Functional responses of four Sahelian tree species to resource availability

2018·0.92 MB·English

by  Joseph S. Diémé

Flora xxx (xxxx) xxx–xxx
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Flora
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☆
Functional responses of four Sahelian tree species to resource availability
Joseph S. Diéméa,b,⁎, Cristina Armasa, Graciela M. Ruschc, Francisco I. Pugnairea,⁎
aEstaciónExperimentaldeZonasÁridas,ConsejoSuperiordeInvestigacionesCientíficas,Ctra.deSacramentos/n,04120,LaCañada,Almería,Spain
bInstitutSénégalaisdeRecherchesAgricoles,Dakar,Senegal
cNorwegianInstituteforNatureResearch,Høyskoleringen9,7034,Trondheim,Norway
ARTICLE INFO ABSTRACT
EditedbyHermannHeilmeier Plantsexperienceafluctuatingenvironmentintimeandspacethataffectsresourcesupply.Ashumanimpactsonthe
Keywords: environmentdirectlyandindirectlyalterresourceavailability,itisimportanttoaddressplantresponsestochanging
Plantfunctionaltraits resourcestobeabletoanticipateimpactsofthesechangesonplantcommunities.Weanalyzedplanttraitstoassess
Phenotypicplasticity responsestoresourcelimitationinfourSaheliantreespeciesofwideecologicalandsocio-economicimportance.We
Relativegrowthrate usedspeciesalreadyadaptedtoharshconditions(hightemperatures,lowrainfall)toanticipatehowclimatechange
Root-to-shootratio couldaffecttheirgrowthpatternsand,indirectly,theirspatialdistributionandtheservicestheyprovide.Seedlings
Specificleafarea grewundertwolevelsofwaterandnutrientadditionsinafactorialdesign.Ourresultsshoweddifferencesamong
Resource-Usestrategies
species,wateringregimes,andnutrientsupplyinthreekeyfunctionaltraitsrelatedtotheplant’sresource-usestrategy,
Waterandnutrientavailability
relativegrowthrate(RGR),root-to-shootratio(R/S),andspecificleafarea(SLA).Onaverage,RGRwasresponsiveto
theamountofwaterandnutrients,withspecieswithhighRGRshowingthelargestresponsetoresourcesupply.RGRin
thespecieswithaconservativeresource-usestrategy(evergreenleaves,lowestRGR)remainedunchangedwithdif-
ferentlevelsofwaterandnutrients.Overall,largeRGRwassupportedbylargeSLA.Allspeciesallocatedmorebiomass
torootsthantoshoots,particularlyunderlowresourcesupply,reflectingadaptivestrategiestokeepRGRleveledto
resourcesupply.Notallspeciesshowedsimilarplasticityintheirfunctionaltraitsresponses;however,Acaciatortilisand
Faidherbiaalbidashowedthegreatestplasticity,whichmayexplaintheirlargegeographicaldistributionrangeinAfrica.
OurdatasuggestthatthedifferentSahelianspecieswillresponddifferentlytofutureenvironmentalchanges,likely
affectingtheirgeographicaldistribution,thestructureofplantcommunities,andtheservicestheyprovide.
1. Introduction responses to resource availability is important to better understand
possibleoutcomesofthesechanges(Cuni-Sanchezetal.,2011;Garnier
Climatealterationsoverthelastdecadesmaybealreadyresponsible etal.,2018;Langetal.,2018).
forchangesintreespeciesranges(Songetal.,2016),andwarmingand Seedlingsarethemostvulnerablestageoftheplantlifecycle,being
alteredprecipitationpatternsmayprofoundlyaltersavannasworldwide particularly sensitive to water limitation during drought (Chaturvedi
(Volderetal.,2013).Futureclimateprojectionspredictseveredroughts et al., 2013; Khurana and Singh, 2001; Montgomery and Chazdon,
intheAfricansavanna(Bokoetal.,2007;Brooks,2004),andtheSahel 2002;PadillaandPugnaire,2007;YavittandWright,2008).Seedling
isexpectedtoexperienceacombinationofincreasedtemperaturesand survivalisstronglydependentontheseverityofdrought,aswaterstress
modifiedprecipitationregimes,whichwillintensifyseasonaldroughts is the main factor affecting seedling mortality in dry environments
(MacCracken et al., 2003; Pope et al., 2000; Wetherald and Manabe, (Comita and Engelbrecht, 2009; Engelbrecht et al., 2005; Pugnaire
1995) potentially altering the function, growth, and distribution of et al., 2006; Slot and Poorter, 2007). Watering experiments in tree
plantfunctionalgroups(Hungateetal.,2002;Knappetal.,2008a,b). species of tropical moist forests also reveal that water availability
Sincedroughttoleranceabilityisoneofthestrongestpredictorsoftree controlsspeciesseasonalgrowthpatternsandthatdroughtstresslimits
speciesdistributioninseasonally-drytropicalenvironments(Box,1995; seedlinggrowthrates(Engelbrechtetal.,2006;EngelbrechtandKursar,
Condit et al., 2013), understanding differences in plant adaptive 2003; Paine et al., 2008; Yavitt and Wright, 2008). Hence, assessing
☆Thisarticleispartofaspecialissueentitled:“Functionaltraitsexplainingplantresponsestopastandfutureclimatechanges”publishedatthejournalFlora254C,
2019.
⁎Correspondingauthorsat:EstaciónExperimentaldeZonasÁridas,ConsejoSuperiordeInvestigacionesCientíficas(EEZA-CSIC),Ctra.deSacramentos/n,04120,
LaCañada,Almería,Spain.
E-mailaddress:[email protected](J.S.Diémé).
https://doi.org/10.1016/j.flora.2018.10.009
Received11April2018;Receivedinrevisedform19October2018;Accepted28October2018
0367-2530/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Joseph S. Diémé, et al., Flora, https://doi.org/10.1016/j.flora.2018.10.009
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
seedlings responses to water availability, and how they modify their Senegal NationalProjectof ForestrySeeds, Dakar)and subjectedtoa
traits,willhelptounderstandthelong-termresponseofforestspeciesto pre-germinationtreatmentusingconcentratedsulfuricacidfor10min
environmentalchange(Capersetal.,2005;Jumpetal.,2007;Pedersen, (T.indica),60min(A.tortilisandF.albida)and12h(A.digitata).Seeds
1998;Peñuelasetal.,2007). of each species were harvested in the same area so that their mother
Further,understandingtheroleofplasticityinresponsetoresource plants were subjected to the same environmental (soil and climatic)
availability will bring insights into plant growth and persistence of conditions.Twoseedsperspeciesweresowninasandandvermiculite
speciesintheircurrentenvironmentsundernovelconditions(Nicotra mixture (1:1 in volume) in 50cm long, 10cm wide PVC tubes and
etal.,2010).Whiledroughtisacknowledgedasacrucialclimaticfactor thinnedtooneaftergermination.Plantswerewateredeverymorning
that would likely undermine tree survival in the future (Allen and and received fertilizer (commercial NPK fertilizer [Mg-S]; 19-19-19
Breshears, 1998; Hanson and Weltzin, 2000), progressive drought-in- [2–8]) once a month between November 2012 and March 2013, just
ducedstressisanon-linearprocesslargelydependentontheinteraction beforetheexperimentstarted.InMarch2013,treatmentsweresetina
betweentemperatureandwateravailability,andtoplants’adaptability factorialdesignwithnutrient(lowandhighnutrientsupply)andwater
tohighertemperaturesintermsofmorphologyandphysiology(Adams (low and high level of watering) as factors (2×2 factorial design;
et al., 2009). The ability of plant species to cope with environmental n=6–9 plants per treatment and species). At the start of the experi-
change will depend on the capacity to adapt physiological and other ment,plantsizediffereddependingonthespecies.Itwas<5cminA.
functionalresponsestothesechanges;but,foraneffectivepredictionof albida, A. digitata, and T. indica, and<15cm in F. albida. Half the
the capacity of populations to persist in a certain environment, em- plantsperspeciesreceivedahighnutrientsolution(N+)of0.5gfer-
pirical studies that aim to assess intra-specific response variability tilizer per liter of water, and the other half received a low nutrient
under controlled environmental conditions are necessary. Therefore, solution(N-;0.05goffertilizerperliterofwater).Inaddition,halfthe
examination of trait variability in heterogeneous environments that plantswerewateredonceaweekwith100ml(lowwatersupply;W-)
reflect population-level responses to the environment can provide and the other half was watered twice a week with 100ml each time
deeperinsightsintohowspeciesmightrespondtofutureenvironmental (high water supply; W+, 200ml of water per week). So, four treat-
changes(OkeandWang,2015).Inaddition,identifyingtrade-offsthat mentswereestablishedaccordingtonutrientandwaterregime,W+N
underlie the diversity of a species’ morphology and function is im- +,W+N-,W-N+,andW-N-.Treatmentswereappliedforfourmonths
portant because trade-offs constrain demographic change rates and andpotswererandomlyredistributedinthegreenhouseonceamonth.
theirlinkagestoecosystemprocesses(Díazetal.,2016;Shipleyetal., Temperaturewithinthegreenhouseranged16–22°Cduringthecourse
2016). oftheexperiment,withnaturaldaylightlength(10.5–14hoursoflight).
Growthrateisaprominentindicatorofplantstrategiesthatdeals Atharvest,ninemonthsaftersowing,plantsweresortedintoabove-
withenvironmentalstressanddisturbance(Pérez-Harguindeguyetal., and below-ground parts, and the aboveground parts were subdivided
2013), and substantial volume of theory and data support the corre- into leaves and stem. Plant parts were dried at 70°C for 48h and
spondence between functional traits and growth rate (Hunt and weighed. Plant traits were calculated following standard protocols
Cornelissen,1997;Reichetal.,1998;Shipley,2006).However,varia- (Pérez-Harguindeguy et al., 2013). In brief, six fully expanded and
tioninindividual-levelaccesstoresourcescancausetraitcorrelations undamaged leaves per plant were scanned with a flatbed scanner to
withinspeciestodifferfrominter-specificcorrelations(vanNoordwijk determinethespecificleafarea(SLA;theratioofleafareatodrymass).
anddeJong,1986)duetophylogeneticconstraints. Totalplantbiomass(TPB)wasobtainedbyaddingthedrymassofthe
Hereweanalyzedfunctionalresponsesofseedlingstosimultaneous different plant parts. Root-to-shoot ratio (R/S) was calculated by di-
effectsofmoisturestressandnutrientvariabilityinfourSaheliantree vidingrootmassbyshootmass.Relativegrowthratewasestimatedas
species of wide ecological and socio-economic importance. Target RGR=(lnTPB2-lnTPB1)/(t2-t1),wheretistheelapsedtimeindays
species were selected as representative of functional groups of the betweensowing(t1)andharvest(t2).TocalculateTPB1,weselected10
highly diverse agroforestry ecosystems in the Sahel (Diémé et al., seeds per species, extracted and dried the embryos in an oven for at
2018).WelinkedRGRandbiomassallocationpatternswithfunctional least72hat70°C,andweighedtheirdrymasswithaprecisionbalance
traits deemed relevant to plant persistence (Kleyer et al., 2008). We (to 10−6 g). We used the mean TPB1 value per species. We also re-
addressedresponsesinrelativegrowthrate(RGR),root-to-shootratio cordedplantheight(measuredwitharulerto0.1cm).
(R/S)andspecificleafarea(SLA)ofseedlingsgrowingundertwolevels Theeffectofwater,soilnutrientadditiononplantfunctionaltraits
of water and nutrient availability in a full factorial greenhouse ex- (RGR, SLA, R/S, biomass, plant height, allocation patterns) was ana-
perimentandexploredpotentialtrade-offsamongtraits.Wehypothe- lyzedwithgenerallinearmodelsincludingafull-factorialdesign.Fixed-
sizethat1)RGRwillincreasewithresourcesupplybutthemagnitude factorswerespecies(aswewereinterestedininter-specificresponsesof
of the response will depend on resource use strategies (Grime et al., species belonging to different functional groups), nutrient addition
1997).Weexpectedthat2)fast-growingspecies,i.e.withexploitative (low, high), watering (low, high), and the interaction across factors.
strategy,willshowhighRGRunderhighwaterandnutrientsupply,but Assumptions of normal distribution of residuals, homogeneity of var-
RGRwilldeclinestronglywithlowresourcesupplylevels;incontrast, iances were tested, met. Differences in means across treatment levels
3)plantswithconservativeresource-usestrategywillhavealessplastic wereanalyzedwithFisher’sleastsignificancedifference(LSD)post-hoc
responsetochangesinwaterandnutrientsupply,i.e.,stableRGRre- test. Statistical analyses were conducted in R (R Development Core
gardless resource levels, with more biomass allocated to roots at low Team, 2013) using the interface implemented in InfoStat-Statistical
levelsofwaterandnutrientsupply(Meieretal.,2018).And4)SLA,a Software(Di-Rienzoetal.,2013).Reportedvaluesthroughoutthetext,
traitstronglyassociatedtotheplantresource-usestrategy,willrespond figuresaremeans±1,standarderror.
inparalleltoRGR.
3. Results
2. Methods
ThereweredifferencesinRGR,R/SandSLAamongspeciesinre-
A greenhouse experiment was established in 2012–2013at the sponse to water and nutrient addition regimes (Table 1). There were
UniversityofAlmería(36°50′N,2°27′W),Spain,usingfourSahelian significantdifferencesinRGRamongallspecies;RGRwasgreatestin
tree species, two dry-season deciduous species, Acacia tortilis (Savi) Acacia tortilis and lowest in Tamarindus indica (Fig. 1). All species in-
Brenan and Adansonia digitata L., one wet-season deciduous species creased RGR with water supply (significant species × water interac-
(Faidherbiaalbida(Del.)Chev.),andoneevergreenspecies,Tamarindus tion, Table 1) except T. indica, whose RGR remained unchanged irre-
indicaL.SeedsofthesespecieswereobtainedinSenegal(PRONASEF, spectiveofwaterandnutrientaddition.Growthoftheother3species
2
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
Table1
Resultsoflinearmodelsanalysingdifferencesinrelativegrowthrate(RGR),roottoshootratio(R/S)andspecificleafarea(SLA)offourSaheliantreespeciesgrowing
underdifferentsoilwaterandnutrientregimes(n=6–9).Species,leveloffertilizerorwatertreatmentswereincludedinthemodelasfixedfactorswithafull-
factorialdesign.Significantpvaluesarehighlightedinbold.
d.f. RGR R/S SLA
F-value p-value F-value p-value F-value p-value
(Intercept) 1 6832.59 <0.0001 1001.79 <0.0001 503.3 <0.0001
Species(S) 3 463.65 <0.0001 53.24 <0.0001 4.01 0.0094
Nutrient(N) 1 12.37 0.0006 7.39 0.0076 4.16 0.0437
Water(W) 1 12.34 0.0007 36.42 <0.0001 6.38 0.0129
S×N 3 0.47 0.7020 2.81 0.0428 1.78 0.1557
S×W 3 2.87 0.0398 8.58 <0.0001 0.71 0.5472
N×W 1 0.31 0.5804 8.58 <0.0001 0.71 0.5472
S×N×W 3 0.38 0.7709 1.2 0.3136 0.64 0.5934
Fig. 1.Relative growth rate (RGR) of Acacia tortilis, Adansonia digitata,
Fig.3.Rootshootratio(R/S)ofAcaciatortilis,Adansoniadigitata,Faidherbia
Faidherbia albida and Tamarindus indica individuals growing at two levels of
albida and Tamarindus indica individuals growing at two levels of nutrient
nutrientavailability(high,N+andlow,N-)andtwowaterregimes(W+and
availability(high,N+andlow,N-)andtwowaterregimes(W+andW-).Data
W-).Dataaremean±1SE(n=6–9).Differentlettersshowsignificantdiffer-
aremean±1SE(n=6–9).Differentlettersshowsignificantdifferences(post-
encesamongspeciesandtreatments(post-hoccomparisonsamongspecies×
hoccomparisonsamongspecies×water×nutrientlevels).
water×nutrientlevels).
interactionSpecies×N;Species×WorSpecies×N×W(Table1).
reactedsimilarlytobothwaterandnutrientavailability,andRGRinthe
Allspecieshad, onaverage,R/Svaluesabove1(Fig.3),meaning
two extreme treatments (W+N+ vs. W-N-) were always different
they allocated more biomass to roots than to aboveground parts
(higher with higher resource supply) regardless of species. RGR re-
(Fig.4).ThereweresignificantdifferencesinR/Samongspecies,and
sponse at intermediate resource supply (W+N- or W-N+) was in be-
R/Sallocationrespondedalsotothenutrientandwaterlevels(Table1).
tweenaboveextremetreatments(Fig.1).
R/Sgenerallyincreasedasresourcesbecamelimiting(Fig.3),andthe
SLA varied among species as well (Table 1), being greatest in
significant interaction N × W indicated that allocation to roots or
Adansoniadigitata(Fig.2).SLArespondedsimilarlytotheadditionof
shootsrespondednon-additivelytonutrientandwaterlevels(i.e.,sig-
nutrient and water in all species; i.e., there were no significant
nificantlylowerandhigherresponsesthanaverageinW-N-andW+N
+treatments).Atthesametime,R/Sresponsestonutrientandwater
levelsdependedonthespecies(significantinteractionS×NandS×
W;Table1).ThehighestdifferencesinR/Sresponsetothetreatments
was observed in F. albida, whereas R/S in T. indicus remained un-
changedregardlessofthetreatment(Fig.3).Overall,A.tortilisandF.
albidawerethemostresponsivespeciestodifferencesinwatersupply
(i.e.,differencesinR/SweregreatestbetweenW-andW+treatments).
However, R/S values are size-dependent and therefore change with
plantsize.Tocheckwhetheritwasthecasewecomparedtheslopesof
ln root vs ln shoot among treatments within a species (Fig. A1). We
foundthattherewastrueplasticity(sensue.g.,Weiner,2004)onlyin
Adansoniadigitata,butFaidherbiaalbidashowedplasticitywithrespect
towateringtreatments.
Nutrient levels affected different morphological traits (Table 2).
Plantsinthehighnutrienttreatmentweretallerandhadhighershoot
andleafmassthanplantsinthelownutrienttreatmentexceptT.indica,
Fig.2.Specificleafarea(SLA)ofAcaciatortilis,Adansoniadigitata,Faidherbia
buttherewasnoeffectofnutrientregimeonrootmassofthedifferent
albida and Tamarindus indica individuals growing at two levels of nutrient
species(Table2).Hence,plantsizeingeneralwasmuchlargerinthe
availability(high,N+andlow,N-)andtwowaterregimes(W+andW-).Data
aremean±1SE(n=6–9).Differentlettersshowsignificantdifferences(post- high-nutrienttreatment(Table2)exceptforT.indica.Wateralsohada
hoccomparisonsamongspecies×water×nutrientlevels). significanteffectonplantsize.Lowwateravailabilitydecreasedoverall
3
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
Fig.4.Meanrelativebiomassallocation(%)toroots,shootsandleavesofAcaciatortilis,Adansoniadigitata,FaidherbiaalbidaandTamarindusindicaplantsgrownat
twolevelsofnutrientavailability(high:N+,andlow:N-)andtwowaterregimes(W+andW-).Differentlettersshowsignificantdifferencesinbiomassallocation
acrossplantorgansandtreatmentsforeachspeciesseparately(post-hoccomparisonsamongplantorgans×water×nutrientlevels).
plantheightandmass(Table3).Totalplantmasswasmuchhigherin resources were high compared to low, in agreement with published
the high-water regime (Table 3), except in A. digitata and T. indica. reports(e.g.,Poorteretal.,1989).Ingeneral,speciesmaintainedaRGR
Overall,T.indicawastheonlyspeciesthatdidnotshowasignificant rankingacross resourceavailability levels, i.e.,A. tortilis,F. albida, A.
response regarding biomass or allocation patterns in response to nu- digitataandT.indicashowedhighesttolowest RGRsregardless ofre-
trientorwateraddition(Fig.4). sourcesupply.AcaciatortilismaintainedhighRGRunderalltreatments
exceptwiththelowestlevelsofnutrientandwatersupply,whileRGR
in T. indica remained unchanged notwithstanding nutrient and water
4. Discussion
levels.Theseresultssupportourpredictionofalargerplasticityinre-
sponse to varying levels of water and nutrient supply in species with
ThefourSaheliantreespeciesinourstudydifferedsignificantlyin
high RGR (resource exploitative strategy) and low plastic capacity in
RGR,andasexpected,plantsizeandgrowthraterespondedpositively
specieswithlowRGR(conservativeresourcestrategy).Ourresultsare
and consistently to both nutrient and water levels (Cornelissen et al.,
also indicative that maintaining anoptimal RGR (i.e., adjusted to en-
1998),althoughtheresponsetowaterlevelswasspecies-specific(sig-
vironmental conditions) seems to be an important plant strategy
nificant interaction S× W). RGRwas significantly higher when both
Table2
Responsesofourfourtargettreespeciestonutrientaddition.Dataaremean±1SE(n=6–9);differentlettersinarowshowsignificantdifferencesbetweenspecies
(p<0.05).
Acaciatortilis Adansoniadigitata Faidherbiaalbida Tamarindusindica
High Low High Low High Low High Low
Shootmass(g) 1.61±0.22a 0.73±0.06b 1.34±0.23a 0.55±0.05c 1.22±0.12a 0.66±0.04bc 0.19±0.02d 0.18±0.02d
Rootmass(g) 2.17±0.3b 1.60±0.19b 2.12±0.42b 1.46±0.21b 4.58±0.29a 4.18±0.27a 0.71±0.09c 0.76±0.09c
Leafmass(g) 1.27±0.14a 0.56±0.05bc 0.97±0.25ab 0.44±0.06c 1.19±0.13a 0.47±0.04c 0.22±0.03d 0.26±0.03d
Totalplantmass(g) 5.05±0.56b 2.86±0.26cd 4.44±0.76bc 2.44±0.32d 6.99±0.47a 5.30±0.31b 1.12±0.13e 1.20±0.13e
Plantheight(cm) 44.67±3.16a 29.97±1.70c 24.45±2.85c 14.62±1.43d 46.96±2.33a 35.55±1.57b 10.22±0.78e 9.23±0.74e
4
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
Table3
Responsesofourfourtargettreespeciestowateraddition.Dataaremean±1SE(n=6–9);differentlettersinarowshowsignificantdifferencesbetweenspecies
(p<0.05).
Acaciatortilis Adansoniadigitata Faidherbiaalbida Tamarindusindica
High Low High Low High Low High Low
Shootmass(g/plant) 1.44±0.21a 0.89±0.09b 1.15±0.22ab 0.74±0.09bc 1.19±0.12a 0.69±0.05c 0.21±0.02d 0.16±0.02d
Rootmass(g/plant) 2.18±0.30b 1.58±0.20b 1.79±0.30b 1.79±0.36b 4.73±0.30a 4.03±0.26a 0.82±0.10c 0.65±0.09c
Leafmass(g/plant) 1.07±0.12a 0.76±0.08bc 0.92±0.25ab 0.49±0.07d 0.98±0.12ab 0.68±0.06c 0.26±0.04d 0.22±0.03d
Totalplantmass(g/plant) 4.70±0.52bc 3.21±0.32d 3.86±0.67cd 3.02±0.47d 6.90±0.47a 5.40±0.31b 1.29±0.14e 1.04±0.12e
Plantheight(cm) 38.14±2.4b 36.49±2.67b 22.86±2.73c 16.21±1.66d 45.33±2.26a 37.17±1.68b 10.16±0.8e 9.29±0.71e
irrespectiveofresourcesupply,sinceahighRGRiscriticalforplantsto maybeconsequenceofdifferencesinplantsize(Husákováetal.,2018).
growandoccupyspace,bothbelow-andabove-ground,togetalarger Inourdataset,however,therewastrueplasticity(sensuWeiner,2004)
share of resources (Grime, 1998; Ruiz-Robleto and Villar, 2005). All in Adansonia digitata, while Faidherbia albida showed plasticity with
species except T. indica are deciduous species and show RGR values respect to watering treatments. Therefore, we can say that, for these
between 0.005 and 0.023 g g−1 d−1, which is a rather high range species, the differential allocation to roots can be interpreted as a
compared to tree species from other dry environments (Atta et al., strategy response to water limitation (Ledo et al., 2018). R/S was
2012;HoffmannandFranco,2003;Lamersetal.,2006).Overall,spe- highestinF.albida,reachingavalueof4underlowwaterandnutrient
cies with high RGR generally have high rates of photosynthesis and levelsandreflectingitsabilitytostronglyalterallocationpatterns.In
respirationperunitmass,requiringhighnutrientlevelstosustainsuch fact, F. albida is a species very sensitive to drought (Roupsard, 1997)
physiological activity and high leaf turnover. Slow-growing species and its ability to quickly reach deeper, moist soil horizons may be
show opposite patterns (Reich et al., 1997; Wright et al., 2004). In criticalincopingwithdroughtatsuchanearlystage,ashasbeenshown
contrasttothedeciduousspeciesinourstudy,theevergreenT.indica forotherwoodyspeciesindryconditions(PadillaandPugnaire,2007).
did not respond to resource addition. It is a slow-growing species OppositetoitsdramaticresponseconcerningR/S,RGRdidnotchange
(Diallo et al., 2008; El-Siddig et al., 2006) native to dry, subtropical much in F. albida, and SLA tended to decrease only under reduced
environments and may have, over evolutionary time, adjusted a low water,buthighNavailability.
resource demand to a low supply to avoid exhausting limiting re- Inourexperiment,R/Sinbaobab(A.digitata)respondedtoNad-
sources.ThiswaythelowRGRisclosertoitsoptimum(Chapin,1980; ditionbutonlywhenwaterwasavailable.Thismaybebecause,while
GrimeandHunt,1975).Thelackofastrongerresponseofspecieswith adult baobab trees accumulate water in their stem, baobab seedlings
aresourceexploitativestrategytoresourceshortageindicatesthepre- use the taproot as main storage organ (Wickens and Lowe, 2008) al-
senceoftrade-offsbetweentraitsandwithbiophysicalconstraintsthat locating more resources to belowground structures than adults (Cuni-
resultinconvergenceofresourceacquisitionstrategies(Reich,2014). Sanchez et al., 2011), particularly when water is limiting. A similar
TheRGRisaproductofnetassimilationrate(NAR)andleafarea strategyhasalsobeenobservedinothertropicaltreespecies(Poorter
ratio(LAR)(Evans,1972).LARinturncanbepartitionedintospecific andMarkesteijn,2008).Giventheimportanceofthetaprootforseed-
leaf area (SLA) and leaf mass ratio (LMR), or the dry mass of leaves lingsurvivalunderdryspells(PadillaandPugnaire,2007;Poorterand
relativetototalplantdrymass.MoststudiesshowthatLARisthefactor Markesteijn, 2008), seedlings with relatively larger taproots have a
thatbestexplainsdifferencesinRGR,andthemostimportantcompo- higherchanceofsurvivalindrought-proneenvironmentsthanseedlings
nentofLARisSLA(Antúnezetal.,2001;HoffmannandFranco,2003; withrelativelysmallertaproots,becausetheycanstoremorewaterand
Ruiz-Robleto and Villar, 2005) further reflecting a trade-off in plant carbohydrates(KabeyaandSakai,2003)andkeeptherootincontact
resource-use strategy tightly coupled to resource availability (Grime withmoistsoilhorizons(PadillaandPugnaire,2007).
etal.,1997).Inourexperiment,SLAdifferedamongspeciesandacross AcharacteristicofplantsinaridenvironmentssuchastheSahelian
water and nutrient supply levels (Coley et al., 1985; Evans, 1972; savannaistoshowhightemporalandspatialvariationingrowthpat-
Lavorel and Garnier, 2002). Therefore, changes in RGR mostly paral- terns, which depends on environmental variability, particularly soil
leledvariationsinSLA,suggestingthatSLAwasakeyfactorsustaining moisture(AbdelrahmanandKrzywinski,2008).Leafhabit,i.e.whether
RGR(PoorterandGarnier,2007). aspeciesisevergreenordeciduous,hasbeenlinkedtodivergentplant
Biomassallocationpatternsvaryamongspeciesandaresensitiveto strategies in seasonal climates (Markesteijn and Poorter, 2009;
environmentalclues(Atkinetal.,2006).Manyreportshaveshownthat Tomlinson et al., 2012) as the Sahel. Deciduous species may allocate
drought influences allocation patterns (Ledo et al., 2018; Liu and more resources to roots than evergreen species in any seasonal en-
Stützel,2004;Poorteretal.,2015;Spollenetal.,1993)particularlyR/S vironment,definingdistinctbiomasspartitioningpatternsbetweenleaf
values(Poorter etal.,2012; Turner,1997). Plantswithahigherallo- habits(Espeltaetal.,2005).Withinourspecies,F.albidaandA.tortilis
cation to roots can compete more effectively for soil resources while showed high plasticity in their functional traits responses allowing
those with a higher proportion of shoots can collect more radiation them to cope with water and nutrient variability, which may be a
(Bloometal.,1985;Tilman,1988).Inourexperiment,R/Svalueswere reasonbehindtheirlargegeographicalspreadinAfrica,astheyareable
generallywellabove1irrespectiveofthespecies,suggestingageneti- tocopewithcontrastedsupplylevelsofwaterandnutrients.
cally-fixed higher biomass allocation to roots in seedlings of species
adapted to infertile environments (Aerts and Chapin, 2000; Chapin,
5. Conclusions
1980;Lambersetal.,2008)orwithseverewatershortage(Fernández
andReynolds,2000;Lambersetal.,2008;Padillaetal.,2009;Wright
Our data show that important plant functional traits changed
and Westoby, 1999). Since seedling growth rate is an important life
stronglyinresponsetochangingresourceavailability,andthathigher
history trait, critical for plant survival and establishment in water-
RGR was supported by larger SLA. Overall, seedlings of the Sahelian
limited environments, we expect traits in early ontogenetic stages to
species in our study allocated more biomass to roots than to shoots,
contributesignificantlytothespecies’adaptivecapacity.Itisworthto
reaching 4-fold at times, reflecting adaptive strategies to keep RGR
note that R/S changes with plant development, as seedlings allocate
leveled to resource supply. Overall, functional traits other than R/S
morebiomasstoroots(Gedrocetal.,1996),andthereforeourresults
respondedmoretonutrientthantowateraddition,andtwospecies,A.
5
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
tortilis and F. albida, showed high phenotypic plasticity, which may morphologyanditsimplicationsforselectingsuperiorplantingmaterial.Sci.Hortic.
underlietheirlargedistributionarea.Ourdatasuggestthatthedifferent (Amsterdam)130,109–117.
Di-Rienzo,J.A.,Casanoves,F.,Balzarini,M.G.,Gonzalez,L.,Tablada,M.,Robledo,C.W.,
Sahelian species will respond differently to future environmental
2013.InfoStat.InfoStat.
changes, which will likely affect their geographic distribution and Diallo,B.,Mckey,D.,Chevallier,M.H.,Joly,H.,Hossaert-Mckey,M.,2008.Breeding
thereforethestructureoftheplantcommunitiestheyarepartof. systemandpollinationbiologyofthesemi-domesticatedfruittree,Tamarindusindica
L.,(Leguminosae:caesalpinioideae):implicationsforfruitproduction,selective
breeding,andconservationofgeneticresources.AfricanJ.Biotechnol.7,4068–4075.
Acknowledgements Díaz,S.,Kattge,J.,Cornelissen,J.H.C.,Wright,I.J.,Lavorel,S.,Dray,S.,Reu,B.,Kleyer,
M.,Wirth,C.,Prentice,I.C.,Garnier,E.,Bönisch,G.,Westoby,M.,Poorter,H.,Reich,
P.B.,Moles,A.T.,Dickie,J.,Gillison,A.N.,Zanne,A.E.,Chave,J.,Wright,S.J.,
We thank Hermann Heilmeier and two anonymous reviewers for
Sheremet’ev,S.N.,Jactel,H.,Baraloto,C.,Cerabolini,B.,Pierce,S.,Shipley,B.,
commentsonanearlierdraftofthismanuscript.Thisworkwasfunded Kirkup,D.,Casanoves,F.,Joswig,J.S.,Günther,A.,Falczuk,V.,Rüger,N.,Mahecha,
bytheFUNCITREEProjectwithintheEU 7thFrameworkProgramme M.D.,Gorné,L.D.,2016.Theglobalspectrumofplantformandfunction.Nature529,
(grant KBBE-2272657FP). Additional funds were provided by AEI- 167–171.
Diémé,J.S.,Diouf,M.,Armas,C.,Rusch,G.M.,Pugnaire,F.I.,2018.Functionalgroupsof
MINECO (grants CGL2014-59010-R and CGL2017-84515-R). JSD re- SaheliantreesinasemiaridagroforestrysystemofSenegal.J.PlantEcol.11,
ceived a PhD fellowship from the Spanish Agency of International 375–384.
Cooperation for Development (AECID). CA was supported by a post- El-Siddig,K.,Gunasena,H.,Prasad,B.,Pushpakumara,D.,Ramana,K.,Vijayand,P.,
Williams,J.,2006.Tamarind(TamarindusindicaL.).SouthamptonCentrefor
doctoral contract from the FUNCITREE Project and currently holds a
UnderutilsedCrops,Southampton,UK.
“Ramón y Cajal” Fellowship (RYC-2012-12277) from the Spanish Engelbrecht,B.M.J.,Kursar,T.A.,2003.Comparativedrought-resistanceofseedlingsof
Government. 28speciesco-occuringtropicalwoodyplants.Oecologia136,383–393.
Engelbrecht,B.M.,Kursar,T.A.,Tyree,M.T.,2005.Droughteffectsonseedlingsurvivalin
atropicalmoistforest.Trees19,312–321.
AppendixA. Supplementarydata Engelbrecht,B.M.J.,Dalling,J.W.,Pearson,T.R.H.,Wolf,R.L.,Galvez,D.A.,Koehler,T.,
Tyree,M.T.,Kursar,T.A.,2006.Shortdryspellsinthewetseasonincreasemortality
oftropicalpioneerseedlings.Oecologia148,258–269.
Supplementarymaterialrelatedtothisarticlecanbefound,inthe
Espelta,J.M.,Cortés,P.,Mangirón,M.,Retana,J.,2005.Differencesinbiomassparti-
onlineversion,atdoi:https://doi.org/10.1016/j.flora.2018.10.009. tioning,leafnitrogencontent,andwateruseefficiency(δ13C)resultinsimilarper-
formanceofseedlingsoftwoMediterraneanoakswithcontrastingleafhabit.
Ecoscience12,447–454.
References
Evans,G.C.,1972.TheQuantitativeAnalysisofPlantGrowth.BlackwellScientific
Publications,Oxford,UK.
Abdelrahman,H.F.,Krzywinski,K.,2008.EnvironmentaleffectsonmorphologyofAcacia Fernández,R.J.,Reynolds,J.F.,2000.Potentialgrowthanddroughttoleranceofeight
tortilisgroupintheRedSeaHills,north-easternSudanandSouth-EasternEgypt.For. desertgrasses:lackofatradeoff?Oecologia123,90–98.
Ecol.Manage.255,254–263. Garnier,E.,Vile,D.,Roumet,C.,Lavorel,S.,Grigulis,K.,Navas,M.L.,Lloret,F.,2018.
Adams,H.D.,Guardiola-Claramonte,M.,Barron-Gafford,G.A.,Villegas,J.C.,Breshears, Inter-andintra-specifictraitshiftsinsitesdifferinginaridityatthenorthwestern
D.D.,Zou,C.B.,Huxman,T.E.,2009.Temperaturesensitivityofdrought-inducedtree edgeoftheMediterraneanBiogeographicRegion(inpress).Flora.https://doi.org/
mortalityportendsincreasedregionaldie-offunderglobal-change-typedrought. 10.1016/j.flora.2018.07.009.
Proc.Natl.Acad.Sci.U.S.A.106,7063–7066. Gedroc,J.J.,McConnaughay,K.D.M.,Coleman,J.S.,1996.Plasticityinroot/shootpar-
Aerts,R.,Chapin,F.S.I.I.I.,2000.Themineralnutritionofwildplantsrevisited:are- titioning:optimal,ontogenetic,orboth?Funct.Ecol.10,44–50.
evaluationofprocessesandpatterns.Adv.Ecol.Res.30,1–67. Grime,J.P.,1998.Benefitsofbiodiversityeffectsonecosystems:immediate,filterand
Allen,C.D.,Breshears,D.D.,1998.Drought-inducedshiftofaforest–woodlandecotone: foundereffects.J.Ecol.86,902–910.
rapidlandscaperesponsetoclimatevariation.Proc.Natl.Acad.Sci.U.S.A.95, Grime,J.P.,Hunt,R.,1975.Relativegrowth-rate:itsrangeandadaptivesignificanceina
14839–14842. localflora.J.Ecol.63,393–422.
Antúnez,I.,Retamosa,E.C.,Villar,R.,2001.Relativegrowthrateinphylogenetically Grime,J.P.,Thompson,K.,Hunt,R.,Hodgson,J.G.,Cornelissen,J.H.C.,Rorison,I.H.,
relateddeciduousandevergreenwoodyspecies.Oecologia128,172–180. Hendry,G.A.F.,Ashenden,T.W.,Askew,A.P.,Band,S.R.,Booth,R.E.,Bossard,C.C.,
Atkin,O.K.,Loveys,B.R.,Atkinson,L.J.,Pons,T.L.,2006.Phenotypicplasticityand Campbell,B.D.,Cooper,J.E.L.,Davison,A.W.,Gupta,P.L.,Hall,W.,Hand,D.W.,
growthtemperature:understandinginterspecificvariability.J.Exp.Bot.57, Hannah,M.A.,Hillier,S.H.,Hodkinson,D.J.,Jalili,A.,Liu,Z.,Mackey,J.M.L.,
267–281. Matthews,N.,Mowforth,M.A.,Neal,A.M.,Reader,R.J.,Reiling,K.,Ross-Fraser,W.,
Atta,H.A.E.,Aref,I.M.,Ahmed,A.I.,Khan,P.R.,2012.Morphologicalandanatomical Spencer,R.E.,Sutton,F.,Tasker,D.E.,Thorpe,P.C.,Whitehouse,J.,1997.Integrated
responseofAcaciaehrenbergianaHayneandAcaciatortilis(Forssk)Haynessubspp. screeningvalidatesprimaryaxisofspecialisationinplants.Oikos79,259–281.
Raddianaseedlingstoinducedwaterstress.AfricanJ.Biotechnol.11,10188–10199. Hanson,P.J.,Weltzin,J.F.,2000.Droughtdisturbancefromclimatechange:responseof
Bloom,A.J.,Chapin,F.S.,Mooney,H.A.,1985.Resourcelimitationinplants–aneco- UnitedStatesforests.Sci.TotalEnviron.262,205–220.
nomicanalogy.Annu.Rev.Ecol.Evol.Syst.16,363–392. Hoffmann,W.A.,Franco,A.C.,2003.Comparativegrowthanalysisoftropicalforestand
Boko,M.,Niang,I.,Nyong,A.,Vogel,C.,Githeko,A.,Medany,M.,Osman-Elasha,B., savannawoodyplantsusingphylogeneticallyindependentcontrasts.J.Ecol.91,
Tabo,R.,Yanda,P.,2007.Africa.In:Parry,M.,Canziani,J.,Palutikof,J.,Linden,Pj, 475–484.
Hanson,C.(Eds.),ClimateChange2007:Impacts,AdaptationandVulnerability. Hungate,B.,Reichstein,M.,Dijkstra,P.,Johnson,D.,Hymus,G.,Tenhunen,J.D.,Hinkle,
ContributionofWorkingGroupIItotheFourthAssessmentReportofthe C.R.,Drake,B.,2002.Evapotranspirationandsoilwatercontentinascrub-oak
IntergovernmentalPanelonClimateChange.CambridgeUniversityPress, woodlandundercarbondioxideenrichment.Glob.ChangeBiol.8,289–298.
Cambridge,UK,pp.433–467. Hunt,R.,Cornelissen,J.H.C.,1997.Componentsofrelativegrowthrateandtheirinter-
Box,E.O.,1995.Factorsdeterminingdistributionsoftreespeciesandplantfunctional relationsin59temperateplantspecies.NewPhytol.135,395–417.
types.Vegetatio121,101–116. Husáková,I.,Weiner,J.,Münzbergová,Z.,2018.Speciestraitsandshoot–rootbiomass
Brooks,N.,2004.DroughtintheAfricanSahel:LongTermPerspectivesandFuture allocationin20dry-grasslandspecies.J.PlantEcol.11,273–285.
Prospects. Norwich,UK.. Jump,A.S.,Hunt,J.M.,Penuelas,J.,2007.Climaterelationshipsofgrowthandestab-
Capers,R.S.,Chazdon,R.L.,Brenes,A.R.,Alvarado,B.V.,2005.Successionaldynamicsof lishmentacrossthealtitudinalrangeofFagussylvaticaintheMontsenyMountains,
woodyseedlingcommunitiesinwettropicalsecondaryforests.J.Ecol.93, northeastSpain.Ecoscience14,507–518.
1071–1084. Kabeya,D.,Sakai,S.,2003.Theroleofrootsandcotyledonsasstorageorgansinearly
ChapinIII.,F.S.,1980.Themineralnutritionofwildplants.Annu.Rev.Ecol.Syst.11, stagesofestablishmentinQuercuscrispula:aquantitativeanalysisofthenon-
233–260. structuralcarbohydrateincotyledonsandroots.Ann.Bot.92,537–545.
Chaturvedi,R.K.,Raghubanshi,A.S.,Singh,J.S.,2013.Growthoftreeseedlingsina Khurana,E.,Singh,J.S.,2001.Ecologyofseedandseedlinggrowthforconservationand
tropicaldryforestinrelationtosoilmoistureandleaftraits.J.PlantEcol.6, restorationoftropicaldryforest:areview.Environ.Conserv.28,39–52.
158–170. Kleyer,M.,Bekker,R.M.,Knevel,I.C.,Bakker,J.P.,Thompson,K.,Sonnenschein,M.,
Coley,P.D.,Bryant,J.P.,Chapin,F.S.I.I.I.,1985.Resourceavailabilityandplantanti- Poschlod,P.,Groenendael,J.M.,van,Klimes,L.,Klimesova,J.,Klotz,S.,Rusch,G.M.,
herbivoredefense.Science230,895–899. Hermy,M.,Adriaens,D.,Boedeltje,G.,Bossuyt,B.,Dannemann,A.,Endels,P.,
Comita,L.S.,Engelbrecht,B.M.J.,2009.Seasonalandspatialvariationinwateravail- Gotzenberger,L.,Hodgson,J.G.,Jackel,A.K.,Kühn,I.,Kunzmann,D.,Ozinga,W.A.,
abilitydrivehabitatassociationsinatropicalforest.Ecology90,2755–2765. Römermann,C.,Stadler,M.,Schlegelmilch,J.,Steendam,H.J.,Tackenberg,O.,
Condit,R.,Engelbrecht,B.M.J.,Pino,D.,Perez,R.,Turner,B.L.,2013.Speciesdistribu- Wilmann,B.,Cornelissen,J.H.C.,Eriksson,O.,Garnier,E.,Peco,B.,2008.TheLEDA
tionsinresponsetoindividualsoilnutrientsandseasonaldroughtacrossacommu- Traitbase:adatabaseoflife-historytraitsoftheNorthwestEuropeanflora.J.Ecol.
nityoftropicaltrees.Proc.Natl.Acad.Sci.U.S.A.110,5064–5068. 96,1266–1274.
Cornelissen,J.H.,Castro-Díez,P.,Carnelli,A.L.,1998.Variationinrelativegrowthrate Knapp,A.K.,Beier,C.,Briske,D.D.,Classen,A.T.,Luo,Y.,Reichstein,M.,Smith,M.D.,
amongwoodyspecies.In:Lambers,H.,Poorter,H.,Van-Vuuren,M.(Eds.),Inherent Smith,S.D.,Bell,J.E.,Fay,P.A.,Heisler,J.L.,Leavitt,S.W.,Sherry,R.,Smith,B.,
VariationinPlantGrowthPhysiologicalMechanismsandEcologicalConsequences. Weng,E.,2008a.Consequencesofmoreextremeprecipitationregimesforterrestrial
BackhuysPublishers,Leiden,pp.363–392. ecosystems.AibsBull.58,811–821.
Cuni-Sanchez,A.,Smedt,S.D.,Haq,N.,Samson,R.,2011.Variationinbaobabseedling Knapp,A.K.,Briggs,J.M.,Collins,S.L.,Archer,S.R.,Bret-Harte,M.S.,Ewers,B.E.,Peters,
6
J.S.Diémé,etal. Flora xxx (xxxx) xxx–xxx
D.P.,Young,D.R.,Shaver,G.R.,Pendall,E.,Cleary,M.B.,2008b.Shrubencroach- Pope,V.D.,Gallani,M.L.,Rowntree,P.R.,Stratton,R.A.,2000.Theimpactofnewphy-
mentinNorthAmericangrasslands:shiftsingrowthformdominancerapidlyalters sicalparametrizationsintheHadleyCentreclimatemodel:HadAM3.Clim.Dyn.16,
controlofecosystemcarboninputs.Glob.ChangeBiol.14,615–623. 123–146.
Lambers,H.,Chapin,F.S.,Pons,T.L.,2008.PlantPhysiologicalEcology,2nded.Springer. Pugnaire,F.I.,Luque,M.T.,Armas,C.,Gutiérrez,L.,2006.Colonizationprocessesinsemi-
Lamers,J.P.A.,Khamzina,A.,Worbes,M.,2006.Theanalysesofphysiologicaland aridMediterraneanold-fields.J.AridEnviron.65,591–603.
morphologicalattributesof10treespeciesforearlydeterminationoftheirsuitability RDevelopmentCoreTeam,2013.R:ALanguageandEnvironmentforStatistical
toafforestdegradedlandscapesintheAralSeaBasinofUzbekistan.For.Ecol. Computing.
Manage.221,249–259. Reich,P.B.,2014.Theworld-wide“fast-slow”planteconomicsspectrum:atraitsmani-
Lang,B.,Geiger,A.,Oyunbileg,M.,Ahlborn,J.,vonWehrden,H.,Wesche,K., festo.J.Ecol.102,275–301.
Oyuntsetseg,B.,Römermann,C.,2018.Intraspecifictraitvariationpatternsalonga Reich,P.B.,Tjoelker,M.G.,Walters,M.B.,Vanderklein,D.W.,Buschena,C.,1998.Close
precipitationgradientinMongolianrangelands(inpress).Flora. associationofRGR,leafandrootmorphology,seedmassandshadetolerancein
Lavorel,S.,Garnier,E.,2002.Predictingchangesincommunitycompositionandeco- seedlingsofnineborealtreespeciesgrowninhighandlowlight.Funct.Ecol.12,
systemfunctionfromplanttraits:revisitingtheholygrail.Funct.Ecol.16,545–556. 327–338.
Ledo,A.,etal.,2018.Treesizeandclimaticwaterdeficitcontrolroottoshootratioin Reich,P.B.,Walters,M.B.,Ellsworth,D.S.,1997.Fromtropicstotundra:globalcon-
individualtreesglobally.NewPhytol.217,8–11. vergenceinplantfunctioning.Proc.Natl.Acad.Sci.U.S.A.94,13730–13734.
Liu,F.,Stützel,H.,2004.Biomasspartitioning,specificleafarea,andwateruseefficiency Roupsard,O.,1997.ÉcophysiologieEtDiversitéGénétiqueDeFaidherbiaalbida(Del.)A.
ofvegetableamaranth(Amaranthusspp.)inresponsetodroughtstress.Sci.Hortic. Chev.(syn.AcaciaalbidaDel.),UnArbreàUsagesMultiplesd’AfriqueSemi-aride.
(Amsterdam)102,15–27. FonctionnementHydriqueEtEfficienced’utilisationDel’eaud’arbresAdultesEnParc
MacCracken,M.C.,Barron,E.J.,Easterling,D.R.,Felzer,B.S.,Karl,T.R.,2003.Climate AgroforestierEtDesJuvénilesEnConditionsContrôlées.PhDThesis.UniversitéH
changescenariosfortheUSnationalassessment.Bull.Am.Meteorol.Soc.84, Poincaréde,NancyI,France.
1711–1723. Ruiz-Robleto,J.,Villar,R.,2005.Relativegrowthrateandbiomassallocationinten
Markesteijn,L.,Poorter,L.,2009.Seedlingrootmorphologyandbiomassallocationof62 woodyspecieswithdifferentleaflongevityusingphylogeneticindependentcontrasts
tropicaltreespeciesinrelationtodrought-andshade-tolerance.J.Ecol.97,311–325. (PICs).PlantBiol.7,484–494.
Meier,I.C.,Knutzen,F.,Eder,L.M.,Müller-Haubold,H.,Goebel,M.-O.,Bachmann,J., Shipley,B.,2006.Netassimilationrate,specificleafareaandleafmassratio:whichis
Hertel,D.,Leuschner,C.,2018.ThedeeprootsystemofFagussylvaticaonsandysoil: mostcloselycorrelatedwithrelativegrowthrate?Ameta-analysis.Funct.Ecol.20,
structureandvariationacrossaprecipitationgradient.Ecosystems21,280–296. 565–574.
Montgomery,R.A.,Chazdon,R.L.,2002.Lightgradientpartitioningbytropicaltree Shipley,B.,DeBello,F.,Cornelissen,J.H.C.,Laliberté,E.,Laughlin,D.C.,Reich,P.B.,
seedlingsintheabsenceofcanopygaps.Oecologia131,165–174. 2016.Reinforcingloosefoundationstonesintrait-basedplantecology.Oecologia
Nicotra,A.B.,Atkin,O.K.,Bonser,S.P.,Davidson,A.M.,Finnegan,E.J.,Mathesius,P.P., 180,923–931.
Purugganan,M.D.,Richards,C.L.,Valladares,F.,vanKleunen,M.,2010.Plant Slot,M.,Poorter,L.,2007.Diversityoftropicaltreeseedlingresponsestodrought.
phenotypicplasticityinachangingclimate.TrendsPlantSci.15,684–692. Biotropica39,683–690.
Oke,T.A.,Wang,J.R.,2015.Assessingpopulation-levelresponsetointeractingtem- Song,X.,Li,J.,Zhang,W.,Tang,Y.,Sun,Z.,Cao,M.,2016.Variantresponsesoftree
peratureandmoisturestress.Ecol.Res.30,931–940. seedlingtoseasonaldroughtstressalonganelevationaltransectintropicalmontane
Padilla,F.M.,Pugnaire,F.I.,2007.RootingdepthandsoilmoisturecontrolMediterranean forests.Sci.Rep.6,36438.
woodyseedlingsurvivalduringdrought.Funct.Ecol.21,489–495. Spollen,W.G.,Sharp,R.E.,Saab,I.N.,Wu,Y.,1993.Regulationofcellexpansioninroots
Padilla,F.M.,Miranda,J.D.,Jorquera,M.J.,Pugnaire,F.I.,2009.Variabilityinamount andshootsatlowwaterpotentials.In:Smith,J.A.C.,Griffiths,H.(Eds.),Water
andfrequencyofwatersupplyaffectsrootsbutnotgrowthofaridshrubs.PlantEcol. Deficits,PlantResponsesfromCelltoCommunity.BiosScientificPublishersOxford,
204,261–270. pp.37–52.
Paine,C.E.T.,Harms,K.E.,Ramos,J.,2008.Supplementalirrigationincreasesseedling Tilman,D.,1988.PlantStrategiesandtheDynamicsandStructureofPlantCommunities.
performanceanddiversityinatropicalforest.J.Trop.Ecol.25,171–180. PrincetonUniversityPress,Princeton.
Pedersen,B.S.,1998.Theroleofstressinthemortalityofmidwesternoaksasindicated Tomlinson,K.W.,Sterck,F.J.,Bongers,F.,daSilva,D.A.,Barbosa,E.R.M.,Ward,D.,
bygrowthpriortodeath.Ecology79,79–93. Bakker,F.T.,vanKaauwen,M.,Prins,H.H.T.,deBie,S.,vanLangevelde,F.,2012.
Peñuelas,J.,Ogaya,R.,Boada,M.,Jump,S.A.,2007.Migration,invasionanddecline: Biomasspartitioningandrootmorphologyofsavannatreesacrossawatergradient.J.
changesinrecruitmentandforeststructureinawarming-linkedshiftofEuropean Ecol.100,1113–1121.
beechforestinCatalonia,NESpain.Ecography30,829–837. Turner,N.C.,1997.Furtherprogressincropwaterrelations.Adv.Agron.58,293–338.
Pérez-Harguindeguy,N.,Díaz,S.,Garnier,E.,Lavorel,S.,Poorter,H.,Jaureguiberry,P., vanNoordwijk,A.J.,deJong,G.,1986.Acquisitionandallocationofresources:their
Bret-Harte,M.S.C.,Ornwell,W.K.,Craine,J.M.,Gurvich,D.E.,Urcelay,C., influenceonvariationinlifehistorytactics.Am.Nat.128,137–142.
Veneklaas,E.J.,Reich,P.B.,Poorter,L.,Wright,I.J.,Ray,P.,Enrico,L.,Pausas,J.G., Volder,A.,Briske,D.D.,Tjoelker,M.G.,2013.Climatewarmingandprecipitationredis-
Vos,A.C.D.,Buchmann,N.,Funes,G.,Quetier,F.,Hodgson,J.G.,Thompson,K., tributionmodifytree–grassinteractionsandtreespeciesestablishmentinawarm-
Morgan,H.D.,Steege,H.T.,Heijden,M.G.A.V.D.,Sack,L.,Blonder,B.,Poschlod,P., temperatesavannah.Glob.Chang.Biol.19,843–857.
Vaieretti,M.V.,Conti,G.,Staver,A.C.,Aquino,S.,Cornelissen,J.H.C.,2013.New Weiner,J.,2004.Allocation,plasticityandallometryinplants.Perspect.PlantEcol.Evol.
handbookforstandardisedmeasurementofplantfunctionaltraitsworldwide.Aust.J. Syst.6,207–215.
Bot.61,167–234. Wetherald,R.T.,Manabe,S.,1995.Themechanismsofsummerdrynessinducedby
Poorter,H.,1989.Interspecificvariationinrelativegrowthrate:onecologicalcausesand greenhousewarming.J.Clim.8,3096–3108.
physiologicalconsequences.In:Lambers,H.,Cambridge,M.L.,Konings,H.,Pons,T.L. Wickens,G.E.,Lowe,P.,2008.TheBaobabs:PachycaulsofAfrica,Madagascarand
(Eds.),CausesandConsequencesofVariationinGrowthRateandProductivityin Australia.Springer,London,UK.
Plants.SPBAcademicPublishing,TheHague,TheNetherlands,pp.101–123. Wright,I.J.,Westoby,M.,1999.Differencesinseedlinggrowthbehaviouramongspecies:
Poorter,H.,Garnier,E.,2007.Ecologicalsignificanceofinherentvariationinrelative traitcorrelationsacrossspecies,andtraitshiftsalongnutrientcomparedtorainfall
growthrateanditscomponents.In:Pugnaire,F.I.,Valladares,F.(Eds.),Handbookof gradients.J.Ecol.87,85–97.
FunctionalPlantEcology.CRCPress,BocaRaton,Florida,pp.82–114. Wright,I.J.,Reich,P.B.,Westoby,M.,Ackerly,D.D.,Baruch,Z.,Bongers,F.,Cavender-
Poorter,H.,Jagodzinski,A.M.,Ruiz-Peinado,R.,Kuyah,S.,Luo,Y.,Oleksyn,J.,Usoltsev, Bares,J.,Chapin,T.,Cornelissen,J.H.C.,Diemer,M.,Flexas,J.,Garnier,E.,Groom,
V.A.,Buckley,T.N.,Reich,P.B.,Sack,L.,2015.Howdoesbiomassdistribution P.K.,Gulias,J.,Hikosaka,K.,Lamont,B.B.,Lee,T.,Lee,W.,Lusk,C.,Midgley,J.J.,
changewithsizeanddifferamongspecies?Ananalysisfor1200plantspeciesfrom Navas,M.L.,Niinemets,U.,Oleksyn,J.,Osada,N.,Poorter,H.,Poot,P.,Prior,L.,
fivecontinents.NewPhytol.208,736–749. Pyankov,V.I.,Roumet,C.,Thomas,S.C.,Tjoelker,M.G.,Veneklaas,E.J.,Villar,R.,
Poorter,H.,Niklas,K.J.,Reich,P.B.,Oleksyn,J.,Poot,P.,Mommer,L.,2012.Biomass 2004.Theworldwideleafeconomicsspectrum.Nature428,821–827.
allocationtoleaves,stemsandroots:meta-analysesofinterspecificvariationand Yavitt,J.B.,Wright,S.J.,2008.Seedlinggrowthresponsestowaterandnutrientaug-
environmentalcontrol.NewPhytol.193,30–50. mentationintheunderstoryofalowlandmoistforest,Panama.J.Trop.Ecol.24,
Poorter,L.,Markesteijn,L.,2008.Seedlingtraitsdeterminedroughttoleranceoftropical 19–26.
treespecies.Biotropica40,321–331.
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