Wood specific gravity and anatomy of branches and roots in 113 Amazonian rainforest tree species

16 Pages·2014·1.38 MB·English

Research
Wood specific gravity and anatomy of branches and roots in 113
Amazonian rainforest tree species across environmental
gradients
ClaireFortunel1,JulienRuelle1,2,JacquesBeauch^ene3,PaulV.A.Fine4andChristopherBaraloto1,5
1INRA,UMREcologiedesForêtsdeGuyane,BP709,97387KourouCedex,France;2INRA,UMR1092Laboratoired’EtudedesressourcesForêtBois,CentreINRAdeNancy-Lorraine,
54280Champenoux,France;3CIRAD,UMREcologiedesForêtsdeGuyane,BP709,97387KourouCedex,France;4DepartmentofIntegrativeBiology,UniversityofCalifornia,Berkeley,
CA94720,USA;5DepartmentofBiology,UniversityofFlorida,Gainesville,FL32611,USA
Summary
Authorforcorrespondence: (cid:1) Woodspecificgravity(WSG)isastrongpredictoroftreeperformanceacrossenvironmental
ClaireFortunel gradients.Yetitremainsunclearhowanatomicalelementslinkedtodifferentwoodfunctions
Tel:[phone]
contributetovariationinWSGinbranchesandrootsacrosstropicalforests.
Email:[email protected]
(cid:1) We examined WSG and wood anatomy in white sand, clay terra firme and seasonally
Received:13August2013
floodedforestsinFrenchGuiana,spanningbroadenvironmentalgradientsfoundthroughout
Accepted:6November2013
Amazonia.Wemeasured15traitsrelatingtobranchesandsmallwoodyrootsin113species
representing the 15 most abundant species in each habitat and representative species from
NewPhytologist(2014)202:79–94 sevenmonophyleticlineagesoccurringinallhabitats.
doi:10.1111/nph.12632 (cid:1) Fiber traits appear to be major determinants of WSG, independent of vessel traits, in
branchesandroots.FibertraitsandbranchandrootWSGincreasedfromseasonallyflooded
speciestoclayterrafirmespeciesandlastlytowhitesandspecies.Branchandrootwoodtraits
Keywords: Amazonianforests,branch,
environmentalgradients,neotropicaltrees, were strongly phylogenetically constrained. Lineages differed in wood design, but exhibited
root,woodanatomicaltraits,wood similarvariationinwoodstructureacrosshabitats.
functions,wooddensity. (cid:1) Weconcludethattropicaltreescaninvestdifferentlyinsupportandtransporttorespondto
environmental conditions. Wind disturbance and drought stress represent significant filters
drivingtreedistributionofAmazonianforests;hencewesuggestthatbiophysicalexplanations
shouldreceivemoreattention.
A growing number of studies have tested these two hypotheses
Introduction
(Ackerly, 2004; Preston etal., 2006; Jacobsen etal., 2007a;
Wood specific gravity has emerged as central to the ecology of Zanne etal., 2010; Martinez-Cabrera etal., 2011; Gleason etal.,
woody plant species as it relates to growth, mechanical strength, 2012),butfewstudieshavesofarintegratedallwoodanatomical
efficiencyandsafetyofhydraulictransport,waterstorage,survival elements to explore their relative contribution to wood specific
and resistance to herbivory (Jacobsen etal., 2008; Chave etal., gravity (Jacobsen etal., 2007a; Pratt etal., 2007; Martinez-
2009; Zanne etal., 2010). Indeed, wood specific gravity reflects Cabreraetal.,2009;Poorteretal.,2010;Lensetal.,2011).Addi-
plant allocation to supportand conduction,which in turn influ- tionally, few studies have investigated the relationship between
ences the performance and life history strategies of woody plant wood specific gravity and wood anatomy in the hyper-diverse
species (Muller-Landau, 2004; Poorter etal., 2010). Wood spe- tropicalforestsandthesestudieshavebeenlimitedtoarelatively
cificgravityisacomplextraitencompassingpropertiesofvarious smallnumberofspecies(Baltzeretal.,2009;Zhu&Cao,2009;
woodelements:vesselsasthemainsap-conductingcellsinangio- Poorter etal., 2010; McCulloh etal., 2011; Fan etal., 2012;
sperms, fibers as the main support structures, and parenchyma Worbes etal., 2013). Still lacking is an understanding of how
which serves forbothstorage andtransportof resourcesbetween woodspecificgravityrelatestotherelativeallocationtothediffer-
xylem and phloem. The tradeoffs involved have led to two non- entanatomicaltissues,especiallyintropicaltreespecies.
mutually exclusive hypotheses: (1) wood specific gravity should Furthermore,thestudyofwoodstructureinwoodyplantspe-
decreasewithincreasingvesselfraction,vesselareaandvesselden- ciesisoftenrestrictedtomainstems andbranches(e.g.Jacobsen
sityaffectingtheamountoflumenspaceinwood(Prestonetal., etal.,2007a;Martinez-Cabreraetal.,2009;Poorteretal.,2010),
2006);and(2)woodspecificgravityshouldincreasewithincreas- mostlybecauseoftheirobviousroleinsaptransportandmechan-
ing fiber fraction, because fiber has the thickest cell walls and ical support, but also because of their accessibility. However,
hencecontributesmosttothewoodmatrix(Poorteretal.,2010). woodspecificgravityasafunctionaltraitisinvolvedinallwoody
(cid:1)2013TheAuthors NewPhytologist(2014)202:79–94 79
NewPhytologist(cid:1)2013NewPhytologistTrust www.newphytologist.com
New
80 Research Phytologist
tissues,fromtherootstothecanopy,soitappearscrucialtostudy Inthepresentstudy,weinvestigatedpatternsofwoodspecific
woodstructureinbothabovegroundandbelowgroundwoodsys- gravityandanatomyofbranchesandsmallwoodyrootsbymea-
tems to better understand wood structure patterns at the whole- suring 15 traits pertaining to support, conduction and storage
plant level (Fortunel etal., 2012). The hydraulic continuity functions on a total of 147 individuals representing 113 species
betweenrootsandstemssuggestsatightrelationshipamongana- across steep environmental gradients in French Guiana. We
tomicaltraitsrelatedtovessels,asdefinedinthepipemodelthe- focused on the three most common habitats in lowland South
ory(Shinozakietal.,1964;Tyree&Ewers,1991;Blonderetal., American rainforests: seasonally flooded, clay terra firme and
2011). However, the increase in flow resistance and the simulta- white sand forests, which represent the range of resource avail-
neousdecreaseinwaterpotentialwithpathlengthhaveledsome ability,flooding and drought stress,forest structure, and floristic
authors to suggest that vessels should taper along the flow path composition found throughout lowland Amazonian forests
fromrootstostems(Westetal.,1999;McCullohetal.,2003).In (Sobrado,2009;Fineetal.,2010;Baralotoetal.,2011;Fortunel
addition, the differences in mechanical constraints and storage etal., 2012). We selected the 15 most abundant species in each
capacity can lead to independent variations of anatomical traits habitattotestforcontrastingdominantstrategiesacrosshabitats,
pertaining to fibers and parenchyma. To our knowledge, roots and also selected species from seven monophyletic lineages that
have been included in only two anatomical studies, which have included species occurring in multiple habitats to test for phylo-
beenlimitedtoarelativelysmallnumberofspecies(ninespecies genetic signal in wood strategies and how they related to habitat
inPrattetal.,2007;fivespeciesinSchuldtetal.,2013).Yetthese association.
twostudiesreportedequivocalcorrelationpatternsbetweenstem Weinvestigatedthefollowingquestions.
androotwoodanatomy. (1) Howdoeswoodspecificgravityrelatetodifferentwoodana-
Several studies have shown that wood specific gravity varies tomicaltraitsinbranchesandroots?Weexpectfiber,lumenand
across environmental gradients, with high wood specific gravity vessel fractions to be correlated to wood specific gravity, while
observed in plant species growing in dry or nutrient-poor soils parenchyma fraction can vary independently. We also expect
(Preston etal., 2006; Martinez-Cabrera etal., 2009; Gleason wood anatomical traits pertaining to transport to be related
etal., 2012). Denser wood generally correlates with lower sap- between branches and roots, while wood anatomical traits per-
wood conductivity, lower wood water storage and thinner bark, taining to support and storage are predicted to vary indepen-
but greater resistance to xylem cavitation (Bucci etal., 2004; dentlybetweenbranchesandroots.
Santiago etal., 2004; Baraloto etal., 2010b). Denser wood also (2) Do wood specific gravity and anatomy show concomitant
requiresgreaterconstructioncosts(Enquistetal.,1999),butcon- variations across habitat types? We predict anatomical traits
fersgreaterresistancetomechanicaldamageandpathogenattack, relatedtotransporttovarybetweenhabitatsaccordingtochanges
leadingtoslowergrowthandlowermortalityrates(Falster,2006; in soil water availability. Specifically, we predict that species in
Poorter etal., 2008; Cornwell etal., 2009). However, a high white sand forests would exhibit higher wood specific gravity,
woodspecificgravitycanbeachievedwithdifferentcombinations greater fiber and parenchyma fractions, but lower vessel fraction
of wood elements, and so far it remains unclear how wood ana- andhydraulicconductivitythanspeciesinterrafirmeandseason-
tomicaltraitscontributetowoodyplantstrategiesacrossenviron- ally flooded forests. As water is available throughout the year in
mental gradients. To bridge the gap between traits, plant seasonally flooded forests, we also predict that species in these
performanceandlifehistorystrategy,itisthusessentialtolookat forests would exhibit even lighter wood, greater hydraulic con-
variations in both wood specific gravity and anatomy across ductivity, and lower fiber and parenchyma fractions than species
environmentalgradients. interrafirmeforests.
In addition to the examination of ecological trends in wood (3) Doesthehighturnoverofplantspeciesamonghabitattypes
structure, several studies have also looked into the evolutionary affect wood trait correlations? According to previous findings on
trendsinanatomicaltraits(e.g.Prestonetal.,2006;Zanneetal., evolutionary patterns in wood specific gravity, we expect wood
2010; Martinez-Cabrera etal., 2011; Gleason etal., 2012; Poor- anatomicaltraitstobeconservedwithintropicaltreegenera.We
teretal.,2012).Woodspecificgravityappearstobephylogeneti- thuspredictthatchangesinplantcommunitycompositionacross
cally conserved at broad and narrow phylogenetic scales environmental gradients can be explained in part by strong
(Cavender-Bares etal., 2004; Chave etal., 2006; Swenson & environmentalfiltersonwoodtraits.
Enquist,2007).However,theanatomicaldesignmaydiffercon-
siderably across plant lineages and it remains unclear whether
MaterialsandMethods
evolutionarychangesinwoodspecificgravityrelatetocongruent
evolutionary changes in wood anatomical traits. The high turn-
Studysites
over of plant species among contrasting forest habitats (Baraloto
etal., 2007; Fine etal., 2010), associated with changes in plant We sampled broad environmental gradients representative of
communityfunctionalcomposition(terSteegeetal.,2006;Kraft lowland South American rainforests, drawing from a network of
etal., 2008), may influence wood trait correlations. In this 35 modified 0.5-ha Gentry plots in French Guiana that covers
respect, a broad range of species functional strategies and evolu- themorecommonlystudiedclayterrafirmeforestsinadditionto
tionaryhistoriesiscrucialtoallowageneraltestofhypothesesof seasonally flooded forests and white sand forests (Baraloto etal.,
woodtraitcoordination. 2011). In all plots we recorded taxonomic identity for all trees
NewPhytologist(2014)202:79–94 (cid:1)2013TheAuthors
www.newphytologist.com NewPhytologist(cid:1)2013NewPhytologistTrust
New
Phytologist Research 81
>2.5cm diameter at 1.3m height (DBH; diameter at breast majorityoftaxatounderstoreylightconditionsandthesmalltree
height), standardizing taxonomy with vouchers referenced with stage. We collected branch and small woody root samples for
the Missouri Botanical Garden Herbarium, and environmental eachselectedindividualduringthedryseason,betweenJuly2009
factors describing climate, soil and forest structure. We selected and November 2009. From a lateral branch in the understorey,
six plots at two locations in French Guiana (Petite Montagne we collected a branch fragment in the last growth unit with a
Tortue to the east, and Laussat to the west), with one plot per diameterof1–2cm.Wedugatthebaseofeachtreetosamplea
habitat per location, to represent the variation in environmental woodyrootsectionwithadiameterof1–2cm,tobeabletocom-
conditions andfloristic composition in theFrench Guianan net- pareitsstructure withthatofthebranch.Weattemptedtosam-
work(Fortuneletal.,2012).Annualaverageofmeasurementsof ple small woody roots within 50cm of the main stem with a
soilwateravailabilityinthethreestudiedplotsinLaussatshowed lateraldirectionofgrowthtocontrolfortensionwoodinthetis-
decreasingsoilhumidityfromseasonallyfloodedforest(40%)to sue. Branch and small woody root fragments were cut into two
terrafirmeforest(17.5%)andfinallytowhitesandforest(5.5%). pieces:one piece was used to measure wood specific gravity, and
theothertodetermineanatomicaltraits.
For wood specific gravity measurements, outer bark was
Traitsampling
removedforbranchandrootwoodsamples.Forbranchsamples,
The aim of our study was not to investigate within-species vari- pith wider than 1mm in diameter was also removed (pith was
ability in wood strategies, but instead to test for differences in negligible in root tissue samples). Branch and root samples were
wood strategies across habitats, accounting for species evolution- saturated with water and saturated volume was estimated using
ary history. Previous work showed that, to represent commu- the Sartorius density determination kit (Goettingen, Germany),
nity-level trait distributions in species-rich plant communities, whichisbasedontheprincipleofwaterdisplacement.Aftermea-
trait sampling can be achieved with only one individual of each surement of the saturated volume, samples were dried at 103°C
species in each plot (Baraloto etal., 2010a). Therefore, our sam- for 72h and dry mass was determined. Branch and root wood
pling design was chosen so as to capture dominant wood strate- specificgravity(Williamson&Wiemann,2010)wasmeasuredas
gies in each habitat by sampling the most abundant species, as thedrymassdividedbythesaturatedvolume.
well as to evaluate phylogenetic constraints on wood strategies For anatomical trait measurements, we cut cross-sections
by sampling representative species from focal monophyletic (15–20lm thick) for each branch and root wood sample with a
lineages. rotary microtome (Leica RM2255; Leica Microsystems, Wetz-
To test for contrasting dominant strategies across habitats, we lar, Germany). Cross-sections were bleached (for 1min), rinsed
first selected the 15 most abundant species per plot. Pooling with distilled water (for 1min) and dipped in ethanol at 50%
together the two studied plots per habitat type to calculate the (for 1min) before being stained for 15min in Safranine O
percentage of the total abundance represented by the 15 most (95%, pure, high-purity biological stain; Acros Organics, Geel,
abundant species in each habitat, our sampling covered 24.6, Belgium) solution (2% w/v). Cross-sections were dehydrated in
19.1 and 47.2% of the total abundance in seasonally flooded, ethanol series at 50% (for 1min), at 75% (for 3min) and at
terrafirmeandwhitesandforests,respectively.Totestforphylo- 100% (for 5min) and then they were dipped in solvent
genetic signal in wood strategies, we additionally selected all (Clearene; Labonord, Templemars, France) before mounting.
species belonging to seven monophyletic lineages that are wide- Up to nine cross-sections per sample were embedded in Eukitt
spreadacrosslowlandAmazonianforests(Fine&Kembel,2011) Mounting Medium (Electron Microscopy, Hatfield, PA, USA)
andthatincludedspeciesoccurringinthethreestudiedhabitats: for histological examination. We selected one cross-section per
Eschweilera (Lecythidaceae), Inga (Fabaceae/Mimosaceae), sample and used a digital camera (Canon EOS 500D; Canon
Licania (Chrysobalanaceae), Micropholis (Sapotaceae), Bombac- Inc., Tokyo, Japan) mounted on a light microscope (Olympus
oideae (Malvaceae), Protium (Burseraceae) and Swartzia (Faba- BX60; Olympus Corporation, Tokyo, Japan) to shoot eight
ceae/Papilionaceae).Theselineagesarephylogeneticallydispersed photographs in natural light with an APO 920 lens that
within the eudicots, the dominant angiosperms in tropical rain together covered most of the wood area of the selected cross-
forests, with representatives of euasterids (Sapotaceae), fabids section for each sample.
(Fabaceae), and malvids (Malvaceae and Burseraceae). The For each of the eight photographs of each branch and small
selected phylogenetic lineages differ in their putative fossil-cali- woody root sample, image analyses were conducted with IMAGEJ
bratedages, withIngaspreadingacrosstheAmazonbasinwithin 1.43 software (http://rsb.info.nih.gov/ij/) to determine branch
the last few million years, Swartzia of intermediate age (10–19 and root anatomical traits (see details in Table1). Anatomical
million yr), and Bombacoideae (Pachira) and Protium likely to traitsmeasuredintheeightphotographsofeachbranchandroot
have longer histories (25–50million yr) (Baum, 1995; samplewerethenaveragedtodetermineindividualvalues.Image
Richardsonetal.,2001;Torke&Schaal,2008). contrast was tuned manually to specifically examine: (1) vessel
We measured wood traits on at least one individual per focal elements, and(2)parenchymaandfiberelements.Wecharacter-
species in each plot (27 species were measured more than once), ized the relative fractions of wood elements in the transversal
representingatotalof147individualsand113speciesacrossthe plan, semi-automatically for vessel elements and manually for
sixplots(Fig.1).Foreachspeciesineachplot,wechosethestem other wood elements: parenchyma fraction (Fp), fiber fraction
nearest to 5cm DBH, to standardize trait measures for the (Ff), mean proportion of cell wall in fibers (Fmfw), total fiber
(cid:1)2013TheAuthors NewPhytologist(2014)202:79–94
NewPhytologist(cid:1)2013NewPhytologistTrust www.newphytologist.com
New
82 Research Phytologist
Oxandra asbeckii
Guatteria conspicua
Anaxagorea dolichocarpa
Iryanthera hostmannii
Siparuna poeppigii
Lauraceae Lauraceae sp. A77
Lauraceae Lauraceae sp. A5
Guapira sp. A1
Gustavia hexapetala
Lecythis poiteaui
Lecythis idatimon
Couratari calycina
Eschweilera pedicellata
Eschweilera sp. A3
Eschweilera parviflora
Eschweilera cf. coriacea
Eschweilera coriacea
Eschweilera grandiflora
Eschweilera micrantha
Pouteria gongrijpii
Manilkara bidentata
Micropholis egensis
Micropholis aff. cayennensis
Micropholis venulosa
Micropholis guyanensis subsp. duckeana
Micropholis guyanensis
Chrysophyllum sanguinolentum
Diospyros cayennensis
Cybianthus fulvopulverulentus subsp. magnoliifolius
Cybianthus sp. A1
Ilex sp. A3
Dendrobangia boliviana
Poraqueiba guianensis
Cordia nodosa
Tabernaemontana sp. A3
Psychotria mapourioides
Posoqueria latifolia
Ferdinandusa aff. goudotiana
Pagamea guianensis
Maytenus amazonica
Sloanea sp. A1
Sloanea meianthera
Rourea frutescens
Cassipourea guianensis
Conceveiba rhytidocarpa
Hevea guianensis
Paypayrola guianensis
Rinorea sp. A7
Drypetes variabilis
Clusia fockeana
Tapura guianensis
Chrysobalanaceae sp. A1
Chrysobalanaceae sp. A12
Licania sp. A4
Licania irwinii
Licania aff. megalophylla
Licania albiflora
Licania densiflora
Licania membranacea
Licania alba
Licania heteromorpha var. heteromorpha
Licania sp. A20
Licania caudata
Licania latistipula
Licania canescens
Licania micrantha
Licania sp. A8
Licania incana
Pourouma minor
Pourouma sp. A5
Vouacapoua americana
Macrolobium guianense
Eperua rubiginosa
Eperua falcata
Eperua grandiflora
Pterocarpus officinalis
Ormosia coutinhoi
Bocoa prouacensis
Swartzia benthamiana
Swartzia leblondii
Swartzia grandifolia
Swartzia canescens
Inga gracilifolia
Inga sertulifera
Inga cf. longipedunculata
Inga rubiginosa
Inga stipularis
Inga melinonis
Inga pezizifera
Inga aff. capitata
Inga laurina
Inga marginata
Inga thibaudiana
Inga sp. A1
Catostemma fragrans
Eriotheca longitubulosa
CPaacrahpiraa pflraovcifelorara Fig.1 Evolutionaryrelationshipsforthe113
Guarea sp. A1 tropicaltreetaxastudiedinFrenchGuiana.
Matayba sp. A5
Cupania sp. A5 ThecladogramisbasedontheAngiosperm
Protium decandrum
Protium pallidum PhylogenyGroup(APG)IIIclassification.
Protium demerarense Colorsindicateoursevenfocalphylogenetic
Protium trifoliolatum
Protium altsonii lineages(red,Eschweilera;yellow,Inga;
Protium gallicum
Protium opacum green,Licania;cyan,Micropholis;blue,
Protium giganteum
Bombacoideae(Pachira);purple,Protium;
Protium aracouchini
Trattinnickia demerarae pink,Swartzia),whilecommonspeciesare
Myrtaceae sp. A2
Myrtaceae sp. A81 indicatedinblack.
NewPhytologist(2014)202:79–94 (cid:1)2013TheAuthors
www.newphytologist.com NewPhytologist(cid:1)2013NewPhytologistTrust
New
Phytologist Research 83
s ss s s s ss s s s s s s s
n nn n n n nn n n n n n n n
OrganF 0.076 0.1461.771 3.264 2.804 0.129 0.6190.923 0.102 0.619 1.809 0.473 1.360 0.486 0.300
Range 0.244;0.946 0.113;0.5560.042;0.403 0.444;0.897 0.432;1.000 0.244;0.880 0.014;0.407930.38210;9321.43910(cid:3)930.00710;(cid:3)930.299100.014;0.407 962.00710;962872.2381022.248;174.050 9.863;10232.107 960.14310;96115.19610 (cid:3)930.00510;(cid:3)930.24010
3 3
3 (cid:3) 6 6 (cid:3)
0 0 0 0 0
1 1 1 1 1
9 9 9 9 9
2 69 6 6 3 51 6 5 5 4 0 5 6
4 07 9 5 4 85 4 8 1 5 3 5 3
1 10 0 1 1 03 0 0 0 7 8 1 0
0. 0.0. 0. 0. 0. 0.3. 0. 0. 2. 7. 8. 9. 0.
4 2 8 1
D 3 8
S 1
3 3
3 (cid:3) 6 6 (cid:3)
0 0 0 0 0
1 1 1 1 1
9 9 9 9 9
1 19 9 2 1 32 1 3 9 5 2 7 9
1 27 0 6 1 11 5 1 0 0 6 3 3
6 31 7 8 6 13 0 1 7 6 0 2 0
Root Mean 0. 0.0. 0. 0. 0. 0.3. 0. 0. 184. 62. 1079. 11. 0. nt.
a
species Range 0.308;0.822 0.092;0.4940.006;0.350 0.558;0.905 0.557;1.000 0.313;0.905 0.034;0.172930.33910;935.57210(cid:3)930.01210;(cid:3)930.345100.035;0.172 961.03710;96418.5171020.897;86.789 57.419;1236.012960.52210;9613.04810 (cid:3)930.000410;(cid:3)930.309610 est.ns,nonsignific
113 30 (cid:3)30 60 60 (cid:3)30 cet
otalof 04 7965 62 43 34 299401 9481 29 9871 56 81 9611 9411 nifican
t 1 00 0 1 1 00 0 0 6 7 4 7 0 g
a 0. 0.0. 0. 0. 0. 0.1. 0. 0. 7. 3. 4. 2. 0. si
g D 7 1 2 d
n S 2 n
nti sa
prese 310 (cid:3)310 610 610 (cid:3)310 atistic
re 9 9 9 9 9 st
dividuals, Branch Mean 0.608 0.2590.139 0.770 0.850 0.657 0.0921.931 0.066 0.092 64.802 50.117 352.661 4.310 0.051 edwithF
n147in (cid:3)1MPa eindicat
suredo Unit Nounit NounitNounit Nounit Nounit Nounit Nounit2lm (cid:3)2lnm Nounit 4lm 2lm 2lnm (cid:3)1kgs Nounit 147)ar
ea =
aotwoodtraitsm Function Mechanicalstrength,sapconductionPorosityCarbohydratestorageMechanicalstrengthMechanicalstrengthMechanicalstrengthSapconductionSapconduction Sapconduction Sapconduction Sapconduction Sapconduction Sapconduction Sapconduction Sapconduction mallroottraits(n
o s
mallr ation hand
ListofbranchandsTable1 TraitAbbrevi WoodspecificWSGgravity LumenfractionFlParenchymaFpfractionFiberfractionFf MeanfiberwallFmfwfractionTotalfiberwallFtfwfractionVesselfractionFvMeanvesselareaA VesseldensityN VessellumenFfractionVesselsizetoSnumberratioVesselmeanDmhhydraulicdiameterConductivityIkindexSpecificxylemKshydraulicconductivityVesselgroupVGIindex aDifferencesbetweenbranc
(cid:1)2013TheAuthors NewPhytologist(2014)202:79–94
NewPhytologist(cid:1)2013NewPhytologistTrust www.newphytologist.com
New
84 Research Phytologist
Table2 Pairwisecorrelationsaamongspeciesmeanbranchandsmallrootwoodtraits(n=113)
Branch
WSG Fl Fp Ff Fmfw Ftfw Fv A N F S Dmh Ik Ks VGI
Branch
WSG (cid:3)0.803 (cid:3)0.430 0.579 0.622 0.725 (cid:3)0.131 (cid:3)0.174 0.138 (cid:3)0.131 (cid:3)0.112 (cid:3)0.180 (cid:3)0.175 (cid:3)0.154 0.190
Fl (cid:3)0.844 0.530 (cid:3)0.752 (cid:3)0.713 (cid:3)0.858 0.180 0.164 (cid:3)0.106 0.180 0.084 0.166 0.180 0.162 (cid:3)0.153
Fp (cid:3)0.492 0.608 (cid:3)0.842 (cid:3)0.207 (cid:3)0.451 (cid:3)0.364 0.369 (cid:3)0.495 (cid:3)0.364 0.426 0.373 0.147 0.183 (cid:3)0.502
Ff 0.614 (cid:3)0.767 (cid:3)0.869 0.397 0.670 (cid:3)0.095 (cid:3)0.343 0.275 (cid:3)0.095 (cid:3)0.282 (cid:3)0.344 (cid:3)0.308 (cid:3)0.301 0.291
Fmfw 0.681 (cid:3)0.707 (cid:3)0.176 0.363 0.931 (cid:3)0.158 (cid:3)0.015 (cid:3)0.020 (cid:3)0.158 0.048 (cid:3)0.031 (cid:3)0.099 (cid:3)0.106 0.027
Ftfw 0.802 (cid:3)0.871 (cid:3)0.427 0.629 0.924 (cid:3)0.198 (cid:3)0.137 0.069 (cid:3)0.198 (cid:3)0.053 (cid:3)0.150 (cid:3)0.198 (cid:3)0.197 0.119
Fv (cid:3)0.158 0.164 (cid:3)0.324 (cid:3)0.063 (cid:3)0.311 (cid:3)0.278 (cid:3)0.134 0.559 1.000 (cid:3)0.370 (cid:3)0.146 0.293 0.203 0.541
A (cid:3)0.200 0.194 0.303 (cid:3)0.337 (cid:3)0.035 (cid:3)0.134 (cid:3)0.111 (cid:3)0.860 (cid:3)0.134 0.958 0.996 0.871 0.856 (cid:3)0.805
N 0.023 (cid:3)0.001 (cid:3)0.368 0.195 (cid:3)0.182 (cid:3)0.087 0.558 (cid:3)0.762 0.559 (cid:3)0.923 (cid:3)0.875 (cid:3)0.549 (cid:3)0.581 0.964
F (cid:3)0.158 0.164 (cid:3)0.324 (cid:3)0.063 (cid:3)0.311 (cid:3)0.278 1.000 (cid:3)0.111 0.558 (cid:3)0.370 (cid:3)0.146 0.293 0.203 0.541
S (cid:3)0.118 0.099 0.362 (cid:3)0.281 0.070 (cid:3)0.025 (cid:3)0.297 0.903 (cid:3)0.781 (cid:3)0.297 0.952 0.730 0.743 (cid:3)0.867
Dmh (cid:3)0.202 0.190 0.320 (cid:3)0.336 (cid:3)0.039 (cid:3)0.135 (cid:3)0.137 0.992 (cid:3)0.795 (cid:3)0.137 0.894 0.866 0.856 (cid:3)0.823
Ik (cid:3)0.205 0.186 0.125 (cid:3)0.282 (cid:3)0.092 (cid:3)0.173 0.220 0.888 (cid:3)0.521 0.220 0.709 0.879 0.934 (cid:3)0.502
Ks (cid:3)0.270 0.243 0.115 (cid:3)0.265 (cid:3)0.164 (cid:3)0.225 0.193 0.865 (cid:3)0.506 0.193 0.699 0.862 0.954 (cid:3)0.521
VGI 0.062 (cid:3)0.035 (cid:3)0.362 0.189 (cid:3)0.116 (cid:3)0.034 0.532 (cid:3)0.717 0.951 0.532 (cid:3)0.739 (cid:3)0.749 (cid:3)0.477 (cid:3)0.466
Root
WSG 0.437 (cid:3)0.483 (cid:3)0.164 0.345 0.448 0.509 (cid:3)0.266 (cid:3)0.141 (cid:3)0.043 (cid:3)0.266 (cid:3)0.023 (cid:3)0.134 (cid:3)0.180 (cid:3)0.221 (cid:3)0.043
Fl (cid:3)0.496 0.486 0.233 (cid:3)0.339 (cid:3)0.396 (cid:3)0.473 0.245 0.055 0.127 0.245 (cid:3)0.043 0.059 0.093 0.138 0.084
Fp (cid:3)0.167 0.190 0.378 (cid:3)0.363 0.017 (cid:3)0.102 (cid:3)0.068 0.336 (cid:3)0.251 (cid:3)0.068 0.320 0.330 0.291 0.227 (cid:3)0.281
Ff 0.211 (cid:3)0.193 (cid:3)0.199 0.287 0.094 0.200 (cid:3)0.207 (cid:3)0.113 (cid:3)0.024 (cid:3)0.207 (cid:3)0.041 (cid:3)0.107 (cid:3)0.112 (cid:3)0.094 (cid:3)0.011
Fmfw 0.537 (cid:3)0.532 (cid:3)0.039 0.177 0.779 0.691 (cid:3)0.296 0.018 (cid:3)0.224 (cid:3)0.296 0.140 0.006 (cid:3)0.035 (cid:3)0.121 (cid:3)0.149
Ftfw 0.558 (cid:3)0.545 (cid:3)0.160 0.324 0.638 0.633 (cid:3)0.373 (cid:3)0.085 (cid:3)0.161 (cid:3)0.373 0.038 (cid:3)0.093 (cid:3)0.149 (cid:3)0.213 (cid:3)0.118
Fv (cid:3)0.132 0.075 (cid:3)0.121 (cid:3)0.052 (cid:3)0.160 (cid:3)0.190 0.428 (cid:3)0.137 0.321 0.428 (cid:3)0.204 (cid:3)0.147 (cid:3)0.040 (cid:3)0.012 0.325
A 0.013 (cid:3)0.008 0.058 (cid:3)0.116 0.036 0.009 (cid:3)0.014 0.372 (cid:3)0.334 (cid:3)0.014 0.312 0.388 0.288 0.324 (cid:3)0.296
N (cid:3)0.100 0.084 (cid:3)0.184 0.074 (cid:3)0.208 (cid:3)0.184 0.415 (cid:3)0.535 0.680 0.415 (cid:3)0.521 (cid:3)0.564 (cid:3)0.337 (cid:3)0.349 0.622
F (cid:3)0.132 0.075 (cid:3)0.121 (cid:3)0.052 (cid:3)0.160 (cid:3)0.190 0.428 (cid:3)0.137 0.321 0.428 (cid:3)0.204 (cid:3)0.147 (cid:3)0.040 (cid:3)0.012 0.325
S 0.064 (cid:3)0.032 0.076 (cid:3)0.077 0.097 0.072 (cid:3)0.168 0.474 (cid:3)0.497 (cid:3)0.168 0.414 0.499 0.357 0.393 (cid:3)0.441
Dmh 0.012 (cid:3)0.008 0.056 (cid:3)0.110 0.040 0.016 (cid:3)0.035 0.383 (cid:3)0.362 (cid:3)0.035 0.313 0.404 0.300 0.338 (cid:3)0.329
Ik (cid:3)0.086 0.056 0.027 (cid:3)0.127 (cid:3)0.035 (cid:3)0.098 0.184 0.188 (cid:3)0.070 0.184 0.135 0.192 0.171 0.205 (cid:3)0.045
Ks (cid:3)0.066 0.050 0.015 (cid:3)0.133 (cid:3)0.065 (cid:3)0.095 0.228 0.176 (cid:3)0.056 0.228 0.102 0.187 0.172 0.220 (cid:3)0.031
VGI (cid:3)0.057 0.054 (cid:3)0.189 0.069 (cid:3)0.163 (cid:3)0.150 0.414 (cid:3)0.500 0.656 0.414 (cid:3)0.471 (cid:3)0.533 (cid:3)0.304 (cid:3)0.324 0.649
aSpearmancorrelationscoefficientsforspeciesdata(abovediagonal)andphylogeneticallyindependentcontrasts(belowdiagonal)areshowninboldtype
whensignificant,followingBonferroni-correctedalphavalues(P<5.37910(cid:3)5).SeeTable1fortraitabbreviations.
wallfraction(Ftfw=Ff9Fmfw),andvesselfraction(Fv);aswell
Dataanalysis
astotal(i.e.ofallwoodtissues)lumenfraction(Fl)asanindica-
tor of wood porosity. We determined vessel size (A, vessel mean Thefirststepofouranalysiswastoinvestigatehowwoodspecific
area; D , vessel mean major diameter; D , vessel mean minor gravityrelatestodifferentwoodanatomicaltraitsinbranchesand
1 2
diameter), vessel density (N, vessel number per unit area) and roots.Datawerenottransformedforthesakeofbetterinterpret-
vessel grouping index (GI, number of groups of vessels divided ability and comparison with other studies, so we used nonpara-
by vessel number) as defined by International Association of metrictests.
Wood Anatomists (Angyalossy Alfonso etal., 1989). We calcu- Toexaminethetrait-by-traitcorrelationsamongtraitsdefining
lated two metrics of vascular strategy related to xylem specific branch and small woody root tissues, we performed pairwise
conductivity: vessel lumen fraction (F=A9N: total cross-sec- Spearman correlation tests between (1) species means (n=113),
tionalareausedforsaptransport)andvesselsizetonumberratio and(2)individualvalues(n=147)using themeanvalueofeach
(S=A/N) (Zanne etal., 2010). We computed hydraulic-related trait for each of the 113 studied species. As correlation tests are
variables from vessel morphometric features. We calculated the sensitivetomissingdata,weusedthetraitmeansfromtheclosest
mean pffiPffiffiffiffiffiffiffiffiffiffiffiffiffiffihffiffiffiyffiffidffiffiffirffiaffiffiuffiffilffiffiifficffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi diameter as: taxonomiclevel(genusorfamily)whenbranchorrootdatawere
D ¼ 4 ð2D2D2=D2þD2Þ=n, where n is the number of missing(n=12and25,respectively).
mh 1 2 1 2
vessels. We used the Poiseuille law to estimate the conductivity We further examined the influence of species evolutionary
index as: I ¼N (cid:4)D4 . We also used the Hagen–Poiseuille histories on the observed correlations between groups of traits
k mh
by performing pairwise correlations between species mean traits
equation to calculate the theoretical specificPxylem hydraulic
conductivity as: Ks¼ðp=128gA Þ (cid:4) D2D2, where (n=113) including phylogenetically independent contrasts
g is water viscosity (1.002910(cid:3)c9roMsssePctaiosn(cid:3)1 at 20°C1) (2Tyree & (PICs). We recovered a phylogenetic tree for our 113 species
Ewers,1991). using the PHYLOMATIC v.3 utility (Webb & Donoghue, 2005),
NewPhytologist(2014)202:79–94 (cid:1)2013TheAuthors
www.newphytologist.com NewPhytologist(cid:1)2013NewPhytologistTrust
New
Phytologist Research 85
Root
WSG Fl Fp Ff Fmfw Ftfw Fv A N F S Dmh Ik Ks VGI
0.479 (cid:3)0.529 (cid:3)0.245 0.266 0.493 0.551 (cid:3)0.077 (cid:3)0.052 0.053 (cid:3)0.077 (cid:3)0.074 (cid:3)0.048 (cid:3)0.078 (cid:3)0.050 0.098
(cid:3)0.497 0.505 0.199 (cid:3)0.206 (cid:3)0.509 (cid:3)0.528 0.028 (cid:3)0.033 (cid:3)0.025 0.028 (cid:3)0.016 (cid:3)0.019 (cid:3)0.007 (cid:3)0.028 (cid:3)0.051
(cid:3)0.264 0.234 0.424 (cid:3)0.243 (cid:3)0.017 (cid:3)0.147 (cid:3)0.140 0.148 (cid:3)0.288 (cid:3)0.140 0.256 0.147 0.024 0.020 (cid:3)0.297
0.431 (cid:3)0.379 (cid:3)0.364 0.333 0.203 0.341 (cid:3)0.056 (cid:3)0.153 0.137 (cid:3)0.056 (cid:3)0.170 (cid:3)0.160 (cid:3)0.133 (cid:3)0.121 0.149
0.483 (cid:3)0.427 (cid:3)0.020 0.112 0.685 0.581 (cid:3)0.061 (cid:3)0.005 (cid:3)0.018 (cid:3)0.061 0.004 (cid:3)0.009 (cid:3)0.027 (cid:3)0.018 0.028
0.544 (cid:3)0.498 (cid:3)0.125 0.217 0.625 0.603 (cid:3)0.101 (cid:3)0.063 0.017 (cid:3)0.101 (cid:3)0.047 (cid:3)0.071 (cid:3)0.092 (cid:3)0.077 0.060
(cid:3)0.152 0.208 (cid:3)0.130 (cid:3)0.142 (cid:3)0.236 (cid:3)0.281 0.388 (cid:3)0.034 0.370 0.388 (cid:3)0.228 (cid:3)0.026 0.203 0.182 0.366
(cid:3)0.187 0.042 0.260 (cid:3)0.080 0.063 0.015 (cid:3)0.148 0.432 (cid:3)0.564 (cid:3)0.148 0.568 0.438 0.177 0.199 (cid:3)0.538
0.127 (cid:3)0.022 (cid:3)0.307 0.068 (cid:3)0.100 (cid:3)0.060 0.257 (cid:3)0.401 0.625 0.257 (cid:3)0.585 (cid:3)0.398 (cid:3)0.097 (cid:3)0.115 0.617
(cid:3)0.152 0.208 (cid:3)0.130 (cid:3)0.142 (cid:3)0.236 (cid:3)0.281 0.388 (cid:3)0.034 0.370 0.388 (cid:3)0.228 (cid:3)0.026 0.203 0.182 0.366
(cid:3)0.110 (cid:3)0.043 0.254 (cid:3)0.012 0.131 0.109 (cid:3)0.239 0.414 (cid:3)0.619 (cid:3)0.239 0.592 0.418 0.108 0.139 (cid:3)0.590
(cid:3)0.193 0.070 0.279 (cid:3)0.106 0.035 (cid:3)0.016 (cid:3)0.143 0.445 (cid:3)0.570 (cid:3)0.143 0.580 0.452 0.190 0.211 (cid:3)0.548
(cid:3)0.233 0.111 0.176 (cid:3)0.108 (cid:3)0.040 (cid:3)0.085 (cid:3)0.004 0.375 (cid:3)0.384 (cid:3)0.004 0.441 0.388 0.231 0.237 (cid:3)0.364
(cid:3)0.186 0.112 0.198 (cid:3)0.123 (cid:3)0.076 (cid:3)0.102 (cid:3)0.008 0.319 (cid:3)0.339 (cid:3)0.008 0.394 0.330 0.199 0.217 (cid:3)0.314
0.145 (cid:3)0.090 (cid:3)0.326 0.090 (cid:3)0.039 0.002 0.229 (cid:3)0.390 0.594 0.229 (cid:3)0.550 (cid:3)0.391 (cid:3)0.104 (cid:3)0.117 0.624
(cid:3)0.684 (cid:3)0.259 0.466 0.442 0.631 (cid:3)0.272 (cid:3)0.386 0.185 (cid:3)0.272 (cid:3)0.348 (cid:3)0.379 (cid:3)0.362 (cid:3)0.370 0.242
(cid:3)0.689 0.417 (cid:3)0.682 (cid:3)0.534 (cid:3)0.830 0.362 0.307 (cid:3)0.066 0.362 0.243 0.315 0.374 0.344 (cid:3)0.152
(cid:3)0.096 0.372 (cid:3)0.615 0.018 (cid:3)0.291 (cid:3)0.260 0.176 (cid:3)0.381 (cid:3)0.260 0.355 0.173 (cid:3)0.017 0.012 (cid:3)0.423
0.489 (cid:3)0.732 (cid:3)0.519 0.131 0.619 (cid:3)0.518 (cid:3)0.499 0.023 (cid:3)0.518 (cid:3)0.327 (cid:3)0.504 (cid:3)0.609 (cid:3)0.586 0.094
0.431 (cid:3)0.482 0.043 0.103 0.817 (cid:3)0.149 (cid:3)0.019 (cid:3)0.075 (cid:3)0.149 0.032 (cid:3)0.023 (cid:3)0.092 (cid:3)0.073 (cid:3)0.021
0.617 (cid:3)0.808 (cid:3)0.239 0.576 0.793 (cid:3)0.396 (cid:3)0.284 (cid:3)0.006 (cid:3)0.396 (cid:3)0.164 (cid:3)0.295 (cid:3)0.389 (cid:3)0.363 0.073
(cid:3)0.459 0.490 (cid:3)0.250 (cid:3)0.587 (cid:3)0.230 (cid:3)0.488 0.436 0.458 1.000 (cid:3)0.003 0.444 0.826 0.759 0.394
(cid:3)0.421 0.290 0.024 (cid:3)0.416 0.003 (cid:3)0.261 0.427 (cid:3)0.524 0.436 0.865 0.993 0.840 0.867 (cid:3)0.556
0.014 0.099 (cid:3)0.271 (cid:3)0.034 (cid:3)0.225 (cid:3)0.133 0.363 (cid:3)0.520 0.458 (cid:3)0.830 (cid:3)0.525 (cid:3)0.028 (cid:3)0.114 0.973
(cid:3)0.459 0.490 (cid:3)0.250 (cid:3)0.587 (cid:3)0.230 (cid:3)0.488 1.000 0.427 0.363 (cid:3)0.003 0.444 0.826 0.759 0.394
(cid:3)0.303 0.213 0.165 (cid:3)0.256 0.030 (cid:3)0.165 0.080 0.835 (cid:3)0.737 0.080 0.849 0.496 0.563 (cid:3)0.836
(cid:3)0.404 0.291 0.022 (cid:3)0.408 0.013 (cid:3)0.254 0.405 0.981 (cid:3)0.551 0.405 0.819 0.839 0.863 (cid:3)0.557
(cid:3)0.470 0.431 (cid:3)0.051 (cid:3)0.588 (cid:3)0.070 (cid:3)0.392 0.741 0.846 (cid:3)0.152 0.741 0.567 0.803 0.974 (cid:3)0.081
(cid:3)0.467 0.391 (cid:3)0.076 (cid:3)0.539 (cid:3)0.109 (cid:3)0.408 0.700 0.863 (cid:3)0.194 0.700 0.597 0.827 0.958 (cid:3)0.168
0.056 0.030 (cid:3)0.276 (cid:3)0.007 (cid:3)0.160 (cid:3)0.077 0.338 (cid:3)0.531 0.969 0.338 (cid:3)0.733 (cid:3)0.572 (cid:3)0.166 (cid:3)0.212
based on the Davies etal. (2004) phylogenetic hypothesis for the effect of habitat and lineage (15 most abundant species and
relationships among angiosperm families, with polytomies seven focal monophyletic lineages) on individual values of wood
applied within most families and genera. For this analysis, specificgravityandanatomyinbranchesandroots.Whenneces-
branch lengths were scaled to 1. PICs were calculated as the sary, we performed post hoc tests (Tukey’s HSD test) to identify
difference in mean trait values for pairs of sister species and variationamonghabitatsorlineages.
nodes (Coomes & Grubb, 1996). AllanalyseswereconductedintheR2.15.3statisticalplatform
To illustrate the correlations both within and among branch (R Development Core Team, 2011), using the packages ADE4
and root wood traits, we performed a principal components (Ellers etal., 2011), APE (Coomes & Grubb, 1996) and VEGAN
analysis(PCA)onspeciesmeantraits.Weconductedthisanalysis (Dixon,2003).
both with and without the PICs to account for the influence of
species evolutionary histories. Additionally, we tested for differ-
Results
ences between branch and root traits using analysis of variance
(ANOVA)withorganasanindependentvariable. Pairwise correlations between species mean traits showed that
To test the generality of the correlation patterns between wood specific gravity was strongly correlated between branches
branchandrootwoodtraitsacrossthethreecontrastinghabitats, and roots (Table2). We found strong patterns of coordination
we performed a PCA on individual traits measured in each plot amongbranchtraits,withspeciesexhibitinghighbranchspecific
andperformedManteltestsforsimilarityofpairwisetraitcorrela- woodgravity alsoshowing highfiberandfiberwallfractionsbut
tionmatricesamongthesixplots. low lumen and parenchyma fractions, while branch vessel traits
Thesecondstepofouranalysiswastoexaminehowwoodspe- varied independently (Table2, Fig.2a,c,e). Species with high
cific gravity and anatomy vary between habitats as well as root specific wood gravity similarly had high fiber and fiber wall
between species. We conducted two-way ANOVA to examine fractionsbutalowlumenfractionandsmallvesselsizeandvessel
(cid:1)2013TheAuthors NewPhytologist(2014)202:79–94
NewPhytologist(cid:1)2013NewPhytologistTrust www.newphytologist.com
New
86 Research Phytologist
(a) (b)
(c) (d)
(e) (f)
Fig.2 Relationshipsbetweenwoodspecificgravity(WSG)andmeanvesselarea(a,b),lumen(c,d)andfiberwall(e,f)fractionsinbranchesandsmall
woodyrootsin113tropicaltreespecies.Spearmancorrelationcoefficients(R)aregivenwithsignificancetest(***,P<0.001;ns,nonsignificant).When
correlationsweresignificantbothwithandwithoutincludingphylogeneticallyindependentcontrasts,ordinaryleast-squaresregressionlinesweredrawn.
Colorsindicateoursevenfocalphylogeneticlineages(red,Eschweilera;yellow,Inga;green,Licania;cyan,Micropholis;blue,Bombacoideae(Pachira);
purple,Protium;pink,Swartzia),whilecommonspeciesareindicatedinblack.
mean hydraulic diameter (Table2, Fig.2b,d,f). The matrices of WhenPICswereincludedinthepairwisecorrelationsbetween
pairwise trait correlations between species means and between species mean traits, the patterns of correlations among branch
individual values showed similar patterns (R =0.99; and root wood traits were generally conserved (Table2). The
Mantel
P<0.0001). matrices of pairwise correlations between species mean traits
NewPhytologist(2014)202:79–94 (cid:1)2013TheAuthors
www.newphytologist.com NewPhytologist(cid:1)2013NewPhytologistTrust
New
Phytologist Research 87
(a) (b)
Fig.3 Principalcomponentsanalysis(PCA)onbranchandsmallwoodyrootwoodtraitmeansin113tropicaltreespecies:(a)correlationcircleofdataand
(b)individualfactormapofdatawithoutphylogeneticallyindependentcontrasts.In(a),stemwoodtraitsareshowningray,whilerootwoodtraitsare
showninblack.In(b),colorsindicateoursevenfocalphylogeneticlineages(red,Eschweilera;yellow,Inga;green,Licania;cyan,Micropholis;blue,
Bombacoideae(Pachira);purple,Protium;pink,Swartzia),whilecommonspeciesareindicatedinblack.SeeTable1fortraitabbreviations.
determined with and without PICs were similar (R =0.98; supported by the consistency of the three PCA axes along broad
Mantel
P<0.0001). Hence there seems to be no effect of species evolu- environmentalgradients.
tionaryhistoryonthecorrelationpatternsamongtraitsrelatedto Species in white sand plots exhibited higher wood specific
branchandrootwoodtissues. gravity of both branches and roots than those in terra firme and
The multivariate analysis of trait correlations showed that seasonallyfloodedplots;whereasspeciesinterrafirmehadhigher
branch and woody root traits defined three major axes (Fig.3a). wood specific gravity of both branches and roots than those in
The first PCAaxis (29.82%)was defined bycoordinated branch seasonally flooded plots(Table3, Fig.4a,b). Similarly, speciesin
andwoodyrootvesseltraits,opposingwoodwithlargevessels,in white sand plots exhibited higher branch fiber, mean fiber wall
terms of area and hydraulic diameter, and vessel size to number and total fiber fractions, but lower branch and root parenchyma
ratioagainstwoodwithhighvesseldensityandhighvesselgroup- fractions and branch lumen fraction than those in seasonally
ingindex.Thesecondaxis ofthePCA(20.41%) wasdefined by flooded plots (Fig.4c–f; see Fig. S1 for complete results). How-
coordinatedrootwoodtraitsrelatedtotissuestructure,opposing ever,mostanatomicaltraitsrelatedtovesselsdidnotvaryamong
wood with high root specific wood gravity and fiber and fiber thethreehabitats(Table3,Fig.S1).
wallfractionsagainstwoodwithhighrootlumenandvesselfrac- We found a strong effect of lineage on branch specific wood
tions as well as a high root vessel lumen fraction. The third axis gravity as well as on branch and woody root anatomy, with sig-
of the PCA (15.80%) was defined by coordinated branch wood nificantdifferencesamongphylogeneticlineagesforalltraits,but
traitsrelatedtotissuestructure,opposingwoodwithhighbranch without any interactions with habitat for most traits (Table3,
specific wood gravity and fiber and fiber wall fractions against Figs3b,4;seeFig.S2forcompleteresults).Forinstance,Licania
woodwithahighbranchlumenfraction. speciesexhibited higher branch specific wood gravity (Fig.5a)as
WhenPICswereincludedinthePCA,thepatternsofcorrela- well as higher branch and root fiber and fiber wall fractions
tions among branch and root wood traits were consistent (Fig.5e,f) but lower branch and root lumen fractions (Fig.5c,d)
(Table2), further confirming that phylogeny was not a strong thanspecies fromotherlineages.Protiumspecieshadhigherves-
predictoroftheobservedpatternsbetweenbranchandrootwood sel fraction and vessel grouping in branches and roots than most
traits. Moreover, we found no differences between branch and otherlineages(Fig.S2).Ingaspeciesexhibitedhigherbranchves-
rootwoodanatomicaltraits(Table1). sel size, but lower branch vessel density than most Micropholis,
The matrices of pairwise correlations between branch and Protiumandcommonspecies(Fig.S2).Bombacoideae(Pachira)
woody root traits were similar among the six plots representing specieshadhighervesselsizeandvesselmeanhydraulicdiameter
the steep gradient of environmental conditions found in French inrootsthanmostMicropholisspecies(Fig.S2).Ingeneral,con-
Guiana (Supporting Information Table S1). The generality of generic species had very similar values across different habitat
coordination patterns of branch and woody root traits was types,andwefoundthattheproportionofvarianceexplainedby
(cid:1)2013TheAuthors NewPhytologist(2014)202:79–94
NewPhytologist(cid:1)2013NewPhytologistTrust www.newphytologist.com
New
88 Research Phytologist
Table3 Influenceofhabitat,lineageandtheirinteractiononbranchandsmallrootwoodtraits(n=147)
Habitat Lineage
Seasonally Common
Trait x² F flooded Terrafirme Whitesand x² F species Eschweilera
Branch WSG 35.73 13.41*** 0.562bc 0.604b 0.665a 33.13 4.29*** 0.604b 0.643b
Fl 13.11 5.13** 0.285b 0.254ab 0.237a 37.54 4.38*** 0.265a 0.214ab
Fp 22.50 6.42** 0.162a 0.138ab 0.114b 19.33 2.40* 0.139ab 0.161ab
Ff 16.36 5.52** 0.748b 0.773ab 0.789a 25.37 3.00** 0.770a 0.766ab
Fmfw 14.03 8.58*** 0.806b 0.843ab 0.908a 56.62 9.74*** 0.843b 0.945ab
Ftfw 19.45 11.06*** 0.605b 0.656ab 0.716a 42.63 7.30*** 0.652b 0.727ab
Fv 1.63 1.48ns 0.090a 0.089a 0.098a 57.13 5.80*** 0.091b 0.073b
A 2.94 1.72ns 2.1339103a 1.8999103a 1.7479103a 53.66 4.75*** 1.7629103b 1.8279103ab
N 8.47 2.83† 0.055910(cid:3)3a 0.067910(cid:3)3a 0.078910(cid:3)3a49.58 4.06*** 0.071910(cid:3)3a 0.043910(cid:3)3ab
F 1.63 1.48ns 0.090a 0.089a 0.098a 57.13 5.80*** 0.091b 0.073b
S 0.34 0.92ns 75.2549106a 64.3409106a 53.6329106a 62.49 5.10*** 51.5859106b 51.5439106b
Dmh 4.74 2.29ns 53.195a 49.553a 47.438a 55.94 5.34*** 47.619b 49.813ab
Ik 0.38 1.08ns 391.250a 333.592a 336.093a 24.86 2.54* 322.890b 279.867ab
Ks 5.26 2.22ns 4.9779106a 4.0639106a 3.9069106a 24.45 2.62* 3.8929106a 2.9629106a
VGI 7.78 2.60† 0.041910(cid:3)3a 0.053910(cid:3)3a 0.060910(cid:3)3a45.88 3.70** 0.053910(cid:3)3ab 0.032910(cid:3)3b
Root WSG 41.93 9.43*** 0.542b 0.616a 0.676a 9.48 1.55ns 0.596a 0.622a
Fl 3.81 2.43† 0.349a 0.311a 0.308a 45.42 5.86*** 0.352ab 0.303ab
Fp 12.12 3.36* 0.195a 0.185ab 0.151b 50.49 3.81** 0.191a 0.203ab
Ff 1.14 0.77ns 0.708a 0.699a 0.724a 50.50 3.90*** 0.704ab 0.699ab
Fmfw 4.59 2.54† 0.820a 0.872a 0.889a 63.59 7.10*** 0.828b 1.000a
Ftfw 3.58 2.33ns 0.880a 0.852a 0.866a 60.02 7.38*** 0.866a 0.802a
Fv 0.75 1.19ns 0.097a 0.115a 0.125a 58.56 5.06*** 0.105b 0.098b
A 2.15 0.38ns 3.4649103a 3.4419103a 2.9239103a 19.76 2.63* 2.9319103b 4.1479103ab
N 2.91 1.50ns 0.041910(cid:3)3a 0.055910(cid:3)3a 0.056910(cid:3)3a54.20 3.66** 0.057910(cid:3)3ab 0.033910(cid:3)3b
F 0.75 1.19ns 0.097a 0.115a 0.125a 58.56 5.06*** 0.105b 0.098b
S 2.16 2.60† 203.1959106a 220.599106a 102.8119106a 20.86 5.40*** 155.7919106b 261.7929106ab
Dmh 4.13 0.15ns 62.760a 63.225a 60.225a 25.71 2.52* 58.072ab 70.198ab
Ik 3.69 0.13ns 1099.217a 1140.331a 951.712a 19.68 2.33* 855.030b 1319.942ab
Ks 2.29 0.30ns 10.8869106a 12.4199106a 9.5919106a 12.81 2.12* 8.7419106a 13.9639106a
VGI 2.66 1.43ns 0.031910(cid:3)3 0.042910(cid:3)3 0.043910(cid:3)3 54.17 3.50** 0.042910(cid:3)3b 0.024910(cid:3)3b
Proportionsofvarianceexplainedbyeachfactor(x²)areindicated;Fstatisticsareshownwithsignificancetest(†,0.05<P<0.07;*,P<0.05;**,P<0.01;
***,P<0.001;ns,nonsignificant).MeansforeachhabitatandlineageareindicatedwithposthocTukey’sHSD(HonestlySignificantDifference)testin
boldletters.SeeTable1fortraitabbreviations.
habitattypewaslowerthantheproportionofvarianceexplained variations in vessel and parenchyma fractions. Thus, wood spe-
bylineageformostanatomicaltraits(Table3). cific gravity of both branches and roots of tropical tree species
mostly depends on the cell wall thickness of fibers, as found in
previousstudiesincludingallwoodanatomicalelementsofstems
Discussion
or roots in Mediterranean, temperate and tropical species
(Jacobsenetal.,2007a;Prattetal.,2007;Martinez-Cabreraetal.,
Relationshipsamongwoodspecificgravityandwood
2009; Schuldt etal., 2013). Previous findings linked increasing
anatomyinbranchesandroots
wood mechanical strength with increasing cavitation resistance:
Ourstudyhelpstorevealhowwoodanatomicaltraitscontribute mechanical reinforcement of vessels by the neighboring fiber
to wood specific gravity in both aboveground and belowground matrix can indeed play an important role in avoiding vessel col-
woody systems of tree species across broad environmental gradi- lapseundernegativepressure(Hackeetal.,2001;Jacobsenetal.,
ents in lowland Amazonian forests. Our hypotheses were that 2005,2007b;Prattetal.,2007;Lensetal.,2011).
wood specific gravity would decrease with increasing vessel frac- At the organ level, we observed that branches and roots dif-
tion(Prestonetal.,2006),butincreasewithincreasingfiberfrac- fered in how wood specific gravity related to anatomical wood
tion (Poorter etal., 2010). We measured 15 branch and small traits involved in sap transport. Contrary to our expectation, we
woody root wood traits pertaining to conduction, support and foundnorelationshipbetweenwoodspecificgravityandvascular
storage functions in 147 individuals representing 113 species traits at the branch level, suggesting no tradeoff between wood
across three contrasting habitats in French Guiana. We found specificgravityandconductioncapacity in branches.Ourresults
thatincreasesinwoodspecificgravityofbothbranchesandroots differfromthoseofpreviousstudiesconductedatrelativelysmall
of tropical tree species were largely driven by decreasing lumen spatial scales that showed that stem wood specific gravity related
faction andincreasing fiberandfiberwall fractions,regardlessof tovesselandvessellumenfractions(Baltzeretal.,2009;Gleason
NewPhytologist(2014)202:79–94 (cid:1)2013TheAuthors
www.newphytologist.com NewPhytologist(cid:1)2013NewPhytologistTrust