Fossil leaf traits as archives for the past — and lessons for the future?

2018·3.9 MB·English

by  Anita Roth-Nebelsick

Flora xxx (xxxx) xxx–xxx
ContentslistsavailableatScienceDirect
Flora
journal homepage: www.elsevier.com/locate/flora
Review
☆
Fossil leaf traits as archives for the past — and lessons for the future?
Anita Roth-Nebelsicka,⁎, Wilfried Konradb,c
aStateMuseumofNaturalHistoryStuttgart,Rosenstein1,D-70191Stuttgart,Germany
bDepartmentofGeosciences,FacultyofScience,UniversityofTübingen,Hölderlinstrasse12,D-72074Tübingen,Germany
cTechnicalUniversityofDresden,InstituteofBotany,ZellescherWeg20b,D-01062Dresden,Germany
ARTICLE INFO ABSTRACT
EditedbyHermannHeilmeier Correlationsofleaftraitswithenvironmentalconditionsarewidelyusedforreconstructionofpalaeoclimateand
Keywords: toanalysetheevolutionoflandplants.Evaluationofclimate-dependentleaftraitsoffossilflorascanpotentially
Palaeoclimate contributetoourunderstandingoflong-termresponsesofvegetationtochangingclimate.Inthiscontribution,
CO2 basicaspectsandmethodsofpalaeoclimatereconstructionbyfossilleafmorphology,suchasleafmarginana-
Leafmarginanalysis lysisandCLAMP,arepresentedanddiscussedwithrespecttorecentresultsonfunctionalleaftraits.Alsoad-
Stomataldensity dressed is the use of stomatal data (density and size) for obtaining palaeoatmospheric CO2 as well as the
Gasexchange (possible)interferenceofCO2withotherabioticenvironmentalparameters,leadingto“non-analogueclimates”
Leaftemperature
Leafheatdissipation whichcannotbefoundtoday.ThereismuchevidencethatCO2,asanessentialfactorforgasexchangeand
thereforepalaeoecophysiology,actedasanimportantdriverinlandplantevolution.Forinstance,elevatedCO2
levels of the past and present are assumed to affect leaf shape evolution, because stomatal conductance is
negativelycorrelatedwithatmosphericCO2therebyaffectingleafheatdissipation.Thistopicisaddressedin
detailasanexemplarycaseoftheinterferenceofmultipleenvironmentalparameters.Resultsofagasexchange
modelwithcoupledheattransferindicatethattheeffectofelevatedCO2onleaftemperaturemaybeminor,at
leastwhenwatersupplyisnotlimited.Thisexampledemonstratesthatecophysiologicalanalysesoftrait–cli-
materelationshipscancontributetoidentifyingadaptivefeaturesofleafarchitectureandtoevaluatepredictions
intothefutureaswellasintothepast.
1. Introduction afunctionalbasisthatremainedconstantfromthepasttothepresent
(Jordan, 2011). If so, then, consequently, these may be extrapolated
Leavesastheprimaryorgansofphotosynthesisaredirectlyexposed intothefuture.Furthermore,evaluationofclimate-dependentleaftraits
to the atmosphere, performing controlled gas exchange under con- offossil florascould contributetoour understandingoflong-term re-
stantlyvaryingconditions.Successfulandeconomicphotosynthesisisa sponsesofvegetationtochangingclimate.
basicnecessityofplantlife,leadingtoahighselectivepressureonleaf Inthiscontribution,variousaspectsofclimatesensitivityofleaves
function. Unsurprisingly, leaves are sensitive to their environment in are considered within the framework of their use as palaeoclimate
variousways.Thesecompriseinstantresponsestoexternalstimuli,such proxy and related problems of extrapolating extant trait–climate cor-
as opening or closing of stomata, as well as correlations between relations into the past. Although a leaf functional basis is generally
macromorphological/micromorphological traits and environmental assumed for trait–climate correlations, a clear causal explanation is
parameters.Correlationsoftraitswithenvironmentcanbeinterspecific lacking for many of them. Recognizing ecophysiological processes
aswellasintraspecific,withthelatterincludingleafplasticitywithin which drive trait–climate correlations is, however, the basis for iden-
oneindividual(forthetopicofplasticity,seealsoPugiellietal.,within tifying and explaining adaptations to environment on various levels,
this volume). Morphological responses of leaves to environment ob- fromplasticitytoevolutionaryadaptationand(abiotic)environmental
served and documented for recent vegetation are the basis for using filtering.Therefore,focuswillbeontraitsforwhichclearphysicaland
morphologicaltraitsoffossilleavesas“climatearchive”.Bydoingso,it physiological explanations for their correlations with environment
istacitlyassumedthatcorrelationsbetweenleaftraitsandclimatehave exist.Theseareleafsizeanditsinterrelationshipswithtemperatureand
☆Thisarticleispartofaspecialissueentitled:“Functionaltraitsexplainingplantresponsestopastandfutureclimatechanges”publishedatthejournalFlora
254C,2019.
⁎Correspondingauthor.
E-mailaddresses:[email protected](A.Roth-Nebelsick),[email protected](W.Konrad).
https://doi.org/10.1016/j.flora.2018.08.006
Received20March2018;Receivedinrevisedform5July2018;Accepted1August2018
0367-2530/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Anita Roth-Nebelsick and Wilfried Konrad, Flora, https://doi.org/10.1016/j.flora.2018.08.006
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
transpirationandstomataldensityanditscorrelationwithatmospheric numberofenvironmentalparameters(Spiceretal.,2009;Wolfe,1993;
CO2concentration.Theseinterrelationshipswillbeconsideredinmore WolfeandSpicer,1999;Yangetal.,2015,seeKunzmannetal.,inthis
detail, including a brief description of mechanistic modelling ap- volume, for an example of applying LMA and CLAMP to a fossil as-
proaches which allow for evaluating putative functional hypotheses semblage).Therearerecenteffortsforfurtheradvancedandsophisti-
(Jordan,2011).Animportantaspectisthatatraitcanbeinfluencedby cated approaches to calculate climate parameters from leaf traits (Li
morethanoneenvironmentalparameter,makingitdifficulttoextract etal.,2016).Theseapproaches,however,seeknottoexplainorinclude
singleclimatesignals.AnexampleisthepossibleeffectofCO2onleaf possiblefunctionalbackgroundsoftrait–climaterelationships.Rather,
size, via its effect on stomatal conductance and — therefore — eva- theobservedpositiveornegativecorrelationsoftraitswithclimateare
porativecooling. The lastpart ofthis contribution isdedicatedtoex- usedinapurelyempiricalstatisticalway.Itshouldalsobeemphasized
ploringthisinterference,asanexemplarystudyofhowtheinteraction thatneitherLMAnorCLAMPrequirestaxonomicidentificationoffossil
ofdifferentparameterscouldbeunravelledbyathoroughecophysio- leaves. Both methods can be applied with the “morphotype” concept
logicalanalysis. whichisbasedoncharacterizingcomponentsofafossilflorabytheir
It should be emphasized that this contribution focuses on angios- morphologicaltraits(DiMichele,1983;Johnson,1989).Thisallowsfor
perms, because many studies are based on angiosperm leaves which includingandanalyzingfossilsforwhichnocleartaxonomicaffiliation
showparticularlystrongandmanifoldresponsestoclimate.Aftertheir tomoderntaxaisavailable.
appearanceanddiversification,angiospermshadasubstantialinfluence LMAusescategoricaldata(presence/absenceofteethatthemargin)
onglobalecology,withtheirleavesplayingamajorrole(Boyceetal., andCLAMPisalsomainlybasedonthecategoricaldatatype.Recently,
2009;BoyceandLee,2011;BoyceandZwieniecki,2012).Althoughthe theadvantagesofcontinuousleaftraitswereputforward(Huffetal.,
majorityofstudiesdedicatedtorelationshipsbetweenenvironmentand 2003;Royeretal.,2005).Asubstantialamountofinformationcanbe
leaf traits focus on angiosperms, there are also data available which conveyedbyquantitativeleafshapeparameters,suchasroundnessor
showthatvarioustrendsfoundforangiospermleavesarealsovalidfor theareacoveredbymarginalteeth(Peppeetal.,2011).
otherplantgroups,suchasferns(KarstandLechowicz,2007;Sessaand It should be emphasized that biological palaeoclimate proxies
Givnish,2014). (=indirectindicatorsprovidingapproximatevaluesfortheparameter
ofinterest),suchastraitsoffossilplantremains,comewithacertain
2. Macromorphologicalleaftraitsassourceforpalaeoclimate errormargincausedbyvariousreasons.Onereasonforpossiblebiasis
reconstruction that taphonomic processescan distortthe compositionof theoriginal
flora in a fossil assemblage (Astorga et al., 2016; Campbell, 1999;
Probablythemostpopular—andhistorical —leaftrait-basedin- Ferguson, 1985, 2005; Gastaldo et al., 1996; Greenwood, 2005;
dicator of climate is the leaf margin. The approach is usually termed Kennedyetal.,2014;Spiceretal.,2011;Steartetal.,2002).Another
Leaf Margin Analysis (LMA) (Wilf, 1997). Globally, the proportion of basicaspectisthatarichassemblageofwell-preservedplantfossilsis
taxashowingtoothedleafmarginsisnegativelycorrelatedwithmean usuallydependentonthepresenceofawaterbodyprovidingconditions
annual temperature (MAT) (Bailey and Sinnott, 1916; Royer et al., which delay or prevent decay. Many fossil localities thus represent
2012).Thereismuchdiscussiononthefunctionalbackgroundofthis habitats with a high groundwater table, such as riparian systems or
climate-dependenttrait.Itwassuggestedthatmarginalteeth—which swampsinwhichwatersupplyofthelocalvegetationislessdependent
areoftenabletoactashydathodes—allowforpressurereleaseduring onprecipitation.Thisisoneofthereasonsforthenotoriousdifficultyto
spring root pressure to avoid mesophyll flooding (Feild et al., 2005). approximateprecipitationonthebasisoffossilplants.
Accordingtoanotherhypothesis,toothedmarginsallowforearlyma- Another plant-based method is the Coexistence Approach (CA)
turationofleafmesophyllatthetipregionsandthereforeforanearly (MosbruggerandUtescher,1997)(forarecentdiscussionandstate-of-
start of photosynthesis at these spots during springtime (Baker-Brosh the-art representation see Utescher et al., 2014), whose operational
andPeet,1997).Thishypothesisissupportedbythefindingthattooth principle is analogous to the Climate Envelope concept: climate re-
areaincreaseswithdecreasingMAT(Peppeetal.,2011).However,not construction is based on the realized abiotic environmental niches of
all taxa featuring toothed leaf margins show early photosynthesis at the nearest living relatives (NLR) of the considered fossil taxa. Max-
theirmarginalteeth(Baker-BroshandPeet,1997),andtherearealso imumandminimumvaluesofvariousclimateparametersarederived
other explanations for the negative correlation between frequency of whichaccommodatetheenvironmentaldemandsof(ideally)allNLRs.
taxa with toothed margins and MAT (Edwards et al., 2016; Givnish, Technically, this corresponds to that interval which provides the
1979;GivnishandKriebel,2017). overlapping region for the climate ranges of the NLRs. In contrast to
The occurrence of taxa with toothed leaf margins in a flora has a leaf-traitbasedmethodssuchasCLAMPandLMA,theCArequiresre-
substantialphylogeneticbackground.Shiftsinproportionsoftaxawith liabletaxonomicidentificationofthefossilplants,otherwiseitwould
entireortoothedmarginsarelargelyduetospeciesmigrationbywhich beimpossibletorecognizeNLRs.Furthermore,CAcanbeappliedtoall
toothed(mostlydeciduous)anduntoothed(mostlyevergreen)taxaare kindsoffossilplantparts,suchaswoodorpollen,andnotjustleaves.
exchanged against one another (Hinojosa et al., 2011; Little et al., Howistheperformanceofleaf-basedpalaeoclimatereconstruction,
2010), making biogeography an important aspect in global distribu- compared with other approaches? Quite often, LMA, CLAMP and CA
tionsoftoothedvs.untoothedplantgroups.Thismeansthatthereisno showsimilartrends,butdifferenceswithrespecttotheabsolutevalues
globally valid calibration possible since biogeographical history and are quite common. For example, evaluation of plant-based palaeocli-
limitations(suchasmigrationbarriers)substantiallyinfluencethefinal matedataforanextendedstratigraphicrange,fromtheEocenetothe
frequency of taxa with and without toothed margins. Calibration Pleistocene, for the Bohemian Massif (Czech Republic) and adjacent
equations which allow for calculating MAT from extant data sets are fossilsitesinGermanyreveals,firstly,thattheCAreturnsamuchmore
thereforeregionallylimited,andvarioussite-relateddatasetsexistso equableMATthanLMAorCLAMP,and,secondly,thatMATcalculated
far(Greenwoodetal.,2004;Peppeetal.,2011). by leaf-based methods is often several degrees below the CA-derived
Besides the leaf margin, there are other macroscopic leaf traits value(TeodoridisandKvaček,2015).
whichshowcorrelationswithenvironmentalfactors.CLAMP(Climate In the case of the CA, the necessity to reliably identify the fossil
Leaf Analysis Multivariate Program) is a multivariate approach based taxon as well as its correct NLR is often a formidable task (Utescher
onvarious(currently31)leaftraits,suchasshapeoftheleaflaminaor etal.,2014).However,eveniftaxonomicidentificationiscorrect,there
the leaf apex, presence of a drip tip or ratio between leaf length and maybesubstantialdifferencesbetweenthefossiltaxonanditsextant
width.Thevariouscorrelationsofthesetraitswithclimatefactorsare counterpart (Jordan, 2011). The frequent occurrence of “outliers”
then used for a statistical multivariate approach which returns a whicharetaxanotfittingintoaclimateintervalenclosingallspecies,or
2
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
even the impossibility to identify suchan interval may be dueto dif- leaves,therebytendingtoalowLMarea,shouldbeabletocopebetter
ferent climate demands of fossil and extant representative (Utescher with low CO2 (Loreto et al., 1992; Medlyn et al., 2011). More robust
etal.,2014).Anotherproblemisrepresentedbythecircumstancethat and dense leaves showing a higher LMarea would particularly benefit
combinations of environmental parameters may have occurred in the from high CO2 (McElwain et al., 2016; Niinemets et al., 2011). This
pastwhichdonolongerexisttoday(“non-analogueclimate”,seealso differential effect of CO2 on the LMarea spectrum is caused by differ-
Section4.2)(WilliamsandJackson,2007). encesinleafinternalconductance:highLMarealeavestendtoalower
Apart from problems which are specific to plant-based proxies, leafinternalconductanceforCO2thanlowLMarealeaves,andtherefore
discussing and evaluating climate and climate-dependency of plant the latter can cope better with low atmospheric CO2 whereas leaf in-
traitsonthebasisofthoseenvironmentalparameterswhichwereob- ternal CO2 transport is promoted for robust and thick leaves under
tainedbyexactlythesetraitscarriesthedangerofacircularargument elevated CO2. This would possibly lead to a CO2-dependent shift in
when no other independent evidence for the environment exists. It is distributionandfrequencyofdeciduous/evergreentaxa.
generally advantageous to combine different proxies, allowing for Additionally, CO2 (and various other environmental factors) may
comparisonbetweenpalaeoclimateinformationderivedbyplantsand directly influence LMarea in individual plants via plasticity (Poorter
those derived by other methods (Jordan, 2011). For example, magni- etal.,2009).WhenexposedtodifferentlevelsofCO2,LMareaisslightly
tudeofMATandminimumannualtemperaturecanbeapproximatedby negativelycorrelatedwithCO2(AinsworthandRogers,2007;Poorter
presenceofcertainanimals,suchascrocodiles(Markwick,1998).Other etal.,2009;Temmeetal.,2015).HigherLMAareaunderelevatedCais,
methodsarebasedonisotopecompositionofanimalremains,suchas however,notnecessarilycausedbystructuralleafchanges,butcanalso
teeth (Kohn and Cerling, 2002; Tütken and Absolon, 2015). For ex- be due to a higher amount of nonstructural carbohydrates (such as
ample, palaeotemperature reconstruction of the Messel pith based on starchorsolublesugars)andthereforereflectchangesinthecarbohy-
18OfromenamelobtainedfromPropalaeotherium(afossilhippomorph) dratesource–sinkratio,suchasincreasedphotosynthesis(Poorteretal.,
teethcoincidessatisfactorilywithtemperaturevaluesderivedbyusing 2009).
plant fossils (Grein et al., 2011). However, it is often not possible in LMAareaisnottheonlytraitwhichisinfluencedbyCO2.SinceCO2is
practicetocombinedifferentproxies,becausefossilsitesfrequentlydo thesubstrateofphotosynthesis,andCO2uptakeanditsfixationisthe
notprovidedifferenttypesoffossilorganismsorothermaterialsuitable central element of leaf function, changing CO2 levels are expected to
forenvironmentalreconstruction. widelyaffectleafecophysiologyandthereforeleaftraits.Atmospheric
CO2changedprofoundlyduringEarth'shistory,withstrongvariations
3. Fossilleafeconomics throughout the Cenozoic, the post-Cretaceous time period which
shaped recent biomes and ecosystems (Beerling and Royer, 2011). In
As noted above, the functional aspects of many leaf traits whose thefollowingsections,basicaspectsofrelationshipsbetweenleaftraits
correlationswithenvironmentalparametersareusedforpalaeoclimate offossilplantsandCO2willbeconsidered.
research are unknown or under debate. Furthermore, fossil leaf traits
appeartoberestrictedtomorphologicaltraits,seeminglytheonlykind 4. LeaftraitsandCO2
oftraitaccessiblefromfossilmaterial.Afunctionalleaftraitofspecial
interestinrecentresearchisleafmassperarea,LMarea,thedryweight 4.1. StomatarespondtoCO2—andcanbeusedasproxydataforthepast
ofaleafrelatedtoitsarea,alsoexpressedasitsreciprocal,specificleaf
area (SLA). LMarea correlates with life life span (LLS) and mass-based Duringthelastyears,alargewealthofdataontheresponseofplant
photosynthesisandiscentralforexplainingleaffunctionwithrespect gas exchange to CO2 was collected, mostly with respect to elevated
toleafeconomics(Reich,2014;Reichetal.,1999;Wrightetal.,2005, levels, such as targeted by the FACE (Free Air Carbon dioxide
2004).Althoughitisnaturallyimpossibletodirectlyobtaintheweight Enrichment) campaign (Ainsworth and Long, 2005; Battipaglia et al.,
ofafossilleaf,amethodforindirectapproximationofLMareafromfossil 2013;Norbyetal.,2016;NorbyandZak,2011).Variousstudiescon-
leaves was introduced (Royer et al., 2007). This method is based on sideredalsoplantresponsestosubambientCO2(Bunce,2007;Gerhart
mechanicalconsiderations,andapproximatesLMareafrompetiolewidth andWard,2010;Pintoetal.,2014;Temmeetal.,2013).Asonegeneral
andlaminaareaofthefossilleafspecimenonthebasisofaquitelarge result,stomatalconductance,g,isnegativelycorrelatedwithCO2,with
calibrationsetobtainedfromextantleaves. plants adapting stomatal opening to atmospheric availability of CO2.
LLS is positively correlated with length of the growing season Thenegativeg–CO2relationshiprepresentsoneofthevariousresponses
(Givnish, 2002). Due tothe relationship between LLS and LMarea,the ofthestomatalcontrolsystemtoenvironmentalparameters,butane-
latter parameter could therefore potentially deliver growing season gativecorrelationbetweenstomataldensity(SDorν)andCO2wasalso
length, thereby complementing other palaeoclimate proxies. For ex- observed,forherbariummaterial(Miller-Rushingetal.,2009;Peñuelas
ample,LMareadataforvariousfossilassemblagesfromCentralEurope and Matamala, 1990; Woodward, 1987) as well as experimentally
from the Paleocene to the Oligocene confirm general palaeoclimate (Beerling et al., 1998; Haworth et al., 2011; Hincke et al., 2016;
resultsindicatingwarmandequableclimateduringtheEocene(Figs.1 Kürschner,1996;Wagneretal.,1996).Contrarytog,stomataldensity
and2).However,meanLMareainalocalvegetationaswellasLLSare represents a morphological trait and can as such be determined from
affectedalsobyotherenvironmentalfactors.Particularly,LMareashows fossil material, if the cuticle of a fossil leaf is properly preserved
anegativecorrelationwithsoilnutrients(McDonaldetal.,2003)and (Fig. 3). Therefore, quite soon after the publication of Woodward
increasesalsowithdecreasingprecipitation(Wrightetal.,2005)(foran (1987),SDadvancedtoawide-spreadtoolforpalaeoatmosphericCO2
exampleoftheimpactofnutrientavailabilityonplanttraits,seeDiéme reconstruction.Inthefollowing,atmosphericCO2concentrationwillbe
etal.,thisvolume).Particularlyavailabilityofsoilnutrientsiscurrently termedCa.
not accessible for past habitats (apart from exceptional settings like AstheSD–Carelationshipisspecies-dependent,theoriginalconcept
peat; Sluiter et al., 2017), a circumstance which adds to the un- was to identify extant species whose existence extended to the time
certainties of plant-based climate reconstruction. Despite these cir- period of interest and to erect calibration curves of their SD–Ca re-
cumstances, fossil LMarea data can potentially provide palaeoclimate lationship, either by herbarium material or from experiments. These
reconstruction data and contribute basic information on ecophysiolo- calibrationcurvesarethenusedtocalculateCafromfossilSDdata(or
gicalfeaturesoffossilplants(Roth-Nebelsicketal.,2017;Royeretal., fromstomatalindexdatarepresentingtheratiobetweenepidermalcell
2007). density and stomata density) (Kürschner et al., 1998; Poole and
AnotherparameterwhichmayinfluenceLMareaisatmosphericCO2 Kürschner, 1999). Naturally, this strategy becomes increasingly diffi-
concentration (Ca). One line of reasoning is that thin and delicate cult to pursue with increasing stratigraphic age. Plant taxa of the
3
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
Fig.1.TwoleavesofPlatanusneptuni(Ettingshausen)Bůžek,Holý
etKvaček,fromtwodifferentlocalities,asanexampleforfossil
leaf material which allowed for determination of LMarea. (A) P.
neptunifromthefossilsiteRauenberg(StateMuseumofNatural
History Stuttgart, SMNS P 1953/36) (Kovar-Eder, 2016). Strati-
graphicage:Oligocene,Rupelian,about32to29.6millionyears
old. (B) P. neptuni from the fossil site Kučlín, Czech Republic.
Stratigraphicage:Eocene,Bartonian,about39.2to37.4million
yearsold(NationalMuseumPrague,NMPG09792)(Teodoridis
andKvaček,2015).
Fig. 3.Abaxial cuticle of the fossil angiosperm taxon Rhodomyrtophyllum re-
ticulosumfromtheMesselpit,about48million yearsold(Ypresian,Eocene)
(CourtesyMichaelaGrein,Übersee-MuseumBremen,Germany).Bar:50μm.
Fig.2.DataformeanLMareaofvariousfossilassemblagesfromCentralEurope,
fromthePaleocene,EoceneandOligocene.Theboxplotsspanthe50%inter- intotheplantisentirelyprocessedbyphotosynthesis,andassimilation
quartile.Thelineswithintheboxesindicatethemedianvalues.The“whiskers” rateAisrelatedtoleafconductancegvia
mark the highest and lowest values. Outliers are drawn as filled circles.
Differences are statistically significant (for more detail, see Traiser et al. A=g(Ca Ci) (1)
(2018)). Note: expression log10(LMarea) (along ordinate axis) is to be under-
stood as the common logarithm of the numerical value of LMarea, provided Furthermore,theFarquharmodelofC3–plantphotosynthesis(Farquhar
LMareaisgiveninunitsofg/m2. et al., 1980) postulates a dependence of A on Ci and on biochemical
parameters
Quaternary, for example, are almost identical to recent taxa, offering A=q Ci R
excellent opportunities to study Ca from fossil material (Beerling and Ci+K d (2)
Rundgren,2000;RundgrenandBeerling,1999;RundgrenandBjörck,
2003; Steinthorsdottir et al., 2013; Wagner et al., 2004). For time withq:carboxylationlimitedbyRubisCOorRuBP,K:parametercon-
periods older than the Miocene, suitable species become increasingly tainingMichaelis–Mentenconstantsofcarboxylationandoxygenation,
scarce,leavingsomefewtaxawithalonghistory(“livingfossils”). Γ: CO2 compensation point, and Rd: mitochondrial respiration rate in
Anotherstrategyistouseplantgasexchangemodellingasbasisfor the daylight as biochemical parameters of photosynthesis (Farquhar
calculatingCafromfossilstomataldata.Thisopensuppossibilitiesfor et al., 1980; Konrad et al., 2008). These parameters depend on tem-
an ecophysiological model framework as basis for deriving palaeocli- perature(Bernacchietal.,2003;Konradetal.,2008).
matefromproxydata,andwillbepresentedinthefollowinginmore The diffusion law provides also a relation between stomatal con-
detail—althoughbriefly—asanexemplarycase.Alldifferentmod- ductance and leaf anatomy (Parlange and Waggoner, 1970; Konrad
elling approaches exploit two relations. The first one, Fick's Law of etal.,2008),
dthiffeiursicoonn,csetnattreastitohnatdtihffeeflreunxceofbCeOtw2emenoleactumleosspinhteorele(aCvae)saisnddrlievaefnibny- g= ast2DCO2
terior(Ci).Understationaryconditions,thenetfluxofCO2–molecules dbl+dasnaass ast+dst (3)
4
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
das, τas, nas are thickness, tortuosity, and porosity of the assimilation Results of CO2 reconstruction with fossil stomata are quite con-
layer, ast, dstare cross-sectionalarea (parallel totheleaf surface)and sistent when compared to CO2 values from ice cores (Franks et al.,
depthofthestoma,andνisthestomataldensity.Alaminarboundary 2014).However,icecoredataareonlyavailableforaboutonemillion
layerofairdevelopsaroundaleafwhosethicknessdependsonleafsize yearsintothepast(Fischeretal.,2013),andtheerrormarginofsto-
landwindspeedvwind,approximatelyaccordingtodbl≈4×10−3m/ mata-basedCO2reconstructionwillincreasewhengoingfurtherbackin
s l . time,duetohigheruncertaintyofphotosynthesisparametersaswellas
vwind
Thebasicmodelideaamountstoderiving—inafirststep—from environmentalparameters.Acomparisonofstomata-derivedCO2with
results of other proxy sources (such as Boron isotopes or alkenon-de-
(1) and (2) a relation between g and Ca and to use this result in (3) rived 13C from marine plankton) reveals various consistent trends
which can then be solved for Ca. Assuming that the photosynthesis
(Beerling and Royer, 2011). However, there are also inconsistencies,
parameters q, K, Γ and Rd are known from extant relatives, the two
particularlyduringatimeofstrongclimatechange,namelytheEoce-
equations(1)and(2)containfourunknowns,g,Ca,AandCi.Thus,a
ne–Oligocene when global cooling terminated the ice-free hothouse
third relation is required in order to extract the desired relation be-
conditions, marked by the Oi-1 glaciation event (Coxall and Wilson,
tweengandCa.
Atthispoint,themodelapproachesdivergesomewhat: 2011; Coxall et al., 2005). There is various evidence for high CO2
duringtheEocene,withamoreorlesscontinuousdeclinetowardsthe
(i) The optimization models include the dependency of stomatal Oligocene. A decrease in Ca would thus accompany global cooling
(Royer et al., 2012). Stomata-based results for the Eocene are often
aperture on environmental parameters, particularly humidity and
substantiallylowerandatoddswithotherproxies(Anagnostouetal.,
temperature and postulate optimized water use (Konrad et al.,
2016;Maxbaueretal.,2014;Steinthorsdottiretal.,2016),despitethe
2008).Thestrategyofplantstogainamaximumofcarbonwitha
given amount of available water (Berninger et al., 1996; Cowan, circumstance that various Eocene Ca data originally reported as ex-
tremely high were meanwhile revised and became more moderate
1977) can be translated into the mathematical language of opti-
(Breeckeretal.,2009;Jagnieckietal.,2015).Thesedisparitiesamong
mization principles. Several of them were successfully applied on
various occasions (Aalto et al., 2002; Berninger et al., 1996; CO2proxiesarecurrentlynotresolved(CuiandSchubert,2017;Royer
etal.,2014).
BuckleyandSchymanski,2013;DeBoeretal.,2011;Katuletal.,
Inthecaseofstomata-basedproxies,onepossiblesourceoferroris
2010; Way et al., 2011). The approach of Konrad et al. (2008)
employsafulloptimizationmodelandisquitecomplex,requiring the increasing insensitivity of gas exchange to CO2, due to the non-
besidesinformationfortemperatureandhumidityalsodetermina- linearresponseofstomatalconductancegandassimilationrateAtoCa
tionofaparameterλwhichquantifiesinasensethe“costofwater” (seeFig.4).AtloworsubambientCO2,g(seeFig.4a)aswellasA(see
andisconstrainedbytheratioCi/Ca.(Noticethatourdefinitionof Fig. 4b) respond strongly and roughly linearly to changing Ca levels
(Franksetal.,2013,2012;Temmeetal.,2013)(seeFig.4).Withele-
λ is the inverse of the definition used in Cowan and Farquhar,
1977.) vated Ca, usually above about 400–500μmolmol−1 (depending on
temperature), the response increasingly levels off: A approaches sa-
(ii) Mostoftheother modelsrestricttheir modeldynamics tocarbon
turation(thesaturationvaluedependsontemperature),aconsequence
balance. They obtain the missing information on stomatal con-
ductance from determining Ci/Ca, based on the well-known fact ofEq.(2),theFarquharmodelofC3-plantphotosynthesis,andequation
thatbothdiffusionandphotosynthesisdiscriminatethe13Cisotope (4), expressing proportionality of the CO2-concentrations inside and
againstthe12Cisotope.Exploitingthisfact,itispossibletocalcu- outsideoftheplant.g,however,becomesaccordingtoEq.(5)smaller
latetheratio under further increasing Ca (Franks et al., 2013, 2012; Konrad et al.,
2008).SDandE,whichareconnectedwithgviaEqs.(3)and(7),follow
= Ci thistrend(seeFig.4c).Therefore,addingacertainincrementofCO2to
Ca (4) analreadyhighCaleadstoaverysmall(decreasing)stepontheSD-axis
whichisstatisticallydifficulttoascertain,particularlywhenthenatu-
from 13C data from fossilized leaves (Beerling, 1994; Diefendorf
rallyhighscatterofSDdataisconsidered.Despitetheseproblemsitis,
etal.,2010;Farquharetal.,1982;Greinetal.,2010).
however,principallypossibletoreconstructelevatedCafromstomatal
data(Greinetal.,2011;Tesfamichaeletal.,2017).
Pursuingthesecondapproach,wecombineEqs.(1),(2)and(4),and
Gas exchange approaches offer the possibility of evaluating the
arriveat(Konradetal.,2017)
errormarginofCO2reconstructedwithfossilstomataldatabyvarying
g= q( Ca ) Rd( Ca+K) theinputparametersovertheirwholerangeof(statistical)uncertainty
(1 )Ca( Ca+K) (1 )Ca (5) (Konrad et al., 2008). Furthermore, it is possible by systematic para-
metervariationtoidentifyparameterswhichexertthehighestinfluence
therighthandsideofwhichcontains—apartfromthephotosynthesis (“criticalparameters”)ontheresults.Inthismanner,itcanbeshown
parameters(obtainablefromlivingrelatives)andκ(obtainablefromthe thatthebiochemicalparameterq(carboxylationlimitedbyRubiscoor
fossilleaves)—onlyCa.Expression(3) connectsg withleaf anatomy RuBP)representsacriticalparameter(Konradetal.,2008).Biochem-
(obtainable from the fossil leaf) and the coefficient of diffusion DCO2. ical parameters are the only ones which have to be borrowed from
Equatingexpressions(3)and(5)resultsinaquadraticequationforthe extantplants,introducingabasicsourceoferrorforCO2reconstructed
atmosphericCO2concentrationCaunderwhichthefossilizedleafhad fromfossilstomata.Thiserrorintroducedbyphotosynthesisparameter
grown. is exacerbated by the circumstance that q itself is affected by CO2: q
Being notbased oncalibrationcurves fromextantspecies,gasex- tendstodecreasesomewhatwhenplantsareexposedexperimentallyto
changemodelapproachesarealsoappliedtoextinctfossiltaxa(Franks elevatedCa(AinsworthandRogers,2007),whereasitincreasesunder
etal.,2014;Greinetal.,2011).Furthermore,incontrasttocalibration subambient CO2 (Pinto et al., 2014). Adaption of the photosynthesis
methods,gasexchangemodelsalsoincludestomatalparametersother system to Ca by this plastic response can be connected to nitrogen
thanSD,namelystomatalporesizeanddepthandthereforeconsiderall contentoftheplant:ittendstobehigherundersubambientconditions
traits which influence stomatal conductance. In fact, stomatal pore comparedtocontrolgroups(Pintoetal.,2014).Probably,qshiftedalso
length may change over time within a taxon which can substantially during land plant evolution, according to changing Ca levels (Franks
altertherelationshipbetweenCa,gandgasexchange(García-Amorena and Beerling, 2009). The possible sensitivity of q to Ca increases the
et al., 2006; Miller-Rushing et al., 2009; Roth-Nebelsick et al., 2012; error margin when determining Ca from fossil stomata. All these un-
Wagneretal.,1996). certainties also affect calibration-based approaches. This
5
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
Fig.4.Resultsobtainedfromapplyingthemodel(expressions(1)through(5)and(7))toQuercuspetraea:(a)leafconductanceg,(b)assimilationrateA,(c)stomatal
densityνand(d)transpirationrateEasafunctionofatmosphericCO2forseveralvaluesofatmospherictemperatureTa.Relativeatmospherichumidityiswrel=0.6,
κ=0.77,leaflengthl=3cm,windspeedvwind=1m/s.AthighCalevels,thestomataldensityresponseν(Ca)increasinglylevelsoff,followingthebasicresponseofg
toincreasingCa.
“ecophysiological” error margin is, however, “hidden” for cali- 2000; Jackson and Blois, 2015; Williams and Jackson, 2007). In fact,
bration–basedmethods. thereisevidenceforshiftsinnichedemandsforpastvegetation,with
speciesdistributionsbeingincongruentwithpalaeoenvironmentaldata
(Worth et al., 2014). Non-analogue environments can also lead to
4.2. InterferenceofCO2withotherenvironmentalparametersandthe species compositions within a flora which cannot be found today
problemofnon-analogueclimates
(JacksonandWilliams,2004;WilliamsandJackson,2007).
tCaobOoo2Rutotehnse1prp8ole0nansnμevtmiorpoofhnlySmmsDieooanll−ontagd1ly,gpaloatnowrdaeCmeracienoitsgleorpgsWa.yr,UDtaEuonrfdcintochgnaesngifdlaiaenrcr-tiraeaebrlafslecy,rh,eCianawsgaitcimhnaflonrueusnaeplntsoecodnesbetooesf aag(ffsCseuaCc)mtoienwsdsaimdtteheorarsitdtnefsgome,rnhastnoiitmwdiveeveveperbeyrer,limtoohwduescehawff.mieWtbchitieteohnlfterCveCaasaptoee(ndcsetgCeataosFcefihugxatc.uhn4rag)ene.CsgIetain,rmtiChsaeeOy,f2iutthdnmuocstingiobhonett
recognized byCi/Ca data offossil plantmaterial derived from carbon bsterotnhgeesctasoentphlaatntwpehhyasivoeloaglyreaanddyepcaoslsoegdy.the period in which Ca acts
ilosowto-hpuems(idGietyrhacrotnedtitaiol.n,s2.01C2o)n.vLeorswelCy,aceolenvdaitteiodnsCcaancatnhemreiftoigreatmeilmowic causTeheevianpfloureanticoenocfoCnsauomnestrhaneaspt.irLaetaiofnteamffpeecrtsatlueraef,tienmtupernra,tduerpe,enbdes-
wateravailability:Plantsmaythereforeneedlesswaterunderelevated
alsoonleafsize,acharacterwhichissensitivetovariousenvironmental
Ca for the same or a higher amount of carbon harvest. The apparent parameters and therefore included as “proxy trait” in, for instance,
influenceofCaonwaterdemandhasvariousconsequences,depending CLAMP. The interrelationships between transpiration, evaporational
on vegetation type and environmental conditions. For example, a
temperateandmesicforestexposedtoelevatedCamayneedlesswater, coofo(alisnsgu,mCeOd2),inletaefrtswizieneadndentvemiropnemraetunrtaelreeffperectssenwthaincheaxrceelsluenittabexleamtopblee
due to lower g, leading to a higher soil water content (Bader et al.,
unraveled by a mechanistic analysis. In the following, these inter-
2013).Atwarmanddriersites,plantscanproducemorefoliagecover
relationships will be evaluated on a physical–physiological basis to
wfaictth,rtihseinrgecCean,tcoamntpharroepdotgoenpirce-rinisdeuisntriCaalCaapp(Deaornsothoueaffetecatl.,ve2g0e1t3a)t.ioInn aexrreirvteoantathfiersctoersrteilmataiotinosnboefttwheeepnulteaatifvesizbeiaasnwdhoicthheCrOe2ncvairnonpmosesnibtlayl
coverinvariousways,promotingLAIor“greening”oflandscapesbe-
parameters.
yondwhatisexpectedfromlocalprecipitation,asindicatedbyremote
sensingandotherdata(Ukkolaetal.,2016;Zhuetal.,2016).Manyof
thesedevelopmentscanbeexplainedby“CO2fertilization”whichisthe 4.3. DoesCO2affectleaftemperatureandleafsize?
enhancement of photosynthesis by elevated Ca, as is widely demon-
stratedbyexperiments(AinsworthandRogers,2007). 4.3.1. Largeleavesvs.smallleaves
Consequently, the taxon-specific humidity threshold limiting the Speciesshowinglargeleavesarepreferentiallyfoundinhumidha-
ecologicalnichecanbeshiftedbyCa.PossibleimpactofCO2onspecies- bitats which also show sufficient availability of nutrients (Givnish,
specific environmental demands means that current abiotic climate 1984;McDonaldetal.,2003;Nicotraetal.,2011;Peppeetal.,2011;
envelope data may not hold true for the past (or the future). Wrightetal.,2017).Also,thexylemoflarge-leavedtaxaisquitevul-
Combination of CO2 values different to extant levels with other en- nerabletocavitation,andthereforenotabletocopewithlowhumidity
vironmental parameters leads to “non-analogue climates”, meaning (Schreiberetal.,2016).Infact,leafsizeisaCLAMPparameterandis
conditionsforwhichnoextantcounterpartexists(BennettandWillis, occasionally also used alone as a proxy for palaeoprecipitation (Wilf
6
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
et al., 1998). The positive correlation of leaf size with humidity is
commonly explained on the basis of boundary layer conductance.
Largerobjectsshow—allotherfactorslikewindvelocityandsurface
topography being equal — a thicker boundary layer and therefore a
lower boundary layer conductance than smaller objects (Schuepp,
1993). Boundary layer conductance is a component of the total leaf
conductance, therefore also affecting gas exchange, but usually to a
minor (or even negligible) degree (Schuepp, 1993). For leaf heat
transfer, however, boundary layer conductance is crucial. With in-
creasing boundary layer thickness resistance to heat dissipation rises,
and large leaves will tend to higher leaf temperatures than smaller
leavesunderidenticalconditions.
Smallleavesshouldthereforebeparticularlysuitableinhotanddry
environmentsbecausenotranspirationisrequiredtopreventheatda-
mageand/ordepressionofphotosynthesisduetoexcessivelyhighleaf
temperatures(Yatesetal.,2010).Preventingheatdamageis,however,
nottheonlyfactorwhichcouplesrisingleaftemperaturetorisingwater
demand. With a given g, elevated leaf temperature promotes leaf-in-
ternal evaporation and, therefore, higher transpiration rates (Jones,
1992).Therelationshipbetweenboundarylayerthickness,leafsizeand
leaf temperature can be modulated by leaf shape, for example by
making the leaf longer and narrower (Monteith and Unsworth, 2008;
Schuepp, 1993).Also,theboundarylayerthicknessoflobedleavesis
substantially decreased and more independent of wind direction as
comparedtounlobedleaves(Roth-Nebelsick,2001;Vogel,2009).
Itisdifficulttoexactlypredictleaftemperatureforrealleavesunder
natural conditions. The well-known approximative equations for
boundarylayerthickness,suchasprovidedinNobel(2009),havetheir
origininengineeringscienceandfocusonartificialflatorroundobjects
with a smooth surface. Moreover, experimental studies often employ Fig. 5.Examples for branching axis systems of Devonian plants without
windchannelenvironmentswithlaminarinflowregimewhilenatural webbedleaves.(A)ApartofthebranchingsystemofPsilophyton,terminating
winds show a high turbulence intensity. Additionally, various leaf withisotomousultimateunits(redrawnfromBanksetal.,1975).(B)Alateral
surfacestructures,suchastrichomecovers,arecapableofanenhanced branchofPseudosporochnus,equippedwithultimateappendages(redrawnfrom
infraredreflectivityandaffectalsotheairflowpatternsaroundleaves. BerryandFairon-Demaret,2002).
Thus, strongly varying wind conditionsand complextopographic leaf
surface profiles substantially affect local leaf temperature and its dis- vegetationwhichisadaptedtolowCa,willindeedrunintoproblems
tributioninrealleaves(Leighetal.,2016;Saudreauetal.,2017;Wigley underthecurrentrisingCaandglobaltemperature?
andClark,1974).Althoughnaturalleaftemperatureprofilesaremuch Withrespecttothermaldamage,avalueofabout40°Cisquotedas
more complex than in approximative models, intensified convective general upper limit for thermostability (Larcher, 2003). However,
cooling will — in contrast to evaporative cooling — be principally plantsgrowinginhot andsunnyhabitatsarequitethermostable,and
advantageousunderconditionsoflimitedwateravailabilitybecauseit canbeabletotolerateleaftemperaturesof50–60°C(Larcher,2003).A
curbstranspirationalwaterloss.Growingsmallerand/orstrongerdis- mainconcernareextremeevents,suchasexceptionalheatwaveswhich
sected leaves represents thus a suitable strategy in warm and dry en- mayinfactdriveleaftemperatureintocriticalheights(O'sullivanetal.,
vironments. Leigh et al. (2016) showed that usually leaf temperature 2017),makingconvectiveheattransferanimportantissue.Beyondthe
exceeds air temperature, that this effect is positively correlated with topicofthermaldamage,thereisstilltheissueofhighertranspiration
effectiveleafwidth,andthatleafshapespromotingconvectiveleafheat rates in “warmer” leaves under a given stomatal conductance and
transfermightbefavouredinopenhabitats,aswasrecentlyfoundfor boundarylayer,duetorisingwatervaporcontentoftheleafinternal
Proteaceae(Onsteinetal.,2016). air.Thus,leaftemperatureandtranspirationrateare—allothercon-
ElevatedCamayindirectlyactuponleaftemperature,viasuppres- ditions being equal — positively and dynamically coupled. The final
singevaporativecoolingbytranspiration,leadingto“warmerleaves”. effectofelevatedCaonleaftemperatureis,however,difficulttopredict
The consequences of high CO2 for leaf temperature regulation were sincehighertranspirationratesleadtohigherevaporativecooling.In
discussedforfutureclimatescenariosunderthecurrentanthropogenic the following chapter, model studies addressing this interrelationship
riseofCO2,proposingthepossibilityofrisingmeanleaftemperatures arepresented.
(Cernusak et al., 2013; Doughty and Goulden, 2008; Voelker et al.,
2016).Also,theimpactofhighCaonleaftemperaturewasdiscussedas
a factor for leaf evolution for climates of the past (Lee et al., 2015; 4.3.2. ModellingtheinteractionofCO2,leaftemperatureandleafsize
ThesimplemodelintroducedinEqs.(1)to(5)canbeexpandedto
Beerling and Berner, 2005; McElwain et al., 1999). It was even pro-
predict leaf temperature T (in addition to leaf conductance g and
posed that high Ca levels which prevailed during early land plant
evolution were responsible for the considerable delay in the develop- transpiration rate E) if atmospheric temperature Ta, atmospheric hu-
mentofmacrophyllousleaves,duetothecircumstancethataverylow miditywa andinsolationaregiven.Thisisachievedbyincludingleaf
energy balance into the already derived system of equations. In the
stomatalconductancewassufficientatthattimetofuelphotosynthesis,
following a brief outline is provided. Conservation of energy under
andtheentirestructureofearlylandplantswasaccordinglyadapted,
stationaryconditionsrequires
showinglowstomataldensityandfinelydividedterminalpartsofthe
branchingstems(seeFig.5;RavenandEdwards,2014;Beerlingetal., (energyintoleaf)={energyoutofleaf}
2001).
+[energyconsumedbyleafmetabolism]
Does this mean that plants with large leaves, as components of a
7
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
Fig.6.DifferencebetweenleaftemperatureTandatmospherictemperatureTaasafunctionofleaflengthlforseveralvaluesofatmosphericCO2forQuercuspetraea.
ThesingleplotsrepresentdifferentcombinationsofwindspeedvwindandatmospherictemperatureTa.Relativeatmospherichumidityiswrel=0.6andCi/Caratiois
κ=0.77,forallcases.ThedifferentcoloursofthecurvesdenotetheatmosphericCO2–concentration.
Sincemetabolisticprocessesconsumeonlyaverysmallamountofthe γ≈45°(angleofsunabovehorizon),τN≈0.7(atmospherictransmit-
leafenergyinput,itisjustifiedtosimplyneglectthem.Inmathematical tance for moderate clear sky at moderate elevation), a≈0.60 (ab-
terms,leafenergybalanceamountsthento(Nobel,2009): sorptance of leaf for global radiation), r≈0.20 (reflectance of the
2K surroundingsforglobalradiation),aIR≈0.96(leafabsorptivityforin-
a(1+r)Sc N1/sin sin +aIR (Ts4urr+Ts4ky)=2eIRT4+ dair(T Ta) frared radiation), Tsurr≈20°C (temperature of the surroundings),
bl
Tsky≈−20°C(radiationtemperatureoftheclearsky),eIR≈0.96(leaf
+H E(T)
vap (6) emissivityforinfraredradiation).Severalofthesequantitiesvarywith
the composition of the surrounding vegetation and with climate. The
Thelefthandsideisthesumofdirectsolarradiationplussolarradia-
numerical values given represent typical values (for details consult
tion reflected by the surroundings (first term) and absorbed infrared
Nobel(2009)).
radiationemanatingfromthesurroundingsandthesky(secondterm).
Inthefollowingwepresentexemplarymodelresultsforleafcooling
The right hand side sums three kinds of leaf energy losses: infrared
and heating effects. From Fig. 6 some basic results concerning leaf
radiationemittedbytheleaf(firstterm),heatconductedthroughthe
boundarylayertotheopenatmosphere(secondterm)andthelossof coolingandheatingandtheimpactofCO2onleaftemperaturemaybe
derivedforQuercuspetraea:
latent heat stored in the water vapour which emanates from the leaf
interior(thirdterm).Thetranspirationrateisgivenby
• LeafheatingtakesplaceforatmospherictemperatureTa=15°Cand
E(T)=ag(wsat(T) wa) (7) cooling for Ta=35°C. At Ta=25°C, leaf temperature T is quite
awherDeH2Ow/aDCOd2e.nTohteestetmhepera(atubrseoludteep)endaetmncoespohfertihce shautumriadtiitoyn caonnd- • Tsniohmnei-ldeaxerpistetonendTtea.nfcoeroTfale=af2t5e°mCp.eTrahteureeffoenctCoafisCqauibteecwoemaeks,amndoraelmporost-
centration of water vapour within the leaf is given by the Clausiu-
sm–3Claanpdeycro2n=e5q3u0a6ti,onT,iwnsatK(eTl)vi=n)(c(1R/Tei)fe, 1(c92/7T4))(.c1F=urt2h.e0r35qu×an1t0it1i0esmaopl/- • LCneoaauofnncseilzedeaffomtreaemtltepevreasrtaeotdunrlCyeaofbocurctuliressanvfooenrseTtwhahe=ilce1hss5aw°rCeeaaksnh.doSrtertleoernvgatehtesatdnimCraop.uagctholyf
pearing in (6) are Sc=1366J/m2/s (solar constant), 3cm.
σ=5.67×10−8J/m2/s/K4 (Stefan–Boltzmann constant),
• Dependenceofleaf temperature onwind speedis not verystrong,
Kair=2.57×10−2J/m/s/K(coefficientofthermalconductivityofair butmorepronouncedforsmallerwindspeeds.
at 20°C), Hvap=40.68×103J/mol (vapourization heat of water),
8
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
Insummary,themodelresultsindicatethatlargeleaves—asop- R.D.,Lunt,D.J.,Pearson,P.N.,2016.ChangingatmosphericCO2concentrationwas
posed to general expectation — do not heat up under high air tem- theprimarydriverofearlyCenozoicclimate.Nature533,380–384.https://doi.org/
10.1038/nature17423.
perature, but evencooldown. Obviously,the transpirationaleffectof
Astorga,G.A.,Jordan,G.J.,Brodribb,T.,2016.Towardsunderstandingthefossilrecord
lowergunderelevatedCaisnotstrongenoughtobeofrelevanceforthe better:insightsfromrecentlydepositedplantmacrofossilsinasclerophyll-dominated
interconnectedprocessesofevaporationandheatdissipation.Moderate subalpineenvironment.Rev.Palaeobot.Palynol.233,1–11.https://doi.org/10.
1016/j.revpalbo.2016.06.004.URL:http://www.sciencedirect.com/science/article/
leaf heating occurs for larger leaves under lower air temperatures, as
pii/S0034666716301154.
wasalsoproposedbyOkajimaetal.(2012),butaretheneasilycooled Bader,M.K.F.,Leuzinger,S.,Keel,S.G.,Siegwolf,R.T.W.,Hagedorn,F.,Schleppi,P.,
bymoderatewindmovementswhichcommonlyoccurintreecanopies. Körner,C.,2013.CentralEuropeanhardwoodtreesinahigh-CO2future:synthesisof
It should, however, be emphasized that availability of water and an8-yearforestcanopyCO2enrichmentproject.J.Ecol.101,1509–1519.https://
doi.org/10.1111/1365-2745.12149.
thereforetranspirationwasnotrestricted.Themodelledsituationthus Bailey,I.,Sinnott,E.,1916.TheclimaticdistributionofcertaintypesofAngiosperm
applies toa situation ofunlimited watersupply and therefore unrest- leaves.Am.J.Bot.3,24–39.
ricted transpiration. Under these conditions, Ca has no or negligible Bakelre-aBvreosshin,Kte.Fm.,pPereaette,Rfo.Kre.s,t1t9r9ee7s..TEhceoleocgoylo7g8ic,a1l2s5ig0n–i1fi2c5a5n.chetotpfsl:o/b/eddoia.onrdg/t1o0ot.1h8ed90/
influence on leaf heat dissipation and does not limit leaf size. The 0012-9658(1997)078[1250:TESOLA]2.0.CO;2.
problem of overheating under elevated Ca is apparently of relevance Banks,H.P.,Leclercq,S.,Hueber,F.M.,1975.AnatomyandmorphologyofPsilophyton
onlyforhabitatsorsituationsoflowsoilwateravailability. dawsoniisp.n.fromthelateLowerDevonianofQuebec(Gaspé),andOntario,
Canada.Palaeontograph.Am.8,77–127.
Battipaglia,G.,Saurer,M.,Cherubini,P.,Calfapietra,C.,McCarthy,H.R.,Norby,R.J.,
5. Summary FrancescaCotrufo,M.,2013.ElevatedCO2increasestree-levelintrinsicwateruse
efficiency:insightsfromcarbonandoxygenisotopeanalysesintreeringsacrossthree
forestFACEsites.NewPhytol.197,544–554.https://doi.org/10.1111/nph.12044.
Thereismuchcurrentinterestinleaftrait–climatecorrelations,and Beerling,D.,1994.Predictingleafgasexchangeandδ13Cresponsestothepast30000
research which involves extrapolations of these correlations into the yearsofglobalenvironmentalchange.NewPhytol.128,425–433.
past,suchasreconstructionofpastclimatesbasedonleaftraits,orinto Beerling,D.,Osborne,C.,Chaloner,W.,2001.Evolutionofleaffrominlandlinkedto
the future would largely benefit from an improved understanding of atmosphericCO2declineinthelatePalaeozoicera.Nature410,352–354.
Beerling,D.,Royer,D.,2011.ConvergentCenozoicCO2history.Nat.Geosci.4,418–420.
functional traits. The circumstance that plant-based proxies for pa- Beerling,D.J.,Berner,R.A.,2005.Feedbacksandthecoevolutionofplantsandatmo-
laeoclimateappeartocatchoveralltrendsreasonablywellsuggeststhat sphericCO2.Proc.Natl.Acad.Sci.U.S.A.102,1302–1305.https://doi.org/10.1073/
pnas.0408724102.URL:http://www.pnas.org/content/102/5/1302.abstract.
variousresponsesofleaftraitstoenvironmentmaybealsoextrapolated
Beerling,D.J.,McElwain,J.C.,Osborne,C.P.,1998.Stomatalresponsesofthe‘living
intofutureclimatescenarios.However,someinconsistenciesandpro- fossil’GinkgobilobaL.tochangesinatmosphericCO2concentrations.J.Exp.Bot.49,
blemsremain.Ofspecialinterestarethemanifoldaspectsoftheimpact 1603–1607.
ofCO2onleaffunction.Vegetationwasrepeatedlyexposedtochanging Beerwlinilglo,wD.J(S.,aRliuxnhdegrbreance,aM).i,n20th0e0.suLbea-afrmcteictatbooltihceapnadstm9o0r0p0hoyloeagricsaolfregslopboanlseesnovfirdown-arf
CO2levelswhichwereoftencombinedwithchangingclimate,andboth mentalchange.NewPhytol.145,257–269.https://doi.org/10.1046/j.1469-8137.
representimportantdriversforlandplantevolution.Theimpactofnon- 2000.00582.x.
analogue climate situations, representing combinations of abiotic en- Bennett,K.D.,Willis,K.J.,2000.Effectofglobalatmosphericcarbondioxideonglacia-
l–interglacialvegetationchange.GlobalEcol.Biogeogr.9,355–361.https://doi.org/
vironmental parameters which do not exist today and particularly so
10.1046/j.1365-2699.2000.00201.x.
withsubambientorelevatedCO2,onplantfunctionisdifficulttopre- Bernacchi,C.,Pimentel,C.,Long,S.,2003.Invivotemperatureresponsefunctionsof
dict.Asanexample,thepossibleriseofleaftemperatureunderelevated parametersrequiredtomodelRuBP-limitedphotosynthesis.PlantCellEnviron.26,
1419–1430.
CO2wasconsidered,being expectedduetothecouplingoftranspira- Berninger,F.,Mäkela,A.,Hari,P.,1996.Optimalcontrolofgasexchangeduringdrought:
tional cooling and stomatal conductance. Since transpiration and leaf empiricalevidence.Ann.Bot.77,469–476.
temperaturearedynamicallylinked,thereis,however,nostraightfor- Berry,C.M.,Fairon-Demaret,M.,2002.ThearchitectureofPseudosporochnusnodosus
LeclercqetBanks:aMiddleDevoniancladoxylopsidfromBelgium.Int.J.PlantSci.
ward prediction of leaf heat dissipation under changing CO2 and a 163,699–713.
closeranalysisbasedonamodelconnectinggasexchangeandleafheat Boyce,C.,Lee,J.E.,2011.Anexceptionalroleforfloweringplantphysiologyintheex-
transfer indicated in fact that the effect of elevated CO2 on leaf tem- pansionoftropicalrainforestsandbiodiversity.Proc.R.Soc.B277,3437–3443.
Boyce,C.K.,Brodribb,T.J.,Feild,T.S.,Zwieniecki,M.A.,2009.Angiospermleafvein
perature may be minor, at least when water supply is not limited.
evolutionwasphysiologicallyandenvironmentallytransformative.Proc.R.Soc.
Correlations of leaf size with abiotic environmental parameters thus Lond.B:Biol.Sci.276,1771–1776.https://doi.org/10.1098/rspb.2008.1919.URL:
appear to be not — or only moderately — affected by Ca, at least in http://www.rspb.royalsocietypublishing.org/content/royprsb/276/1663/1771.full.
habitats with sufficient wateravailability. This example demonstrates pdf.
Boyce,C.K.,Zwieniecki,M.A.,2012.Leaffossilrecordsuggestslimitedinfluenceofat-
thatecophysiologicalanalysesoffunctionalleaftraitscanparticularly mosphericCO2onterrestrialproductivitypriortoangiospermevolution.Proc.Natl.
contribute to identifying adaptive features of leaf architecture and to Acad.Sci.109,10403–10408.https://doi.org/10.1073/pnas.1203769109.URL:
evaluatepredictionsintothefutureaswellasintothepast. http://www.pnas.org/content/109/26/10403.abstract.
Breecker,D.,Sharp,Z.,McFadden,L.D.,2009.Seasonalbiasintheformationandstable
isotopiccompositionofpedogeniccarbonateinmodernsoilsfromcentralNew
Acknowledgements Mexico,USA.Geol.Soc.Am.Bull.121,630–640.
Buckley,T.N.,Schymanski,S.J.,2013.Stomataloptimisationinrelationtoatmospheric
This work was partially financially supported by a grant of the CO2.NewPhytol.201,372–377.https://doi.org/10.1111/nph.12552.
Bunce,J.A.,2007.Lowcarbondioxideconcentrationscanreversestomatalclosureduring
Volkswagen Foundation to A.R.-N. within the program “Research in waterstress.Physiol.Plant.130,552–559.https://doi.org/10.1111/j.1399-3054.
Museums” (Ref. 87139). We thank the Editor and two anonymous 2007.00937.x.
Campbell,I.,1999.Quaternarypollentaphonomy:examplesofdifferentialredeposition
Reviewers for their constructive comments, and James Nebelsick,
anddifferentialpreservation.Palaeogeogr.Palaeoclimatol.Palaeoecol.149,
UniversityofTübingen,forcriticallyreadingtheEnglishmanuscript. 245–256.
Cernusak,L.A.,Winter,K.,Dalling,J.W.,Holtum,J.A.M.,Jaramillo,C.,Körner,C.,
Leakey,A.D.B.,Norby,R.J.,Poulter,B.,Turner,B.L.,Wright,S.J.,2013.Tropical
References
forestresponsestoincreasingatmosphericCO2:currentknowledgeandopportunities
forfutureresearch.Funct.PlantBiol.40,531–551.https://doi.org/10.1071/
Aalto,T.,Hari,P.,Vesala,T.,2002.Comparisonofanoptimalstomatalregulationmodel FP12309.URL:http://www.publish.csiro.au/paper/FP12309.
andabiochemicalmodelinexplainingCO2exchangeinfieldconditions.Sil.Fenn. Cowan,I.,1977.Stomatalbehaviourandtheenvironment.Adv.Bot.Res.4,117–227.
36,615–623. Cowan,I.,Farquhar,G.,1977.Stomatalfunctioninrelationtoleafmetabolismanden-
Ainsworth,E.A.,Long,S.P.,2005.Whathavewelearnedfrom15yearsoffree-airCO2 vironment.SymposiaoftheSocietyforExperimentalBiology471.
enrichment(FACE)?Ameta-analyticreviewoftheresponsesofphotosynthesis,ca- Coxall,H.,Wilson,P.,Pälike,H.,Lear,C.,Backman,J.,2005.Rapidstepwiseonsetof
nopypropertiesandplantproductiontorisingCO2.NewPhytol.165,351–372. AntarcticglaciationanddeepercalcitecompensationinthePacificOcean.Nature
Ainsworth,E.A.,Rogers,A.,2007.Theresponseofphotosynthesisandstomatalcon- 433,53–57.
ductancetorising[CO2]:mechanismsandenvironmentalinteractions.PlantCell Coxall,H.K.,Wilson,P.A.,2011.EarlyOligoceneglaciationandproductivityinthe
Environ.30,258–270. easternequatorialPacific:insightsintoglobalcarboncycling.Paleoceanography
Anagnostou,E.,John,E.H.,Edgar,K.M.,Foster,G.L.,Ridgwell,A.,Inglis,G.N.,Pancost, 26https://doi.org/10.1029/2010PA002021.n/a–n/a.
9
A.Roth-NebelsickandW.Konrad Flora xxx (xxxx) xxx–xxx
Cui,Y.,Schubert,B.A.,2017.AtmosphericpCO2reconstructedacrossfiveearlyEocene Hincke,A.J.C.,Broere,T.,Kürschner,W.M.,Donders,T.H.,Wagner-Cremer,F.,2016.
globalwarmingevents.EarthPlanet.Sci.Lett.478,225–233. Multi-yearleaf-levelresponsetosub-ambientandelevatedexperimentalCO2in
DeBoer,H.,Lammertsma,E.,Wagner-Cremer,F.,Dilcher,D.,Wassen,M.,Dekker,S., Betulanana.PLoSONE11,e0157400.https://doi.org/10.1371/journal.pone.
2011.Climateforcingduetooptimizationofmaximalleafconductanceinsubtropical 0157400.
vegetationunderrisingCO2.Proc.Natl.Acad.Sci.U.S.A.108,4041–4046.https:// Hinojosa,L.F.,Pérez,F.,Gaxiola,A.,Sandoval,I.,2011.Historicalandphylogenetic
doi.org/10.1073/pnas.1100555108. constraintsontheincidenceofentireleafmargins:insightsfromanewSouth
Diefendorf,A.F.,Mueller,K.E.,Wing,S.L.,Koch,P.L.,Freeman,K.H.,2010.Globalpat- Americanmodel.GlobalEcol.Biogeogr.20,380–390.https://doi.org/10.1111/j.
ternsinleaf13Cdiscriminationandimplicationsforstudiesofpastandfuturecli- 1466-8238.2010.00595.x.
mate.Proc.Natl.Acad.Sci.107,5738–5743.https://doi.org/10.1073/pnas. Huff,P.,Wilf,P.,Azumah,E.,2003.Digitalfutureforpaleoclimateestimationfromfossil
0910513107.URL:http://www.pnas.org/content/107/13/5738.abstract. leaves?Preliminaryresults.Palaios18,266–274.https://doi.org/10.1669/0883-
DiMichele,W.A.,1983.LepidodendronhickiiandgenericdelimitationinCarboniferous 1351(2003)018<0266:dffpef>2.0.co;2.URL:http://www.palaios.sepmonline.org/
lepidodendridlycopods.Syst.Bot.317–333. content/18/3/266.abstract.
Donohue,R.J.,Roderick,M.L.,McVicar,T.R.,Farquhar,G.D.,2013.ImpactofCO2fer- Jackson,S.T.,Blois,J.L.,2015.Communityecologyinachangingenvironment:per-
tilizationonmaximumfoliagecoveracrosstheglobe'swarm,aridenvironments. spectivesfromthequaternary.Proc.Natl.Acad.Sci.112,4915–4921.https://doi.
Geophys.Res.Lett.40,3031–3035. org/10.1073/pnas.1403664111.URL:http://www.pnas.org/content/112/16/4915.
Doughty,C.E.,Goulden,M.L.,2008.Aretropicalforestsnearahightemperature abstract.
threshold?J.Geophys.Res.Biogeosci.113https://doi.org/10.1029/2007JG000632. Jackson,S.T.,Williams,J.W.,2004.Modernanalogsinquaternarypaleoecology:here
n/a–n/a. today,goneyesterday,gonetomorrow?Annu.Rev.EarthPlanet.Sci.32,495–537.
Edwards,E.J.,Spriggs,E.L.,Chatelet,D.S.,Donoghue,M.J.,2016.Unpackingacentury- https://doi.org/10.1146/annurev.earth.32.101802.120435.
oldmystery:winterbudsandthelatitudinalgradientinleafform.Am.J.Bot.103, Jagniecki,E.A.,Lowenstein,T.K.,Jenkins,D.M.,Demicco,R.V.,2015.Eoceneatmo-
975–978. sphericCO2fromthenahcoliteproxy.Geology43,1075–1078.
Farquhar,G.,O’Leary,M.,Berry,J.,1982.Ontherelationshipbetweencarbonisotope Johnson,K.,1989.AhighresolutionmegafloralbiostratigraphyspanningtheCretaceous/
discriminationandintercellularcarbondioxideconcentrationinleaves.Aust.J.Plant TertiaryboundaryinthenorthernGreatPlains. UnpublishedPh.D.Thesis.
Physiol.9,121–137. Jones,H.,1992.PlantsandMicroclimate.PlantsandMicroclimate.CambridgeUniversity
Farquhar,G.,VonCaemmerer,S.,Berry,J.,1980.Abiochemicalmodelofphotosynthetic Press,Cambridge.
CO2assimilationinleavesofC3species.Planta149,78–90. Jordan,G.,2011.Acriticalframeworkfortheassessmentofbiologcialpalaeoproxies:
Feild,T.S.,Sage,T.L.,Czerniak,C.,Iles,W.J.D.,2005.Hydathodalleafteethof predictingpastclimateandlevelsofatmosphericCO2fromfossilleaves.NewPhytol.
Chloranthusjaponicus(Chloranthaceae)preventguttation-inducedfloodingofthe 192,29–44.
mesophyll.PlantCellEnviron.28,1179–1190.https://doi.org/10.1111/j.1365- Karst,A.L.,Lechowicz,M.J.,2007.Arecorrelationsamongfoliartraitsinfernsconsistent
3040.2005.01354.x. withthoseintheseedplants?NewPhytol.173,306–312.
Ferguson,D.,1985.Theoriginofleaf-assemblages–newlightonanoldproblem.Rev. Katul,G.,Manzoni,S.,Palmroth,S.,Oren,R.,2010.Astomataloptimizationtheoryto
Palaeobot.Palynol.46,117–188. describetheeffectsofatmosphericCO2onleafphotosynthesisandtranspiration.
Ferguson,D.K.,2005.Planttaphonomy:ruminationsonthepast,thepresent,andthe Ann.Bot.105,431–442.
future.Palaios20,418–428.https://doi.org/10.2110/palo.2005.P05-25p.URL: Kennedy,E.M.,Arens,N.C.,Reichgelt,T.,Spicer,R.A.,Spicer,T.E.V.,Stranks,L.,Yang,J.,
http://palaios.geoscienceworld.org/content/palaios/20/5/418.full.pdf. 2014.Derivingtemperatureestimatesfromsouthernhemisphereleaves.
Fischer,H.,Severinghaus,J.,Brook,E.,Wolff,E.,Albert,M.,Alemany,O.,Arthern,R., Palaeogeogr.Palaeoclimatol.Palaeoecol.412,80–90.https://doi.org/10.1016/j.
Bentley,C.,Blankenship,D.,Chappellaz,J.,2013.Wheretofind1.5millionyroldice palaeo.2014.07.015.URL:http://www.sciencedirect.com/science/article/pii/
fortheIPICS“Oldest-Ice”icecore.Clim.Past9,2489–2505. S0031018214003708.
Franks,P.,Beerling,D.,2009.CO2-forcedevolutionofplantgasexchangecapacityand Kohn,M.,Cerling,T.,2002.Stableisotopecompositionsofbiologicalapatite.Rev.
water-useefficiencyoverthePhanerozoic.Geobiology7,227–236. Mineral.Geochem.48,455–488.
Franks,P.J.,Adams,M.A.,Amthor,J.S.,Barbour,M.M.,Berry,J.A.,Ellsworth,D.S., Konrad,W.,Katul,G.,Roth-Nebelsick,A.,Grein,M.,2017.Areducedordermodelto
Farquhar,G.D.,Ghannoum,O.,Lloyd,J.,McDowell,N.,Norby,R.J.,Tissue,D.T.,von analyticallyinferatmosphericCO2concentrationfromstomatalandclimatedata.
Caemmerer,S.,2013.SensitivityofplantstochangingatmosphericCO2concentra- Adv.WaterResourc.104,145–157.https://doi.org/10.1016/j.advwatres.2017.03.
tion:fromthegeologicalpasttothenextcentury.NewPhytol.197,1077–1094. 018.URL:http://www.sciencedirect.com/science/article/pii/S0309170816305024.
https://doi.org/10.1111/nph.12104. Konrad,W.,Roth-Nebelsick,A.,Grein,M.,2008.Modellingofstomataldensityresponse
Franks,P.J.,Leitch,I.J.,Ruszala,E.M.,Hetherington,A.M.,Beerling,D.J.,2012. toatmosphericCO2.J.Theor.Biol.253,638–658.
PhysiologicalframeworkforadaptationofstomatatoCO2fromglacialtofuture Kovar-Eder,J.,2016.EarlyOligoceneplantdiversityalongtheUpperRhineGraben:the
concentrations.Phil.Trans.R.Soc.B:Biol.Sci.367,537–546. fossilfloraofRauenberg,Germany.ActaPalaeobot.56,329–440.
Franks,P.J.,Royer,D.L.,Beerling,D.J.,VandeWater,P.K.,Cantrill,D.J.,Barbour,M.M., Kürschner,W.,1996.LeafstomataasbiosensorsofpalaeoatmosphericCO2levels. PhD
Berry,J.A.,2014.NewconstraintsonatmosphericCO2concentrationforthe Thesis.
Phanerozoic.Geophys.Res.Lett.41,4685–4694.https://doi.org/10.1002/ Kürschner,W.,Stulen,I.,Wagner,F.,Kuiper,P.,1998.Comparisonofpalaeobotanical
2014GL060457. observationswithexperimentaldataontheleafanatomyofDurmastoak[Quercus
García-Amorena,I.,Wagner,F.,VanHoof,T.,GómezManzaneque,F.,2006.Stomatal petraea(Fagaceae)]inresponsetoenvironmentalchange.Ann.Bot.81,657–664.
responsesindeciduousoaksfromsouthernEuropetotheanthropogenicatmospheric Larcher,W.,2003.PhysiologicalPlantEcology,4thed.CambridgeUniversityPress,
CO2increase;refiningthestomatal-basedCO2proxy.Rev.Palaeobot.Palynol.141, Cambridge.
303–312. Lee,A.P.,Upchurch,G.,Murchie,E.H.,Lomax,B.H.,2015.Leafenergybalancemodelling
Gastaldo,R.A.,Ferguson,D.K.,Walther,H.,Rabold,J.M.,1996.Criteriatodistinguish asatooltoinferhabitatpreferenceintheearlyangiosperms.Proceedingsofthe
parautochthonousleavesinTertiaryalluvialchannel-fills.Rev.Palaeobot.Palynol. RoyalSocietyofLondonB:BiologicalSciences282https://doi.org/10.1098/rspb.
91,1–21. 2014.3052.URL:http://rspb.royalsocietypublishing.org/content/royprsb/282/
Gerhart,L.M.,Harris,J.M.,Nippert,J.B.,Sandquist,D.R.,Ward,J.K.,2012.Glacialtrees 1803/20143052.full.pdf.
fromtheLaBreatarpitsshowphysiologicalconstraintsoflowCO2.NewPhytol.194, Leigh,A.,Sevanto,S.,Close,J.D.,Nicotra,A.B.,2016.Theinfluenceofleafsizeandshape
63–69.https://doi.org/10.1111/j.1469-8137.2011.04025.x. onleafthermaldynamics:doestheoryholdupundernaturalconditions?PlantCell
Gerhart,L.M.,Ward,J.K.,2010.Plantresponsestolow[CO2]ofthepast.NewPhytol. Environ.https://doi.org/10.1111/pce.12857.n/a-n/a.
188,674–695.https://doi.org/10.1111/j.1469-8137.2010.03441.x. Li,S.F.,Jacques,F.M.B.,Spicer,R.A.,Su,T.,Spicer,T.E.V.,Yang,J.,Zhou,Z.K.,2016.
Givnish,T.,1979.OntheAdaptiveSignificanceofLeafForm.ColumbiaUniversityPress, Artificialneuralnetworksrevealahigh-resolutionclimaticsignalinleafphysiog-
NewYork,pp.375–473. nomy.Palaeogeogr.Palaeoclimatol.Palaeoecol.442,1–11.https://doi.org/10.1016/
Givnish,T.,2002.AdaptiveSignificanceofEvergreenvs.DeciduousLeaves:Solvingthe j.palaeo.2015.11.005.URL:http://www.sciencedirect.com/science/article/pii/
TripleParadox,vol.36https://doi.org/10.14214/sf.535.URL:http://www. S0031018215006434.
silvafennica.fi/article/535. Little,S.A.,Kembel,S.W.,Wilf,P.,2010.Paleotemperatureproxiesfromleaffossilsre-
Givnish,T.J.,1984.LeafandCanopyAdaptationsinTropicalForests.Springer interpretedinlightofevolutionaryhistory.PLoSONE5,e15161.https://doi.org/10.
Netherlands,Dordrecht,pp.51–84. 1371/journal.pone.0015161.
Givnish,T.J.,Kriebel,R.,2017.Causesofecologicalgradientsinleafmarginentirety: Loreto,F.,Harley,P.C.,DiMarco,G.,Sharkey,T.D.,1992.Estimationofmesophyll
evaluatingtherolesofbiomechanics,hydraulics,veingeometry,andbudpacking. conductancetoCO2fluxbythreedifferentmethods.PlantPhysiol.98,1437–1443.
Am.J.Bot.104,354–366. https://doi.org/10.1104/pp.98.4.1437.URL:http://www.plantphysiol.org/content/
Greenwood,D.,2005.Leafmarginanalysis:taphonomicconstraints.Palaios20,498–505. 98/4/1437.abstract.
Greenwood,D.,Wilf,P.,Wing,S.,Christophel,D.,2004.Paleotemperatureestimation Markwick,P.J.,1998.FossilcrocodiliansasindicatorsofLateCretaceousandCenozoic
usingleaf-marginanalysis:isAustraliadifferent?Palaios19,129–142. climates:implicationsforusingpalaeontologicaldatainreconstructingpalaeocli-
Grein,M.,Konrad,W.,Wilde,V.,Utescher,T.,Roth-Nebelsick,A.,2011.Reconstruction mate.Palaeogeogr.Palaeoclimatol.Palaeoecol.137,205–271.https://doi.org/10.
ofatmosphericCO2duringtheearlymiddleEocenebyapplicationofagasexchange 1016/S0031-0182(97)00108-9.URL:http://www.sciencedirect.com/science/
modeltofossilplantsfromtheMesselFormation,Germany.Palaeogeogr. article/pii/S0031018297001089.
Palaeoclimatol.Palaeoecol.309,383–391. Maxbauer,D.P.,Royer,D.L.,LePage,B.A.,2014.HighArcticforestsduringthemiddle
Grein,M.,Roth-Nebelsick,A.,Wilde,V.,2010.Carbonisotopecompositionofmiddle EocenesupportedbymoderatelevelsofatmosphericCO2.Geology42,1027–1030.
EoceneleavesfromtheMesselPit,Germany.Palaeodiversity3,1–7. McDonald,P.G.,Fonseca,C.R.,Overton,J.M.,Westoby,M.,2003.Leaf-sizedivergence
Haworth,M.,Elliott-Kingston,E.,McElwain,J.,2011.ThestomatalCO2proxydoesnot alongrainfallandsoil-nutrientgradients:isthemethodofsizereductioncommon
saturateathighatmosphericCO2concentrations:evidencefromstomatalindexre- amongclades?Funct.Ecol.17,50–57.https://doi.org/10.1046/j.1365-2435.2003.
sponsesofAraucariaceaeconifers.Oecologia167,11–19. 00698.x.
10