=52sites16years)(b)Morsquoorea(n=18sites11years)(c)theFloridaKeys(n=40sites20years)and(d)StJohnUSVirginIslands(n=13sites24years)PointsrepresentaveragecoralcoverofreplicatesitessurveyedineachyearwithineachfocalregionThefittedlines(LOESScurve)showthesmoothedchangeincoralcoverfortheregionwhilethepointsshowempiricaldatabysiteandyearaveragedacrossreplicatesusedintheoriginalstudies(egquadratstransectsetc)Notedifferentscalesony-axisandtimelineonthex-axis0

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(d)

emspensp emsp | emsp7Journal of Applied EcologyGUEST ET al

to ~54kgmminus2 yminus1 for Morsquoorea ~02 to ~35kgmminus2 yminus1 for theFlorida Keys and ~01 to ~19kgmminus2 yminus1 for St John (SupportingInformationTableS4)AlthoughCCCvariedwidelybetween loca-tionstherewasasignificantpositiverelationshipbetweenmedianz-scoreofcoralcoverandCCCforallfourfocallocations(Figure5)Among focal locationsvariation inmedianz-scoresofcoral coverexplained79ndash87ofthevariationinCCC(Figure5)

4emsp |emspDISCUSSION

Thereareseveralmechanismsthatcanallowcoralcovertopersistat relatively high levels when disturbances degrade neighbouringreefs Firstly oases could exist in a physical setting that is morelikelytoescapedamagebecausetheyareindeeperwaterinareasoutsideof stormtracksorwhereupwellingprovidescooling (egRiegl amp Piller 2003) Secondly oases could possess biological orecologicalcharacteristicsthatallowthemtoresistdamageaffect-ingnearbyreefsforexamplebecausetheirfaunaisacclimatisedor

adaptedtocertaindisturbanceevents(egBrownampCossins2011)Finallyoasesmayreboundrapidlyfollowingdisturbancesbecausekeyecologicalprocessesremainintactforexampleherbivoryandcoral recruitment (eg Gilmour etal 2013Graham etal 2015)We hypothesise therefore that oases identified using the frame-workdescribedherecanbecharacterizedbasedontheircoralcovertrajectories environmental conditions and disturbance historiesasfollows(a)resistantoasesthatareabletotoleratedisturbanceswithoutlosingcoralcoverduetospecifictraitsofthecoralsatthatsite (b)escape oases thathave so far avoidedmajordisturbancesobserved at neighbouring sites due to the physical and environ-mentalcharacteristicsofthesite(c)reboundoasesthatarecapableofrecoveringrapidlyfromdisturbancesduetoarangeofphysicalbiologicalandecologicalprocessesand(d)phase-shiftedoasesthathavehighcoralcoverforlongperiodsoftimebutthathaverecentlydeclinedrapidlyThisfinalcategoryappearscounterintuitivebutaswe argue below some sites that havemaintained high cover his-toricallymaybetargetsforrestorationundercertaincircumstancesEscapeandresistantoasesarelikelytoexhibitlowerCVsandhigh

F IGURE 3emspMapsshowingthefourfocalregionsusedforthisstudy(a)mainHawaiianIslands(b)FloridaKeys(c)MorsquooreaFrenchPolynesiaand(d)StJohnUSVirginIslandsCirclesmarkingsitesarecolourcodedandsizedbasedontheirmedianz-scoreswithincreasingdiametersofsymbolsdenotingincreasingmedianz-scoresImagecreditsEsriDigitalGlobeGeoEyei-cubedUSDAFSAUSGSAEXGetmappingAerogridIGNIGPswisstopoGISusercommunity

(a) (b)

(c) (d)

8emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

positivemedianz-scoreswhereasreboundandphase-shiftedoasesarelikelytoexhibithigherCVsandlowerpositivemedianz- scores Thisframeworkisimportantfromamanagementperspectiveasitpromptsconsiderationofstabilityresistanceorrecoveryofcoralcommunity structurewithin ahistorical contextwhenassigning ameasure of quality to individual siteswithin ecosystems (MumbyChollettBozecampWolff2014)

In this study potential escape oases include Molokini Crater(MauimainHawaiianIslands)andtheTektitesiteat14-mdepthinSt John asbothare relativelyprotected fromstormsandexperi-encerelativelylowlevelsofland-basedinfluences(Edmunds2002Rodgers etal 2015 RogersMcLain amp Tobias 1991) PotentiallyresistantoasesincludeseveralpatchreefsintheFloridaKeys(egWestWasherWomenWesternHeadJaapReef)as theyoccur inareas with high variability in turbidity and temperature that mayhavefavouredhighertolerancetoacutethermalanomalies(Lirmanetal2011Ruzickaetal2013)Potential reboundoases includeanouterfore-reefsiteinMorsquooreaat10-mdepth(LTER1Outer10m)

asthissitehad~47coralcoverin2005lt1in2010(duetopre-dationbyAcanthaster planciandCycloneOliin2010)but~54in2015Similarlyoneshallowsite(2-mdepth)onOʻahu(MokuoLoʻein Kāneʻohe Bay main Hawaiian Islands) increased in coral coverfrom16in2001to49in2012KāneʻoheBayhasalonghistoryofanthropogenicdisturbancesbutcoralcoverappears to recoverwhen localiseddisturbancesareeffectivelymanaged (Bahr JokielampToonen2015)Thehistoryofthissitesuggestsitpossessesprop-ertiesofbothresistantandreboundoasesPotentialphaseshiftedoasesincludeAdmiralintheFloridaKeysasthissitedeclinedfromrelativelyhightolowcoralcoverwithoutrecoveryfollowingararecold-watereventin2010(Lirmanetal2011)Consideringthatthissitemaintainedaveragecoralcoverge21foratleast15yearspriorto2010itseemslikelythattypicalenvironmentalconditionstheremaystillbesuitableforcoralgrowthandsurvivalIfsowesuggestthatAdmiralmaybeapotentiallystrongcandidatefortargetedcoralrestoration(egLirmanampSchopmeyer2016seeFigure4bforex-amplesofcoralcovertrajectories)

F IGURE 4emsp (a)Scatterplotdisplayingrelationshipsbetweenstandardizedcoralcover (median z-scores)andvariabilityincoralcover(coefficientofvariation)forstudysitesidentifiedasoaseswithineachfocalregionfor(redcircles)mainHawaiianIslands(bluesquares)Morsquoorea(greentriangles)FloridaKeysand(bluecrosses)StJohnUSVirginIslands(basedondatainFigure2)SeelegendforFigure1forinterpretation(b)Examplesofcoral-covertrajectoriesfromselectedoasissites(1)MokuoLoʻe2(2)LTER1Outer10(3)Admiral(4)WestWasherWomen(5)Tektite1and(6)Molokini13BlacklinesshowmeancoralcoverforthesiteandtheredlineisoverallmeancoralcoverfortheregionErrorbarsshowplusmnSESitelabelsindicatethepointinthescatterplotin(a)forreferenceLabelsaboveeachsiteindicatesuggestedcategorisationofeachoasistype(seeSection4forexplanation)

emspensp emsp | emsp9Journal of Applied EcologyGUEST ET al

Thereisampleevidencesupportingtheroleofphysicalandbi-ologicaldrivers indeterminingecosystemstateofcoralreefs (egGrahametal2015)NonethelessitispossiblethatsomeoasesexistbecausetheyhavebeensparedfromdisturbancebychancealoneThese ldquoluckyrdquooasesdiffer fromescapeoasesas theydonotpos-sessanyspecificphysicalcharacteristicsthatreducethelikelihoodofbeingdisturbedIfitisthecasethatecosystemstateonreefsisdeterminedmorebystochasticitythanbymechanisticdriversthenconservationplanningwillneedtoincludeaswidearangeofreefsaspossibletomitigateagainstthisuncertainty(Websteretal2017)

While coral cover is an excellent proxy for reef conditionchanges in coral cover alone cannot capture the full spectrum ofchangesthathavenegativelyaffectedcoralreefsinthelastfewde-cadesForexample shifts in taxonomic community structurealsooccurfollowingdisturbancesandthesemayresultinchangesinreeffunction(KuffnerampToth2016)Suchshiftsdescribedasldquorecoverywithoutresiliencerdquohavebeendocumentedonanumberofreefsinthe Indo-WestPacific (egBerumenampPratchett2006)Boththetotalcoverofcoralsandcommunitycompositionplayaroleinde-terminingCCCItisconceivablethereforethatasitedominatedbyslowgrowingtaxacouldexhibitlowCCCandviceversaasitewithlowercoveroffastgrowingtaxacouldexhibitrelativelyhighCCCItisencouragingthereforethatthegenerallyhigherCCCobservedforoasesinthisstudysuggestsagreaterpotentialtomaintainposi-tivenetcoralreef-carbonateproductionrelativetotheirneighboursIt isworthnotinghoweverthat lowratesofCCCforoasesinthetwoCaribbeanfocalregions(egmaxCCCStJohn19kgmminus2 yminus1FloridaKeys35kgmminus2 yminus1)suggestthatnetcarbonateproductionbudgets for these sites may be close to zero once the additional

factors such as bioerosion andCaCO3 dissolution are taken intoaccount(Perryetal2012)

Due to uncertainties about future environmental conditionsnon-oasissitesthathavehistoricallyperformedpoorlymayimproveandsomeoaseswilldeclineiftheypassatippingpoint(Hughesetal2017)We suggest therefore that our frameworkbeusedwithinadaptivenetworksof protected areas that also considerdiversityconnectivity metapopulation conservation and risk mitigation(Websteretal2017)Thereisconsiderableuncertaintyaboutreeffutures due to global change however combiningdetailed distur-bancehistorieswithourapproachcouldlessenthisuncertaintyThepresenceofoasesinsomelocationsdoesnotadvocatecomplacencyabouttheseverityofthecrisisfacingmostoftheworldrsquoscoralreefsOnlyconcertedactiontomanagehumandisturbancesatalocallevelandtacklecarbonemissionsgloballywillsecureafuturefortropicalreefsNonethelesswehope thatour studywill furtherefforts toidentifysimilarldquooasesrdquoinotherecosystems(egtropicalforests)andtoimproveourunderstandingofthemechanisticdriversunderlyingpersistenceofthesesitesinthefaceofglobalscaledegradation

ACKNOWLEDG EMENTS

The ideas presented in this paperwere generated by participantsof theUSGeological Survey (USGS) JohnWesley Powell Centerfor Analysis and Synthesis working group ldquoLocal-scale ecosystemresilienceamidglobal-scaleoceanchangethecoralreefexamplerdquoThisworkwasfundedbytheUSGSthroughtheJohnWesleyPowellCenter (award to PJE RDG and IBK) which supported twomeetingsandaPowellFellowship (award to JRG)The following

F IGURE 5emspScatterplotsshowingtherelationshipbetweenmedianz-scoresofcoralcoverandcoralcalcificationcapacity(CCCkgCaCO3 mminus2 yminus1)forstudysiteswithineachfocalregionfor(a)mainHawaiianIslands(b)Morsquoorea(c)FloridaKeysand(d)StJohnUSVirginIslandsFittedlinesareModelIleast-squareslinearregressionsforpredictedcarbonateproductionr2valuesandsignificancelevelsfortherelationshipareshownforeachplot

(a) (b)

(c) (d)

10emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

group members also received support from the National ScienceFoundationTACKG EAL andAJAThis isHIMBcontribu-tionnumber1728andSOESTContributionnumber10363Wearegrateful to Michael Bode Alasdair Edwards and two anonymousreviewerswhosecommentsandsuggestionsgreatly improved themanuscriptAnyuseoftradenameshereinwasfordescriptivepur-posesonlyanddoesnotimplyendorsementbytheUSGovernmentNoneoftheco-authorshaveanyconflictofinteresttodeclare

AUTHORSrsquo CONTRIBUTIONS

AllauthorscontributedtotheconceptualisationofthisstudyJRGPJERDGandIBKwrotethemanuscriptREproducedthenu-mericalsimulationsTACandAJAproducedthecalculationsofcoral-communitycalcificationcapacityAllauthorsreadandeditedthefinaldraftofthemanuscript

DATA ACCE SSIBILIT Y

Data available via USGS data release httpsdoiorg105066f78w3c7w(Guestetal2018)

ORCID

James R Guest httporcidorg0000-0002-9714-9009

Ilsa B Kuffner httporcidorg0000-0001-8804-7847

Hollie M Putnam httporcidorg0000-0003-2322-3269

R E FE R E N C E S

AdamTBurkepileDRuttenbergBampPaddackM(2015)HerbivoryandtheresilienceofCaribbeancoralreefsKnowledgegapsandim-plicationsformanagementMarine Ecology Progress Series5201ndash20httpsdoiorg103354meps11170

BahrKDJokielPLampToonenRJ(2015)TheunnaturalhistoryofKānersquooheBayCoralreefresilienceinthefaceofcenturiesofanthro-pogenicimpactsPeerJ3e950httpsdoiorg107717peerj950

BerumenMIampPratchettMS(2006)RecoverywithoutresiliencePersistentdisturbancesandlong-termshiftsinthestructureoffishandcoralcommunitiesatTiahuraReefMooreaCoral Reefs25647ndash653httpsdoiorg101007s00338-006-0145-2

Brown B E amp Cossins A R (2011) The potential for temperatureacclimatisation of reef corals in the face of climate change In ZDubinskyampNStambler(Eds)Coral reefs An ecosystem in transition (pp 421ndash433) Dordrecht The Netherlands Springer httpsdoiorg101007978-94-007-0114-4

CinnerJEHucheryCMacNeilMAGrahamNAJMcClanahanT R Maina J hellip Mouillot D (2016) Bright spots among theworldrsquoscoral reefsNature535416ndash419httpsdoiorg101038nature18607

DavisJPavlovaAThompsonRampSunnucksP(2013)Evolutionaryrefugia and ecological refuges Key concepts for conservingAustralianarid zone freshwaterbiodiversityunder climatechangeGlobal Change Biology 19 1970ndash1984 httpsdoiorg101111gcb12203

DersquoathG FabriciusK E SweatmanHampPuotinenM (2012) The27-year decline of coral cover on the Great Barrier Reef and its

causes Proceedings of the National Academy of Sciences of the United States of America 109 17995ndash17999 httpsdoiorg101073pnas1208909109

Doney SC RuckelshausM EmmettDuffy J Barry J PChan FEnglishCAhellipTalleyLD(2012)Climatechangeimpactsonma-rineecosystemsAnnual Review of Marine Science411ndash37httpsdoiorg101146annurev-marine-041911-111611

EdmundsPJ(2002)Long-termdynamicsofcoralreefsinStJohnUSVirginIslandsCoral Reefs21357ndash367

GilmourJPSmithLDHeywardAJBairdAHampPratchettMS (2013) Recovery of an isolated coral reef system following se-vere disturbance Science 340 69ndash71 httpsdoiorg101126science1232310

GrahamNA JenningsSMacNeilMAMouillotDampWilsonSK (2015) Predicting climate-driven regime shifts versus reboundpotentialincoralreefsNature51894ndash97httpsdoiorg101038nature14140

Guest J R Edmunds P J Gates R D Kuffner I B Brown E KRodgersKShellipRogersCS (2018)Time-seriescoral-coverdatafromHawaiiFloridaMooreaandtheVirginIslandsUnitedStatesGeologicalSurveydatareleasehttpsdoiorg105066f78w3c7w

GuestJRTunKLowJVergeacutesAMarzinelliEMCampbellAHhellipSteinbergPD(2016)27yearsofbenthicandcoralcommunitydynamicsonturbidhighlyurbanisedreefsoffSingaporeScientific Reports636260httpsdoiorg101038srep36260

HaberlHErbKHKrausmannFGaubeVBondeauAPlutzarC hellipFischer-KowalskiM(2007)Quantifyingandmappingthehumanappropriation of net primary production in earthrsquos terrestrial eco-systems Proceedings of the National Academy of Sciences of United States of America 104 12942ndash12947 httpsdoiorg101073pnas0704243104

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDrsquoAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences of the United States of America1078650ndash8655httpsdoiorg101073pnas0912668107

Hilborn R (2007) Managing fisheries is managing people Whathas been learned Fish and Fisheries 8 285ndash296 httpsdoiorg101111j1467-2979200700263_2x

Hughes T P BarnesM L Bellwood D R Cinner J E CummingG S Jackson J B C hellip Scheffer M (2017) Coral reefs in theAnthropocene Nature 546 82ndash90 httpsdoiorg101038nature22901

Idjadi J A Lee S C Bruno J F PrechtW F Allen-Requa L ampEdmunds P J (2006) Rapid phase-shift reversal on a Jamaicancoral reef Coral Reefs 25 209ndash211 httpsdoiorg101007s00338-006-0088-7

JacksonJDonovanMCramerKampLamV(2014)Status and trends of Caribbean coral reefs 1970ndash2012IUCNSwitzerlandGlobalCoralReefMonitoringNetwork

Jokiel P L amp Brown E K (2004) Global warming regional trendsand inshore environmental conditions influence coral bleach-ing in Hawaii Global Change Biology 10 1627ndash1641 httpsdoiorg101111j1365-2486200400836x

KuffnerIBampTothLT(2016)Ageologicalperspectiveonthedegra-dationandconservationofwesternAtlanticcoralreefsConservation Biology30706ndash715httpsdoiorg101111cobi12725

LirmanD amp Schopmeyer S (2016) Ecological solutions to reef deg-radation Optimizing coral reef restoration in the Caribbeanand Western Atlantic PeerJ 4 e2597 httpsdoiorg107717 peerj2597

emspensp emsp | emsp7Journal of Applied EcologyGUEST ET al

to ~54kgmminus2 yminus1 for Morsquoorea ~02 to ~35kgmminus2 yminus1 for theFlorida Keys and ~01 to ~19kgmminus2 yminus1 for St John (SupportingInformationTableS4)AlthoughCCCvariedwidelybetween loca-tionstherewasasignificantpositiverelationshipbetweenmedianz-scoreofcoralcoverandCCCforallfourfocallocations(Figure5)Among focal locationsvariation inmedianz-scoresofcoral coverexplained79ndash87ofthevariationinCCC(Figure5)

4emsp |emspDISCUSSION

Thereareseveralmechanismsthatcanallowcoralcovertopersistat relatively high levels when disturbances degrade neighbouringreefs Firstly oases could exist in a physical setting that is morelikelytoescapedamagebecausetheyareindeeperwaterinareasoutsideof stormtracksorwhereupwellingprovidescooling (egRiegl amp Piller 2003) Secondly oases could possess biological orecologicalcharacteristicsthatallowthemtoresistdamageaffect-ingnearbyreefsforexamplebecausetheirfaunaisacclimatisedor

adaptedtocertaindisturbanceevents(egBrownampCossins2011)Finallyoasesmayreboundrapidlyfollowingdisturbancesbecausekeyecologicalprocessesremainintactforexampleherbivoryandcoral recruitment (eg Gilmour etal 2013Graham etal 2015)We hypothesise therefore that oases identified using the frame-workdescribedherecanbecharacterizedbasedontheircoralcovertrajectories environmental conditions and disturbance historiesasfollows(a)resistantoasesthatareabletotoleratedisturbanceswithoutlosingcoralcoverduetospecifictraitsofthecoralsatthatsite (b)escape oases thathave so far avoidedmajordisturbancesobserved at neighbouring sites due to the physical and environ-mentalcharacteristicsofthesite(c)reboundoasesthatarecapableofrecoveringrapidlyfromdisturbancesduetoarangeofphysicalbiologicalandecologicalprocessesand(d)phase-shiftedoasesthathavehighcoralcoverforlongperiodsoftimebutthathaverecentlydeclinedrapidlyThisfinalcategoryappearscounterintuitivebutaswe argue below some sites that havemaintained high cover his-toricallymaybetargetsforrestorationundercertaincircumstancesEscapeandresistantoasesarelikelytoexhibitlowerCVsandhigh

F IGURE 3emspMapsshowingthefourfocalregionsusedforthisstudy(a)mainHawaiianIslands(b)FloridaKeys(c)MorsquooreaFrenchPolynesiaand(d)StJohnUSVirginIslandsCirclesmarkingsitesarecolourcodedandsizedbasedontheirmedianz-scoreswithincreasingdiametersofsymbolsdenotingincreasingmedianz-scoresImagecreditsEsriDigitalGlobeGeoEyei-cubedUSDAFSAUSGSAEXGetmappingAerogridIGNIGPswisstopoGISusercommunity

(a) (b)

(c) (d)

8emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

positivemedianz-scoreswhereasreboundandphase-shiftedoasesarelikelytoexhibithigherCVsandlowerpositivemedianz- scores Thisframeworkisimportantfromamanagementperspectiveasitpromptsconsiderationofstabilityresistanceorrecoveryofcoralcommunity structurewithin ahistorical contextwhenassigning ameasure of quality to individual siteswithin ecosystems (MumbyChollettBozecampWolff2014)

In this study potential escape oases include Molokini Crater(MauimainHawaiianIslands)andtheTektitesiteat14-mdepthinSt John asbothare relativelyprotected fromstormsandexperi-encerelativelylowlevelsofland-basedinfluences(Edmunds2002Rodgers etal 2015 RogersMcLain amp Tobias 1991) PotentiallyresistantoasesincludeseveralpatchreefsintheFloridaKeys(egWestWasherWomenWesternHeadJaapReef)as theyoccur inareas with high variability in turbidity and temperature that mayhavefavouredhighertolerancetoacutethermalanomalies(Lirmanetal2011Ruzickaetal2013)Potential reboundoases includeanouterfore-reefsiteinMorsquooreaat10-mdepth(LTER1Outer10m)

asthissitehad~47coralcoverin2005lt1in2010(duetopre-dationbyAcanthaster planciandCycloneOliin2010)but~54in2015Similarlyoneshallowsite(2-mdepth)onOʻahu(MokuoLoʻein Kāneʻohe Bay main Hawaiian Islands) increased in coral coverfrom16in2001to49in2012KāneʻoheBayhasalonghistoryofanthropogenicdisturbancesbutcoralcoverappears to recoverwhen localiseddisturbancesareeffectivelymanaged (Bahr JokielampToonen2015)Thehistoryofthissitesuggestsitpossessesprop-ertiesofbothresistantandreboundoasesPotentialphaseshiftedoasesincludeAdmiralintheFloridaKeysasthissitedeclinedfromrelativelyhightolowcoralcoverwithoutrecoveryfollowingararecold-watereventin2010(Lirmanetal2011)Consideringthatthissitemaintainedaveragecoralcoverge21foratleast15yearspriorto2010itseemslikelythattypicalenvironmentalconditionstheremaystillbesuitableforcoralgrowthandsurvivalIfsowesuggestthatAdmiralmaybeapotentiallystrongcandidatefortargetedcoralrestoration(egLirmanampSchopmeyer2016seeFigure4bforex-amplesofcoralcovertrajectories)

F IGURE 4emsp (a)Scatterplotdisplayingrelationshipsbetweenstandardizedcoralcover (median z-scores)andvariabilityincoralcover(coefficientofvariation)forstudysitesidentifiedasoaseswithineachfocalregionfor(redcircles)mainHawaiianIslands(bluesquares)Morsquoorea(greentriangles)FloridaKeysand(bluecrosses)StJohnUSVirginIslands(basedondatainFigure2)SeelegendforFigure1forinterpretation(b)Examplesofcoral-covertrajectoriesfromselectedoasissites(1)MokuoLoʻe2(2)LTER1Outer10(3)Admiral(4)WestWasherWomen(5)Tektite1and(6)Molokini13BlacklinesshowmeancoralcoverforthesiteandtheredlineisoverallmeancoralcoverfortheregionErrorbarsshowplusmnSESitelabelsindicatethepointinthescatterplotin(a)forreferenceLabelsaboveeachsiteindicatesuggestedcategorisationofeachoasistype(seeSection4forexplanation)

emspensp emsp | emsp9Journal of Applied EcologyGUEST ET al

Thereisampleevidencesupportingtheroleofphysicalandbi-ologicaldrivers indeterminingecosystemstateofcoralreefs (egGrahametal2015)NonethelessitispossiblethatsomeoasesexistbecausetheyhavebeensparedfromdisturbancebychancealoneThese ldquoluckyrdquooasesdiffer fromescapeoasesas theydonotpos-sessanyspecificphysicalcharacteristicsthatreducethelikelihoodofbeingdisturbedIfitisthecasethatecosystemstateonreefsisdeterminedmorebystochasticitythanbymechanisticdriversthenconservationplanningwillneedtoincludeaswidearangeofreefsaspossibletomitigateagainstthisuncertainty(Websteretal2017)

While coral cover is an excellent proxy for reef conditionchanges in coral cover alone cannot capture the full spectrum ofchangesthathavenegativelyaffectedcoralreefsinthelastfewde-cadesForexample shifts in taxonomic community structurealsooccurfollowingdisturbancesandthesemayresultinchangesinreeffunction(KuffnerampToth2016)Suchshiftsdescribedasldquorecoverywithoutresiliencerdquohavebeendocumentedonanumberofreefsinthe Indo-WestPacific (egBerumenampPratchett2006)Boththetotalcoverofcoralsandcommunitycompositionplayaroleinde-terminingCCCItisconceivablethereforethatasitedominatedbyslowgrowingtaxacouldexhibitlowCCCandviceversaasitewithlowercoveroffastgrowingtaxacouldexhibitrelativelyhighCCCItisencouragingthereforethatthegenerallyhigherCCCobservedforoasesinthisstudysuggestsagreaterpotentialtomaintainposi-tivenetcoralreef-carbonateproductionrelativetotheirneighboursIt isworthnotinghoweverthat lowratesofCCCforoasesinthetwoCaribbeanfocalregions(egmaxCCCStJohn19kgmminus2 yminus1FloridaKeys35kgmminus2 yminus1)suggestthatnetcarbonateproductionbudgets for these sites may be close to zero once the additional

factors such as bioerosion andCaCO3 dissolution are taken intoaccount(Perryetal2012)

Due to uncertainties about future environmental conditionsnon-oasissitesthathavehistoricallyperformedpoorlymayimproveandsomeoaseswilldeclineiftheypassatippingpoint(Hughesetal2017)We suggest therefore that our frameworkbeusedwithinadaptivenetworksof protected areas that also considerdiversityconnectivity metapopulation conservation and risk mitigation(Websteretal2017)Thereisconsiderableuncertaintyaboutreeffutures due to global change however combiningdetailed distur-bancehistorieswithourapproachcouldlessenthisuncertaintyThepresenceofoasesinsomelocationsdoesnotadvocatecomplacencyabouttheseverityofthecrisisfacingmostoftheworldrsquoscoralreefsOnlyconcertedactiontomanagehumandisturbancesatalocallevelandtacklecarbonemissionsgloballywillsecureafuturefortropicalreefsNonethelesswehope thatour studywill furtherefforts toidentifysimilarldquooasesrdquoinotherecosystems(egtropicalforests)andtoimproveourunderstandingofthemechanisticdriversunderlyingpersistenceofthesesitesinthefaceofglobalscaledegradation

ACKNOWLEDG EMENTS

The ideas presented in this paperwere generated by participantsof theUSGeological Survey (USGS) JohnWesley Powell Centerfor Analysis and Synthesis working group ldquoLocal-scale ecosystemresilienceamidglobal-scaleoceanchangethecoralreefexamplerdquoThisworkwasfundedbytheUSGSthroughtheJohnWesleyPowellCenter (award to PJE RDG and IBK) which supported twomeetingsandaPowellFellowship (award to JRG)The following

F IGURE 5emspScatterplotsshowingtherelationshipbetweenmedianz-scoresofcoralcoverandcoralcalcificationcapacity(CCCkgCaCO3 mminus2 yminus1)forstudysiteswithineachfocalregionfor(a)mainHawaiianIslands(b)Morsquoorea(c)FloridaKeysand(d)StJohnUSVirginIslandsFittedlinesareModelIleast-squareslinearregressionsforpredictedcarbonateproductionr2valuesandsignificancelevelsfortherelationshipareshownforeachplot

(a) (b)

(c) (d)

10emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

group members also received support from the National ScienceFoundationTACKG EAL andAJAThis isHIMBcontribu-tionnumber1728andSOESTContributionnumber10363Wearegrateful to Michael Bode Alasdair Edwards and two anonymousreviewerswhosecommentsandsuggestionsgreatly improved themanuscriptAnyuseoftradenameshereinwasfordescriptivepur-posesonlyanddoesnotimplyendorsementbytheUSGovernmentNoneoftheco-authorshaveanyconflictofinteresttodeclare

AUTHORSrsquo CONTRIBUTIONS

AllauthorscontributedtotheconceptualisationofthisstudyJRGPJERDGandIBKwrotethemanuscriptREproducedthenu-mericalsimulationsTACandAJAproducedthecalculationsofcoral-communitycalcificationcapacityAllauthorsreadandeditedthefinaldraftofthemanuscript

DATA ACCE SSIBILIT Y

Data available via USGS data release httpsdoiorg105066f78w3c7w(Guestetal2018)

ORCID

James R Guest httporcidorg0000-0002-9714-9009

Ilsa B Kuffner httporcidorg0000-0001-8804-7847

Hollie M Putnam httporcidorg0000-0003-2322-3269

R E FE R E N C E S

AdamTBurkepileDRuttenbergBampPaddackM(2015)HerbivoryandtheresilienceofCaribbeancoralreefsKnowledgegapsandim-plicationsformanagementMarine Ecology Progress Series5201ndash20httpsdoiorg103354meps11170

BahrKDJokielPLampToonenRJ(2015)TheunnaturalhistoryofKānersquooheBayCoralreefresilienceinthefaceofcenturiesofanthro-pogenicimpactsPeerJ3e950httpsdoiorg107717peerj950

BerumenMIampPratchettMS(2006)RecoverywithoutresiliencePersistentdisturbancesandlong-termshiftsinthestructureoffishandcoralcommunitiesatTiahuraReefMooreaCoral Reefs25647ndash653httpsdoiorg101007s00338-006-0145-2

Brown B E amp Cossins A R (2011) The potential for temperatureacclimatisation of reef corals in the face of climate change In ZDubinskyampNStambler(Eds)Coral reefs An ecosystem in transition (pp 421ndash433) Dordrecht The Netherlands Springer httpsdoiorg101007978-94-007-0114-4

CinnerJEHucheryCMacNeilMAGrahamNAJMcClanahanT R Maina J hellip Mouillot D (2016) Bright spots among theworldrsquoscoral reefsNature535416ndash419httpsdoiorg101038nature18607

DavisJPavlovaAThompsonRampSunnucksP(2013)Evolutionaryrefugia and ecological refuges Key concepts for conservingAustralianarid zone freshwaterbiodiversityunder climatechangeGlobal Change Biology 19 1970ndash1984 httpsdoiorg101111gcb12203

DersquoathG FabriciusK E SweatmanHampPuotinenM (2012) The27-year decline of coral cover on the Great Barrier Reef and its

causes Proceedings of the National Academy of Sciences of the United States of America 109 17995ndash17999 httpsdoiorg101073pnas1208909109

Doney SC RuckelshausM EmmettDuffy J Barry J PChan FEnglishCAhellipTalleyLD(2012)Climatechangeimpactsonma-rineecosystemsAnnual Review of Marine Science411ndash37httpsdoiorg101146annurev-marine-041911-111611

EdmundsPJ(2002)Long-termdynamicsofcoralreefsinStJohnUSVirginIslandsCoral Reefs21357ndash367

GilmourJPSmithLDHeywardAJBairdAHampPratchettMS (2013) Recovery of an isolated coral reef system following se-vere disturbance Science 340 69ndash71 httpsdoiorg101126science1232310

GrahamNA JenningsSMacNeilMAMouillotDampWilsonSK (2015) Predicting climate-driven regime shifts versus reboundpotentialincoralreefsNature51894ndash97httpsdoiorg101038nature14140

Guest J R Edmunds P J Gates R D Kuffner I B Brown E KRodgersKShellipRogersCS (2018)Time-seriescoral-coverdatafromHawaiiFloridaMooreaandtheVirginIslandsUnitedStatesGeologicalSurveydatareleasehttpsdoiorg105066f78w3c7w

GuestJRTunKLowJVergeacutesAMarzinelliEMCampbellAHhellipSteinbergPD(2016)27yearsofbenthicandcoralcommunitydynamicsonturbidhighlyurbanisedreefsoffSingaporeScientific Reports636260httpsdoiorg101038srep36260

HaberlHErbKHKrausmannFGaubeVBondeauAPlutzarC hellipFischer-KowalskiM(2007)Quantifyingandmappingthehumanappropriation of net primary production in earthrsquos terrestrial eco-systems Proceedings of the National Academy of Sciences of United States of America 104 12942ndash12947 httpsdoiorg101073pnas0704243104

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDrsquoAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences of the United States of America1078650ndash8655httpsdoiorg101073pnas0912668107

Hilborn R (2007) Managing fisheries is managing people Whathas been learned Fish and Fisheries 8 285ndash296 httpsdoiorg101111j1467-2979200700263_2x

Hughes T P BarnesM L Bellwood D R Cinner J E CummingG S Jackson J B C hellip Scheffer M (2017) Coral reefs in theAnthropocene Nature 546 82ndash90 httpsdoiorg101038nature22901

Idjadi J A Lee S C Bruno J F PrechtW F Allen-Requa L ampEdmunds P J (2006) Rapid phase-shift reversal on a Jamaicancoral reef Coral Reefs 25 209ndash211 httpsdoiorg101007s00338-006-0088-7

JacksonJDonovanMCramerKampLamV(2014)Status and trends of Caribbean coral reefs 1970ndash2012IUCNSwitzerlandGlobalCoralReefMonitoringNetwork

Jokiel P L amp Brown E K (2004) Global warming regional trendsand inshore environmental conditions influence coral bleach-ing in Hawaii Global Change Biology 10 1627ndash1641 httpsdoiorg101111j1365-2486200400836x

KuffnerIBampTothLT(2016)Ageologicalperspectiveonthedegra-dationandconservationofwesternAtlanticcoralreefsConservation Biology30706ndash715httpsdoiorg101111cobi12725

LirmanD amp Schopmeyer S (2016) Ecological solutions to reef deg-radation Optimizing coral reef restoration in the Caribbeanand Western Atlantic PeerJ 4 e2597 httpsdoiorg107717 peerj2597

8emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

positivemedianz-scoreswhereasreboundandphase-shiftedoasesarelikelytoexhibithigherCVsandlowerpositivemedianz- scores Thisframeworkisimportantfromamanagementperspectiveasitpromptsconsiderationofstabilityresistanceorrecoveryofcoralcommunity structurewithin ahistorical contextwhenassigning ameasure of quality to individual siteswithin ecosystems (MumbyChollettBozecampWolff2014)

In this study potential escape oases include Molokini Crater(MauimainHawaiianIslands)andtheTektitesiteat14-mdepthinSt John asbothare relativelyprotected fromstormsandexperi-encerelativelylowlevelsofland-basedinfluences(Edmunds2002Rodgers etal 2015 RogersMcLain amp Tobias 1991) PotentiallyresistantoasesincludeseveralpatchreefsintheFloridaKeys(egWestWasherWomenWesternHeadJaapReef)as theyoccur inareas with high variability in turbidity and temperature that mayhavefavouredhighertolerancetoacutethermalanomalies(Lirmanetal2011Ruzickaetal2013)Potential reboundoases includeanouterfore-reefsiteinMorsquooreaat10-mdepth(LTER1Outer10m)

asthissitehad~47coralcoverin2005lt1in2010(duetopre-dationbyAcanthaster planciandCycloneOliin2010)but~54in2015Similarlyoneshallowsite(2-mdepth)onOʻahu(MokuoLoʻein Kāneʻohe Bay main Hawaiian Islands) increased in coral coverfrom16in2001to49in2012KāneʻoheBayhasalonghistoryofanthropogenicdisturbancesbutcoralcoverappears to recoverwhen localiseddisturbancesareeffectivelymanaged (Bahr JokielampToonen2015)Thehistoryofthissitesuggestsitpossessesprop-ertiesofbothresistantandreboundoasesPotentialphaseshiftedoasesincludeAdmiralintheFloridaKeysasthissitedeclinedfromrelativelyhightolowcoralcoverwithoutrecoveryfollowingararecold-watereventin2010(Lirmanetal2011)Consideringthatthissitemaintainedaveragecoralcoverge21foratleast15yearspriorto2010itseemslikelythattypicalenvironmentalconditionstheremaystillbesuitableforcoralgrowthandsurvivalIfsowesuggestthatAdmiralmaybeapotentiallystrongcandidatefortargetedcoralrestoration(egLirmanampSchopmeyer2016seeFigure4bforex-amplesofcoralcovertrajectories)

F IGURE 4emsp (a)Scatterplotdisplayingrelationshipsbetweenstandardizedcoralcover (median z-scores)andvariabilityincoralcover(coefficientofvariation)forstudysitesidentifiedasoaseswithineachfocalregionfor(redcircles)mainHawaiianIslands(bluesquares)Morsquoorea(greentriangles)FloridaKeysand(bluecrosses)StJohnUSVirginIslands(basedondatainFigure2)SeelegendforFigure1forinterpretation(b)Examplesofcoral-covertrajectoriesfromselectedoasissites(1)MokuoLoʻe2(2)LTER1Outer10(3)Admiral(4)WestWasherWomen(5)Tektite1and(6)Molokini13BlacklinesshowmeancoralcoverforthesiteandtheredlineisoverallmeancoralcoverfortheregionErrorbarsshowplusmnSESitelabelsindicatethepointinthescatterplotin(a)forreferenceLabelsaboveeachsiteindicatesuggestedcategorisationofeachoasistype(seeSection4forexplanation)

emspensp emsp | emsp9Journal of Applied EcologyGUEST ET al

Thereisampleevidencesupportingtheroleofphysicalandbi-ologicaldrivers indeterminingecosystemstateofcoralreefs (egGrahametal2015)NonethelessitispossiblethatsomeoasesexistbecausetheyhavebeensparedfromdisturbancebychancealoneThese ldquoluckyrdquooasesdiffer fromescapeoasesas theydonotpos-sessanyspecificphysicalcharacteristicsthatreducethelikelihoodofbeingdisturbedIfitisthecasethatecosystemstateonreefsisdeterminedmorebystochasticitythanbymechanisticdriversthenconservationplanningwillneedtoincludeaswidearangeofreefsaspossibletomitigateagainstthisuncertainty(Websteretal2017)

While coral cover is an excellent proxy for reef conditionchanges in coral cover alone cannot capture the full spectrum ofchangesthathavenegativelyaffectedcoralreefsinthelastfewde-cadesForexample shifts in taxonomic community structurealsooccurfollowingdisturbancesandthesemayresultinchangesinreeffunction(KuffnerampToth2016)Suchshiftsdescribedasldquorecoverywithoutresiliencerdquohavebeendocumentedonanumberofreefsinthe Indo-WestPacific (egBerumenampPratchett2006)Boththetotalcoverofcoralsandcommunitycompositionplayaroleinde-terminingCCCItisconceivablethereforethatasitedominatedbyslowgrowingtaxacouldexhibitlowCCCandviceversaasitewithlowercoveroffastgrowingtaxacouldexhibitrelativelyhighCCCItisencouragingthereforethatthegenerallyhigherCCCobservedforoasesinthisstudysuggestsagreaterpotentialtomaintainposi-tivenetcoralreef-carbonateproductionrelativetotheirneighboursIt isworthnotinghoweverthat lowratesofCCCforoasesinthetwoCaribbeanfocalregions(egmaxCCCStJohn19kgmminus2 yminus1FloridaKeys35kgmminus2 yminus1)suggestthatnetcarbonateproductionbudgets for these sites may be close to zero once the additional

factors such as bioerosion andCaCO3 dissolution are taken intoaccount(Perryetal2012)

Due to uncertainties about future environmental conditionsnon-oasissitesthathavehistoricallyperformedpoorlymayimproveandsomeoaseswilldeclineiftheypassatippingpoint(Hughesetal2017)We suggest therefore that our frameworkbeusedwithinadaptivenetworksof protected areas that also considerdiversityconnectivity metapopulation conservation and risk mitigation(Websteretal2017)Thereisconsiderableuncertaintyaboutreeffutures due to global change however combiningdetailed distur-bancehistorieswithourapproachcouldlessenthisuncertaintyThepresenceofoasesinsomelocationsdoesnotadvocatecomplacencyabouttheseverityofthecrisisfacingmostoftheworldrsquoscoralreefsOnlyconcertedactiontomanagehumandisturbancesatalocallevelandtacklecarbonemissionsgloballywillsecureafuturefortropicalreefsNonethelesswehope thatour studywill furtherefforts toidentifysimilarldquooasesrdquoinotherecosystems(egtropicalforests)andtoimproveourunderstandingofthemechanisticdriversunderlyingpersistenceofthesesitesinthefaceofglobalscaledegradation

ACKNOWLEDG EMENTS

The ideas presented in this paperwere generated by participantsof theUSGeological Survey (USGS) JohnWesley Powell Centerfor Analysis and Synthesis working group ldquoLocal-scale ecosystemresilienceamidglobal-scaleoceanchangethecoralreefexamplerdquoThisworkwasfundedbytheUSGSthroughtheJohnWesleyPowellCenter (award to PJE RDG and IBK) which supported twomeetingsandaPowellFellowship (award to JRG)The following

F IGURE 5emspScatterplotsshowingtherelationshipbetweenmedianz-scoresofcoralcoverandcoralcalcificationcapacity(CCCkgCaCO3 mminus2 yminus1)forstudysiteswithineachfocalregionfor(a)mainHawaiianIslands(b)Morsquoorea(c)FloridaKeysand(d)StJohnUSVirginIslandsFittedlinesareModelIleast-squareslinearregressionsforpredictedcarbonateproductionr2valuesandsignificancelevelsfortherelationshipareshownforeachplot

(a) (b)

(c) (d)

10emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

group members also received support from the National ScienceFoundationTACKG EAL andAJAThis isHIMBcontribu-tionnumber1728andSOESTContributionnumber10363Wearegrateful to Michael Bode Alasdair Edwards and two anonymousreviewerswhosecommentsandsuggestionsgreatly improved themanuscriptAnyuseoftradenameshereinwasfordescriptivepur-posesonlyanddoesnotimplyendorsementbytheUSGovernmentNoneoftheco-authorshaveanyconflictofinteresttodeclare

AUTHORSrsquo CONTRIBUTIONS

AllauthorscontributedtotheconceptualisationofthisstudyJRGPJERDGandIBKwrotethemanuscriptREproducedthenu-mericalsimulationsTACandAJAproducedthecalculationsofcoral-communitycalcificationcapacityAllauthorsreadandeditedthefinaldraftofthemanuscript

DATA ACCE SSIBILIT Y

Data available via USGS data release httpsdoiorg105066f78w3c7w(Guestetal2018)

ORCID

James R Guest httporcidorg0000-0002-9714-9009

Ilsa B Kuffner httporcidorg0000-0001-8804-7847

Hollie M Putnam httporcidorg0000-0003-2322-3269

R E FE R E N C E S

AdamTBurkepileDRuttenbergBampPaddackM(2015)HerbivoryandtheresilienceofCaribbeancoralreefsKnowledgegapsandim-plicationsformanagementMarine Ecology Progress Series5201ndash20httpsdoiorg103354meps11170

BahrKDJokielPLampToonenRJ(2015)TheunnaturalhistoryofKānersquooheBayCoralreefresilienceinthefaceofcenturiesofanthro-pogenicimpactsPeerJ3e950httpsdoiorg107717peerj950

BerumenMIampPratchettMS(2006)RecoverywithoutresiliencePersistentdisturbancesandlong-termshiftsinthestructureoffishandcoralcommunitiesatTiahuraReefMooreaCoral Reefs25647ndash653httpsdoiorg101007s00338-006-0145-2

Brown B E amp Cossins A R (2011) The potential for temperatureacclimatisation of reef corals in the face of climate change In ZDubinskyampNStambler(Eds)Coral reefs An ecosystem in transition (pp 421ndash433) Dordrecht The Netherlands Springer httpsdoiorg101007978-94-007-0114-4

CinnerJEHucheryCMacNeilMAGrahamNAJMcClanahanT R Maina J hellip Mouillot D (2016) Bright spots among theworldrsquoscoral reefsNature535416ndash419httpsdoiorg101038nature18607

DavisJPavlovaAThompsonRampSunnucksP(2013)Evolutionaryrefugia and ecological refuges Key concepts for conservingAustralianarid zone freshwaterbiodiversityunder climatechangeGlobal Change Biology 19 1970ndash1984 httpsdoiorg101111gcb12203

DersquoathG FabriciusK E SweatmanHampPuotinenM (2012) The27-year decline of coral cover on the Great Barrier Reef and its

causes Proceedings of the National Academy of Sciences of the United States of America 109 17995ndash17999 httpsdoiorg101073pnas1208909109

Doney SC RuckelshausM EmmettDuffy J Barry J PChan FEnglishCAhellipTalleyLD(2012)Climatechangeimpactsonma-rineecosystemsAnnual Review of Marine Science411ndash37httpsdoiorg101146annurev-marine-041911-111611

EdmundsPJ(2002)Long-termdynamicsofcoralreefsinStJohnUSVirginIslandsCoral Reefs21357ndash367

GilmourJPSmithLDHeywardAJBairdAHampPratchettMS (2013) Recovery of an isolated coral reef system following se-vere disturbance Science 340 69ndash71 httpsdoiorg101126science1232310

GrahamNA JenningsSMacNeilMAMouillotDampWilsonSK (2015) Predicting climate-driven regime shifts versus reboundpotentialincoralreefsNature51894ndash97httpsdoiorg101038nature14140

Guest J R Edmunds P J Gates R D Kuffner I B Brown E KRodgersKShellipRogersCS (2018)Time-seriescoral-coverdatafromHawaiiFloridaMooreaandtheVirginIslandsUnitedStatesGeologicalSurveydatareleasehttpsdoiorg105066f78w3c7w

GuestJRTunKLowJVergeacutesAMarzinelliEMCampbellAHhellipSteinbergPD(2016)27yearsofbenthicandcoralcommunitydynamicsonturbidhighlyurbanisedreefsoffSingaporeScientific Reports636260httpsdoiorg101038srep36260

HaberlHErbKHKrausmannFGaubeVBondeauAPlutzarC hellipFischer-KowalskiM(2007)Quantifyingandmappingthehumanappropriation of net primary production in earthrsquos terrestrial eco-systems Proceedings of the National Academy of Sciences of United States of America 104 12942ndash12947 httpsdoiorg101073pnas0704243104

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDrsquoAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences of the United States of America1078650ndash8655httpsdoiorg101073pnas0912668107

Hilborn R (2007) Managing fisheries is managing people Whathas been learned Fish and Fisheries 8 285ndash296 httpsdoiorg101111j1467-2979200700263_2x

Hughes T P BarnesM L Bellwood D R Cinner J E CummingG S Jackson J B C hellip Scheffer M (2017) Coral reefs in theAnthropocene Nature 546 82ndash90 httpsdoiorg101038nature22901

Idjadi J A Lee S C Bruno J F PrechtW F Allen-Requa L ampEdmunds P J (2006) Rapid phase-shift reversal on a Jamaicancoral reef Coral Reefs 25 209ndash211 httpsdoiorg101007s00338-006-0088-7

JacksonJDonovanMCramerKampLamV(2014)Status and trends of Caribbean coral reefs 1970ndash2012IUCNSwitzerlandGlobalCoralReefMonitoringNetwork

Jokiel P L amp Brown E K (2004) Global warming regional trendsand inshore environmental conditions influence coral bleach-ing in Hawaii Global Change Biology 10 1627ndash1641 httpsdoiorg101111j1365-2486200400836x

KuffnerIBampTothLT(2016)Ageologicalperspectiveonthedegra-dationandconservationofwesternAtlanticcoralreefsConservation Biology30706ndash715httpsdoiorg101111cobi12725

LirmanD amp Schopmeyer S (2016) Ecological solutions to reef deg-radation Optimizing coral reef restoration in the Caribbeanand Western Atlantic PeerJ 4 e2597 httpsdoiorg107717 peerj2597

emspensp emsp | emsp9Journal of Applied EcologyGUEST ET al

Thereisampleevidencesupportingtheroleofphysicalandbi-ologicaldrivers indeterminingecosystemstateofcoralreefs (egGrahametal2015)NonethelessitispossiblethatsomeoasesexistbecausetheyhavebeensparedfromdisturbancebychancealoneThese ldquoluckyrdquooasesdiffer fromescapeoasesas theydonotpos-sessanyspecificphysicalcharacteristicsthatreducethelikelihoodofbeingdisturbedIfitisthecasethatecosystemstateonreefsisdeterminedmorebystochasticitythanbymechanisticdriversthenconservationplanningwillneedtoincludeaswidearangeofreefsaspossibletomitigateagainstthisuncertainty(Websteretal2017)

While coral cover is an excellent proxy for reef conditionchanges in coral cover alone cannot capture the full spectrum ofchangesthathavenegativelyaffectedcoralreefsinthelastfewde-cadesForexample shifts in taxonomic community structurealsooccurfollowingdisturbancesandthesemayresultinchangesinreeffunction(KuffnerampToth2016)Suchshiftsdescribedasldquorecoverywithoutresiliencerdquohavebeendocumentedonanumberofreefsinthe Indo-WestPacific (egBerumenampPratchett2006)Boththetotalcoverofcoralsandcommunitycompositionplayaroleinde-terminingCCCItisconceivablethereforethatasitedominatedbyslowgrowingtaxacouldexhibitlowCCCandviceversaasitewithlowercoveroffastgrowingtaxacouldexhibitrelativelyhighCCCItisencouragingthereforethatthegenerallyhigherCCCobservedforoasesinthisstudysuggestsagreaterpotentialtomaintainposi-tivenetcoralreef-carbonateproductionrelativetotheirneighboursIt isworthnotinghoweverthat lowratesofCCCforoasesinthetwoCaribbeanfocalregions(egmaxCCCStJohn19kgmminus2 yminus1FloridaKeys35kgmminus2 yminus1)suggestthatnetcarbonateproductionbudgets for these sites may be close to zero once the additional

factors such as bioerosion andCaCO3 dissolution are taken intoaccount(Perryetal2012)

Due to uncertainties about future environmental conditionsnon-oasissitesthathavehistoricallyperformedpoorlymayimproveandsomeoaseswilldeclineiftheypassatippingpoint(Hughesetal2017)We suggest therefore that our frameworkbeusedwithinadaptivenetworksof protected areas that also considerdiversityconnectivity metapopulation conservation and risk mitigation(Websteretal2017)Thereisconsiderableuncertaintyaboutreeffutures due to global change however combiningdetailed distur-bancehistorieswithourapproachcouldlessenthisuncertaintyThepresenceofoasesinsomelocationsdoesnotadvocatecomplacencyabouttheseverityofthecrisisfacingmostoftheworldrsquoscoralreefsOnlyconcertedactiontomanagehumandisturbancesatalocallevelandtacklecarbonemissionsgloballywillsecureafuturefortropicalreefsNonethelesswehope thatour studywill furtherefforts toidentifysimilarldquooasesrdquoinotherecosystems(egtropicalforests)andtoimproveourunderstandingofthemechanisticdriversunderlyingpersistenceofthesesitesinthefaceofglobalscaledegradation

ACKNOWLEDG EMENTS

The ideas presented in this paperwere generated by participantsof theUSGeological Survey (USGS) JohnWesley Powell Centerfor Analysis and Synthesis working group ldquoLocal-scale ecosystemresilienceamidglobal-scaleoceanchangethecoralreefexamplerdquoThisworkwasfundedbytheUSGSthroughtheJohnWesleyPowellCenter (award to PJE RDG and IBK) which supported twomeetingsandaPowellFellowship (award to JRG)The following

F IGURE 5emspScatterplotsshowingtherelationshipbetweenmedianz-scoresofcoralcoverandcoralcalcificationcapacity(CCCkgCaCO3 mminus2 yminus1)forstudysiteswithineachfocalregionfor(a)mainHawaiianIslands(b)Morsquoorea(c)FloridaKeysand(d)StJohnUSVirginIslandsFittedlinesareModelIleast-squareslinearregressionsforpredictedcarbonateproductionr2valuesandsignificancelevelsfortherelationshipareshownforeachplot

(a) (b)

(c) (d)

10emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

group members also received support from the National ScienceFoundationTACKG EAL andAJAThis isHIMBcontribu-tionnumber1728andSOESTContributionnumber10363Wearegrateful to Michael Bode Alasdair Edwards and two anonymousreviewerswhosecommentsandsuggestionsgreatly improved themanuscriptAnyuseoftradenameshereinwasfordescriptivepur-posesonlyanddoesnotimplyendorsementbytheUSGovernmentNoneoftheco-authorshaveanyconflictofinteresttodeclare

AUTHORSrsquo CONTRIBUTIONS

AllauthorscontributedtotheconceptualisationofthisstudyJRGPJERDGandIBKwrotethemanuscriptREproducedthenu-mericalsimulationsTACandAJAproducedthecalculationsofcoral-communitycalcificationcapacityAllauthorsreadandeditedthefinaldraftofthemanuscript

DATA ACCE SSIBILIT Y

Data available via USGS data release httpsdoiorg105066f78w3c7w(Guestetal2018)

ORCID

James R Guest httporcidorg0000-0002-9714-9009

Ilsa B Kuffner httporcidorg0000-0001-8804-7847

Hollie M Putnam httporcidorg0000-0003-2322-3269

R E FE R E N C E S

AdamTBurkepileDRuttenbergBampPaddackM(2015)HerbivoryandtheresilienceofCaribbeancoralreefsKnowledgegapsandim-plicationsformanagementMarine Ecology Progress Series5201ndash20httpsdoiorg103354meps11170

BahrKDJokielPLampToonenRJ(2015)TheunnaturalhistoryofKānersquooheBayCoralreefresilienceinthefaceofcenturiesofanthro-pogenicimpactsPeerJ3e950httpsdoiorg107717peerj950

BerumenMIampPratchettMS(2006)RecoverywithoutresiliencePersistentdisturbancesandlong-termshiftsinthestructureoffishandcoralcommunitiesatTiahuraReefMooreaCoral Reefs25647ndash653httpsdoiorg101007s00338-006-0145-2

Brown B E amp Cossins A R (2011) The potential for temperatureacclimatisation of reef corals in the face of climate change In ZDubinskyampNStambler(Eds)Coral reefs An ecosystem in transition (pp 421ndash433) Dordrecht The Netherlands Springer httpsdoiorg101007978-94-007-0114-4

CinnerJEHucheryCMacNeilMAGrahamNAJMcClanahanT R Maina J hellip Mouillot D (2016) Bright spots among theworldrsquoscoral reefsNature535416ndash419httpsdoiorg101038nature18607

DavisJPavlovaAThompsonRampSunnucksP(2013)Evolutionaryrefugia and ecological refuges Key concepts for conservingAustralianarid zone freshwaterbiodiversityunder climatechangeGlobal Change Biology 19 1970ndash1984 httpsdoiorg101111gcb12203

DersquoathG FabriciusK E SweatmanHampPuotinenM (2012) The27-year decline of coral cover on the Great Barrier Reef and its

causes Proceedings of the National Academy of Sciences of the United States of America 109 17995ndash17999 httpsdoiorg101073pnas1208909109

Doney SC RuckelshausM EmmettDuffy J Barry J PChan FEnglishCAhellipTalleyLD(2012)Climatechangeimpactsonma-rineecosystemsAnnual Review of Marine Science411ndash37httpsdoiorg101146annurev-marine-041911-111611

EdmundsPJ(2002)Long-termdynamicsofcoralreefsinStJohnUSVirginIslandsCoral Reefs21357ndash367

GilmourJPSmithLDHeywardAJBairdAHampPratchettMS (2013) Recovery of an isolated coral reef system following se-vere disturbance Science 340 69ndash71 httpsdoiorg101126science1232310

GrahamNA JenningsSMacNeilMAMouillotDampWilsonSK (2015) Predicting climate-driven regime shifts versus reboundpotentialincoralreefsNature51894ndash97httpsdoiorg101038nature14140

Guest J R Edmunds P J Gates R D Kuffner I B Brown E KRodgersKShellipRogersCS (2018)Time-seriescoral-coverdatafromHawaiiFloridaMooreaandtheVirginIslandsUnitedStatesGeologicalSurveydatareleasehttpsdoiorg105066f78w3c7w

GuestJRTunKLowJVergeacutesAMarzinelliEMCampbellAHhellipSteinbergPD(2016)27yearsofbenthicandcoralcommunitydynamicsonturbidhighlyurbanisedreefsoffSingaporeScientific Reports636260httpsdoiorg101038srep36260

HaberlHErbKHKrausmannFGaubeVBondeauAPlutzarC hellipFischer-KowalskiM(2007)Quantifyingandmappingthehumanappropriation of net primary production in earthrsquos terrestrial eco-systems Proceedings of the National Academy of Sciences of United States of America 104 12942ndash12947 httpsdoiorg101073pnas0704243104

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDrsquoAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences of the United States of America1078650ndash8655httpsdoiorg101073pnas0912668107

Hilborn R (2007) Managing fisheries is managing people Whathas been learned Fish and Fisheries 8 285ndash296 httpsdoiorg101111j1467-2979200700263_2x

Hughes T P BarnesM L Bellwood D R Cinner J E CummingG S Jackson J B C hellip Scheffer M (2017) Coral reefs in theAnthropocene Nature 546 82ndash90 httpsdoiorg101038nature22901

Idjadi J A Lee S C Bruno J F PrechtW F Allen-Requa L ampEdmunds P J (2006) Rapid phase-shift reversal on a Jamaicancoral reef Coral Reefs 25 209ndash211 httpsdoiorg101007s00338-006-0088-7

JacksonJDonovanMCramerKampLamV(2014)Status and trends of Caribbean coral reefs 1970ndash2012IUCNSwitzerlandGlobalCoralReefMonitoringNetwork

Jokiel P L amp Brown E K (2004) Global warming regional trendsand inshore environmental conditions influence coral bleach-ing in Hawaii Global Change Biology 10 1627ndash1641 httpsdoiorg101111j1365-2486200400836x

KuffnerIBampTothLT(2016)Ageologicalperspectiveonthedegra-dationandconservationofwesternAtlanticcoralreefsConservation Biology30706ndash715httpsdoiorg101111cobi12725

LirmanD amp Schopmeyer S (2016) Ecological solutions to reef deg-radation Optimizing coral reef restoration in the Caribbeanand Western Atlantic PeerJ 4 e2597 httpsdoiorg107717 peerj2597

10emsp |emsp emspenspJournal of Applied Ecology GUEST ET al

group members also received support from the National ScienceFoundationTACKG EAL andAJAThis isHIMBcontribu-tionnumber1728andSOESTContributionnumber10363Wearegrateful to Michael Bode Alasdair Edwards and two anonymousreviewerswhosecommentsandsuggestionsgreatly improved themanuscriptAnyuseoftradenameshereinwasfordescriptivepur-posesonlyanddoesnotimplyendorsementbytheUSGovernmentNoneoftheco-authorshaveanyconflictofinteresttodeclare

AUTHORSrsquo CONTRIBUTIONS

AllauthorscontributedtotheconceptualisationofthisstudyJRGPJERDGandIBKwrotethemanuscriptREproducedthenu-mericalsimulationsTACandAJAproducedthecalculationsofcoral-communitycalcificationcapacityAllauthorsreadandeditedthefinaldraftofthemanuscript

DATA ACCE SSIBILIT Y

Data available via USGS data release httpsdoiorg105066f78w3c7w(Guestetal2018)

ORCID

James R Guest httporcidorg0000-0002-9714-9009

Ilsa B Kuffner httporcidorg0000-0001-8804-7847

Hollie M Putnam httporcidorg0000-0003-2322-3269

R E FE R E N C E S

AdamTBurkepileDRuttenbergBampPaddackM(2015)HerbivoryandtheresilienceofCaribbeancoralreefsKnowledgegapsandim-plicationsformanagementMarine Ecology Progress Series5201ndash20httpsdoiorg103354meps11170

BahrKDJokielPLampToonenRJ(2015)TheunnaturalhistoryofKānersquooheBayCoralreefresilienceinthefaceofcenturiesofanthro-pogenicimpactsPeerJ3e950httpsdoiorg107717peerj950

BerumenMIampPratchettMS(2006)RecoverywithoutresiliencePersistentdisturbancesandlong-termshiftsinthestructureoffishandcoralcommunitiesatTiahuraReefMooreaCoral Reefs25647ndash653httpsdoiorg101007s00338-006-0145-2

Brown B E amp Cossins A R (2011) The potential for temperatureacclimatisation of reef corals in the face of climate change In ZDubinskyampNStambler(Eds)Coral reefs An ecosystem in transition (pp 421ndash433) Dordrecht The Netherlands Springer httpsdoiorg101007978-94-007-0114-4

CinnerJEHucheryCMacNeilMAGrahamNAJMcClanahanT R Maina J hellip Mouillot D (2016) Bright spots among theworldrsquoscoral reefsNature535416ndash419httpsdoiorg101038nature18607

DavisJPavlovaAThompsonRampSunnucksP(2013)Evolutionaryrefugia and ecological refuges Key concepts for conservingAustralianarid zone freshwaterbiodiversityunder climatechangeGlobal Change Biology 19 1970ndash1984 httpsdoiorg101111gcb12203

DersquoathG FabriciusK E SweatmanHampPuotinenM (2012) The27-year decline of coral cover on the Great Barrier Reef and its

causes Proceedings of the National Academy of Sciences of the United States of America 109 17995ndash17999 httpsdoiorg101073pnas1208909109

Doney SC RuckelshausM EmmettDuffy J Barry J PChan FEnglishCAhellipTalleyLD(2012)Climatechangeimpactsonma-rineecosystemsAnnual Review of Marine Science411ndash37httpsdoiorg101146annurev-marine-041911-111611

EdmundsPJ(2002)Long-termdynamicsofcoralreefsinStJohnUSVirginIslandsCoral Reefs21357ndash367

GilmourJPSmithLDHeywardAJBairdAHampPratchettMS (2013) Recovery of an isolated coral reef system following se-vere disturbance Science 340 69ndash71 httpsdoiorg101126science1232310

GrahamNA JenningsSMacNeilMAMouillotDampWilsonSK (2015) Predicting climate-driven regime shifts versus reboundpotentialincoralreefsNature51894ndash97httpsdoiorg101038nature14140

Guest J R Edmunds P J Gates R D Kuffner I B Brown E KRodgersKShellipRogersCS (2018)Time-seriescoral-coverdatafromHawaiiFloridaMooreaandtheVirginIslandsUnitedStatesGeologicalSurveydatareleasehttpsdoiorg105066f78w3c7w

GuestJRTunKLowJVergeacutesAMarzinelliEMCampbellAHhellipSteinbergPD(2016)27yearsofbenthicandcoralcommunitydynamicsonturbidhighlyurbanisedreefsoffSingaporeScientific Reports636260httpsdoiorg101038srep36260

HaberlHErbKHKrausmannFGaubeVBondeauAPlutzarC hellipFischer-KowalskiM(2007)Quantifyingandmappingthehumanappropriation of net primary production in earthrsquos terrestrial eco-systems Proceedings of the National Academy of Sciences of United States of America 104 12942ndash12947 httpsdoiorg101073pnas0704243104

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDrsquoAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences of the United States of America1078650ndash8655httpsdoiorg101073pnas0912668107

Hilborn R (2007) Managing fisheries is managing people Whathas been learned Fish and Fisheries 8 285ndash296 httpsdoiorg101111j1467-2979200700263_2x

Hughes T P BarnesM L Bellwood D R Cinner J E CummingG S Jackson J B C hellip Scheffer M (2017) Coral reefs in theAnthropocene Nature 546 82ndash90 httpsdoiorg101038nature22901

Idjadi J A Lee S C Bruno J F PrechtW F Allen-Requa L ampEdmunds P J (2006) Rapid phase-shift reversal on a Jamaicancoral reef Coral Reefs 25 209ndash211 httpsdoiorg101007s00338-006-0088-7

JacksonJDonovanMCramerKampLamV(2014)Status and trends of Caribbean coral reefs 1970ndash2012IUCNSwitzerlandGlobalCoralReefMonitoringNetwork

Jokiel P L amp Brown E K (2004) Global warming regional trendsand inshore environmental conditions influence coral bleach-ing in Hawaii Global Change Biology 10 1627ndash1641 httpsdoiorg101111j1365-2486200400836x

KuffnerIBampTothLT(2016)Ageologicalperspectiveonthedegra-dationandconservationofwesternAtlanticcoralreefsConservation Biology30706ndash715httpsdoiorg101111cobi12725

LirmanD amp Schopmeyer S (2016) Ecological solutions to reef deg-radation Optimizing coral reef restoration in the Caribbeanand Western Atlantic PeerJ 4 e2597 httpsdoiorg107717 peerj2597

emspensp emsp | emsp11Journal of Applied EcologyGUEST ET al

Lirman D Schopmeyer SManzello D Gramer L J PrechtW FMuller-Karger FRhellipThanner S (2011) Severe2010cold-watereventcausedunprecedentedmortalitytocoralsoftheFloridareeftract and reversed previous survivorship patterns PLoS ONE 6e23047httpsdoiorg101371journalpone0023047

Morgan K M amp Kench P S (2012) Skeletal extension and calcifi-cation of reef-building corals in the central Indian OceanMarine Environmental Research8178ndash82httpsdoiorg101016jmarenv res201208001

MumbyPJChollettIBozecY-MampWolffNH(2014)Ecologicalresilience robustness and vulnerability How do these con-cepts benefit ecosystem management 2014 Current Opinion in Environmental Sustainability 7 22ndash27 httpsdoiorg101016 jcosust201311021

OrsquoLeary J KMicheli F Airoldi L Boch C de LeoG Elahi RhellipWongJ(2017)Theresilienceofmarineecosystemstoclimaticdis-turbancesBioScience67208ndash220httpsdoiorg101093bioscibiw161

PerryCTEdingerENKenchPSMurphyGNSmithersSGSteneckRSampMumbyPJ(2012)EstimatingratesofbiologicallydrivencoralreefframeworkproductionanderosionAnewcensus-basedcarbonatebudgetmethodologyandapplicationstothereefsof Bonaire Coral Reefs 31 853ndash868 httpsdoiorg101007s00338-012-0901-4

PerryCT SteneckRSMurphyGNKenchPS EdingerENSmithersSGampMumbyPJ(2015)Regional-scaledominanceofnon-frameworkbuildingcoralsonCaribbeanreefsaffectscarbonateproductionandfuturereefgrowthGlobal Change Biology211153ndash1164httpsdoiorg101111gcb12792

RichardsDRampFriessDA(2016)Ratesanddriversofmangrovede-forestationinSoutheastAsia2000-2012Proceedings of the National Academy of Sciences of the United States of America113 344ndash349httpsdoiorg101073pnas1510272113

RieglBampPillerWE(2003)Possiblerefugiaforreefsintimesofenvi-ronmentalstressInternational Journal of Earth Sciences92520ndash531httpsdoiorg101007s00531-003-0328-9

RodgersKSJokielPLBrownEKHauSampSparksR(2015)Overa decade of change in spatial and temporal dynamics ofHawaiiancoral reef communities 1 Pacific Science 69 1ndash13 httpsdoiorg1029846911

RoffGBejaranoSBozecY-MNuguesMSteneckRSampMumbyP J (2014)Porites and thePhoenix effectUnprecedented recov-ery after a mass coral bleaching event at Rangiroa Atoll FrenchPolynesiaMarine Biology1611385ndash1393httpsdoiorg101007s00227-014-2426-6

RogersCSMcLainLNampTobiasCR(1991)EffectsofHurricaneHugo(1989)onacoralreefinStJohnUSVIMarine Ecology Progress Series78189ndash199httpsdoiorg103354meps078189

RuzickaRColellaMPorterJMorrisonJKidneyJBrinkhuisVM hellip Colee J (2013) Temporal changes in benthic assemblages onFlorida Keys reefs 11 years after the 19971998 El NintildeoMarine Ecology Progress Series 489 125ndash141 httpsdoiorg103354meps10427

SterninM Sternin J ampMarsh D L (1997) Rapid sustained child-hoodmalnutritionalleviationthroughapositive-devianceapproachin ruralVietnamPreliminary findingsPages49ndash60 inWollinkaEKeeley B Burkhalter BR Bashir N eds The Hearth NutritionModelApplications inHaitiVietnamandBangladeshAgencyforInternational Development and World Relief Corporation by theBasicSupportforInstitutionalizingChildSurvival(BASICS)Project

TurnerIMampCorlettTR(1996)TheconservationvalueofsmallisolatedfragmentsoflowlandtropicalrainforestTrends in Ecology amp Evolution11330ndash333httpsdoiorg1010160169-5347(96)10046-X

WangYampChenH-J(2012)Useofpercentilesandz-scoresinanthro-pometryInVRPreedy(Ed)Handbook of anthropometry(pp29ndash48)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-1788-1

WaycottMDuarteCMCarruthersT JBOrthR JDennisonWCOlyarnikShellipWilliamsSL(2009)Acceleratinglossofsea-grassesacrosstheglobethreatenscoastalecosystemsProceedings of the National Academy of Sciences of the United States of America10612377ndash12381httpsdoiorg101073pnas0905620106

WebsterMSMadhaviACDarlingESArmstrongJPinskyMLKnowltonNampSchindlerDE(2017)Whoshouldpickthewin-nersofclimatechangeTrends in Ecology and Evolution32167ndash173httpsdoiorg101016jtree201612007

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGuestJREdmundsPJGatesRDetalAframeworkforidentifyingandcharacterisingcoralreefldquooasesrdquoagainstabackdropofdegradationJ Appl Ecol 2018001ndash11 httpsdoiorg1011111365-266413179