Characteristics of wood CO2 efflux in a Bornean tropical rainforest

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Agricultural and Forest Meteorology

jou rn al h om ep a ge :w w w . e l s e v i e r . c o m / l o c a t e / a g r f o r m e t

Characteristics of wood CO ₂ efflux in a Bornean tropical rainforest

Ayumi Katayama

^a,∗

, Tomonori Kume

^b

, Mizue Ohashi

^c

, Kazuho Matsumoto

^d

, Michiko Nakagawa

^e

, Takami Saito

^f

, Tomo’omi Kumagai

^f

, Kyoichi Otsuki

^a

aKasuyaResearchForest,KyushuUniversity,Sasaguri,Fukuoka,811-2415,Japan

bSchoolofForestryandResourceConservation,NationalTaiwanUniversity,Taipei,106-17,Taiwan

cSchoolofHumanScienceandEnvironment,UniversityofHyogo,Himeji,Hyogo,670-0092,Japan

dFacultyofAgriculture,UniversityoftheRyukyus,Okinawa,903-0213,Japan

eGraduateSchoolofBioagriculturalSciences,NagoyaUniversity,Chikusa-ku,Nagoya,464-8601,Japan

fInstituteforSpace-EarthEnvironmentalResearch,NagoyaUniversity,Chikusa-ku,Nagoya,464-8601,Japan

a r t i c l e i n f o

Articlehistory:

Received13September2015

Receivedinrevisedform16January2016 Accepted20January2016

Keywords:

Emergenttrees Ecosystemscale Inter-individualvariation Scaling

StemCO2efflux

a b s t r a c t

WoodCO2efflux(Rwood)isanimportantcarboncyclingprocessinforestecosystemsandislessunderstood inBorneantropicalrainforestscomparedwiththatinNeotropics,whichhavedifferingbioticandabiotic characteristics.Borneantropicalrainforestshaveparticularlyhigherabovegroundbiomassbecauseof highstanddensitiesoftallemergenttrees,andnoregularseasonaldryperiod.Thesepropertiesmay reflectspecificRwoodvariationandhigherannualRwoodattheecosystemscale(annual-Rwood)inBorneo.

Hence,inthisstudy,weinvestigatedfactorsthataffectinter-individualvariationinchamber-basedRwood

onstemsurfacesatbreastheight(chamber-Rwood)andestimatedRwoodattheecosystemscale(ecosystem- Rwood)inaBorneantropicalrainforest.Subsequently,weexaminedtemporalvariationinecosystem-Rwood

withenvironmentalfactors,estimatedannual-Rwood,andthenevaluatedtheeffectsoflargetreeson ecosystem-Rwood.

Stemgrowthrateswerethemostsignificantpredictorofinter-individualvariationinchamber-Rwood

duringallfivemeasurementperiodsbetween2012and2014.Accordingly,stemgrowthratesallowed accurateestimatesofecosystem-Rwood,althoughchamber-Rwoodvariedwithdiameteratbreastheight (DBH)andtreespeciesinsomemeasurementcampaigns.Ecosystem-Rwooddecreasedwithsoilmoisture.

Consideringtheinter-individualandtemporalvariation,annual-Rwoodwasestimatedat7.06±2.09MgC ha⁻¹year⁻¹.ThisvaluewascomparabletothosedeterminedinNeotropicalforests,eventhoughabove- groundbiomassinthepresentstudysitewasapproximatelytwiceofthoseinNeotropicalsites.Large treeswithDBH>70cmcomprised38%ofabovegroundbiomassbutaccountedforonly23%ofecosystem- Rwoodbecauseofthesmallportionofwoodytissuesurfaceareaofthelargetrees.Thesedataindicatethat thestanddensityoflargetreescanconsiderablyaffectabovegroundbiomassbutexertlessinfluenceon variationinecosystem-Rwoodamongvariousforests.

©2016ElsevierB.V.Allrightsreserved.

1. Introduction

Tropicalforestsplayimportantrolesinglobalcarbon cycling becauseofthehighestphotosynthesisandrespirationratesoffor- estecosystems(Beeretal.,2010;Malhi,2012).WoodCO₂efflux (R_wood)isameasureofcarbonreleasefromstemsandbranchesand isanimportantindicatorofforestecosystemproductivity,because itaccountsforabout20–25%ofplantrespiration(Chambersetal., 2004;Malhietal.,2009)and13–27%ofcarbonassimilationfrom photosynthesis(Malhietal.,2009;daCostaetal.,2013;Doughty

∗Correspondingauthor.Tel.:+81929483101;fax:+81929483127.

E-mailaddress:ayumi.katayama0920@gmail.com(A.Katayama).

etal.,2013).RecentstudieshaveestimatedR_woodattheecosystem- scale(ecosystem-R_wood,␮molm⁻²s⁻¹)inNeotropicalrainforests (Chambersetal.,2004;Cavalerietal.,2006;daCostaetal.,2013;

Rowlandetal.,2014),althoughstudiesonecosystem-R_woodoutside Neotropicalareasremainlimited(MeirandGrace,2002).Measure- mentsofecosystem-R_woodinvariouskindsoftropicalrainforests areimportantforinvestigationsofglobalcarboncycling,because variationofecosystem-R_woodwithbioticandabioticfactorsremains poorlyunderstood.

R_woodonwoodysurfaceareas(chamber-R_wood,␮molm⁻²s⁻¹) isgenerallyestimatedusingthechambermethod,andecosystem- R_woodisusuallyestimatedbymultiplyingchamber-R_woodatbreast height by woody tissue surface areas or volumes (Meir and Grace,2002;Chambersetal.,2004).Estimatesofecosystem-R_wood http://dx.doi.org/10.1016/j.agrformet.2016.01.140

0168-1923/©2016ElsevierB.V.Allrightsreserved.

still remainchallengedby intra-andinter-individualvariations in chamber-R_wood that can lead to errors in scaled estimates (Chambers et al.,2004; Malhi etal., 2009).Recently,Katayama etal.(2014)showedlimitedverticalvariationinchamber-R_wood basedonmeasurementsofupto40-mhightreesin aBornean tropicalrainforest,suggestingthatintra-individualvariation has limitedeffectsonestimatesofwholetreestemCO₂efflux.However, theeffectsofinter-individualvariationremainunclear,warranting carefulexaminationespeciallyinold-growthtropicalrainforests wheretreespeciesandsizesvary.

Multiple factors have been shown to affect inter-individual variation in chamber-R_wood, and various scaling methods have beensuggested.Inpreviousstudiesoftropicalrainforests,inter- individualvariation in chamber-R_woodwas related todiameters atbreast height(DBH;Cavaleri etal.,2006), stemgrowthrates (Ryan et al.,1994),and both (Chambers etal.,2004; Robertson etal.,2010).Subsequently,thesefactorswereusedtoextrapolate chamber-R_woodvaluesinindividualswithoutdirectmeasurements andthentoestimateecosystem-R_wood.InrecentstudyofNeotrop- icalforests,ecosystem-R_woodvalueswereestimatedbymeansof measuredchamber-R_woodvalues(Rowlandetal.,2014).Previous studiesalsoreportedthatecosystem-R_woodvarytemporallywith soilmoisture,reflectingchangesinstemgrowthinresponsetosea- sonaldryperiodsinNeotropicalrainforests(Chambersetal.,2004;

Malhietal.,2014).Thesestudieswarrantinvestigationoffactors that affecttemporal variationin ecosystem-R_wood.Furthermore, thefactorsaffectinginter-individualvariation inchamber-R_wood mayvarytemporally.Thus,examinationsofinter-individualvari- ationinchamber-R_woodacrossmeasurementperiodsarerequired toinvestigatetemporalvariationinecosystem-R_woodandtoesti- mate annual R_wood at the ecosystem scale (annual-R_wood, MgC ha⁻¹year⁻¹).

It iswellknownthat Borneantropicalrainforests have high aboveground biomass. Accordingly, two-fold higher stand den- sities of large trees (DBH>70cm) resulted in 60% increases in abovegroundbiomasscomparedwiththoseinNeotropicalforests (Paoli etal., 2008;Sliket al.,2010).Moreover,largetrees con- tributedconsiderablytoabovegroundbiomassandaboveground biomassincrementsattheecosystemscaleinBorneo(Paoliand Curran,2007).Inarecentstudy,higherstemgrowthrateswere shown in larger trees than in small trees according to global analyses(Stephensonetal.,2014).Thesedataindicatethatlarge trees can have higher individual R_wood because of both effects of highchamber- R_wood caused by highstem growthrates and DBH, and large surface area or volume. Thus, large trees may alsocontributeconsiderablytoecosystem-R_wood,potentiallylead- ingtogreaterecosystem-R_woodvalues inBorneanthanthose in Neotropicalforests.Higherannual-R_woodinBorneoisalsoexpected withconsiderationoftemporalvariation.Thereisnoregularsea- sonaldryperiodbutirregularshort-termdroughtperiodoccurs inBorneo,whilethereareseveralseasonaldrymonthsinmost Neotropicalarea(Malhietal.,2006)wherelowerchamber-R_wood valueswereobservedduringdrymonths(Chambersetal.,2004;

Malhietal.,2014).Althoughhigherannual-R_woodisexpectedin Borneo,thestudyonannual-R_woodhasnotbeenconductedinsuch forests.

Inthisstudy,wemeasuredchamber-R_woodatbreastheightsof morethan50individualtreesof36speciesinaBorneantropical rainforestwithhighabovegroundbiomassandnoregularseasonal dryperiod.Measurementswereperformedfivetimesundervari- oussoilwaterconditions.Insubsequentanalyses,factorsaffecting inter-individualvariationinchamber-R_woodforeachmeasurement periodwereidentified,andecosystem-R_woodwassubsequentlycal- culated.Wealsodeterminedtheeffectsofenvironmentalfactors, suchassoilmoistureandairtemperature,ontemporalvariationin ecosystem-R_wood,andannual-R_wood,anditsratiotogrossprimary

production(GPP)wereestimatedaccordingly.Finally,weexam- inedthecontributionoflargetreestoecosystem-R_wood.

2. Materialsandmethods 2.1. Studysite

This study was conducted in Lambir Hills National Park, Sarawak,Malaysia(4^◦12N,114^◦02E)atabout20kmsouthwestof Miri,SarawakontheislandofBorneo.Lowlandmixed-dipterocarp forest,whichisatypicalmaturelowlandtropicalrainforesttypein SoutheastAsia,covers85%ofthis6949hapark.Thecontinuoustree layerisapproximately40mabovetheground,buttheheightsof treeswithDBH>100cmoftenexceed50m(Katayamaetal.,2014).

Theleafareaindexrangesspatiallybetween4.8and6.8m²m⁻², withameanof6.2m²m⁻²(Kumagaietal.,2004).Between2000 and2009,themeanannualtemperatureatthis sitewas25.8^◦C and rainfall wasdistributed throughout the year with a mean annualrainfallof2600mm(Kumeetal.,2011).Themonthlyrain- fallbetween1958and2001averagedmorethan100mm(Kumagai etal.,2005).Althoughthereisnoclearseasonalityintempera- tureandprecipitation,unpredictabledryperiodssometimesoccur throughouttheyear.

A 4ha study plot was established surrounding a crane for ecologicalobservation.Previously,weperformedcarboncycling measurements,includingeddycovariancemeasurements,carbon allocation(Katayamaetal.,2013),andsoilrespiration(Katayama etal.,2009)atthissite.

2.2. R_woodmeasurements

Chamber-R_woodwasmeasuredfivetimesatbreastheightduring 9–28January2012,5–8May2013,13–14July2013,24December 2013–2January2014,and29June–7July2014,mainlyinthe4- ha plot.Measuredtrees were selectedrandomly from52 trees duringeachmeasurementperiod,andthenumbersofmeasured treeswere48,48,47,50,and38inJanuary2012,May2013,July 2013,December2013,andJune2014,respectively(TableA1).DBH rangedfrom10 to158cm.The52 samplesincluded36species, and24oftheseweretheDipterocarpaceaefamily.Tominimizethe effectsofdiurnalvariationinR_wood,measurementswereconducted between8:30and15:00accordingtoapreviousstudy(Katayama etal.,2014).Diurnalmeasurementschamber-R_woodoffivetrees wereperformedevery2hbetween7:30and17:30onJanuary1, 2014,toexaminetheeffectofdiurnalvariationonthedailyR_wood estimatebasedonone-timemeasurementsduringdaytime.

Chamber-R_wood was measured using a closed-static system withaninfraredgasanalyzer(GMP343,Vaisala,Helsinki,Finland) attachedinsideachamber.Thechamberandcollarsweremadeof polyvinylchloride.Asmall8-Vbattery-operatedfanwasinstalled tocirculateairinsidethechamber,collarswereattachedtostems usingglueandsiliconsealant,andgapsbetweenstemsandcollars werefilledwithnondryingclay.Leakswerecheckedaftermeasure- mentsbybreathingaroundthechamber.For allmeasurements, incubationperiodsrangedfrom60to180s,andCO₂ concentra- tionswithinthechamberweremeasuredevery5sandrecorded usingamonitor(M170,Vaisala).Chamber-R_wood(␮molm⁻²s⁻¹) wascalculatedusingEq.(1)asfollows:

Rwood=

₂₇₃

.2 273.2+Ta

× V 22.4×dc

dt ×10⁶×1

A, (1)

where V is the chamber volume (0.389l), Ta is air tempera- ture inside the chamber (^◦C), A is the projected area of the chamber(3.849×10⁻³m²),anddCistheincrementofCO₂ con- centration (ppm) during the incubation time (s, dt). Eq. (1) assumesthatrespirationismeasuredunderstandardbarometric

pressure. Allmeasurements at each point were replicated two orthreetimesandmeanswerecalculated.Systemaccuracywas determined by measuring R_wood of some trees using a com- mercial respirometer(LI-6400, Li-CorInc., Lincoln, NE, USA) at thesame timepoints.TherelationshipbetweenR_wood observed usingthesystem(Rwood-system)andLI-6400(Rwood-LI6400)waslinear (Rwood-LI6400=1.1394×Rwood-system,R²=0.97);thus,chamber-R_wood wasestimatedbycorrectingRwood-systemusingthisequation.

Stemsurfaceand airtemperaturesweremeasuredconcomi- tantlyusingathermometer(Ondotori;T&DCo.Ltd.,Nagano,Japan).

Toeliminatetheeffectsoftemperature,chamber-R_woodvalueswere correctedtoareferencetemperatureof25^◦CusingEq.(2)asfol- lows:

R25=R(st)Q₁₀^(25−st)/10, (2)

whereR25ischamber-R_woodat25^◦C,stisthestemsurfacetemper- ature(^◦C)whereR_wood wasmeasured,andQ₁₀isatemperature coefficient of R_wood. Because Q₁₀ was not calculated from the presentdata,itwasassumedthatQ10wasequalto2.0,asshown previouslybyCavalerietal.(2006)intropicalrainforestsinLaSelva, CostaRica.Inthepresentstudy,chamber-R_woodwasusedasR₂₅ basedonsurfacearea,whichwascorrectedat25^◦C.

Environmentalobservations wereincorporatedintoanalyses of temporal variation in ecosystem-R_wood. Air temperaturewas monitoredonthecraneat75mabovethegroundusingather- mohygrograph(HMP35A,Visala)andthedatawasloggedusinga programmabledatalogger(CR10X,CampbellScientific,Utah,USA).

Rainfallwasmonitoredusingatippingbucketraingauge(RS102, OgasawaraKeiki,Tokyo,Japan)withadatalogger(HOBOevent, OnsetComputer,USA)atthetopofthecrane(85.8mabovethe ground).Soilwatercontentwasdeterminedatdepthsof10,30, 60,and100cmusingtimedomainrefrectometrysensors(CS616, Champbell) and a data logger nearthe crane, and mean daily soilwater content(SWC, m³m⁻³)wascalculated ata depthof 0–120cm.Measurementswereinitiatedon3rdSeptember2012, andsoilmoisturecontentswereinterpolatedbetween1stJanuary 2011and2ndSeptember2012(SWC_estimate)usingtherelationship betweencumulative30dayrainfall(Rcum)andmeasuredsoilwater contents(SWC_estimate=0.1631×Rcum0.107,R²=0.67).

2.3. Treecensus

Atreecensuswasconductedinthe4-haplotin2012and2013.

DBHvaluesfortreeswithDBH>10cmweremeasuredwithareso- lutionof1mm,anddifferencesindiameterbetween2012and2013 werecalculatedasstemcircumferencegrowthrates(sg,cmy⁻¹)for alltrees.AbovegroundbiomassinBorneowasestimatedusingDBH andapreviouslydescribedallometricequation(Yamakuraetal., 1986).

2.4. Scalingmethodandstatisticalanalysis

Toestimateannual-R_wood,ecosystem-R_woodforeachmeasure- mentserieswasestimatedfrommeasuredchamber-R_wood(spatial scaling),and dailyecosystem-R_woodin 2013wasalsoestimated from the relationship between the estimated ecosystem-R_wood andenvironmentalfactors(temporalscaling).Forspatialscaling, ecosystem-R_wood in the 4-haplot wasestimated by two meth- ods.Inone,ecosystem-R_woodwasestimatedbymultiplyingmean measuredchamber-R_woodvaluesbywoodytissuesurfaceareasin the4-haplotandthendividingbythegroundarea,asdefinedby Model0.Intheother,ecosystem-R_woodwasestimatedasthesum ofindividualR_wood(individual-R_wood,␮moltree⁻¹s⁻¹)foralltrees inthe4-haplotanddividedbythegroundarea.Individual-R_wood wasestimatedbymultiplyingindividualchamber-R_woodvaluesby woody tissue surface areas. Chamber-R_wood values for all trees

were estimated by regression models. Predictors of the model includedsg(continuousvariable),DBH(continuousvariable),and treespecies(categoricalvariable;DipterocarpaceaeDryobalanops aromatica,DipterocarpaceaeShoreabeccariana,MoraceaeArtocar- pus anisophyllus, and others) (Table A1). The three species for whichmorethanthreeindividualsweremeasuredwereselectedas variables.Toexaminetheeffectofpredictorsonecosystem-R_wood estimates,weconstructedthreemodelsforchamber-R_wood esti- mate,thebest-fitmodel,Model1,andModel2.Thebest-fitmodel wasdefinedasthemodelforwhichpredictorsweredetermined accordingtothelowestAICvaluefromthefullmodel.Predictor variablesinModel1weresgandDBHandthepredictorinModel2 wassg. Thesame coefficients of sgand DBH wereused across species.Woodytissuesurfaceareaswereestimatedusingtherela- tionshipbetweenDBHandsurfacearea,aspreviouslydescribed (Chambersetal.,2004)forNeotropicalforests,andsurfaceareaof woodytissueperunitgroundarea(stemareaindex,SAI,m²m⁻²) wascalculated for comparison withprevious studies.Errors in ecosystem-R_woodforModel0werestandarddeviationsofmeasured chamber-R_wood,anderrorsforothermodelswerederivedfrom95%

confidencelimitsforeachmodel.

Temporalscalingwasperformedusingaregressionmodelwith environmentalfactorssuchasSWCandairtemperature.Onlypre- dictivefactorswithsignificantcorrelationwereusedforthemodel.

Annualecosystem-R_woodwereestimatedusingthebest-fitmodel, Model1,Model2, andModel0. Errorsinannualecosystem-R_wood werederivedfrom95%confidencelimitsforeachmodelfortempo- ralscaling.AllstatisticalanalyseswereconductedusingRversion 3.1.3.

Althoughsomepreviousstudiesdemonstrateverticalvariation inR_woodforscaling(Yodaetal.,1965;Damesinetal.,2002),we assumedconstantR_woodwithheightbecausepreviousstudiesshow limitedverticalvariationinR_woodbasedonsurfaceareainthisstudy site(Katayamaetal.,2014).Inthepresentstudy,theuseofsurface areaforscalingindividual-R_woodfromchamber-R_woodwasdeter- minedbasedontheresultofagraphicaltechnique(LevyandJarvis, 1998;Cavalerietal.,2006)usingverticalR_wooddatafromaprevious study(Katayamaetal.,2014;Fig.A1).

2.5. GPPestimates

GPPwasdefinedasthesumofabovegroundplantrespiration (R_above), abovegroundnet primaryproduction (ANPP), and total belowground carbon flux (TBCF) according to a previousstudy (Littonetal.,2007).R_aboveisthesumofecosystem-R_woodandfoliage CO₂efflux(R_foliage).Ecosystem-R_woodwasestimatedinthepresent study(seeSection2.4).Ecosystem-R_foliagewasestimatedasthesum ofleafareadensitiesmultipliedbyR_foliageatevery5m.Leafarea densitieswereestimatedusingtheplantareaindex(PAI)profile andtotalleafareas.ThePAIprofilewasreportedbyKumagaietal.

(2006),whomeasuredverticalvariationintheplantareaindexat fourpointsusingapairofcanopyanalyzers(LAI-2000,Li-Cor,Lin- coln,Nebraska)inthisstudysite.Subsequently,totalleafareasat theecosystem-scalewereestimatedusingtheequationdescribed byYamakura etal. (1986). R_foliage wasreported byKenzo etal.

(2015),whomeasuredfoliage darkrespirationratesin24 fam- ilies,62 species,and 123individualtreesfromtheground toa heightof52.5minthisstudysiteusingacommercialrespirometer (LI-6400,LI-CORInc.,Lincoln,NE).R_foliagewascorrectedtotheres- pirationrateat25^◦CusingQ10.Q10wasnotmeasuredeitherinthe presentstudyorinpreviousstudiesinAsiantropicalrainforests.

AlthoughtherewashighvariationinQ₁₀amongtreespeciesinthe Neotropics(Asaoetal.,2015),Q10wasnotdifferentamongcanopy positionsandthevalueofQ₁₀averagedamongvariousspecieswas 2.0inAustralia(Weerasingheetal.,2014)and2.3inCostaRica (Cavalerietal.,2008).Inthepresentstudy,Q10wasassumedto

be2.3,avaluereportedintropicalrainforestsinLaSelva(Cavaleri etal.,2008)thatwasobtainedbecauseofahighernumberofmea- surements.SeveralstudiesshowedlowerR_foliageinthelightthan inthedark(Atkinetal.,2000).Thus,toaccommodatelightinhi- bitionof R_foliage, daytimeR_foliage wascalculated as 67%of night timeR_foliageaccordingtopreviousstudies(Malhietal.,2009,2014;

daCostaetal.,2013;Doughtyetal.,2013).AnnualR_foliage atthe ecosystemscale(annual-R_foliage,MgCha⁻¹year⁻¹)wasestimated assuming12hofdaytimeandnighttimeandaconstanttempera- tureof25^◦Ceachdaythroughouttheyear,andtheerrorinannual R_foliage representsspatialvariationaccordingtoapreviousstudy (Metcalfeet al.,2010).ANPP(6.76±0.57 MgCha⁻¹year⁻¹)and TBCF(19.63±6.37MgCha⁻¹year⁻¹)werepreviouslyestimatedin thisstudysite(Katayamaetal.,2013).ANPPwasestimatedbasedon treecensusandlitterfallmeasurementsbetween2001and2006in the4-haplot,andtheerrorwasthestandarddeviationforthefive years.TBCFwasestimatedasthedifferencebetweenannualsoil respirationandannuallitterfallCusingasteady-stateassumption forsoilC(RaichandNadelhoffer,1989).Soilrespirationmeasure- mentswereperformedbetween2002and2006,andtheerrorsfor soilrespirationandlitterfall representedspatialvariation. Thus, eacherrorofannualfluxforGPPestimatewasestimatedbasedon measurementsormodels,resultingindifferentrepresentationsof variation.Errorpropagationwasappliedforallcombinedquanti- tiesusingstandardrulesofquadratureaccordingtoMalhietal.

(2014),assumingthat uncertaintieswereindependentandnor- mallydistributed.Uncertaintiesintheestimatesaredescribedin Section4.

2.6. Effectsoflargetreesonecosystem-R_woodandaboveground biomass

Ecosystem-R_woodandabovegroundbiomassinresponsetostand densitiesoflargetreeswereinvestigatedtoassessthepotential effectsoflargetreesonecosystem-R_woodandabovegroundbiomass.

Large trees were defined as those with DBH>70cm according toSliketal.(2013).Ecosystem-R_wood forvarious fictionalstand densitiesoflargetreeswascalculatedasthesumofecosystem- R_wood for large trees (ecosystem-R_woodlarge, ␮molm⁻²s⁻¹) and ecosystem-R_woodfortreeswithDBH<70cm(ecosystem-R_woodsmall,

␮molm⁻²s⁻¹).Ecosystem-R_woodlarge wasestimatedbymultiply- ing mean individual-R_wood values for large trees obtained by the best-fit model in January/2012with standdensities. Stand density of large trees differed between zero and actual den- sities (16.5 trees ha⁻¹). Ecosystem-R_woodsmall was the sum of individual-R_woodvaluesfortreeswithDBH<70cm.Aboveground biomasswassimilarlycalculatedforvariousstanddensitiesoflarge trees.

3. Results

3.1. Inter-individualvariationinR_wood

Average±standard deviation (S.D.) chamber-R_wood values at breastheightwere1.39±0.74,0.99±0.58,0.81±0.52,1.23±0.87, and0.91±0.65␮molm⁻²s⁻¹inJanuary2012,May2013,July2013, December2013,andJuly2014,respectively.Multipleregression analysesofeachmeasurementperiodshowedthatsgandDBHwere positivelycorrelatedwithchamber-R_wood(Fig.1),althoughselected variablesdifferedforthebest-fitmodelofchamber-R_wood.Among variables,sgwasthemostpredictiveofchamber-R_wood(Table1), althoughDBHandspeciessignificantlyaffectedchamber-R_woodin somecases.Specifically,chamber-R_woodwashigherforD.aromat- icaandlowerforS.beccarianathantheotherspecieswhenselected asthebest-fitmodel.Diurnalvariationpatternsdifferedbetween

0 1 2 3 4 5

0 1 2 3 4 5

0 1 2 3 4 5

0 1 2 3 4 5

0 50 100 150 0

1 2 3 4 5

-1 0 1 2 3 4 5 Chamber_Rwood(μmolm-2s-1)

sg (cm yr^-1) DBH (cm) Jan-12

May-13

Jul-13

Dec-13

Jul-14

Fig.1.Relationshipsofchamber-R_wood duringeachmeasurementperiod,with diametersatbreastheight(DBH;right)andstemgrowthrates(sg;left).Sym- bolsindicatetreespecies:circles,DIPTEROCARPACEAEShoreabeccariana;squares, DIPTEROCARPACEAEDryobalanopsaromatic;cross,MORACEAEArtocarpusaniso- phyllus;closeddiamond,otherspecies.

individuals(Fig.A2).Chamber-R_woodpeakedintheearlyafternoon forsometreesbutinthelateafternoonforothers.ThemeanCVof diurnalvariationwas13±7%,anddailychamber-R_woodwithcon- siderationofdiurnalvariationwas1.09±0.17higherthanthose basedononlyone-timemeasurementsinthedaytime,suggest- inganapproximately10%underestimateofchamberR_woodinthis study.

Table1

Statisticalresultofmultipleregressionanalysisforeachmeasurementsperiod.Theobjectivevariableischamber-Rwood,predictorvariablesforthebest-fitmodelwere determinedaccordingtothelowestAICvaluefromallpredictorsincludingstemgrowthrate(sg),dbhandtreespecies.PredictorvariablesofModel1andModel2aresgand DBH,andsg,respectively.

Jan-12 May-13 Jul-13 Dec-13 Jul-14

Best-fit model

Model1 Mode2 Best-fit model

Model1 Mode2 Best-fit model

Model1 Mode2 Best-fit model

Model1 Mode2 Best-fit model

Model1 Mode2

Coefficientsofindependentvariables

sg 0.28^* 0.28^* 0.47^*** 0.36^*** 0.36^*** 0.49^*** 0.32^*** 0.32^*** 0.41^*** 0.26^* 0.30^* 0.55^*** 0.37^*** 0.33^** 0.37^***

DBH 0.007^* 0.007^* – 0.005^* 0.005^* – n.s. 0.003 – 0.007^* 0.008^* – n.s. 0.002 –

D.beccariana n.s. – – −0.28 – – n.s. – – n.s. – – n.s. – –

D.aromatica n.s. – – 0.44 – – 0.63^** – – 0.58 – – – – –

A.anisophyllus n.s. – – n.s. – – n.s. – – n.s. – – n.s. – –

Intercept 0.84^*** 0.84^*** 1.03^*** 0.53^*** 0.51^*** 0.64^*** 0.53^*** 0.44^*** 0.52^*** 0.61^*** 0.58^*** 0.79^*** 0.61^*** 0.56^*** 0.61^***

AIC 84.34 84.34 87.67 34.19 45.31 47.75 36.23 43.52 43.58 106.37 107.33 110.00 63.63 65.42 63.63

R² 0.47 0.47 0.40 0.72 0.62 0.58 0.60 0.53 0.51 0.46 0.43 0.37 0.36 0.36 0.36

N 48 48 47 50 38

***P<0.001.

** P<0.01.

* P<0.1.

“n.s.”meansthatthefactorswerenotselectedbythebest-fitmodel.“–”meansthatthefactorwerenotusedforthemodel.

Fig.2.Temporalvariationsin(a)airtemperature,(b)soilmoisture,and(c)R_wood betweenJanuary2012andJuly2014.Linesin(c)showecosystem-R_woodvaluesesti- matedusingalinearregressionmodelwithsoilmoisture.Circlesin(c)indicate ecosystem-R_woodvaluesthatwereestimatedusingthebest-fitmodelanderrorbars indicatethe95%confidencelineofthemodel.

3.2. Temporalvariationsinecosystem-R_wood,R_foliage,andGPP Seasonalvariationsinairtemperatureandsoilmoisturewere notclear,althoughairtemperaturedecreasedinJanuary2014,and soilmoisture decreased in June 2013and March 2014(Fig.2).

Onthe otherhand,hightemporal variationin ecosystem-R_wood wasobserved(Fig.2),withbest-fitmodelestimatesof2.48±0.34, 1.68±0.20,1.32±0.21,2.08±0.40,and1.44±0.43␮molm⁻²s⁻¹ duringJanuary2012,May2013,July2013,December2013,andJuly 2014,respectively (Table2).Estimatesofecosystem-R_woodfrom eachmodelweresignificantlyrelatedtoSWCexceptforModel2 (Table3)butwerenot relatedtoair temperature.Annual-R_wood between2012and2013estimatedfromthelinearregressionmodel withthepredictorofSWCforBest-fitmodel,Model1,Model2,and Model0were7.06±2.09,7.07±2.18,6.68±2.26,and8.56±2.20 MgCha⁻¹year⁻¹,respectively.Ecosystem-R_woodandannual-R_wood werecomparablebetweenthebest-fitmodel,Model1,andModel2,

butModel0gavehighervaluesthantheothermodels(Table2), suggesting that sg is necessary for scaling, and that DBH and treespeciesarenot.Annual-R_foliageandGPPwere9.54±0.46and 42.99±6.74MgCha⁻¹year⁻¹,respectively,andratiosofR_woodand R_foliage toGPPwere0.17±0.05 and0.23±0.01MgCha⁻¹year⁻¹ (MgCha⁻¹year⁻¹)⁻¹,respectively.

3.3. EffectoflargetreesonR_woodandabovegroundbiomass The number of large trees strongly influenced aboveground biomass,butlessstronglyinfluencedecosystem-R_wood.Largetrees werepresentinthestudysiteat16.5treesha⁻¹,accountingfor only3%ofalltrees(567treesha⁻¹),theycomprised21%oftotal ecosystem-R_wood,38%oftotalabovegroundbiomass,and16%of totalwoodysurfacearea(Fig.3).Thehighercontributionoflarge trees(38%)toabovegroundbiomassthantosurfacearea(16%)was causedbythedifferencesinallometricequations.Theallometric equationfor aboveground biomasshasan exponentialfunction (Yamakuraetal.,1986),whereastheallometricequationforsur- faceareahasalogarithmicfunction(Chambersetal.,2004).Thus, abovegroundbiomassexponentiallyincreasedwithDBH,whereas theincrease ratio ofa woody surface areawithDBHgradually decreasedwithDBHandalmostsaturatedathighDBHontheindi- vidualscale.Aschamber-R_woodincreasedwithDBH,theratioof largetreestoecosystem-R_wood(21%)wasslightlyhigherthanthe ratiotowoodytissuesurfacearea(16%).Accordingly,decreasein standdensityoflargetreesmorestronglyaffectedaboveground biomassthanecosystem-R_wood(Fig.4).Whenstanddensitiesof largetreesweredecreasedby55%tolevelsthatarecomparable tothose inNeotropicalareas(7.5treesha⁻¹;Paolietal.,2008), abovegroundbiomassdecreasedto79%,andecosystem-R_woodwas decreasedto87%.Accordingly,AGBwasdecreasedto62%inthe absence of large trees in this forest and ecosystem-R_wood was decreasedto79%,suggestingthatwhereasstanddensitiesoflarge trees affectaboveground biomass considerably,theireffects on ecosystem-R_woodaremoderate.

4. Discussion

4.1. Inter-individualandtemporalvariationinR_wood

Sgwasthemostimportantfactoraffectinginter-individualvari- ationinchamber-R_woodforallmeasurementperiods,ratherthan DBHortreespecies(Table1).DBHand/orsghavebeenusedfor scalinginpreviousstudiesintropicalareas(MeirandGrace,2002;

Table2

Ecosystem-Rwoodandannualecosystem-Rwoodwithsoilmoistureestimatedbydifferentmodels.Multi-regressionanalyseswereconductedforecosystem-Rwoodestimates.

Predictorvariablesforthebest-fitmodelweredeterminedaccordingtothelowestAICvaluefromallpredictorsincludingstemgrowthrate(sg),dbhandtreespecies.

PredictorvariablesofModel1andModel2aresgandDBH,andsg,respectively.Annualecosystem-Rwoodwasestimatedbylinearregressionmodelwhichobjectivevariables wereecosystem-RwoodforeachmodelandpredictorvariableisSWCforeachmeasurementsperiod.

Measuredvalue Ecosystem-Rwood(␮molm⁻²s⁻¹) Annualecosystem-Rwood(MgCha⁻¹year⁻¹)

SWC(m³m⁻³) Bestmodel Model1 Model2 Model0 BestModel Model1 Model2 Model0

Jan-12 0.303±0.004 2.48±0.34 2.48±0.34 2.37±0.41 2.85±1.5 7.06±2.09 7.07±2.18 6.68±2.26 8.56±2.20 May-13 0.287±0.004 1.68±0.20 1.65±0.22 1.56±0.27 2.04±1.20

Jul-13 0.239±0.001 1.32±0.21 1.34±0.22 1.27±0.27 1.67±1.10 Dec-13 0.309±0.005 2.08±0.40 2.08±0.40 1.91±0.49 2.53±1.80 Jun-14 0.253±0.003 1.44±0.43 1.47±0.37 1.44±0.43 1.88±1.34

Table3

Statisticalresultoflinearregressionanalysisfortemporalvariationinecosystem- Rwood.

Bestmodel Model1 Model2 Model0 Coefficientsofindependentvariables

SWC 18.17^* 17.46^* 15.43 18.16^*

Intercept −3.36 −3.16 −2.68 −2.97

R² 0.75 0.71 0.65 0.72

*P<0.1.

Fig.3. RatioofeachDBHclassestoecosystem-R_wood,abovegroundbiomass(AGB), surfaceareasofwoodytissue(SA),andnumbersoftrees(number).

Chambersetal.,2004;Robertsonetal.,2010).DBHisanindica- torofsapwoodvolume,andchamber-R_woodincreaseswithDBH becausesapwoodvolumedirectlyaffectsmaintenancerespiration, reflecting increases in livecell numberswith sapwoodvolume (Ryanetal.,1994).Thus,strongrelationshipsbetweenchamber- R_woodandDBHhavebeenshownpreviously.However,thepresent studysuggestedthatDBHwasnotparticularlyimportantforscal- inginthisstudy,potentiallyreflectingdifferencesinmeasuredtree sizes.WemeasuredmultipletreeswithDBHof>100cm,whereas chamber-R_woodwasmeasuredfortreeswithDBH<100cminpre- viousstudies.For suchlargetrees,sapwoodvolumesunderthe collarmaynotincreasewithDBH,probablyowingtolimitedsap- wooddepthof<10cm(Ichie,unpublisheddata).Atthestudysite, sapwooddepths,whichweremeasuredbydyeexperiments(Ichie etal.,unpublisheddata),didnotcorrelatewithDBH(n=34,P=0.66, 32<DBH<106cm),suggestingthatsgisthemostsignificantpre- dictorofinter-individualvariationinforestswithverylargetrees.

Inthepresentbest-fitmodel,chamber-R_woodforD.aromatica washigherthanthatforS.beccariana,especiallyinJuly2013(Fig.

A3).However,DBHandsgofmeasuredtreesdidnotdifferbetween the two species (P>0.1, respectively). Differences in chamber- R_woodmaybereflectedbythedifferenceinsapwooddepthsand wooddensitybetweenthetwospecies.SapwooddepthsforD.aro- matica(5.4±1.4cmfortreeswithDBHof59–96cm,n=3)were

50%

60%

70%

80%

90%

100%

0% 50% 100%

Decreased ratio in ecosystem-Rwood and AGB

Decreased ratio in stand denstiy Rwood AGB

Fig.4.Decreasedratiosofecosystem-R_woodandabovegroundbiomass(AGB)with differentstanddensityoflargetrees;100%,actualstanddensityoflargetrees(16.5 treeha⁻¹).

significantlyhigherthanthose forS.beccariana(3.2±0.4cmfor treeswithDBHof93–102cm,n=3,P<0.05;Ichieetal.,unpublished data,Fig.A4).Wood densityforD.aromatica(0.796gcm⁻³)was higherthanthatforS.beccariana(0.531gcm⁻³,Inoueunpublished data).Thedifferencemayresultinhigherconstructionrespiration forD.aromaticathanforS.beccarianawithcomparablesgbecause constructionrespirationcanbeestimatedbysgandwoodydensity (e.g.,Ryan,1991;Ryanetal.,1994).Hence,highersapwoodvolumes and wood density mayhave affectedspecies-specific chamber- R_woodinthisstudy,eventhoughthesespeciesbelongtothesame dipterocarpfamily.

Thetemporalvariationinecosystem-R_woodinthepresentstudy wasassociatedwithsoilmoisturedespitetheabsenceofaregu- larseasonaldryperiod(Table3,Fig.2).Thisfindingmaybedueto growthphenology,giventhatR_woodseasonallyincreasedingrow- ingstems(e.g.,Ryan and Yoder,1997)and stemthegrowthof severaltreespeciesofDepterocarpaceawasobservedafterdrought (Ichieetal.,2004).R_woodalsorespondedtosoilmoisturecondi- tionsandlikelyreflectedstemgrowthphenologyinNeotropical rainforests,wherestemgrowthishighestatthestartofthewet seasonandlowestatthestartofthedryseason(Chambersetal., 2004;Malhietal.,2014).Incontrast,Cavalerietal.(2006)reported noseasonalityinR_wood inCostaRica,where therewerenodis- tinctdryseasons,asisthecaseinBorneanforests.Cavalerietal.

(2006)attributedtheabsenceofseasonalvariationinR_woodtothe asynchronyofthephenologiesofallspecies.Thus,stemgrowth phenologyinresponsetosoilwateravailabilityislikelylinkedwith temporal variationin R_wood intropical rainforests.Thereis also anotherpossibility:moreCO₂respiredforrootsmightbetrans- ported bythetranspirationstreamand releasedfromthestem becauseoflowdiffusioninwetsoil(Teskeyetal.,2008).Continuous

measurementsofchamber-R_woodandstemgrowthratesinaddition tosapfluxmeasurementsarenecessaryforaninvestigationofthe causeofincreaseinecosystem-R_woodinawetperiod.

Therangeof temporalvariation inecosystem-R_wood(ratioof highesttolowestecosystem-R_wood,1.89)washigherinthisstudy sitethanthatobservedinNeotropicalforests(1.30,Chambersetal., 2004).Moreover,thelowestecosystem-R_woodwasobservedduring aseveredroughtinJune2013,andwasfollowedby“generalflow- ering,”withmastingatthecommunitylevelatirregularintervals ofonetoseveralyears(Sakaietal.,2006;Nakagawaetal.,2012).

Thephenomenon of generalflowering is reported in aseasonal tropicalrainforestsinAsiaandislikelytriggeredbyunexpected droughtsinLambir(Sakaietal.,2006).Strongtemporalvariation innetprimaryproductionwasalsoreportedinastudyinLambir thatincludedaperiodofgeneralflowering(Khoetal.,2013),and annualabovegroundbiomassincrementsdecreasedintheyearof generalflowering,whereaslitterfallofflowersandseedssignifi- cantlyincreased(Nakagawaetal.,2012).Thesestudiesindicatethat generalfloweringfollowsdynamictemporalvariationinnetpri- maryproductionandR_wood,reflectingincreasedcarbonallocation tothecanopyforreproductiveorgansduringgeneralflowering.

4.2. Annual-R_woodandimpactoflargetrees

Annual-R_woodestimatesbasedonthebest-fitmodelwerecom- parabletothosebased onModel1andModel2, suggesting that DBHand treespeciesarenotalwaysnecessaryfor estimatesof ecosystem-R_woodinthisstudysite.Incontrast,annual-R_woodbased onModel0 was higher than that from the best-fit model, and thedifference(1.50±3.03MgCha⁻¹year⁻¹)washigherthanthe netecosystemproductioninaNeotropicalforest(0.71±9.34MgC ha⁻¹year⁻¹,Phillips etal.,1998)andwasmorethanhalfofthe netecosystemproductioninanold-growthforest(2.4±0.8MgC ha⁻¹year⁻¹,Luyssaertetal.,2007).Thesedatasuggestthatscaling byaveragesonlymayleadtolargeerrors.Nonetheless,thisdiffer- encelikelyreflectsdifferencesinsgdistributionbetweensampled treesandthoseinthepresent4-haplot.Accordingly,averagemea- suredsg(0.80±0.95cmy⁻¹)wasmuchhigherthanthatinthe4-ha plot(0.2±0.3cmy⁻¹).Thus,sgdistributionsshouldbeconsidered duringscalingofaveragedchamber-R_woodvalues.

Annual-R_woodvaluesdifferedamongthestudysites(Table4).

This variation was not explained by aboveground biomass, althoughsomestudieshaveshownpositiverelationshipsbetween plantrespirationandbiomass(KiraandShidei,1967;Deluciaetal., 2007).Inthepresentstudy,possiblefactorsaffectingvariationin annual-R_woodamongforestssuchasSAI,chamber-R_wood,andsamp- lingmethodarediscussedusingcomparisonsofannual-R_woodand biomasswiththoseofpreviousstudies(Table4).Comparedwith annual-R_woodvaluesobservedinPeru(Malhietal.,2014),annual- R_wood values in thepresent studysite were similardespitethe twicehigherabovegroundbiomass.ComparableSAIandchamber- R_woodledtocomparableannual-R_woodbetweenthetwostudysites.

Higherstanddensityoflargetreesin thepresentstudysiteled tohigherbiomassbutcomparableSAI.ComparedwithbothBrazil studies(daCostaetal.,2013;Doughtyetal.,2013),annual-R_woodin thisstudysitewaslowerdespitehigherbiomass.Lowerchamber- R_woodandslightlyhigherSAIinthisstudysiteresultedinlower annual-R_wood.Cavalerietal.(2006)reportedmuchlowerabove- groundbiomassbutslightlylowerannual-R_woodinCostaRica.The reasonfortheseresultsmaybeattributedtothedifferenceinthe samplingmethod;theymeasuredchamber-R_woodfor lianas and palmsinadditiontoverticalvariationfortrees.Lianaandpalms accountedfor24and 9%oftotalR_woodintheforest,andunder- estimatesusingdatawithnoverticalmeasurementshaveoften beenreported(e.g.,Katayamaetal.,2014).Theseresultssuggest thatannual-R_woodinthepresentstudyandpreviousstudiesmay

beunderestimated.Considerationoftreesizedistributions,inaddi- tiontodifferencesinSAI,chamber-R_woodandsamplingdesign,may bethekeytounderstandingtherelationshipbetweenecosystem- R_woodandbiomassacrossvariousforests.

GPPandannual-R_foliage werethehighestandsecondhighest, respectively,amongtropicalrainforestsreportedintheliterature, whereasratiosofR_woodandR_foliagetoGPPwerewithintherangeof thoseshowninNeotropicalforests(Table4).MostratiosofR_wood andR_foliagetoGPPinthisstudyandothertropicalrainforestswere higherthantheaveragesforvariousforestecosystems,including borealandtemporal,andyoungandold-growthforests(0.16and 0.16,respectively,Littonetal.,2007).Hence,ratiosofR_abovetoGPP (0.38–0.51)were higherthantheaverageamong variousforest ecosystems(0.32,Littonetal.,2007).Inagreement,previousstud- iesshowedthatratiosofplantrespirationtoGPPwerehigherin tropicalforeststhanintemperateforests(Luyssaertetal.,2007;

Piaoetal.,2010).Althoughthecausesofthesedifferencesremain unclear,hightemperatures(Piaoetal.,2010),biomass(Kiraand Shidei,1967), andstandages(Deluciaetal.,2007)mayleadto higherratiosinmaturetropicalrainforests.

We estimated annual-R_wood with consideration of inter- individualandtemporalvariationinthepresentstudy,butthereare stilllargeuncertaintiesineachcomponentoftheGPPestimate.For annual-R_wood,therearefourmajorsourcesofuncertainty.First,ver- ticalvariationforsmallertreesandbrancheswasnotinvestigated, andcanleadtounderestimateswhenmeasurementsareconducted onlyatbreastheight(e.g.,Katayamaetal.,2014).Second,tempo- ralvariationwasinvestigatedinthepresentstudy,butonlyfor fivemeasurementscampaign,resultinginlargeerrorsinannual- R_wood.Toimproveaccuracy,relationshipsofenvironmentalfactors withtreephenologyshouldbeexaminedbymoremeasurement timeseries.Third,thesurfaceareaofwoodytissuewasestimated byanequationobtainedinthecentralAmazon(Chambersetal., 2004).Itisreportedthatheight–diameterrelationshipsweredif- ferentamongcontinents;foragivendiameter,stemsweretallest inAsia,followedbyAfrica,America,andAustralia,basedonameta- analysis(Baninetal.,2012).Thisresultsuggeststhatanequationfor woodytissuesurfaceareausingDBHmaybedifferentandunder- estimatedecosystem-R_woodinthepresentstudy.Finally,thereis considerableuncertaintywhetherthesourceofchamber-R_woodcan include root-respiredCO2 and stem-respiredCO2 can betrans- portedtothecanopy(Teskeyetal.,2008).Thisisoftenassociated withdiurnalvariationinchamber-R_wood.Differentdiurnalvariation inindividualtreesmaybeaffectedbythisuncertainty.

ThereareuncertaintiesinothercarbonfluxesusedforGPPesti- mation.Forannual R_foliage,seasonalvariationsinR_foliage and LAI werenotconsideredinthepresentstudyandthevariationsmay leadtounder-oroverestimationalthoughR_foliage attheecosys- temscaledidnotvaryseasonallyinPeru(Malhietal.,2014)and Brazil(Metcalfeetal.,2010).Inthepresentstudy,R_foliageat25^◦C wasestimatedusingQ10of2.3reportedinCostaRica.IfQ10value of2.0,whichwasreportedinAustralia(Weerasingheetal.,2014), isusedfortheestimateinthepresentstudy,annual-R_foliageisesti- matedas10.23MgCha⁻¹year⁻¹,suggestingunderestimationinthe presentstudy.Aswell,therearelargeuncertaintiesinTBCFinthe presentstudysite.TBCFwasestimatedasthedifferencebetween annualsoilCO2 effluxandannuallitterfall-C,basedonasteady- stateassumption(RaichandNadelhoffer,1989),whereasTBCFwas estimatedasasumofbelowgroundrespirationandnetprimary productioninpreviousstudiesinTable4.Furthermore,annualsoil CO₂ effluxwasestimatedbymeasurementsonlyinthedaytime andtemporalvariationwasnotconsidered.Thispracticemaylead tooverestimationduetodiurnalvariationinsoilCO2efflux.

Climatechangeispredictedtocausemorefrequentdroughtsof greaterseverityintropicalareasMalhiandPhillips(2004).Drought mayaffectphenologyandcarbonallocationinthepresentstudy

Table4

Abovegroundbiomass,annual-Rwood,annual-Rfoliage,annual-Rabove,GPPandratiostoGPPinvarioustropicalrainforests.

Site Malaysia CostaRica French

Guiana

Brazil Brazil Peru

Borneo LaSelva Paracou Caxiuana

tower

Caxiuana Terrapreta

Caxiuana Control

Caxiuana Dry

TAM-05 (Nutri- entpoor)

TAM-06 (Nutri- entrich) Aboveground

biomass (MgCha⁻¹)

272.4 81 228 179.5 110.9 213.9 200.6 138.2 115.6

Annual-Rwood

(MgCha⁻¹ year⁻¹)

7.06±2.09 5.08±1.35 5.44±0.99 8.71±1.07 8.46±2.82 10.21±4.49 11.17±4.96 5.43±1.77 7.62±2.48

Surfacearea index(m²m⁻²)

2.01 1.1(diame-

ter<10cm)

1.3 1.65 1.63 − − 1.98 2.09

AverageCham- berRwood

0.81±0.52 (dry) 1.39±0.74 (wet) 1.07±0.48 (average)

0.60(DBH of10cm) 0.83(DBH of80cm)

1.13±0.55 (dry) 1.56±0.65 (wet)

2.08±0.15 2.11±0.17 1.61±0.12 1.94±0.19 0.95±0.03 1.03±0.08

Scalingfactors Growth, dbh, species

Growth, diameter, Species, height, slope

Average Growth Growth Growth

Samples DBH>10cm Alltrees, Liana,Palm

DBH>10cm Alltrees Alltrees Alltrees

Annual-Rfoliage

(MgCha⁻¹ year⁻¹)

9.54±0.46 − 11.59±0.54 5.02±1.58 5.09±1.67 5.69±2.14 9.26±3.63 8.86±2.84 6.43±2.07

Annual-Rabove

(MgCha⁻¹ year⁻¹)

16.60±2.14 − 17.03±0.55 13.73±4.4 13.55±4.49 15.9±6.63 20.43±8.59 14.29±4.61 14.05±4.55

ANPP 6.76±0.57 − − 9.35±0.49 8.75±0.59 6.78±0.14 5.71±0.20 9.96±0.83 11.59±1.62

TBCF 19.63±6.37 − − 9.01±1.22 13.3±1.62 16.5±4.03 14.3±4.20 11.26±1.11 8.85±1.06

GPP(MgCha⁻¹ year⁻¹)

42.99±6.74 − 37.57 32.08±3.46 35.68±3.65 39.18±1.81 40.44±6.39 35.47±3.55 34.47±3.53 Rwood/GPP 0.17±0.05 − 0.14 0.27±0.09 0.24±0.08 0.26±0.12 0.28±0.13 0.15±0.05 0.22±0.08

Rfoliage/GPP 0.23±0.01 − 0.31 0.16±0.05 0.14±0.05 0.15±0.06 0.23±0.10 0.25±0.08 0.19±0.06

Rabove/GPP 0.40±0.06 − 0.45 0.43±0.11 0.38±0.10 0.41±0.14 0.51±0.17 0.40±0.10 0.41±0.10

Reference Thisstudy Cavaleri etal.,2006

Stahletal., 2011

Doughty etal.,2013

daCosta etal.,2013

Malhietal., 2014 Rowland

etal.,2014

daCosta etal.,2010 site,andseveredroughtofteninduceshightreemortality(Allen

etal.,2010).InLambirHillsNationalPark,severedroughtcaused byElNinoin1997–1998inducedhightreemortality,especially amonglargetrees(Nakagawaetal.,2000).Recentstudiesalsoshow thatlargetreesdriveforestabovegroundbiomassvariationinmoist lowlandforestsacrossthetropics (Slik etal.,2013)and higher stemgrowthattheplotlevelinBorneo(Baninetal.,2014).These observationssuggestthatlargetreesareimportantcarbonstores.

PreviousstudiesinLambirshowedthatpartialvariationinsoilCO₂ effluxwasaffectedbylargetrees(Katayamaetal.,2009),andsoil CO2 effluxwashigherinthepresenceofemergenttrees(Ohashi etal.,2014).Moreover,photosyntheticabilityreportedlyincreases linearlywithheight(Kenzoetal.,2015),suggestinghigherpho- tosynthesisratesforlargertrees.Hence,soilCO2effluxandGPP mightdecreasewiththelossoflargetreesduetoseveredroughts, whereasR_woodmightbeconserved.Takentogether,futureclimate changecanaltercarboncyclingthroughthechangeincarbonallo- cationnotonlybythephysiologicalandphenologicalresponseto droughtforlargetrees,butalsochangesinnumberoflargetrees.

5. Conclusions

Wemeasuredchamber-R_wood intrees ofvariousspecies and sizes in a Bornean tropical rainforest. All measurements were performedfive times between2012and 2014,and subsequent analyses indicated that the factor of stem growth rate was

themostimportantdeterminantofinter-individualvariationin chamber-R_wood,followedbyDBHandtreespecies.Inthis study, ecosystem-R_woodwasestimatedbasedonthemodelforindividual chamber-R_woodusingthepredictivefactorsofstemgrowthrate, DBH,andtreespecies,andtheaveragemeasuredchamber-R_wood value.Estimatesofecosystem-R_woodusingstemgrowthrateonly weresimilartothoseestimatedusingtheallfactors,whereasmean measuredecosystem-R_woodwashigherthanthatestimatedusing regressionmodels,suggestingthatspatialscalingshouldbecon- ducted withconsideration of factorsthat affectchamber-R_wood. Moreover,ecosystem-R_woodvariedtemporally,reflectingchanges insoilmoisturedespitetheabsenceofaregularseasonaldryperiod.

Thesedatasuggestthatcarbonallocationmaydynamicallyvary withtimeandchangesinsoilmoisture.Annual-R_woodvalueswere comparabletothoseinNeotropicalforests,despitehigherabove- groundbiomassinthepresentBorneanstudysite.Higherstand density of largetrees caused higher aboveground biomass, but comparableecosystem-R_woodcomparedwithNeotropicalforests.

Althoughtheeffectsofstandageorbiomassonautotrophicrespira- tionremainunclear,thepresentdatasuggeststhatstandstructure maymediatetheseeffectsonrespirationattheecosystemscale.

Acknowledgments

WethanktheForestDepartmentofSarawakandtheSarawak ForestryCorporationfortheirpermissionandkindassistancein