predictable ecological response to rising co2 of a community of...

Ecology and Evolution 20181ndash11 emsp|emsp1wwwecolevolorg

Received2February2018emsp |emsp Accepted9February2018DOI101002ece33971

O R I G I N A L R E S E A R C H

Predictable ecological response to rising CO2 of a community of marine phytoplankton

Jacob Pardew emsp|emspMacarena Blanco Pimentel emsp|emspEtienne Low-Decarie

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

UniversityofEssexColchesterUK

CorrespondenceEtienneLow-DeacutecarieDepartmentofBiologicalSciencesUniversityofEssexColchesterUKEmailelowdeessexacuk

Funding information Thestudywassupportedbystart-upfundsfromtheUniversityofEssextoEtienneLow-Deacutecarie

AbstractRisingatmosphericCO2andoceanacidificationarefundamentallyalteringconditionsforlifeofallmarineorganismsincludingphytoplanktonDifferencesinCO2relatedphysiologybetweenmajorphytoplanktontaxaleadtodifferencesintheirabilitytotakeupandutilizeCO2Thesedifferencesmaycausepredictableshiftsinthecompo-sitionofmarinephytoplanktoncommunitiesinresponsetorisingatmosphericCO2 Wereportanexperimentinwhichsevenspeciesofmarinephytoplanktonbelongingto fourmajor taxonomicgroups (cyanobacteria chlorophytesdiatomsandcocco-lithophores)weregrownatbothambient (500μatm)and future (1000μatm)CO2 levelsThesephytoplanktonweregrownasindividualspeciesasculturesofpairsofspeciesandasacommunityassemblageofallsevenspeciesintwocultureregimes(high-nitrogenbatchculturesandlower-nitrogensemicontinuousculturesalthoughnotundernitrogenlimitation)AllphytoplanktonspeciestestedinthisstudyincreasedtheirgrowthratesunderelevatedCO2 independentofthecultureregimeWealsofindthatdespitespecies-specificvariationingrowthresponsetohighCO2theiden-tityofmajortaxonomicgroupsprovidesagoodpredictionofchangesinpopulationgrowthandcompetitiveabilityunderhighCO2TheCO2-inducedgrowthresponseisagoodpredictorofCO2-inducedchanges incompetition (R

2gt93)andcommunitycomposition(R2gt73)ThisstudysuggeststhatitmaybepossibletoinferhowmarinephytoplanktoncommunitiesrespondtorisingCO2levelsfromtheknowledgeofthephysiologyofmajortaxonomicgroupsbutthatthesepredictionsmayrequirefurthercharacterizationofthesetraitsacrossadiversityofgrowthconditionsThesefindingsmustbevalidatedinthecontextoflimitationbyothernutrientsAlsoinnaturalcom-munitiesofphytoplanktonnumerousotherfactorsthatmayallrespondtochangesinCO2includingnitrogenfixationgrazingandvariationinthelimitingresourcewilllikelycomplicatethisprediction

K E Y W O R D S

competitioncoefficientglobalchangeprimaryproducerstaxonomicgroup

2emsp |emsp emspensp PARDEW Et Al

1emsp |emspINTRODUC TION

AtmosphericCO2concentrationsrecentlyexceededahistorichighof400partspermillion(μatm)alevelwhichhasnotbeensurpassedinatleastthepast420000years(GriggsampNoguer2002)Thisin-creaseinatmosphericCO2hasledtoadecreaseintheoceanpHof01unitssincetheonsetoftheIndustrialRevolution(IPCC2014)TheconcentrationofCO2intheatmosphereisexpectedtocontinuetoincreaseataratewhichistentimesfasterthanhasbeenrecordedinthepast55millionyears(Almeacutenetal2016)PredictionssuggestthatbytheendofthiscenturyatmosphericCO2 levelsmayreachbetween700and1000μatmandoceanpHwilldecreaseto~78ndash77(Breweretal2014)ThesechangesinatmosphericCO2 concen-trationandinoceanpHcombinetoincreasetheavailabilityofCO2 formarineprimaryproducershampertheabilityoforganismstocal-cifyandaffectthegrowthratesofmarinephytoplankton(KroekerKordasCrimampSingh2010Reinfelder2011)

Majorphytoplanktontaxonomicgroupsdiffer in theefficiencyof their RuBisCO (Ribulose-15-bisphosphate carboxylaseoxygen-ase)activityandoftheircarbonconcentrationmechanisms(CCMs)and thus in their expected response to the rise inCO2 and ocean acidification(Reinfelder2011Tortell2000)Thosephytoplanktonthataremoreefficientattakingupandutilizingcarbon(highersur-facearea tovolume ratiohigherCCMefficiencyhigherRuBisCOspecificityandorlowercarbonrequirements)arehypothesizedtobenefit less from the increase inCO2 as their growth is currentlyleastCO2-limited(Reinfelder2011)CyanobacteriapossessahighlyspecializedCCMinvolvingcarboxysomestodealwithlowdissolvedCO2 levelsandaRuBisCOwithCO2specificitycomparabletothatof chlorophytes (Price Badger Woodger amp Long 2008 Tortell2000)CyanobacteriaarecapableofincreasingtheconcentrationofCO2atthesiteofphotosynthesisover1000timesthelevelsofitssurroundingenvironment(BadgerampPrice2003)whichisanorderofmagnitudehighercarbonconcentrationefficiencythanthenextmostefficientmajortaxonomicgroups(Tortelletal2008)Althoughcyanobacteriaarecapableofincreasingtheirgrowthrateunderel-evatedCO2[egtwospeciestestinFuWarnerZhangFengandHutchins (2007)] themagnitudeof this increase ingrowth isgen-erallyconsideredtobesmallandthuscyanobacteriawouldbeex-pectedtodecreaseincompetitiveabilityunderelevatedCO2 all else being equal However nitrogen-fixing cyanobacteria (diazotrophiccyanobacteria) are found to increase nitrogen fixation under el-evatedCO2andhaveagreater increase ingrowthratethanothergroupsofphytoplankton(Dutkiewiczetal2015)Diazotrophiccya-nobacterialikelydifferfromothercyanobacteriaintheircarbonup-takeandutilizationhoweverpartoftheirlargerresponseandthuspartofthisdifferencebetweendiazotrophsandnonnitrogen-fixingcyanobacteriamaybeattributedtocultureconditionsinwhichni-trogen is completely omittedwhen culturing dizaotrophes for themeasurementofnitrogenfixationbutothernutrientsaresuppliedinabundance(egHutchinsFuWebbWalworthampTagliabue2013)Similarlytoexpectationsforcyanobacteriathatdonotfixnitrogensomediatomshavebeenshowntoexhibitalimitationresponseonly

at CO2 concentrations below present-day levels suggesting thattheyalsohaveahighlyefficientCCM(HopkinsonDupontAllenampMorel2011)howeverotherdiatomsdoappeartohavealargein-creaseingrowthunderfutureCO2conditions(egWuetal2010)ChlorophytesandcoccolithophoreshavealowerRuBisCOspecific-itythandiatomsandlowerCCMefficiencythandinoflagellatesandcyanobacteria but comparable efficiency to thatof diatoms (Priceetal2008Tortell2000)ChlorophytesandcoccolithophoresarethereforeexpectedtobemostlimitedbymoderndayCO2 availabil-ityandwouldthusbeexpectedtobenefitmostfromthe increaseinCO2 and increase in relative abundanceHowever the benefitsof higherCO2 for thephotosynthesis of coccolithophoresmaybeoffsetbyitseffectoncalcificationCalcificationismadecostlierbythedecrease inpHassociatedwith risingatmosphericCO2 levels Calcification incoccolithophores isgenerallyhamperedby theex-tentofacidificationexpectedinthiscenturybuttheeffectsappearto be species-specific (Meyer amp Riebesell 2015) so that it is notclearthatcoccolithophoreswillhaveaconsistentchangeingrowthandabundanceunderelevatedCO2Althoughtherearesubstantivevariationanduncertaintywithinmajortaxonomicgroupsforthesetraits given themajor taxa or species-specific differences in car-bonuptakeandutilizationand thedifferencesbetweencalcifyingand noncalcifying phytoplankton species in response to acidifica-tionitmaybepossibletopredictsomeoftheshiftsincommunityassemblages under increasing CO2 with an expected decrease innondiazotrophiccyanobacteriaanincreaseinchlorophytesandanintermediateresponseofdiatoms

Amodelparametrizedusingameta-analysisofgrowthresponseto increasedCO2 and assuming that this growth responsewill di-rectlytranslateintoproportionalchangesincommunitycompositionhas led to the expectation thatmajor changes in the compositionofcommunitiesshouldbeexpectedwithrisingCO2andthatthesechangeswillexceedthosecausedbywarmingorchangesinnutrientavailability (Dutkiewicz etal 2015) The assumption that growthresponsewill directly translate into proportional changes in com-munitycompositionremainstobetestedDespitetheseimportantdifferences in CO2-related physiology between major taxonomicgroups few studies have focused on how these differences willtranslate into changes in competition between groups and ulti-matelyhowtheyaltercommunitycompositionwithincreasingCO2

Studies of natural assemblages of marine phytoplankton havefoundthathighCO2resultedinanincreaseintheabundanceofthecyanobacterium Synechococcus and a decrease in the abundanceof the coccolithophore Emiliania huxleyi (Paulino Egge amp Larsen2007) Similar experiments also found a decrease in fucoxanthin-containingphytoplanktonincludingdiatoms(Yoshimuraetal2009)or that community composition remains unchanged (Bermuacutedezetal2016)WithintaxonomicgroupsanincreaseinCO2benefitslarger over smaller diatoms (Tortell etal 2008) as expected fromfacilitationofCO2diffusionwith largersurfaceareatovolumera-tiosChangesincompositionofmarinephytoplanktoncommunitiesassociatedwithchangesinCO2concentrationcouldpotentiallybepredictedfrompublishedinformationontheCO2-relatedphysiology

emspensp emsp | emsp3PARDEW Et Al

associatedwithmajortaxonomicgroups(includingCCMefficiencyandRuBisCOspecificity)orthemeasurementofgrowthresponsetoCO2ofthephytoplanktonspeciespresentinthenaturalassemblagebutthishasnotbeentestedAlthoughthishasnotbeenexplicitlytested other physico-chemical conditionsmay alter the responsetoelevatedCO2NotablytheavailabilityofnutrientscanaffectpHthustheavailabilityofCO2andgrowthrateorpeakbiomassthusthedrawdownandcompetitionforCO2

Infreshwaterphytoplanktonithasbeendemonstratedthatdif-ferences in thecapacity touptakeandutilizeCO2 betweenmajorphytoplankton taxa can lead to predictable changes in their com-petitiveabilityinresponsetorisingatmosphericCO2(Low-DeacutecarieFussmann amp Bell 2011) In contrast tomost freshwater systemsmarine environments have very little dissolved inorganic carbon(DIC)availableaspCO2 requiring specific investigationof thedif-ferencesbetweenmajortaxonomicgroupsintheirgrowthresponsetoCO2andpredictabilityofassociatedshiftsincommunitycompo-sitioninmarinesystems

Thisstudyaimstotestwhetherinformationondifferencesbe-tween major taxonomic groups of marine phytoplankton are suf-ficient topredict theeffectof increasingCO2ontheircapacity tocompeteTaxonomicgroupsthataremoreefficientatconcentratingand utilizingCO2 such as the genusSynechococcuswould be ex-pectedtohaveasmallergrowthresponseandadecreasedabilitytooutcompetetaxonomicgroupsthatarelessefficientatconcentrat-ingandutilizingCO2suchaschlorophytesunderelevatedCO2 all elsebeingequal Incontrasttaxonomicgroupswithspecificfunc-tional traits such as calcification in the coccolithophores maybedeleteriously affected by the increase in CO2Wemeasured howthegrowthratespairedcompetitiveabilitiesandcompositionsofacommunityofsevenphytoplanktonspeciesbelongingtofourmajortaxa (cyanobacteria chlorophytes diatoms and coccolithophores)respondedtoanincreaseinCO2Wetesthowrobustourfindingsaretochangesinthegrowthregimeandnutrientconcentrationbyreplicatingthisstudyinbothhigh-nitrogenbatchculturesandlower-nitrogensemicontinuouscultures

2emsp |emspMATERIAL S AND METHODS

21emsp|emspPhytoplankton cultures

We studied seven species from four dominant marine phyto-plankton groups the cyanobacterium Synechococcus sp (CCMP2370 meanplusmnrange 12plusmn04μm diameter Hughes Franklinamp Malin 2011) the chlorophytes Dunaliella tertiolecta (CCMP1320 11plusmn1μm diameter) and Prasinococcus capsulatus (CCMP1194 45plusmn1μm diameter) the diatoms Phaeodactylum tricornu-tum (CCMP2561 ~21μmby35μm) andThalassiosira weissflogii (CCMP 1051 15plusmn10μm diameter) and finally the calcifyingcoccolithophores E huxleyi (PLY 1516 4plusmn1μm diameter) andCoccolithus pelagicus (PLY18325plusmn15μmdiameter)Eachmajortaxonwiththeexceptionof thecyanobacteriawasrepresentedbytwospecieseachselectedbasedonbeingecologicallyrelevant

andbeingclearlyidentifiablethroughmorphologicalfeaturesvisi-bleundermicroscopyTherewasalargedifferenceinsizebetweenthe pairs of species from a group (25 difference for diatoms240 for chlorophytes and 625 for coccolithophores) so thattherewas an overlap in cell size (and associated surface area tovolumeratio)betweenallgroupswiththeexceptionofthesmallercyanobacterium

22emsp|emspGrowth conditions

All phytoplankton species were grown in Enriched SeawaterArtificial Water (ESAW) (Berges Franklin amp Harrison 2001) at15plusmn01degC under a 1212hr lightdark cycle at irradiance levelsof 2501plusmn45μmolmminus2 sminus1 All cultures were kept in suspensionon platform rockers set to 70 rotations per minute (rpm) in twoCO2-controlled growth chambers (Adaptis CMP6010 ConvironCanada) The relativehumidity levels acrossboth chambers aver-aged 82plusmn63One chamber simulated ambientCO2 conditions(506plusmn6μatmlocalconditionsleadtohigherthantheglobalaverageof400μatm)andtheotherfutureCO2conditions(1000plusmn7μatm)predictedfortheyear2100(IPCC2014)Thegrowthmediumwasfirstequilibratedinthechamberconditionsforaperiodof3daysprior to inoculating the phytoplankton in test tubes Each of thephytoplankton species was acclimated for a period of 2weeks(one transfer cycle) before experimentation bymaintaining stockcultures ineachCO2andnutrient treatmentStockculturesweremaintainedin50mlofmediawithin150mlglassflasksstopperedwithair-permeablefoamcapsandweremaintainedinexponentialgrowthwithweekly110dilution

23emsp|emspGrowth and competition experiments

All experiments were conducted in 8ml of medium in 15ml testtubes fittedwithpolyurethane foamstoppersand initiatedwithastartinginoculationof1times105cellsmltakenfromeachofthesinglespeciesculturespre-acclimatedundereachnutrientandCO2regimeAllculturesremainedinexponentialgrowththroughouteachofthe5-dayexperimentsTriplicatesofsevenpure(individualspecies)21pairwisemixturesandonefullcommunityculturewere inoculatedforeachcondition(CO2treatmentandcultureregime)ToaccountforanychambereffectstheexperimentswererepeatedswitchingtheCO2 treatmentbetweenchambersandrepeatedtwice ineachchamberconfiguration(totalreplicationifpoolingacrosschambersis12foratotalof1392experimentalcultures)

Totesttheeffectofgrowthregimeonthelinkbetweengrowthand community response all experimentswere conducted in twogrowthregimesthatdifferedinnutrientconcentrationandmaximalcelldensityInthehigh-nitrogenbatchcultureregimethestandardESAWmedium(882μmolLnitrogenasinF2mediumJutsonPipeamp Tomas 2016)was used and the culturewas tracked for 5dayswithoutreplenishingthemediumLong-termculturingofspeciesinour culture collectionwas carriedout usingESAWensuring accli-mationtothismediaInthelower-nitrogensemicontinuousculture


regimethenitrogenconcentrationinthemediumwas55μmolLNallothernutrientswereat thesame levelsas in thehigh-nitrogenbatchcultureregime(ieF2medium)andallcultureswerereplen-isheddailyoverthe5-dayperiodwith1mloffreshlowernitrogenmedia(18replenishment)

24emsp|emspQuantification

Totrackchangesintheculturesthroughouttheexperimentsam-pleswere takendaily fromall test tubes Samples fromboth thesingle species cultures and the control tubes containing only thegrowthmedia (blanks)weretakenonthefinaldayofeachruntomeasurebothpHandalkalinity(SnoeyinkampJenkins1980)toper-mittheestimationofthelevelofdissolvedCO2usingtheCO2Calcapplication(RobbinsHansenKleypasampMeylan2010)Purecul-turecelldensitiesweremeasureddailyfromthedayofinoculationuntilthefinaldaythrougheitherhaemocytometryorflowcytom-etryforthecalculationoftheirrespectivegrowthratesFreshsam-plesofallotherpurecultureswerepasseddirectlythroughaflowcytometer(AccuriC6BDBioscienceUSA)Forflowcytometryaprotocolwithamediumflowrateof0583μlsandatotalof10000eventsrecordedwasusedfollowingtheproductionofatemplatefileusingforwardandsidescatterprofiles tostandardizethecellcountsDuetoflowcytometeruseandsetupcyanobacteriacouldnot be counted on the flow cytometer Cyanobacteria sampleswere immediately fixedwithLugolrsquos solution (1finalconcentra-tion)andinjectedintoahaemocytometerslideandcountedusingmicroscopySamplesfromeachofthecompetitionmixtureswerealsoimmediatelyfixedwithLugolrsquossolutionandstoredat4degCuntiltheywerecountedviamicroscopywherebytheabundanceofeachspeciescomprising themixtureswerecountedusinga totalmini-mumcountof400cells

25emsp|emspStatistical analysis

To measure the response of growth to treatments exponentialgrowth rates of each culture were calculated as the ratio of thenatural-log of cell densities over the 5-day experimental periodPredictedcompetitioncoefficientswerecalculated frompurecul-turegrowthratewhilerealizedcompetitioncoefficientswerecalcu-latedfromchangesinfrequency(Low-Deacutecarieetal2011)Achangeinthesignofthecompetitioncoefficientindicatesachangeincom-petitivedominancebutachangeinthecompetitioncoefficientthatdoesnotalterthesignindicatesachangeinthespeedofcompetitiveexclusionPredicted(p)competitioncoefficientofspecies1(c1)wascalculatedasthedifferenceofitsgrowthratewiththegrowthrateofacompetingspecies (r2)standardizedbythegrowthrateoftheentirecompetingcommunity(rcommunity)

Realized (r) competition coefficients (Equation 2) were calcu-lated from the change in the frequency (aka relative frequency

f )ofeachspeciesthroughtimeaccountingforthegrowthofthecommunityoverall(numberofgenerationsacrossthecommunitygcommunity)

Inthefullcommunityofsevenspeciesf2wasthefrequencyofallotherspeciescombinedPhytoplanktonresponsestoCO2 were calculatedas thedifferencebetweengrowth ratesorcompetitioncoefficients in ambient and high CO2 treatments The measuredcompetition coefficient based on change in frequency integratesany effect of one species on the frequency of another species(whether through limitedgrowth through resourcecompetitionorthroughsomeotherecologicalinteractionsincludingfacilitationorallelopathy)

The responseof dissolvedCO2 in cultures growth rates andcompetition coefficientswere assessedusing an analysisof vari-ance(ANOVA)inwhichthemaineffectsandinteractionsofCO2 treatmentcultureregimeandmajortaxonomicgroupweretestedthemain effect of species was also includedWhen needed in-dividualANOVAswere conducted for the responseof each sep-arate taxonomicgroupwith themaineffectsand interactionsofCO2treatmentcultureregimeandspeciesFullcommunitycom-petitionswere assessed using amultivariate analysis of variance(MANOVA)whenphytoplanktonweregroupedbymajortaxaandwhengroupedbyspeciesPredictionsoftheresponseofcompeti-tiontoCO2fromtheresponseofgrowthrateswasassessedbyav-eragingthecompetitionandgrowthresponsebyspeciesandfittinga linear regression

In text values are expressed asmeans plusmn1 standard deviationAnalyses were conducted within the R statistical coding package(R Development Core Team 2013) and figures were produced inMicrosoftExcel

3emsp |emspRESULTS

31emsp|emspDissolved CO2 concentration

CO2 concentration was controlled in the atmosphere and someCO2drawdownwasexpectedingrowingculturessotheeffectoftreatment onDIC concentration needed to be testedChanges inatmospheric CO2 concentrations caused the expected changes inpCO2 (FigureS1 3107plusmn235ndash7112plusmn944μatm F1336=10427plt001)andpH (from815plusmn002to785plusmn003)Theconcentra-tion of nitrogen in each culture regime also had an effect on thepH (802plusmn016 in high-N vs 788plusmn014 in lower nitrogen) andthus pCO2 (190plusmn200μatm higher in low-nitrogen F1336=267plt001)Allculturesdrewdownonaverage1404plusmn1171μatmofCO2comparedtoblankmediaoverthe5-dayexperimentbutthedifference between ambient and high CO2 treatments remainedthroughout thegrowthof thecultures (average1983plusmn762μatm

(1)Predicted competition coefficient c1p=r1minus r2

rcommunity

(2)Realized competition coefficient c1r=1

gcommunity

ln

⎛⎜⎜⎜⎝

f1finalf2final

f1initialf2initial

⎞⎟⎟⎟⎠


differenceF1336=2389thinspplt001TableS1fordrawdownforeachspecies)

32emsp|emspGrowth response

The effect of an increase in atmospheric CO2 on phytoplanktongrowth rateswas assessed Growth rates recorded for each phy-toplanktonculturebetweenchambersdidnotdiffer (TableS2) in-dicatingthattherewasnoconfoundingchambereffectupontheirresponses so assays in each chamberwere treated as replicatesGrowthratesofallspeciesincreasedwithhighCO2independentofculture regimewhereonaveragean increaseof012plusmn007dayminus1 wasobserved inphytoplanktonexposedtohighCO2comparedtoambient conditions (Figure1 F1336=106 plt001) The scale ofthis changewas taxa- andculture-regimedependent (F3336=240plt001)Chlorophyteshadthelargestaverageincreaseingrowthrate between CO2 treatments of 020plusmn004day

minus1 whereasSynechococcus had the smallest increase of 006plusmn001dayminus1 Specieswithineachmajor taxonalsodiffered in their response tohighCO2(TableS3)

33emsp|emspPairwise competitions

TheeffectofincreasingatmosphericCO2uponthecompetitiveabil-ityofeachspecieswithineachofthepairwisecompetitionswasas-sessedacrossbothcultureregimesTherewasa log-linearchangein species frequency in each competition culture (FiguresS2 andS3)Onaveragetheresponseofcompetitionsbetweenspeciesofthesametaxonomicgroupwassmallerthantheaveragechangeincompetitioncoefficientbetweenspeciesofdifferentmajorgroups(samegroupaverageabsolutechangeof028plusmn023Figure2andashcdifferentgroupaverageabsolutechange=102plusmn048t144=1178plt001 Figure2dndashi) The competitive ability of Synechococcus declined under the high CO2 treatment independent of the taxo-nomicgroup itwascompetingwith (Figure2dndashfaveragedecreaseof 124plusmn098 in competition coefficient F1288=1386 plt001)ThechlorophytesonaveragecompetedbetterwithincreasedCO2

levels (Figure2dgndashh average increase of 11plusmn076 in competi-tioncoefficientF1480=2118plt001)howeverapartialreversalof this trend was observed under batch high-nitrogen conditionswhen competing against diatoms (F2480=96 plt001) The com-petitiveresponseofthediatomsandcoccolithophorestoelevatedCO2conditionswasdependentonthecompetingtaxonomicgroup(Figure2endashf diatom average decrease of 032plusmn092 in competi-tion coefficient F3480=518 plt001 coccolithophore averagedecrease of 028plusmn041 F3480=1837 plt001) andwas species-specific when the coccolithophores competed with the diatoms(F2192=182plt001)

34emsp|emspFull community competitions

Theassembledcommunitywasnotstable(extinctionswereeventuallyexpectedbutnotobserved)andtherewasalog-linearchangeinspeciesfrequencyinthecommunitycomprisingallsevenspecies(FigureS4)Thesecompetitivedynamicsinthefullcommunitywerealsoalteredby theCO2 treatmentThecompetitiveabilityofSynechococcus de-creased themostwhenCO2 levels increased (Figure3 averagede-crease of 077plusmn029 in competition coefficient F148=21976plt001)althoughitremainedadominantcompetitorwithapositivecompetitioncoefficientandthediatomsalsodecreasedalthoughtoalesserextent(averagedecreaseof020plusmn021incompetitioncoef-ficientF196=1944plt001)Thechlorophytesontheotherhandweretheonlytaxonwhichincreasedtheircompetitiveabilities(aver-age increaseof044plusmn034 incompetitioncoefficientF196=1071plt001)andtheresponseofthecoccolithophoreswasfoundtobespecies-specific (TableS3)whereE huxleyirsquos competitioncoefficientincreasedbyonaverage019plusmn031atelevatedCO2levels(plt001)butC pelagicuswasunaffected(averageincrease001plusmn060incom-petitioncoefficientpgt05)

35emsp|emspPredicting phytoplankton community changes

Changesincompetitionandcommunitydynamicsinresponsetoris-ingCO2werepredictablefromknowndifferenceintheCO2-related

F IGURE 1emspPhytoplanktongrowthratesacrossCO2andcultureregimesPlainbarsarebatchhighnitrogenconditions(highandlowCO2)barswithstripesaresemicontinuouslowernitrogenconditions(highandlowCO2)whitebarsareambientCO2(~500μatm)andshadedbarsarehighCO2(~1000μatm)Eachbarshowsthemeanvalueswithplusmn1standarddeviation(N=12)AllspecieshadahighergrowthrateinhighCO2comparedtolowCO2independentofcultureregime


F I GURE 2emspCompetitioncoefficientinallpairwisecompetitions(andashc)Competitionsbetweenmembersbelongingtothesametaxonomicgroup(dndashf)competitionswherethefocalcompetitorwasSynechococcussp(Synespcyanobacterium)(gndashh)competitionswithchlorophytes(Dunaliella tertiolectamdashDt- and Prasinococcus capsulatusmdashPc-)asfocalcompetitors(f)comparisonswithdiatomsasfocalcompetitorspecies(Phaeodactylum tricornutummdashPt- Thalassiosira weissflogiimdashTw)Thecoccolithophoresareshownincompetitionbutnotasfocalspecies(Emiliania huxleyimdashEh- and Coccolithus pelagicusmdashCp-)StatisticsandlegendmatchFigure1shading(highCO2)stripes(semicontinuouslowernitrogen)eachbarshowsthemeanvalueswithplusmn1standarddeviation(N=12)HighCO2decreasesthecompetitiveabilityofSynechococcuswhilemostlyincreasingthecompetitiveabilityofchlorophytes

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)


taxonomictraitsandgrowthresponsestoelevatedCO2Themeancompetitive response for each species within pairwise competi-tionswasagood indicatorof thecompetitiveabilityofeachphy-toplankton specieswithin the full community (FigureS5) in batchhighnitrogen(R2=75plt001)andsemicontinuouslowernitrogenconditions(R2=93plt001)

Pureculturegrowthresponseswerealsoagoodpredictoroftheoverallcompetitiveresponseofeachspecieswithinpairwisecompe-titions(Figure4a)inbothbatchhighnitrogen(R2=94plt001)andsemicontinuous lower nitrogen conditions (R2=93 plt001) andofthecompetitiveresponseinthefullcommunityofsevenspecies(Figure4b) inbatchhighnitrogen(R2=73plt001)andsemicon-tinuouslowernitrogenconditions(R2=80plt001)

4emsp |emspDISCUSSION

41emsp|emspCO2 as a limiting resource

Marineenvironmentsarehighlydynamicsystemsinwhichgrowthrate is an important parameter for phytoplankton population dy-namicsInsitugrowthratesofcommunitiesofphytoplanktonrangefrom01to36doublingperday(Furnas1990)Eveninconditionswereother factors such as grazing pathogens ormaximum totalbiomassachievablegrowthrateswillinfluencedynamicsandcom-positionofcommunitiesAllphytoplanktonspeciesexaminedinthisstudyhadanincreasedgrowthratewhenexposedtofutureatmos-phericCO2 levelsacrossbothcultureregimesThiscontrastswithexpectationsbasedonnutrient limitation innaturalmarinephyto-planktoncommunitieswherethemainlimitingresourcesareusuallynitrogenandiron(DowningOsenbergampSarnelle1999)Howeverthey match extensive laboratory experiments looking at growthresponse to elevated CO2 in nutrient-replete and nutrient-limitedconditions(egmeta-analysisDutkiewiczetal2015)Thenitrogen

levels on our experiment did not limit growth in either treatmentandwerehighcomparedtooceanictotalnitrogenrangesbetween219and410μmolL(GuildfordampHecky2000)butthelowernitro-gentreatment(55μmolLN)waswithinnaturalrangeforestuarineandcoastalmarineecosystems inwhichtotalnitrogencanexceed150μmolLN(Smith2006)Biomassofprimaryproducersinmarineenvironmentsisgenerallyexpectedtobelimitedbynitrogenorironalthoughthereisgrowingunderstandingthatmultiplenutrientspo-tentiallynitrogenandCO2canlimitprimaryproductionsimultane-ously(Harpoleetal2011Mooreetal2013)CO2couldplayaroleasarate-limitingnutrientlimitinggrowthratebutnotmaximalbio-mass(Low-DeacutecarieFussmannampBell2014)andthusmayexhibitastrongerlimitationroleindynamicmarineenvironmentswheremax-imalbiomass israrelyreachedanddynamicsare inpartcontrolledbygrowthratesIncreasedCO2increasesprimaryproducerbiomassinnaturalmarinephytoplanktoncommunitieswhenothernutrientsareaddedsimultaneously(Riebeselletal2007)andeveninlownu-trientconcentrationandtheabsenceofnutrientaddition(Eberleinetal2017)HoweverunderstandingtheroleofCO2amongotherlimitingresourcesrequiresfurtherexperimentation

42emsp|emspPredictability of changes in the composition of communities to a changing environment

OurresultsontheecologicalresponsetoincreasedCO2 inmarinephytoplanktonalignwithpreviousstudiesofchangeincompetitioninfreshwaterphytoplankton(Low-Deacutecarieetal2011)andwithex-pectationbasedon theCO2-relatedphysiologyof themajor taxo-nomicgroups(egReinfelder2011)SynechococcuswhichhasthemostefficientuptakeandutilizationofCO2loseoutmostlyatthebenefitofchlorophytesunderhighCO2aschlorophyteshavelikelyinvestedinfunctionaltraitsnotrelatedtocarbonutilizationandac-quisitionsuchasnitrogenscavengingorlightharvestingHowever

F IGURE 3emspFullcommunitycompetitioncoefficientsElevatedCO2decreasesthecompetitiveabilityofSynechococcusandthediatomsincreasesthecompetitiveabilityofthechlorophytesbutdidnotexhibitanoveralleffectonthecoccolithophoresunlessinteractingwithcultureregimewheretheircompetitiveabilitywithinsemicontinuous-lowernitrogenculturesincreasedbutdecreasedinbatchhigh-nitrogenculturesMatchespreviousfiguresgray(highCO2)stripes(semicontinuouslowernitrogen)barvalue(mean)anderrorbars(onestandarddeviationN =12)


this change in competitive ability did not prevent Synechococcus fromincreasinginfrequencyinthefullcommunityunderelevatedCO2 The change in competition between groups that havemoresimilarcapacitiesforcarbonutilizationandacquisition(chlorophytesvsdiatomsordiatomsvscoccolithophores)islesspredictable(morespecies-specific or dependsmore on culture regime)Other traitsthatarenotspecifictoanymajorgroupssuchassizeandassociatedsurfaceareatovolumeratiocouldalsoinfluencetheexpectedre-sponsetoincreasingCO2withlargertaxabenefitingmostfromtheincrease inCO2However changes in competitionunderelevatedCO2betweenspeciesofthesamegroupwasnotconsistentthisdif-ferencewassmallwhenpresentanditdidnotalignwithpredictionsmadebysize (smaller species tended tobenefit fromthe increase

inCO2)Our findings contrastwith findings from some studiesofinsitunaturalmarinephytoplanktonassemblagesincludingastudyshowinganincreaseinthecyanobacteriumSynechococcus(Paulinoetal2007)andadecrease inauroxanthin-containingphytoplank-ton(diatomsYoshimuraetal2009)Intheseexperimentsonnatu-ralcommunitiesasinourexperimentsgrowthresponseisexpectedto dominate the community dynamics and as these experimentstracktheresponse inabloomelicitedthroughtheadditionofnu-trientsAmesocosmexperimentwithout theadditionofnutrientsdidfindadecreaseinSynechococcusandanincreaseinmajorgroupsofchlorophytes(CrawfurdAlvarez-FernandezMojicaRiebesellampBrussaard2017)Differenceintheresponseofnaturalassemblagesand thoseof simplified laboratorycommunitiesarenot surprising

F IGURE 4emspPredictingresponsesfrompureculturegrowthresponsesThegrowthresponseofeachphytoplanktonspecieswasusedtopredicttheaveragecompetitiveresponse(a)inpairwisecompetitionsand(b)inthefullcommunitycomprisedofallsevenspeciesCirclesarebatchhigh-nitrogenwithdashedlinefortheregression[(a)R2=94and(b)R2=73]andtrianglesaresemicontinuouslowernitrogenwithdottedlinefortheregressionline[(a)R2=93and(b)R2=80]AllvaluesarelabeledwiththefirstletterofitsgenusandspeciesnamesandarecoloredaccordingtobothtaxonomicgroupandspeciesThechlorophytesareshownasdark(Dunaliella tertiolecta)andlightgreen(Prasinococcus capsulatus)thediatomsasdark(Phaeodactylum tricornutum)andlightbrown(Thalassiosira weissflogii)thecoccolithophoresasblack(Emiliania huxleyi)andgray(Coccolithus pelagicus)andthecyanobacteriaareshownasorange(Synechococcussp)Allpointsdisplayedarethemeanforaspecieswithplusmn1standarddeviation(N=12)Thegreatestresponseswerealwaysexhibitedbythechlorophytesfollowedbythediatoms(inbatchhigh-nitrogenconditions)orcoccolithophores(insemicontinuouslowernitrogenconditions)andthelowestresponsesweregenerallyexhibitedbySynechococcus

(a)

(b)


and can be explained by factors including interactionswith othertreatments (including nutrient addition) changes in communitiesselectivegrazerorpathogensinresponsetotheCO2treatmentorgreaterimportanceofheterotrophicandmixotrophicprocessesuti-lizingexistingorganiccarbonstocksInnaturalmarinecommunitiescompetitive dynamics and the response toCO2may also be con-trolledbythecapacitytoreachmaximalbiomass(carryingcapacity)or other types of interactions between competitors (eg throughallelopathy or facilitation) Results of both controlled laboratorystudiesandnaturalphytoplanktonassemblagesarelikelytobede-pendentontheexperimentaldurationduetotheinterplayofplasticandevolutionaryresponsesofindividualspecies

43emsp|emspPlasticity and evolution

PhytoplanktonareabletoregulatetheirCCMssuchthatinhighCO2 conditionstheyareabletoreducetheiractivityandthereforeen-ergy consumption (GiordanoBeardallampRaven 2005Reinfelder2011) High CO2 exposure is suggested to be accompanied by adown-regulation of the genes involved with these cellular CCMs(CrawfurdRavenWheelerBaxterampJoint2011VandeWaaletal2013)DifferentlifestagesdonothavethesameresponsestorisingCO2forexamplehaploidanddiploidstagesincoccolithophoresdonothavethesameresponsetoacidification(RokittaJohnampRost2012)thereforeaplasticresponsecouldarisefromachangeinlife-historystrategyIftheseplasticresponsesingeneregulationarenotcaptured by the time scale of our experiments (5days) and differmarkedlybetweentaxatheycouldaffectthepredictabilityofthechangesincompetitionsunderelevatedCO2

Marine phytoplankton may eventually adapt to higher CO2 concentrationsAsforplasticitypotentialdifferencesintherateofadaptationorscaleofadaptivegainsbetweenmajortaxonomicgroupsorspeciesmayaltertheexpectedchangesincompetitionHowever freshwater phytoplankton were not found to specifi-callyadapt toelevatedCO2 (CollinsampBell20042006CollinsSultemeyerampBell2006Low-DecarieJewellFussmannampBell2013)althoughprolongedexposuretoelevatedCO2canleadtoadecreasedabilitytogrowunderlowerCO2(CollinsampBell2004)Thesefindingsinfreshwaterphytoplanktonmaynotbetransfer-able tomarine algae In calcifyingphytoplankton the change inpHassociatedwithhigherCO2concentrationscouldbeexpectedtoactasastrongselectivepressureleadingtofasterevolutioninthisgroup(CollinsRostampRynearson2014)ThecoccolithophoreE huxleyi a calcifying phytoplankton has been shown to adapttohighCO2conditionsinmarinesystemswithin500generations(LohbeckRiebesellCollinsampReusch2013LohbeckRiebesellampReusch2012)AnothercoccolithophorespeciesGephyrocapsa oceanicadidevolveunderhighCO2althoughit isnotclearthatobservedchangeswereanadaptiveresponsetoCO2(TongGaoampHutchins 2018)Beyond calcifyingphytoplankton the evolu-tionary implications of elevated CO2 formarine phytoplanktonand thus its potential effect on the predictability of changes incompetitionandcommunitycompositionisnotwellresolvedAn

experiment with the cyanobacterium Trichodesmium a globallyimportant diazotroph showed adaptation to elevated CO2 con-ditionswhenmaintainedathighCO2butitwasnotCO2specificwithlinesevolvedatelevated-CO2growingbetterthantheambi-entselectedlinesindependentofCO2concentrations(WalworthLeeFuHutchinsampWebb2016)Totestfortheimpactofadap-tation on the predicted changes in competitive dynamics underelevated CO2 the experiment presented in this study could berepeatedwith high CO2-adapted lines of eachmajor taxonomicgroup if the required long-term selection experiments areconducted

44emsp|emspImplications of changes in community composition

Inadditiontodifferinginthecarbonacquisitionandusethemajortaxonomic groups of phytoplankton have different ecologicalrolesOn average diatomshave someof the fastest sinking rates(Fahnenstieletal1995)andplayamajorroleinexportingprimaryproductivityfromtheeuphoticzoneCoccolithophoresreleaseCO2 throughcalcificationanddecreasetheDICpoolsothattheincreaseincoccolithophoreswithhigherCO2 seen forat least thespeciesfromthisstudy(E huxleyiwhichismostabundantandwidespreadcoccolithophoresintheocean)couldleadtoafeedbackandafur-therincreaseindissolvedCO2concentrationTheassociationofCO2 response and ecological role of marine phytoplankton taxonomicgroupsleadmodelstosuggestthattherepercussionsofchangeinthecommunitycompositionforecologicalfunctionwillexceedtheeffectsofwarmingandreducednutrientsupplyarisingfromglobalchange(Dutkiewiczetal2015)

Our laboratory experiments and the resulting predictions ofmajor ecosystem level repercussions from the change in phyto-planktoncommunitieswith risingCO2 ignorenumerousecologicalcomplexitiesInadditiontothelimitationalreadyraisedabouthigh-nutrientconcentrationsandasmallsetoflaboratorystrainsfurthercaveatsincludethatthenaturalphytoplanktoncommunitiesareem-beddedincomplexfoodwebsinwhicheachtrophicleveloreveneachspeciesmayrespondtooceanacidificationandthusmodulatetheresponseofphytoplanktontorisingCO2RisingCO2couldthusstillaffectphytoplanktoninwaysthatdonotdependonthecapac-ityofmajortaxonomicgroupsofphytoplanktontouptakeanduti-lizeCO2InadditionoceanacidificationisonlyoneofmanycurrentanthropogenicchangesaffectingourworldrsquosoceansNonethelessthatthechangeincommunitycompositionwithrisingCO2ofafunc-tionallydiversecommunityofphytoplanktoncanbepredictedfromgrowthresponseofindividualspeciessuggeststhatsomeusefulin-ferencescanbemadefromthestudyofindividualtaxaforthepre-dictionofhowmarinecommunitieswillrespondtoglobalchanges

ACKNOWLEDG MENTS

We thank Tania Cresswell-Maynard for the maintenance of theUniversity of Essex culture collectionKirraleeBaker andMichael


SteinkeforcommentonthemanuscriptThestudywassupportedbystart-upfundsfromtheUniversityofEssextoEtienneLow-Deacutecarie

CONFLIC T OF INTERE S T

Nonedeclared

AUTHORSrsquo CONTRIBUTIONS

JacobPardewdesignedandconductedtheexperimentanalyzedtheresults and drafted portions of themanuscriptMacarenaBlancoPimentelconductedapilotexperimentandcontributed to theex-perimental design Etienne Low-Deacutecarie advised on the design oftheexperimentitsanalysisanddraftedportionsofthemanuscriptAll authorscontributed to the reviewandeditingof thecompletemanuscript

DATA ACCE SSIBILIT Y

Data and analysis script are available on Zenodo (httpsdoiorg105281zenodo1172665)

ORCID

Jacob Pardew httporcidorg0000-0001-9979-4514

Macarena Blanco Pimentel httporcidorg0000-0001-9004-1591

Etienne Low-Decarie httporcidorg0000-0002-0413-567X

R E FE R E N C E S

AlmeacutenAKVehmaaABrutemarkABachLLischkaSStuhrAhellipEngstroumlm-OumlstJ(2016)NegligibleeffectsofoceanacidificationonEurytemora affinis (Copepoda)offspringproductionBiogeosciences131037ndash1048httpsdoiorg105194bg-13-1037-2016

Badger M R amp Price G D (2003) CO2 concentrating mechanismsin cyanobacteria Molecular components their diversity and evo-lution Journal of Experimental Botany 54 609ndash622 httpsdoiorg101093jxberg076

BergesJAFranklinDJampHarrisonPJ(2001)Evolutionofanartifi-cialseawatermediumImprovementsinenrichedseawaterartificialwateroverthelasttwodecadesJournal of Phycology371138ndash1145httpsdoiorg101046j1529-8817200101052x

BermuacutedezRWinderMStuhrAAlmeacutenA-KEngstroumlm-Oumlst JampRiebesellU (2016) Effect of ocean acidification on the structureandfattyacidcompositionofanaturalplanktoncommunity intheBalticSeaBiogeosciences136625ndash6635httpsdoiorg105194bg-13-6625-2016

BrewerPFabryViHilmiK JungSPoloczanskaEampSundbyS(2014)TheOceanFifth Assessment ReportmdashImpacts Adaptation and VulnerabilitymdashIPCC(pp1ndash51)

CollinsSSampBellG(2004)Phenotypicconsequencesof1000gen-erationsof selection at elevatedCO2 in a green alga Nature431566ndash569httpsdoiorg101038nature02945

Collins S amp Bell G (2006) Evolution of natural algal popula-tions at elevated CO2 Ecology Letters 9 129ndash135 httpsdoiorg101111j1461-0248200500854x

Collins S Rost B amp Rynearson T A (2014) Evolutionary potentialof marine phytoplankton under ocean acidification Evolutionary Applications7140ndash155httpsdoiorg101111eva12120

Collins S Sultemeyer D amp Bell G (2006) Changes in C uptakein populations of Chlamydomonas reinhardtii selected at highCO2 Plant Cell and Environment 29 1812ndash1819 httpsdoiorg101111j1365-3040200601559x

CrawfurdKJAlvarez-FernandezSMojicaKDARiebesellUampBrussaardCPD(2017)Alterationsinmicrobialcommunitycom-position with increasing fCO2 A mesocosm study in the easternBalticSeaBiogeosciences143831ndash3849httpsdoiorg105194bg-14-3831-2017

CrawfurdKJRavenJAWheelerGLBaxterEJampJointI(2011)TheresponseofThalassiosira pseudonana to long-termexposuretoincreasedCO2anddecreasedpHPLoS ONE61ndash9

DowningJAOsenbergCWampSarnelleO(1999)Meta-analysisofmarinenutrient-enrichmentexperimentsVariationinthemagnitudeofnutrientlimitationEcology801157ndash1167httpsdoiorg1018900012-9658(1999)080[1157MAOMNE]20CO2

Dutkiewicz S Morris J J Follows M J Scott J Levitan ODyhrmanSTampBerman-Frank I (2015) Impactofoceanacid-ification on the structure of future phytoplankton communitiesNature Climate Change 5 1002ndash1006 httpsdoiorg101038nclimate2722

EberleinTWohlrabSRostBJohnUBachLTRiebesellUampVanDeWaalDB(2017)Effectsofoceanacidificationonprimaryproduction inacoastalNorthSeaphytoplanktoncommunityPLoS ONE121ndash15

FahnenstielGLMcCormickMJLangGARedaljeDGLohrenzSEMarkowitzMhellipCarrickHJ (1995)Taxon-specificgrowthand loss rates for dominant phytoplankton populations from thenorthernGulf ofMexicoMarine Ecology Progress Series117 229ndash239httpsdoiorg103354meps117229

Fu FXWarnerME ZhangY FengYampHutchinsDA (2007)Effects of increased temperature and CO2 on photosynthe-sis growth and elemental ratios in marine Synechococcus and Prochlorococcus (cyanobacteria) Journal of Phycology43 485ndash496httpsdoiorg101111j1529-8817200700355x

Furnas M J (1990) In situ growth-rates of marine-phytoplanktonApproachestomeasurementcommunityandspeciesgrowthratesJournal of Plankton Research121117ndash1151httpsdoiorg101093plankt1261117

Giordano M Beardall J amp Raven J A (2005) CO2 concentratingmechanisms in algaeMechanisms environmentalmodulation andevolution Annual Review of Plant Biology 56 99ndash131 httpsdoiorg101146annurevarplant56032604144052

GriggsDJampNoguerM(2002)Climatechange2001Thescientificbasis Contribution of Working Group I to the Third AssessmentReportoftheIntergovernmentalPanelonClimateChangeWeather57267ndash269httpsdoiorg101256004316502320517344

GuildfordSJampHeckyRE(2000)TotalnitrogentotalphosphorusandnutrientlimitationinlakesandoceansIsthereacommonrela-tionship Limnology and Oceanography45 1213ndash1223 httpsdoiorg104319lo20004561213

HarpoleWSNgai JTClelandEESeabloomEWBorerETBrackenMEShellipSmithJE(2011)Nutrientco-limitationofpri-maryproducer communitiesEcology Letters14 852ndash862 httpsdoiorg101111j1461-0248201101651x

Hopkinson B M Dupont C L Allen A E amp Morel F M M(2011) Efficiency of the CO2-concentrating mechanism of dia-tomsProceedings of the National Academy of Sciences of the United States of America 108 3830ndash3837 httpsdoiorg101073pnas1018062108

HughesCFranklinDJampMalinG(2011)Iodomethaneproductionby two important marine cyanobacteria Prochlorococcus marinus


(CCMP2389)andSynechococcussp(CCMP2370)Marine Chemistry12519ndash25httpsdoiorg101016jmarchem201101007

Hutchins D A Fu F-XWebb E AWalworth N amp Tagliabue A(2013) Taxon-specific response of marine nitrogen fixers to ele-vatedcarbondioxideconcentrationsNature Geoscience6790ndash795httpsdoiorg101038ngeo1858

IPCC (2014) Observations Ocean In Intergovernmental Panel onClimateChange(Ed)Climate change 2013mdashThe physical science basis (pp255ndash316)CambridgeUKCambridgeUniversityPress

JutsonMGSPipeRKampTomasCR (2016)Thecultivationofmarinephytoplankton InM-NTsaloglou (Ed)Microalgae Current research and applications (pp 11ndash26) PooleUK Caister AcademicPresshttpsdoiorg10217759781910190272

KroekerK JKordasR LCrimRNamp SinghGG (2010)Meta-analysisrevealsnegativeyetvariableeffectsofoceanacidificationon marine organisms Ecology Letters 13 1419ndash1434 httpsdoiorg101111j1461-0248201001518x

Lohbeck K T Riebesell U Collins S amp Reusch T B H (2013)Functional genetic divergence in high CO2 adapted Emiliania huxleyi populations Evolution 67 1892ndash1900 httpsdoiorg101111j1558-5646201201812x

LohbeckKTRiebesellUampReuschTBH(2012)Adaptiveevolu-tion of a key phytoplankton species to ocean acidificationNature Geoscience51ndash6

Low-Deacutecarie E FussmannG FampBellG (2011) Theeffect of ele-vatedCO2ongrowthandcompetitioninexperimentalphytoplank-toncommunitiesGlobal Change Biology172525ndash2535httpsdoiorg101111j1365-2486201102402x

Low-Deacutecarie E FussmannG F amp Bell G (2014) Aquatic primaryproduction inahigh-CO2 world Trends in Ecology amp Evolution291ndash10

Low-DecarieEJewellMDFussmannGFampBellG(2013)Long-termcultureatelevatedatmosphericCO2failstoevokespecificad-aptationinsevenfreshwaterphytoplanktonspeciesProceedings of the Royal Society B Biological Sciences 280 20122598ndash20122598httpsdoiorg101098rspb20122598

MeyerJampRiebesellU(2015)ReviewsandsynthesesResponsesofcoc-colithophorestooceanacidificationAmeta-analysisBiogeosciences121671ndash1682httpsdoiorg105194bg-12-1671-2015

MooreCMMillsMMArrigoKRBerman-FrankIBoppLBoydPWhellipUlloaO(2013)ProcessesandpatternsofoceanicnutrientlimitationNature Geoscience6 701ndash710 httpsdoiorg101038ngeo1765

PaulinoA I Egge JKampLarsenA (2007)Effectsof increasedat-mosphericCO2onsmallandintermediatesizedosmotrophsduringanutrientinducedphytoplanktonbloomBiogeosciences Discussions44173ndash4195httpsdoiorg105194bgd-4-4173-2007

PriceGDBadgerMRWoodgerFJampLongBM(2008)Advancesin understanding the cyanobacterialCO2-concentrating-mechanism(CCM)FunctionalcomponentsCitransportersdiversitygeneticregu-lationandprospectsforengineeringintoplantsJournal of Experimental Botany591441ndash1461httpsdoiorg101093jxberm112

R Development Core Team (2013) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputingRetrievedfromhttpwwwR-projectorg

ReinfelderJR(2011)CarbonconcentratingmechanismsineukaryoticmarinephytoplanktonAnnual Review of Marine Science3291ndash315httpsdoiorg101146annurev-marine-120709-142720

Riebesell U Schulz K G Bellerby R G J BotrosM Fritsche PMeyerhoumlfer M hellip Zoumlllner E (2007) Enhanced biological carbonconsumptioninahighCO2 ocean Nature450545ndash548httpsdoiorg101038nature06267

Robbins L L Hansen M E Kleypas J A amp Meylan S C (2010)CO2calc A user-friendly seawater carbon calculator for Windows Mac OS X and iOS (iPhone)RestonVAUSGeologicalSurvey

Rokitta S D John U amp Rost B (2012)Ocean acidification affectsredox-balance and ion-homeostasis in the life-cycle stages ofEmiliania huxleyi PLoS ONE7e52212httpsdoiorg101371jour-nalpone0052212

Smith V H (2006) Responses of estuarine and coastal marine phy-toplankton to nitrogen and phosphorus enrichment Limnology and Oceanography 51 377ndash384 httpsdoiorg104319lo2006511_part_20377

SnoeyinkVampJenkinsD(1980)Water chemistry1stedNewYorkNYJohnWileyampSons

TongSGaoKampHutchinsDA(2018)Adaptiveevolutioninthecoc-colithophoreGephyrocapsa oceanica following1000generationsofselectionunderelevatedCO2 Global Change Biology3842ndash49

TortellPD(2000)EvolutionaryandecologicalperspectivesoncarbonacquisitioninphytoplanktonLimnology and Oceanography45744ndash750httpsdoiorg104319lo20004530744

TortellPDPayneCDLiYTrimbornSRostBSmithWOhellipDiTullioGR(2008)CO2sensitivityofSouthernOceanphytoplank-tonGeophysical Research Letters35L04605

VandeWaalDBJohnUZiveriPReichartGJHoinsMSluijsAampRostB(2013)Oceanacidificationreducesgrowthandcalci-ficationinamarinedinoflagellatePLoS ONE8e65987httpsdoiorg101371journalpone0065987

WalworthNG LeeMD Fu F-XHutchinsDAampWebb EA(2016)MolecularandphysiologicalevidenceofgeneticassimilationtohighCO2inthemarinenitrogenfixerTrichodesmium Proceedings of the National Academy of Sciences of the United States of America113E7367ndashE7374httpsdoiorg101073pnas1605202113

Wu Y Gao K Riebesell U (2010) CO2-induced seawater acidifi-cation affects physiological performance of the marine diatomPhaeodactylum tricornutum Biogeosciences72915ndash2923

Yoshimura T Nishioka J Suzuki K Hattori H Kiyosawa H ampWatanabeYW(2009)ImpactsofelevatedCO2onphytoplanktoncommunity composition and organic carbon dynamics in nutrient-depletedOkhotskSeasurfacewatersBiogeosciences Discussions64143ndash4163httpsdoiorg105194bgd-6-4143-2009

SUPPORTING INFORMATIONAdditional Supporting Information may be found online in thesupportinginformationtabforthisarticle

How to cite this articlePardewJBlancoPimentelMLow-DecarieEPredictableecologicalresponsetorisingCO2 ofacommunityofmarinephytoplanktonEcol Evol 2018001ndash11 httpsdoiorg101002ece33971


1emsp |emspINTRODUC TION

AtmosphericCO2concentrationsrecentlyexceededahistorichighof400partspermillion(μatm)alevelwhichhasnotbeensurpassedinatleastthepast420000years(GriggsampNoguer2002)Thisin-creaseinatmosphericCO2hasledtoadecreaseintheoceanpHof01unitssincetheonsetoftheIndustrialRevolution(IPCC2014)TheconcentrationofCO2intheatmosphereisexpectedtocontinuetoincreaseataratewhichistentimesfasterthanhasbeenrecordedinthepast55millionyears(Almeacutenetal2016)PredictionssuggestthatbytheendofthiscenturyatmosphericCO2 levelsmayreachbetween700and1000μatmandoceanpHwilldecreaseto~78ndash77(Breweretal2014)ThesechangesinatmosphericCO2 concen-trationandinoceanpHcombinetoincreasetheavailabilityofCO2 formarineprimaryproducershampertheabilityoforganismstocal-cifyandaffectthegrowthratesofmarinephytoplankton(KroekerKordasCrimampSingh2010Reinfelder2011)

Majorphytoplanktontaxonomicgroupsdiffer in theefficiencyof their RuBisCO (Ribulose-15-bisphosphate carboxylaseoxygen-ase)activityandoftheircarbonconcentrationmechanisms(CCMs)and thus in their expected response to the rise inCO2 and ocean acidification(Reinfelder2011Tortell2000)Thosephytoplanktonthataremoreefficientattakingupandutilizingcarbon(highersur-facearea tovolume ratiohigherCCMefficiencyhigherRuBisCOspecificityandorlowercarbonrequirements)arehypothesizedtobenefit less from the increase inCO2 as their growth is currentlyleastCO2-limited(Reinfelder2011)CyanobacteriapossessahighlyspecializedCCMinvolvingcarboxysomestodealwithlowdissolvedCO2 levelsandaRuBisCOwithCO2specificitycomparabletothatof chlorophytes (Price Badger Woodger amp Long 2008 Tortell2000)CyanobacteriaarecapableofincreasingtheconcentrationofCO2atthesiteofphotosynthesisover1000timesthelevelsofitssurroundingenvironment(BadgerampPrice2003)whichisanorderofmagnitudehighercarbonconcentrationefficiencythanthenextmostefficientmajortaxonomicgroups(Tortelletal2008)Althoughcyanobacteriaarecapableofincreasingtheirgrowthrateunderel-evatedCO2[egtwospeciestestinFuWarnerZhangFengandHutchins (2007)] themagnitudeof this increase ingrowth isgen-erallyconsideredtobesmallandthuscyanobacteriawouldbeex-pectedtodecreaseincompetitiveabilityunderelevatedCO2 all else being equal However nitrogen-fixing cyanobacteria (diazotrophiccyanobacteria) are found to increase nitrogen fixation under el-evatedCO2andhaveagreater increase ingrowthratethanothergroupsofphytoplankton(Dutkiewiczetal2015)Diazotrophiccya-nobacterialikelydifferfromothercyanobacteriaintheircarbonup-takeandutilizationhoweverpartoftheirlargerresponseandthuspartofthisdifferencebetweendiazotrophsandnonnitrogen-fixingcyanobacteriamaybeattributedtocultureconditionsinwhichni-trogen is completely omittedwhen culturing dizaotrophes for themeasurementofnitrogenfixationbutothernutrientsaresuppliedinabundance(egHutchinsFuWebbWalworthampTagliabue2013)Similarlytoexpectationsforcyanobacteriathatdonotfixnitrogensomediatomshavebeenshowntoexhibitalimitationresponseonly

at CO2 concentrations below present-day levels suggesting thattheyalsohaveahighlyefficientCCM(HopkinsonDupontAllenampMorel2011)howeverotherdiatomsdoappeartohavealargein-creaseingrowthunderfutureCO2conditions(egWuetal2010)ChlorophytesandcoccolithophoreshavealowerRuBisCOspecific-itythandiatomsandlowerCCMefficiencythandinoflagellatesandcyanobacteria but comparable efficiency to thatof diatoms (Priceetal2008Tortell2000)ChlorophytesandcoccolithophoresarethereforeexpectedtobemostlimitedbymoderndayCO2 availabil-ityandwouldthusbeexpectedtobenefitmostfromthe increaseinCO2 and increase in relative abundanceHowever the benefitsof higherCO2 for thephotosynthesis of coccolithophoresmaybeoffsetbyitseffectoncalcificationCalcificationismadecostlierbythedecrease inpHassociatedwith risingatmosphericCO2 levels Calcification incoccolithophores isgenerallyhamperedby theex-tentofacidificationexpectedinthiscenturybuttheeffectsappearto be species-specific (Meyer amp Riebesell 2015) so that it is notclearthatcoccolithophoreswillhaveaconsistentchangeingrowthandabundanceunderelevatedCO2Althoughtherearesubstantivevariationanduncertaintywithinmajortaxonomicgroupsforthesetraits given themajor taxa or species-specific differences in car-bonuptakeandutilizationand thedifferencesbetweencalcifyingand noncalcifying phytoplankton species in response to acidifica-tionitmaybepossibletopredictsomeoftheshiftsincommunityassemblages under increasing CO2 with an expected decrease innondiazotrophiccyanobacteriaanincreaseinchlorophytesandanintermediateresponseofdiatoms

Amodelparametrizedusingameta-analysisofgrowthresponseto increasedCO2 and assuming that this growth responsewill di-rectlytranslateintoproportionalchangesincommunitycompositionhas led to the expectation thatmajor changes in the compositionofcommunitiesshouldbeexpectedwithrisingCO2andthatthesechangeswillexceedthosecausedbywarmingorchangesinnutrientavailability (Dutkiewicz etal 2015) The assumption that growthresponsewill directly translate into proportional changes in com-munitycompositionremainstobetestedDespitetheseimportantdifferences in CO2-related physiology between major taxonomicgroups few studies have focused on how these differences willtranslate into changes in competition between groups and ulti-matelyhowtheyaltercommunitycompositionwithincreasingCO2

Studies of natural assemblages of marine phytoplankton havefoundthathighCO2resultedinanincreaseintheabundanceofthecyanobacterium Synechococcus and a decrease in the abundanceof the coccolithophore Emiliania huxleyi (Paulino Egge amp Larsen2007) Similar experiments also found a decrease in fucoxanthin-containingphytoplanktonincludingdiatoms(Yoshimuraetal2009)or that community composition remains unchanged (Bermuacutedezetal2016)WithintaxonomicgroupsanincreaseinCO2benefitslarger over smaller diatoms (Tortell etal 2008) as expected fromfacilitationofCO2diffusionwith largersurfaceareatovolumera-tiosChangesincompositionofmarinephytoplanktoncommunitiesassociatedwithchangesinCO2concentrationcouldpotentiallybepredictedfrompublishedinformationontheCO2-relatedphysiology

























3emsp |emspRESULTS




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predictable ecological response to rising co2 of a community of...

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