Temperate and Tropical Forest Canopies are Already Functioning beyond Their Thermal ...

24 Pages·2017·2.15 MB·English

Article
Temperate and Tropical Forest Canopies are Already
Functioning beyond Their Thermal Thresholds
for Photosynthesis
AlidaC.Mau1,SashaC.Reed2,TanaE.Wood3andMollyA.Cavaleri1,*
1 SchoolofForestResources&EnvironmentalScience,MichiganTechnologicalUniversity,1400TownsendDr.,
Houghton,MI49931,USA;[email protected]
2 U.S.GeologicalSurvey,SouthwestBiologicalScienceCenter,2290S.WestResourceBlvd,Moab,UT84532,
USA;[email protected]
3 USDAForestService,InternationalInstituteofTropicalForestry,JardínBotánicoSur,1201CalleCeiba,
RíoPiedras,PR00926-1115,USA;[email protected]
* Correspondence:[email protected];Tel.:[phone]
Received:21December2017;Accepted:15January2018;Published:22January2018
Abstract: Tropicaltreespecieshaveevolvedunderverynarrowtemperaturerangescomparedto
temperateforestspecies. Studiessuggestthattropicaltreesmaybemorevulnerabletocontinued
warming compared to temperate species, as tropical trees have shown declines in growth and
photosynthesisatelevatedtemperatures. However,regionalandglobalvegetationmodelslackthe
dataneededtoaccuratelyrepresentsuchphysiologicalresponsestoincreasedtemperatures,especially
fortropicalforests. Toaddressthisneed,wecomparedinstantaneousphotosynthetictemperature
responsesofmaturecanopyfoliage,leaftemperatures,andairtemperaturesacrossverticalcanopy
gradientsinthreeforesttypes: tropicalwet,tropicalmoist,andtemperatedeciduous. Temperatures
atwhichmaximumphotosynthesisoccurredweregreaterinthetropicalforestscanopiesthanthe
temperatecanopy(30±0.3◦Cvs.27±0.4◦C).However,contrarytoexpectationsthattropicalspecies
would be functioning closer to threshold temperatures, photosynthetic temperature optima was
exceededbymaximumdailyleaftemperatures,resultinginsub-optimalratesofcarbonassimilation
for much of the day, especially in upper canopy foliage (>10 m). If trees are unable to thermally
acclimatetoprojectedelevatedtemperatures,theseforestsmayshiftfromnetcarbonsinkstosources,
withpotentiallydireimplicationstoclimatefeedbacksandforestcommunitycomposition.
Keywords: forestcanopies;tropicalforests;photosynthesis;temperature;climatechange
1. Introduction
Temperateandtropicalforestsmakeupmuchoftheworld’sbiomass,withtropicalforestsalone
accounting for over 60% of terrestrial global carbon [1]. Forests can mitigate the effects of climate
change,suchaselevatedtemperature,throughcarbondioxide(CO )uptakeduringphotosynthesis.
2
However,globalsurface-airtemperatureisexpectedtoincreaseby1to5◦Cby2100,withaneven
greaterincreaseexpectedinnorthernlatitudes,alongwithanincreaseinthefrequencyandintensity
ofshort-termheatwaves[2,3]. Astemperaturesincrease,thereisatheoreticalthermaltippingpoint
afterwhichphotosynthesisbeginstodeclinewhileplantrespirationmaystillbeincreasing. Ifdeclines
inCO uptakearesevereenoughthatforest-widerespirationexceedsphotosynthesis,forestscould
2
become net sources of carbon to the atmosphere [4,5]. Determining where this thermal threshold
existsandwhetherdifferentforesttypesareclosetoshiftingfromcarbonsourcestosinksiscrucialto
understandingandmodelingglobalclimatefeedbacks[6].
ManyglobalvegetationmodelsarebasedonFarquhar’smodelofphotosynthesis[7],butour
ability to accurately parameterize these models is hampered by a lack of mechanistic data on
Forests 2018,9,47;doi:10.3390/f9010047 www.mdpi.com/journal/forests
Forests 2018, 9, x FOR PEER REVIEW 2 of 24
Many global vegetation models are based on Farquhar’s model of photosynthesis [7], but our
ability to accurately parameterize these models is hampered by a lack of mechanistic data on
Forests 2018,9,47 2of24
physiological responses to warming and thermal acclimation potential of canopy photosynthesis
and respiration, especially for tropical forests [8–16]. Models analyzing the responses of tropical
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athrearneg eiso af tsecmarpceitrya toufr edsaatare onf etchees ssahroyrtto-teimrmp reofvfeecmts oodf eelsleavnadtesde tteambpaseeralitnueretos donet eprhmoitnoesyhnotwhecslios sien
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scarciLtyigohft dsaattauorafttehde pshhoortto-steyrnmtheeftfiecc trsesopfoenlesve attoe dtetmemppereartauturer eisnocrnepasheost otosy an tmheasxisiminumma (tAuropet)f oarte asnt
coapntoimpiuesma nldeaffo rtelmonpge-rteartumrete m(Tpopet)r,a ttuhreen acdcelcimreaatsieosn a[2g4a]i.n, following a parabolic curve (Figure 1)
[7,25L,2ig6]h. t saturated photosynthetic response to temperature increases to a maximum (A ) at an
opt
optimumleaftemperature(T ),thendecreasesagain,followingaparaboliccurve(Figure1)[7,25,26].
opt
9.5
9.0 Aopt=8.8 µmolCO2m-1s-2
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1 8.5
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T = 29°C
6.5 opt
20 22 24 26 28 30 32 34 36 38
Temperature (°C)

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Aopt.
Below T , photosynthesis typically increases as the rates of biochemical reactions increase
opt
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photosynthetic decline occurs at leaf temperatures between 26 and 32 °C, due to direct biochemical
limitationsand/ortoindirectstomatalresponsestoincreasesinvaporpressuredeficit[7,26]. Thetwo
limitations and/or to indirect stomatal responses to increases in vapor pressure deficit [7,26]. The
components of net photosynthesis commonly used for model parameterization are the rate of
two components of net photosynthesis commonly used for model parameterization are the rate of
ribulose-1,5-bisphosphate (RuBP) carboxylation (V ) and the rate of RuBP regeneration from
cmax
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a ctivase (Rubisco activase) and thylakoid membrane dysfunction, which affects efficiency of light
reactionsandelectrontransport[29,30],andincreasedratesofphotorespirationduetothedecreaseof
Forests 2018,9,47 3of24
bothspecificityofRubiscoforCO andtherelativesolubilityofCO versusO [31]. Irreversibleleaf
2 2 2
damagefromhightemperaturestypicallybeginsabove45◦Casplasmamembranesinthechloroplast
becomepermeableandproteinsbegintodenature[26].
Perhapsduetorelativelylowdiurnalandinter-annualvariability,tropicaltreeshavebeenshown
tobemoresusceptibletowarmingincomparisontotemperateandborealspecies,andhaveshown
photosyntheticdeclinesattemperaturesofonly3◦Cabovemeanambientairtemperatures[32,33].
Recent evidence suggests that lowland tropical forests, which are already consistently warm
throughouttheyear,mayalreadybeoperatingclosetotheirphotosyntheticthermaloptima,beyond
which carbon uptake declines [5,22,34–38]. Due to greater diurnal, seasonal, and inter-annual
variabilityintemperatureintemperateecosystems,therangeoftemperaturefromambienttoT will
opt
likelybegreaterintemperatespeciesandthereforethesehighlatitudespeciesmaynotbeoperatingas
closetotheirthermalthresholdsastropicalspecies[25,32,39–41].
Foraccuratemodelrepresentation,itisimportanttomeasurephotosynthesisacrosstheentire
vertical transect of the canopy, as upper and lower branches have different traits, are exposed to
different environmental gradients, and can respond differently to temperature [42]. For example,
lightconditionsarehighlyvariableacrossaverticalgradientwithincanopiesduetodensityoffoliage
limitinglightaccessinthelowercanopy[40,43],andlightcanbeespeciallylimitinginecosystems
withhighannualcloudcoverandmeanannualprecipitation(MAP),suchastropicalrainforests[44].
Aslightavailabilitytypicallyincreaseswithcanopyheight,leaftemperaturedoesaswell. Thedirect
radiationhittinguppercanopyleaveswarmssunleavesmorethandiffusescatteredlightinlower
shadedleaves[45]. Inmanyforests,leaftemperaturescanbe1–7◦Caboveambientairtemperature,
especiallyintheuppercanopy[46]. Therefore,uppercanopyleavesofbothtemperateandtropical
specieshavebeenshowntohavegreaterphotosyntheticcapacity,buttheyalsomaybemoresusceptible
toheatstressduetoelevatedtemperaturesandvaporpressuredeficit[47].
Variousleaffunctionaltraitscanalsobestrongpredictorsofphotosyntheticcapacityand,inturn,
photosynthetic response to elevated temperature. Leaf nitrogen (N) content in canopies has been
foundtocorrelatewithgreaterphotosyntheticcapacityinvariousforesttypes[48–50],andleaf-area
basedphosphorus(P)hasalsoshownsimilarpatternsacrossuppercanopygradientsaslight-saturated
ratesofphotosynthesis[51–53]. Additionally,leafmassperarea(LMA)isanextremelyusefulleaf
traitthatcorrelateswithnumerouswithin-canopytraitsthataremorechallengingtomeasure(e.g.,
gasexchange,leafnutrients)[54]. LMAtypicallyincreaseswithheightintemperateandtropicalforest
canopies,eitherduetolightorhydrostaticgradients[55–57]andsinceLMAhasbeenfoundtohave
significantrelationshipswithlightsaturatedratesofphotosynthesis(A ),itmayalsobeastrong
max
predictorofmaximumratesofphotosynthesisundervaryingtemperatures[12,56,58]. Thus,leafP,
N,and/orLMAmaybeabletopredictphotosynthetictemperatureresponseparameters(A and
opt
T ). ThehighlyweatheredclaysoilsoftropicalforestsareoftenconsideredtobemorelimitedbyP
opt
whiletheyoungertemperateforestsaregenerallyconsideredtobemorelimitedbyN[59–61]. Wemay
thereforeexpectPtobestronglycorrelatedtophotosyntheticparametersinthetropicalforestwithN
moreimportantinthetemperateforestcanopies[62–64].
Overall, this study sought to investigate how ambient leaf temperatures and instantaneous
photosyntheticresponsestotemperaturevariedwithinmaturetreecanopiesandacrossthreeforest
types: temperate deciduous, tropical moist, and tropical wet, in order to see how close to their
physiological temperature optima the dominant tree species of these forests may be operating.
Ourspecifichypotheseswere:
(A) Comparedtolowerleaves,uppercanopyleavesatallsiteswillhavehighertemperatureoptima
forphotosynthesis(T ),highermaximumratesofphotosynthesis(A ),andbothparameters
opt opt
willincreasewithincreasinglightavailability.
(B) T and A will increase with increasing mean annual temperatures across forest types,
opt opt
but tropical tree species will be functioning closer to photosynthetic thresholds than
temperatespecies.
Forests 2018,9,47 4of24
(C) T andA willincreasewithincreasingLMAatallsitesbutwillbebetterpredictedbyleafN
opt opt
inthetemperatesite,andleafPatthetropicalsites.
2. MaterialsandMethods
Samplingtookplacefromfourcanopyaccesstowersatthreesites: atemperatedeciduousforest
in Upper PeninsulaMichigan and two sites inPuerto Rico. The Puerto Ricosites weredefined as
subtropicalmoistandsubtropicalwetforests,respectivelybytheHoldridgelifezonesystemandboth
tropicalforestsweredominatedbybroadleafevergreentreespecies[19].
2.1. TemperateDeciduousForest
ThetemperatedeciduousstudysitewaslocatedattheMichiganTechFordCenterandForest
nearL’Anse,MI(46◦64(cid:48)N,88◦48(cid:48)W).Meanannualtemperature(MAT)was5◦C,thoughmeanannual
growingtemperature(MAGT)was17.4◦C.Meanannualprecipitation(MAP)was879mmfrom2009
to2011,with401mmoccurringduringthegrowingseason,typicallyMaythroughSeptember[65].
ThesoilatthesitewasanAllouezgravellycoarsesandyloam,extendingtoadepthof40cm(http:
//websoilsurvey.sc.egov.usda.gov/). Acersaccharumwasthedominantspeciesonthesite,makingup
97%oftotaltreedensity,withonlyfivespeciesperhectareatthesite. Othernon-dominantspecies
included Ulmus americana, Tilia americana, Betula alleghaniensis, and Ostrya virginiana. The average
heightofthecanopywas23m,whiletheaverageheighttolivecrownwas14m[56]. Foradditional
informationaboutforestcomposition,structure,andsitehistory,seeCampioneetal.[66].
Gas exchange and leaf trait data were acquired at the temperate site with a 19-m tall mobile
aluminumwalk-uptower(Upright,Inc.,Selma,CA,USA),constructedinthesummerof2012.
2.2. TropicalMoistForest
ThetropicalmoistforeststudysitewaslocatedinElTallonalForestReserve,a114haprivately
ownednaturalareainthemunicipalityofArecibo,PuertoRico(18◦40(cid:48) N,66◦73(cid:48) W).TheMATwas
25.5◦CandtheMAPwas1295mm(Table1). ThewetseasonatthissitelastsfromJulytoSeptember,
whilethedryseasonisgenerallyfromJanuarytoMarch. ThisnorthcentralregionofPuertoRicois
dominatedbykarsttopographyandhassoilsderivedfromlimestoneparentmaterialwithanoverlay
ofInceptisolsinthelowlyingvalleys[67]. Thereareanestimated24treespeciesperhectareatthesite,
andthedominanttreespeciesisCastillaelastica[68]. Theforestwasestimatedtobeover70yearsold
atthetimeofthestudy[68,69]. Historically,theareawasusedforgrazingcattleandagricultureuntil
1950,whentheselandswereabandonedandnaturallyregeneratedtoforest[69].
Table1.Siteinformationforeachtower.Speciesmeasured,elevation(metersabovesealevel),mean
annualprecipitation(MAP,mm),meanannualgrowingseasontemperature(MAGT,◦C),towerheight.
Species Elevation MAP MAGT TowerHeight
Site Measured SpeciesCode (m) (mm) (◦C) (m)
Temperate
Acersaccharum Acer 189 879 17.4 19
Deciduous
Ocotealeucoxylon Oco
TropicalMoist Guareaguidonia Gua 122 1295 25.5 25
Castillaelastica Cas
TropicalWet Dacryodesexcelsa Dac 361 3936 24.8 24.7
Two identical 25 m steel towers, constructed 12 m apart in 2008, were used at the tropical
moistforestsite(BilJax,Archbold,OH,USA).C.elastica,Guareaguidonia,andOcotealeucoxylonwere
measuredfromthesetowers. C.elasticaisafastgrowing,earlysuccessionalbroadleavedevergreen
treewithrelativelyhighLMAandlightsaturatedphotosyntheticrates(A )[70]. G.guidoniaisa
max
Forests 2018,9,47 5of24
mid-successionaldeciduoustreenativetoCentralandSouthAmerica[71,72]. O.leucoxylon,whichis
alsoaCaribbeannative,isanearlysuccessionalbroad-leavedevergreentree[73].
Leavesofthesethreespeciesweresampledfromsevenheights(7,12,14,16,20,22,and25m)
acrossbothtowers. Otherspecieswereaccessible,however,theywerenotsamplediftheywerenot
presentataminimumoftwoheights.
2.3. TropicalWetForest
ThetropicalwetforestwaslocatedintheLuquilloExperimentalForestinnortheasternPuerto
Rico(18◦31(cid:48) N,65◦74(cid:48) W)[19,74–76]. MAPofthesitewas3936mmandMATis25◦C,atanelevation
of361mabovesealevel[74]. Temperaturevariesjust4◦Cfrommonthtomonththroughouttheyear
withnodayswithtemperaturesbelowfreezing. AdrierseasontypicallyoccursfromJanuarythrough
April,whilethewettestperiodrangesfromMaytoNovember[75]. Thesoilsatthetropicalwetforest
areUltisols,clayeypoorlydrainedsoilwithredmottles[75]. Thisforestasawholeaverages10tree
speciesperhectare,withanaverageof516stemsperha[77,78]. Theaverageheightofthecanopywas
20m[79]. Dacryodesexcelsa(commonname: tabonuco),wasthedominanttreespeciesoftheforest[80].
DacryodesexcelsaisoneofthedominantnativetreesinPuertoRico,growingatelevationsbetween
200 to 800 m [81]. Other species located near the tower include: Prestoea montana, Casearia arborea,
Ingalaurina,Manilkarabidentata,andSloaneaberteriana[82]. Foradditionalsitehistory,see[75,83].
Thetropicalwetforesttowerwasa24.7-mtallmobilealuminumwalk-upbuiltin1991,witha
footprintof2.5m2 (Upright,Inc.,Selma,CA,USA)(Table1). Dacryodesexcelsawastheonlyspecies
accessibleacrosstheentireverticalcanopygradient. Dacryodesexcelsaisalong-livedbroad-leaved
evergreenspecies,anditisestimatedthatmaturetreesliveupto400yearswithaverageheightsof30
to35m[81]. Dacryodesexcelsahashistoricallyshownrelativelylowlightsaturatedphotosynthesis,
about 2.7 µmol CO m−2 s−1 [84]. Leaves were sampled from seven heights (8, 11, 15, 18, 20, 23,
2
and25m).
2.4. EnvironmentalMeasurements
Diffusenon-interceptance(DIFN%),definedasdiffuselighttransmittedthroughthecanopyasa
proportionofincident(abovecanopy)radiation,wasmeasuredateachstudysitewithanLAI-2200
(LI-CORBiosciences,Lincoln,NE,USA).DIFN%inforestsiscloselyrelatedtoseasonallyintegrated
photosyntheticphotonfluxdensity[85]andweuseithereasameasurementofcanopyopenness
andlightavailabilityintegratedovertime. ‘Abovecanopy’measurementsweretakenatthetopof
thetowers,andmeasurementsweretakenateverysamplingheightforeachtowerateachforestsite.
DIFN%wasonlysampledunderuniformlycloudyconditionswheneverpossibleatmid-dayforall
threesites,andawhitediffusercapwasusedtocorrectfordirectsunlightwhenuniformlycloudy
conditionswerenotpresent. DIFN%wasmeasuredon1June2014inPuertoRico,andon20June2014
inthetemperateforest.
Leaf temperature was measured using a Fluke 572 infrared thermometer (Fluke Corporation,
Everett,WA,USA).Fiveleavesofallaccessiblespeciesweremeasuredateverysamplingheightonce
anhour,forthreedaysatallsites. Leaftemperaturewasmeasuredfromthe1–5Juneandthe4–22
Augustatthetropicalmoistandtropicalwetsites,and8–16Augustatthetemperatedeciduoussite.
Air temperature was measured in thirty-minute increments and automatically logged from
26May–27August2014atthetropicalmoistandwetforests(HOBOProV2temp/RH,OnsetComputer
Corporation, Cape Cod, MA, USA). Air temperature sensors in solar shields were tethered to the
towerswithziptiesat5,15,and25matthetropicalmoistforest,andat7,13,18,and23matthe
tropicalwetforest. AirtemperaturedatawerecollectedatthetemperatedeciduousforestfromMayto
Augustof2013atheights3,8,and11m.
Forests 2018,9,47 6of24
2.5. SamplingDesignforPhotosyntheticMeasurements
In the temperate forest, photosynthetic temperature response curves were conducted on two
leaves of Acer saccharum at every accessible height of the tower. Leaves were collected from four
individualmaturetreesbetween7to20m,andfromfiveindividualunderstorysaplingsatlessthan
1minheight. Photosyntheticlightresponsecurveswereconductedontwohealthymatureleaves
atthetop(20m),middle(11m),andunderstory(<1m)toextractthelightsaturationpointforuse
intemperatureresponsecurves. Allphysiologicalmeasurementswereperformedfromthetowers
onintactleaves. Allsamplingfromthetemperateforestsitetookplaceduringthegrowingseason,
from7–21July2014between8amand4pm.
In the tropical wet forest site, two mature leaves of Dacryodes excelsa were measured at every
heightforthetemperatureresponsecurvesfromthreeaccessibletrees. Lightresponsecurveswere
taken on two healthy mature leaves at 25, 20, and 11 m to extract the light saturation point (the
lightconcentrationatwhichphotosynthesislevelsoff). Samplingtookplaceintwofieldcampaigns:
onefrom6–9June2014andanotherfrom6–28August2014between8amand4pm.
Inthetropicalmoistsite,twoleavesofeachspecies(C.elasticafromfourtrees,G.guidoniatwotrees,
andO.leucoxylontwotrees)weresampledateachaccessibleheightforthephotosynthetictemperature
responsecurves. C.elasticawassampledat12, 14, 16, 20and22m, G.guidoniaat8and12m, and
O.leucoxylonat20,22,and25m. Thelightsaturationpointusedforthesespecieswasfromaprevious
study[86]. Samplingtookplacebetween9amand5pmintwocampaigns: onefrom11–13June2014
andanotherfrom13–22August2014.
2.6. PhotosynthesisMeasurementsandParameterExtractions
Photosynthesis measurements were taken with a LI-6400XT with a 6400-02B Red/Blue light
source (LI-COR Biosciences, Lincoln, NE, USA). Light response curves were conducted to obtain
thelightsaturationpoint(I )foreachspecies,sinceitisanecessaryparameterforthetemperature
sat
responsecurves. Temperatureresponsecurveswereconductedusingawaterjacket(6400-88expanded
temperature kit, Licor Biosciences, Lincoln, NE, USA) to increase and decrease leaf temperature.
LeaftemperatureswereachievedbyintroducingheatedorcooledwaterthroughaBev-A-Linetube
throughthewaterjacketandawaitingequilibriumattargettemperatures. Waterwascontinuously
introducedthroughthesystemusinggravity,withreceptaclesbothaboveandbelowthemeasurement
chamber. Usingthismethod,wemeasuredphotosyntheticratesat22,24,27,29,30,31,32,33,and
35◦C.Relativehumiditywaskeptbetween50%and60%,andwasregulatedbyflow(200umols−1for
temperatesamplesand300umols−1 fortropicalsamples)anddesiccant. CO waskeptatambient
2
concentrationsof400ppm,andPhotosyntheticallyactiveradiation(PAR)waskeptattheaverageI
sat
foreachspecies(800,700,1200,1300,and1200µmolm−2 s−1 respectivelyforDac,Cas,Acer,Oco,
and Gua) as extracted from light response curves. T was calculated by taking the second order
opt
polynomial function on the temperature response curves and solving for the highest point on the
x-axis,andA wasextractedbysolvingforthephotosyntheticvaluefromtheregressionequationat
opt
T (Figure1)[87].
opt
2.7. LeafTraits
Leaf area for all leaves measured for gas exchange at the temperate site was measured using
aleafareameter(LI-3100LI-CORBiosciences,Lincoln,NE,USA).Theleafareaofleavesmeasured
forgasexchangedatthetropicalsiteswasmeasuredbyscanningpicturesofleavesalongsidearuler
(HP deskjet), then tracing the outline of the scanned image in ImageJ (Rasband, W.J 1997–2014,
http://imagej.nih.gov/ij). Leaveswerethendriedfor24hat65◦Candweighed. Leafmassperarea
(LMA;gm−2)wasdeterminedbytakingtheratioofdryweighttoleafarea.Samplesweregroundwith
aballbearinggrinder(8000MMixer/Mill,SpexSamplePrep,Metuchen,NJ,USA)forthreeminutes.
Prior to elemental analysis, ground samples were dried for an additional 24 h at 65 ◦C, weighed
Forests 2018,9,47 7of24
withaSartoriusCubismicrobalance(DataWeighingSystems,ElkGrove,IL,USA)for4–6mgofleaf
material,andfoldedinto5by9mmtincapsules. Leafnitrogen(N)analysiswasperformedusingan
ElementarvarioMicrocubeelementalanalyzer(ElementarInc.,Hanau,Germany). Leafphosphorus
(P)analysiswasanalyzedwithinductivelycoupledplasmaopticalemissionspectrometryusinga
Thermo Jarrell Ash IRIS Advantage Inductively Coupled Plasma Optimal Emission Spectrometer
(PrecisionDynamicsCorporation,SanFernando,CA,USA).
2.8. DataAnalysis
An F-protected Least Significant Difference Test was performed to determine if means were
significantlydifferentamongspeciesandforesttypes. Forallsubsequentregressionanalyses,species
datawithintropicalmoistforestwerepooled. Maximumdailyleaftemperature(T ),maximum
LEAFmax
dailyairtemperature(T ), andphotosynthetictemperatureoptima(T )ofleaveswereeach
AIRmax opt
analyzedwithheightusingsimplelinearregression. ThepointswhereT andT intersected
LEAFmax opt
werefoundbyalgebraicallycomparingwherethecoordinatesofT =a (height)+b andT =
opt 1 1 LEAFmax
a (height)+b intersected. SimplelinearregressionwasalsousedtocompareT andA withfoliar
2 2 opt opt
nutrients(N ,N ,P ,P ),andLMA.DIFN%wasexpressedasapercentoflightreaching
mass area mass area
eachcanopylevelgraphicallyandwastransformedwithanaturallogfunctionforstatisticalanalyses.
AllstatisticalanalyseswereperformedinR(RCoreTeam,Vienna,Austria,2013).
3. Results
3.1. Within-CanopyVariabilityofPhotosyntheticResponsetoTemperature
Overall mean T values were 2.5 ◦C greater for both tropical forests than for the temperate
opt
forest (30 ◦C and 27.5 ◦C, respectively; Table 1). A , however, was highest in the tropical moist
opt
forest(9.8µmolCO m−1s−2),followedbythetemperateforest(7.3µmolCO m−1s−2),andlastly,
2 2
thetropicalwetforest(4.9µmolCO m−1s−2).
2
Highphotosyntheticratesinthepooledmeanofthetropicalmoistforestweremainlydrivenby
highratesofO.leucoxylon,11.5µmolCO m−1s−2,comparedtothenexthighestvaluesbyspecies:
2
Castillaelasticaat9.9µmolCO m−1s−2andAcersaccharumat7.3µmolCO m−1s−2(Table2).
2 2
Table 2. Mean values by species (see Table 1 for species codes) and forest type of gas exchange.
Standard errors are displayed in parentheses. The number of samples (n) corresponds with the
numberoftemperatureresponsecurves.Parametersinclude:temperatureoptimumforphotosynthesis
(Topt,◦C),maximumrateofphotosynthesisinresponsetotemperature(Aopt,µmolCO2 m−1 s−2),
leafmassperarea(LMA,gm−2),phosphorusonaleafareabasis(Parea,gm−2),phosphorusonaleaf
massbasis(Pmass,mgg−1),nitrogenonaleafareabasis(Narea,gm−2),andnitrogenonaleafmass
basis(Nmass,mgg−1). LettercodesshowsignificantdifferencesamongmeansusingTukey’smean
separationprocedures(α=0.05)(Table2).
Species/Forest n Topt Aopt
Acer 23 27.4(0.4)b 7.31(0.55)b
Oco 6 30.3(0.5)a 11.51(0.96)a
Gua 4 29.5(0.8)ab 7.03(3.03)ab
Cas 14 30.0(0.4)a 9.88(0.65)a
Dac 12 29.9(0.9)a 4.90(0.59)b
TemperateDeciduous 23 27.4(0.4)B 7.31(0.55)A
TropicalMoist 24 30.0(0.3)A 9.76(0.69)B
TropicalWet 12 29.9(0.9)A 4.90(0.59)A
A increasedwithheightinthetemperateandtropicalmoistforests,butshowednorelationship
opt
withheightinthetropicalwetforest(Figure2a–c). HeightasapredictorforT wasnotsignificant
opt
foranyforesttype(Figure2d–f).
Forests 2018, 9, x FOR PEER REVIEW 8 of 24
Aopt increased with height in the temperate and tropical moist forests, but showed no
Forreesltasti2o0n18s,h9i,p47 with height in the tropical wet forest (Figure 2a–c). Height as a predictor for Topt w8aosf n24ot
significant for any forest type (Figure 2d–f).
16 40
y = 0.09x + 28.4
Cas
Gua R2 0.11 ns
36
12 Oco
32
8
28
y = 0.42x + 2.60
4
R2 0.38 *** 24
0 5 10 15 20 25 30 0 5 10 15 20 25 30
(a) (d)
16 40
Dac y = 0.009x + 4.40 y = 0.03x + 29.3
-2) R2 0.0003 ns 36 R2 0.001 ns
s 12
1
-
m
)
2 C
O o 32
olC 8 (opt
m T
µ 28
(
opt 4
A
24
0 5 10 15 20 25 30 0 5 10 15 20 25 30
(b) (e)
16 40
y = 0.107x + 26.1
Acer y = 0.325x + 3.31
R2 0.06 ns
R2 0.69*** 36
12
32
8
28
4
24
0 5 10 15 20 25 30 0 5 10 15 20 25 30
(c) (f)
Height (m)
FµimFmgiuogorlul erCCe2O O.2L2. Limmnine−−1ae 1rasr−rs2 e−)rg e2wrg)erwisetshsiits ohicnoacsnnasoon fopoofyp po yhptiehtmiiemguihgumthm t(tme (tmme)m,)p ,wpewreharhetaeurterure ertteh(hT e(eTo pdodtp;ata;t◦ t°aCaC )ww) aaeennrrdeed pccpoohhllololeettoccotstseeyyddnn tftfhohoerert ttiitrccro orrpapaittcieecasasl alam tmt ToTooiospipsttt t((( AAa(,aoodpp,td;)t ;;µ);
tropical w2 et (b,e); and temperate deciduous forests (c,f). Species-level data within the tropical moist
tropicalwet(b,e);andtemperatedeciduousforests(c,f).Species-leveldatawithinthetropicalmoist
forest were pooled. Levels of significance: *** p < 0.001 and ns (non-significant). Dotted lines
forestwerepooled.Levelsofsignificance:***p<0.001andns(non-significant).Dottedlinesrepresent
represent non-significant regressions.
non-significantregressions.
Light showed a significant log-linear relationship with Aopt in all forest types (Figure 3a–c),
whiLleig Thotpt sihnocwreeadseads sigignnifiifcicaannttlloyg w-liinthe alrigrhetl aotniolnys ihni pthwe ittrhopAiocpatli nmaolilsfto froersetstty (pFeigsu(Freig 3udre–f3).a –c),while
T increasedsignificantlywithlightonlyinthetropicalmoistforest(Figure3d–f).
opt
Forests 2018,9,47 9of24
Forests 2018, 9, x FOR PEER REVIEW 9 of 24
20
y = 5.72ln(x) + 1.67 y = 28.2ln(x) + 0.74
36
R2 0.32** R2 0.37**
16
32
12
28
8
Cas
Gua
4 Oco 24
0 40 80 120 0 40 80 120
(a) (d)
40
y = 1.09ln(x) + 1.14 y = 24.9ln(x) + 1.60
16 Dac
2) R2 0.44* R2 0.32 ns
-s 36
1
-m2 12 C)
O o 32
molC 8 T (opt
µ
(pt 28
o
A
4
24
0 40 80 120 0 40 80 120
(b) (e)
16 Acer y = 6.08ln(x) + 0.74 36 y = 27.0ln(x) + 0.22
R2 0.28** R2 0.05 ns
32
12
28
8
24
4
20
0 40 80 120 0 40 80 120
(c) (f)
DIFN (%)

FigureFi3g.uLreo 3g.- lLinoge-alirnreeagr rreesgsrieosnsisonosf oofp otipmtiummumte tmemppeerraattuurree ((TToopptt; ;°◦CC) )anadn dphpohtoostoynsythnetthice triactersa taet sTaoptt Topt
(Aopt;(µAmopt;o µl CmOol2 CmO−2 1ms−−1 s2−)2)w witihthn naattuurraall lloogg ooff ppeerrcceennt tddififfufuses enonno-nin-itnertceerpcteapntcaen [clen([DlnIF(DNI]F fNor] tfroorpitcraolp ical
moistm(ao,idst) ;(at,rdo)p; itcroapliwcael tw(bet, e()b;,ea)n; dantde mtepmepreartaeted deeccididuuoouuss ffoorreessttss ((cc,f,)f.) .SpSepceiecsi-elesv-leelv dealtda awtaithwini tthhien the
tropictarlompicoails tmfooriesst twforeerset pwooelreed .pLooelveedl.s oLfevseiglsn iofifc asnigcne:if*icpan<ce0:. 0*5 ,p* *<p <0.00.50, 1,**a npd n< s0(.n0o1,n -asnigdn infisc ant).
Dotted(nolinn-essigrneipfirceasnet)n. tDnoottne-ds ilginneisfi rceapnrtesreengtr neossni-osnigsn.ificant regressions.
3.2. Relationships between Photosynthetic Temperature Optima and Maximum Leaf and Air Temperatures
3.2. RelationshipsbetweenPhotosyntheticTemperatureOptimaandMaximumLeafandAirTemperatures
In all forest types, the relationship between TLEAFmax and height was significant and showed a steep
In all forest types, the relationship between T and height was significant and showed
positive increase. TLEAFmax spanned 8–10 °C in all foresLtEsA frFommax understory to canopy top (Figure 4).
a steep positive increase. T spanned 8–10 ◦C in all forests from understory to canopy top
LEAFmax
(Figure4).
T ,however,onlyincreasedsignificantlywithheightinthetropicalwetforest,andslopes
AIRmax
wererelativelyshallowforallforesttypes. Weonlyhaduppercanopyairtemperaturedatainthe
Forests 2018,9,47 10of24
tropicalmoistforest,whereT exceededmaximumairtemperaturesby4◦Catheightsof25m
LEAFmax
(Figure4a).
Forests 2018, 9, x FOR PEER REVIEW 10 of 24
40
Tropical moist
36 TLmax
TAmax
Topt
32
28
24
0 5 10 15 20 25 30
(a)
40
Tropical wet
) 36
C
°
(

e
ur 32
at
r
e
p
m 28
e
T
24
0 5 10 15 20 25 30
(b)
40
Temperate Deciduous
36
32
28
24
20
0 5 10 15 20 25 30
(c)
Height (m)
Figure 4. Comparisons with height (m) of: photosynthetic temperature optima (Topt), mean maximum
Figured4a.ilCy olemafp taermispoenrsatwurieth (ThLeEiAgFmhaxt),( man)do mf:epahno mtoasxyinmtuhmet idcatielym apier rtaetmupreeroaptutirme (aT(ATIRompatx)) ,imn: e(aan) tmroapxiciaml um
dailylemaofitset mfopreesrta; t(ubr)e t(rTopLEicAaFlm waxe)t, faonrdesmt; e(ca)n temmapxeirmatue mdedciadiulyouasir ftoermespt.e Srpateucirees-(lTevAeIRl mdaaxt)a inw:it(hai)nt rtohpe ical
moisttfroorpeiscta;l (mbo)itsrt ofopriecsatl wwereet pfooorelesdt;. D(co)ttteedm lipneersa rteeprdeesecnidt unoonu-ssifgonriefiscta.ntS rpeegcreiesssi-olenvs.e l data within the
tropicalmoistforestwerepooled.Dottedlinesrepresentnon-significantregressions.
TAIRmax, however, only increased significantly with height in the tropical wet forest, and slopes
were relatively shallow for all forest types. We only had upper canopy air temperature data in the