Boosted nutritional quality of food by CO2 enrichment fails to offset energy demand of herbivores under ocean warming, causing energy depletion and mortality

2018·1 MB·English

by  Jonathan Y.S. Leung

ScienceoftheTotalEnvironment639(2018)360–366
ContentslistsavailableatScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
Boosted nutritional quality of food by CO enrichment fails to offset
2
energy demand of herbivores under ocean warming, causing energy
depletion and mortality
JonathanY.S.Leunga,⁎,IvanNagelkerkena,BaydenD.Russella,b,CamiloM.Ferreiraa,SeanD.Connella
aSouthernSeasEcologyLaboratories,TheEnvironmentInstitute,SchoolofBiologicalSciences,TheUniversityofAdelaide,SouthAustralia,Australia
bTheSwireInstituteofMarineScience,SchoolofBiologicalSciences,TheUniversityofHongKong,HongKongSpecialAdministrativeRegion
H I G H L I G H T S G R A P H I C A L A B S T R A C T
• Wetestedifenergytransferviafeeding
isboostedunderfutureseawatercondi-
tions.
• Energy budget of herbivores and
nutritionalqualityoftheirfoodwere
determined.
• Energybudgetraisedbyfeedingonthe
more nutritious food under ocean
acidification.
• When combined with warming,
however,massmortalityoccurreddue
toenergydepletion.
• Enhanced food quality inadequately
offsetstheenergydemandunderocean
warming.
a r t i c l e i n f o a b s t r a c t
Articlehistory: TheCO-boostedtrophictransferfromprimaryproducerstoherbivoreshasbeenincreasinglydiscoveredatnatural
2
Received23March2018 CO ventsandinlaboratoryexperiments.Despitetheemergingknowledgeofthisboostingeffect,wedonotknow
2
Receivedinrevisedform5May2018 theextenttowhichitmaybeenhancedordampenedbyoceanwarming.Weinvestigatedwhetheroceanacidifica-
Accepted13May2018
tionandwarmingenhancethenutritionalquality(C:Nratio)andenergycontentofturfalgae,whichisspeculatedto
Availableonline20May2018
drivehigherfeedingrate,greaterenergybudgetandeventuallyfastergrowthofherbivores.Thisproposalwastested
byobservingthephysiological(feedingrate,respirationrateandenergybudget)anddemographicresponses
Editor:HennerHollert
(growthandsurvival)ofacommongrazinggastropod(Phasianellaaustralis)tooceanacidificationandwarming
Keywords: ina6-monthmesocosmexperiment.Whilstweobservedtheboostingeffectofoceanacidificationandwarming
Fitnessandsurvival inisolationontheenergybudgetofherbivoresbyeitherincreasingfeedingrateonthemorenutritiousalgaeorin-
Gastropod creasingenergygainperfeedingeffort,theirgrowthandsurvivalwerereducedbythesublethalthermalstress
Herbivory underoceanwarming,especiallywhenbothclimatechangestressorswerecombined.Thisreducedgrowthandsur-
Oceanacidification vivaloccurredasaconsequenceofdepletedenergyreserves,suggestingthattheboostingeffectviatrophictransfer
Oceanwarming mightnotsufficientlycompensatefortheincreasedenergydemandimposedbyoceanwarming.Incircumstances
Trophictransfer whereoceanacidificationandwarmingcreateanenergydemandonherbivoresthatoutweighstheenergyen-
hancementoftheirfood(i.e.primaryproducers),theperformanceofherbivorestocontroltheirbloomingresources
likelydeterioratesandthusrunawayprimaryproductionensues.
©2018ElsevierB.V.Allrightsreserved.
⁎ Correspondingauthor.
E-mailaddress:[email protected](J.Y.S.Leung).
https://doi.org/10.1016/j.scitotenv.2018.05.161
0048-9697/©2018ElsevierB.V.Allrightsreserved.
J.Y.S.Leungetal./ScienceoftheTotalEnvironment639(2018)360–366 361
1.Introduction warming)inducedmassmortalityofherbivoresasaconsequenceofen-
ergydepletion,despitethegreaternutritionalqualityoftheirfood.
Giventheglobalaccelerationinanthropogeniccarbondioxideemis-
sion,marineorganismsandtheecosystemsthattheysupportarecon- 2.Materialsandmethods
sideredtobethreatenedbyoceanacidificationandwarming,possibly
altering the functioning of marine ecosystems in the near future 2.1.Experimentalprotocol
(Fabryetal.,2008;NagelkerkenandConnell,2015).However,recent
evidence shows that trophic dynamics in a community may allow Toexaminethedirecteffectsofoceanacidificationandwarmingon
marineorganismsandtheircommunitiestoresisttheimpactsoffuture gastropods,wemeasuredtheirrespirationrate,feedingrateandab-
climate (Goldenberg et al., 2017, 2018). Indeed, the strength of sorptionrate.Theindirecteffectswereobservedbymeasuringthenu-
consumer-resourceinteractionsisoftencriticaltoshapingthestability tritionalqualityoftheirfoodsothattheenergybudgetofgastropods
offoodwebs(May,1973;McCannetal.,1998),particularlywhere wasestimated.Ifoceanacidificationandwarmingcanincreasetheen-
they adjust to stabilize ecosystem processes during environmental ergytransfer,wehypothesizedthat(1)thefeedingrateandenergy
changes (Connell and Ghedini, 2015). Herbivory is a key class of budgetofgastropodswouldbeelevatedunderoceanacidificationso
consumer-resourceinteractionbecauseitdeterminesthefluxofenergy thattheirbodycondition,growthandsurvivalareunaffectedoreven
andmaterialsfromprimaryproducerstoherbivoresandhasthecapac- promoted;(2)theincreasedenergydemandunderoceanwarming
itytocompensateforclimate-drivenchangesinprimaryproduction wouldbeinsufficientlyoffsetwhentheelevatedtemperatureisclose
(Ghedinietal.,2015). tothethermaltoleranceofgastropods,causingreducedbodycondition
Recentstudiesrevealthatthelinksbetweenprimaryproductionand andgrowth;(3)mortalitywouldbeincurredwhenenergydeficitper-
itsconsumptioncanbefacilitatedbyoceanacidificationwhichboosts sists,asindicatedbyreducedbodycondition.Toassessthecircum-
thetrophictransferofcarbonfromprimaryproducerstoherbivores stances where thermal stress is posed on gastropods by ocean
(Goldenbergetal.,2017),sothatthereproductiveoutput(Heldtetal., warming, we determined the performance of aerobic metabolism
2016)andpopulationsizeofherbivorescanbepromoted(Connellet alongatemperaturegradientandcriticalthermalmaximum(CT )
max
al.,2017).Indeed,CO canactasaresourceforprimaryproducersand asaproxyforthermaltolerance(LutterschmidtandHutchison,1997).
2
hencepropagatethroughoutfoodwebs,includingomnivoresandcarni-
vores(Vizzinietal.,2017).Keytounderstandingsuchcommunity-wide 2.2.Experimentalsetup
changesmaycentreonrecognisinghowthenutritionalqualityofpri-
maryproducersmightbeboostedbyCO enrichment(Falkenberget Acommonsubtidalgrazinggastropod,Phasianellaaustralis,was
2
al.,2013,butseeGordilloetal.,2016),possiblyleadingtoensuingfaster chosenasthestudyspeciesduetoitsabundanceinshallowseagrass
feedingrate,greaterenergygainandeventuallybetterfitnessofherbi- androckyreefhabitats(Kinlochetal.,2007).Thisherbivorepredomi-
vores (Cruz-Rivera and Hay, 2001; Hemmi and Jormalainen, 2002; nantlyfeedsonthefilamentousalgaegrowingonsubstratumsurface
GhediniandConnell,2016;Kamyaetal.,2017).Inthisregard,theener- (Keuskamp,2004),whicharecalledturfalgaehereafter(Connellet
geticcostsofoceanacidification(e.g.acid-baseregulationandkinetic al., 2014). Individuals were collected in summer from the subtidal
constraintsoncalcification;Pörtner,2008;Thomsenetal.,2015),may zone (~5–10m depth) at Wirrina Cove, South Australia (35°29′S,
beoffset.SuchindirecteffectofCO (i.e.boostednutritionalqualityof 138°15′E).Mesocosmsystemswereconstructedinaconstanttempera-
2
food)maybeakeymechanismthatallowsherbivorestomaintain tureroom(airtemperature:23°C)toofferamorerealisticsimulationof
theirfitnessandsurvivalunderoceanacidification. thesubtidalhabitat(Goldenbergetal.,2017).Eachmesocosmsystem
Warmingmayalsoenhancethetrophictransferofenergyfrompri- was composed of a large circular mesocosm (1.8m diameter; 1m
mary producers to herbivores via two possible mechanisms. First, depth;~1800L)andasmallenrichmenttank(60L)whereseawater
warmingmayincreasethenutritionalqualityofprimaryproducers pHandtemperaturewereregulated.Twoheadertanks(800L)were
(Renaudetal.,2002;Gordilloetal.,2016),andhenceindirectlypro- madetomaintaintheinflowofseawaterwithpre-treatmentconditions
motestheenergygainofherbivoresviaconsumption.Second,warming tothemesocosms(seeSupplementarymethodforthetechnicaldetails
canelevatethemetabolicrateofherbivores,whichinturnleadsto ofthemesocosmsystem).A2×2crosseddesignofpCO (400ppmvs.
2
greaterfeedingrateandultimatelyenergygain(Brownetal.,2004). 1000ppm)andtemperature(21°Cvs.24°C)wasusedwiththreerep-
Critically,however,suchpositiveinfluenceofwarmingonconsumption licatemesocosmspertreatmentcombination.21°Cistheaveragesea-
dependsonthethermaltoleranceofherbivoresthemselves.Wherethe watertemperatureatthecollectionsiteinsummer,andtheelevated
temperatureexceedstheirthermaltolerance,theenergysupplyfrom pCO andtemperaturelevelssimulatetheRCP8.5scenariofortheyear
2
aerobicmetabolismfallsbelowtheenergydemandforbasalmainte- 2100(IPCC,2013).TheelevatedpCO levelwasachievedbybubbling
2
nance(i.e.energydeficit,Pörtner,2002,2012;Sokolova,2013).Asare- theseawaterintheheadertankswithpureCO andthenmaintained
2
sult, the physiological and behavioural performance of herbivores byaeratingtheseawaterintheenrichmenttankwithCO -enriched
2
deteriorates,leadingtoreducedfitnessandsurvival(Sokolova,2013; airusingagasmixer(Pegas4000MF,ColumbusInstruments,USA).
Leungetal.,2017a).Therefore,thekeyiswhethertheboostedenergy Thedesiredseawatertemperaturewasmaintainedusingtwotitanium
transferfromprimaryproducerstoherbivorescansufficientlycompen- heaters(300W×1and500W×1),whichwereputintotheenrich-
satefortheelevatedenergydemandunderfutureclimaticconditions. ment tank. The mesocosm systems were allowed to run for three
Inthisstudy,weassessedwhetheroceanacidificationandwarming weekstoensurethattheseawaterandhabitatconditionswerestabi-
enhancetheenergytransferfromprimaryproducerstoherbivores, lizedbeforeexperimentation.Theseawatercarbonatesystemparame-
whichcaninturncompensatefortheadditionalenergeticcostsim- tersfortheexperimentalperiodareshowninTableS1.
posedonherbivoressothattheirfitnessandsurvivalcanbesustained. TwentyindividualsofjuvenileP.australis(shelllength:10±3.5mm;
Weusedabioenergetics-basedapproachtoassesswhethertheenergy totalbiomass:4.0±0.25g)weretransferredintoeachmesocosmand
budgetofherbivorousgastropodswaspromotedwhentheyandtheir allowedtoacclimateforoneweekpriortocommencementoftheex-
food were reared at the future levels of ocean acidification and periment.Then,theyweremaintainedinthemesocosmforsixmonths.
warming.Ifthetrophictransferofenergyissufficienttocompensate Turfalgaegrowingonthewallofmesocosmwerethemajorfoodsource
forthedirectnegativeeffectsofoceanwarmingandacidificationon ofP.australisinviewoftheiravailabilityandaccessibility.Grazingtrails
herbivores(i.e.energybudgetismaintainedorenhanced),herbivory cleared of turf algae were observed following consumption by
islikelymaintainedinfuturemarineecosystems.Instead,wefound P.australis,indicatingitsnon-selectivefeedingonturfalgae.Afterthe
thatfuture climate (i.e. thecombination of ocean acidification and 6-monthexposureperiod,mortalitywasdeterminedbycollectingand
362 J.Y.S.Leungetal./ScienceoftheTotalEnvironment639(2018)360–366
enumerating the individuals in each mesocosm (n=3 replicate analysedusingsoftwareeCognition9(Trimble,Germany),whichpro-
mesocosmspertreatment).Anelectronicbalancewasusedtomeasure videshighaccuracyformeasuringspatialcoverage.Feedingratewas
thetotalweightofeachindividualsothatthechangeintotalbiomassin expressedasthedryweightofturfalgaeconsumedperfleshweight
eachmesocosmwasdetermined(n=3replicatemesocosmspertreat- ofgastropodperhour,wherethedryweightofturfalgaeperareawas
ment). Following the experiments for energetics (see Section 2.3 measuredbyscrapingthetilewithascalpeltocollecttheturfalgaein
below), all individuals were dissected to obtain the flesh weight aknownarea,whichwerethenoven-driedandweighed.
whichwasfurtherseparatedintoorganweightandfootweight.The Toestimateabsorptionrate(i.e.energygainbyfeeding),assimila-
organweighttofleshweightratioofeachindividualwascalculatedto tionefficiencywasdeterminedbymeasuringtheorganicmattercon-
indicatebodycondition(Leungetal.,2017b).Theinitialorganweight tentin turf algaeandfaeces. Thefaecesofgastropods in the cages
tofleshweightratiowasobtainedbydissectingadditional20individ- werecollected,rinsedwithdeionizedwateranddriedonapre-weighed
ualsbeforetheexposureperiodsothatthechangeinthisratiocanbe aluminiumfoiltoobtainthedryweightoffaeces.Theash-freedry
calculated.Bodyconditionisimprovedwhenthisratiohaspositive weightsofturfalgaeandfaecesweredeterminedbyweightlossonig-
change,andviceversa.Alltheweightsweremeasuredonafreshweight nitionat550°Cinamufflefurnacefor6hsothatassimilationefficiency
basis.Toassessthenutritionalqualityoffood,turfalgaegrowingonthe wascalculatedusingConoverratio(Conover,1966):
wallofmesocosmwerecollectedfortheanalysisofenergycontentand
Cm:Nenrtaatlioanuaslinysgearb(o2m40b0cSaelorrieimseIIt,ePre(rAkCin-3E5l0m,LeErC,UOS,UA)SA()na=nd3CrHeNplSicealete- AEð%Þ¼(cid:1)1−F0E−0(cid:3)E(cid:1)0F0(cid:3)(cid:2)100
mesocosmspertreatment;2trialsperreplicate),respectively.
whereAEistheassimilationefficiency;F′istheash-freedryweightto
2.3.Energeticsofgastropodsfollowingexposure dryweightratiooffood;E′istheash-freedryweighttodryweight
ratiooffaeces.
Followingthe6-monthexposureperiod,energylossbyrespiration Absorptionratecanthenbecalculatedbymultiplyingthefeeding
andenergygainbyfeedingwereestimatedbecausetheyarethekey ratebyassimilationefficiency,whereasenergybudgetisgivenbyen-
processesdeterminingenergybudgetinmarinemolluscs(Widdows ergygainbyfeedingminusenergylossbyrespiration.Theenergycon-
andJohnson,1988;Wangetal.,2015;Zhangetal.,2015).Tomeasure tentofturfalgaeandaconversionfactorof14.14JmgO−1wereusedto
2
respirationrate,oneindividualwastransferredintoa73mLairtight convertfeedingrateandrespirationrateintoenergyequivalent(Elliott
chamberfilledwithseawateradjustedtotherespectivepCO andtem- andDavison,1975),respectively.
2
peraturelevelsofthemesocosmandallowedtorestfor1htoeliminate
potentialhandlingstress.Then,theseawaterinthechamberwasfully 2.4. Thermal tolerance and aerobic metabolism along a temperature
replacedwithoxygen-saturatedexperimentalseawater(i.e.pCO and gradient
2
temperaturemanipulated)withinitialdissolvedoxygenconcentration
measured by an optical dissolved oxygen probe (Fibox 4, PreSens, Aerobicmetabolismofgastropodswasassessedbymeasuringrespi-
Germany).Thechamberwasthenclosedandputintoawaterbathat rationratefrom15°Cto35°Cwithanincreasingtemperaturerampof
the target temperature so that the temperature of seawater in the 2°Ch−1(Giomietal.,2016),whereasthermaltolerancewasindicated
chamberwasmaintained.After1h,thechamberwasopenedtomea- by CT at which motor coordination is lost (Lutterschmidt and
max
surethefinaldissolvedoxygenconcentrationsofseawater.Twoindi- Hutchison,1997).Theprocedureforthisexperimenthasbeenprevi-
vidualsfromeachmesocosmweretestedandtheaveragerespiration ouslydescribedinLeungetal.(2017a)(seeSupplementarymethod
rate was taken as a replicate for each mesocosm (n=3 replicate forthedetails).
mesocosmspertreatment).Thebackgroundchangeindissolvedoxy-
genconcentrationwascorrectedbyblanksamples(i.e.noindividual 2.5.Statisticalanalysis
inthechamber).Respirationratewasexpressedasoxygenconsumed
perfleshweightperhour,wherethefleshweightwasobtainedfollow- Two-waypermutationalanalysisofvariancewithpCO andtemper-
2
ingdissection.Thesameprocedurewasalsoappliedbeforetheexpo- atureasfixedfactorswasappliedtotesttheireffectsontheaforemen-
sureperiod(i.e.followingthe1-weekacclimationperiod)toexamine tionedresponsevariables(i.e.calorificvalue,C:Nratio,totalbiomass,
thetemporalchangeinrespirationrate,whichcanindicatethehealth mortalityandrespirationrate)witheachmesocosmasareplicate,ex-
statusofgastropodsafterthe6-monthexposureperiod. ceptfororganweighttofleshweightratiowitheachindividualasarep-
Beforefeedingtrials,tileswereputintoeachmesocosmforone licate in view of the large number of individuals used. Given the
monthwhichallowsadequatequantityofturfalgaetogrowonthe substantialmortalityundercombinedelevatedpCO andtemperature
2
tilesurfaceforexperimentation.Tostandardizehungerlevel,gastro- conditions,feedingtrialswerenotperformedforthistreatment.There-
pods in each mesocosm were temporarily transferred into a nylon fore,t-testwasappliedtoexaminetheeffectsofpCO andtemperature
2
meshcagewithoutfood,whichwasthenputbacktotherespective onfeedingrateandenergybudget.
mesocosm.Afterstarvingforoneday,oneindividualwasplacedintoa
clean, tailor-made plastic cage (12cm×12cm×5cm), which 3.Results
containedatile(5cm×10cm)withturfalgaegrowingunderthere-
spectivetreatmentconditions.Onlythetileswithfullcoverageofturf The energy content of turf algae was promoted from 9.8kJg−1
algaewereselectedandusedforthefeedingtrials.Bothendsofthe (control)to15.0kJg−1byelevatedtemperatureand13.9kJg−1by
cagewerecoveredbynylonmeshtoallowcontinuouswaterflow.The combinedelevatedpCO andtemperature(Fig.1a,TableS2).However,
2
individualwasthenputbacktotherespectivemesocosmandallowed pCO inisolationhadnodetectableeffect.C:Nratiowasreducedbyel-
2
tofeedinthecagefor3h.Themesocosmwascoveredwithanopaque evatedpCO atambienttemperature,meaningthatCO enrichmentcan
2 2
tarpsothatthefeedingtrialwascarriedoutinthedark.Twotofourin- increasetherelativenitrogencontentinturfalgae(Fig.1b,TableS2).
dividualsfromeachmesocosmweretestedinseparatecagesandtheir ElevatedtemperaturealsoreducedtheC:Nratioofturfalgaecompared
feedingrateswereaveragedasareplicateforeachmesocosm(n=3 to the control, but this positive effect of nitrogen enrichment was
replicatemesocosmspertreatment).Eachtilewasphotographedata slightlyreducedwhencombinedwithelevatedpCO .
2
fixeddistanceof37cmusingahigh-definitioncamera(CanonEOS TheorganweighttofleshweightratioofP.australisincreasedby~7%
1100D)beforeandafterthefeedingtrialtoestimatethetotalgrazed undercontroland~5%underelevatedpCO conditions,butremained
2
space on the tile (i.e. no turf algae). The photographs were then nearlyunchangedunderelevatedtemperatureinisolation(Fig.2a).
J.Y.S.Leungetal./ScienceoftheTotalEnvironment639(2018)360–366 363
Fig. 1. Energy content and C:N ratio of turf algae growing at different pCO2and
temperaturelevels(mean±S.E.,n=3).N.S.:Notsignificant.
Statistically,thisratiowasreducedbyelevatedtemperature,whilstthe
effectofpCO wasnotdiscernible(TableS2).Yet,thisratiodecreased
2
markedlyby~12%undercombinedelevatedpCO andtemperature
2
conditions,indicatingreducedenergyreservesandbodycondition.
Elevatedtemperature,butnotelevatedpCO ,negativelyimpactedthe
2
increase in total biomass of P. australis in the mesocosms (Fig. 2b,
TableS2).NeitherelevatedpCO nortemperatureinisolationsignifi-
2
cantlyaffectedthemortalityofP.australis(c.f.control),rangingfrom
33%to45%.However,mortalityincreaseddrasticallyto~90%under
combinedelevatedpCO andtemperatureconditions(Fig.2c,TableS2).
2
Comparedtothecontrol,thefeedingrateofP.australisincreasedby
approximately two times at elevated pCO (t=3.81, p=0.019),
2
butremainedinsignificantlychangedatelevatedtemperature(t=
1.58,p=0.189)followingthe6-monthexposureperiod(Fig.3a).As- Fig.2.(a)Changeinorganweighttofleshweightratio(mean+S.E.;n=41individuals
similationefficiency,rangingfrom60%to73%,wasneitheraffectedby for21°C,400ppm,n=40individualsfor21°C,1000ppm,n=32individualsfor24°C,
elevatedpCO (t=0.96,p=0.391)nortemperature(t=2.75,p= 400ppmandn=3individualsfor24°C,1000ppm),(b)changeintotalbiomassand
0.051)(Fig.32b).Comparedtothecontrol,energybudgetwasabout (c)mortalityofP.australisfollowingthe6-monthexposureperiodatdifferentpCO2and
temperaturelevels(mean+S.E.;n=3replicatemesocosms).N.S.:Notsignificant.
three-foldhigheratelevatedpCO (t=4.59,p=0.010)andtwo-fold
2
higheratelevatedtemperature(t=3.37,p=0.028)(Fig.3c).Asignif-
icantnegativecorrelationwasfoundbetweenC:Nratioandfeedingrate whichrepresentstheCT (i.e.upperthermaltolerance)ofP.australis.
max
(Fig.3d),meaningthatthefeedingrateofgastropodshadapositive Respiration rate increased with temperature from 15°C to 25°C
relationshipwiththerelativenitrogencontentoftheirfood. (maximum),abovewhichtherespirationratedeclinedgraduallywith
Afterthe6-monthexposureperiod,therespirationrateofP.australis increasingtemperatureirrespectiveofpCO level(Fig.5).Theeffectof
2
wassubstantiallyreducedbynearly40%undercombinedelevatedpCO pCO onrespirationratewasnotdiscernible.
2 2
andtemperatureconditions(Fig.4,TableS2).Yet,elevatedpCO or
2
temperatureinisolationhadlimitedeffectonthechangeinrespiration 4.Discussion
rate(Fig.S1fortherespirationratebeforeandafterexposure).
Alongan increasing temperature ramp, P.australiswasinactive Enhancedtrophictransferfromprimaryproducerstoherbivores
below 17°C but became more active with increasing temperature maybethekeymechanismallowingherbivorestomaintaintheirpop-
from 17°C to 25°C (Fig. 5). Motor coordination was lost at 27°C ulations under ocean acidification and warming (Boyd and Brown,
364 J.Y.S.Leungetal./ScienceoftheTotalEnvironment639(2018)360–366
Fig.3.(a)Feedingrate,(b)assimilationefficiencyand(c)energybudgetofP.australisunderdifferenttreatmentconditions(mean+S.E.;n=3);(d)Relationshipbetweenfeedingrateof
P.australisandC:Nratioofturfalgae.Control:21°C,400ppm;OA:21°C,1000ppm;Temp:24°C,400ppm.
2015;RosenblattandSchmitz,2016).Here,wedemonstratedthatthe Ithasbeenwell-recognizedthatoceanacidificationdisruptstheen-
boostingeffectthroughtrophictransferelevatestheenergybudgetof ergyhomeostasisofmarineorganisms,especiallycalcifyingmolluscs,
acommonmarineherbivoreunderoceanacidificationorwarmingin becausetheyrequireextrametabolicenergyforacid-baseregulation
isolation,whichisfavourableforlong-termsurvival.However,suchin- andcalcification(Pörtner,2008;Thomsenetal.,2015).Inaddition,re-
directpositiveeffectwasoverwhelmedbythedirectnegativeeffectof ducedpHcanunderminetheirfeedingperformance,energygainand
theseclimatechangesstressorsincombination,leadingtoasubstantial eventuallygrowth(Fabryetal.,2008;Gazeauetal.,2013;Leungetal.,
declineinfitnessandsurvival. 2015). Nevertheless, we found that ocean acidification has little
Fig.4.ChangeinrespirationrateofP.australisfollowingthe6-monthexposureperiodat Fig.5.RespirationrateofP.australisalonganincreasingtemperaturerampfrom15°Cto
differentpCO2andtemperaturelevels(mean+S.E.;n=3).N.S.:Notsignificant. 35°CatdifferentpCO2levels(mean±S.E.;n=3).
J.Y.S.Leungetal./ScienceoftheTotalEnvironment639(2018)360–366 365
influenceonthebodycondition,biomassandsurvivalofP.australis, aerobicmetabolismshouldbepromotedtoprovidesufficientmetabolic
suggestingthatenergyhomeostasiswasmaintained.Inotherwords, energyformoleculardefencemechanisms,suchasenhancedproduc-
theelevatedenergydemandunderoceanacidificationwasprobably tionofheatshockproteinsandantioxidativeenzymes(Pörtner,2002;
offsetbytheincreasedfeedingrateandhenceenergygain.Basedon Somero,2002;Tomanek,2010).However,theaerobicmetabolismof
themetabolictheoryofecology(Brownetal.,2004),increasedfeeding gastropodsdroppedsubstantiallyundercombinedelevatedpCO and
2
ratecanbedrivenbyelevatedmetabolicrate,asshowninsomegrazing temperature conditions (c.f. elevated temperature in isolation),
gastropods(Mertensetal.,2015;McSkimmingetal.,2016),buttheres- implyingnotonlyinsufficientmetabolicenergyforbasalmaintenance,
pirationrateofourstudygastropodwasnotupregulatedbyoceanacid- butalsoimpairmentincellularfunctions(e.g.energyproductionby
ification (Fig. S1), meaning that the feeding rate is not driven by mitochondria)(Pörtner,2002;Sokolovaetal.,2012).Theconsiderable
metabolic rate. We suggest that the increased feeding rate under reductioninmetabolicenergywouldworsenoverallbiologicalperfor-
oceanacidificationismediatedbythereducedC:Nratioofturfalgae, mance(Pörtner,2012;Sokolova,2013),includingfeeding(Mertenset
whichcouldbeattributedtothehigherassimilationofnitrogenor al.,2015).Althoughwedidnotexaminefeedingrateduetothemass
moreefficientphotosynthesisthatallowsreallocationofnitrogenin mortality, energy reserves (i.e. organ weight to flesh weight ratio)
metabolicprocesses(Zou,2005;Hurdetal.,2009;Kochetal.,2013; weremarkedlyreduced,indicatingacriticalmismatchbetweenenergy
Xuetal.,2017).Asnitrogenisoftenlimitingforherbivores(Mattson, gainandenergydemand.Usingenergyreservesonlyprovidestempo-
1980),thehigherrelativenitrogencontentinturfalgaecanenhance raryreliefunderadverseenvironmentalconditionsandismaladaptive
the feeding rate of gastropods, as also shown in other herbivores inthelongterm(Sokolova,2013).Whenenergyreservesaredepleted,
(Falkenberg et al., 2013; Ghedini and Connell, 2016; Kamya et al., vitalcellularfunctionsandphysiologicalprocesseswillbearrested,cul-
2017).Regardlessoftheunderlyingmechanism,weshowedthatthein- minatinginmortalityandthusaffectingpopulationpersistence(Leung
creasedfeedingrateonthemorenutritiousturfalgaepromotesenergy etal.,2017a).Weproposethatthisenergetics-basedmechanismis
budget,ultimatelyenablingthegastropodstomaintainfitnessunder fundamentaltoaccountingforthecombinednegativeeffectsofocean
oceanacidification.Indeed,suchboostingeffectthroughtrophictrans- acidificationandwarmingonthefitnessandsurvivalofmarineorgan-
fercouldoutweighthedirectnegativeeffectsofoceanacidification isms,asobservedincorals(Pradaetal.,2017),bivalves(Talmageand
(Falkenbergetal.,2013;Kamyaetal.,2017),andevenboostthepopu- Gobler,2011;Ivaninaetal.,2013)andgastropods(Melatunanetal.,
lationofherbivoresasobservedundernatural(Connelletal.,2017; 2013).
Vizzinietal.,2017)andmesocosmconditions(Goldenbergetal.,2017). Herbivoryisafundamentalcomponentofecosystemstabilitybe-
Oceanwarminginisolationwasalsoshowntoenhancetheenergy causeitnotonlydeterminesthefluxofenergyandmaterialsfrompri-
budget of gastropods, but their body condition and biomass were maryproducerstoherbivores,butalsohasthecapacitytocompensate
lowerthanthoseinthecontrol,suggestingthatlessenergywasallo- forclimate-drivenchangesinprimaryproduction(PostandPedersen,
catedtogrowth.Thermaltoleranceisoftentheoverridingfactordeter- 2008;Ghedinietal.,2015).Indeed,thestabilityoffoodwebsoftenre-
miningtheeffectofelevatedtemperatureonaerobicscope(orenergy flectssuchconsumer-resourceinteractions(May,1973;McCannetal.,
budget)andhencegrowth.WefoundthattheCT ofP.australisap- 1998)andtheircapacitytoadjusttoenvironmentalchanges(Connell
max
pearsat27°Cwheremotorcoordinationislostandrespirationrateis andGhedini,2015).Wedemonstratedthatfutureclimate(i.e.ocean
declining.Assuch,aerobicscopeandoverallperformancearedimin- acidificationandwarming)canincreasethenutritionalqualityofpri-
ishedaccordingtotheoxygen-andcapacity-limitedthermaltolerance maryproducerstoboosttheenergybudgetofherbivores.However,
concept(Pörtner,2002,2012).Topreventthisacutethermalstress,lo- wefoundthatthispositiveeffectonfoodqualitycouldbeoverwhelmed
comotoryactivitywasmaximizedat25°Castheavoidancebehaviour. bytheelevatedenergydemandofoceanacidificationandwarmingon
Since the respiration rate at elevated temperature (i.e. 24°C) was theherbivoresthemselves,leadingtoreducedfitnessandsurvival.In
closetothemaximumat25°C,thegastropodslikelysufferedfromsub- such situations, theloss of trophic compensation mayincrease the
lethalthermalstressinthemesocosms,whichcanreduceenergybud- chance of ecosystem collapse (e.g. climate-driven collapse of kelp
getandgrowthinthelongterm(Pörtner,2002,2012;Sokolova,2013; forests,Connelletal.,2018).Whilstherbivorescouldmaintaintheirho-
Gianguzzaetal.,2014;Leungetal.,2017a).Tocompensateforthe meostasisunderincreasinglystressfulconditions(GhediniandConnell,
greaterenergydemandatelevatedtemperature,energygainbyfeeding 2016),furtherincreaseinstressinevitablycrossatippingpointatwhich
shouldbepromoted,butourstudygastropodfailedtoincreasefeeding theincreasingmetaboliccostscausethiscompensatorymechanismto
ratepossiblyduetothesublethalthermalstress(Leungetal.,2017a). fail.Assuch,theinnatecapacityofherbivorestocontroltheirblooming
Nevertheless,thehigherenergycontentofturfalgaeincreasesenergy resourcesfailsandrunawayprimaryproductionislikelytoensue.
gainperfeedingeffortandhenceenergybudget,whichhelpsoffset
theelevatedenergydemandunderoceanwarming.Despitetheadvan-
Acknowledgements
tageofthisboostingeffect,growthwasstillretarded,implyingthatthe
energybudgetofgastropodsisallocatedmostlytosomaticmaintenance
SupportwasprovidedbytheIPRSScholarshipfromtheUniversityof
andlesstogrowthandreproductionbasedonthedynamicenergybud-
AdelaidetoJ.Y.S.L.,anAustralianResearchCouncilDiscoveryProgram
getmodel(Nisbetetal.,2012).Indeed,survivalundersublethalthermal
granttoB.D.R.andS.D.C.(DP150104263),andARCFutureFellowships
stressrequiresadisproportionateenergyallocationforsomaticmainte-
toS.D.C.(FT0991953)andI.N.(FT120100183).
nancebecausecellularandstructuraldamagecanalreadybeinflicted
(Pörtner,2002;Somero,2002).Forexample,productionofheatshock
AppendixA.Supplementarydata
proteins, which incurs substantial energy demand, is upregulated
undersublethalthermalstresstorepairdamagedproteinsandstabilize
Supplementarydatatothisarticlecanbefoundonlineathttps://doi.
denaturingproteins(Milleretal.,2009;Tomanek,2010).Consequently,
org/10.1016/j.scitotenv.2018.05.161.
theboostingeffectviatrophictransferwasinadequatetofullycompen-
sateforthedirectnegativeeffectsofsublethalthermalstressonenergy
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