PART OF A HIGHLIGHT ON TRAITS WITH ECOLOGICAL FUNCTIONS Seedlings of temperate rainforest conifer and angiosperm trees differ in leaf area display Christopher H. Lusk 1, *, Manuel M. Pe ´rez-Millaqueo 2 , Alfredo Saldan ˜a 2 , Bruce R. Burns 3 , Daniel C. Laughlin 1 and Daniel S. Falster 4 1 Department of Biological Sciences, The University of Waikato, Private Bag 3105, Hamilton, New Zealand, 2 Departamento de Bota ´nica, Universidad de Concepcio ´n, Concepcio ´n, Chile, 3 School of Biological Sciences, University of Auckland, Auckland 1142, New Zealand and 4 Department of Biological Sciences, Macquarie University, NSW 2019, Australia * For correspondence. E-mail [email protected]Received: 25 December 2011 Returned for revision: 22 February 2012 Accepted: 6 March 2012 Published electronically: 14 May 2012 † Background and Aims The contemporary relegation of conifers mainly to cold or infertile sites has been ascribed to low competitive ability, as a result of the hydraulic inefficiency of tracheids and their seedlings’ initial dependence on small foliage areas. Here it is hypothesized that, in temperate rainforests, the larger leaves of angiosperms also reduce self-shading and thus enable display of larger effective foliage areas than the numerous small leaves of conifers. † Methods This hypothesis was tested using 3-D modelling of plant architecture and structural equation modelling to compare self-shading and light interception potential of seedlings of six conifers and 12 angiosperm trees from temperate rainforests. The ratio of displayed leaf area to plant mass (LAR d ) was used to indicate plant light inter- ception potential: LAR d is the product of specific leaf area, leaf mass fraction, self-shading and leaf angle. † Results Angiosperm seedlings self-shaded less than conifers, mainly because of differences in leaf number (more than leaf size), and on average their LAR d was about twice that of conifers. Although specific leaf area was the most pervasive influence on LAR d , differences in self-shading also significantly influenced LAR d of large seedlings. † Conclusions The ability to deploy foliage in relatively few, large leaves is advantageous in minimizing self- shading and enhancing seedling light interception potential per unit of plant biomass. This study adds significant- ly to evidence that vegetative traits may be at least as important as reproductive innovations in explaining the success of angiosperms in productive environments where vegetation is structured by light competition. Key words: Biomass distribution, competition, gymnosperms, independent contrasts, light interception efficiency, plant architecture, specific leaf area, structural equation modelling, YPLANT. INTRODUCTION The rise of the angiosperms at the expense of conifers and other gymnosperms is considered one of the most sweeping biotic replacements in the history of the Earth (Benton, 1991; Lupia et al., 1999; Turner and Cernusak, 2011). After dominating the overstoreys of forests worldwide during the Triassic and Jurassic (Florin, 1963; Miller, 1977), conifers were almost entirely supplanted by angiosperm trees in the lowland tropics during the Cretaceous, as well as losing much ground in temperate forests (Lupia et al., 1999). Conifer dominance is now restricted mainly to cold or infertile sites (Bond, 1989), though they still coexist with angiosperms in a variety of forest types (Enright and Hill, 1995; Becker, 2000). Bond (1989) attributed the scarcity of conifers on productive sites to low competitive ability as seedlings, as a result of the hydraulic inefficiency of tracheids and an initial dependence on small foliage areas. He therefore claimed that, although some conifers can attain high productivity in later life by accu- mulating many leaf cohorts, their seedlings are likely to be outcompeted by angiosperms on productive sites that permit rapid growth. In essence, conifers are relegated mainly to cold or infertile sites because these adverse environments nullify or reduce the potential carbon gain and growth advan- tages of angiosperm competitors. Comparative studies have since shown that although both lineages encompass a wide range of seedling growth rates, conifers are unable to match the performance of the fastest growing early successional angiosperm trees (e.g. Cornelissen et al., 1996; Reich et al., 1998). Furthermore, field comparisons in mixed evergreen forests have confirmed that conifers generally operate with lower hydraulic supply and photosynthetic capacity than angiosperm associates (Brodribb and Feild, 2000; Lusk et al., 2003; Brodribb et al., 2005). Notwithstanding differences in total leaf area, advantages in leaf display and light interception efficiency might also con- tribute to angiosperm competitive superiority in productive habitats. Reticulate venation enables angiosperms to develop an impressive variety of leaf sizes and shapes (Brodribb et al., 2010), but the more limited venation of conifers restricts them to a smaller range of options (Bond, 1989). In the ever- green temperate forests of the southern hemisphere, many con- ifers have lanceolate, flattened leaves (Biffin et al., 2012), but these have minimal petiole development and are usually smaller than those of their angiosperm competitors. Conifer # The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected]Annals of Botany 110: 177–188, 2012 doi:10.1093/aob/mcs095, available online at www.aob.oxfordjournals.org Downloaded from https://academic.oup.com/aob/article/110/1/177/2769002 by guest on 09 January 2022
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PART OF A HIGHLIGHT ON TRAITS WITH ECOLOGICAL FUNCTIONS
Seedlings of temperate rainforest conifer and angiosperm trees differin leaf area display
Christopher H. Lusk1,*, Manuel M. Perez-Millaqueo2, Alfredo Saldana2, Bruce R. Burns3,Daniel C. Laughlin1 and Daniel S. Falster4
1Department of Biological Sciences, The University of Waikato, Private Bag 3105, Hamilton, New Zealand, 2Departamento deBotanica, Universidad de Concepcion, Concepcion, Chile, 3School of Biological Sciences, University of Auckland, Auckland
1142, New Zealand and 4Department of Biological Sciences, Macquarie University, NSW 2019, Australia* For correspondence. E-mail [email protected]
Received: 25 December 2011 Returned for revision: 22 February 2012 Accepted: 6 March 2012 Published electronically: 14 May 2012
† Background and Aims The contemporary relegation of conifers mainly to cold or infertile sites has beenascribed to low competitive ability, as a result of the hydraulic inefficiency of tracheids and their seedlings’initial dependence on small foliage areas. Here it is hypothesized that, in temperate rainforests, the largerleaves of angiosperms also reduce self-shading and thus enable display of larger effective foliage areas thanthe numerous small leaves of conifers.† Methods This hypothesis was tested using 3-D modelling of plant architecture and structural equation modellingto compare self-shading and light interception potential of seedlings of six conifers and 12 angiosperm trees fromtemperate rainforests. The ratio of displayed leaf area to plant mass (LARd) was used to indicate plant light inter-ception potential: LARd is the product of specific leaf area, leaf mass fraction, self-shading and leaf angle.† Results Angiosperm seedlings self-shaded less than conifers, mainly because of differences in leaf number (morethan leaf size), and on average their LARd was about twice that of conifers. Although specific leaf area was the mostpervasive influence on LARd, differences in self-shading also significantly influenced LARd of large seedlings.† Conclusions The ability to deploy foliage in relatively few, large leaves is advantageous in minimizing self-shading and enhancing seedling light interception potential per unit of plant biomass. This study adds significant-ly to evidence that vegetative traits may be at least as important as reproductive innovations in explaining thesuccess of angiosperms in productive environments where vegetation is structured by light competition.
The rise of the angiosperms at the expense of conifers andother gymnosperms is considered one of the most sweepingbiotic replacements in the history of the Earth (Benton,1991; Lupia et al., 1999; Turner and Cernusak, 2011). Afterdominating the overstoreys of forests worldwide during theTriassic and Jurassic (Florin, 1963; Miller, 1977), coniferswere almost entirely supplanted by angiosperm trees in thelowland tropics during the Cretaceous, as well as losingmuch ground in temperate forests (Lupia et al., 1999).Conifer dominance is now restricted mainly to cold or infertilesites (Bond, 1989), though they still coexist with angiospermsin a variety of forest types (Enright and Hill, 1995; Becker,2000).
Bond (1989) attributed the scarcity of conifers on productivesites to low competitive ability as seedlings, as a result of thehydraulic inefficiency of tracheids and an initial dependenceon small foliage areas. He therefore claimed that, althoughsome conifers can attain high productivity in later life by accu-mulating many leaf cohorts, their seedlings are likely to beoutcompeted by angiosperms on productive sites that permitrapid growth. In essence, conifers are relegated mainly to
cold or infertile sites because these adverse environmentsnullify or reduce the potential carbon gain and growth advan-tages of angiosperm competitors. Comparative studies havesince shown that although both lineages encompass a widerange of seedling growth rates, conifers are unable to matchthe performance of the fastest growing early successionalangiosperm trees (e.g. Cornelissen et al., 1996; Reich et al.,1998). Furthermore, field comparisons in mixed evergreenforests have confirmed that conifers generally operate withlower hydraulic supply and photosynthetic capacity thanangiosperm associates (Brodribb and Feild, 2000; Lusket al., 2003; Brodribb et al., 2005).
Notwithstanding differences in total leaf area, advantages inleaf display and light interception efficiency might also con-tribute to angiosperm competitive superiority in productivehabitats. Reticulate venation enables angiosperms to developan impressive variety of leaf sizes and shapes (Brodribbet al., 2010), but the more limited venation of conifers restrictsthem to a smaller range of options (Bond, 1989). In the ever-green temperate forests of the southern hemisphere, many con-ifers have lanceolate, flattened leaves (Biffin et al., 2012), butthese have minimal petiole development and are usuallysmaller than those of their angiosperm competitors. Conifer
# The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
seedlings are thus constrained to display their foliage in anarrow cylinder around the stem; a large foliage area canonly be developed by accumulating large numbers of leaves,probably resulting in heavy self-shading. The limitationsimposed by small leaves are illustrated by a comparativestudy of 38 Australian woodland angiosperms (Falster andWestoby, 2003): leaf size was strongly negatively correlatedwith self-shading within shoots, and positively correlatedwith the total foliage area per metre of stem. Duursma et al.(2012) attribute this pattern to more pronounced foliageclumping in small-leaved species. Continued growth ofpetioles after lamina expansion gives some angiosperms anadditional option for ameliorating self-shading, enablingplants to reposition leaves as they become shaded by newerones (Galvez and Pearcy, 2003).
Here we examine the determinants of light interceptionpotential in conifer and angiosperm tree seedlings from tem-perate rainforest. Coexistence of conifers and evergreen angio-sperms is common in the temperate forests of the southernhemisphere, but, as in other biomes, conifers tend to be con-centrated on cold and/or nutrient-poor sites (Read, 1995;Burns and Leathwick, 1996; Lusk and Matus, 2000). Weaddressed three questions. (1) Do conifer seedlings self-shademore than competing angiosperm seedlings? (2) What traitsunderlie variation in self-shading? (3) To what extent is seed-ling leaf area display determined by variation in self-shading,as opposed to biomass distribution traits and leaf angle?
To answer these questions, we measured biomass distribu-tion and leaf area of conifer and angiosperm seedlings fromfive sites differing in climatic and edaphic characteristics,and used the architectural model YPLANT (Pearcy andYang, 1996) to quantify variation in self-shading, leaf anglesand leaf display. We then used structural equation modelling(Wright, 1934; Shipley, 2000) to obtain a multivariate perspec-tive on how leaf, crown and biomass distribution traits shapedifferences in self-shading and leaf area display.
MATERIALS AND METHODS
Study sites and species
We sampled seedlings of common conifer and angiospermspecies, at four temperate rainforest sites in Chile and one inNew Zealand (Table 1), chosen to represent a range of climaticand edaphic conditions. Conifers are a major component of theforest overstorey at three of these sites (Los Mallines, PinoHuacho and Miranda), a relatively minor component at onesite (El Manzano) and absent at another (Anticura). AsYPLANT and the software we used to capture plant architec-ture (FLORADIG) are able to deal adequately only with flat-tened leaves (excluding imbricate or needle-leaved taxa), ourselection of conifers was restricted to species from thePodocarpaceae and Araucariacae; species with this type ofleaf form as juveniles make up slightly more than half of theconiferous flora of the humid temperate forests of the southernhemisphere (Enright and Hill, 1995). The six conifer speciesthat we sampled encompassed a wide range of leaf sizewithin these constraints (Fig. 1), and all are important over-storey dominants over extensive tracts of South American or
New Zealand rainforest. Leaves of five of the six coniferswere lanceolate or linear in shape. Although very young seed-lings of the sixth conifer species (Phyllocladus trichoma-noides) also produce linear leaves, these are succeeded byrhombic phylloclades (Fig. 1). Leaves of the 12 angiospermspecies we sampled varied more widely in size and shape.All had simple leaves, with shapes including lanceolate, oblan-ceolate, ovate, obovate, oblong and rhomboid (Fig. 1).
We sampled 15–21 seedlings of each species, ranging inheight from 50 to 350 mm tall. This range of size enabled usto examine the effect of early ontogeny on leaf, crown andbiomass distribution traits. We stratified our sampling withinthis size range, deliberately choosing at least seven seedlingsof each species between 50 and 150 mm tall, and at leastseven more in the 150–350 mm height range. Seedlingswere of each species chosen haphazardly from throughoutthe range of light environments they were found to occupynaturally.
Seedling light environments
Seedling light environments were quantified using hemi-spherical photography. A Nikon Coolpix 4500 digital camera(Nikon Corporation, Japan) with a 183 º fisheye adaptor wasused to take a hemispherical photograph directly above eachseedling, orienting the top of the camera towards north.Photos were analysed using the Gap Light Analyzer (GLA)software package (Frazer et al., 1999), to determine percentagecanopy openness above each plant.
Digital capture of seedling architecture
Each seedling was excavated carefully, removing a sod ofsufficient width and depth to include the root system, aftercutting through any intruding coarse roots from neighbouringplants. Seedlings were transplanted to pots of sufficient sizeto accommodate the excavated sod, taken to the laboratory,and their architecture digitized within 3 d.
We used digital capture of plant architecture to create virtualplants, which is much less time-consuming than the manualmethods often used in conjunction with YPLANT (Hananand Room, 1997; Falster and Westoby, 2003; Pearcy et al.,2011). The 3-D leaf arrangement of each seedling was recor-ded using a FASTRAKw 3D-digitizer (Polhemus, Colchester,VT, USA), in conjunction with the software packageFLORADIG (CSIRO Entomology, Brisbane, Australia). Thedigitizer includes a magnetic signal receiver and pointer,allowing the user to record the 3-D spatial co-ordinates ofthe pointer within a hemisphere of 3 m diameter from the re-ceiver. Individual plants are reconstructed virtually by record-ing a series of point co-ordinates, and the relevant connectivitybetween points. Stem segments (and petioles, if present) arecharacterized by their elevation angle, azimuth, length anddiameter. Individual leaves are characterized by their lengthtogether with the azimuth and elevation angle of two vectorson the lamina surface.
Model leaves, digitized in two dimensions, were used topopulate the nodes of each virtual plant. With the exceptionof four markedly heteroblastic species (Aextoxicon punctatum,Eucryphia cordifolia, Myrceugenia planipes and Phyllocladus
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trichomanoides), one representative leaf of each species wasdigitized, so that all virtual leaves of a given species had thesame fixed shape, despite variation in size. Myrceugenia pla-nipes initially produces obovate leaves, which are succeededby apiculate, oblanceolate leaves after seedlings reach 8–10 cm tall. Eucryphia cordifolia initially develops obovateleaves with toothed margins, succeeded by oblong leaves onlarger plants. The first few leaves of A. punctatum are orbicu-lar, with shape shifting to oblanceolate on larger seedlings, andeventually oblong on plants larger than those included in thepresent study. Accordingly, we digitized two different leafshapes for this species, and used whichever was more appro-priate for each plant. The complex growth dynamics ofP. trichomanoides required us to digitize three differenttypes of photosynthetic unit. The linear true leaves producedby very young seedlings can persist for several years, and soare often still present on older seedlings that developrhombic cladodes on both determinate and indeterminateshoots. Determinate shoots typically bear 9–15 cladodes,which are all displayed in roughly the same plane like the leaf-lets of a compound leaf (Fig. 1). As well a true leaf ofP. trichomanoides, we therefore also digitized a representativedeterminate shoot, and a single cladode that was used topopulate indeterminate shoots.
After digitizing, plants were separated into leaf, stem androot fractions, dried for at least 48 h at 65 8C, and thenweighed for determination of biomass parameters.
Self-shading, leaf angles and leaf display
The YPLANT software (Pearcy and Yang, 1996) was usedto quantify crown architectural properties. The 3-D descriptionof leaf arrangement of each seedling, as recorded inFLORADIG, was converted to the appropriate YPLANTformat using a program written in the C programminglanguage (Falster and Westoby, 2003).
As light interception by plant crowns is determined by leafinclination angles as well as overlap among leaves (i.e. self-shading), we used YPLANT output to estimate both theseparameters. YPLANT output includes leaf area projectedtowards each of 160 sectors of the hemisphere (20 elevationclasses × 8 azimuth classes) without taking into accountoverlap of leaves, and leaf area displayed towards eachsector, i.e. the effective area for light interception (Pearcyand Yang, 1996). The mean leaf elevation angle of a plantcrown, weighted by the size of individual leaves, can beestimated as:
Angle = arccosine (PAV/LA) (1)
where PAV ¼ leaf area projected towards the vertical, andLA ¼ actual leaf area of the plant (Pearcy et al., 2004). Theself-shaded fraction (SS) of the crown leaf area was estimatedas SS ¼ (PA – DA)/PA, where PA ¼ projected leaf area andDA ¼ displayed leaf area. This parameter was averaged for
TABLE 1. Environmental and floristic data from five temperate rainforest sites in Chile and New Zealand
Soil total nutrient concentrations Common tree species
SiteGrid
referenceElevation
(m)MAT(8C) P (ppm.) N (ppm) C (%) C:N Angiosperms Conifers
Mean annual temperature (MAT) data were derived from Almeyda and Saez (1958) and National Institute of Water and Atmospheric Research(http://www.niwa.co.nz/our-science/climate/our-services/mapping). We assumed an adiabatic lapse rate of 0.65 8C 100 m21 in estimating site MAT fromdata obtained at the nearest meteorological stations.
*Species whose seedlings were studied.
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FI G. 1. Crown reconstructions of selected seedlings of temperate rainforest conifer and angiosperm trees, using YPLANT. Each row shows species from one site,from top to bottom, respectively, Los Mallines, Pino Huacho, Miranda, El Manzano, Anticura (see Table 1). Crown architecture was described in three dimen-
sions using a magnetic digitizer. Each section of the scale bar on the right ¼ 100 mm.
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the uppermost 80 sectors of the hemisphere, as under forestcanopies most direct photosynthetic photon flux density (PPFD)comes from angles .45 º above the horizontal, because ofthe effect of solar elevation on optical path length throughvegetation.
After harvesting plants, we calculated a new parameter thatintegrates the effects of biomass distribution and architecturaltraits on the effective leaf area that plants actually display: thedisplayed leaf area ratio (LARd). This was computed as DA/plant dry mass, after averaging DA for the uppermost 80sectors of the hemisphere. LARd was used as an indicator ofthe relative light interception potential of each of our studyspecies.
Our third question is about the relative importance of self-shading vs. other components of variation in LARd. This vari-able can be shown to be the product of leaf mass fraction(LMF), specific leaf area (SLA), self-shading and leaf angle,because:
LARd = DA/Mtot (2)
where Mtot ¼ total plant dry mass;
DA = PA × (1 − SS) (3)
PA = LA × f (Angle) (4)
where f (Angle) is an adjustment function which depends onlyon leaf angle, and finally
LA = Mleaf × SLA (5)
It follows from eqns (2)–(5) that LARd ¼ Mleaf × SLA ×f(Angle) × (1 – SS)/Mtot ¼ LMF × SLA × f(Angle) × (1 –SS). By measuring these four components, we should beable to account for 100 % of variation in LARd. In reality,our study accounted for slightly less than 100 % of thisvariation, because of the difference between our averagingof DA over the upper half of the hemisphere [eqn (3)], andour simple calculation of leaf angles as departures from thehorizontal [eqn (1)].
Statistical analyses
Nested analysis of variance (ANOVA) was used to examinethe effects of site, lineage (conifer vs. angiosperm) and specieson leaf and whole-plant traits. As both lineages were repre-sented by different species at each site, we nested lineageswithin each site, and species within lineages.
Bivariate relationships among the measured leaf and whole-plant traits were measured using best-fit linear or log correla-tions of species averages. Because of ontogenetic variationin many traits, some relationships were influenced by seedlingsize; relationships were therefore assessed separately for small(50–149 mm) and large (150–349 mm) seedlings. We alsoused COMPARE (Martins, 2004) to carry out phylogeneticallyindependent contrasts of bivariate relationships among leaf,crown and biomass distribution traits (Felsenstein, 1985;Harvey and Pagel, 1991). This approach enabled us to differ-entiate between (a) any patterns attributable to the ancient
divergence of angiosperms and conifers, and (b) moregeneral relationships occurring more universally across seedplants, irrespective of phylogenetic relationships (Ackerlyand Reich, 1999). A phylogenetic tree was constructed usingStevens (2001) and Biffin et al. (2012) as sources for angio-sperm and coniferous clades, respectively (SupplementaryData Fig. S1).
We used observed-variable structural equation modelling(SEM) (Wright, 1934; Shipley, 2000) to gain a multivariateperspective on how leaf, crown and biomass distributiontraits shape interspecific variation in self-shading and leafarea display. Structural equation models are systems of linearequations used to model relationships of implied conditionaldependency among variables, and to test whether the covari-ance structure of the empirical data matches the structureimplied by the multivariate model. We used a multigroupmodel to examine trait relationships within the two seedlingsize classes simultaneously; thus, any differences betweenthe two models can be attributed to an interaction with seed-ling size. The multigroup model was first evaluated usingcross-species trait covariances (n ¼ 18). The final model struc-ture of the cross-species analysis was used to evaluate phylo-genetically independent contrasts (n ¼ 17). We fixed theintercepts of this model to zero (Grafen, 1992), thereby in-creasing the d.f. of this model by 4. Cross-species correlationsamong all the measured variables are given in SupplementaryData Table S1, as are the results of phylogenetically independ-ent contrasts.
Our initial model (not illustrated) consisted of two linearequations where self-shading was hypothesized to be a func-tion of leaf number, leaf shape, leaf length, leaf angle and spe-cific leaf area (SLA), and leaf area display (LARd) a functionof leaf mass fraction, self-shading, leaf angle and SLA. Thisinitial model tests the hypothesis that the effects of leafnumber, leaf shape and lamina length on LARd are indirectlymediated through self-shading. Total leaf length (lamina pluspetiole) was chosen as the most informative variable amonga suite of collinear leaf size traits; initial trials indicated thatoverall, total leaf length explained more variation in self-shading and LARd than petiole length or the area of individualleaves. The explanatory power of lamina length was similar tothat of total leaf length, but the latter was preferred as integrat-ing more information about shoot architecture. The averagelight environment occupied by each species (percentagecanopy openness) was originally considered as an external in-fluence on leaf angles and SLA, but was dropped when foundto have very little explanatory power.
We used maximum likelihood estimates and a x2 goodnessof fit measure to evaluate model adequacy with Mplus soft-ware (Muthen and Muthen, 2005). The standardized residualcovariance matrix and modification indices were used toobtain a final model that fit the observed data. Model fit statis-tics evaluate the discrepancy between the covariance structureof the observed data and the covariance structure implied bythe model. Therefore, well fitting models yield small x2
values and large P-values (.0.05), indicating no significantdifference between model and data. We report the standardizedpath coefficients to illustrate the relative strengths of each rela-tionship. Standardized path coefficients indicate the change instandard deviations of the dependent variable due to a change
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of one standard deviation of the independent variable. Unlikecorrelation coefficients (i.e. r), these path coefficients arenot necessarily bounded by the envelope between –1 and 1.We also report, in Table S2 of Supplementary Data, theunstandardized coefficients in equation form for the analysisusing cross-species covariances.
RESULTS
Differences between conifers and angiosperms
In both size classes, conifer and angiosperm seedlings signifi-cantly differed in all measured leaf, crown and biomass distri-bution traits (Table 2; Figs 2 and 3). Angiosperm leaves wereon average longer than those of conifers, and their widest pointswere displaced proportionally further away from the stem.Angiosperms developed larger SLAs and allocated morebiomass to leaves, although the latter difference was lesspronounced in larger seedlings (Figs 2 and 3). Angiospermseedlings had shallower leaf angles and less self-shading thanthose of conifers. The result of these differences in leaf,crown and biomass distribution traits was that angiosperms dis-played about twice as much foliage area per unit plant biomassas conifers: LARd of small seedlings showed minimal overlapbetween the two lineages (Fig. 2), and that of large seedlings,no overlap at all (Fig. 3).
Although there was significant interspecific variation inthe mean light environments occupied by seedlings, therewas no significant difference between conifers and angios-perms overall (Table 2).
Site differences
There was significant site-to-site variation in all measuredleaf, crown and biomass distribution traits of seedlings inboth size classes, as well as in the mean light environmentsoccupied by seedlings (Table 2).
Of the environmental variables that were measured orestimated (Table 1), soil C:N ratio was the only one thatclearly differentiated sites where conifers were abundant
TABLE 2. Summary of nested ANOVA testing for trait differencesbetween sites, lineages (conifer vs. angiosperm) and species, aswell as differences in mean light environments occupied by
(Los Mallines, Pino Huacho and Miranda) from those whereconifers were uncommon (El Manzano) or absent (Anticura).Soil C:N ratio was negatively correlated with average LARd
of all study species at each site (Fig. 4).
Determinants of variation in self-shading and leaf area display
The initial structural equation model did not fit the cross-species data well (x2 ¼ 40.7, d.f. ¼ 12, P ¼ 0.0001). After
removing leaf shape from the model, and adding pathwaysfrom leaf angle to self-shading and from leaf number toLARd, a good fit was achieved (Fig. 5A, B; x2 ¼ 6.8, d.f. ¼ 6,P ¼ 0.34). When this same model structure was used to evalu-ate phylogenetically independent contrasts, a good fit wasagain found (Fig. 5C, D; x2 ¼ 13.5, d.f. ¼ 10, P ¼ 0.20).
Leaf area display of small seedlings was shaped mainly bybiomass distribution traits (Fig. 5A, C). Although self-shadingwas strongly negatively influenced by leaf length, species dif-ferences in self-shading contributed very little to variation inLARd, which was driven primarily by SLA, and to a lesserextent by leaf mass fraction (Fig. 5). As a result, none of thetraits we studied appeared to influence LARd of small seed-lings indirectly through the mediating effects of self-shading.Cross-species correlations and independent contrasts yieldedvery similar results, suggesting that the traits responsible fordifferences in self-shading and leaf area display between con-ifers and angiosperms were essentially the same as thoseshaping patterns across more recent divergences (Fig. 5A, C).
Self-shading of large seedlings was determined mainly byleaf number and angle, rather than lamina length (Fig. 5B).Species differences in self-shading were in turn a major deter-minant of variation in LARd of large seedlings; SLA exerted a
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FI G. 3. Leaf and whole-plant traits of large seedlings (150–349 mm tall) oftemperate rainforest conifers (n ¼ 6) and angiosperms (n ¼ 12). Box plots
show the range, upper and lower quartiles, and median.
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FI G. 4. Relationships of displayed leaf area ratio (LARd) to soilcarbon-to-nitrogen ratio, at five temperate rainforest sites. (A) Small seedlings(50–149 mm tall); (B) large seedlings (50–149 mm tall). Triangles showmeans of all species studied at each site, with lines showing significant fitsat P ¼ 0.05. Circles show means of angiosperm species only (no significant fit).
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similarly strong influence, and leaf angle and leaf mass fractionmade lesser but nevertheless significant contributions (Fig. 5).In large seedlings, leaf number and angle therefore indirectlyinfluenced LARd through the mediating effects of self-shading,and leaf angle also has exerted a direct influence on LARd.Cross-species correlations and independent contrasts againyielded very similar results (Fig. 5B, D).
DISCUSSION
In agreement with our hypothesis, conifer seedlings on averageself-shaded more than angiosperms (Table 2), despite consid-erable overlap between the two lineages (Figs 2 and 3). As pre-dicted, in small seedlings this pattern was shaped mainly bydifferences in leaf length (Fig. 5). This result correspondswell with Falster and Westoby (2003), who reported that leafsize was the most important determinant of interspecific
variation in self-shading of woody angiosperms in Australiansclerophyll forest. In large seedlings, in contrast, the lesserself-shading of angiosperms was primarily the result of theirhaving far fewer leaves on average than conifers (Fig. 5). Inboth size classes, the similarity of results from phylogenetical-ly independent contrasts and cross-species analyses suggeststhat the traits underlying interspecific variation in self-shadingacross the data set were essentially the same as those determin-ing differences between the two lineages (Fig. 5). Theincreased influence of leaf number on self-shading in thelarger size class in part reflects the manifestation of speciesdifferences in leaf life span. Although leaf life span was notmeasured in the present study, data collated from previouswork on 16 of the 18 species (Lusk and Contreras, 1999;Lusk, 2001; Lusk et al., 2003, 2011) confirm that leaf lifespans are much more strongly correlated with self-shading oflarge seedlings (r ¼ 0.71, P ¼ 0.002) than with that of small
c2 = 6·8, d.f. = 6, P = 0·34
c2 = 13·5, d.f. = 10, P = 0·20
A
C D
B
Independentcontrasts
Leaf number
0·38
–0·27
Small seedlings
–0·50
–0·37–0·15
SLA
0·03R2
= 0·71 R2 = 0·98
0·64
0·40
Whole-plant traits
Leaf traits
Leaf length
Acrossspecies
Leaf angle
Self-shading
LMF
LARd
Leaf number
0·29
–0·25
–0·55
–0·20
–0·01
–0·28
SLA
R2 = 0·68 R2
= 0·96
0·75
0·57
Whole-plant traits
Leaf traits
Leaf length
Leaf angle
Self-shading
LMF
LARd
Leaf number
1·10
–0·06
Large seedlings
–0·20
–0·53
–0·47
–0·37
SLA
R2 = 0·73 R2
= 0·98
0·56
0·27
Whole-plant traits
Leaf traits
Leaf length
Leaf angle
Self-shading
LMF
LARd
Leaf number
0·54
0·07
–0·16
–0·68
–0·41
–0·41
SLA
R2 = 0·67 R2
= 0·96
0·67
0·39
Whole-plant traits
Leaf traits
Leaf length
Leaf angle
Self-shading
LMF
LARd
FI G. 5. Final structural equation models illustrating how leaf and whole-plant traits influence self-shading and leaf area display (LARd) in 18 temperate rainforesttree species in small (50–149 mm) and large (150–350 mm) seedling size classes. The top row (A, B) shows results for cross-species correlations (n ¼ 18) andthe bottom row (C, D) shows results based on phylogenetically independent contrasts (n ¼ 17). Thick arrows represent significant standardized path coefficients(P , 0.05), whereas dashed pathways are not significant (P . 0.05). The sizes of the arrows are proportional to the strength of the relationships. Path coefficientsindicate the change in standard deviations of the dependent variable due to a change of one standard deviation of the independent variable. Bivariate correlations
among all variables are given in Supplementary Data Table S1.
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seedlings (r ¼ 0.40, P ¼ 0.13). Overlap in self-shadingbetween the two lineages in our study reflects overlap in leaflength and number (Figs 2 and 3); notably, self-shading ofthe conifer Podocarpus saligna, which deployed relativelyfew, but long, leaves (Fig. 1), was slight enough to rival thatof large-leaved angiosperms such as Drimys winteri andPersea lingue (Table 3).
Seedling size modulated the relative importance of self-shading and other traits in determining the effective leaf areadisplayed by plants at a given size. Although LARd of smallseedlings was largely a function of biomass distributiontraits, self-shading vied with SLA as the main control onLARd of large seedlings. Again, phylogenetic relationshipshad little bearing on this pattern (Fig. 5), indicating that themain traits underlying interspecific variation in LARd acrossthe data set were the same as those determining the substantial
differences in LARd between the two lineages (Figs 2 and 3).It has previously been shown that evergreen angiosperm treestend to have larger SLA than their coniferous associates,coupled to differences in leaf life span (Lusk et al., 2003;Lusk, 2011); on the other hand, we are not aware of previouswork comparing self-shading in these two lineages.Unexpectedly, differences in leaf angles also contributed toangiosperms displaying larger effective leaf areas than conifers(Figs 2, 3 and 5). Although leaf angles are known to differwidely across plant species (e.g. Barclay, 2001; Falster andWestoby, 2003), we are unaware of previous studies showingdifferences between conifers and angiosperms.
The reported differences in LARd suggest a 2-fold angio-sperm advantage in average light interception per unit whole-plant biomass. Despite our relatively small sample sizes, thereare several grounds for believing that this pattern is likely to
TABLE 3. Mean light environments, leaf, biomass distribution and crown traits of seedling conifers and angiosperms from Chileanand New Zealand temperate rainforests
‘Widest point of leaf’ refers to the distance of the widest point of the leaf from the base of the petiole, as a fraction of total leaf length; LMF, leaf massfraction; SLA, specific leaf area; LARd, displayed leaf area.
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hold across temperate rainforests in general: the wide ranges ofleaf number and size encompassed by our data set (Figs 2 and3), the categorical differences in LARd between the twolineages (Figs 2 and 3) and the very weak influence of phy-logenetic relationships on results (Fig. 5). The 3-D technologywe used for describing architecture and modelling leaf displaydoes not accommodate species with scale-like leaves, whichmake up .40 % of the coniferous flora of the humid temperateforests of the southern hemisphere (Enright and Hill, 1995).However, data obtained using a simpler 2-D approach showthat the average shoot LARd of three temperate rainforest con-ifers with small scale-like leaves (Dacrycarpus dacrydioides,Dacrydium cupressinum and Halocarpus biformis) was slight-ly lower than the average of six laminate-leaved conifers(Leverenz et al., 2000), providing further evidence that the dif-ferences in LARd reported in our study may be representativeof temperate rainforests in general.
Allied to differences in leaf vascularization and assimilationrates (Brodribb and Feild, 2000; Lusk et al., 2003; Brodribbet al., 2005), an advantage in LARd may explain angiospermdominance on productive sites in temperate forests. In thisrespect it is noteworthy that the angiosperms with the largestLARd occurred on sites where low soil C:N ratios suggestrapid decomposition rates and relatively high nutrient avail-ability (Fig. 4). These were sites where conifers were eitherabsent (Anticura) or else a sub-ordinate component of thevegetation (El Manzano) (Table 1). The presence of conifer-dominant or mixed stands on harsher sites reflects the factthat the superior net carbon gain potential of angiospermswill not be realized under all conditions. Under cold condi-tions, greater susceptibility to freeze–thaw embolism willreduce or nullify the potential carbon gain advantages ofvessel-bearing angiosperms (Feild and Brodribb, 2001), andin nutrient-poor habitats some angiosperms may struggle toobtain enough nutrients to sustain their more rapid foliageturnover (Escudero et al., 1992). Those angiosperms that docoexist with conifers on harsh sites tend to have more conser-vative functional traits than their counterparts native to moreproductive sites, e.g. small conduits on cold sites (Feild andBrodribb, 2001), and low specific leaf areas on nutrient-poorsites (Midgley et al., 1995).
We found no significant effect of leaf shape on self-shadingor leaf area display. Work elsewhere has supported the expect-ation that obovate or oblanceolate leaves should intercept lightmore efficiently than leaves that are widest near the base(Pearcy et al., 2004). In our study, however, leaf shape – asindexed by the position of the widest point – did not haveany significant explanatory power once leaf length and leafnumber were taken into account (Fig. 5). This reflects the col-linearity of leaf shape with both these other variables in ourdata set (Supplementary Data Table S1). It is also possiblethat other, unquantified, aspects of leaf shape influenced inter-specific variation in self-shading and leaf area display in ourdata set.
Our study complements recent advances in leaf hydraulicsby showing for the first time that the ability to deployfoliage in relatively few, large leaves has important conse-quences for the light interception potential of juvenile trees.The advantage of vessels over tracheids in productive environ-ments has been well established (Zimmerman and Brown,
1971; Sperry et al., 2006), but the evolution of hydraulicsystems capable of adequately irrigating broad laminas maybe of comparable importance. The single-veined condition ofmost conifer leaves imposes a severe constraint on laminawidth (Brodribb et al., 2007); this also appears to constrainleaf length in conifers indirectly, presumably because the dis-proportionate increase in support requirements with the lengthof cantilevered structures (Gere and Timoshenko, 1997;Niinemets et al., 2007) outweighs the increase in light inter-ception if lamina width cannot be increased (Brodribb et al.,2010). Podocarpus saligna is an example of a conifer that isable to develop quite large leaves that minimize self-shading(Fig. 1, Tables 2 and 3), because of the abundant developmentof accessory transfusion tracheids that conduct water to meso-phyll tissues distant from the midvein. Accessory transfusiontissue is well developed in large-leaved podocarps from warm-temperate to tropical regions (Buchholz and Gray, 1948;Brodribb et al., 2007) but scarce or absent in small-leavedspecies from colder regions, such as Saxegothaea conspicua(T.J. Brodribb, pers. comm.), suggesting some type of climaticconstraint on the viability of this system. Some lowland trop-ical and sub-tropical podocarps have much larger leaves thanP. saligna, possibly enabling more efficient leaf displaythan that reported for any conifer in the present study. Forreasons that are not well understood, angiosperm leaves alsotend to be larger in tropical forests (Webb, 1968); a tropicalcounterpart of the present study would be very informative,to determine whether angiosperm advantages in light intercep-tion potential extend to warmer climates. The performance ofthe angiosperm D. winteri is another potent demonstration ofthe importance of leaf hydraulics for light interception andcarbon gain potential of seedlings. Despite lacking vessels,D. winteri has reticulate venation, enabling the deploymentof large leaves that conferred one of the lowest levels ofself-shading in both size classes (Table 3).
Although YPLANT assumes parallel solar beam geometryand therefore ignores penumbral effects, this omission is un-likely to have much impact on calculations of self-shadingby plants of the sizes we studied. Stenberg (1995) simulatedthe impact of penumbral effects on light interception andphotosynthesis of Pinus sylvestris L. shoots. She found that al-though the shading of one shoot by another .250 mm awaywas dominated by penumbra, the assumption of parallelsolar beam geometry within a shoot ,250 mm long did notlead to serious underestimates of the rate of carbon gain.Umbral lengths within canopies are proportional to leafwidth (Horn, 1971) and, as leaves of all of the species in thepresent study are broader than those of P. sylvestris, penumbraleffects should not be a significant influence on light intercep-tion and carbon gain over the range of seedling sizes that westudied. Penumbral effects will increasingly dominate lightenvironments within crowns of small-leaved species as theygrow taller (Stenberg, 1995), and probably explain the highleaf area indices and/or deep crowns developed by adulttrees of some conifers (e.g. Gower et al., 1993; Whiteheadet al., 2004). Stenberg (1995) showed that the shade cast bya P. sylvestris shoot situated further away than approx.250 mm from the target point could be best characterized as‘diffuse’, due to the prevalence of penumbra. Carbon gain ofshaded foliage within conifer canopies can thus be
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considerably higher than that predicted by models assumingparallel solar beam geometry, i.e. assuming that all foliageobscured by other leaves is in umbra (Stenberg, 1995).
Although the first explanations of the rise of the angios-perms emphasized their reproductive innovations (Raven,1977; Regal, 1977), our data support the more recent proposalthat features of angiosperm vegetative form and function maybe at least as important (Bond, 1989). This study adds signifi-cantly to evidence for the paramount importance of vascularinnovations in determining the outcome of plant competitionin productive habitats (Zimmerman and Brown, 1971;Brodribb et al., 2010), by influencing the efficiency of lightcapture – and presumably carbon gain – per unit of plantbiomass.
SUPPLEMENTARY DATA
Supplementary data are available online at www.aob.oxford-journals.org and consist of the following. Figure S1: phylogen-etic tree showing inferred evolutionary relationships among 18conifer and angiosperm tree species from temperate rainforestsin Chile and New Zealand. Table S1: correlations among lightenvironment, leaf, biomass distribution and crown traits oftemperate rainforest conifer and angiosperms, for small andlarge seedlings. Table S2: structural equations with unstandar-dized coefficients using the cross-species dataset.
ACKNOWLEDGEMENTS
We thank FONDECYT for funding through grant 1030811, theAustralian Research Council for Discovery grant 1094606,CONAF for permission to work in Parque NacionalPuyehue, and the New Zealand Department of Conservationfor permission to work in the Miranda Scientific Reserve.
LITERATURE CITED
Ackerly DD, Reich PB. 1999. Convergence and correlations among leaf sizeand function in seed plants: a comparative test using independent con-trasts. American Journal of Botany 86: 1272–1281.
Almeyda E, Saez F. 1958. Recopilacion de datos climaticos de Chile y mapassinopticos respectivos. Santiago de Chile: Ministerio de Agricultura.
Barclay HJ. 2001. Distribution of leaf orientations in six conifer species.Canadian Journal of Botany 79: 389–397.
Becker P. 2000. Competition in the regeneration niche between conifersand angiosperms: Bond’s slow seedling hypothesis. Functional Ecology14: 401–412.
Benton MJ. 1991. Extinction, biotic replacements and clade interactions.In: Dudley EC. ed. The unity of evolutionary biology, Vol. 1. Portland,OR: Dioscorides, 89–102.
Biffin E, Brodribb TJ, Hill RS, Thomas P, Lowe AJ. 2012. Leaf evolution inSouthern Hemisphere conifers tracks the angiosperm ecological radiation.Proceedings of the Royal Society B: Biological Sciences 279: 341–348.
Bond WJ. 1989. The tortoise and hare: ecology of angiosperm dominance andgymnosperm persistence. Biological Journal of the Linnean Society36: 227–249.
Brodribb TJ, Feild TS. 2000. Stem hydraulic supply is linked to leaf photo-synthetic capacity: evidence from New Caledonian and Tasmanian rain-forests. Plant, Cell and Environment 23: 1381–1388.
Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B. 2005. Leaf hydraul-ic capacity in ferns, conifers and angiosperms: impacts on photosyntheticmaxima. New Phytologist 165: 839–846.
Brodribb T, Feild T, Jordan G. 2007. Leaf maximum photosynthetic rate andvenation are linked by hydraulics. Plant Physiology 144: 1890–1898.
Brodribb TJ, Feild TS, Sack L. 2010. Viewing leaf structure and evolutionfrom a hydraulic perspective. Functional Plant Biology 37: 488–498.
Buchholz JT, Gray NE. 1948. A taxonomic revision of Podocarpus. I. Thesections of the genus and their subdivisions with special reference toleaf anatomy. Journal of the Arnold Arboretum 29: 49–63.
Burns BR, Leathwick JR. 1996. Vegetation–environment relationships atWaipoua Forest, Northland, New Zealand. New Zealand Journal ofBotany 34: 79–92.
Cornelissen JHC, Diez PC, Hunt R. 1996. Seedling growth, allocation andleaf attributes in a wide range of woody plant species and types.Journal of Ecology 84: 755–765.
Duursma RA, Falster DS, Valladares F, et al. 2012. Light interception effi-ciency explained by two simple variables: a test using a diversity ofsmall- to medium-sized woody plants. New Phytologist 193: 397–408.
Enright NJ, Hill RS. 1995. Ecology of the Southern conifers. Melbourne:Melbourne University Press.
Escudero A, Delarco JM, Sanz IC, Ayala J. 1992. Effects of leaf longevityand retranslocation efficiency on the retention time of nutrients in the leafbiomass of different woody species. Oecologia 90: 80–87.
Falster DS, Westoby M. 2003. Leaf size and angle vary widely across species:what consequences for light interception? New Phytologist 158:509–525.
Feild TS, Brodribb T. 2001. Stem water transport and freeze–thaw xylemembolism in conifers and angiosperms in a Tasmanian treeline heath.Oecologia 127: 314–320.
Felsenstein J. 1985. Phylogenies and the comparative method. AmericanNaturalist 125: 1–15.
Florin R. 1963. The distribution of conifer and taxad genera in time and space.Acta Horticulturae Bergiani 20: 121–312.
Frazer GW, Canham CD, Lertzman KP. 1999. Gap Light Analyzer (GLA),Version 2.0: imaging software to extract canopy structure and gap lighttransmission indices from true-colour fisheye photographs, usersmanual and program documentation. Simon Fraser University,Burnaby, British Columbia, and the Institute of Ecosystem Studies,Millbrook, New York.
Galvez D, Pearcy RW. 2003. Petiole twisting in the crowns of Psychotrialimonensis: implications for light interception and daily carbon gain.Oecologia 135: 22–29.
Gower ST, Reich PB, Son Y. 1993. Canopy dynamics and aboveground pro-duction of five tree species with different leaf longevities. TreePhysiology 12: 327–345.
Grafen A. 1992. The uniqueness of the phylogenetic regression. Journal ofTheoretical Biology 156: 405–423.
Hanan JS, Room PM. 1997. Practical aspects of virtual plant research. In:Michalewicz MT. ed. Plants to ecosystems: advances in computationallife sciences. Melbourne, Australia: CSIRO, 28–44.
Harvey PH, Pagel M. 1991. The comparative method in evolutionary biology.Oxford: Oxford University Press.
Horn HS. 1971. The adaptive geometry of trees. Princeton, NJ: PrincetonUniversity Press.
Leverenz JW, Whitehead D, Stewart GH. 2000. Quantitative analyses ofshade-shoot architecture of conifers native to New Zealand. Trees:Structure and Function 15: 42–49.
Lupia R, Lidgard S, Crane PR. 1999. Comparing palynological abundanceand diversity: implications for biotic replacement during the Cretaceousangiosperm radiation. Paleobiology 25: 305–340.
Lusk CH. 2001. Leaf lifespans of some conifers of the temperate rainforests ofSouth America. Revista Chilena de Historia Natural 74: 711–718.
Lusk CH. 2011. Conifer–angiosperm interactions: physiological ecology andlife history. In: Turner BL, Cernusak LA. eds. Smithsonian Contributionsto Botany, no. 95: Ecology of the Podocarpaceae in tropical forests.Washington, DC: Smithsonian Institution Scholarly Press, 157–164.
Lusk CH, Contreras O. 1999. Foliage area and crown nitrogen turnover intemperate rain forest juvenile trees of differing shade tolerance. Journalof Ecology 87: 973–983.
Lusk CH, Matus F. 2000. Juvenile tree growth rates and species sorting onfine-scale soil fertility gradients in a Chilean temperate rain forest.Journal of Biogeography 27: 1011–1020.
Lusk CH, Wright I, Reich PB. 2003. Photosynthetic differences contribute tocompetitive advantage of evergreen angiosperm trees over evergreen con-ifers in productive habitats. New Phytologist 160: 329–336.
Lusk et al. — Leaf display by conifer and angiosperm seedlings 187
Dow
nloaded from https://academ
ic.oup.com/aob/article/110/1/177/2769002 by guest on 09 January 2022
Lusk CH, Perez-Millaqueo MM, Piper FI, Saldana A. 2011. Ontogeny, under-storey light interception and simulated carbon gain of juvenile rainforest ever-greens differing in shade tolerance. Annals of Botany 108: 419–428.
Martins EP. 2004.. COMPARE, version 4.6b. Computer programs for the stat-istical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Department of Biology, Indiana University,Bloomington, IN
Midgley JJ, Bond WJ, Geldenhuys CJ. 1995. The ecology of southernAfrican conifers. In: Enright NJ, Hill RS. eds. Ecology of the Southernconifers. Melbourne: Melbourne University Press, 64–80.
Miller CN. 1977. Mesozoic conifers. Botanical Review 43: 217–280.Muthen LK, Muthen BO. 2005. Mplus user’s guide. Los Angeles, California.Niinemets U, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F.
2007. Do we underestimate the importance of leaf size in plant econom-ics? Disproportional scaling of support costs within the spectrum of leafphysiognomy. Annals of Botany 100: 283–303.
Pearcy RW, Duursma RA, Falster DS, PrometheusWikicontributors.2011. Studying plant architecture with Y-plant and 3D digitising.Available online via http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Architecture [accessed 23 August 2011].
Pearcy RW, Valladares F, Wright SJ, de Paulis EL. 2004. A functional ana-lysis of the crown architecture of tropical forest Psychotria species: dospecies vary in light capture efficiency and consequently in carbon gainand growth? Oecologia 139: 163–177.
Pearcy RW, Yang WM. 1996. A three-dimensional crown architecture modelfor assessment of light capture and carbon gain by understory plants.Oecologia 108: 1–12.
Raven PH. 1977. A suggestion concerning the Cretaceous rise to dominanceof the angiosperms. Evolution 31: 451–452.
Read J. 1995. The importance of comparative growth rates in determining thecanopy composition of Tasmanian rainforest. Australian Journal ofBotany 43: 243–271.
Regal PJ. 1977. Ecology and evolution of flowering plant dominance. Science196: 622–629.
Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Bushena C.1998. Close association of RGR, leaf and root morphology,seed mass and shade tolerance in seedlings of nine borealtree species grown in high and low light. Functional Ecology 12:327–338.
Shipley B. 2000. Cause and correlation in biology: a user’s guide to path ana-lysis, structural equations and causal inference. Cambridge, UK:Cambridge University Press.
Sperry JS, Hacke UG, Pittermann J. 2006. Size and function of conifer trac-heids and angiosperm vessels. American Journal of Botany 93:1490–1500.
Stenberg P. 1995. Penumbra in within-shoot and between-shoot shading inconifers and its significance for photosynthesis. Ecological Modelling77: 215–231.
Stevens PF. 2001. Angiosperm Phylogeny Website. Version 9. MissouriBotanical Garden.
Turner BL, Cernusak LA. 2011. Ecology of the Podocarpaceae in tropicalforests. Washington, DC: Smithsonian Institution Scholarly Press.
Webb LJ. 1968. Environmental relationships of the structural types ofAustralian rainforest vegetation. Ecology 49: 296–311.
Whitehead D, Walcroft AS, Griffin KL, et al. 2004.. Scaling carbon uptakefrom leaves to canopies: insights from two forest with contrasting proper-ties. In: Mencuccini M, Grace JB, Moncrieff J, McNaughton KG. eds.Forests at the land–atmosphere interface. Wallingford, UK: CABInternational, 231–254.
Wright S. 1934. The method of path coefficients. Annals of Mathematics andStatistics 5: 161–215.
Zimmerman MH, Brown CL. 1971. Trees, structure and function.New York: Springer.
Lusk et al. — Leaf display by conifer and angiosperm seedlings188
Dow
nloaded from https://academ
ic.oup.com/aob/article/110/1/177/2769002 by guest on 09 January 2022
