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HYPOTHESISANDTHEORYARTICLE published:17October2013 doi:10.3389/fpls.2013.00409 Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale JofreCarnicer1,2,3*,AdriàBarbeta2,3,DominikSperlich2,3,4,MartaColl2,3 andJosepPeñuelas2,3 1CommunityandConservationEcologyGroup,CentreforEcologicalandEvolutionaryStudies,UniversityofGroningen,Groningen,Netherlands 2CREAF,Barcelona,Spain 3GlobalEcologyUnit,ConsejoSuperiordeInvestigacionesCientíficas,CREAF-CEAB-CSIC-UAB,Barcelona,Spain 4DepartmentofEcology,UniversityofBarcelona,Barcelona,Spain Editedby: Recent large-scale studies of tree growth in the Iberian Peninsula reported contrasting NateMcDowell,LosAlamos positiveandnegativeeffectsoftemperatureinMediterraneanangiospermsandconifers. NationalLaboratory,USA Herewereviewthedifferenthypothesesthatmayexplainthesetrendsandproposethat Reviewedby: the observed contrasting responses of tree growth to temperature in this region could FrankGallagher,RutgerstheState be associated with a continuum of trait differences between angiosperms and conifers. UniversityofNewJersey,USA HenrikHartmann,Max-Planck Angiosperm and conifer trees differ in the effects of phenology in their productivity, in InstituteforBiogeochemistry, theirgrowthallometry,andintheirsensitivitytocompetition.Moreover,angiospermsand Germany coniferssignificantlydifferinhydraulicsafetymargins,sensitivityofstomatalconductance *Correspondence: to vapor-pressure deficit (VPD), xylem recovery capacity or the rate of carbon transfer. JofreCarnicer,Communityand Thesedifferencescouldbeexplainedbykeyfeaturesofthexylemsuchasnon-structural ConservationEcologyGroup,Centre forEcologicalandEvolutionary carbohydratecontent(NSC),woodparenchymalfractionorwoodcapacitance.Wesuggest Studies,UniversityofGroningen, thatthereviewedtraitdifferencesdefinetwocontrastingecophysiologicalstrategiesthat Nijenborgh7,9747AGGroningen, may determine qualitatively different growth responses to increased temperature and Netherlands drought. Improved reciprocal common garden experiments along altitudinal or latitudinal e-mail:[email protected] gradients would be key to quantify the relative importance of the different hypotheses reviewed. Finally, we show that warming impacts in this area occur in an ecological context characterized by the advance of forest succession and increased dominance of angiosperm trees over extensive areas. In this context, we examined the empirical relationships between the responses of tree growth to temperature and hydraulic safety margins in angiosperm and coniferous trees. Our findings suggest a future scenario in Mediterraneanforestscharacterizedbycontrastingdemographicresponsesinconiferand angiospermtreestobothtemperatureandforestsuccession,withincreaseddominance ofangiospermtrees,andparticularlynegativeimpactsinpines. Keywords: conifers, angiosperms, functional traits, mediterranean ecosystems, drought, temperature, carbon metabolism,growth INTRODUCTION et al., 2009; Carnicer et al., 2012) or the impacts of secondary Theassimilationandallocationofcarbonarefundamentalpro- consumersanddiseases(Baleetal.,2002). cessesallowingtreegrowth,development,survival,reproduction Recentecophysiologicalstudieshighlightthecoupleddynamic and defense (McDowell, 2011; Galiano et al., 2012; Sala et al., linksbetweenNSCcontentinwoodytissuesandseveralclimate- 2012). In addition, non-structural carbohydrates (NSCs) play dependent tree responses such as embolism prevention and a variety of functions in tree physiology, providing a temporal repair, growth, bud burst and leaf emergence (Johnson et al., buffer to reconcile differences in carbon supply and demand, 2012; Sala et al., 2012; Meinzer and McCulloh, 2013). These maintaining hydraulic transport and facilitating osmotic regu- studies suggest the existence of contrasting trait-based ecophys- lation, allowing leaf emergence and bud burst and actively par- iological strategies in major plant groups (Choat et al., 2012; ticipating in the prevention of frost and drought embolismand Johnsonetal.,2012;Meinzeretal.,2013)suchasangiospermand repair(Salaetal.,2012).Thedemographicperformanceoftrees, coniferoustrees.Arguably,anextnecessarystepistoanalyzehow however, is generally co-limited by other factors that frequently these contrasting ecophysiological strategies may be influencing interact in complex ways with the processes of carbon uptake thedistributionandabundanceoftreespeciesandtheirresponses and allocation, such as direct climatic effects on photosynthe- toglobalwarming. sis,growthandnutrientuptake(Körner,1998,2003;Rennenberg Recentlarge-scalestudieshavereportedcontrastingresponses et al., 2006), species-specific traits (Wright et al., 2004; Chave ofgrowthtotemperatureinangiospermandconiferoustreesin www.frontiersin.org October2013|Volume4|Article409|1 Carniceretal. Treegrowthandtraitsyndromes MediterraneanforestsoftheIberianPeninsula(Gómez-Aparicio angiospermtrees.Thefirsthypothesis(Table1.1)statesthatpos- et al., 2011; Coll et al., 2013). For example, Gómez-Aparicio itivegrowthresponsestoincreasedtemperatureinangiosperms et al. (2011) reported a positive effect of rising temperatures could be mediated by a less strict stomatal control, allow- on growth of angiosperm trees, but neutral or negative effects ing them to assimilate carbon for longer during warmer and on coniferous trees. These contrasting trends between the two drier periods. While this could imply that angiosperm could phylogenetic groups were later also observed and confirmed by be more vulnerable to xylem cavitation and hydraulic fail- Coll et al. (2013). Critically, whereas a reduction in precipi- ure, they have a greater capacity for embolism repair. On the tation was predicted to decrease tree growth in both groups, other hand, most conifers function with a wider hydraulic increases in temperature could produce a performance disad- safety margin to avoid cavitation but with the cost of lower vantage in conifers compared to angiosperm broadleaved trees carbon gain. Beside this specific hypothesis, several other fac- (Gómez-Aparicioetal.,2011;Colletal.,2013).Consistentwith tors could also contribute to explain the differences in growth theseempiricalfindingsthatassociatethenegativeeffectsoftem- responses between conifer and angiosperm trees. For example, peratures and growth in Pinus species, palaeoecological studies thesetwogroupsdifferintheeffectsofphenologyintheirpro- suggestapersistentlinkbetweenPinaceaedistributionsandlow ductivity, in the sensitivity of growth to competition, and in temperatures during the last 100 million years (Millar, 1993; growth allometry (Table1.2–1.4). In addition, local adaptation Brodribbetal.,2012).ColdperiodsinthePaleoceneandEocene processes and phenotypic plasticity also largely influence tree are associated with an increased abundance of fossils of the growth responses to temperature and drought (Table1.5–1.9). genusPinus,andthereverseoccursduringwarmperiods(Millar, Finally,theavailableempiricalevidencesuggeststhatthediverse 1993; Brodribb et al., 2012). Similarly, warm periods during factors significantly interact in determining growth responses theMioceneandPlioceneareapparentlyassociatedwithnorth- (Table1.7). For example, several studies report strong interac- wardcontractionsoftherangesofPinaceaespecies(Millar,1993; tions between tree size, drought, and stand density effects in Brodribbetal.,2012).Notably,theecophysiologicalbasisofthese determining large-scale growth patterns in the Mediterranean contrasting growth and distributional responses to temperature basin. Below we briefly review the hypotheses listed in Table1 remainpoorlydiscussedandresolved. anddiscusstheexperimentaltestsrequiredtoassesstheirrelative Herewereviewthehypothesesthatmaycontributetoexplain importance. the observed contrasting responses of growth to temperature observedinMediterraneanconifersandangiosperms.Wereview ECO-PHYSIOLOGICALANDHYDRAULICTRAITS.DIFFERENT the differences between Mediterranean conifer and angiosperm ECOPHYSIOLOGICALANDCARBON-ALLOCATIONSTRATEGIESIN treesingrowth-relatedtraits,includingphenology,crownallom- ANGIOSPERMSANDCONIFERS(HYPOTHESIS1.1) etry, sensitivity to competition, and drought and winter freez- Table2summarizesthetraitdifferencesbetweenangiospermand ing responses. Furthermore, we hypothesize that angiosperm coniferoustrees.Keytraitsthatdifferbetweenthesetwogroups andconiferousecophysiologicalstrategiesdifferentiallyintegrate includestomatalsensitivitytoVPD,xylemanatomy,foliartraits, diversetraitssuchasstomatalsensitivitytovapor-pressuredeficit hydraulic safety margins, capacity for embolism repair, NSC (VPD), hydraulic safety margins and capacity for embolism content, carbon transfer rates, wood parenchymal fraction, and repair, which in turn are linked to features of the xylem such wood capacitance. The available published evidence shows that as NSC content, carbon transfer rates, wood parenchymal frac- these diverse traits are functionally related and define two con- tion and wood capacitance. In sum, our main aims in this trastingecophysiologicalstrategiesinconifersandangiosperms. study are: (i) to list the different hypotheses that may explain Compared to angiosperms, conifers have a lower stomatal- contrasting growth responses to temperature in Mediterranean conductance sensitivity to increased VPD (sensu Johnson et al., conifer andangiosperm trees and review thedifferences ineco- 2012).Inturn,thiskeydifferenceinstomatalresponseappearsto physiological traits associated with temperature- and drought- betightlyrelatedtothedifferenthydraulicsafetymarginsinboth induced responses in these two groups, (ii) to briefly review groups (Tyree and Sperry, 1988; Nardini et al., 2001; Table2). the multiple effects of temperature on basic tree ecophysio- The wider hydraulic safety margins in conifers thus imply early logical functions (e.g., photosynthesis, growth, respiration and responses of stomatal closure, which reduce hydraulic conduc- nutrient uptake and transport), (iii) to analyze the specific tivity before substantial cavitation occurs. On the other hand, case study of forests in the Iberian Peninsula, which present angiospermscanmaintainrelativelyhighstomatalconductances divergingtreegrowthresponsestotemperatureinAngiosperms evenwhenthexylempressurecausedbyhighVPDissufficientto and Conifers, and (iv) to briefly discuss the implications of induceextensivecavitation(Meinzeretal.,2009,2013;Johnson our findings. Below we dedicate a section to each of these etal.,2012). objectives. In support of these trends, Choat et al. (2012) recently reportedthatspeciesinconiferousforestsgenerallyhaveahigher AREVIEWOFTHEDIVERSEHYPOTHESESTHATMAY resistancetodrought-inducedcavitationandoperatewithwider EXPLAINCONTRASTINGGROWTHRESPONSESTO hydraulic safety margins than do angiosperms. The minimum TEMPERATUREINMEDITERRANEANANDANGIOSPERM xylempressuresinconifersmeasuredinthefieldweremorepos- TREES itive than the xylem pressures causing a 50% loss of hydraulic Table1 lists the different hypotheses that may explain contrast- conductivity,andthustheriskofhydraulicfailurebycollapseof inggrowthtrendstotemperature inMediterranean coniferand thewater-conductingsystemwaslow.Incontrast,thehydraulic FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|2 Carniceretal. Treegrowthandtraitsyndromes Table1|MainhypothesesthatmaycontributetoexplaincontrastinggrowthresponsestotemperatureinIberianAngiospermandConifer treesonalargescale. Hypotheses Angiosperms Conifers References 1.1Eco-physiologicaland Narrowerhydraulicsafety Widehydraulicsafetymargins, Martínez-Ferrietal.,2000;Brodersen hydraulictraits marginsandhighercapacity earlydrought-inducedstomatal etal.,2010;Choatetal.,2012;Epronetal., toreverseembolisms closureandlowercarbongain, 2012;Johnsonetal.,2012;Michelotetal., lowstomatalconductance 2012;Salaetal.,2012;Brodersenand sensitivitytoVPD McElrone,2013;Colletal.,2013;Meinzer etal.,2013;Ogasaetal.,2013 1.2Phenology Treeproductivitymore Positivelyaffectedbutless Churkinaetal.,2005;Piaoetal.,2007; sensitivetogrowingseason sensitivetogrowingseason Welpetal.,2007;Delpierreetal.,2009; length length Richardsonetal.,2010;Gómez-Aparicio etal.,2011;Colletal.,2013 1.3Intra-andinter-specific Growthlesssensitivetointra Growthseverelyreducedbyintra- Sánchez-Gómezetal.,2008; competitionandforest andinter-specificstand andinter-specificcompetencein Gómez-Aparicioetal.,2011;Carniceretal., succession competition small,non-dominanttrees 2013a;Colletal.,2013;Vayredaetal.,2013 1.4Size,ageandallometry Differentgrowthallometry Peakofcrowngrowthreachedat Gómez-Aparicioetal.,2011;Poorteretal., andlessapicaldominance lowersizes 2012 1.5Droughtandtemperature Angiospermtreesareableto Droughtandheatwavesoften Martínez-Ferrietal.,2000;deLuisetal., maintainsubstantial resultsinearlystomatalclosurein 2007,2011;Zweifeletal.,2007;Eilmann transpirationlevelsduring Mediterraneanconifers etal.,2009;Camareroetal.,2010;Klein summerdroughtevents etal.,2011;Colletal.,2013;Poyatosetal., 2013 1.6Winterfreezing Angiospermtreesaremore Lesssensitivetofreeze-thaw SperryandSullivan,1992;Gómez-Aparicio vulnerabletofreeze-thaw embolism etal.,2011;Brodribbetal.,2012 embolism 1.7Interactionsbetweenmultiple Yes Yes Linaresetal.,2010;Gómez-Aparicioetal., factors 2011;Vayredaetal.,2012;Colletal.,2013; Ruiz-Benitoetal.,2013 1.8Localadaptation,individual Yes Yes Rehfeldt,1978,1982;Santosetal.,2010; andprovenancevariation Ramírez-Valienteetal.,2010,2011; Chmuraetal.,2011;Robsonetal.,2012; Albertoetal.,2013 1.9Phenotypicplasticity Yes Yes Camareroetal.,2010;Nicotraetal.,2010; deLuisetal.,2011 safety margins reported for angiosperms were narrower, being sensitivitytoVPDandlowresilience(gymnosperms)and(ii)low slightlypositiveorevennegative. cavitationresistancebuthighresilience(angiosperms). Thereporteddifferencesinstomatalsensitivityandhydraulic These two basic strategies are in turn functionally linked safetymarginshaveinturnbeenfunctionallyassociatedwithdif- to anatomical differences in cell anatomy, NSC content, wood ferent responses between both groups in the capacity of xylems parenchymalfraction,andwooddensity(Table2).Forexample, torecoverfromembolisms.Recentstudieshavereportedhigher boththepercentageoflivingparenchymaandtheconcentration capacitiesinspecieswithnarrowsafetymarginsandhigherstom- ofNSCsinthexylemaresignificantlyhigherinangiospermsthan atal sensitivities to VPD (see Johnson et al., 2012 for a precise inconifers(Johnsonetal.,2012andcitationstherein).Duringthe definition of stomatal sensitivity to VPD; Meinzer et al., 2013). reversalofembolisms,vesselrefillingprobablyrequiresaninput Thereversalofcavitationhasbeendemonstratedtobefeasibleon of energy (Meinzer et al., 2013) and the mobilization of stored anhourlyordailybasisandtooccurevenunderhighxylemten- carbohydrates.Livingwoodparenchymathusactsasareservoir sion(HackeandSperry,2003;Salleoetal.,2004;Brodersenetal., of both water and carbohydrates. Hence, NSCs stored in cells 2010;Zuffereyetal.,2011).Twogeneralbutcontrastinghydraulic surrounding vessels are likely to be the source of sugars needed strategies arise: (i) high cavitation resistance, low stomatal forthemaintenanceofvascularintegrity(Brodersenetal.,2010; www.frontiersin.org October2013|Volume4|Article409|3 Carniceretal. Treegrowthandtraitsyndromes Table2|Summaryofdifferencesinkeyfunctionaltraitsbetweenconifersandangiosperms. Trait Angiosperms Conifers References Woodanatomy Vessels Tracheids Brodribbetal.,2012 Ring-porousanddiffuse-porous Homogeneouspitmembrane Torus-margopitmembrane Cylindricalphloemsieveelements Cuboidalphloemsieveelements Jensenetal.,2012 Companioncells Strasburgercells Woodparenchymalfraction High Low Nardinietal.,2011;Meinzerand McCulloh,2013 Woody-tissueNSCcontent High Low Hochetal.,2003;Michelot etal.,2012 Wooddensity High Low Poorteretal.,2012 Xylemembolismrecoverycapacity High Low Buccietal.,2003;Salleoetal., 2004;Brodribbetal.,2010 Sensitivitytofreeze-thawembolism High Loworabsent Cavender-Baresetal.,2005 Hydraulicsafetymargins Narrowornegative Wide Choatetal.,2012 Waterpotentialcausing50%lossof Low High Choatetal.,2012 hydraulicconductivity Xylemcapacitance High(ring-porous) Low MeinzerandMcCulloh,2013 Medium(diffuse-porous) RateofCtransfer High Low Jensenetal.,2012 Sapflowvelocity High Low Jensenetal.,2012 Phloemconductivity High Low Jensenetal.,2012 Phloemsieve-elementresistance Low High Jensenetal.,2012 Leaflifespan Shorter Longer Lusketal.,2003 Shadetolerance High Low Poorteretal.,2012 Interspecific Yes Yes NiinemetsandValladares,2006 shade-tolerance/drought-tolerance trade-off Mesophyllicconductance High Low Niinemetsetal.,2011 Photosyntheticcapacity High Low Lusketal.,2003;Flexasetal., 2012 Stomataldensity High Low Flexasetal.,2012 Stomatalconductance High(ring-porous) Low Johnsonetal.,2012;Barbeta sensitivitytoVPD(m) Medium-low(diffuse-porous) etal.,2013;Meinzeretal.,2013; Poyatosetal.,2013 Distalleafandrootembolismand Rare Frequent Johnsonetal.,2012 refilling Salaetal.,2012).Sugarsarepossiblytransferredfromparenchy- tocavitationandthuscouldwithstandacertainlossofhydraulic malcellstoembolizedvesselsforestablishingagradienttodrive conductivity. waterawayfromeitherthephloem(Nardinietal.,2011)ornon- Finally, conifers and angiosperms also differ in cell anatomy embolizedvessels(Brodersenetal.,2010).Furthermore,Améglio and wood density (Table2), and several studies suggest func- et al. (2004) reported the catabolism of starch into sugars and tionalimplicationsforthesetraitsinclimate-inducedresponses. the subsequent efflux from parenchymal cells to the vessels in For example, wood density has been proposed as a good pre- late winter during the recovery of Juglans regia from cavitation dictor of the resistance of the xylem to drought stress, because inducedbythewinterfreeze-thaw.Likewise,thereporteddiffer- specieswithdenserwoodtendtohaveahigherresistancetocav- encesbetweenthecapacitiestoreverseembolismsinangiosperms itation(Jacobsenetal.,2007;Prattetal.,2007).Moreover,Ogasa andconifers(Johnsonetal.,2012;BrodersenandMcElrone,2013; et al. (2013) found a negative correlation between wood den- Meinzer et al., 2013) are likely associated with the differences sity and xylem recovery in deciduous angiosperm trees (Salix, insapwoodNSCcontentbetweenthesetwogroupsreportedby Betula, Carpinus, Cerasus), suggesting in turn a negative asso- Hoch et al. (2003). This empirical evidence suggests that NSC ciation between increased cavitation resistance and resilience of reservesinwoodparenchymalcellsplayakeyroleindetermin- xylemfunction.WooddensityinMediterraneanevergreenshrubs ing the hydraulic strategies of plants, because species with high was also negatively correlated with the percentage of parenchy- NSC and parenchymal fractions would have a higher resilience malareainthexylem(Jacobsenetal.,2007).Thiscorrelationis FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|4 Carniceretal. Treegrowthandtraitsyndromes consistentwiththehighercapacityofxylemstorecoverinspecies bequitevariable(speciesandsitespecific),wesuggestthatearly with wood of lower density reported by Ogasa et al. (2013), stomatalclosureandtheassociatedlargerreductionsofassimila- becauselivingxylemparenchymamaybeinvolvedinthereversal tion rates in conifers may consistently produce a more negative ofembolisms(Buccietal.,2003;Brodersenetal.,2010;Nardini impactonbothcarbonbalanceandgrowthresponsesoftrees. etal.,2011;Zuffereyetal.,2011;BrodersenandMcElrone,2013). Ontheotherhand,increasedwintertemperaturescanreduce In addition, low wood density has been associated with high the costs associated with the impacts of freeze-thaw embolism capacitance(Prattetal.,2007;Sperryetal.,2008;McCullohetal., andmayalsodifferentlyaffectthecarbonbalanceofangiosperms 2012).Inwater-stressedplants,ahighercapacitancefacilitatesthe andconifers.Critically,angiospermshaveahighersensitivityto transientreleaseofwaterstoredinlivingwoodcellstotheconduit freeze-thawembolism(Table2)andmayexperiencehighercosts. lumen, increasing xylem water potential (Meinzer et al., 2009; Thisgroupcouldthusbenefitmorefromincreasedwintertem- Barnardetal.,2011;Zhangetal.,2011). peratures.Higherwintertemperatureswouldtherebyentailfewer The higher resistance of conifers to both freeze-thaw and freeze-thaw cavitations, which are responsible for the almost drought-induced cavitation (Sperry and Sullivan, 1992; Wang complete loss of hydraulic conductivity in ring-porous species et al., 1992; Choat et al., 2012) has also been associated with and for the partial loss in diffuse-porous species by late winter differences in wood anatomy (Table2). The main difference in (Sperry and Sullivan, 1992). The restoration of water transport wood anatomy between angiosperms and gymnosperms is that in angiosperms is achieved by the production of earlywood or the latter have tracheids that also provide mechanical strength byvesselrefilling,whichhavecarbondemandssuppliedbyNSCs (Hackeetal.,2001;Poorteretal.,2012).Inparticular,thickcon- (BarbarouxandBréda,2002;Epronetal.,2012;Michelotetal., duitwallsprovidingmechanicalstrengthhavebeensuggestedas 2012).Incontrast,sincethexylemsofconifersarehighlyresistant the factor limiting the size of tracheids in conifers (Pittermann to freeze-thaw cavitation (Sperry and Sullivan, 1992; Brodribb et al., 2006). Small tracheids are less prone to freeze-thaw cav- et al., 2012), this group may not have very different NSC costs itation in conifers (Tyree and Zimmermann, 1988; Sperry and fortherestorationofwatertransportaftermildorcoldwinters. Sullivan, 1992; Pittermann and Sperry, 2003), as are small ves- Winter temperature is a major driver for switching carbon selsinangiosperms(SperryandSullivan,1992),inwhichother allocationeithertostorageortogrowthandrespiration(Epron woodycellssuchasfibersareresponsibleformechanicalsupport et al., 2012; Körner, 2013) and for the conditioning accumula- oftheplant.Inbothgroups,however,nodirectrelationshiphas tion of starch (Oleksyn et al., 2000). When temperature is too beenfoundbetweenconduitsizeanddrought-inducedcavitation low for growth, carbon assimilation is still significant, so NSCs acrossspecies.Pitmembranearea,though,mustbelimited(asit derivedfromwinterphotosynthesisaremainlyallocatedtostor- iswhereair-seedingdevelops)toachieveacertainlevelofsafety ageduringcoldperiods(Rossietal.,2008;Fajardoetal.,2012). fromdrought-inducedcavitation,whichinturnlimitsthesurface In addition, the catabolism of starch into soluble carbohydrates areaandthusthesizeofconduitcells(Hackeetal.,2006;Jansen duringcoldperiodsmaypossiblymaintainintracellularosmotic etal.,2009;Brodribbetal.,2012). concentration,whichispositivelycorrelatedwithcoldhardiness We hypothesize that the reported trait differences between (Cavender-Baresetal.,2005;Morinetal.,2007).Inbothconifers conifers and angiosperms (Table2) constitute two different andangiosperms,increasedwintertemperaturesarelikelytoalter strategiesthatmayimplyqualitativelydifferentgrowthresponses cambiumactivation,growthallocationandthedynamicbalance to increased temperatures and drought in the Mediterranean among winter photosynthesis, starch storage, and soluble sugar region. The different stomatal responses to heat waves and concentrations. summer droughts, inducing drought-avoidance strategies and Finally,increasedwinter,springandautumntemperaturescan stomatal closure in conifers, would be key to determining these significantlyinfluencephenologicalresponses,advancingwinter differentgrowthresponses(Martínez-Ferrietal.,2000;Colletal., cambiumactivation,springbudburstandleafunfoldingordelay- 2013;Poyatosetal.,2013).Critically,thehighersensitivityofthe ing autumn leaf fall (Peñuelas and Filella, 2001). The derived stomatal conductance to increases in VPD in conifers may pro- extensionofthephenologicalperiodcouldhavestrongeffectson motenear-zeroassimilationratesandmaystronglylimitcarbon treeheightandgrowth(Vitasseetal.,2009a,b,2013;Lenzetal., uptakeandphotosynthesisoverextendedperiods(Martínez-Ferri 2012). Both the phenological cycles and the growth-associated et al., 2000; Johnson et al., 2012; Meinzer et al., 2013; Poyatos carbondynamics,however,arequalitativelydifferentinconifers, etal.,2013).Summerdroughtmaystronglyaffectcarbondynam- ring-porousdeciduoustrees,diffuse-porousdeciduoustrees,and icsandNSCmobilizationandconsumptioninbothconifersand evergreen oaks (Epron et al., 2012; Table3). These differences angiosperms,forexamplebyenhancingthecatabolismofstarch suggest that these groups may qualitatively differ in the relative to soluble sugars for increasing xylem tension and sap osmo- effectsofincreasedspringtemperaturesoncarbondynamicsand larity (Sala et al., 2012), mobilizing NSCs for embolism repair, treegrowth.Forexample,anincreaseintemperatureearlyinthe producingsolublesugarstostabilizecellularproteinsandmem- growing season may also increase vessel diameter in deciduous branes,stoppingcelldivisionandtreegrowthfavoringinturnthe angiospermsbutnotinconifers(MatisonsandBrumelis,2012). accumulationofphotosynthatesinstarch(PeñuelasandEstiarte, 1998; Estiarte and Peñuelas, 1999; Körner, 2003) or promoting PHENOLOGY(HYPOTHESIS1.2) increased allocation of NSCs in roots and declines in fine-root An average lengthening of the growing season of about 11 days biomass (Anderegg, 2012). Even though the coupled effect of hasbeendetectedinEuropefromtheearly1960stotheendofthe these complex processes on the carbon balance of the tree may twentiethcentury(MenzelandFabian,1999;PeñuelasandFilella, www.frontiersin.org October2013|Volume4|Article409|5 Carniceretal. Treegrowthandtraitsyndromes es. Autumn Allocationofcarbontostorage(Epronetal.,2012).Extendedgrowingseason(Peñuelasetal.,2002;Vitasseetal.,2009a,b;GordoandSanz,2010).Anincreaseofdrought-inducedembolismmayalsoleadtoprematureleafabscission(Wangetal.,1992). Allocationofcarbontostorage(Epronetal.,2012;Rosasetal.,2013).Mediterraneanevergreenssometimeshaveagrowthpeakinautumn(Gutiérrezetal.,2011). (Continued) e evergreenbroadleafandconiferoustr Summer NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).ThesolublefractionofNSCsisusedtomaintainxylemandphloemintegrityandcellturgorunderdroughtconditions(Salaetal.,2012).Thesolublefractionincreasesindiffuse-porousspecies(Michelotetal.,2012).Anotherstudy,though,didnotobserveanincreaseinsolublefractionsorobservedreductions(Hochetal.,2003).HigherstomatalconductanceanddynamicembolismrepaircapacitymayallowCassimilationevenunderacertaindegreeofwaterdeficit(Johnsonetal.,2012). NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).ThesolublefractionofNSCsisusedtomaintainxylemandphloemintegrityandcellturgorunderdroughtconditions(Salaetal.,2012).Thesolublefractionpeaksinsummerinsomespecies(Rosasetal.,2013).Donotclosestomatacompletelyevenunderhighevaporativedemandandlowsoilwatercontent(OgayaandPeñuelas,2003;Barbetaetal.,2012).Narrowerxylemvesselsthanindeciduousoaksreducelossesofhydraulicconductance(SperryandSullivan,1992;Wangetal.,1992inotherspecies). af, wthphenologyindeciduousbroadle Spring Theonsetofradialgrowthoccursbeforebudburstinring-porousspeciesandafterbudburstindiffuse-porousspecies(Michelotetal.,2012).NSCscontributetogrowthinbothring-anddiffuse-porousspecies(Epronetal.,2012)butmoreimportantlyinring-porousspecies(BarbarouxandBréda,2002;Palacioetal.,2011;Michelotetal.,2012).Starchcontentdecreasesinring-poroustrees,andsugarsdecreaseindiffuse-poroustrees(Michelotetal.,2012).Milderwintertemperaturesmayfavortheformationofwidervesselsinring-porousspeciesinearlyspring(MatisonsandBrumelis,2012).Extendedgrowingseasonwithhigherspringtemperatures(Peñuelasetal.,2002;GordoandSanz,2010). DeclineinNSCcontentbylatespring(Rosasetal.,2013),probablyinvestedingrowth.Asindeciduoustrees,vesseldiameterisalsoconstrainedbywintertemperatures(Cavender-Baresetal.,2005).Extendedgrowingseasonwithhighertemperatures(Peñuelasetal.,2002;GordoandSanz,2010). o gr e heseasonaldynamicsofNSCsand Winter Lossofhydraulicconductivityduetofreeze-thaws,beinghigherinring-porousthanindiffuse-porousspecies(SperryandSullivan,1992;Wangetal.,1992;Cavender-Baresetal.,2005;Michelotetal.,2012).Beforebudburst,somespeciesmayrefillembolizedvesselsusingNSCs(Améglioetal.,2004). Reducedlossesinhydraulicconductivitycausedbyfreeze-thaws,althoughevergreentreesaremoreresistantthandeciduousspecies(Cavender-Baresetal.,2005).Cassimilationallocatedmainlytostoragewhentemperatureistoolowforgrowth(Körner,2003).NSCreservesincreasethroughoutthwinter(Rosasetal.,2013).Annualpeakinphotosyntheticratesforsomespecies(OgayaandPeñuelas,2003). t maryof mtrees mtrees briefsum angiosper angiosper e3|A duous green Tabl Deci Ever FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|6 Carniceretal. Treegrowthandtraitsyndromes h0; n 2001; Linderholm, 2006; Menzel et al., 2006). Growing season owt201 pro lengthhasastrongeffectontreeproductivity,Consequently,the agral., e(E reportedtemperature-inducedchangesinphenologycouldaffect aveoet orag tree growth responses (White et al., 1999; Kramer et al., 2000; her st Picardetal.,2005;Delpierreetal.,2009;Richardsonetal.,2009; ersmar to Vitasse et al., 2009a,b; Dragoni et al., 2011; Rossi et al., 2011; anconifmn(Ca2012).carbon Lthuagtotheteapl.r,o2d0u1c2t)i.vEitmypoifriecvaelregvriedeenncneeeindlteelmeapfefroarteesttsreiesslseussggseesnt-s Autumn MediterranepeakinautuPashoetal.,Allocationofetal.,2012). sf2soie0tnri1evs0sei)ttsi.tvo(FiWtopyreholiepfnnnseotetaltoaneglcc.y,eo2,st0yhC0saht7neu;mrDikspeipnlrproaoideedruturceactlite.vitvi(tia2ytly0.t,0oo25f0g)0rdor9eew;cpRiiodnirucgthoesaduerasdassobodnrnioflafeeedntrlgeaentalh.tf, in deciduous forests (5.8+0.7g C m−2 d−1), compared with evergreen needleleaf forests (3.4+0.3g C m−2 d−1). Similarly, Summer NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).Peakofstarchcontentbeforetheonsetoflatewood(Oberhuberetal.,2011).Xylemstructureisingeneralhighlyresistanttocavitation(Choatetal.,2012;Johnsonetal.,2012).Verytightstomatalcontrolmayleadtonear-zerocarbonassimilation(Poyatosetal.,2013). PtdiuMtsbrnerepo−niamsaeett1npHeodchevosisiipofiletnetncaerwetrcotsrodgdeeaenrdreeslaviiewf.ucnfneifeei(necrhtednr2,octaeubi0tvntansdoou0hinitetu7deofhdcyef)rsfoedebtarfrrnqlupooeeeniurhpnlrfegseaegeeotvtialrsronriitfsatotdtrsosnaweep,fealtddoeoneciinvrnrogcgbddeemgyemruslioyftdasfopswptene)dnrasora.tgerieehsifeeitTnntfoosdrerohttn,seersapweessaovelpeneiteungrvtootnmhrrasbngopirets4ctkwihieeheot.vnens9rttminohyet(or+iew9o.peenos.lspllF8of2eeaoomogdx.+s5rlryfpgaatgeerageyi2rg,ndcnre.Ceoi6ssodieattpsscgsmalscoo-cnrsasuCenen−pcplcmrgesee2eoe.m,ccaadssaiilfiyen−−fitnoissindc21r---s tudinalandlatitudinalgradients,reportingbothadvances,delays andnon-significantclines(Vitasseetal.,2009a,b,2013;Alberto etal.,2013).Forexample,dependingonthespeciesconsidered, ot Spring Carbohydratedemandofnew-leafcohortsissuppliedmainlybyoldercohorts(Eilmannetal.,2010;Micheletal.,2012).GrowthisapparentlynotdependentonNSCs(Michelotetal.,2012).Hightemperaturesmayleadtoanearlieronsetofradialgrowth(Camareroetal.,2010). VbwpcdYstoepoueuehiametutlseraIawcelnmnpytsditeresoeieeesasrtlnsenophlal(.geotgr,Kepautwiy2chödnrMaa0erevgaltnnn1san.he0pneohdde(pr)hlc2aiortefgaev0aoeugdnrnen0rdyoldor9fidbluwae(lblecBoaGnlat)eemfghaefnofysaef.ceerolmnionecdFdaurtmtooene,nrrdrneodp2adgigtfn0elfeieifgx1fidpnocexra0ehorcnoSm)deaesi,wa.lninlpantaimttdinsnlhlzvey,gdeet,cha2(eosaraKne0atuennr1römqnonlda0ryutnunan)ei.njgaanerroH-nelreurwimggdnaoadaraltwenotlrruaniidmawevivttntveeestiiBedvh,nrsrcsea.gu,wosmoMtcelrhihefcfnraiofreeedcxe,srlhweeciasem2cftitoifsoimi0nedovun1tcoeuname0atrny-rssl;, oftemperatureonthephenologyofmanyconiferandangiosperm tree species in the Mediterranean basin remain yet relatively poorly quantified (Maseyk et al., 2008). It remains also uncer- nued Winter Freeze-thawresistantspecies.Noaccumulatedlossesinhydraulicconductivity(Wangetal.,1992).LowtemperaturesmayresultinanincreaseofNSCs(Hoch,2008;Fajardoetal.,2012;Gruberetal.,2012;HochandKörner,2012).HighminimumtemperaturesmayadvanceearlywoodformationinMediterraneanconifers(Pashoetal.,2012). Tflbeltdbbaaeaatnieaahatliltstdleanifewezi-ldn.aratawe,sae,trunea2ietthotndmeed0euenn,r0ttMmeogtihh7nicur,oeeneaoocgrd2npiswrfhn0iterpttsttroc1arelharais1sr(peetetdrL;esieadadeniCrsmn-aafieaaoooebnmdumfadrodeftranssttuaitghlsrrmatibsekefarilecerer.gdno,otsoienewsfp2nskp-iefafie0io(rhtfnae0oLcfeonanf7asroshltdtn).cot,aa.dtkbhisnvl2nFayhyeeed0mcintan1woaabrtaaa0amfdteenfgl,)tveeelee.gp1ynnac,Fi9lmntsoeoi8todctsnoba3reebpeyro;slliteaoaetndhLerghyafrsmieeeeffvtc,fsaldneMheepnatduraorrnceafteqiweidnudrenu,piiitgsetcauiihenrnnzl(flmeeri,tdcctrnsua1rrrenaposeete9noihaamlL8voelnssiuee4naeegosali)nddgyye-sf. nti o to drought in holm oak forests (Bussotti et al., 2003; Misson C ble3| nifers eintainl.,co2m01p0l)e.tDelreoaufgnhuttarliseontcaturasnesslfooclaiatigoentoanfadllienacrrleiearseadndnurtersiuelntst Ta Co concentrationinlitter(Martínez-Alonsoetal.,2007). www.frontiersin.org October2013|Volume4|Article409|7 Carniceretal. Treegrowthandtraitsyndromes INTRA-SPECIFICCOMPETITION,INTER-SPECIFICCOMPETITIONAND different ecophysiological responses in Mediterranean conifers FORESTSUCCESSION(HYPOTHESIS1.3) andangiospermtrees(Martínez-Ferrietal.,2000;Zweifeletal., Empiricalstudiesrevealthatintra-specificcompetitionactsasa 2007; Eilmann et al., 2009). For instance, while drought often major determinant of growth patterns in Mediterranean forests results in early stomatal closure in Mediterranean conifers in both conifer and angiosperm trees (Gómez-Aparicio et al., (Martínez-Ferri et al., 2000; Klein et al., 2011; Poyatos et al., 2011). Forest densification due to land abandonment and the 2013), angiosperm trees are able to maintain substantial tran- advanceofsuccessionisoccurringoverextensiveareas,increas- spiration levels during summer drought events (Quero et al., ingcompetition,reducingtreegrowth,andincreasingmortality 2011). (Gómez-Aparicioetal.,2011;Vilà-Cabreraetal.,2011;Colletal., Drought largely determines cambium growth in 2013). Coll et al. (2013) reported much higher negative effects Mediterraneanforests,producingplasticandseasonallyvariable offoreststandbasalareaonconifergrowththaninangiosperm patterns, ranging from one single annual peak to markedly treesinbothdryandwetextremesofalarge-scalerainfallgradi- bimodal trends (Maseyk et al., 2008; Camarero et al., 2010; de ent,andthesetrendswereparalleledbyhighereffectsofbasalarea Luis et al., 2011). However, large-scale studies in the Iberian onsmall-treemortalityobservedinconifers.Theseresultscoin- peninsula reveal that competition effects on growth are often cidewithstudiesrevealingoakslesssensitivetocompetitionthan strongerthandroughteffects(Gómez-Aparicioetal.,2011;Coll pinesinthisarea(Sánchez-Gómezetal.,2008;Gómez-Aparicio et al., 2013). Nevertheless, strong interactions between compe- etal.,2011). tition and drought effects have been reported, and significantly Inter-specific competition also plays an important role in increase at the edge of climatic gradients (Linares et al., 2010; determining growth responses in Mediterranean conifer and Vayreda et al., 2012; Coll et al., 2013; Ruiz-Benito et al., 2013). angiosperm trees. Specifically, large-scale surveys suggest that Finally,thereisalsosomeevidenceofindividualpredispositions small-sized conifers are more sensitive to growth suppression to winter-drought induced tree dieback in P. sylvestris (Voltas bylatesuccessionalspecies(Gómez-Aparicioetal.,2011;Zavala et al., 2013), local adaptation for water use efficiency in P. etal.,2011;Colletal.,2013).Angiospermtreesaresignificantly halepensis (Voltas et al., 2008), and correlations of temperature expanding their distributional ranges, increasing recruitment and genetic variability at candidate loci for drought tolerance across extensive areas (Coll et al., 2013; Vayreda et al., 2013). in P. halepensis and P. pinaster (Grivet et al., 2011), suggesting Morover, during the last decades the expansion of the domi- important interactions between individual adaptive traits and nant angiosperm tree Quercus ilex hasnegatively influenced the droughtimpacts. recruitment success of five Pinus species on a large scale in this area(Carniceretal.,2013a). WINTERFREEZING(HYPOTHESIS1.6) Angiosperm trees are more vulnerable to freeze-thaw embolism SIZE,AGE,ANDALLOMETRY(HYPOTHESIS1.4) and this may contribute to explain the dominance of conifer Mediterranean conifers differ from angiosperm trees in their trees at high altitudes (Cavender-Bares et al., 2005; Brodribb allometrical relationships between tree size (diameter at breast et al., 2012) and could in turn result in qualitatively different height) and crown growth variables (Poorter et al., 2012). The growthresponsesinconifersandangiospermtrees.Forexample, peak of crown growth is generally reached at lower sizes in Gómez-Aparicio et al. (2011) reported that Atlantic deciduous conifers,whichalsoshowamuchsteeperdecreasewithsizethan broadleavedtreesintheIberianpeninsulahadlowercompetitive broadleaved species (Poorter et al., 2012). These different allo- response ability at lower temperatures, in contrast to mountain metric relationships are in turn associated with several other conifer species. In this study, tree growth of Atlantic deciduous traits (maximal height, crown size, shade tolerance, wood den- broadleaved trees was negatively affected by low temperatures sity,apicaldominance)andalsointeractwithlocalhabitataridity (Gómez-Aparicio et al., 2011). In line with this, several studies (Poorter et al., 2012). Similarly, Gómez-Aparicio et al. (2011) havedemonstratedthatlowwintertemperaturesdirectlyinhibit reported that in Iberian forests competitive effects for conifers celldivisionandtreegrowthincoldlocalities(Körner,1998,2013; scaleapproximatelyquadraticallywithdiameteratbreastheight Fajardoetal.,2012). (dbh2) and linearly for broadleaved trees. To our knowledge, it remains untested whether these different allometric relation- INTERACTIONSBETWEENMULTIPLEFACTORS(HYPOTHESIS1.7) shipsmightberelatedtothecontrastingtreegrowthresponsesto Tree growth patterns in the Iberian peninsula have several con- temperaturereportedinMediterraneanconifersandangiosperm tributingdriversthatinteractalonggeographicalgradients(Coll trees(Gómez-Aparicioetal.,2011). etal.,2013).Forinstance,Gómez-Aparicioetal.(2011)studied treegrowthresponsesin15treespeciesinSpainandreportedthat DROUGHTANDTEMPERATURE(HYPOTHESIS1.5) sensitivitytocompetitionincreasedwithdecreasingprecipitation Large-scalestudiesdemonstratethatdroughtandincreasedtem- inallspecies.Notably,thebestpredictivemodelsfortreegrowth peratures significantly limit tree growth in xeric regions of the in Gómez-Aparicio et al. (2011) included interactions between Mediterraneanbasin(Andreuetal.,2007;Martínez-Alonsoetal., size, competitive effects and climate variables. Similarly, Coll 2007;Sarrisetal.,2007;BoginoandBravo,2008;Martínez-Vilalta etal.(2013)modeledgrowthresponsesintheIberianpeninsula et al., 2008; Gómez-Aparicio et al., 2011; Vilà-Cabrera et al., and reported a significant increase in the strength of interac- 2011; Candel-Pérez et al., 2012; Sánchez-Salguero et al., 2012; tions between tree size, tree height and climate variables at the Vayreda et al., 2012;Coll et al., 2013) and produce qualitatively drier and wetter edges of rainfall gradients. These interactions FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|8 Carniceretal. Treegrowthandtraitsyndromes could increase with ongoing climate change, and several stud- assertthatmultiplecommongardenexperimentslocatedinlat- iessuggestthatwarmingcouldincreasecompetitionforwaterin itudinal and altitudinal gradients are particularly relevant to Mediterraneanforests(Linaresetal.,2010). studyphenologyandgrowthresponsestotemperature(Reichand Oleksyn,2008;Vitasseetal.,2010).Furthermore,theinclusionof LOCALADAPTATION,INDIVIDUAL-ANDPROVENANCEVARIATION differentprovenancesinthesereciprocalexperimentsallowsthe (HYPOTHESIS1.8) quantificationofenvironmentallyinducedphenotypicplasticity, Local selection processes may affect the adaptive traits deter- genotypicvarianceandtheirinteraction(e.g.,Vitasseetal.,2013). mining the different growth responses to temperature observed Complementarily, drought effects on growth could be studied in Iberian conifers and angiosperm trees. For example, prove- bymanipulativeexperimentscombinedwithreciprocalcommon nancestudiesinbothconiferandangiospermtreeshaverevealed garden designs (reviewed in Klein et al., 2011; Wu et al., 2011). genetic differences in growth rates and other growth-related Similarly,theeffectsofintra-andinter-specificcompetitioncould traits (age at reproduction, timing of bud burst and bud set, be studied manipulating tree densities and composition in dif- leaftraits,floweringphenology),suggestingthatpopulationsare ferentexperimentalgroups.Finally,toassesstreesizeeffectsand oftenadaptedtotheirlocalconditionsoftemperatureandwater allometric relationships, the study of saplings of different ages availability (Rehfeldt, 1978, 1982, 1988; Borghetti et al., 1993; would be required. Alternatively, long-term experiments could Climent et al., 2008; Mátyás et al., 2009; Rose et al., 2009; provide also relevant information to quantify allometric rela- Ramírez-Valienteetal.,2010,2011;Santosetal.,2010;Chmura tionships.Finally,inalltheseexperimentaldesigns,theperiodic et al., 2011; Robson et al., 2012; Alberto et al., 2013). In prove- measurementofecophysiologicaltraitsshouldbeimplementedto nance trial studies, populations from cold environments often assesstheirseasonalvariationandtheirputativeroleindetermin- cease growth earlier, while populations from warm localities inggrowthresponses. generally grow faster (Alberto et al., 2013). Notably, local selec- tion for increased growth rates may induce lower resistance COMPLEXANDMULTIPLEEFFECTSOFTEMPERATUREAND to drought and frost. For instance, in conifers fast-growing DROUGHTONTREEPHYSIOLOGY provenances often exhibit lower cold hardiness and/or lower Climate produces multiple and complex effects on tree physi- resistance to drought stress (Hannerz et al., 1999; Cregg and ology. As highlighted in Table1, we expect that multiple phys- Zhang, 2001; Chuine et al., 2006). These differences have been iological processes can simultaneously react to the changes in attributed to trade-offs between resistance to frost and drought environmentaltemperaturesandinfluencegrowthresponses.For and growth (Chuine et al., 2006 and see Martin St Paul et al., example,temperatureanddroughtdirectlyaffectseveralecophys- 2012). iological processes such as carbon and nutrient uptake, carbon PHENOTYPICPLASTICITY(HYPOTHESIS1.9) allocationbetweentissues,photosynthesis,respiration,processes Mediterraneantreesshowstrongplasticresponsesintreegrowth of embolism prevention and repair, phenological cycles, cam- patterns, which are associated with seasonal climate variabil- biumreactivation,celldivisionandexpansionorcarbontransfer ity (e.g., Camarero et al., 2010; de Luis et al., 2011). Critically, rates (Körner, 1998; Bréda et al., 2006; Rennenberg et al., 2006; phenologyandgrowthplasticityresponsesdifferbetweenprove- Sanz-Pérezetal.,2009;Camareroetal.,2010;Epronetal.,2012; nances and species and may determine observed demographic Michelotetal.,2012).Moreover,thesedirectclimaticeffectson and evolutionary responses to global warming (Nicotra et al., tree physiology can in turn produce secondary indirect effects, 2010). For example, low elevation provenances often exhibit forexamplethepromotionofsignalingandregulatoryresponses, greaterphenologicalplasticitytotemperaturethanhighelevation acclimation and phenotypically plastic responses or changes in provenances(Vitasseetal.,2013)andthiscouldinturninfluence geneexpression(reviewedinPeñuelasetal.,2013b).Table4pro- observed tree growth responses. To our knowledge, it remains vides a brief, non-exhaustive description of the diverse effects untested whether Mediterranean conifers exhibit higher growth of temperature and drought on tree physiology. It is impor- plasticity than angiosperm trees, although it has been reported tant to bear in mind that all these ecophysiological processes thatIberianconifersshowhighergrowthratesthanangiosperm often have different sensitivities and thresholds to temperature trees in absence of competition (Gómez-Aparicio et al., 2011; and water deficit. For example, tree growth and cambium acti- Poorteretal.,2012). vation are more sensitive to low temperatures than is photo- synthesis (Körner, 1998; Fajardo et al., 2012). In addition, as EXPERIMENTALASSESSMENTOFTHERELATIVECONTRIBUTIONOF shown in Table4, responses to climate are often species or tis- THEHYPOTHESES sue specific or depend on developmental stage and seasonal The available empirical evidence suggest that several factors phase and can be influenced by regulatory feedbacks that can interact and seem to determine contrasting growth responses oftenimplymulti-tissuecoordinatedresponses.Despitetheover- to temperature in Mediterranean conifer and angiosperm trees. whelmingcomplexityanddiversityoftheeffectsoftemperature Therefore, improved experimental approaches are required to and drought reported in Table4, several studies have demon- quantitatively assess the relative importance of these factors. strated consistent differences between major plant groups, such While several experimental and observational approaches could asconifersandangiosperms,inclimate-inducedresponses(e.g., be applied, we suggest that reciprocal provenance trial experi- Way and Oren, 2010; Gómez-Aparicio et al., 2011; Coll et al., mentsmaybeespeciallysuitedforthispurpose.Previousstudies 2013). www.frontiersin.org October2013|Volume4|Article409|9 Carniceretal. Treegrowthandtraitsyndromes Table4|Anon-exhaustiveandsyntheticreviewofthedifferenteffectsoftemperature(A)anddrought(B)ondifferenttreephysiological processes. References (A)EFFECTSOFTEMPERATUREONTREEPHYSIOLOGY Photosynthesis.Temperatureshigher/lowerthantheoptimumdecreasephotosynthesisandaffectmultiple Rennenbergetal.,2006 biochemicalprocesses.Forexample,hightemperaturescanreducetheefficiencyofelectrontransportinthe Morinetal.,2007 thylakoidmembraneofchloroplasts,whichinturndown-regulatethecontentofribulose-1,5-bisphosphateand KattgeandKnorr,2007 deactivateRubisco.HightemperaturesalsoinhibitRubiscoactivase,duetotheirlowthermaloptimum.The Chavesetal.,2012 solubilityofthetwosubstratesofRubisco,CO2,andO2,isdifferentiallyaffectedbytemperature,stimulating Flexasetal.,2012;Sharkeyand photorespirationandinhibitingphotosynthesisathightemperatures. Bernacchi,2012 PhotosystemIIisalsosensitivetohightemperatures,whichstimulatemechanismstoavoidphoto-oxidationand membranedenaturation,suchasisopreneproductionandthexanthophyllcycle. Lowtemperaturescauseavarietyofphysiologicalandacclimativeresponses,includingmodificationsinthe structureofthethylakoidmembraneinchloroplasts,alleviationofphotoinhibitionthroughupregulationofcarbon metabolismandincreasedsynthesisofstoragecarbohydrates,increasedproductionofantioxidants,preventionof intracellularfreezingbyincreasedsolublecarbohydrates(mobilizationofstarchtosucrose)andchangesingene expressionandsignalingpathways. Thegrowthenvironmentofplantsdeterminesthetemperatureoptimumofphotosynthesis.Inwarmer environments,plantsacclimatetoincreasethethermaloptimumofthemaximumcarboxylationvelocity(Vcmax) andthemaximumpotentialrateofelectrontransport(Jmax). Abovethethermaloptimumforphotosynthesis,theemissionofbiogenicvolatileorganiccompoundssuchas LlusiàandPeñuelas,2000; isopreneandmonoterpenesprogressivelyincreases. Rennenbergetal.,2006 Leaf respirationisstronglyaffectedbytemperature,increasingathightemperatures(e.g.,above35–40◦C)and Rennenbergetal.,2006;Smith peakingathighertemperaturesthanphotosynthesis. andDukes,2013 Hightemperaturesoftenincreasenetprimaryproductionandplantgrowth.Incold-adaptedtrees,photosynthesis Körner,1998;WayandOren, islesssensitivetolowtemperaturesthanistreegrowth(celldivisionandgrowth,cambiumactivation).Inalpine 2010;Wuetal.,2011;Fajardo treelines,newtissueformationisnearlyabsentattemperaturesaround5◦C,butconsiderableratesof etal.,2012;Lenzetal.,2012 photosynthesisaremaintainedbetween0and10◦C. Highertemperaturesinfluencefoliarphenology,promotingearlierbudburstanddelayingleaffall. PeñuelasandFilella,2001; Peñuelasetal.,2002;Vitasse etal.,2009a,b,2013 Intheabsenceofdrought,temperatureoftenincreasesnutrient-uptakecapacity(NH+,NO−,PO−,K+). Rennenbergetal.,2006 4 3 43 Temperaturecanalsoincreasebothxylemloadingofaminocompoundsandnitrogenallocationinaboveground tissues. Freezingcausescelldehydration,formationoficeinintracellularspacesandembolism.Budsaremoreresistant Morinetal.,2007;Augspurger, thanleavestofrost. 2009 Temperature,inabsenceofdrought,positivelyaffectsratesofsoilrespirationandlitterdecomposition. Wuetal.,2011 Organs,individuals,lifestagesandspeciesconsistentlydifferintheirphenologicalresponsestotemperatureand NiinemetsandValladares, sensitivitytodamagefromfrostanddrought. 2006;Morinetal.,2007; Augspurger,2009 (B)EFFECTSOFDROUGHTONTREEPHYSIOLOGY Photosynthesis.Droughtlimitsphotosynthesisbystomatalclosure,diffusionlimitationsinthemesophylland Chavesetal.,2012 metabolicimpairment.Itcanalsolimitphotosynthesisviasecondaryeffects,suchasreducedhydraulic SharkeyandBernacchi,2012 conductanceandoxidativestress. Droughtactivatesdiversesignalingpathwaysassociatedwithstomatalclosure.Forexample,itmodifiesabscisic acid(ABA)signalinginleaves,shootsandroots;increasesxylem-sappHandchangesaquaporinconcentrations, leafhydraulicconductancesignalsandelectricsignals. Droughtreducesosmoticpotentialinthesoilandpredawnleafwaterpotentialsandlimitswateruptake.To Rennenbergetal.,2006. maintainwateruptake,plantsincreasetheproductionofosmolites,down-regulateelectronfluxandincreasethe activityofantioxidantenzymes.Droughtcanalsoincreasethedegradationoffoliarproteinsandtheconcentration ofsolubleaminoacidsandNSCsintheleaves,whichmayactinturnasosmoprotectantstostabilizeproteinsand membranes.Droughtalsopromotesanincreaseintheconcentrationsofsolubleantioxidants. (Continued) FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|10

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Keywords: conifers, angiosperms, functional traits, mediterranean ecosystems, drought, temperature, carbon metabolism, growth . processes and phenotypic plasticity also largely influence tree growth responses to .. uptake and photosynthesis over extended periods (Martínez-Ferri et al., 2000
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Contrasting trait syndromes in angiosperms and conifers are associated with different responses of PDF

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HYPOTHESISANDTHEORYARTICLE published:17October2013 doi:10.3389/fpls.2013.00409 Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale JofreCarnicer1,2,3*,AdriàBarbeta2,3,DominikSperlich2,3,4,MartaColl2,3 andJosepPeñuelas2,3 1CommunityandConservationEcologyGroup,CentreforEcologicalandEvolutionaryStudies,UniversityofGroningen,Groningen,Netherlands 2CREAF,Barcelona,Spain 3GlobalEcologyUnit,ConsejoSuperiordeInvestigacionesCientíficas,CREAF-CEAB-CSIC-UAB,Barcelona,Spain 4DepartmentofEcology,UniversityofBarcelona,Barcelona,Spain Editedby: Recent large-scale studies of tree growth in the Iberian Peninsula reported contrasting NateMcDowell,LosAlamos positiveandnegativeeffectsoftemperatureinMediterraneanangiospermsandconifers. NationalLaboratory,USA Herewereviewthedifferenthypothesesthatmayexplainthesetrendsandproposethat Reviewedby: the observed contrasting responses of tree growth to temperature in this region could FrankGallagher,RutgerstheState be associated with a continuum of trait differences between angiosperms and conifers. UniversityofNewJersey,USA HenrikHartmann,Max-Planck Angiosperm and conifer trees differ in the effects of phenology in their productivity, in InstituteforBiogeochemistry, theirgrowthallometry,andintheirsensitivitytocompetition.Moreover,angiospermsand Germany coniferssignificantlydifferinhydraulicsafetymargins,sensitivityofstomatalconductance *Correspondence: to vapor-pressure deficit (VPD), xylem recovery capacity or the rate of carbon transfer. JofreCarnicer,Communityand Thesedifferencescouldbeexplainedbykeyfeaturesofthexylemsuchasnon-structural ConservationEcologyGroup,Centre forEcologicalandEvolutionary carbohydratecontent(NSC),woodparenchymalfractionorwoodcapacitance.Wesuggest Studies,UniversityofGroningen, thatthereviewedtraitdifferencesdefinetwocontrastingecophysiologicalstrategiesthat Nijenborgh7,9747AGGroningen, may determine qualitatively different growth responses to increased temperature and Netherlands drought. Improved reciprocal common garden experiments along altitudinal or latitudinal e-mail:[email protected] gradients would be key to quantify the relative importance of the different hypotheses reviewed. Finally, we show that warming impacts in this area occur in an ecological context characterized by the advance of forest succession and increased dominance of angiosperm trees over extensive areas. In this context, we examined the empirical relationships between the responses of tree growth to temperature and hydraulic safety margins in angiosperm and coniferous trees. Our findings suggest a future scenario in Mediterraneanforestscharacterizedbycontrastingdemographicresponsesinconiferand angiospermtreestobothtemperatureandforestsuccession,withincreaseddominance ofangiospermtrees,andparticularlynegativeimpactsinpines. Keywords: conifers, angiosperms, functional traits, mediterranean ecosystems, drought, temperature, carbon metabolism,growth INTRODUCTION et al., 2009; Carnicer et al., 2012) or the impacts of secondary Theassimilationandallocationofcarbonarefundamentalpro- consumersanddiseases(Baleetal.,2002). cessesallowingtreegrowth,development,survival,reproduction Recentecophysiologicalstudieshighlightthecoupleddynamic and defense (McDowell, 2011; Galiano et al., 2012; Sala et al., linksbetweenNSCcontentinwoodytissuesandseveralclimate- 2012). In addition, non-structural carbohydrates (NSCs) play dependent tree responses such as embolism prevention and a variety of functions in tree physiology, providing a temporal repair, growth, bud burst and leaf emergence (Johnson et al., buffer to reconcile differences in carbon supply and demand, 2012; Sala et al., 2012; Meinzer and McCulloh, 2013). These maintaining hydraulic transport and facilitating osmotic regu- studies suggest the existence of contrasting trait-based ecophys- lation, allowing leaf emergence and bud burst and actively par- iological strategies in major plant groups (Choat et al., 2012; ticipating in the prevention of frost and drought embolismand Johnsonetal.,2012;Meinzeretal.,2013)suchasangiospermand repair(Salaetal.,2012).Thedemographicperformanceoftrees, coniferoustrees.Arguably,anextnecessarystepistoanalyzehow however, is generally co-limited by other factors that frequently these contrasting ecophysiological strategies may be influencing interact in complex ways with the processes of carbon uptake thedistributionandabundanceoftreespeciesandtheirresponses and allocation, such as direct climatic effects on photosynthe- toglobalwarming. sis,growthandnutrientuptake(Körner,1998,2003;Rennenberg Recentlarge-scalestudieshavereportedcontrastingresponses et al., 2006), species-specific traits (Wright et al., 2004; Chave ofgrowthtotemperatureinangiospermandconiferoustreesin www.frontiersin.org October2013|Volume4|Article409|1 Carniceretal. Treegrowthandtraitsyndromes MediterraneanforestsoftheIberianPeninsula(Gómez-Aparicio angiospermtrees.Thefirsthypothesis(Table1.1)statesthatpos- et al., 2011; Coll et al., 2013). For example, Gómez-Aparicio itivegrowthresponsestoincreasedtemperatureinangiosperms et al. (2011) reported a positive effect of rising temperatures could be mediated by a less strict stomatal control, allow- on growth of angiosperm trees, but neutral or negative effects ing them to assimilate carbon for longer during warmer and on coniferous trees. These contrasting trends between the two drier periods. While this could imply that angiosperm could phylogenetic groups were later also observed and confirmed by be more vulnerable to xylem cavitation and hydraulic fail- Coll et al. (2013). Critically, whereas a reduction in precipi- ure, they have a greater capacity for embolism repair. On the tation was predicted to decrease tree growth in both groups, other hand, most conifers function with a wider hydraulic increases in temperature could produce a performance disad- safety margin to avoid cavitation but with the cost of lower vantage in conifers compared to angiosperm broadleaved trees carbon gain. Beside this specific hypothesis, several other fac- (Gómez-Aparicioetal.,2011;Colletal.,2013).Consistentwith tors could also contribute to explain the differences in growth theseempiricalfindingsthatassociatethenegativeeffectsoftem- responses between conifer and angiosperm trees. For example, peratures and growth in Pinus species, palaeoecological studies thesetwogroupsdifferintheeffectsofphenologyintheirpro- suggestapersistentlinkbetweenPinaceaedistributionsandlow ductivity, in the sensitivity of growth to competition, and in temperatures during the last 100 million years (Millar, 1993; growth allometry (Table1.2–1.4). In addition, local adaptation Brodribbetal.,2012).ColdperiodsinthePaleoceneandEocene processes and phenotypic plasticity also largely influence tree are associated with an increased abundance of fossils of the growth responses to temperature and drought (Table1.5–1.9). genusPinus,andthereverseoccursduringwarmperiods(Millar, Finally,theavailableempiricalevidencesuggeststhatthediverse 1993; Brodribb et al., 2012). Similarly, warm periods during factors significantly interact in determining growth responses theMioceneandPlioceneareapparentlyassociatedwithnorth- (Table1.7). For example, several studies report strong interac- wardcontractionsoftherangesofPinaceaespecies(Millar,1993; tions between tree size, drought, and stand density effects in Brodribbetal.,2012).Notably,theecophysiologicalbasisofthese determining large-scale growth patterns in the Mediterranean contrasting growth and distributional responses to temperature basin. Below we briefly review the hypotheses listed in Table1 remainpoorlydiscussedandresolved. anddiscusstheexperimentaltestsrequiredtoassesstheirrelative Herewereviewthehypothesesthatmaycontributetoexplain importance. the observed contrasting responses of growth to temperature observedinMediterraneanconifersandangiosperms.Wereview ECO-PHYSIOLOGICALANDHYDRAULICTRAITS.DIFFERENT the differences between Mediterranean conifer and angiosperm ECOPHYSIOLOGICALANDCARBON-ALLOCATIONSTRATEGIESIN treesingrowth-relatedtraits,includingphenology,crownallom- ANGIOSPERMSANDCONIFERS(HYPOTHESIS1.1) etry, sensitivity to competition, and drought and winter freez- Table2summarizesthetraitdifferencesbetweenangiospermand ing responses. Furthermore, we hypothesize that angiosperm coniferoustrees.Keytraitsthatdifferbetweenthesetwogroups andconiferousecophysiologicalstrategiesdifferentiallyintegrate includestomatalsensitivitytoVPD,xylemanatomy,foliartraits, diversetraitssuchasstomatalsensitivitytovapor-pressuredeficit hydraulic safety margins, capacity for embolism repair, NSC (VPD), hydraulic safety margins and capacity for embolism content, carbon transfer rates, wood parenchymal fraction, and repair, which in turn are linked to features of the xylem such wood capacitance. The available published evidence shows that as NSC content, carbon transfer rates, wood parenchymal frac- these diverse traits are functionally related and define two con- tion and wood capacitance. In sum, our main aims in this trastingecophysiologicalstrategiesinconifersandangiosperms. study are: (i) to list the different hypotheses that may explain Compared to angiosperms, conifers have a lower stomatal- contrasting growth responses to temperature in Mediterranean conductance sensitivity to increased VPD (sensu Johnson et al., conifer andangiosperm trees and review thedifferences ineco- 2012).Inturn,thiskeydifferenceinstomatalresponseappearsto physiological traits associated with temperature- and drought- betightlyrelatedtothedifferenthydraulicsafetymarginsinboth induced responses in these two groups, (ii) to briefly review groups (Tyree and Sperry, 1988; Nardini et al., 2001; Table2). the multiple effects of temperature on basic tree ecophysio- The wider hydraulic safety margins in conifers thus imply early logical functions (e.g., photosynthesis, growth, respiration and responses of stomatal closure, which reduce hydraulic conduc- nutrient uptake and transport), (iii) to analyze the specific tivity before substantial cavitation occurs. On the other hand, case study of forests in the Iberian Peninsula, which present angiospermscanmaintainrelativelyhighstomatalconductances divergingtreegrowthresponsestotemperatureinAngiosperms evenwhenthexylempressurecausedbyhighVPDissufficientto and Conifers, and (iv) to briefly discuss the implications of induceextensivecavitation(Meinzeretal.,2009,2013;Johnson our findings. Below we dedicate a section to each of these etal.,2012). objectives. In support of these trends, Choat et al. (2012) recently reportedthatspeciesinconiferousforestsgenerallyhaveahigher AREVIEWOFTHEDIVERSEHYPOTHESESTHATMAY resistancetodrought-inducedcavitationandoperatewithwider EXPLAINCONTRASTINGGROWTHRESPONSESTO hydraulic safety margins than do angiosperms. The minimum TEMPERATUREINMEDITERRANEANANDANGIOSPERM xylempressuresinconifersmeasuredinthefieldweremorepos- TREES itive than the xylem pressures causing a 50% loss of hydraulic Table1 lists the different hypotheses that may explain contrast- conductivity,andthustheriskofhydraulicfailurebycollapseof inggrowthtrendstotemperature inMediterranean coniferand thewater-conductingsystemwaslow.Incontrast,thehydraulic FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|2 Carniceretal. Treegrowthandtraitsyndromes Table1|MainhypothesesthatmaycontributetoexplaincontrastinggrowthresponsestotemperatureinIberianAngiospermandConifer treesonalargescale. Hypotheses Angiosperms Conifers References 1.1Eco-physiologicaland Narrowerhydraulicsafety Widehydraulicsafetymargins, Martínez-Ferrietal.,2000;Brodersen hydraulictraits marginsandhighercapacity earlydrought-inducedstomatal etal.,2010;Choatetal.,2012;Epronetal., toreverseembolisms closureandlowercarbongain, 2012;Johnsonetal.,2012;Michelotetal., lowstomatalconductance 2012;Salaetal.,2012;Brodersenand sensitivitytoVPD McElrone,2013;Colletal.,2013;Meinzer etal.,2013;Ogasaetal.,2013 1.2Phenology Treeproductivitymore Positivelyaffectedbutless Churkinaetal.,2005;Piaoetal.,2007; sensitivetogrowingseason sensitivetogrowingseason Welpetal.,2007;Delpierreetal.,2009; length length Richardsonetal.,2010;Gómez-Aparicio etal.,2011;Colletal.,2013 1.3Intra-andinter-specific Growthlesssensitivetointra Growthseverelyreducedbyintra- Sánchez-Gómezetal.,2008; competitionandforest andinter-specificstand andinter-specificcompetencein Gómez-Aparicioetal.,2011;Carniceretal., succession competition small,non-dominanttrees 2013a;Colletal.,2013;Vayredaetal.,2013 1.4Size,ageandallometry Differentgrowthallometry Peakofcrowngrowthreachedat Gómez-Aparicioetal.,2011;Poorteretal., andlessapicaldominance lowersizes 2012 1.5Droughtandtemperature Angiospermtreesareableto Droughtandheatwavesoften Martínez-Ferrietal.,2000;deLuisetal., maintainsubstantial resultsinearlystomatalclosurein 2007,2011;Zweifeletal.,2007;Eilmann transpirationlevelsduring Mediterraneanconifers etal.,2009;Camareroetal.,2010;Klein summerdroughtevents etal.,2011;Colletal.,2013;Poyatosetal., 2013 1.6Winterfreezing Angiospermtreesaremore Lesssensitivetofreeze-thaw SperryandSullivan,1992;Gómez-Aparicio vulnerabletofreeze-thaw embolism etal.,2011;Brodribbetal.,2012 embolism 1.7Interactionsbetweenmultiple Yes Yes Linaresetal.,2010;Gómez-Aparicioetal., factors 2011;Vayredaetal.,2012;Colletal.,2013; Ruiz-Benitoetal.,2013 1.8Localadaptation,individual Yes Yes Rehfeldt,1978,1982;Santosetal.,2010; andprovenancevariation Ramírez-Valienteetal.,2010,2011; Chmuraetal.,2011;Robsonetal.,2012; Albertoetal.,2013 1.9Phenotypicplasticity Yes Yes Camareroetal.,2010;Nicotraetal.,2010; deLuisetal.,2011 safety margins reported for angiosperms were narrower, being sensitivitytoVPDandlowresilience(gymnosperms)and(ii)low slightlypositiveorevennegative. cavitationresistancebuthighresilience(angiosperms). Thereporteddifferencesinstomatalsensitivityandhydraulic These two basic strategies are in turn functionally linked safetymarginshaveinturnbeenfunctionallyassociatedwithdif- to anatomical differences in cell anatomy, NSC content, wood ferent responses between both groups in the capacity of xylems parenchymalfraction,andwooddensity(Table2).Forexample, torecoverfromembolisms.Recentstudieshavereportedhigher boththepercentageoflivingparenchymaandtheconcentration capacitiesinspecieswithnarrowsafetymarginsandhigherstom- ofNSCsinthexylemaresignificantlyhigherinangiospermsthan atal sensitivities to VPD (see Johnson et al., 2012 for a precise inconifers(Johnsonetal.,2012andcitationstherein).Duringthe definition of stomatal sensitivity to VPD; Meinzer et al., 2013). reversalofembolisms,vesselrefillingprobablyrequiresaninput Thereversalofcavitationhasbeendemonstratedtobefeasibleon of energy (Meinzer et al., 2013) and the mobilization of stored anhourlyordailybasisandtooccurevenunderhighxylemten- carbohydrates.Livingwoodparenchymathusactsasareservoir sion(HackeandSperry,2003;Salleoetal.,2004;Brodersenetal., of both water and carbohydrates. Hence, NSCs stored in cells 2010;Zuffereyetal.,2011).Twogeneralbutcontrastinghydraulic surrounding vessels are likely to be the source of sugars needed strategies arise: (i) high cavitation resistance, low stomatal forthemaintenanceofvascularintegrity(Brodersenetal.,2010; www.frontiersin.org October2013|Volume4|Article409|3 Carniceretal. Treegrowthandtraitsyndromes Table2|Summaryofdifferencesinkeyfunctionaltraitsbetweenconifersandangiosperms. Trait Angiosperms Conifers References Woodanatomy Vessels Tracheids Brodribbetal.,2012 Ring-porousanddiffuse-porous Homogeneouspitmembrane Torus-margopitmembrane Cylindricalphloemsieveelements Cuboidalphloemsieveelements Jensenetal.,2012 Companioncells Strasburgercells Woodparenchymalfraction High Low Nardinietal.,2011;Meinzerand McCulloh,2013 Woody-tissueNSCcontent High Low Hochetal.,2003;Michelot etal.,2012 Wooddensity High Low Poorteretal.,2012 Xylemembolismrecoverycapacity High Low Buccietal.,2003;Salleoetal., 2004;Brodribbetal.,2010 Sensitivitytofreeze-thawembolism High Loworabsent Cavender-Baresetal.,2005 Hydraulicsafetymargins Narrowornegative Wide Choatetal.,2012 Waterpotentialcausing50%lossof Low High Choatetal.,2012 hydraulicconductivity Xylemcapacitance High(ring-porous) Low MeinzerandMcCulloh,2013 Medium(diffuse-porous) RateofCtransfer High Low Jensenetal.,2012 Sapflowvelocity High Low Jensenetal.,2012 Phloemconductivity High Low Jensenetal.,2012 Phloemsieve-elementresistance Low High Jensenetal.,2012 Leaflifespan Shorter Longer Lusketal.,2003 Shadetolerance High Low Poorteretal.,2012 Interspecific Yes Yes NiinemetsandValladares,2006 shade-tolerance/drought-tolerance trade-off Mesophyllicconductance High Low Niinemetsetal.,2011 Photosyntheticcapacity High Low Lusketal.,2003;Flexasetal., 2012 Stomataldensity High Low Flexasetal.,2012 Stomatalconductance High(ring-porous) Low Johnsonetal.,2012;Barbeta sensitivitytoVPD(m) Medium-low(diffuse-porous) etal.,2013;Meinzeretal.,2013; Poyatosetal.,2013 Distalleafandrootembolismand Rare Frequent Johnsonetal.,2012 refilling Salaetal.,2012).Sugarsarepossiblytransferredfromparenchy- tocavitationandthuscouldwithstandacertainlossofhydraulic malcellstoembolizedvesselsforestablishingagradienttodrive conductivity. waterawayfromeitherthephloem(Nardinietal.,2011)ornon- Finally, conifers and angiosperms also differ in cell anatomy embolizedvessels(Brodersenetal.,2010).Furthermore,Améglio and wood density (Table2), and several studies suggest func- et al. (2004) reported the catabolism of starch into sugars and tionalimplicationsforthesetraitsinclimate-inducedresponses. the subsequent efflux from parenchymal cells to the vessels in For example, wood density has been proposed as a good pre- late winter during the recovery of Juglans regia from cavitation dictor of the resistance of the xylem to drought stress, because inducedbythewinterfreeze-thaw.Likewise,thereporteddiffer- specieswithdenserwoodtendtohaveahigherresistancetocav- encesbetweenthecapacitiestoreverseembolismsinangiosperms itation(Jacobsenetal.,2007;Prattetal.,2007).Moreover,Ogasa andconifers(Johnsonetal.,2012;BrodersenandMcElrone,2013; et al. (2013) found a negative correlation between wood den- Meinzer et al., 2013) are likely associated with the differences sity and xylem recovery in deciduous angiosperm trees (Salix, insapwoodNSCcontentbetweenthesetwogroupsreportedby Betula, Carpinus, Cerasus), suggesting in turn a negative asso- Hoch et al. (2003). This empirical evidence suggests that NSC ciation between increased cavitation resistance and resilience of reservesinwoodparenchymalcellsplayakeyroleindetermin- xylemfunction.WooddensityinMediterraneanevergreenshrubs ing the hydraulic strategies of plants, because species with high was also negatively correlated with the percentage of parenchy- NSC and parenchymal fractions would have a higher resilience malareainthexylem(Jacobsenetal.,2007).Thiscorrelationis FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|4 Carniceretal. Treegrowthandtraitsyndromes consistentwiththehighercapacityofxylemstorecoverinspecies bequitevariable(speciesandsitespecific),wesuggestthatearly with wood of lower density reported by Ogasa et al. (2013), stomatalclosureandtheassociatedlargerreductionsofassimila- becauselivingxylemparenchymamaybeinvolvedinthereversal tion rates in conifers may consistently produce a more negative ofembolisms(Buccietal.,2003;Brodersenetal.,2010;Nardini impactonbothcarbonbalanceandgrowthresponsesoftrees. etal.,2011;Zuffereyetal.,2011;BrodersenandMcElrone,2013). Ontheotherhand,increasedwintertemperaturescanreduce In addition, low wood density has been associated with high the costs associated with the impacts of freeze-thaw embolism capacitance(Prattetal.,2007;Sperryetal.,2008;McCullohetal., andmayalsodifferentlyaffectthecarbonbalanceofangiosperms 2012).Inwater-stressedplants,ahighercapacitancefacilitatesthe andconifers.Critically,angiospermshaveahighersensitivityto transientreleaseofwaterstoredinlivingwoodcellstotheconduit freeze-thawembolism(Table2)andmayexperiencehighercosts. lumen, increasing xylem water potential (Meinzer et al., 2009; Thisgroupcouldthusbenefitmorefromincreasedwintertem- Barnardetal.,2011;Zhangetal.,2011). peratures.Higherwintertemperatureswouldtherebyentailfewer The higher resistance of conifers to both freeze-thaw and freeze-thaw cavitations, which are responsible for the almost drought-induced cavitation (Sperry and Sullivan, 1992; Wang complete loss of hydraulic conductivity in ring-porous species et al., 1992; Choat et al., 2012) has also been associated with and for the partial loss in diffuse-porous species by late winter differences in wood anatomy (Table2). The main difference in (Sperry and Sullivan, 1992). The restoration of water transport wood anatomy between angiosperms and gymnosperms is that in angiosperms is achieved by the production of earlywood or the latter have tracheids that also provide mechanical strength byvesselrefilling,whichhavecarbondemandssuppliedbyNSCs (Hackeetal.,2001;Poorteretal.,2012).Inparticular,thickcon- (BarbarouxandBréda,2002;Epronetal.,2012;Michelotetal., duitwallsprovidingmechanicalstrengthhavebeensuggestedas 2012).Incontrast,sincethexylemsofconifersarehighlyresistant the factor limiting the size of tracheids in conifers (Pittermann to freeze-thaw cavitation (Sperry and Sullivan, 1992; Brodribb et al., 2006). Small tracheids are less prone to freeze-thaw cav- et al., 2012), this group may not have very different NSC costs itation in conifers (Tyree and Zimmermann, 1988; Sperry and fortherestorationofwatertransportaftermildorcoldwinters. Sullivan, 1992; Pittermann and Sperry, 2003), as are small ves- Winter temperature is a major driver for switching carbon selsinangiosperms(SperryandSullivan,1992),inwhichother allocationeithertostorageortogrowthandrespiration(Epron woodycellssuchasfibersareresponsibleformechanicalsupport et al., 2012; Körner, 2013) and for the conditioning accumula- oftheplant.Inbothgroups,however,nodirectrelationshiphas tion of starch (Oleksyn et al., 2000). When temperature is too beenfoundbetweenconduitsizeanddrought-inducedcavitation low for growth, carbon assimilation is still significant, so NSCs acrossspecies.Pitmembranearea,though,mustbelimited(asit derivedfromwinterphotosynthesisaremainlyallocatedtostor- iswhereair-seedingdevelops)toachieveacertainlevelofsafety ageduringcoldperiods(Rossietal.,2008;Fajardoetal.,2012). fromdrought-inducedcavitation,whichinturnlimitsthesurface In addition, the catabolism of starch into soluble carbohydrates areaandthusthesizeofconduitcells(Hackeetal.,2006;Jansen duringcoldperiodsmaypossiblymaintainintracellularosmotic etal.,2009;Brodribbetal.,2012). concentration,whichispositivelycorrelatedwithcoldhardiness We hypothesize that the reported trait differences between (Cavender-Baresetal.,2005;Morinetal.,2007).Inbothconifers conifers and angiosperms (Table2) constitute two different andangiosperms,increasedwintertemperaturesarelikelytoalter strategiesthatmayimplyqualitativelydifferentgrowthresponses cambiumactivation,growthallocationandthedynamicbalance to increased temperatures and drought in the Mediterranean among winter photosynthesis, starch storage, and soluble sugar region. The different stomatal responses to heat waves and concentrations. summer droughts, inducing drought-avoidance strategies and Finally,increasedwinter,springandautumntemperaturescan stomatal closure in conifers, would be key to determining these significantlyinfluencephenologicalresponses,advancingwinter differentgrowthresponses(Martínez-Ferrietal.,2000;Colletal., cambiumactivation,springbudburstandleafunfoldingordelay- 2013;Poyatosetal.,2013).Critically,thehighersensitivityofthe ing autumn leaf fall (Peñuelas and Filella, 2001). The derived stomatal conductance to increases in VPD in conifers may pro- extensionofthephenologicalperiodcouldhavestrongeffectson motenear-zeroassimilationratesandmaystronglylimitcarbon treeheightandgrowth(Vitasseetal.,2009a,b,2013;Lenzetal., uptakeandphotosynthesisoverextendedperiods(Martínez-Ferri 2012). Both the phenological cycles and the growth-associated et al., 2000; Johnson et al., 2012; Meinzer et al., 2013; Poyatos carbondynamics,however,arequalitativelydifferentinconifers, etal.,2013).Summerdroughtmaystronglyaffectcarbondynam- ring-porousdeciduoustrees,diffuse-porousdeciduoustrees,and icsandNSCmobilizationandconsumptioninbothconifersand evergreen oaks (Epron et al., 2012; Table3). These differences angiosperms,forexamplebyenhancingthecatabolismofstarch suggest that these groups may qualitatively differ in the relative to soluble sugars for increasing xylem tension and sap osmo- effectsofincreasedspringtemperaturesoncarbondynamicsand larity (Sala et al., 2012), mobilizing NSCs for embolism repair, treegrowth.Forexample,anincreaseintemperatureearlyinthe producingsolublesugarstostabilizecellularproteinsandmem- growing season may also increase vessel diameter in deciduous branes,stoppingcelldivisionandtreegrowthfavoringinturnthe angiospermsbutnotinconifers(MatisonsandBrumelis,2012). accumulationofphotosynthatesinstarch(PeñuelasandEstiarte, 1998; Estiarte and Peñuelas, 1999; Körner, 2003) or promoting PHENOLOGY(HYPOTHESIS1.2) increased allocation of NSCs in roots and declines in fine-root An average lengthening of the growing season of about 11 days biomass (Anderegg, 2012). Even though the coupled effect of hasbeendetectedinEuropefromtheearly1960stotheendofthe these complex processes on the carbon balance of the tree may twentiethcentury(MenzelandFabian,1999;PeñuelasandFilella, www.frontiersin.org October2013|Volume4|Article409|5 Carniceretal. Treegrowthandtraitsyndromes es. Autumn Allocationofcarbontostorage(Epronetal.,2012).Extendedgrowingseason(Peñuelasetal.,2002;Vitasseetal.,2009a,b;GordoandSanz,2010).Anincreaseofdrought-inducedembolismmayalsoleadtoprematureleafabscission(Wangetal.,1992). Allocationofcarbontostorage(Epronetal.,2012;Rosasetal.,2013).Mediterraneanevergreenssometimeshaveagrowthpeakinautumn(Gutiérrezetal.,2011). (Continued) e evergreenbroadleafandconiferoustr Summer NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).ThesolublefractionofNSCsisusedtomaintainxylemandphloemintegrityandcellturgorunderdroughtconditions(Salaetal.,2012).Thesolublefractionincreasesindiffuse-porousspecies(Michelotetal.,2012).Anotherstudy,though,didnotobserveanincreaseinsolublefractionsorobservedreductions(Hochetal.,2003).HigherstomatalconductanceanddynamicembolismrepaircapacitymayallowCassimilationevenunderacertaindegreeofwaterdeficit(Johnsonetal.,2012). NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).ThesolublefractionofNSCsisusedtomaintainxylemandphloemintegrityandcellturgorunderdroughtconditions(Salaetal.,2012).Thesolublefractionpeaksinsummerinsomespecies(Rosasetal.,2013).Donotclosestomatacompletelyevenunderhighevaporativedemandandlowsoilwatercontent(OgayaandPeñuelas,2003;Barbetaetal.,2012).Narrowerxylemvesselsthanindeciduousoaksreducelossesofhydraulicconductance(SperryandSullivan,1992;Wangetal.,1992inotherspecies). af, wthphenologyindeciduousbroadle Spring Theonsetofradialgrowthoccursbeforebudburstinring-porousspeciesandafterbudburstindiffuse-porousspecies(Michelotetal.,2012).NSCscontributetogrowthinbothring-anddiffuse-porousspecies(Epronetal.,2012)butmoreimportantlyinring-porousspecies(BarbarouxandBréda,2002;Palacioetal.,2011;Michelotetal.,2012).Starchcontentdecreasesinring-poroustrees,andsugarsdecreaseindiffuse-poroustrees(Michelotetal.,2012).Milderwintertemperaturesmayfavortheformationofwidervesselsinring-porousspeciesinearlyspring(MatisonsandBrumelis,2012).Extendedgrowingseasonwithhigherspringtemperatures(Peñuelasetal.,2002;GordoandSanz,2010). DeclineinNSCcontentbylatespring(Rosasetal.,2013),probablyinvestedingrowth.Asindeciduoustrees,vesseldiameterisalsoconstrainedbywintertemperatures(Cavender-Baresetal.,2005).Extendedgrowingseasonwithhighertemperatures(Peñuelasetal.,2002;GordoandSanz,2010). o gr e heseasonaldynamicsofNSCsand Winter Lossofhydraulicconductivityduetofreeze-thaws,beinghigherinring-porousthanindiffuse-porousspecies(SperryandSullivan,1992;Wangetal.,1992;Cavender-Baresetal.,2005;Michelotetal.,2012).Beforebudburst,somespeciesmayrefillembolizedvesselsusingNSCs(Améglioetal.,2004). Reducedlossesinhydraulicconductivitycausedbyfreeze-thaws,althoughevergreentreesaremoreresistantthandeciduousspecies(Cavender-Baresetal.,2005).Cassimilationallocatedmainlytostoragewhentemperatureistoolowforgrowth(Körner,2003).NSCreservesincreasethroughoutthwinter(Rosasetal.,2013).Annualpeakinphotosyntheticratesforsomespecies(OgayaandPeñuelas,2003). t maryof mtrees mtrees briefsum angiosper angiosper e3|A duous green Tabl Deci Ever FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|6 Carniceretal. Treegrowthandtraitsyndromes h0; n 2001; Linderholm, 2006; Menzel et al., 2006). Growing season owt201 pro lengthhasastrongeffectontreeproductivity,Consequently,the agral., e(E reportedtemperature-inducedchangesinphenologycouldaffect aveoet orag tree growth responses (White et al., 1999; Kramer et al., 2000; her st Picardetal.,2005;Delpierreetal.,2009;Richardsonetal.,2009; ersmar to Vitasse et al., 2009a,b; Dragoni et al., 2011; Rossi et al., 2011; anconifmn(Ca2012).carbon Lthuagtotheteapl.r,o2d0u1c2t)i.vEitmypoifriecvaelregvriedeenncneeeindlteelmeapfefroarteesttsreiesslseussggseesnt-s Autumn MediterranepeakinautuPashoetal.,Allocationofetal.,2012). sf2soie0tnri1evs0sei)ttsi.tvo(FiWtopyreholiepfnnnseotetaltoaneglcc.y,eo2,st0yhC0saht7neu;mrDikspeipnlrproaoideedruturceactlite.vitvi(tia2ytly0.t,0oo25f0g)0rdor9eew;cpRiiodnirucgthoesaduerasdassobodnrnioflafeeedntrlgeaentalh.tf, in deciduous forests (5.8+0.7g C m−2 d−1), compared with evergreen needleleaf forests (3.4+0.3g C m−2 d−1). Similarly, Summer NSCsinleavesdecreasefromsummerthroughautumn(Hochetal.,2003).Peakofstarchcontentbeforetheonsetoflatewood(Oberhuberetal.,2011).Xylemstructureisingeneralhighlyresistanttocavitation(Choatetal.,2012;Johnsonetal.,2012).Verytightstomatalcontrolmayleadtonear-zerocarbonassimilation(Poyatosetal.,2013). PtdiuMtsbrnerepo−niamsaeett1npHeodchevosisiipofiletnetncaerwetrcotsrodgdeeaenrdreeslaviiewf.ucnfneifeei(necrhtednr2,octaeubi0tvntansdoou0hinitetu7deofhdcyef)rsfoedebtarfrrnqlupooeeeniurhpnlrfegseaegeeotvtialrsronriitfsatotdtrsosnaweep,fealtddoeoneciinvrnrogcgbddeemgyemruslioyftdasfopswptene)dnrasora.tgerieehsifeeitTnntfoosdrerohttn,seersapweessaovelpeneiteungrvtootnmhrrasbngopirets4ctkwihieeheot.vnens9rttminohyet(or+iew9o.peenos.lspllF8of2eeaoomogdx.+s5rlryfpgaatgeerageyi2rg,ndcnre.Ceoi6ssodieattpsscgsmalscoo-cnrsasuCenen−pcplcmrgesee2eoe.m,ccaadssaiilfiyen−−fitnoissindc21r---s tudinalandlatitudinalgradients,reportingbothadvances,delays andnon-significantclines(Vitasseetal.,2009a,b,2013;Alberto etal.,2013).Forexample,dependingonthespeciesconsidered, ot Spring Carbohydratedemandofnew-leafcohortsissuppliedmainlybyoldercohorts(Eilmannetal.,2010;Micheletal.,2012).GrowthisapparentlynotdependentonNSCs(Michelotetal.,2012).Hightemperaturesmayleadtoanearlieronsetofradialgrowth(Camareroetal.,2010). VbwpcdYstoepoueuehiametutlseraIawcelnmnpytsditeresoeieeesasrtlnsenophlal(.geotgr,Kepautwiy2chödnrMaa0erevgaltnnn1san.he0pneohdde(pr)hlc2aiortefgaev0aoeugdnrnen0rdyoldor9fidbluwae(lblecBoaGnlat)eemfghaefnofysaef.ceerolmnionecdFdaurtmtooene,nrrdrneodp2adgigtfn0elfeieifgx1fidpnocexra0ehorcnoSm)deaesi,wa.lninlpantaimttdinsnlhlzvey,gdeet,cha2(eosaraKne0atuennr1römqnonlda0ryutnunan)ei.njgaanerroH-nelreurwimggdnaoadaraltwenotlrruaniidmawevivttntveeestiiBedvh,nrsrcsea.gu,wosmoMtcelrhihefcfnraiofreeedcxe,srlhweeciasem2cftitoifsoimi0nedovun1tcoeuname0atrny-rssl;, oftemperatureonthephenologyofmanyconiferandangiosperm tree species in the Mediterranean basin remain yet relatively poorly quantified (Maseyk et al., 2008). It remains also uncer- nued Winter Freeze-thawresistantspecies.Noaccumulatedlossesinhydraulicconductivity(Wangetal.,1992).LowtemperaturesmayresultinanincreaseofNSCs(Hoch,2008;Fajardoetal.,2012;Gruberetal.,2012;HochandKörner,2012).HighminimumtemperaturesmayadvanceearlywoodformationinMediterraneanconifers(Pashoetal.,2012). Tflbeltdbbaaeaatnieaahatliltstdleanifewezi-ldn.aratawe,sae,trunea2ietthotndmeed0euenn,r0ttMmeogtihh7nicur,oeeneaoocgrd2npiswrfhn0iterpttsttroc1arelharais1sr(peetetdrL;esieadadeniCrsmn-aafieaaoooebnmdumfadrodeftranssttuaitghlsrrmatibsekefarilecerer.gdno,otsoienewsfp2nskp-iefafie0io(rhtfnae0oLcfeonanf7asroshltdtn).cot,aa.dtkbhisnvl2nFayhyeeed0mcintan1woaabrtaaa0amfdteenfgl,)tveeelee.gp1ynnac,Fi9lmntsoeoi8todctsnoba3reebpeyro;slliteaoaetndhLerghyafrsmieeeeffvtc,fsaldneMheepnatduraorrnceafteqiweidnudrenu,piiitgsetcauiihenrnnzl(flmeeri,tdcctrnsua1rrrenaposeete9noihaamlL8voelnssiuee4naeegosali)nddgyye-sf. nti o to drought in holm oak forests (Bussotti et al., 2003; Misson C ble3| nifers eintainl.,co2m01p0l)e.tDelreoaufgnhuttarliseontcaturasnesslfooclaiatigoentoanfadllienacrrleiearseadndnurtersiuelntst Ta Co concentrationinlitter(Martínez-Alonsoetal.,2007). www.frontiersin.org October2013|Volume4|Article409|7 Carniceretal. Treegrowthandtraitsyndromes INTRA-SPECIFICCOMPETITION,INTER-SPECIFICCOMPETITIONAND different ecophysiological responses in Mediterranean conifers FORESTSUCCESSION(HYPOTHESIS1.3) andangiospermtrees(Martínez-Ferrietal.,2000;Zweifeletal., Empiricalstudiesrevealthatintra-specificcompetitionactsasa 2007; Eilmann et al., 2009). For instance, while drought often major determinant of growth patterns in Mediterranean forests results in early stomatal closure in Mediterranean conifers in both conifer and angiosperm trees (Gómez-Aparicio et al., (Martínez-Ferri et al., 2000; Klein et al., 2011; Poyatos et al., 2011). Forest densification due to land abandonment and the 2013), angiosperm trees are able to maintain substantial tran- advanceofsuccessionisoccurringoverextensiveareas,increas- spiration levels during summer drought events (Quero et al., ingcompetition,reducingtreegrowth,andincreasingmortality 2011). (Gómez-Aparicioetal.,2011;Vilà-Cabreraetal.,2011;Colletal., Drought largely determines cambium growth in 2013). Coll et al. (2013) reported much higher negative effects Mediterraneanforests,producingplasticandseasonallyvariable offoreststandbasalareaonconifergrowththaninangiosperm patterns, ranging from one single annual peak to markedly treesinbothdryandwetextremesofalarge-scalerainfallgradi- bimodal trends (Maseyk et al., 2008; Camarero et al., 2010; de ent,andthesetrendswereparalleledbyhighereffectsofbasalarea Luis et al., 2011). However, large-scale studies in the Iberian onsmall-treemortalityobservedinconifers.Theseresultscoin- peninsula reveal that competition effects on growth are often cidewithstudiesrevealingoakslesssensitivetocompetitionthan strongerthandroughteffects(Gómez-Aparicioetal.,2011;Coll pinesinthisarea(Sánchez-Gómezetal.,2008;Gómez-Aparicio et al., 2013). Nevertheless, strong interactions between compe- etal.,2011). tition and drought effects have been reported, and significantly Inter-specific competition also plays an important role in increase at the edge of climatic gradients (Linares et al., 2010; determining growth responses in Mediterranean conifer and Vayreda et al., 2012; Coll et al., 2013; Ruiz-Benito et al., 2013). angiosperm trees. Specifically, large-scale surveys suggest that Finally,thereisalsosomeevidenceofindividualpredispositions small-sized conifers are more sensitive to growth suppression to winter-drought induced tree dieback in P. sylvestris (Voltas bylatesuccessionalspecies(Gómez-Aparicioetal.,2011;Zavala et al., 2013), local adaptation for water use efficiency in P. etal.,2011;Colletal.,2013).Angiospermtreesaresignificantly halepensis (Voltas et al., 2008), and correlations of temperature expanding their distributional ranges, increasing recruitment and genetic variability at candidate loci for drought tolerance across extensive areas (Coll et al., 2013; Vayreda et al., 2013). in P. halepensis and P. pinaster (Grivet et al., 2011), suggesting Morover, during the last decades the expansion of the domi- important interactions between individual adaptive traits and nant angiosperm tree Quercus ilex hasnegatively influenced the droughtimpacts. recruitment success of five Pinus species on a large scale in this area(Carniceretal.,2013a). WINTERFREEZING(HYPOTHESIS1.6) Angiosperm trees are more vulnerable to freeze-thaw embolism SIZE,AGE,ANDALLOMETRY(HYPOTHESIS1.4) and this may contribute to explain the dominance of conifer Mediterranean conifers differ from angiosperm trees in their trees at high altitudes (Cavender-Bares et al., 2005; Brodribb allometrical relationships between tree size (diameter at breast et al., 2012) and could in turn result in qualitatively different height) and crown growth variables (Poorter et al., 2012). The growthresponsesinconifersandangiospermtrees.Forexample, peak of crown growth is generally reached at lower sizes in Gómez-Aparicio et al. (2011) reported that Atlantic deciduous conifers,whichalsoshowamuchsteeperdecreasewithsizethan broadleavedtreesintheIberianpeninsulahadlowercompetitive broadleaved species (Poorter et al., 2012). These different allo- response ability at lower temperatures, in contrast to mountain metric relationships are in turn associated with several other conifer species. In this study, tree growth of Atlantic deciduous traits (maximal height, crown size, shade tolerance, wood den- broadleaved trees was negatively affected by low temperatures sity,apicaldominance)andalsointeractwithlocalhabitataridity (Gómez-Aparicio et al., 2011). In line with this, several studies (Poorter et al., 2012). Similarly, Gómez-Aparicio et al. (2011) havedemonstratedthatlowwintertemperaturesdirectlyinhibit reported that in Iberian forests competitive effects for conifers celldivisionandtreegrowthincoldlocalities(Körner,1998,2013; scaleapproximatelyquadraticallywithdiameteratbreastheight Fajardoetal.,2012). (dbh2) and linearly for broadleaved trees. To our knowledge, it remains untested whether these different allometric relation- INTERACTIONSBETWEENMULTIPLEFACTORS(HYPOTHESIS1.7) shipsmightberelatedtothecontrastingtreegrowthresponsesto Tree growth patterns in the Iberian peninsula have several con- temperaturereportedinMediterraneanconifersandangiosperm tributingdriversthatinteractalonggeographicalgradients(Coll trees(Gómez-Aparicioetal.,2011). etal.,2013).Forinstance,Gómez-Aparicioetal.(2011)studied treegrowthresponsesin15treespeciesinSpainandreportedthat DROUGHTANDTEMPERATURE(HYPOTHESIS1.5) sensitivitytocompetitionincreasedwithdecreasingprecipitation Large-scalestudiesdemonstratethatdroughtandincreasedtem- inallspecies.Notably,thebestpredictivemodelsfortreegrowth peratures significantly limit tree growth in xeric regions of the in Gómez-Aparicio et al. (2011) included interactions between Mediterraneanbasin(Andreuetal.,2007;Martínez-Alonsoetal., size, competitive effects and climate variables. Similarly, Coll 2007;Sarrisetal.,2007;BoginoandBravo,2008;Martínez-Vilalta etal.(2013)modeledgrowthresponsesintheIberianpeninsula et al., 2008; Gómez-Aparicio et al., 2011; Vilà-Cabrera et al., and reported a significant increase in the strength of interac- 2011; Candel-Pérez et al., 2012; Sánchez-Salguero et al., 2012; tions between tree size, tree height and climate variables at the Vayreda et al., 2012;Coll et al., 2013) and produce qualitatively drier and wetter edges of rainfall gradients. These interactions FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|8 Carniceretal. Treegrowthandtraitsyndromes could increase with ongoing climate change, and several stud- assertthatmultiplecommongardenexperimentslocatedinlat- iessuggestthatwarmingcouldincreasecompetitionforwaterin itudinal and altitudinal gradients are particularly relevant to Mediterraneanforests(Linaresetal.,2010). studyphenologyandgrowthresponsestotemperature(Reichand Oleksyn,2008;Vitasseetal.,2010).Furthermore,theinclusionof LOCALADAPTATION,INDIVIDUAL-ANDPROVENANCEVARIATION differentprovenancesinthesereciprocalexperimentsallowsthe (HYPOTHESIS1.8) quantificationofenvironmentallyinducedphenotypicplasticity, Local selection processes may affect the adaptive traits deter- genotypicvarianceandtheirinteraction(e.g.,Vitasseetal.,2013). mining the different growth responses to temperature observed Complementarily, drought effects on growth could be studied in Iberian conifers and angiosperm trees. For example, prove- bymanipulativeexperimentscombinedwithreciprocalcommon nancestudiesinbothconiferandangiospermtreeshaverevealed garden designs (reviewed in Klein et al., 2011; Wu et al., 2011). genetic differences in growth rates and other growth-related Similarly,theeffectsofintra-andinter-specificcompetitioncould traits (age at reproduction, timing of bud burst and bud set, be studied manipulating tree densities and composition in dif- leaftraits,floweringphenology),suggestingthatpopulationsare ferentexperimentalgroups.Finally,toassesstreesizeeffectsand oftenadaptedtotheirlocalconditionsoftemperatureandwater allometric relationships, the study of saplings of different ages availability (Rehfeldt, 1978, 1982, 1988; Borghetti et al., 1993; would be required. Alternatively, long-term experiments could Climent et al., 2008; Mátyás et al., 2009; Rose et al., 2009; provide also relevant information to quantify allometric rela- Ramírez-Valienteetal.,2010,2011;Santosetal.,2010;Chmura tionships.Finally,inalltheseexperimentaldesigns,theperiodic et al., 2011; Robson et al., 2012; Alberto et al., 2013). In prove- measurementofecophysiologicaltraitsshouldbeimplementedto nance trial studies, populations from cold environments often assesstheirseasonalvariationandtheirputativeroleindetermin- cease growth earlier, while populations from warm localities inggrowthresponses. generally grow faster (Alberto et al., 2013). Notably, local selec- tion for increased growth rates may induce lower resistance COMPLEXANDMULTIPLEEFFECTSOFTEMPERATUREAND to drought and frost. For instance, in conifers fast-growing DROUGHTONTREEPHYSIOLOGY provenances often exhibit lower cold hardiness and/or lower Climate produces multiple and complex effects on tree physi- resistance to drought stress (Hannerz et al., 1999; Cregg and ology. As highlighted in Table1, we expect that multiple phys- Zhang, 2001; Chuine et al., 2006). These differences have been iological processes can simultaneously react to the changes in attributed to trade-offs between resistance to frost and drought environmentaltemperaturesandinfluencegrowthresponses.For and growth (Chuine et al., 2006 and see Martin St Paul et al., example,temperatureanddroughtdirectlyaffectseveralecophys- 2012). iological processes such as carbon and nutrient uptake, carbon PHENOTYPICPLASTICITY(HYPOTHESIS1.9) allocationbetweentissues,photosynthesis,respiration,processes Mediterraneantreesshowstrongplasticresponsesintreegrowth of embolism prevention and repair, phenological cycles, cam- patterns, which are associated with seasonal climate variabil- biumreactivation,celldivisionandexpansionorcarbontransfer ity (e.g., Camarero et al., 2010; de Luis et al., 2011). Critically, rates (Körner, 1998; Bréda et al., 2006; Rennenberg et al., 2006; phenologyandgrowthplasticityresponsesdifferbetweenprove- Sanz-Pérezetal.,2009;Camareroetal.,2010;Epronetal.,2012; nances and species and may determine observed demographic Michelotetal.,2012).Moreover,thesedirectclimaticeffectson and evolutionary responses to global warming (Nicotra et al., tree physiology can in turn produce secondary indirect effects, 2010). For example, low elevation provenances often exhibit forexamplethepromotionofsignalingandregulatoryresponses, greaterphenologicalplasticitytotemperaturethanhighelevation acclimation and phenotypically plastic responses or changes in provenances(Vitasseetal.,2013)andthiscouldinturninfluence geneexpression(reviewedinPeñuelasetal.,2013b).Table4pro- observed tree growth responses. To our knowledge, it remains vides a brief, non-exhaustive description of the diverse effects untested whether Mediterranean conifers exhibit higher growth of temperature and drought on tree physiology. It is impor- plasticity than angiosperm trees, although it has been reported tant to bear in mind that all these ecophysiological processes thatIberianconifersshowhighergrowthratesthanangiosperm often have different sensitivities and thresholds to temperature trees in absence of competition (Gómez-Aparicio et al., 2011; and water deficit. For example, tree growth and cambium acti- Poorteretal.,2012). vation are more sensitive to low temperatures than is photo- synthesis (Körner, 1998; Fajardo et al., 2012). In addition, as EXPERIMENTALASSESSMENTOFTHERELATIVECONTRIBUTIONOF shown in Table4, responses to climate are often species or tis- THEHYPOTHESES sue specific or depend on developmental stage and seasonal The available empirical evidence suggest that several factors phase and can be influenced by regulatory feedbacks that can interact and seem to determine contrasting growth responses oftenimplymulti-tissuecoordinatedresponses.Despitetheover- to temperature in Mediterranean conifer and angiosperm trees. whelmingcomplexityanddiversityoftheeffectsoftemperature Therefore, improved experimental approaches are required to and drought reported in Table4, several studies have demon- quantitatively assess the relative importance of these factors. strated consistent differences between major plant groups, such While several experimental and observational approaches could asconifersandangiosperms,inclimate-inducedresponses(e.g., be applied, we suggest that reciprocal provenance trial experi- Way and Oren, 2010; Gómez-Aparicio et al., 2011; Coll et al., mentsmaybeespeciallysuitedforthispurpose.Previousstudies 2013). www.frontiersin.org October2013|Volume4|Article409|9 Carniceretal. Treegrowthandtraitsyndromes Table4|Anon-exhaustiveandsyntheticreviewofthedifferenteffectsoftemperature(A)anddrought(B)ondifferenttreephysiological processes. References (A)EFFECTSOFTEMPERATUREONTREEPHYSIOLOGY Photosynthesis.Temperatureshigher/lowerthantheoptimumdecreasephotosynthesisandaffectmultiple Rennenbergetal.,2006 biochemicalprocesses.Forexample,hightemperaturescanreducetheefficiencyofelectrontransportinthe Morinetal.,2007 thylakoidmembraneofchloroplasts,whichinturndown-regulatethecontentofribulose-1,5-bisphosphateand KattgeandKnorr,2007 deactivateRubisco.HightemperaturesalsoinhibitRubiscoactivase,duetotheirlowthermaloptimum.The Chavesetal.,2012 solubilityofthetwosubstratesofRubisco,CO2,andO2,isdifferentiallyaffectedbytemperature,stimulating Flexasetal.,2012;Sharkeyand photorespirationandinhibitingphotosynthesisathightemperatures. Bernacchi,2012 PhotosystemIIisalsosensitivetohightemperatures,whichstimulatemechanismstoavoidphoto-oxidationand membranedenaturation,suchasisopreneproductionandthexanthophyllcycle. Lowtemperaturescauseavarietyofphysiologicalandacclimativeresponses,includingmodificationsinthe structureofthethylakoidmembraneinchloroplasts,alleviationofphotoinhibitionthroughupregulationofcarbon metabolismandincreasedsynthesisofstoragecarbohydrates,increasedproductionofantioxidants,preventionof intracellularfreezingbyincreasedsolublecarbohydrates(mobilizationofstarchtosucrose)andchangesingene expressionandsignalingpathways. Thegrowthenvironmentofplantsdeterminesthetemperatureoptimumofphotosynthesis.Inwarmer environments,plantsacclimatetoincreasethethermaloptimumofthemaximumcarboxylationvelocity(Vcmax) andthemaximumpotentialrateofelectrontransport(Jmax). Abovethethermaloptimumforphotosynthesis,theemissionofbiogenicvolatileorganiccompoundssuchas LlusiàandPeñuelas,2000; isopreneandmonoterpenesprogressivelyincreases. Rennenbergetal.,2006 Leaf respirationisstronglyaffectedbytemperature,increasingathightemperatures(e.g.,above35–40◦C)and Rennenbergetal.,2006;Smith peakingathighertemperaturesthanphotosynthesis. andDukes,2013 Hightemperaturesoftenincreasenetprimaryproductionandplantgrowth.Incold-adaptedtrees,photosynthesis Körner,1998;WayandOren, islesssensitivetolowtemperaturesthanistreegrowth(celldivisionandgrowth,cambiumactivation).Inalpine 2010;Wuetal.,2011;Fajardo treelines,newtissueformationisnearlyabsentattemperaturesaround5◦C,butconsiderableratesof etal.,2012;Lenzetal.,2012 photosynthesisaremaintainedbetween0and10◦C. Highertemperaturesinfluencefoliarphenology,promotingearlierbudburstanddelayingleaffall. PeñuelasandFilella,2001; Peñuelasetal.,2002;Vitasse etal.,2009a,b,2013 Intheabsenceofdrought,temperatureoftenincreasesnutrient-uptakecapacity(NH+,NO−,PO−,K+). Rennenbergetal.,2006 4 3 43 Temperaturecanalsoincreasebothxylemloadingofaminocompoundsandnitrogenallocationinaboveground tissues. Freezingcausescelldehydration,formationoficeinintracellularspacesandembolism.Budsaremoreresistant Morinetal.,2007;Augspurger, thanleavestofrost. 2009 Temperature,inabsenceofdrought,positivelyaffectsratesofsoilrespirationandlitterdecomposition. Wuetal.,2011 Organs,individuals,lifestagesandspeciesconsistentlydifferintheirphenologicalresponsestotemperatureand NiinemetsandValladares, sensitivitytodamagefromfrostanddrought. 2006;Morinetal.,2007; Augspurger,2009 (B)EFFECTSOFDROUGHTONTREEPHYSIOLOGY Photosynthesis.Droughtlimitsphotosynthesisbystomatalclosure,diffusionlimitationsinthemesophylland Chavesetal.,2012 metabolicimpairment.Itcanalsolimitphotosynthesisviasecondaryeffects,suchasreducedhydraulic SharkeyandBernacchi,2012 conductanceandoxidativestress. Droughtactivatesdiversesignalingpathwaysassociatedwithstomatalclosure.Forexample,itmodifiesabscisic acid(ABA)signalinginleaves,shootsandroots;increasesxylem-sappHandchangesaquaporinconcentrations, leafhydraulicconductancesignalsandelectricsignals. Droughtreducesosmoticpotentialinthesoilandpredawnleafwaterpotentialsandlimitswateruptake.To Rennenbergetal.,2006. maintainwateruptake,plantsincreasetheproductionofosmolites,down-regulateelectronfluxandincreasethe activityofantioxidantenzymes.Droughtcanalsoincreasethedegradationoffoliarproteinsandtheconcentration ofsolubleaminoacidsandNSCsintheleaves,whichmayactinturnasosmoprotectantstostabilizeproteinsand membranes.Droughtalsopromotesanincreaseintheconcentrationsofsolubleantioxidants. (Continued) FrontiersinPlantScience|FunctionalPlantEcology October2013|Volume4|Article409|10

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Keywords: conifers, angiosperms, functional traits, mediterranean ecosystems, drought, temperature, carbon metabolism, growth . processes and phenotypic plasticity also largely influence tree growth responses to .. uptake and photosynthesis over extended periods (Martínez-Ferri et al., 2000
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