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TropicalforestresponsestoincreasingatmosphericCO2:currentknowledgeandopportunitiesforfutureresearchLucasA.
CernusakA,H,KlausWinterB,JamesW.
DallingC,JosephA.
M.
HoltumB,D,CarlosJaramilloB,ChristianKrnerE,AndrewD.
B.
LeakeyC,RichardJ.
NorbyF,BenjaminPoulterG,BenjaminL.
TurnerBandS.
JosephWrightBASchoolofMarineandTropicalBiology,JamesCookUniversity,Cairns,Qld4878,Australia.
BSmithsonianTropicalResearchInstitute,POBox0843-03092,Balboa,Ancon,RepublicofPanama.
CDepartmentofPlantBiology,UniversityofIllinois,Urbana-Champaign,Urbana,IL61801,USA.
DSchoolofMarineandTropicalBiology,JamesCookUniversity,Townsville,Qld4811,Australia.
EInstituteofBotany,UniversityofBasel,Basel,CH-4056,Switzerland.
FEnvironmentalSciencesDivisionandClimateChangeScienceInstitute,OakRidgeNationalLaboratory,OakRidge,TN37831,USA.
GLaboratoiredesSciencesduClimatetdel'Environnement,GifsurYvetteFrenchCentreNationaldelaRechercheScientique,theAtomicEnergyCommissionandtheUniversityofVersaillesSaint-Quentin,91191,France.
HCorrespondingauthor.
Email:lcernusak@gmail.
comAbstract.
ElevatedatmosphericCO2concentrations(ca)willundoubtedlyaffectthemetabolismoftropicalforestsworldwide;however,criticalaspectsofhowtropicalforestswillrespondremainlargelyunknown.
Here,wereviewthecurrentstateofknowledgeaboutphysiologicalandecologicalresponses,withtheaimofprovidingaframeworkthatcanhelptoguidefutureexperimentalresearch.
Modellingstudieshaveindicatedthatelevatedcacanpotentiallystimulatephotosynthesismoreinthetropicsthanathigherlatitudes,becausesuppressionofphotorespirationbyelevatedcaincreaseswithtemperature.
However,canopyleavesintropicalforestscouldalsopotentiallyreachahightemperaturethresholdunderelevatedcathatwillmoderatetheriseinphotosynthesis.
Belowgroundresponses,includingnerootproduction,nutrientforagingandsoilorganicmatterprocessing,willbeespeciallyimportanttotheintegratedecosystemresponsetoelevatedca.
Wateruseefciencywillincreaseascarises,potentiallyimpactinguponsoilmoisturestatusandnutrientavailability.
Recruitmentmaybedifferentiallyalteredforsomefunctionalgroups,potentiallydecreasingecosystemcarbonstorage.
Whole-forestCO2enrichmentexperimentsareurgentlyneededtotestpredictionsoftropicalforestfunctioningunderelevatedca.
Smallerscaleexperimentsintheunderstoreyandingapswouldalsobeinformative,andcouldprovidesteppingstonestowardsstand-scalemanipulations.
Additionalkeywords:carbonstorage,CO2enrichment,liana,phosphorus,succession,wateruseefciency.
Received20October2012,accepted21March2013,publishedonline16May2013IntroductionTheriseinatmosphericCO2concentration(ca)causedbyhumanindustrialisationisunprecedented,rapidandubiquitous.
Likeallvegetationonearth,tropicalforestsexistedunderacalessthan300partspermillion(ppm)foratleast800000yearsbeforethestartofthe20thcentury(Lüthietal.
2008).
Thecarosefrom300ppmearlyinthetwentiethcenturyto392ppmin2011,andprojectionsforintermediateemissionsscenariossuggestitcouldexceed800ppmbytheyear2100(IntergovernmentalPanelonClimateChange2011).
BecauseCO2istheprimarysubstrateforphotosynthesis,thisdramaticincreaseincawillundoubtedlyaffectthemetabolismoftropicalforestsworldwide.
Thequalitativeandquantitativeexpressionofsucheffects,however,islargelyunknownandrepresentsamajorsourceofuncertaintythatlimitsourcapacitytounderstandtropicalecosystemprocesses,assesstheirvulnerabilitiestoclimatechangeandimprovetheirrepresentationinEarthsystemmodels.
Tropicalforestsplayasignicantroleintheglobalcarboncycle.
Theycontainabouthalfthecarbonstoredinplantbiomassintheterrestrialbiosphereandaccountforaboutone-thirdofglobalterrestrialproductivity(Fieldetal.
1998;MalhiandGrace2000;Royetal.
2001;Beeretal.
2010;Panetal.
2011;Saatchietal.
2011).
Ingeneral,responsestoelevatedcahavebeenstudiedfarlessintropicalforeststhanintemperateforests(Hoganetal.
1991;Storketal.
2007;Krner2009;Luoetal.
2011;Leakeyetal.
2012).
Thisgapinresearcheffortmaypartlyreectthechallengesassociatedwithstudyingtropicalforestcommunities,giventheirlargestatureandbiologicalcomplexity,andlogisticalCSIROPUBLISHINGFunctionalPlantBiology,2013,40,531–551Reviewhttp://dx.
doi.
org/10.
1071/FP12309JournalcompilationCSIRO2013www.
publish.
csiro.
au/journals/fpbchallengesassociatedwithconductingresearchintropicalenvironments.
FreeairCO2enrichment(FACE)experimentsconductedintemperateforestsindicatedthatenrichingcato550ppmcauseda23%increaseinnetprimaryproductivity(NPP)comparedwiththatobservedatambientcaof~380ppm(Norbyetal.
2005),withoneexperimentshowingasubsequentdecreaseto9%NPPstimulationcausedbylimitednitrogenavailability(Norbyetal.
2010).
NoFACEexperimenthasbeenconductedinatropicalforestforcomparisonsofar.
Tropicalecosystemsdifferfromtemperateecosystemsinimportantclimatic,edaphic,oristicandecologicalattributes,andthesearelikelytoinuencehowtheyrespondtorisingca.
Hightropicaltemperaturesincreasethepotentialforstimulationofnetphotosynthesis(A)byelevatedcathroughsuppressionofphotorespirationcomparedwithpredictionsforcoolertemperateandborealecosystems(Farquharetal.
1980;Long1991).
Ontheotherhand,ithasbeenarguedthattropicalforestplantsmaybenearahightemperaturethreshold,beyondwhichAcoulddecline(DoughtyandGoulden2008;Doughty2011).
ItisnotknownhowthenegativeeffectsofhightemperatureonAwillinteractwiththepositiveeffectsofhighca.
Inaddition,itispossiblethatbiomassproductionandthecompetitiveabilityoftropicalcanopytreesarenotcarbon-limitedatthecurrentca,suchthatincreasingAmayhavelittleinuenceonoverallgrowthperformance(Krner2003,Krner2009).
FACEexperimentshaveindicatedthatnitrogenavailabilityplaysanimportantroleinconstrainingproductivityresponsestoelevatedcaintemperateforests(NorbyandZak2011).
However,nitrogenavailabilityishighinmanytropicalforests(Hedinetal.
2009;Brookshireetal.
2012).
Phosphorusorsomeotherrock-derivednutrient,ratherthannitrogen,couldpresenttheprimarynutritionalconstraintongrowthresponsestoelevatedcaintropicalecosystems(Quesadaetal.
2010;Vitouseketal.
2010).
Shiftsinoristiccompositionduetoelevatedcaexposuremayalsobemoreimportantintropicalecosystems.
Forexample,woodyclimbingplants(lianas)andpotentiallyN2-xinglegumesarefarmoreabundantintropicalforeststhanintemperateforests.
Functionaltype-specicresponsesinthesegroupscouldhavesignicantconsequencesfortropicalforeststructureandfunctionunderelevatedca,ascouldanincreasingabundanceoflight-woodedandrelativelyshort-livedpioneerspecies.
Weexploretheseissuesinmoredetailbelow,andhighlightthechallengesandopportunitiesassociatedwithtacklingthemexperimentally.
Ourgoalistoprovideaframeworkthatcanbeusedtoguidefutureexperimentalresearchaimedatunderstandinghowwoodyplantsintropicalforestswillrespondtorisingca.
Conjectureandspeculationarenecessaryingredientsinthisendeavour,duetotherelativelysmallamountofresearchthathasthusfarbeenconductedintotropicalforests'responsestoelevatedca.
EffectsofelevatedcaonleafgasexchangeInthissection,wediscusstheeffectsofelevatedcaonleaf-levelA,typicallyexpressedasCO2uptakeperunitleafareaperunitoftime.
Foraxedleafareaindex,anincreaseinAwillcauseaproportionalincreaseingrossprimaryproductivity(GPP).
GPPdescribestherateofphotosyntheticcarbonuptakefromtheatmospherebyaplantcanopy,typicallyexpressedperunitofgroundareaperunitoftime.
ElevatedcagenerallycausesAtoincreaseinplantsthatusetheC3photosyntheticpathway(LloydandFarquhar1996;Drakeetal.
1997).
Theoverwhelmingmajorityoftropicalwoodyplantsusethisphotosyntheticpathway,withnotableexceptionsinthegeneraEuphorbia(PearcyandTroughton1975)andClusia(Holtumetal.
2004).
Anexampleoftheshort-termresponseofAtocaisshowninFig.
1foraseedlingofaC3tropicalpioneertree,FicusinsipidaWilld.
(K.
Winter,unpublished).
ThemeasurementsweremadeundernearoptimalconditionsforphotosynthesisinatropicalC3plant.
Fig.
1clearlyshowsthepotentialforsignicantincreasesinAinresponsetorisingca.
Inprinciple,theAoftropicalwoodyplantshasgreaterpotentialtorespondpositivelytoelevatedcathanthatofplantsathigherlatitudes,asaresultofthehigherleaftemperaturesassociatedwithtropicalclimates.
RubiscoistheprimarycarboxylatingenzymeinC3plants.
CompetitionbetweenCO2andO2attheactivesitesofRubiscocausestheenzymetocatalysethexationofbothofthesesubstrates.
FixationofO2byRubiscoleadstothereleaseofCO2frommitochondriathroughtheprocessofphotorespiration.
Asleaftemperatureincreases,thespecicityofRubiscoforxingCO2insteadofO2decreasesandthesolubilityofCO2relativetoO2alsodecreases.
Therefore,photorespirationincreasesasaproportionofgrossphotosynthesiswithincreasingleaftemperature(Farquharetal.
1980;Long1991).
Ontheotherhand,photorespirationcanbesuppressedbyincreasingtheconcentrationofCO2relativetothatofO2aroundtheactivesitesofRubisco.
TheupshotisthatthereisgreateropportunitytoincreasenetCO2uptakebysuppressingphotorespirationathighertemperatures.
FurtherpredictionsresultingfromconsiderationofRubiscokineticsthatarerelevanttotropicalforestresponsestoelevatedcaare:(1)thetemperatureoptimum4030201000200400Ambient[CO2](ppm)6008001000PPFD1500molm–2s–1Netphotosynthesis(molm–2s–1)FicusinsipidaFig.
1.
NetphotosynthesisofaleafofaFicusinsipidaseedlinginresponsetovariationintheCO2concentration([CO2])oftheairsurroundingtheleaf.
Measurementsweremadeataleaftemperatureof30Candaphotosyntheticphotonuxdensity(PPFD)of1500mmolm–2s–1(K.
Winter,unpublished).
532FunctionalPlantBiologyL.
A.
Cernusaketal.
forAshouldincreasewithincreasingca;(2)theproportionalincreaseinthemaximumquantumyieldofCO2uptakecausedbyelevatedcashouldincreasewithincreasingleaftemperature;and(3)theproportionaldecreaseinthelightcompensationpointcausedbyelevatedcashouldbelargerathigherthanatlowerleaftemperatures(Farquharetal.
1980;Long1991).
ThesepredictionsoftheinteractionbetweenelevatedcaandtemperatureattheleaflevelarealsoapparentwhenAisscaleduptothecanopy(Long1991).
Asaresult,ecosystemmodelsgenerallypredictalargerproportionalstimulationofNPPinwarmtropicalclimates,comparedwithcooler,higherlatitudes.
Forexample,aglobaldynamicvegetationmodelemployingamodiedversionoftheFarquharetal.
photosynthesismodel(Farquharetal.
1980;Collatzetal.
1991)predicteda35%increaseinNPPfortropicalforestsatcaof550ppmrelativetothatatcaof370ppm,whereasthepredictedincreasefortemperateforestswas26%.
ThisgeographicdifferenceinthesimulatedproportionalstimulationofNPPwaslargelycausedbypredicteddifferencesinphotorespiration,assumingsufcientnutrientandwateravailabilitytosupportincreasedNPP(Hickleretal.
2008).
Ontheotherhand,theproportionalincreaseinAinresponsetocamaybedampedifenvironmentalconditionsarenototherwisefavourableforphotosyntheticgasexchange.
Onereasonthismightoccurisifthestomataclosetoslowtherateofwaterlossfromleaves.
Stomatalconductance(gs)typicallydecreasesinresponsetoincreasingleaf-to-airvapourpressuredifference(VPD),andAtypicallyshowsalinearorcurvilinearrelationshipwithgs(Wongetal.
1979;CernusakandMarshall2001;Cernusaketal.
2011a;Medlynetal.
2011).
Thus,areductioningscausedbyincreasedVPDwillalsocauseareductioninA,withtheproportionalreductioninAlikelytobesomewhatlessthanthatings(FarquharandSharkey1982).
TheVPDcanvaryasafunctionofthevapourpressureoftheairsurroundingtheleaforasafunctionofthevapourpressureinsidetheleaf.
Becausethevapourpressureinsideleavesisassumedtobeatornearsaturation,itiseffectivelycontrolledbyleaftemperature.
Thus,foraxedvapourpressureoutsidetheleaf,theVPDincreasesexponentiallyasleaftemperatureincreases,andgsandAarelikelytodecreaseaccordingly(SageandKubien2007;LloydandFarquhar2008).
Leaftemperaturesintropicalforestsareexpectedtoincreasewithincreasingcaasaresultofincreasingairtemperatureandtheincreasingelevationofleaftemperatureaboveairtemperature.
AirtemperatureisexpectedtoincreaseduetotheradiativeeffectsofCO2andothergreenhousegasesintheatmosphere,andduetodecreasedevapotranspiration(Sellersetal.
1996).
Overthelastcentury,theglobalaveragesurfacetemperatureincreasedby0.
74C,accompanyinganincreaseincafrom280ppmto380ppmbetween1750and2005(Solomonetal.
2007).
Intropicalforestregions,therateofsurfacewarmingsincethemid-1970shasaveraged0.
26Cperdecade(MalhiandWright2004).
Attheleaflevel,gstypicallydeclinesinresponsetoelevatedca(Wullschlegeretal.
2002;AinsworthandRogers2007),althoughnotalways(KrnerandWürth1996;Keeletal.
2007).
Declininggsinresponsetoelevatedcahasbeenobservedinseedlingsandsaplingsoftropicaltreespecies(Berrymanetal.
1994;Goodfellowetal.
1997;Cernusaketal.
2011b).
AnexampleoftheresponseofgstogrowthatelevatedcomparedwithambientcaisshowninFig.
2afortheseedlingsof10tropicaltreespecies.
Here,itcanbeclearlyseenthatgsgenerallydecreasedinresponsetoelevatedcabuttheresponsewasvariableamongspecies.
Lowergsresultsinalowertranspirationrate(E),causinganincreaseinleaftemperature(Fig.
3a,b),withassociatedincreasesinVPD(Fig.
3c,d).
ManytropicalforesttreesdisplayapronouncedmiddaydepressioninbothgsandAonsunnydays(RoyandSalager1992;Kochetal.
1994;Zotzetal.
1995;Ishidaetal.
1999;Kosugietal.
2009).
Thishasalsobeendetectedatthecanopyscalewitheddycovariancemeasurements(Gouldenetal.
2004;DoughtyandGoulden2008;Kosugietal.
2008).
ItcoincideswiththehighVPDassociatedwithincreasingleaftemperaturesunderhighirradiance(Fig.
4).
ThemiddaydepressioningsandAoccursindependentlyofsoilmoisturestatus(Kosugietal.
2009).
Forexample,thedatashowninFig.
4wererecordedduringtherainyAlbiziaadenocephalaChrysophyllumcainitoCoccolobauviferaDalbergiaretusaHyeronimaalchorneoidesAmbient[CO2](400ppm)Elevated[CO2](700ppm)(a)(b)StomatalconductancetoH2O(molm–2s–1)IngapunctataOrmosiamacrocalyxPachiraquinataSchizolobiumparahybumSwieteniamacrophylla0.
00.
20.
40.
60.
80.
00.
51.
01.
52.
02.
5Whole-plantwater-useefficiency(gCkg–1H2O)Fig.
2.
(a)Stomatalconductanceand(b)whole-plantwateruseefciencyforseedlingsof10tropicaltreespeciesgrownatambientandelevatedCO2concentrations([CO2]).
DataaretakenfromCernusaketal.
(2011b).
Tropicalforestsandelevated[CO2]FunctionalPlantBiology533PPFD=2000molm–2s–1404550Airtemperature=40°CAirtemperature=35°CAirtemperature=30°CAirtemperature=25°C(a)PPFD=1000molm–2s–1(b)Leaftemperature(°C)202530354020PPFD=2000molm–2s–14567(c)PPFD=1000molm–2s–1(d)Leaf-to-airvapourpressuredifference(kPa)123Stomatalconductance(molH2Om–2s–1)0.
00.
10.
20.
30.
40.
50.
60.
10.
00.
20.
30.
40.
50.
60.
7Fig.
3.
(a,b)Predictedleaftemperatureand(c,d)leaf-to-airvapourpressuredifferenceasafunctionofstomatalconductanceatairtemperaturesrangingfrom25Cto40C.
(a,c)predictionsforanincidentphotosyntheticphotonuxdensity(PPFD)of2000mmolphotonsm–2s–1;(b,d)predictionsforaPPFDof1000mmolphotonsm–2s–1.
Calculationswereperformedusingleafenergybalance(CampbellandNorman1998),assumingarelativehumidityof50%,awindspeedof1.
5ms–1andaleafwidthof10cm.
seasoninPanama,whensoilmoisturewashigh.
Thus,ascacontinuestoriseoverthecomingcentury,higherVPDcausedbyhigherleaftemperaturescouldcausemiddaydepressionsofgsandAtooccurmorefrequentlyandforlongerperiodsduringtheday.
ThiswoulddampenthepositiveresponseofAtorisingca,althoughanoverallincreaseinAisstillpredicted(LloydandFarquhar2008).
NonstomataleffectscanalsolimitAathighleaftemperatures.
Thelight-saturatedpotentialelectrontransportrateappearstohaveatemperatureoptimumof~40Cintropicaltreeleaves(Lloydetal.
1995;Mercadoetal.
2006).
Thus,AwouldbeexpectedtodecreaseforagivenchloroplasticCO2concentrationatleaftemperatureshigherthan40C.
Exposuretoleaftemperatureshigherthan45CcancausedenaturationofRubiscoandotherphotosyntheticenzymes(BerryandBjrkman1980).
Necrosisandtissuedeathtypicallyoccurafterexposuretoleaftemperaturesbetween50and53C(Krauseetal.
2010).
Sun-exposedoutercanopyleavesinatropicalforestreachedtemperaturesbetween46Cand48C,suggestingtheymaybeoperatingneartheirlimitofheattoleranceundercurrentconditions(Krauseetal.
2010).
AninsituwarmingexperimentrecentlydemonstratedthatAintropicaltreeandlianaleaveswassignicantlyreducedbyawarmingof2–3Covera13-weekperiod,withtheleaftemperaturesofwarmedleavesreaching45C(Doughty2011).
Thisiswithintherangeofleafwarmingthatcouldbeexpectedtooccurinresponsetoelevatedcainthenextfewdecades.
ThereductioninAwasattributedmainlytononstomatallimitations.
Ithasbeensuggestedthatelevatedcacouldmitigatetheadverseeffectsofelevatedtemperaturesonthephotosyntheticperformanceoftropicaltreeleaves(Hoganetal.
1991)throughthesuppressionofphotorespirationandtheassociatedalleviationofphotoinhibitionunderhighirradiance(Kriedemannetal.
1976;Rasinenietal.
2011).
Furthermore,thegsoftropicaltreeseedlingswasobservedtodeclinelessinresponsetoincreasingleaftemperatureforseedlingsgrownunderelevatedcacomparedwiththosegrownunderambientca(Berrymanetal.
1994).
Thus,elevatedcahasthepotentialtoalleviateboththestomatalandnonstomatallimitationsonAassociatedwithhighleaftemperatures.
Futureexperimentsthatexposetropicaltreeleavestobothwarmingandelevatedcawillbecriticalfortestingthishypothesisfurther.
Growthunderelevatedcahasbeenshowntocauseacclimationofphotosyntheticcapacityinarangeofspecies,generallyexplainedbyreducedRubiscoactivity,whichisoftencorrelatedwithreducedleafnitrogenconcentrations(Drakeetal.
1997).
Ingeneral,thistypeofacclimationallowsplantstooptimiseoverallperformancebybalancingsinkandsourceactivity.
Forexample,whenRubiscoexpressionisreduced,nitrogencanbereallocatedawayfromthephotosynthetic534FunctionalPlantBiologyL.
A.
Cernusaketal.
2500200015001000500015105007911131517195Timeofday(hour)79111315171914534920.
332.
8(a)(b)(c)(d)9June199430June1994Netphotosynthesis(molm–2s–1)PPFD(molm–2s–1)PseudobombaxseptenatumFig.
4.
Netphotosynthesisandincidentphotosyntheticphotonuxdensity(PPFD)ofoutercanopyleavesofatallPseudobombaxseptenatum(Jacq.
)DugandtreeinParqueNaturalMetropolitano,RepublicofPanama,on(a,c)asunnydayand(b,d)onanovercastday.
(a,b)PPFDonthe2days;(c,d)netphotosynthesis.
Numbersinsidethepanelsshowthesummationsoftheshadedareasunderthecurvesinmolm–2day–1forPPFDandmmolm–2day–1fornetphotosynthesis(K.
Winter,unpublished).
apparatustostructuressuchasnerootsthatallowincreasednutrientforaging(Mooreetal.
1999;Longetal.
2004).
InFACEexperimentswithtemperateforesttrees,themaximumRubiscocarboxylationvelocitydecreasedby~7%inresponsetogrowthatcaelevatedto200ppmaboveambientCO2concentration(AinsworthandLong2005).
Withthisloweredphotosyntheticcapacity,light-saturatedphotosynthesiswasstillstimulatedby47%intheelevatedcatreatments.
Sofar,nocomparabledatahavebeencollectedintropicalforesttrees.
TheaboveconsiderationssuggestthatbothstomatalandnonstomatallimitationsonAwillincreasewithincreasingleaftemperaturesintropicalcanopies,andthereisfurtherpotentialforacclimationordownregulationofphotosyntheticcapacitytobalancesourceandsinkactivity.
ThenatureandextentoftheinteractionbetweentheselimitationsandthepositiveeffectsofelevatedcaonAandGPPintropicalforestswillhavefar-reachingconsequencesfortropicalforestfunctionunderelevatedca.
EffectsofelevatedcaongrowthNPPisthenetamountofcarbonxedintoorganicmatterinagiventimeafteraccountingforautotrophicrespiration(Eqn1):NPPGPPRa;1whereRaisautotrophic(plant)respiration.
NPPcanbecalculatedasthechangeinplantmassovertimeplusnonrespiratorycarbonlosses(i.
e.
tissueturnover,reproduction,herbivory,exudationoforganiccompoundsfromroots,biogenicvolatileemissions,etc.
),suchthatNPP=dM/dt+L,whereMisthemassofcarboninaplantoracommunityofplants,tistime,dM/dtischangeinmassoverchangeintime,andLisnonrespiratorycarbonlosses(LloydandFarquhar1996).
Thus,anincreaseinNPPmayormaynotleadtoanincreaseinecosystemcarbonstorageinplantbiomass(denotedbyM),dependingonhowNPPispartitionedbetweendM/dtandL.
Fromthefewdatasetssofarpublished,tropicalforestsappeartofunctionwitharelativelylowcarbonuseefciency(ChambersandSilver2004;Malhi2012),denedastheratioofNPPtoGPP.
ThisindicatesproportionallyhighRaandthepotentialforashiftinRatosignicantlyaffectNPP(Metcalfeetal.
2010).
Todate,littleisknownaboutwhetherorhowRawillbeaffectedbyelevatedcaintropicalforests.
Increasingtemperatureorincreasingsupplyofrespiratorysubstratesassociatedwithincreasingcacouldbeexpectedtocauseanincreaseinmaintenancerespiration(Leakeyetal.
2009;Clarketal.
2010).
Ontheotherhand,responsestotemperaturemaybetemperedbyacclimation,suchthatmaintenancerespirationratesareaffectedlittlebyagradualshiftintemperatureregime(Atkinetal.
2005).
Nitrogenallocationtotropicaltreeleaveswasobservedtodecreaseunderelevatedca(Berrymanetal.
1993;Winteretal.
2000;Cernusaketal.
2011b),andthiscouldcauseadecreaseinleafmaintenancerespirationatagiventemperature(Ryan1995;Gonzàlez-Meleretal.
2009).
Tropicalforestsandelevated[CO2]FunctionalPlantBiology535LeafdarkrespirationcomprisesmorethanathirdoftotalRaintropicalforests(ChambersandSilver2004;Cavalerietal.
2008).
Notsurprisingly,thewayRaistreatedinecosystemmodelshasalargeimpactonpredictionsofthetropicalforestNPPresponsetorisingca,especiallywithregardtothetemperaturedependenceofRa(Galbraithetal.
2010).
Shiftingallocationpatternscouldaffecthowthechangeinbiomassovertime,dM/dt,respondstoelevatedcaintropicalforests.
Inarticialtropicalminiecosystems,itwasobservedthatAnearlydoubledunderelevatedca.
However,theextraphotosynthateproducedintheelevatedcatreatmentwasmostlyallocatedtoincreasednerootproductionandrootexudation,therebyincreasingL,ratherthantoabovegroundbiomassandcoarseroots,whichwouldhaveacceleratedtheincreaseinM(KrnerandArnone1992).
Similarresponseswerealsoobservedinsometemperateecosystems(Krneretal.
2005;Norbyetal.
2010),asoriginallyforeshadowedbyStrainandBazzaz(1983).
Acrossabroadrangeoftropicalforestplots,atradeoffwasobservedbetweenNPPallocationtonerootproductionversusallocationtowoodproduction,withallocationtothecanopyremainingrelativelyinvariant(Malhietal.
2011).
ThissuggeststhatincreasedallocationtonerootproductionunderelevatedcacouldcauseLtoincreaseattheexpenseofincreasedallocationtotheproductionoflong-livedwoodytissues,whichwouldcauseMtoincrease.
MuchofthecontroloverdM/dtinplantshastraditionallybeenattributedtochangesinA.
Thishasrecentlybeentermeda'carbon-centric'perspective(Salaetal.
2012).
Alternatively,ithasbeensuggestedthatdemandforphotosynthateatthesitesofnewtissuesynthesiscouldexertgreatercontroloverdM/dtthandoesA(Krner2003).
ThiswouldrequirethatthecarbohydratesproducedbyAinexcessoftheirconsumptionbyanabolicprocessesmustbelostfromtheplantthroughRaorL.
Undersuchascenario,itisalsolikelythatsomefractionoftheexcessphotosynthatewouldaccumulateasnonstructuralcarbohydrates(NSC).
Thus,analysisoftheNSCconcentrationsintreescouldprovideasensorthatindicatescarbonshortageorsurplusforfuellinganabolicmetabolism(Krner2003).
AsteadyandveryhighNSCconcentrationwouldindicatethatthecurrentlevelofAprovideseitherafullyadequatesupplyoranoversupplyofreducedcarboncompoundstotheplant.
InaseasonalforestinPanama,NSCconcentrationswereobservedtobesteadythroughtheyearortoincreaseduringthedryseason(Newelletal.
2002;Würthetal.
2005).
ThiswasinterpretedtosuggestthatdM/dtwasnotlimitedbyA(Krner2003;Würthetal.
2005).
IncreasingcaaroundthecanopyleavesatthesamesiteledtoincreasesinAandinNSCconcentrations(Würthetal.
1998b;Lovelocketal.
1999),butdidnotaffectthegrowthratesofbranches.
ThisfurtherreinforcedtheideathatgrowthwillnotrespondtoincreasedAinthesetrees,althoughincreasedgrowthintheseasonfollowingexposuretoelevatedcacouldnotberuledout(Lovelocketal.
1999).
Thisinterpretationwasnotsupportedbytheresultsofanotherexperimentatthesamesite,inwhichsupplementallightingwasprovidedtocanopytreesundercloudyskies.
Inthatcase,growthincreased,whichwasdrivenbyincreasesinA(Grahametal.
2003).
Adenitivetestofthehypothesiswillrequirelonger-termexperimentsonwoodyspeciesgrowingunderelevatedcaintropicalforests.
ItwasrecentlysuggestedthatNSCmayplayanimportantphysiologicalroleinmaintainingtheintegrityofthevascularsystemoflargewoodyplants(Salaetal.
2012).
ItwasalsosuggestedthatincreasedallocationtotheNSCpoolmaybeageneralresponsetostress,indicatingmoreseverecarbonlimitationtogrowth,ratherthanviceversa(WileyandHelliker2012).
Further,highsolublesugarconcentrationsintheleavesmayimprovetheirabilitytophotosynthesiseathightemperatures(Hüveetal.
2006).
Iftheseassertionsarecorrect,theremaynotbeadirectnegativerelationshipbetweenthesizeoftheNSCpoolandtheabilityoftropicaltreesandlianastoincreasegrowthinresponsetoelevatedca.
Ontheotherhand,ifNSCconcentrationsaregenerallyhigh,andthisreectsanoversupplyofcarbonforgrowthsuchthatgrowthwillnotrespondtoastimulationofA(KrnerandArnone1992;Baderetal.
2010),thisshouldbeincorporatedintocoupledclimate–carbonmodels,whichtreatcarbonreservepoolsverysimply,ifatall.
Growthatlownutrientavailabilityconsistentlyreducesthepercentagegrowthresponsetoelevatedca(McMurtrieetal.
2008).
Thispatternwasdemonstratedinexperimentswithseedlingsofmanytropicaltreespecies(Oberbaueretal.
1985;ReekieandBazzaz1989;Ziskaetal.
1991;Lovelocketal.
1998;Winteretal.
2000;Winteretal.
2001a,2001b;Cernusaketal.
2011b;deOliveiraetal.
2012),althoughsomeexceptionsalsooccurred(KrnerandArnone1992;ArnoneandKrner1995;Carswelletal.
2000).
Overall,itislikelythatnutrientavailabilitywillplayamajorroleindeterminingtheproductivityresponsesofwoodytropicalforestplantstorisingca.
Nitrogenappearstoberelativelyabundantintropicalforests,asindicatedbyhighratesofnitrogenloss(Hedinetal.
2009;Brookshireetal.
2012)andincreasingratesoflong-termatmosphericnitrogendeposition(Chenetal.
2010;Hietzetal.
2011).
However,vastareasoftropicalforestsoccuronold,stablelandscapes(e.
g.
largepartsofSouthAmerica,Africa,South-EastAsiaandAustralia).
Intheseregions,severelyphosphorus-impoverishedsoils,aresultofprolongedweatheringinmoistclimates(Lambersetal.
2008),presentamajorconstraintonplantgrowth(Vitouseketal.
2010).
ItwasrecentlydemonstratedthattotalsoilphosphorusstatuswasthemeasureofsoilfertilitythatbestpredictedvariationinproductivityacrossawiderangeofAmazonianforestplots(Quesadaetal.
2012).
Inadditiontolowphosphorusavailabilityintropicalsoils,anapparentlinkbetweentranspirationandphosphorusacquisitionmayfurtherdiminishtheconcentrationsofphosphorusinplanttissuesascarises(Cernusaketal.
2011c).
Ontheotherhand,ithasbeenarguedthatphosphorusavailabilityanduptakecouldbemaintainedunderrisingcabythestrongbufferpowerofsoilsforinorganicphosphorus,andbyincreasedcarbonallocationtomycorrhizalfungiandotherspecialisedmechanismsforphosphorusacquisition(Lovelocketal.
1996;Lloydetal.
2001;LloydandFarquhar2008;Turner2008).
Organicphosphorusisabundantintropicalforestsoils(Johnsonetal.
2003;Vincentetal.
2010;TurnerandEngelbrecht2011)andmayfurthersupportanyincreasedgrowthoftropicalforesttreesunderelevatedca.
Althoughphosphorusislikelytobethenutrientthatconstrainsproductivityintropicalforestsingeneral,itisalsoworthpointingoutthatconsiderableheterogeneityexistsacrossthetropicalbiomesuchthatothernutrientscanalsobelimiting.
For536FunctionalPlantBiologyL.
A.
Cernusaketal.
example,nitrogenappearedtolimitproductivityintropicalforestsonveryyoungandveryoldsoils(Fyllasetal.
2009;Mercadoetal.
2011),inrecentlyestablishedsecondaryforests(Davidsonetal.
2007)andintropicalmontaneforests(Tanneretal.
1998).
RecentresearchhasshownthatthecapacityfornitrateassimilationintheshootsofC3plantsdecreasesunderelevatedcaasaresultofdecreasedphotorespiration(Rachmilevitchetal.
2004;Bloometal.
2012).
Ifthispatternextendstowoodytropicalforestplants,thelimitationsimposedontropicalforestproductivitybynitrogenavailabilitycouldincrease.
Othernutrientsmayalsoplayimportantrolesinregulatingproductivityintropicalforests,forexample,calcium,molybdenumandpotassium(Vitousek1984;Barronetal.
2009;Wrightetal.
2011),andtheiravailabilitycouldalsoconstrainproductivityresponsestoelevatedca.
ItisclearthattherearemanyunresolvedissuesassociatedwithpredictingwhetherandtowhatextenttropicalforestNPPwillbestimulatedbyfutureincreasesinca.
Tropicaleldexperimentsareurgentlyneededtoaddresstheseissues(Leakeyetal.
2012).
EffectsofelevatedcaonresistancetodroughtBothseasonalandinterannualdroughtssignicantlyimpactupontheproductivityandspeciescompositionoftropicalforests(Conditetal.
1995;Engelbrechtetal.
2007;Nepstadetal.
2007;Brandoetal.
2008;Phillipsetal.
2009;daCostaetal.
2010).
Elevatedcacouldmakewoodytropicalforestplantsmoreabletowithstanddroughtintwoways.
First,elevatedcacouldincreasewateruseefciency(WUE),therebyallowingagreateramountofphotosynthesisforagivenamountofwatertranspiredtotheatmosphere(Eamus1991;Winteretal.
2001a;Battipagliaetal.
2013).
Thiscouldleadtoareductioninsoilwaterdepletionduetoreducedcanopy-scaletranspiration,whichcouldsustaintranspiration,andthereforephotosynthesis,foralongertimebetweenrainevents(Morganetal.
2004;Keeletal.
2007;LeuzingerandKrner2007;HoltumandWinter2010;LeuzingerandKrner2010;Macinnis-Ngetal.
2011).
Suchwatersavingscouldalsofacilitatemicrobialactivityandnutrientprovision,andenableturgorpressureinmeristemtissuestoremainabovethecriticalthresholdrequiredforcellexpansion(Boyer1968;Eamusetal.
1995),therebyfacilitatinggrowth.
Second,elevatedcacouldincreasetheNSCpool,which,inturn,couldbeusedtosustainplantmetabolismforlongerperiodsfollowingstomatalclosureandcessationofAinresponsetodrought,accordingtothecarbon-centricperspective(Salaetal.
2012).
BecauseAtendstoincreaseunderelevatedcaforagivengs,leaf-levelWUEtypicallyincreases.
Leaf-levelWUEcanbedenedastheratioofphotosynthesistotranspiration,A/E.
A/EcanbedenedastheratioofthediffusiongradientforCO2tothatforwatervapourbetweentheexternalairandtheintercellularairspacesintheleaf(FarquharandRichards1984):AEca1cica1:6VPD;2whereciistheintercellularCO2concentration.
Thefactor1.
6inthedenominatoristheratioofthediffusivityofwatervapourtothatofCO2inthestomatalpores.
Eqn(2)showsthatifci/caremainsconstant,A/Ewillincreaseproportionallywithincreasingca,solongasVPDisalsoconstant.
IfVPDalsoincreasesascaincreases,assuggestedabove,thiswilldamptheresponseofA/Etoincreasingca(Bartonetal.
2012).
Variationinci/cainresponsetoelevatedcacanbeassessedinstantaneouslybymeasuringchangesintheCO2andwatervapourconcentrationsofairpassingoveraleaf(vonCaemmererandFarquhar1981).
Inaddition,time-integratedassessmentsofci:cacanbeobtainedbymeasuringcarbon-isotopediscrimination(D13C)inplantbiomass(Farquharetal.
1982).
AlthoughEqn(2)appliesattheleaflevel,theincreaseinWUEunderelevatedcaisalsomanifestedatthewhole-plantlevel,asshowninFig.
2bforseedlingsof10tropicaltreespecies.
MeasurementofD13Cprovidesanopportunitytoexaminethehistoricalresponsesofci/catoincreasingcaintropicaltreessincepreindustrialtimes.
ThiscanbeaccomplishedbyanalysingD13Cintreeringsorinleafdrymatterpreservedinherbaria.
Thefewstudiesconductedsofarontropicaltreesshowthatci/catendedtoremainconstantascaincreasedfrompreindustrialtopresentconcentrations(Hietzetal.
2005;Nocketal.
2011;Bonaletal.
2011;Loaderetal.
2011),orthatci/cadecreasedinatropicaldryforesttreespecies(Brienenetal.
2011).
Bothtrends(constantci/caanddecreasingci/ca),wouldindicatelargeincreasesinA/Eascaincreasedfrom280ppmto380ppmifVPDalsoremainedconstant.
However,historicalchangesinVPDaremoredifculttodetermine.
Asnotedabove,decreasinggsinresponsetoincreasingcashouldleadtoanincreaseinleaftemperatureassociatedwithadecreaseinevaporativecoolingoftheleafbytranspiration(Fig.
3).
ThiscouldleadtoanincreaseinVPD,whichwouldthendampentheincreaseinA/Ecausedbyincreasingca.
Overall,itseemslikelythatA/Ehasincreasedoverthepastcenturyandwillcontinuetoincreaseascaincreases.
Thissuggestionisconsistentwiththeresponseofwhole-plantWUEtoelevatedca,asshowninFig.
2b,becausethewhole-plantresponseincorporatestheincreaseinVPDassociatedwithlowergs.
ItiscriticaltodeterminehowstomatalresponsestocaandVPDarelikelytoinuenceevapotranspiration,cloudformationandprecipitationpatternsintropicalregionsascarises.
Atthecontinentalscale,anincreaseinWUEintropicalforestscouldhaveimportantimplicationsforthehydrologicalcycle,includingincreasedrunoff(Gedneyetal.
2006).
IfWUEincreasesmorethanNPP,excesswaterislikelytoenterriverinesystems.
Thiscouldaccelerateweatheringprocessesandtheexportofsedimentsandassociatednutrientstotheocean.
Conversely,adecreaseintheamountofwaterreturnedtotheatmospherebytranspirationcouldcauseadecreaseincloudformationandprecipitation(Bettsetal.
2004).
Modelsprovideanopportunitytoinvestigatethiscomplexweboffeedbackoverdecadaltocentennialtimescales(Luoetal.
2011).
Assessmentofhistoricalchangesinci/cathroughanalysesofD13Candexperimentalinvestigationsoftheresponsesofgsandci/catoelevatedcaprovideameanstoparameteriseorconstrainsuchmodels(Buckley2008;deBoeretal.
2011;Prenticeetal.
2011).
GrowthunderwaterdecitgenerallycausesNSCconcentrationstoincrease,andthismaybebecausecellexpansionismoresensitivetowaterstressthanisA(Hsiao1973;Chavesetal.
2003;Mulleretal.
2011).
This,combinedwiththeconsiderationsdescribedabove,ledKrner(2009)topredictthatfortropicaltrees,'CO2wouldhavefewifanyeffectsTropicalforestsandelevated[CO2]FunctionalPlantBiology537underperiodicdrought,giventhetendencyforgrowthtobecontrolledbycarbonsinkswhenwaterisinshortsupply.
'ThispredictionisbasedontheideathattheNSCpoolrepresentsapassiveoveroworrepositoryforcarbonsupply.
However,ithasbeenshownexperimentallythatgrowthcanrespondtoelevatedcaunderwaterdecitintropicaltreeseedlings(Cernusaketal.
2011b).
Seedlingsoftwotropicaltreespeciesweregrownatambientandelevatedca,andatavolumetricsoilwatercontentof0.
27or0.
08m3m–3.
Thelowwatersupplywassufcienttoreducegstolessthanhalfthatobservedathighwatersupply.
Thepercentageincreaseinplantbiomasscausedbygrowthatelevatedcomparedwithambientcawaslargeronaveragefortheplantsgrownunderwaterdecitthanforthewell-wateredplants.
Thisagreeswiththeresultsobtainedfortemperatewoodyplantseedlingsandsaplings,whichalsoshowedpositivegrowthresponsestoelevatedcaunderwaterdecit(TolleyandStrain1984;Arpetal.
1998;Centrittoetal.
1999),althoughnotineverycase(Guehletal.
1994;Duursmaetal.
2011).
ThesizeoftheNSCpoolinplantsgenerallyincreasesinresponsetoelevatedca(Drakeetal.
1997;AinsworthandLong2005).
Therehasrecentlybeendebateaboutwhetherdrought-inducedtreemortalityintheabsenceofbioticagentsresultsfromcarbonstarvation,hydraulicfailure,impairedcarbontranslocationoracombinationoftheseprocesses(McDowelletal.
2008;Salaetal.
2010;Andereggetal.
2012).
Totheextentthatdrought-inducedmortalitycanbedelayedbyhavingalargerreserveofNSC,elevatedcashouldallowtropicalwoodyplantstosurviveforlongerperiodsunderdrought.
Ontheotherhand,thismaynotbethecaseintropicaltreeswithsunlitcanopiesifNSCstorageisalreadyhighunderpresent-dayca(Newelletal.
2002;Krner2003;Würthetal.
2005).
ThusitmaybetheheavilyshadedindividualsintheunderstoreythatbenetmostfromhigherNSCconcentrationsascarises(Würthetal.
1998a;LloydandFarquhar2008).
Theinteractionbetweenpotentiallyincreasingdroughtfrequencyandintensityintropicalforestsandpotentiallyincreasingabilitytowithstanddroughtunderelevatedcawillplayacriticalroleindeningtheoverallresponseofcarboncyclingintheseecosystemsascarises.
IncreasedWUEwasoneofthemostconsistentlyobservedresponsestoelevatedcainpottedtropicaltreeseedlings(Ziskaetal.
1991;Eamusetal.
1993;Winteretal.
2001a;HoltumandWinter2010;Cernusaketal.
2011b).
Experimentsarenowrequiredtobuildupontheseinitialresults,involvingwoodytropicalforestplantsgrowingintheirnativesoilenvironmentsandexposedtoeithernaturallyoccurringorexperimentallyimposeddroughtsincombinationwithelevatedca.
EffectsofelevatedcaonspeciescompositionMuchuncertaintysurroundingthefunctioningoftropicalforestsunderelevatedcaderivesfrompotentialshiftsinforestcomposition.
Althoughitiscurrentlyunknownhowchangesinspeciesregenerationsuccessunderelevatedcawillalterthefuturecarboncyclingoftropicalforests,thepotentialeffectsmaybelarge.
Forexample,spatialvariationinspeciescompositionwithinthesingleforesttypeofthe50-haplotonBarroColoradoIslandinPanamawasassociatedwithvariationinstandingdrybiomassrangingfrom180Mgha–1to440Mgha–1(Chaveetal.
2003).
Inafurtheranalysisofcompositionaleffectsonecosystemfunction,Bunkeretal.
(2005)showedthatarangeofpotentialextinctionscenariosinuencingtreespecieswithdifferentfunctionaltraitscouldresultindeclinesincarbonstorageofupto70%onBarroColoradoIsland.
Clearly,theimportanceofcaeffectsonspeciesregenerationsuccessshouldberecognisedandinvestigatedasacriticaldriveroffuturecarboncycling.
Thelargestimpactonforestcompositionandassociatedcarbonstoragewillariseifforestdisturbanceregimesarealtered.
Inmaturetropicalforests,typicaladulttreemortalityratesare1–2%oftreesdyingperyear(Lewisetal.
2004),withtheresultingdisturbancetotheforestcanopyrangingfromsingletreefallgapstolargecanopyopenings.
Tropicalforestplantspeciesliealongacontinuumfromextremelyshade-toleranttoabsolutelylight-demanding(Wrightetal.
2005).
Themostshade-tolerantrecruitandsurviveeverywhere.
Themostlight-demandingspecieswillonlyrecruitinlargeforestopenings.
Whereassmallforestdisturbancesoftenresultinthereplacementofcanopytreesbyslow-growingshade-tolerantjuvenilescharacterisedbyhighwooddensityandlargeadultstature,largerdisturbancesresultingfrommultipletreefallsfavourtheinitialrecruitmentoffast-growing,light-demandingpioneerspecies,generallycharacterisedbyalowwooddensityandashortlifespan(SwaineandWhitmore1988).
Elevatedcamayinuenceforestdisturbanceregimesinthreeways.
First,elevatedcamaycauseforestturnoverratestoincreaseifthereisanincreaseincompetitioncausedbyhigherresourceavailability(i.
e.
CO2)(Lewisetal.
2009a;BugmannandBigler2011).
Second,increasesinsurfacetemperatureareexpectedtoresultinstrongerconvectionalstorms,suchasthosethatpropagateacrosstheAmazonbasin(Nelsonetal.
1994;Garstangetal.
1998;Knutsonetal.
2010).
Eventhoughthesestormsarerareevents(Glooretal.
2009;Lloydetal.
2009),theycanproducecanopyblow-downsextendingoverhundredstothousandsofhectares,resultinginlargepatchesofearlysuccessionalvegetation(Negron-Juarezetal.
2010).
Third,moresevereorfrequentclimateanomalies(Timmermannetal.
1999;Neelinetal.
2006)canresultinbiome-wideincreasesinadulttreemortality.
ThesewereobservedintheAmazonbasinfollowingseveredroughtin1997(Williamsonetal.
2000)andin2005(Phillipsetal.
2009),andareinferredtohavealsooccurredin2010(Lewisetal.
2011).
Dependingonthespatialdistributionoftreemortalitywithinthestand,theseeventshavethepotentialtopromotethewidespreadrecruitmentofpioneerspecies.
Elevatedcamayalsopromotetheregenerationofpioneerspeciesintheabsenceofchangesinforestdisturbancebyinuencingthecompetitivebalancebetweenearlyandlatesuccessionalspeciesingaps.
Forsmall-seededpioneers,acriticalltertorecruitmentsuccessissurvivalthroughtheearlyestablishmentphase(DallingandHubbell2002).
Germinatingseedsandemergingseedlingsareparticularlysusceptibletodrought-inducedmortalityduringshortdryspells(Engelbrechtetal.
2006;Dawsetal.
2008),andsmallseedlingscanbesmotheredbyfallinglitter(DallingandHubbell2002).
Elevatedcamaypromoteseedlingestablishmentifitacceleratesseedlinggrowthandeffectivelyshortensthisvulnerableestablishmentperiodoramelioratestheeffectsofshort-termdroughtbyincreasingWUE.
538FunctionalPlantBiologyL.
A.
Cernusaketal.
Seedlingsestablishinginnewlyformedgapsalsofacecompetitionfrompre-existingrecruitsofshade-tolerantspecies(advanceregeneration)andpotentiallyfromadulttreesthatsurroundthegapandcontributetothelateralin-llingofthecanopy.
Ifseedlinggrowthratesarenotconstrainedbynutrientavailability,thehighermaximalassimilationratesofpioneersrelativetoshade-tolerantspeciesshouldtranslatetoagreatergrowthstimulationandcompetitiveadvantage(Oberbaueretal.
1985).
Thismaybeampliedbygreaterstimulationofphotosynthesisduringsunecks,whichdominateunderstoreylightenvironments(Leakeyetal.
2002).
Conversely,elevatedcamayintensifycompetitionbetweenpioneerrecruitsandtheadvanceregeneration.
Elevatedcahasbeenshowntosignicantlyenhancethegrowthofshade-tolerantseedlingsunderverylowlightconditions(Würthetal.
1998a)andmaybeexpectedtoalsoenhanceseedlingsurvival.
Growthenhancementsarealsolikelytobestrongforshade-tolerantlianaspeciesthatawaitgapformationtorecruittothecanopy(Krner2009).
Lianasappeartobeincreasingintropicalforestsoverrecentdecades(Phillipsetal.
2002;Wrightetal.
2004;SchnitzerandBongers2011).
Thischangeinthefunctionalcompositionoftropicalforestsmaybetheresultofrisingca(Lewisetal.
2009a;SchnitzerandBongers2011)orotherprocessessuchasshiftingdynamicsofseeddispersalcausedbyhuntingthatfavourspredominantlywind-dispersedlianasoverpredominantlyanimal-dispersedtrees(Wrightetal.
2007).
BothlianaandtreeseedlingshavebeenshowntoprotfromelevatedCO2whengrownindeepshade(Krner2009).
Beneaththecanopy,lianasarelikelytoexhibitbetterlightforagingperunitofcarbongainedthantreesaplings,duetotheirexiblegrowthstrategy.
Thisprovidesahypothesisedmechanismbywhichlianascouldbenetmorefromelevatedcathantrees(Krner2009).
Shouldlianasbecomemorevigorousduetoafunctionaltype-specicbenetfromelevatedca,thiswouldhavefar-reachingconsequencesforcarbonstorage(Phillipsetal.
2002).
Lianainfestationsincreasetreemortalityandsuppresstreegrowth,whereaslianasthemselvesallocaterelativelylittlebiomasstowood.
Woodylegumesarebothabundantanddiverseintropicalforests,especiallyintheNeotropicsandAfrica(Gentry1988;LososandLeigh2004;terSteegeetal.
2006).
SomeoftheseleguminoustreeandlianaspecieshavetheabilitytoformbacterialnodulesontheirrootsthatcanxatmosphericN2(deSouzaMoreiraetal.
1992;Sprent2009).
Suchspeciesmaybeabletorespondmorestronglytoelevatedcathannonxingspecies,especiallyinnitrogen-poorsoils(Thomasetal.
1991;Tissueetal.
1997;Cernusaketal.
2011b).
Anabilitytoacquirenitrogenfromtheatmospheremayalsoprovideanadvantageforphosphorusacquisitionbypromotingproductionofnitrogen-richphosphataseenzymesinroots(Houltonetal.
2008).
Suchenzymescanbeboundtorootsurfacesorreleasedintotherhizospheretohydrolyseorganically-boundphosphorus,makingitavailableforplantuptake(Richardsonetal.
2005;Turner2008).
Ontheotherhand,apan-tropicalincreaseinnitrogendeposition(Chenetal.
2010;Hietzetal.
2011)mightlimittherelativeadvantageoflegumesoverplantspeciesthatareincapableofN2xation.
Inaninsituexperimentinatropicalforestunderstorey,anodulatedlegume,TachigaliversicolourStandl.
&L.
O.
Williams,hadagrowthresponsetoelevatedcasimilartothatofnonlegumes(Würthetal.
1998a).
However,demandfornitrogenislowinplantsindeepshadeandthebenetofN2xationmaythereforebegreatestinagapenvironment(McHargue1999;Barronetal.
2011).
Futureexperimentsontheresponsesofnodulatedlegumestoelevatedcashouldconsiderinteractionswithirradiance.
IncreasedcarbonallocationtoreproductionwasobservedfortemperatetreesexposedtoFACE(LadeauandClark2006;Wayetal.
2010).
Increasedreproductiveeffortunderelevatedcaintropicalforestscouldhaveimportantconsequencesforlong-termpopulationdynamics.
Inaddition,increasedcarbonallocationtoshort-livedtissues,suchasowersandfruits,wouldnotleadtothesameincreaseincarbonstorageasincreasedallocationtowood.
Asignicantincreaseinowerproductionhasbeenobservedover18yearsinatropicalforestinPanama(WrightandCalderon2006).
Ifthispatternisrelatedtoincreasingca,thismayportendfurtherincreasesincarbonallocationtoreproductionascacontinuestorise.
TheLatePaleocene–EoceneThermalMaximum(PETM)wasaglobalwarmingeventthatoccurred~56millionyearsago,inwhichtheglobalmeantemperaturerapidlyincreasedby~5Cin~10000years(Zachosetal.
2003).
Thisglobalwarmingeventwasassociatedwithalargeinjectionofgreenhousegasesintotheatmosphereandariseincato~1000ppm.
ThePETMmayprovideahistoricanalogueforanthropogenicclimatechange,althoughthelatterisoccurringatamuchfasterrate.
PollenassemblagesinthreestratigraphicsectionsineasternColombiaandwesternVenezuelademonstratedanincreaseinthediversityoftropicalwoodyplantsinresponsetothePETM(Jaramilloetal.
2010).
Importantly,thePETMwasassociatedwithanintensicationofthehydrologicalcycle,whichprobablyresultedineitherincreasedprecipitationinthetropicsoratleastnoincreaseinaridity(Jaramilloetal.
2010;ClementzandSewall2011).
Itisnotknowntowhatextentsimilarconditionswillprevailasanthropogenicclimatechangeunfolds.
Nevertheless,thediversicationoftropicalwoodyplantsinresponsetothePETMprovidesanextremelyvaluableinsightintopotentialresponsesoftropicalforeststoelevatedcaandclimatechange.
Currently,ourabilitytopredictchangesinthespeciescompositionoftropicalforestsunderelevatedcaispoorforatleastfourreasons:(1)temperateecosystemshavebeenthefocusofmostofresearchefforttodate;(2)elevatedcaeldstudieshavefocussedoneven-agedstandswheregapdynamicsandgapregenerationwereabsent;(3)manystudiesofseedlingshavefeaturedplantsthatwereisolatedfromecologicalinteractionsorgrownwithadisturbedsoil–microbe–plantcomplex;and(4)thetraitsthatdrivevariationinresponsetoelevatedcaarenotwellunderstoodingeneral,particularlyintropicalspecies(Leakeyetal.
2012;LeakeyandLau2012).
EffectsofelevatedcaonecosystemcarbonstorageForestshavebeenasignicantcarbonsinkinrecentdecades,bothgloballyandinthetropics(Lewisetal.
2009b;Panetal.
2011).
Althoughitislikelythatrisingcahasplayedatleastsomeroleindrivingtheincreaseintropicalforestbiomass(Lewisetal.
2009a),severalothermechanismsmayalsohavecontributed.
ThesepossibilitiesincludesecondarysuccessionTropicalforestsandelevated[CO2]FunctionalPlantBiology539onabandonedagriculturallands,recoveryfromotheranthropogenicuses,includingtimberandrewoodextraction,andincreaseddepositionoflimitingnutrientsresultingfromanthropogenicactivities.
Ofthecarbonstoredintropicalforests,morethanhalfisinlivebiomass(Panetal.
2011).
Repeatedcensusesofforestinventoryplotsovertimehaveindicatedthatlivebiomassisincreasinginsomeold-growthtropicalforests.
Theaverageannualisedchangeinabovegroundbiomass(AGB)in79plotsinAfricantropicalforestswasabout+0.
6MgCha–1peryearduringtheperiod1968–2007(Lewisetal.
2009b).
Similarly,theaverageAGBchangeacross59Amazonianplotswasabout+0.
6MgCha–1peryearfromthe1980suntiltheearly2000s(Bakeretal.
2004).
Theglobalterrestrialcarbonsinkof~2PgCperyearforthe1990s(Solomonetal.
2007)impliesanincreaseinecosystemcarbonstorageof~0.
2MgCha–1peryear,ifitwerespreadevenlyovertheglobalvegetatedlandsurface.
Krner(2009)suggestedonecouldoptimisticallyallowforthreetimesmoremissingcarbontobelocatedintropicalforeststhaninextratropicalregions.
Thus,forarstapproximation,theestimatedincreaseinAGBof0.
6MgCha–1peryearisseeminglyconsistentwiththecarbonbalanceoftheEarthsystem.
Aboutone-thirdofcarbonstoredintropicalforestsisinsoilorganicmatter(Panetal.
2011).
Themeanresidencetimeforsoilorganicmatterissimilartothatforlivebiomassintropicalforests,ontheorderof10–15years(Malhietal.
1999).
Thisdiffersmarkedlyfromhighlatitudeforests,wherethemeanresidencetimeforsoilorganicmattercanbe10timeslongerthanthatforlivebiomass.
Littleisknownabouthowelevatedcawillaffectsoilcarbonstorageintropicalforestsascarises.
IncreasedNPPunderelevatedcacouldacceleratethedecompositionofsoilorganicmatterthroughaprimingeffect,inwhichincreasedlitterfallprovidesthecarbonthatfuelsthemicrobialdecompositionofsoilorganicmatter(Sayeretal.
2011).
However,likeotherresponsesoftropicalforeststoelevatedCO2,soilprimingeffectsappeartoberegulatedbynutrientavailability(Nottinghametal.
2013).
Ingeneral,smallchangesinsoilcarbonaredifculttodetect,andeventhelongestmanipulativeexperimentsmaynotprovidesufcienttimefordirectionalchangestobedetected.
FACEexperimentsconductedwithtemperateforesttreesprovideanimportantsourceofinformationtodrawuponwhenconsideringthelikelyresponsesofecosystemcarbonstorageintropicalforestsinresponsetorisingca.
Inexperimentsconductedinyoungforeststands,therewaseitherasustainedincreaseinAGBthroughthefullcourseoftheexperiment(McCarthyetal.
2010);ortherewasatransitoryincreaseinAGB,withtheincreaserestrictedtotherstfewyearsoftheexperiment,andanincreasedallocationtonerootproductionandincreasedcarboninthesoil(Norbyetal.
2010).
Ina100-year-olddeciduousforest35mtall,therewasnoincreaseinbasalareaincrementduring8yearsofFACE(Krneretal.
2005).
Theseexperimentsdemonstratenoconsistentevidenceforsustainedincreasesintemperateecosystemcarbonstorageunderelevatedca(NorbyandZak2011).
IncreasedNPPcausedbyelevatedcacouldpotentiallybeassociatedwithlesscarbonstorageintropicalforestsifspeciescompositionshiftsinfavouroflianasandshorter-lived,fastergrowingtreespecieswithlowerwooddensity(Phillipsetal.
2002;Krner2004;Lauranceetal.
2004;Krner2009).
ThecurrentdistributionofAGBandNPPacrossAmazoniaindicatesanegativerelationshipbetweenthetwo,suchthatmoreproductiveforeststendbeofalowerbiomass(Malhietal.
2006;Saatchietal.
2011).
HighermortalityratesandlowerwooddensitybothcontributetothelowerAGBintheAmazoniansiteswithhigherNPP(Malhietal.
2006).
Lianainfestationsincreasetreemortality(Putz1984;Ingwelletal.
2010),especiallyoflatesuccessionaltreespecies(SchnitzerandBongers2011),whichhavehighwooddensitycomparedwithearlysuccessionaltreespecies(Wrightetal.
2010).
Thus,iflianaabundancecontinuestoincreaseandtropicalforestscontinuetobecomemoredynamicunderelevatedca,theymaystorelesscarbonasaresult.
Interestingly,AmazonianforestplotsappeartobeincreasingindynamismwhileincreasinginAGB(Bakeretal.
2004;Lewisetal.
2004;Phillipsetal.
2004).
ContinuedmonitoringisrequiredtodeterminewhetherthisisatransientresponsethatwilleventuallygivewaytodecliningAGBfollowingashifttowardsamoregap-dominatedstructure(Malhi2012).
Thefutureoftropicalforestcarbonstorageunderclimatechangeremainsalargesourceofuncertaintyinglobalclimatesimulations.
FortheAmazonBasin,uncertaintyinfuturecarbonstorageresultsbothfromvariabilityinclimateprojections(Salazaretal.
2007;Poulteretal.
2010b)andfromuncertaintyassociatedwithdirecteffectsofelevatedcaontheproductivityandWUEoftropicalforests(Lapolaetal.
2009;Rammigetal.
2010).
Insimulationswiththedirecteffectsofincreasingcaonplantphysiologicalprocessesturnedoff,bothrisingtemperatureandprecipitationreductioncauseddeclinesinAmazonianforestbiomass.
However,withdirecteffectsofelevatedcaonplantphysiologyturnedon,risingcamitigatedmuchoftheclimate-drivendeclineinforestbiomass(Galbraithetal.
2010).
Thesemodellingstudieshighlightthecriticalrolethatexperimentalresearchcanplayinreducingtheuncertaintyassociatedwiththedirecteffectsofelevatedcaonthephysiologyofwoodytropicalforestplants.
ChallengesandopportunitiesfortropicalCO2enrichmentexperimentsFACEstudieswerehelpfulforextendingobservationsintemperateforeststotheforeststandscale,butcompromisesinexperimentaldesignwerenecessarybecausethesystemswereexpensivetoconstructandoperate(NorbyandZak2011).
Forexample,althoughthereismuchinterestinunderstandingthecarboncyclingresponsesofintactmatureforests,mostoftheFACEexperimentswereconductedinyoungmonocultureplantations.
AnexampleisshowninFig.
5a,b.
Theoneexception,inwhichmature,temperateforesttreeswereexposedtoelevatedca(Krneretal.
2005),necessarilyrequiredadifferentcompromise:afocusonindividualtreesratherthanthewholeecosystem(Fig.
5c,d).
Tropicalforestscontainlargetreesandarespecies-rich.
Instudiesofforestdynamics,representativeplotsconsequentlytendtobe1haorlargertoadequatelycapturetheabundanceofco-occurringspecies.
Giventhegreaterstature,diversityandcomplexityoftropicalforests,aswellasmanyinfrastructureconstraints(e.
g.
roads,power,CO2supply),aFACEexperimentwillbeevenmorechallengingtoimplementinatropicalforest.
Thismay540FunctionalPlantBiologyL.
A.
Cernusaketal.
requirethedevelopmentofnewapproaches,differentfromthosedeployedinpreviousexperimentsintemperateforests.
Despitethesechallenges,investigatingstand-levelresponsestoelevatedcaintropicalforestsmustremainalong-termgoal,asthisisthescalerelevanttopredictingglobalclimatechangefeedbackoverthecomingcentury.
web-FACEattheSwissCanopyCranesiteGasanalysisGascontrolCO2+13CtracerCO2(f)(e)(c)(d)(a)(b)Fig.
5.
Somepossibilitiesforstand-scaleCO2enrichmentexperiments:(a,b)freeairCO2enrichment(FACE)atOakRidgeNationalLaboratory;(c,d)webFACEattheSwissCanopyCranesite;(e)theEdenProject(2013)asanexampleofalarge,naturally-litenclosurethatcouldaccommodatetallforesttreesforglobalchangeexperiments,constructedofethylenetetrauoroethylene(ETFE)cushions(credit:JürgenMatern/WikimediaCommons,CC-BY-3.
0);(f)atestoftheperformanceofETFEcushionsinthehumidtropicsattheSantaCruzExperimentalFieldFacility,SmithsonianTropicalResearchInstitute,Panama.
Theredarrowin(d)pointstothetubingusedtoemitCO2inthewebFACEexperiment.
Tropicalforestsandelevated[CO2]FunctionalPlantBiology541Fieldexperimentstoexplorehowelevatedcawillaffectestablishmentofearlyandlatesuccessionaltreespeciescouldprovideatractablealternativeinthenearterm,becausecompositionalshiftsintropicalforestcanopiesarelikelytobedrivenbychangesinseedlingestablishmentsuccess.
BecauseFACEsystemsrequirewindtodisperseCO2andbecausewindvelocitiesareoftenlowinforestgaps,CO2enrichmentsystemswithforcedventilation,suchassimpleopen-topchambers,wouldbeasuitabletoolforthestudyofgapdynamics,particularlyinsmalltreefallgaps.
Anysuchexperimentshouldpaycarefulattentiontosoilconditionsinordertoensureundisturbed,intactplant–soilinteractions.
Wenotethattheairwithin1–2moftheforestoorintropicalforeststendstobenaturallyenrichedinCO2comparedwithairabovethecanopy.
However,duringtheday,whenphotosynthesisispossible,thisnaturalCO2enrichmentrarelyexceeds50ppm(Lloydetal.
1996;Buchmannetal.
1997;Würthetal.
1998a;HoltumandWinter2001).
Lianaresponsestoelevatedcaintheunderstoreycouldbesuccessfullystudiedusingopen-topchambersorsimilarsystemsforCO2augmentation.
Thistypeofexperimentwouldfurtherlenditselftodifferentialtestsacrossotherplantfunctionaltypes,forexample,comparisonsofN2-xingtreeandlianaspecieswithnonxingspecies.
Multifactorexperimentsunderelevatedcacouldalsobeimplementedintheunderstorey,includingvariableintensityofdrought,irradianceorboth.
Interactionswithirradiancemaybeparticularlyimportant,becauseelevatedcacanlowerthelightcompensationpointindeepshade,withpotentiallylargeeffectsonplantcarbonbalanceunderextremephotonshortage.
Treeandlianabranchesintropicalforestcanopiescanbeexposedtoelevatedcawithlow-costinstallations(KrnerandWürth1996;Würthetal.
1998b;Lovelocketal.
1999)andaccessedforphysiologicalmeasurementsusinganexistingnetworkoftropicalforestcanopycranes(Bassetetal.
2003).
Inaddition,individualleavesorbranchescanbewarmedinsituinordertoexamineresponsestobothelevatedcaandelevatedtemperature.
Lianaresponsestoelevatedcaalongtheirgrowthtrajectoriesfromtheforestoortothecanopycouldbesuccessfullystudiedinthisway(Zotzetal.
2006).
Experimentsexposingonlyapartoftheplanttoelevatedcashouldfocusonshort-termresponses,asinteractionsatthewhole-plantscalewillnotbepresentinsuchexperiments.
Inaddition,thedegreetowhichbranchesbehaveautonomouslyintheircarbonrelationswithotherpartsoftheplantcouldinuencephysiologicalresponses,andthisshouldbetakenintoaccountinexperimentaldesignandinterpretationoftheresults(Sprugeletal.
1991;Lovelocketal.
1999).
Thestudyofforestsegmentscontainingtalltreesshouldbefeasibleinclosedsystems,apossibilitythathasbeentrialledbutnotextensivelyexploitedinreplicatedexperiments(Osmondetal.
2004).
Examplesofmodern,large,naturally-litenclosuresthatwouldaccommodatetallforesttreesincludehighlytransparentethylenetetrauoroethylenecovereddomes(Fig.
5e,f)suchasthoseintheEdenProject(EdenProject2013).
Closedsystemswouldrequiretemperaturecontrol,butuserelativelylittleCO2foraugmentationcomparedwithFACEsystems.
Moreover,plantscanbemaintainedataboveorbelowcurrentambientCO2conditions.
Temperaturecanalsobemanipulated.
UnlikeopenCO2enrichmentsystemsinwhichCO2concentrationsexhibitpronouncedshort-termuctuationsaroundthetargetconcentration(HoltumandWinter2003;Bunce2012),relativelystableCO2concentrationscanbemaintainedinenclosedsystems.
Althoughenclosedsystemshavedisadvantagesintermsofarticialrainandrequiresustainedairmixing,thistechnologyopensexcitingpossibilitiesforexperimentalecosystemscience,includingthemeasurementofecosystemgasexchange(Osmondetal.
2004),eitherbyplacingpremanufacturedenclosuresoverexistingtropicalvegetationorbyestablishingtreestandsinpurpose-builtenclosures.
Belowgroundresponses,includingrootdeploymentandfunction,nutrientturnoverandsoilorganicmatterprocessing,areespeciallyimportanttotheintegratedecosystemresponsetoelevatedCO2.
Belowgroundprocessesaredifculttomeasureandarestillpoorlyquantied.
Forexample,becauseofthepastfocusontemperateforests,inwhichnitrogenisbelievedtobethemajorlimitingnutrient,therehasbeenlittleresearchontheeffectsofelevatedcaonphosphoruscycling,andphosphoruscyclingispoorlyrepresentedinmodels.
Experimentalapproachesandsiteselectionmustcarefullyconsidertheimportanceofthebelowgroundenvironmentbyavoidingartefactsassociatedwithsoildisturbanceandincludethecapabilityforsufcientbelowgroundmeasurements.
Manyofthecriticalquestionsabouttheroleoftropicalforestsinglobalcarboncyclingareinherentlylong-termquestions(e.
g.
50–100years).
Furthermore,noexperimentorsmallsetofexperimentscaneverrepresentthefulldiversityofthetropicalbiome.
Modelsthatarewellinformedbyexperimentalobservationsofferanopportunitytoextrapolatethroughspaceandtime.
Henceanimportantstrategyfordesigningexperimentsthatwillprovidethemostusefulandneededdataandthegreatestunderstandingofprocessesistoengageamodellingperspectivefromthestart.
OpportunitiesforreducinguncertaintyinmodelsThecurrentgenerationofecosystemmodelsdemonstratesthepotentialforelevatedcatomitigatemuchoftheclimate-drivenlossoftropicalforestbiomassthatmightotherwiseoccurbytheyear2100(Lapolaetal.
2009;Galbraithetal.
2010;Poulteretal.
2010a;Rammigetal.
2010).
However,modelpredictionsarecurrentlybasedonverylimitedinformationandomitwhatarelikelytobecriticalmodifyingprocesses.
Uncertaintiesintherepresentationofelevatedcaeffectsontropicalforestvegetationincludethepotentialforelevatedcatorelievethelimitationsoncanopyphotosynthesiscausedbyhigh-temperaturestress,nutrientlimitationsonNPPresponsestoelevatedca,theeffectsofelevatedcaondroughtinducedtreemortalityandtheeffectsofelevatedcaonspeciescomposition.
Theresultsofexistingecosystemmodelsrepresenttestablehypothesesthatcanguideexperimentaldesign,andunderstandingthecriticalpointsofuncertaintyinthemodelswithregardtorepresentationofelevatedcaresponsescanhelptoidentifythehighestpriorityresearchneeds.
Progresscanbeachievedintherepresentationofleafandcanopyresponsestohightemperaturebycomparingmodelledresponsecurveswiththoseobservedinleafcuvettesandbyeddycovariance(Lloydetal.
1995;DoughtyandGoulden2008;542FunctionalPlantBiologyL.
A.
Cernusaketal.
Verbeecketal.
2011).
Forexample,observationsinatropicalforestinAmazoniaindicatedthata3Criseinbulkairtemperatureabove28.
5C,causedbyanincreaseinirradiance,resultedina40%reductioninwhole-canopygrossgasexchange(DoughtyandGoulden2008).
Thiswascausedbyincreasesinleaftemperaturesof5–8Cinthesunlitfractionofthecanopy,andsubsequentdeclinesingsandAinsunlitleaves.
Fig.
6showsanexampleofmodelledresponsecurvesforcanopyphotosynthesisfortwodynamicglobalvegetationmodels,Lund-Potsdam-Jena(LPJ)andOrganizingCarbonandHydrologyinDynamicEcosystems(ORCHIDEE),whichdifferintheirtreatmentoflightdiffusionthroughacanopy,gs,parameterisationoftheFarquharetal.
(1980)photosynthesismodelandsoil–waterbalance(Sitchetal.
2003;Krinneretal.
2005).
Althoughtemperatureandradiationresponsesdifferbetweenthetwomodels,neitherappearscapableofcapturingthepatternobservedintheAmazonianforest,namelyanalmostlineardeclineincanopyphotosynthesisbetweenbulkairtemperaturesof28.
5and31.
5C.
Inordertoextendtherepresentationoftemperatureresponsestoelevatedcaconditions,validationdatafromexperimentalmanipulationexperimentsareessential.
Recentprogresshasbeenmadetowardsincludingtheeffectsofphosphorusavailabilityinecosystemmodels(Lloydetal.
2001;Wangetal.
2007;Mercadoetal.
2011;Golletal.
2012).
However,therepresentationofphosphorusdynamicsinmodelsisalsolimitedbyuncertaintyabouttheextenttowhichtropicalwoodyplantscanaccessorganicphosphorus,andthemobilityoforganicphosphoruscompoundsintropicalforestsoils(Turner2008;Cernusaketal.
2011c;TurnerandEngelbrecht2011).
Animprovedunderstandingofphosphoruscyclingintropicalforestsisneeded.
Furthermore,theeffectsofphosphorusavailabilityontheresponsivenessoftropicalvegetationtoelevatedcahavenotbeentestedexperimentally.
Suchexperimentsshouldbegivenahighpriority.
Predictingdrought-inducedvegetationmortalityremainsasignicantchallenge(Nepstadetal.
2007;McDowelletal.
2011).
Itwasrecentlyshownthathydraulicimpairmentwasabetterpredictorofdrought-inducedmortalitythanwasthesizeoftheNSCpoolinatemperatedeciduoustreespecies(Andereggetal.
2012).
Carbonstarvationthusdidnotappeartobeausefulpredictor.
However,ifitisshownthattheNSCpoolplaysasignicantroleinembolismrepair(Salaetal.
2012),thiscouldhaveimplicationsforrecoveryfromdroughtunderelevatedca,becauseNSCconcentrationsarelikelytoincrease.
Furtherexperimentationisrequiredtodevelopamechanisticmodelofmortalitymechanismsandplantagestructurethatcanaccountfortheeffectsofelevatedca.
Atthecommunityscale,incorporatingpredictionsregardingtheeffectsofelevatedcaoncompositionalchangeintoecosystemmodelsrepresentsafurtherchallenge.
Ifexperimentalmanipulationsofcaintropicalforestsarelimitedtotargetingjuvenilestages,thenmodelswillneedtoupscaleobservedshiftsintherecruitmentsuccessofplantfunctionaltypestothedynamicsofentireforestassemblages.
Thedevelopmentofmodels,suchastheEcosystemDemographymodel(Moorcroftetal.
2001;Medvigyetal.
2009;Fisheretal.
2010),whichlinkmechanisticrepresentationsofecophysiologyandbiogeochemistrytothesize-structuredcompetitionandsuccessionfoundinforestgapmodelswillprovideapotentialtooltoachievethisintegration.
Inaddition,anewapproachtorepresentingfunctionaldiversityindynamicglobalvegetationmodelswasrecentlydeveloped,basedongeneratingplanttraitsfromdistributionsofgrowthstrategiesratherthanfromxedtraits(Pavlicketal.
2012).
Thisapproachcouldproveusefulforsimulatingtropicalforests,allowingforamoreexiblerepresentationoftheirstructureandfunctionthroughspaceandtime.
Modelvalidationunderambientcausingexistinglong-termtropicalforestdynamicsdatafromlargeplots(Condit1995)willbeessential.
ConclusionsModelsimulationssuggestthattropicalforestNPPwillrespondmorestronglytoelevatedcathanthatoftemperateandborealforests.
Thishypothesiscouldhavesignicantimplicationsfortheglobalcarboncycleandforclimatechangepredictions.
500wm–2750ppm750ppm450ppm300ppm450ppm300ppm250wm–2100wm–2020040060080010001002003004005001560402002025303540Anet(molCm–2s–1)@25°CAmbientCO2(ppm)Shortwaveradiation(Wm–2)Airtemperature(°C)Anet(molCm–2s–1)@400Wm–2(a)(b)(c)Fig.
6.
Theoreticalresponsecurvesforwhole-canopyphotosynthesisversus(a)ambientCO2,(b)shortwaveradiationand(c)airtemperatureusingthemodiedFarquharetal.
formulationintheLPJandORCHIDEEdynamicglobalvegetationmodels(Farquharetal.
1980;Collatzetal.
1991;Sitchetal.
2003;Krinneretal.
2005).
Simulationsareforatropicalevergreenplantfunctionaltype,assuminganondroughtratioofintercellularCO2concentrationtoambientCO2concentrationof0.
80(LPJ)or0.
67(ORCHIDEE).
BlacklinesrefertopredictionsofLPJandredlinestopredictionsofORCHIDEE.
Panel(a)showsresponsesatthreedifferentirradiances.
(b)and(c)showresponsesatthreedifferentatmosphericCO2concentrations.
Tropicalforestsandelevated[CO2]FunctionalPlantBiology543Itissufcientlycompellingtojustifylarge-scaleinvestmentinexperimentaltesting.
Ultimately,wewouldliketoknowwhetherandtowhatextentelevatedca-inducedincreasesinNPPintropicalforestswillresultinincreasedcarbonstorageandnegativefeedbacktoca.
Addressingthisquestionwillrequireacombinationofexperimentalandmodel-basedapproaches.
Additionalsupportinghypothesesthatshouldalsohaveahighpriorityforexperimentalresearcharethefollowing:(1)elevatedcawillincreasethehightemperaturetoleranceofphotosynthesisintropicaltreeleaves;(2)phosphorusavailabilitywilllimittropicalforestNPPresponsestoelevatedca;(3)elevatedcawillincreasethedroughtresistanceoftropicalforests;and(4)elevatedca-inducedchangesinspeciescompositionwillcausedirectionalchangesincarbonstorageintropicalforests.
Carefullyconsideredexperimentsthatneednotnecessarilytakeplaceatthestandscalecouldmakeimportantcontributionstowardstestingtheselatterhypotheses.
Understoreyexperimentsthatquantifythepotentialforelevatedcatoaltertheregenerationsuccessofspeciesrepresentingimportantfunctionalgroups,andaccountforinteractionswithsoilnutrientandwaterstatus,wouldbeachievableintheneartermandcost-effective.
Open-topchambersandbranchbagsinstalledinthecanopytoelevateca,incombinationwithinsituwarming,couldprovideausefulmethodforansweringquestionsaboutcanopyleafphysiologyinrelationtotemperatureanddrought.
Theseexperimentsshouldnotbeviewedasreplacementsforstand-levelexperiments,butratherastractablerststeps.
Stand-levelCO2enrichmentexperimentswillprovideinvaluableresults,andshouldbevigorouslypursued.
ThecriticalroleoftropicalforestsintheterrestrialcarboncycleandthepaucityofexperimentaldatasofaravailabletogethershouldmaketropicalforestCO2enrichmentexperimentsaveryhighpriorityforglobalclimatechangeresearch.
AcknowledgementsThisreviewresultedfromasymposiumheldattheSmithsonianTropicalResearchInstituteon31Marchand1April2011.
FundingforthesymposiumwasprovidedbytheSmithsonianTropicalResearchInstitute.
LACwassupportedbyaFutureFellowshipfromtheAustralianResearchCouncil(FT100100329).
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