Spatial trends in leaf size of Amazonian rainforest trees

14 Pages·2009·1.56 MB·English

Biogeosciences,6,1563–1576,2009
Biogeosciences
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©Author(s)2009. Thisworkisdistributedunder
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Spatial trends in leaf size of Amazonian rainforest trees
A.C.M.Malhado1,*,Y.Malhi1,**,R.J.Whittaker1,**,R.J.Ladle1,**,H.terSteege2,**,***,O.L.Phillips3,**,***,
N.Butt1,**,L.E.O.C.Araga˜o1,***,C.A.Quesada3,***,A.Araujo-Murakami4,***,L.Arroyo4,***,J.Peacock3,***,
G.Lopez-Gonzalez3,***,T.R.Baker3,***,L.O.Anderson1,**,S.Almeida5,***,N.Higuchi6,***,T.J.Killeen7,***,
A.Monteagudo8,***,D.Neill9,***,N.Pitman10,***,A.Prieto11,***,R.P.Saloma˜o5,***,R.Va´squez-Mart´ınez8,***,and
W.F.Laurance6,***
1SchoolofGeographyandtheEnvironment,OxfordUniversity,UK
2Dept.ofPlantEcologyandBiodiversity,UtrechtUniversity,TheNetherlands
3EarthandBiosphereInstitute,SchoolofGeography,UniversityofLeeds,UK
4MuseoNoelKempffMercado,SantaCruz,Bolivia
5MuseuParaenseEmilioGoeldi,Bele´m,Brazil
6InstitutoNationaldePesquisasAmazoˆnicas,Manaus,Brazil
7CenterforAppliedBiodiversityScience,ConservationInternational,Washington,DC,USA
8HerbarioVargas,UniversidadNacionalSanAntonioAbaddelCusco,Cusco,Peru´
9HerbarioNacionaldelEcuador,Quito,Ecuador
10CenterforTropicalConservation,DukeUniversity,Durham,USA
11InstitutodeInvestigacio´ndeRecursosBiolo´gicosAlexandervonHumboldt,Bogota´ DC,Colombia
*Conceivedthestudy,collectedleafdata,undertooktheanalysis,wrotemanuscript.
**Developedtheidea,reviewedandimprovedmanuscript.
***Provideddata.
Received: 17December2008–PublishedinBiogeosciencesDiscuss.: 23February2009
Revised: 17June2009–Accepted: 3August2009–Published: 10August2009
Abstract. Leafsizeinfluencesmanyaspectsoftreefunction of such trees in the northwest of the region. Spatially cor-
such as rates of transpiration and photosynthesis and, con- rectedregressionsrevealweakcorrelationsbetweenthepro-
sequently, often varies in a predictable way in response to portionoflarge-leavedspeciesandmetricsofwateravailabil-
environmental gradients. The recent development of pan- ity. Wealsofindasignificantnegativerelationshipbetween
Amazonian databases based on permanent botanical plots leafsizeandwooddensity.
hasnowmadeitpossibletoassesstrendsinleafsizeacross
environmental gradients in Amazonia. Previous plot-based
studieshaveshownthatthecommunitystructureofAmazo-
1 Introduction
niantreesbreaksdownintoatleasttwomajorecologicalgra-
dientscorrespondingwithvariationsinsoilfertility(decreas-
Leaf size is one of the most plastic traits of a tree and it is
ing from southwest to northeast) and length of the dry sea-
notuncommontoseegreatvariabilitywithingenera,species,
son(increasingfromnorthwesttosouthandeast). Herewe
individuals within a species, and even between the same
describe the geographic distribution of leaf size categories
individual at different stages of development (e.g. sapling,
based on 121plots distributed across eight South American
canopy tree) or on different parts of the same tree (e.g. sun
countries. WefindthattheAmazonforestispredominantly
versus shade leaves). Despite this very large variation it is
populated by tree species and individuals in the mesophyll
often possible to detect significant associations between a
size class (20.25–182.25cm2). The geographic distribution
rangeofenvironmentalvariablesandleafsize. Forexample,
ofspeciesandindividualswithlargeleaves(>20.25cm2)is
Givnish (1987) reviewed comparative studies of leaf form
complexbutisgenerallycharacterizedbyahigherproportion
and concluded that effective leaf size – the width of a leaf
oritslobesorleaflets–increasesalonggradientsofincreas-
ingrainfall,humidityand/orsoilfertility,anddecreaseswith
Correspondenceto: A.C.M.Malhado increasing irradiance. Leaf size also tends to decrease with
([email protected]) increasingelevation onmountains inregions receivinghigh
PublishedbyCopernicusPublicationsonbehalfoftheEuropeanGeosciencesUnion.
1564 A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees
rainfall at low elevation, and to increase and then decrease words,manydifferentleafsizestrategiesfrequentlyco-exist
with elevation in more arid regions. Givnish (1987) also in physically similar environments. It is likely that within-
observed that older plants often possess smaller leaves than site (or within plot) variation in leaf size arises because the
youngeronesofthesamespecies. ecologicalopportunitiesforeachspeciesarealsostronglyde-
The existence of broad-scale (macrogeographic) pendentontheotherspeciespresentinthecommunity(West-
environment-leaf size correlations probably reflect the oby et al., 2002). Thus, the ability of a species to establish
evolutionary response of this trait to its environment successfullyinahabitatmaybedependentuponwhichother
(Givnish, 1987; Westoby et al., 2002). The size of leaves species are present and may be influenced by other traits
onatreecanthereforebeproductivelyconsideredasa“so- apartfromleafformandsize. Thesecomplextrade-offsand
lution” to the complex environmental “problems” of, most the multiple selective pressures on leaf size have generated
notably, light capture for photosynthesis (Falster and West- considerablediversityinthistrait,evenbetweenecologically
oby, 2003), economics of gas and water vapour exchange similarspecies(Ackerly,1996).
(Givnish and Vermeij, 1976; Givnish, 1984), avoidance of Care should also be taken not to interpret everything
heatstressfromintensesunlight,mechanicalstability(West- purely in terms of optimisation of a single trait (leaf size)
obyetal.,2002),anddefenceagainstherbivores(Molesand sincedevelopmentalandphysiologicalconstraintsandtrade-
Westoby, 2000). Certainlythesizeofaleafisbynomeans offs(cf.Dawkins,1982)mayalsoplayaroleindetermining
ecologically trivial since, as Givnish (1987) points out, leaf leaf size. This is clearly illustrated by the associations be-
sizevariationwillhaveadirecteffectonwhole-plantgrowth tweenleafsizeandcanopyarchitectureandbranchingmor-
rate,mainlythroughsize-relatedchangesintheconductance phology(MidgleyandBond,1989;AckerlyandDonoghue,
of the boundary layer, which affects heat exchange, uptake 1998). Furthermore,theselattertraitsmay,inturn,influence
ofcarbondioxideandlossofwatervapour. leafsizeevolutionindependentofecophysiologicalfunction
Leaf size theory predicts that the costs and benefits of (Ackerly and Reich, 1999). An example of the importance
a “large leaf” or a “small leaf” strategy should vary in a of such trade-offs could be the commonly observed neg-
predictable way with environmental parameters such as hu- ative relationship between wood density and leaf size (re-
midity, water availability, and soil fertility (Parkhurst and viewed in Wright et al., 2007). The explanation for this re-
Loucks, 1972; Givnish and Vermeij, 1976; Givnish, 1978, lationship is still uncertain but may relate to the higher hy-
1979, 1984; Westoby et al., 2002). Larger leaves have a draulic conductivity of trees with low-density wood that al-
thickerboundarylayerofslow-moving,non-turbulentairand lowsthemtodeployalargertotalleafareaperstem(Wright
slower convective heat loss and therefore tend to be hotter et al., 2007). Alternatively, this relationship is perhaps re-
thanambientairtemperaturewhenexposedtonetincoming latedtothe“pioneer-climax”treegradientormaybedueto
radiation. This can be disadvantageous, especially in areas co-varyingfactorsthatdonotdirectlyinteractandarethere-
wherewaterislimiting,becauseitmayleadtohigherratesof foredifficulttoidentify. However, thefactthatthereisstill
respirationanddecreasedratesofphotosynthesis(Lloydand considerablevariationinleafsizebetweenspecieswithsimi-
Farquhar, 2008) through the following mechanism: higher larwooddensitiessuggeststhatthisisbynomeansthewhole
leaftemperaturescauseahigherwatervapourdeficitthat,in story.
turn, leads to increased transpiration/water loss. The plant Despite the fact that ecologists have had a long-standing
adaptivelyrespondstothisbyclosingstomata,whichhasthe interest in explaining variations in leaf size between, and
net effect of reducing CO uptake and reducing the rate of within, species and habitats it is still a subject that appears
2
photosynthesis. Reduced water availability might therefore farfromresolution. Forinstance,Westobyetal.(2002)con-
be expected to favour smaller leaves (Givnish, 1987). With sidertheleafsize–twigsizespectrumofecologicalvariation
respect to soil fertility, trees growing in oligotrophic (low asbeingfundamentaltoourunderstandingofthetextureand
nutrient) soils may, all other things being equal, be limited function of forest canopies, but acknowledge that the costs
in their rate of construction of photosynthetic enzymes and andbenefitsoflargeversussmallleafandtwigsizearestill
therefore benefit less from temperature-related increases in poorly understood. Ackerly and Reich (1999, p. 1279) also
photosynthetic metabolism – once again favouring the evo- feel obliged to admit that, “variation (in leaf size) among
lution and development of smaller leaves (Givnish, 1984, specieswithinhabitatsisstillpoorlyexplained”.
1987). However,predictionssuchastheseneedtobetreated Givnish (1987), in his agenda-setting review of compar-
with caution and may not hold true under all circumstances ative studies in leaf form, suggests two methodological ap-
since leaves may have other adaptations (e.g. sclerophylly) proaches that may lead towards a better understanding of
that strongly influence the optimal leaf size strategy under leafsize. Firstly,in-depthphysiologicalstudiesmaybeable
anyparticularsetofenvironmentalconditions. to tease apart the various constraints and trade-offs that af-
The complex nature of the relationship between environ- fect leaf size (e.g. Parkhurst and Loucks’ (1972) general
mentandleafsizeisalsoreflectedbytheconsiderablevari- eco-physiological model of leaf size). Secondly, broader
ationinleafsizethatcanbeobservedwithinareaswithsim- comparative studies are required, since the more intensive
ilar macroclimatic conditions (Cornelissen, 1999). In other physiologically-basedapproacheswillnecessarilybesubject
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A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees 1565
tobiasesstemmingfromarangeofgeneticinfluencessuchas notalldatawereavailableforallplots,soplotslackingrel-
linkage,epistasisandpleiotropythatarepeculiartothestudy evantenvironmentaldatawereremovedfromcertainanaly-
population,inadditiontoanyinfluenceofnaturalselection. ses. 20plotswerealsoexcludedfromthestudybecausethey
In this paper we adopt the broader comparative approach had>30%ofspeciesthatwereeitherunidentifiedatspecies
advocated by Givnish (1987). With the recent creation of level(475speciesfromentiredatabase)orforwhichherbar-
verylargedatabasesofAmazoniantreesbasedonpermanent ium/flora data were not available (61species). As a conse-
plotsscatteredthroughouttheAmazonregionithasnowbe- quence, the number of plots included in the analyses varied
come possible to conduct a comprehensive study of broad from 51 to 121. The database at the time of extraction for
scalepatternsofleafsizevariationwithinthelargestblockof thisstudy(August2006)contained111123individualtrees
rainforestintheworld.Here,weusetheRAINFORdatabase (≥100mmDBH)from3324species.
of121permanentplotsto:1)describethespatialdistribution The plots used in this study span local and regional en-
ofleafsizecategoriesacrosstheAmazonBasinandGuyana vironmental gradients that naturally occur in Amazonia, in-
Shield,and; 2)investigatetheenvironmentalfactorsdriving cluding mature forests that are seasonally flooded, water-
regionalscalepatternsinleafsize. Wedothistogainfurther logged and non-flooded lowland terra firme forests (88%
insightsintotheecologicalsignificanceofleafsizeandim- of plots) on both clay-rich and white-sand substrates. All
proveourunderstandingofthefunctioningoftheAmazonian sites consisted of an apparently mature old-growth for-
rainforest. est with natural gap-phase dynamics and a canopy dom-
Specifically,weseekanswerstothefollowingquestions: inated by non-pioneer species. None of the plots is be-
lieved to have experienced any recent human-caused dis-
– Which leaf size categories dominate the canopy of the turbance. The individual plots range in size from 0.25 to
Amazonrainforest? 9ha (1.17ha±1.04=mean±SD) and in total encompass
141.5ha of forest. The density of stems per plot (includ-
– Are there spatial patterns in leaf size distribution in ing undetermined stems) ranged from 265 to 1307perha
Amazonia? (672±167perha=mean±SD).
To this existing database, information was added on leaf
– Arethefrequenciesofdifferentleafsizecategoriesas-
size for each species (2788) using digital images from flo-
sociated with environmental variables that reflect their
ras and herbaria (Table 1). A digital image, representing
adaptivefunction(e.g.rainfall,soilfertility,andlength
an average leaf for a particular species, was located us-
ofdryseason)?
ing a number of online herbaria. Leaf-size was determined
from the herbarium or flora specimen using the geometric
– Areleafsizecategoriesassociatedwiththegrowthstrat-
leaf-size classification of Raunkiaer (1934) as modified by
egyoftrees?
Webb(1959).Raunkiaer(1934)definedsixleaf-sizeclasses:
leptophyll(leavesupto0.25cm2 inarea), nanophyll(0.25–
– Areleafsizeandwooddensitynegativelycorrelated?
2.25cm2),microphyll(2.25–20.25cm2),mesophyll(20.25–
182.25cm2), macrophyll (182.25–1640.25cm2), and mega-
Wewilltestthefollowingkeyhypothesesaboutleafsizein
phyll (>1640.25cm2). Webb (1959) divided the mesophyll
Amazonia: a) small leaves are an adaptation to relatively
size class into two further size classes (see Table 2): noto-
drier conditions and will show a macrogeographic pattern
phyll(20.25–45.0cm2)andmesophyll(45.0–182.25cm2).
thatreflectsthis;b)smallleavesarefavouredonoligotrophic
soils;andc)thereisanegativerelationshipbetweenleafsize
2.2 Leafsizemetrics
andwooddensity.
The spatial patterns of variation in leaf size were assessed
through the use of several simple metrics, which then acted
2 Materialandmethods
asdependentvariableswithinOLS(OrdinaryLeastSquares)
regressions. FollowingDolphandDilcher(1980),ourmain
2.1 Databaseconstruction
metrics for describing the geographic distribution of leaf
sizes are the proportion of species or individuals that pos-
Our main source of data and research tool for exploring
sesslargeleaves(Category5,mesophyll;Category6,macro-
spatial variation in leaf size categories across the Amazon
phyll; and Category 7, megaphyll). Where appropriate for
basin was the RAINFOR database (Peacock et al., 20071)
analysis or illustration we also collapse Categories 6 and 7
and 26plots from the Guyanas and Suriname compiled by
intoacombined“very-large”leavescategory(Table2). Fur-
the ATDN network (ter Steege et al., 2003). The combined
thermore,palmtreeswereplacedinaseparatepalm-leafcat-
database uses information from 141 permanent plots dis-
egoryandwereonlyusedtoreportabundance.
tributed across eight South American countries. However,
1http://www.rainfor.org
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1566 A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees
Table1.Listofflorasandherbariausedasinformationsourcesandnumberofspeciesretrievedfromeachsource.
Source Totalspecies
1. NeotropicalHerbariumSpecimens–TheFieldMuseum 1918
2. NewYorkBotanicalGarden 160
3. TheNationaalHerbariumNederland(NHN) 159
4. Flo´ruladelasReservasBiolo´gicasdeIquitos,Peru´.Va´squez-Mart´ınez(1997) 154
5. Mobot–MissouriBotanicalGardensHerbarium 140
6. CentreIRDdeCayenne,FrenchGuiana 99
7. InstitutoNacionaldePesquisasdaAmazoˆniaHerbarium,INPA,Brazil 55
8. BotanicGardenandBotanicalMuseum,Berlin,Germany 18
9. Cainetal.(1954) 18
10. MuseuParaenseEmilioGoeldiHerbarium,Brazil 16
11. OxfordUniversity–PlantScienceHerbarium,UK 13
12. TheHerbariumoftheUniversityofAarhus,AAU,Denmark 9
13. HerbW–VirtualHerbariaAustria 4
14. http://images.nbii.gov/ 2
15. Others 23
Table 2. Derivation and correspondence of leaf size categories used in study. Collapsed categories are used as dependent variables in
analyses.
Category Dimensions Raunkiaer(1931) Webb(1959) Mergedcategories
1 <0.25cm2 Leptophyll
2 0.25–2.25cm2 Nanophyll
Smallleaves
3 2.25–20.25cm2 Microphyll
4 20.25–45.0cm2 Notophyll -----
Mesophyll
5 20.25–182.25cm2 Mesophyll
6 182.25–1640.25cm2 Macrophyll Largeleaves -----
“Very-large”leaves
7 >1640.25cm2 Megaphyll
2.3 Geographictrendsinleafsize To better detect and visualize regional patterns in leaf
size categories, and accounting for tree diameters, we also
Previous studies using the RAINFOR database have sug- quantifiedtherelativecontribution(proportion)ofeachleaf
gested that forests in Western Amazonia have higher wood size (Categories 1 to 6) across eight tree trunk diame-
productivity(Malhietal.,2004),higherturnover(Phillipset ter (DBH) classes (100–190mm, >190–280mm, >280–
al., 2004), and lower wood density and biomass (Baker et 370mm, >370–480mm, >480–550mm, >550–640mm,
al.,2004)thanforestsgrowingoninfertilesoilsfurthereast. >640–730mm, >730mm) for each region. The relative
Here,toaiddirectcomparisonswiththesestudies(including abundancewasquantifiedthroughatwo-stageprocess: first,
avarietyofleaftraits–e.g.Malhadoetal.,2009),wefollow theproportionoftreeswithineachDBHcategorywithinare-
thepracticeofsplittingtheAmazonintofourmainregions: gionwascalculated; second, therelativeproportionofeach
Region 1, North Amazonia, containing plots from Guyana, sizeclassacrossthefourregionswascalculated(proportion
Suriname and Venezuela; Region 2, Northwest Amazonia, oftreesinDBHcategory andregion /sumofproportionsin
i i
containing plots from Ecuador, Colombia, and North Peru; categoryforallregions).
Region 3, Central and East Amazonia, all Brazilian plots
(states of Amazonas and Para´ only); Region 4, Southwest 2.4 Lifehistorymetrics
Amazonia,containingplotsfromBoliviaandSouthPeru.
Theregionaldistributionofleafsizemightbeaffectedby
In this paper, we define the growth strategy of each species
thedistributionofthelargestfamily, theFabaceae, soanal-
throughasimpleindex(henceforthreferredtoasthepioneer
yseswererepeatedbothwiththeFabaceaeremoveddataset
index) based on expert judgment. The pioneer index was
andwithintheFabaceaedataset.
usedtorankgeneraaccordingtotheextenttowhichtheyare
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A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees 1567
perceived to be pioneers (plants that are specialists in for- topographic positions, usually located a few metres outside
est gaps and other disturbed areas). This index reflects the thepermanentsampleplotsinordertoreducepotentialdis-
degreeofconsensusamongbotanistsfamiliarwiththetaxa, turbances. All soil samples were analysed (Quesada et al.,
inthiscaseOliverPhillips, RodolfoVa´squez-Mart´ınez, and 2009) and exchangeable Ca, Mg, K, Na and Al were de-
AbelMonteagudo,andwascross-referencedwithherbarium termined by the silver thiourea method (Pleysier and Juo,
materialcollector’slabels. Tocalculatetheindexeachtaxon 1980) as described in detail in ISRI (1995). The sum of
wasjudgedindependentlybyeachbotanistandgivenavalue bases (SB) was calculated as: [SB]=[Ca]+[Mg]+[K]+[Na]
betweenzero(“non-pioneer”)andone(“pioneer”). Thepio- (Units: mmolkg−1). Soil analyses ranged from regional to
neerindexwasthencalculatedastheaveragescoreforeach global scales and used individual leaf size categories (leaf
species. Wooddensityforeachspecieswascalculatedusing Categories 1, 2, 3, 4, 5, 6) and clustered categories (small,
informationavailableintheRAINFORdatabase(Bakerand large, “very-large”) for partial datasets (all trees, Fabaceae
Lopez-Gonzalez, 2006)andderivedfrompublishedsources removed,onlyFabaceae).
(Bakeretal.,2004;Peacocketal.,2007).
2.6 Statisticalanalysis
2.5 Environmentalvariables
Leafsizevariedconsiderablywithintaxonomicgroupsinthe
study,suggestingthatitisunnecessarytocontrolformallyfor
Thechoicesofindependent(predictor)variablesforourspa-
phylogeny. However, RAINFOR plots do show a degree of
tiallycontrolledregressionmodelswerebasedonbothobser-
spatialclusteringandecologicalandphysicalvariablesmay
vation and theory. Since one of the main hypotheses is that
therefore be more similar (or dissimilar) because of spatial
smallleavesintropicalforestsareanadaptationtorelatively
proximity, anditisthereforeappropriatetoaccountstatisti-
drier conditions (Givnish, 1984, 1987), we used a series of
callyforspatialautocorrelation(Legendre,1993).Withmul-
metrics of precipitation retrieved from the monthly TRMM
tiple variables it is a common strategy to perform Ordinary
(Tropical Rainfall Measuring Mission – TRMM 3B43-V6,
0.25◦ spatial resolution). This product combines multiple Least Squares (OLS) regressions of response variables (in
thiscasemetricsofleafsize)ontherawenvironmentalfac-
data sources including satellite information on rainfall with
tors and use Moran’s I correlograms to check for the pres-
groundprecipitationgaugeadjustment(HuffmanandBolvin,
enceofspatialautocorrelationintheresiduals(Rangeletal.,
2007). These data have recently been shown to accurately
2006). Whencorrelogramsshowedevidenceofspatialauto-
represent the rainfall patterns over the Amazonian region
correlationweusedaspatialfilteringapproachtocontrolfor
(Araga˜o et al., 2007). For each month we calculate the av-
theinfluenceofspatialpositionontherelationshipbetween
erage mean from 1998 to 2005. The monthly mean sur-
explanatoryandresponsevariables. Furthermore, wetested
faces (one for each month of the year, combining twelve
foranassociationbetweenthesumofbases(plotsoilfertil-
geo-referencedsurfaces)werethenusedtoestimateforeach
pixel: (1)theannualrainfall(mmyear−1),basedonthesum itydata)andproportionofleafsizecategoriesadjustingfor
the number of degrees of freedom using Dutilleul’s (1993)
of the monthly values; (2) the standard deviation (SD) of
method. Allspatialanalyseswereperformedusingthesoft-
rainfallwithintheyear, asameasureofseasonality; (3)the
wareSpatialAnalysisinMacroecology(SAMv2)(Rangelet
maximum climatological water deficit (MWD; mm), calcu-
al.,2006).
latedbyassumingthattheevapotranspirationrateisapproxi-
mately100mmmonth−1intropicalforestsandacumulative Trends in the distribution of the various leaf size metrics
(see Materials and Methods) in relation to the four Amazo-
deficit is thus incurred if the rainfall is less than this value
nian regions (regional analyses) were assessed using a one-
(Araga˜oetal.,2007);and(4)thelengthofthedryseason,as
way analysis of variance (ANOVA). We used Kruskal Wal-
the number of months with rainfall <100mm (Fig. 1). Al-
lis test to assess relationship between leaf size categories
though crude, the MWD is thought to be a useful indicator
and pioneer index and wood density. These analyses were
ofmeteorologically-inducedwaterstresswithouttakinginto
performed using SPSS 14.0. Significance level was set at
account local soil conditions and plant adaptations, and its
5%(0.05)forallinferentialstatistics.
annualvariationhasbeenshowntostronglyaffecttreemor-
tality(Phillipsetal.,2009).
Small leaves may also be favoured on oligotrophic soils
3 Results
even under wet conditions (Givnish, 1987) and we there-
fore used data on soil fertility (sum of bases), where avail- 3.1 Abundanceofleafsizecategories
able (51plots, Quesada et al., 2009). Soil sampling for the
sites was carried out in accordance with a standard proto- Based on our analysis of herbaria specimens, among the
coldevelopedfortheRAINFORproject2. Soilpitsweresit- 2788studiedspecies50%fellintothemesophyll(Webb)cat-
uated at representative locations for the dominant soil and egory(Category5),1.2%leptophyll,1.3%nanophyll,7.6%
microphyll, 23.6% notophyll, 13.7% macrophyll, and 0.1%
2http://www.geog.leeds.ac.uk/projects/rainfor/projdocs.html megaphyll (Fig. 2). The final 2% were palms, which were
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1568 A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees
Fig.1. ThespatialdistributionoffourwateravailabilityvariablesacrossAmazonia: totalannualrainfall,maximumwaterdeficit(MWD),

length of the dry season, and standard deviation of total annual rainfall. These data were derived from the Tropical Rainfall Measuring
Mission(TRMMF–ifgruomre 119 98to2005).
70 categories(30.9%). Only13.6%ofthefamilieswerecharac-
ory 60 SSppeecciieess terizedbyalltheirspeciesbelongingtoasingleleafsizecat-
ateg IInnddiivviidduuaallss egory–althoughitisimportanttonotethatthevastmajority
e c 50 ofthesefamiliescontainedonly1or2species. Thespecies-
h siz 40 rich Fabaceae family is the group with the largest distribu-
ac
%) in e 30 ttihoantaorfelreeapfressieznetecdatiengo6r(ieosutaonfdthisec7h)aleraacftcelraissesdes.by species
n ( 20
o Theleafsizedistributionofthelargestfamilies(thosewith
porti 10 >60species)followsaunimodaldistributionwithadistinct
o
Pr peak in the mesophyll leaf size category (Fig. 3a). Further
0
leptophyll nnaannoopphhyyllll microphyll notophyll mesophyll mm aaccrroopphhyyllll m egaphyll analysesonfamilieswhereallspeciespossesssimpleleaves
and on families displaying at least one species with com-
Fig.2.Meanpercentageofspeciesandindividualtreesindifferent poundleaves(leaflets)alsofollowedaunimodaldistribution
leafsizecategoriesin121Amazonianplots. Errorbars=1standard (Fig.3b,c). Twofamiliesdeviatefromthegeneralform: the
errorofthemean.
FabaceaeandMyrtaceae,bothofwhicharecharacterizedby
aflatterdistribution(lowerkurtosis)ofleafsizecategories.
excludedfromfurtheranalysis. Theproportionofindividual 3.2 Spatialtrendsinleafsize
treesthatfallintodifferentleafsizecategoriescloselymirror
theobservedproportionofspecies:52.4%of84554individ-
There is a significant difference in the mean proportion of
ualtreesfellintomesophyllcategory,1.3%wereleptophyll,
specieswithlargeleaves(Categories5to7)amongthefour
0.6% nanophyll, 4.1% microphyll, 18.5% notophyll, 11.9%
Amazonian regions (n=121, df=3, F=14.455, p<0.001),
macrophyll,and0.6%megaphyll(Fig.2). Palmsaccountfor
withplotsfromNorthwestAmazonia(Region2)possessing
10.5%ofthetotalnumberofindividualtreesacrossthestud-
agreaterproportionoflarger-leavedspeciesonaveragethan
iedplots.
plotsfromtheotherregions(Fig.4). Itisinterestingtonote
Leaf size classes are broadly distributed within and be- that Region 4 appears to consist of two quantitatively dis-
tween families. This is clearly illustrated by the proportion tinct clusters of plots (Fig. 4), a western set and an eastern
of families that contain species in two leaf size categories set. Thenorthwesterncluster(nearesttoRegion2)features
(24.7%), three leaf size categories (29.6%) or four leaf size forestswithasimilarproportionoflarge-leavedtreestothose
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A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees 1569
0.7 Sapindaceae
Burseraceae Region 1
0.6 Clusiaceae
Frequencies 00..45 AMLepecoylactyshtniodamacceaeataeaeceae Region 2
Euphorbiaceae
0.3 Moraceae
0.2 Rubiaceae Region 3
Chrysobalanaceae
0.1 Sapotaceae
Annonaceae
0 Lauraceae
leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll
Myrtaceae
(a) Leaf size categories Fabaceae
0.7
Clusiaceae
Frequencies 000...456 AMLRCSeahupecprboylyoaictastyshocatniebocdaaeamacealceaaeeantaeaaecceeaaee Region 4
0.3 Annonaceae
Lauraceae
0.2 Myrtaceae
0.1
0
leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll
Fig.4.Mapoftheincidenceofspecieswithlargeleafsizecategory
(b) Leaf size categories (simple leaf)
(Categories5to7)ineachplotorganizedbyproportioncategories
0.7 Sapindaceae andregions(Region1,NorthAmazonia;Region2,NorthwestAma-
Frequencies 000...456 BEMFauuobprrsahaecocrereaabaceieeaaceeae zAsoommniaeaz;opRnloieatgs)i.owFniot3hr,itnChecelnputusrtareplroassnhedsavEoeafsbctelAeeanmravadzisjouunsaitlaei;sdaR,tiaeongndiotmnhea4yp,oSnsooiuttitochnowsreroesf-t
0.3 spondtoexactgeographiclocation.
0.2
0.1
0
leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll individualtreeswithlargeleavesamongtheregions(n=118,
(c) Leaf size categories (compound leaf) df=3, F=13.068, p<0.001). Tukey’s post-hoc test reveals
Figure 3 two distinct clusters: 1) North and Southwest Amazonia
Fig.3.Leafsizedistributionsofthelargest(mostspeciesrich)fam-
(Regions 1 and 4) that display a lower mean proportion of
ilies(>60species)intheRAINFORdataset: (a)alllargefamilies;
trees with large leaves, and 2) Northwest Amazonia and
(b)excludingfamiliesthathaveanyspecieswithcompoundleaves;
(c) families that have one or more species displaying compound Central-Eastern Amazonia (Regions 2 and 3) that display a
leaves. highermeanproportionoftreeswithlargeleaves. Aniden-
tical geographical pattern and level of significance was ob-
servedwhentheproportionoftreeswith“very-large”leaves
found in plots in Region 2. When the analysis is repeated
(classes6and7)wasusedasthedependentvariable(n=118,
using the two largest leaf size categories (Categories 6 and
df=3,F=7.464,p<0.001).
7), a significant difference is found between the mean pro-
WhentheanalysiswasrepeatedwithintheFabaceaeonly
portion of species with leaves in these classes between all
wefoundaweaklysignificantdifferenceamongtheregions
4regions.Inthiscase,NorthwestAmazonia(Region2)once
in the mean proportion of trees with large leaves (n=118,
again has the greatest proportion of species with the largest
df=3, F=2.715, p=0.048). In this case Northwest Amazo-
leaves,followedbySouthwestAmazonia(Region4),Central
nia (Region 2) still contains the largest mean proportion of
and Eastern Amazonia (Region 3), and finally, North Ama-
Fabaceae trees with large leaves although Tukey’s post hoc
zonia(Region1).
testrevealedthatnoneofthemeans(forregions)arestatisti-
Verysimilargeographicalpatternsareobservedwhenwe
callydifferentfromeachother. However,whenthesametest
consider relative abundance of individual trees with large
is performed using the mean proportion of Fabaceae trees
leaves (Categories 5 to 7), or “very-large” leaves (Cate-
with“very-large”leavesastronglysignificantresultisgained
gories6and7).
(n=118, df=3, F=4.639, p=0.004), once again following
There is still a significant difference among the four re-
the “typical” geographic pattern outlined above: trees with
gions in terms of the mean proportion of trees with large
“very-large” leaves being relatively less abundant in North
leaves(and“very-large”leaves)whenwecontrolforthepos-
and Southwest Amazonia and relatively more abundant in
sibleinfluenceofthenumericallyabundantFabaceaefamily.
NorthwestAmazoniaandCentral-EasternAmazonia.
Specifically, when all the Fabaceae trees are removed from
the analysis there was a significant difference observed for
www.biogeosciences.net/6/1563/2009/ Biogeosciences,6,1563–1576,2009
1570 A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees
Themeanfrequencyofdifferentleafsizecategoriesshows 0.7
a consistent pattern across the four Amazonian regions and 0.6 RReeggiioonn 12:: NNW a.
imh(nsFaaeisncgshcoa.eap5srhialasiyc)g.tlrheletrpAcliyzeaneatledtaaegrldobgmryewyortshhf(treFeeniiqdgdtue.ohnem5entaiiccm)ny.aaolnoRspcfteaesngtmtuoieomfarnnlielne1rodircf-i(vlaNemiladloyevursetaaohdlbptuAihrnneymddelilsaavnzdiidotnounamtainhalides-) Frequencies (all trees) 0000....2345 RReeggiioonn 34:: CSWE
species rich family, the Fabaceae, are removed from the 0.1
datasetwithRegion1conformingmostcloselytothe“typi- 0
leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll
cal”pattern(Fig.5b). Whenthesizedistributionofindivid-
uals within the Fabaceae is plotted each region appears to 0.7
haveitsownsingulardistribution(Fig.5c). Region 1: N b.
0.6
atDCortfeaiBvWetFHeesagebpiocnararloiaclesepseosasoaecre1lshtoiaoa(olcFnnekrsidaoegfdso.2sfs6aitit)zhtsr.eeetiehTncrseehaicgtenreoieogndllneociasasrottiyfrrvadisenbiainduznpetcDirroeoeCBnlpaawoHttoeiriofttgshinootirzrnteteihoeeeocssflrd3aienisgisnasitlneodresidniabv.sfu4iRdtsaiuaieonzralndee-l Frequencies (no Fabaceae)Frequencies 00000.....34512 RRReeegggiiiooonnn 234::: NCSWEW
relativelyevenamongourregions,althoughitispossibleto 0
detectaslightincreaseinrelativeproportionforRegion4for leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll
treesinthehigherDBHranks(Fig.6). Therelativepropor-
0.7
tionsoftreesinleafsizeclasses5and6areveryconsistent Region 1: N
igglibneniiyaoosRvannmeaaehsagllilgisa(loecehnnplreaaarlD4syrpsaBse(rtiSosiHsopoo5noucfartithtnstoiemwogt7nheaoeslrocltiohfe(AmicslgalmbbahrgusieansetrzeesoDDsdhn)BBo1iawrHHt)eo,vatcwer4atearthecelesisongcmdtoahhrboaisiesiftinnspidegn(oidFucss)rltisaeigeanra.sngss6pdiu)naei.lgsitattRhherregreeende-r- Frequencies (only Fabaceae) 000000......123456 RRReeegggiiiooonnn 234::: NCSWEW c.
smaller leaves or larger leaves (Fig. 7). Region 1 shows a 0
leptophyll nanophyll microphyll notophyll mesophyll macrophyll megaphyll
trendofarelativelylowerproportionoflargeleavedtreesin
largerDBHcategories(Fig.7). Fig. 5. The mean frequency (0Figtuore 15) of different leaf size cate-
gories across the four Amazonian regions (Region 1, north; Re-
3.3 Leafsizeandtreecharacteristics gion2,northwest;Region3,centralandeast;Region4,Southwest
Amazonia). Figure(a)representsallindividualtrees;figure(b)il-
Species with small leaves show significantly lower “pio- lustratesallindividualtreeswiththeexceptionofmembersofthe
neer”scoresthanspecieswithlargeleaves(x2=10.215,df=1, Fabaceae;figure(c)showsonlytreesfromtheFabaceaetaxa.
p=0.001).Amoredetailedanalysisusingleafcategoriesone
tosixalsoshowsasignificantdifferenceinidentifiedgrowth
strategy among the classes (x2=18.332, df=5, p=0.003).
Further analysis reveals that the significance is being pri- 3.4 Environmentalcorrelatesofleafsize
marily driven by the growth strategy of species with large
leaves(Category6)3,whicharecharacterizedbyalmost40% Theproportionofspeciespersitewithlargeleaveswassig-
highermeanscoresthanspecieswithsmallerleafsizes(Cat- nificantlycorrelatedwiththreeprecipitationmetricsusedin
egories3,4and5). thestudy: lengthofthedryseason(months<100mmrain-
Species with large leaves (Categories 5 to 7) have lower fall), maximum water deficit, and a metric of the variation
wooddensity(approximately10%less)whencomparedwith in water availability based on the standard deviation of to-
species with small leaves (Categories 1 to 4) (x2=23.885, tal rainfall (full results given in Table 3). However, no sig-
df=1,p<0.001;meanwooddensitylargeleaves:0.62;small nificant relationships were seen at the individual level or
leaves: 0.68). Individualtreeswithsmallleavestendtohave for species or individuals when the leaf size metric was the
larger diameters (DBH), while larger leaves present smaller proportion of trees per plot with “very-large” leaves (Cate-
diameters although, interestingly, it is also possible to find gories6and7).
individualtreeswithlargeDBHpossessinglargeleaves. Analyses of the large leaf subsets of data controlling for
theinfluenceoftheFabaceae–withFabaceaetreesremoved
3Speciesinthelargestleafsizecategory(7)werenotsignificant
inthistest,possiblybecausetheyaccountforaverysmallpropor- tion(0.1%)ofthetotalnumberofspecies.
Biogeosciences,6,1563–1576,2009 www.biogeosciences.net/6/1563/2009/
A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees 1571

Fig.6.Relativeabundance(percentage)oftreesineachdiameter(DBH)classforeachindividualleafsizecategory.Therelativeabundance
iscalculatedfollowingtwosteps:firstly,relativeabundancewithintheregion;secondly,relativeabundanceamongregionstoallowcompar-
ison.DBH1=100–190mm;DBH2=>190–280mm;DBH3=>280–370mm;DBH4=>370–460mm;DBH5=>460–550mm;DBH6=>550–
640mm;DBH7=>640–730mm;DBH8=>730mm.Theregionsare:Region1,NorthAmazonia;Region2,NorthwestAmazonia;Region3,
CentralandEastAmazonia;Region4,SouthwestAmazonia.
and with only Fabaceae trees included - also resulted in a withinRegion3(Central-EastAmazonia)producedonlyone
small number of significant correlations (Table 3). When significant(positive)correlationbetweenindividualtreesand
the Fabaceae were removed, the proportion of trees with leafsizeCategory1. AninterestingcontrastisfoundinRe-
large leaves and “very-large” leaves did not correlate with gion4(SouthwestAmazonia)with18significantresultssup-
any variables. However, when the Fabaceae were analysed portinganinversecorrelationbetweentheproportionsofin-
separately significant correlations were found between the dividual trees with large leaves and soil fertility (Table 4)
proportion of trees with large leaves and length of the dry – the opposite trend to that observed by previous authors
season. TheproportionofFabaceaeindividualswith“very- (Wrightetal.,2007).
large”leavesonlycorrelatedwiththecoefficientofvariation
(SD)ofrainfall(Table3).
The relationship between soil fertility and leaf size was 4 Discussion
complexand revealed nostrongpatterns orconsistentasso-
ciations. From the global dataset (individual and clustered Richards (1952), in his pioneering study on tropical rain-
leafcategoriesofproportionofindividualtreesandspecies) forests, noted that plants of different families in a trop-
onlyonecorrelationwassignificant–betweentheproportion ical forest tended towards similar morphologies far more
ofindividualtreeswithinthesmallestleafsizecategoryand than species, even of the same genera, in temperate forests.
soilfertility(Table4). Nocorrelationswerefoundwhenwe This is very apparent for traits such as leaf size, where
removed the Fabaceae, while only Categories 6 and “very- species within tropical forests can be remarkably homoge-
large”leaveswerecorrelatedwithintheFabaceaetreessub- nous in the leaf size properties that they possess. In low-
set(Table4). Wealsoexploredtotalphosphorusavailability land rainforests the predominant leaf size category is mes-
(asanadditionalmeasureofsoilfertility)and,onceagain,no ophyll (sensu Raunkiaer, 1934) – Grubb and his colleagues
correlationswerefound. describe64%ofspeciesinEcuador,84%oftheirsamplein
Analyses within Region 2 did not reveal any significant Brazil,and98%oftheirsampleinAustraliaasbelongingto
correlation with soil fertility and leaf size, while analyses the mesophyll category (Grubb et al., 1963). Turner (2001)
www.biogeosciences.net/6/1563/2009/ Biogeosciences,6,1563–1576,2009
1572 A.C.M.Malhadoetal.: SpatialtrendsinleafsizeofAmazonianrainforesttrees
100 sultinginahighproportionofFabaceae,manyofwhichare
mall 8900 a. characterizedbythepossessionofsmallleaves(orleaflets).
Proportion (%) of trees with sleaves 123456700000000 RRRReeeeggggiiiioooonnnn1234:::: NNCSWEW lMvpsateortonTiseositthtoctniehrosystenioegsdnaspfainrprfitodeaacmvtaifitaunootlhntulteicsyrdt,eGimenotneudnatricsiafarSyniocntagertoeewSlesgohsoaegiferAemalstdpmiazahtjaelooi.zcrcSo(as2ngotn0iuruaa0dtb.dh6ieeiw)eTsirnenheisttnecsteeerfitrinphnnrtrelseAytttrAemegudemrsaaeizacdndozoioenimrnnenia---t.
DBH1 DBH2 DBH3 DBH4 DBH5 DBH6 DBH7 DBH8
andisprimarilycharacterizedbychangesintheabundanceof
severalcommonspeciesoflegumesintheGuyanas.Thisob-
servedgradientintreecompositionisparalleledbydeclines
100 b.
with large 789000 imnafiunnecctioolnoaglictraalitdsrisvuecrhoafsthwiosogdraddeinensittyisahnydpsoetehdesmizaesds.toThbee
Proportion (%) of trees leaves1234560000000 RRRReeeeggggiiiioooonnnn1234:::: NNCSWEW teCtthhhroneeeloicfinnomoccrrebrrneesieaatarssstoiioonnfnggSAlotyphmurepteahoszseeoooanrunsctitsehaeo.erionalTsfsAhtmaeemsronsoareeznecoedodngnraieodapupogagrfnrohadAatd-ciiamsehdneacatszhposatttehnrradeieact,nsctephowreerihtczshiiefecedrshaosbmiityns-
DBH1 DBH2 DBH3 DBH4 DBH5 DBH6 DBH7 DBH8 postulated to be driven by a parallel gradient of dry season
length(terSteegeetal.,2006).
F ig.7. Relativeabundanceoftreesineachdiameter(DBH)class
In the present study the relative predominance of larger-
f orclustFeigruered 7 (smallandlarge)leafsizecategory.Therelativeabun-
leaved species in West and Southwest Amazonia closely
danceiscalculatedfollowingtwosteps: firstly,relativeabundance
alignswiththescoresforthesecondaxisofterSteege’sDCA
within the region; secondly, relative abundance among regions to
allow comparison. DBH1=100–190mm; DBH2=>190–280mm; analysis of genus level community composition (ter Steege
DBH3=>280–370mm; DBH4=>370–460mm; DBH5=>460– et al., 2006) and indicates a possible influence of length of
550mm; DBH6=>550–640mm; DBH7=>640–730mm; the dry season on leaf size. This interpretation is further
DBH8=>730mm. The regions are: Region 1, North Amazo- supported, although weakly, by the spatially-corrected OLS
nia; Region 2, Northwest Amazonia; Region 3, Central and East regressions, which identified three metrics of water avail-
Amazonia; Region 4, Southwest Amazonia. (a) Trees with small ability (see Materials and Methods) as being significantly
leaves (size Categories 1 to 4). (b) Trees with large leaves (size
associated with the proportion of tree species with large
Categories5and6).
leaves. However, the data do not generate a clear signal
when the Fabaceae are excluded from the dataset, or when
theFabaceaeareanalysedindependently. Itisworthnoting
proposes that trees in this category normally constitute ap-
thatterSteegeetal.(2006)didnotcorrectforspatialautocor-
proximatelythree-quartersofallspeciesinlowlandtropical
relation,anditisnotclearifthepatternwouldbethesameif
rainforestsacrosstheglobe. Thecurrentpan-Amazonstudy
ithadbeenaccountedfor.
supportsthesefindings,with73.6%ofspeciesidentifiedbe-
In summary, the data presented here do not provide any
longingtothissizecategory.Thisresultalsosupportstheob-
clearsupportforthehypothesisthatleafsizeinrainforestsis
servationthatthemesophyllcategorydominatesinNeotrop-
positively correlated with annual rainfall. This may be due
ical rainforests (Grubb et al., 1963; Thompson et al., 1992;
to the geographic scale of the study. However, the results
Kelly et al., 1994). Another characteristic feature of trop-
do broadly support the work of Dolph and Dilcher (1980),
ical rainforests is to have a small proportion of (non-palm)
whoreporteddistinctleafsizeproportionsindifferenttropi-
species with very large leaves. Once again this was further
calforestlifezones(dryforests,wetforests,montaneforests)
supportedbythisstudyinthatweobserved0.01%ofspecies
rather than a positive environment gradient that correlates
withleavesinthemegaphyllsizecategory.
leaf size and climate, reflecting an increase in temperature
4.1 Spatialtrendsandenvironmentalcorrelates and/orprecipitationandincreaseintheproportionofleafsize
inleafsize (DolphandDilcher,1980).
Therelationshipbetweensoilfertilityandleafsizeproved
Ourstudydemonstratescomplexpatternsofvariationinleaf to be complex and revealed no strong patterns. This is in
size characteristics across the Amazon rainforest. At the agreement with McDonald et al. (2003) who suggest that
crudestlevelofanalysisthereisatrendtowardsgreaterpro- there is no clear basis for the negative correlation between
portions of individuals and species in large leaf size cate- leafsizeandlowersoilphosphoruslevels.Nevertheless,they
goriesinthewesternplots.Therelativelylowerproportionof didfindapatternofdecreasingleafsize(length,width,leaf
treeswithlargeleavesintheGuianaShieldmaybeduetothe surfacearea)inoligotrophicsoils(whilecontrollingforrain-
unusual ecology of the area (see ter Steege et al., 2006) re- fall) in Southeast Australia. There study spanned a whole
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