Annals of Botany 110: 177 –188, 2012
doi:10.1093/aob/mcs095, available online at www.aob.oxfordjournals.org
PART OF A HIGHLIGHT ON TRAITS WITH ECOLOGICAL FUNCTIONS
Seedlings of temperate rainforest conifer and angiosperm trees differ
in leaf area display
Christopher H. Lusk1,*, Manuel M. Pérez-Millaqueo2, Alfredo Saldaña2, Bruce R. Burns3,
Daniel C. Laughlin1 and Daniel S. Falster4
1
Department of Biological Sciences, The University of Waikato, Private Bag 3105, Hamilton, New Zealand, 2Departamento de
Botánica, Universidad de Concepción, Concepción, 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 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 (LARd) was used to indicate plant light interception 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 (more
than leaf size), and on average their LARd was about twice that of conifers. Although specific leaf area was the most
pervasive 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 selfshading and enhancing seedling light interception potential per unit of plant biomass. This study adds significantly 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.
IN T RO DU C T IO N
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 accumulating 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 advantages 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 contribute 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 evergreen temperate forests of the southern hemisphere, many conifers 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
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178
Lusk et al. — Leaf display by conifer and angiosperm seedlings
seedlings are thus constrained to display their foliage in a
narrow cylinder around the stem; a large foliage area can
only be developed by accumulating large numbers of leaves,
probably resulting in heavy self-shading. The limitations
imposed by small leaves are illustrated by a comparative
study of 38 Australian woodland angiosperms (Falster and
Westoby, 2003): leaf size was strongly negatively correlated
with self-shading within shoots, and positively correlated
with the total foliage area per metre of stem. Duursma et al.
(2012) attribute this pattern to more pronounced foliage
clumping in small-leaved species. Continued growth of
petioles after lamina expansion gives some angiosperms an
additional option for ameliorating self-shading, enabling
plants to reposition leaves as they become shaded by newer
ones (Gálvez and Pearcy, 2003).
Here we examine the determinants of light interception
potential in conifer and angiosperm tree seedlings from temperate rainforest. Coexistence of conifers and evergreen angiosperms is common in the temperate forests of the southern
hemisphere, but, as in other biomes, conifers tend to be concentrated on cold and/or nutrient-poor sites (Read, 1995;
Burns and Leathwick, 1996; Lusk and Matus, 2000). We
addressed three questions. (1) Do conifer seedlings self-shade
more than competing angiosperm seedlings? (2) What traits
underlie variation in self-shading? (3) To what extent is seedling 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 distribution and leaf area of conifer and angiosperm seedlings from
five sites differing in climatic and edaphic characteristics,
and used the architectural model YPLANT (Pearcy and
Yang, 1996) to quantify variation in self-shading, leaf angles
and leaf display. We then used structural equation modelling
(Wright, 1934; Shipley, 2000) to obtain a multivariate perspective on how leaf, crown and biomass distribution traits shape
differences in self-shading and leaf area display.
M AT E R IA L S A ND M E T HO DS
Study sites and species
We sampled seedlings of common conifer and angiosperm
species, at four temperate rainforest sites in Chile and one in
New Zealand (Table 1), chosen to represent a range of climatic
and edaphic conditions. Conifers are a major component of the
forest overstorey at three of these sites (Los Mallines, Pino
Huacho and Miranda), a relatively minor component at one
site (El Manzano) and absent at another (Anticura). As
YPLANT and the software we used to capture plant architecture (FLORADIG) are able to deal adequately only with flattened leaves (excluding imbricate or needle-leaved taxa), our
selection of conifers was restricted to species from the
Podocarpaceae and Araucariacae; species with this type of
leaf form as juveniles make up slightly more than half of the
coniferous flora of the humid temperate forests of the southern
hemisphere (Enright and Hill, 1995). The six conifer species
that we sampled encompassed a wide range of leaf size
within these constraints (Fig. 1), and all are important overstorey dominants over extensive tracts of South American or
New Zealand rainforest. Leaves of five of the six conifers
were lanceolate or linear in shape. Although very young seedlings of the sixth conifer species (Phyllocladus trichomanoides) also produce linear leaves, these are succeeded by
rhombic phylloclades (Fig. 1). Leaves of the 12 angiosperm
species we sampled varied more widely in size and shape.
All had simple leaves, with shapes including lanceolate, oblanceolate, ovate, obovate, oblong and rhomboid (Fig. 1).
We sampled 15– 21 seedlings of each species, ranging in
height from 50 to 350 mm tall. This range of size enabled us
to examine the effect of early ontogeny on leaf, crown and
biomass distribution traits. We stratified our sampling within
this size range, deliberately choosing at least seven seedlings
of each species between 50 and 150 mm tall, and at least
seven more in the 150 –350 mm height range. Seedlings
were of each species chosen haphazardly from throughout
the range of light environments they were found to occupy
naturally.
Seedling light environments
Seedling light environments were quantified using hemispherical photography. A Nikon Coolpix 4500 digital camera
(Nikon Corporation, Japan) with a 183 º fisheye adaptor was
used to take a hemispherical photograph directly above each
seedling, 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 percentage
canopy openness above each plant.
Digital capture of seedling architecture
Each seedling was excavated carefully, removing a sod of
sufficient width and depth to include the root system, after
cutting through any intruding coarse roots from neighbouring
plants. Seedlings were transplanted to pots of sufficient size
to accommodate the excavated sod, taken to the laboratory,
and their architecture digitized within 3 d.
We used digital capture of plant architecture to create virtual
plants, which is much less time-consuming than the manual
methods often used in conjunction with YPLANT (Hanan
and Room, 1997; Falster and Westoby, 2003; Pearcy et al.,
2011). The 3-D leaf arrangement of each seedling was recorded using a FASTRAKw 3D-digitizer (Polhemus, Colchester,
VT, USA), in conjunction with the software package
FLORADIG (CSIRO Entomology, Brisbane, Australia). The
digitizer includes a magnetic signal receiver and pointer,
allowing the user to record the 3-D spatial co-ordinates of
the pointer within a hemisphere of 3 m diameter from the receiver. Individual plants are reconstructed virtually by recording a series of point co-ordinates, and the relevant connectivity
between points. Stem segments (and petioles, if present) are
characterized by their elevation angle, azimuth, length and
diameter. Individual leaves are characterized by their length
together with the azimuth and elevation angle of two vectors
on the lamina surface.
Model leaves, digitized in two dimensions, were used to
populate the nodes of each virtual plant. With the exception
of four markedly heteroblastic species (Aextoxicon punctatum,
Eucryphia cordifolia, Myrceugenia planipes and Phyllocladus
Lusk et al. — Leaf display by conifer and angiosperm seedlings
179
TA B L E 1. Environmental and floristic data from five temperate rainforest sites in Chile and New Zealand
Soil total nutrient concentrations
Common tree species
Site
Grid
reference
Elevation
(m)
MAT
(8C)
P (ppm.)
N (ppm)
C (%)
C:N
Angiosperms
Los
Mallines
40844’S,
72815’W
750
7.3
1746 + 260
1.17 + 0.07
33.5 + 3.0
28.7 + 2.1
Nothofagus nitida*,
N. dombeyi (Nothofagaceae),
Amomyrtus luma* (Myrtaceae)
Anticura
40839’S,
72811’W
350
9.6
1813 + 193
0.69 + 0.07
12.2 + 0.3
17.6 + 1.5
Pino
Huacho
37841’S,
73812’W
850
7.8
506 + 60
0.27 + 0.02
7.6 + 0.3
27.8 + 1.4
El
Manzano
37847’S,
72851’W
550
10.1
509 + 42
0.19 + 0.01
3.2 + 0.2
17.3 + 0.8
Miranda
37815’S,
175818’E
100
13.5
214 + 37
0.26 + 0.03
5.9 + 0.6
22.3 + 0.8
Laureliopsis philippiana*
(Atherospermataceae),
Aextoxicon puntatum*
(Aextoxicaceae), Eucryphia
cordifolia* (Cunoniaceae),
Myrceugenia planipes*
(Myrtaceae), Nothofagus
dombeyi (Nothofagaceae)
Drimys winteri* (Winteraceae),
Nothofagus dombeyi
*(Nothofagaceae)
Persea lingue* (Lauraceae),
Lomatia hirsuta* (Proteaceae),
Nothofagus obliqua
(Nothofagaceae)
Knightia excelsa* (Proteaceae),
Nothofagus truncata*
(Nothofagaceae), Kunzea
ericoides (Myrtaceae)
Conifers
Saxegothaea
conspicua*,
Podocarpus
nubigena*
(Podocarpaceae)
Araucaria araucana*
(Araucariaceae)
Podocarpus saligna*
(Podocarpaceae)
Agathis australis*
(Araucariaceae),
Phyllocladus
trichomanoides*
(Podocarpaceae)
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 from
data obtained at the nearest meteorological stations.
*Species whose seedlings were studied.
trichomanoides), one representative leaf of each species was
digitized, so that all virtual leaves of a given species had the
same fixed shape, despite variation in size. Myrceugenia planipes initially produces obovate leaves, which are succeeded
by apiculate, oblanceolate leaves after seedlings reach 8 –
10 cm tall. Eucryphia cordifolia initially develops obovate
leaves with toothed margins, succeeded by oblong leaves on
larger plants. The first few leaves of A. punctatum are orbicular, with shape shifting to oblanceolate on larger seedlings, and
eventually oblong on plants larger than those included in the
present study. Accordingly, we digitized two different leaf
shapes for this species, and used whichever was more appropriate for each plant. The complex growth dynamics of
P. trichomanoides required us to digitize three different
types of photosynthetic unit. The linear true leaves produced
by very young seedlings can persist for several years, and so
are often still present on older seedlings that develop
rhombic cladodes on both determinate and indeterminate
shoots. Determinate shoots typically bear 9 – 15 cladodes,
which are all displayed in roughly the same plane like the leaflets of a compound leaf (Fig. 1). As well a true leaf of
P. trichomanoides, we therefore also digitized a representative
determinate shoot, and a single cladode that was used to
populate indeterminate shoots.
After digitizing, plants were separated into leaf, stem and
root fractions, dried for at least 48 h at 65 8C, and then
weighed for determination of biomass parameters.
Self-shading, leaf angles and leaf display
The YPLANT software (Pearcy and Yang, 1996) was used
to quantify crown architectural properties. The 3-D description
of leaf arrangement of each seedling, as recorded in
FLORADIG, was converted to the appropriate YPLANT
format using a program written in the C programming
language (Falster and Westoby, 2003).
As light interception by plant crowns is determined by leaf
inclination angles as well as overlap among leaves (i.e. selfshading), we used YPLANT output to estimate both these
parameters. YPLANT output includes leaf area projected
towards each of 160 sectors of the hemisphere (20 elevation
classes × 8 azimuth classes) without taking into account
overlap of leaves, and leaf area displayed towards each
sector, i.e. the effective area for light interception (Pearcy
and Yang, 1996). The mean leaf elevation angle of a plant
crown, weighted by the size of individual leaves, can be
estimated as:
Angle = arccosine (PAV /LA)
(1)
where PAV ¼ leaf area projected towards the vertical, and
LA ¼ actual leaf area of the plant (Pearcy et al., 2004). The
self-shaded fraction (SS) of the crown leaf area was estimated
as SS ¼ (PA – DA)/PA, where PA ¼ projected leaf area and
DA ¼ displayed leaf area. This parameter was averaged for
180
Lusk et al. — Leaf display by conifer and angiosperm seedlings
Nothofagus nitida
Amomyrtus luma
Saxegothaea conspicua
Nothofagus dombeyi
Drimys winteri
Araucaria araucana
Nothofagus truncata
Knightia excelsa
Lomatia hirsuta
Eucryphia cordifolia
Persea lingue
Myrceugenia planipes
Phyllocladus trichomanoides
Podocarpus nubigena
Agathis australis
Podocarpus saligna
Aextoxicon punctatum
Laureliopsis philippiana
F I 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 dimensions using a magnetic digitizer. Each section of the scale bar on the right ¼ 100 mm.
Lusk et al. — Leaf display by conifer and angiosperm seedlings
the uppermost 80 sectors of the hemisphere, as under forest
canopies most direct photosynthetic photon flux density (PPFD)
comes from angles .45 º above the horizontal, because of
the effect of solar elevation on optical path length through
vegetation.
After harvesting plants, we calculated a new parameter that
integrates the effects of biomass distribution and architectural
traits on the effective leaf area that plants actually display: the
displayed leaf area ratio (LARd). This was computed as DA/
plant dry mass, after averaging DA for the uppermost 80
sectors of the hemisphere. LARd was used as an indicator of
the relative light interception potential of each of our study
species.
Our third question is about the relative importance of selfshading vs. other components of variation in LARd. This variable 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 only
on 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 be
able to account for 100 % of variation in LARd. In reality,
our study accounted for slightly less than 100 % of this
variation, because of the difference between our averaging
of DA over the upper half of the hemisphere [eqn (3)], and
our simple calculation of leaf angles as departures from the
horizontal [eqn (1)].
Statistical analyses
Nested analysis of variance (ANOVA) was used to examine
the effects of site, lineage (conifer vs. angiosperm) and species
on leaf and whole-plant traits. As both lineages were represented by different species at each site, we nested lineages
within each site, and species within lineages.
Bivariate relationships among the measured leaf and wholeplant traits were measured using best-fit linear or log correlations of species averages. Because of ontogenetic variation
in many traits, some relationships were influenced by seedling
size; relationships were therefore assessed separately for small
(50 – 149 mm) and large (150 –349 mm) seedlings. We also
used COMPARE (Martins, 2004) to carry out phylogenetically
independent contrasts of bivariate relationships among leaf,
crown and biomass distribution traits (Felsenstein, 1985;
Harvey and Pagel, 1991). This approach enabled us to differentiate between (a) any patterns attributable to the ancient
181
divergence of angiosperms and conifers, and (b) more
general relationships occurring more universally across seed
plants, irrespective of phylogenetic relationships (Ackerly
and Reich, 1999). A phylogenetic tree was constructed using
Stevens (2001) and Biffin et al. (2012) as sources for angiosperm and coniferous clades, respectively (Supplementary
Data Fig. S1).
We used observed-variable structural equation modelling
(SEM) (Wright, 1934; Shipley, 2000) to gain a multivariate
perspective on how leaf, crown and biomass distribution
traits shape interspecific variation in self-shading and leaf
area display. Structural equation models are systems of linear
equations used to model relationships of implied conditional
dependency among variables, and to test whether the covariance structure of the empirical data matches the structure
implied by the multivariate model. We used a multigroup
model to examine trait relationships within the two seedling
size classes simultaneously; thus, any differences between
the two models can be attributed to an interaction with seedling size. The multigroup model was first evaluated using
cross-species trait covariances (n ¼ 18). The final model structure of the cross-species analysis was used to evaluate phylogenetically independent contrasts (n ¼ 17). We fixed the
intercepts of this model to zero (Grafen, 1992), thereby increasing the d.f. of this model by 4. Cross-species correlations
among all the measured variables are given in Supplementary
Data Table S1, as are the results of phylogenetically independent contrasts.
Our initial model (not illustrated) consisted of two linear
equations where self-shading was hypothesized to be a function of leaf number, leaf shape, leaf length, leaf angle and specific leaf area (SLA), and leaf area display (LARd) a function
of leaf mass fraction, self-shading, leaf angle and SLA. This
initial model tests the hypothesis that the effects of leaf
number, leaf shape and lamina length on LARd are indirectly
mediated through self-shading. Total leaf length (lamina plus
petiole) was chosen as the most informative variable among
a suite of collinear leaf size traits; initial trials indicated that
overall, total leaf length explained more variation in selfshading and LARd than petiole length or the area of individual
leaves. The explanatory power of lamina length was similar to
that of total leaf length, but the latter was preferred as integrating more information about shoot architecture. The average
light environment occupied by each species ( percentage
canopy openness) was originally considered as an external influence on leaf angles and SLA, but was dropped when found
to have very little explanatory power.
We used maximum likelihood estimates and a x2 goodness
of fit measure to evaluate model adequacy with Mplus software (Muthén and Muthén, 2005). The standardized residual
covariance matrix and modification indices were used to
obtain a final model that fit the observed data. Model fit statistics evaluate the discrepancy between the covariance structure
of the observed data and the covariance structure implied by
the model. Therefore, well fitting models yield small x2
values and large P-values (.0.05), indicating no significant
difference between model and data. We report the standardized
path coefficients to illustrate the relative strengths of each relationship. Standardized path coefficients indicate the change in
standard deviations of the dependent variable due to a change
182
Lusk et al. — Leaf display by conifer and angiosperm seedlings
of one standard deviation of the independent variable. Unlike
correlation coefficients (i.e. r), these path coefficients are
not necessarily bounded by the envelope between –1 and 1.
We also report, in Table S2 of Supplementary Data, the
unstandardized coefficients in equation form for the analysis
using cross-species covariances.
RES ULT S
Site differences
There was significant site-to-site variation in all measured
leaf, crown and biomass distribution traits of seedlings in
both size classes, as well as in the mean light environments
occupied by seedlings (Table 2).
Of the environmental variables that were measured or
estimated (Table 1), soil C:N ratio was the only one that
clearly differentiated sites where conifers were abundant
Response variable
Small seedlings
% canopy openness
Leaf mass fraction
Specific leaf area*
No. of leaves*
Leaf length*
Leaf angle
Self-shading
LARd*
Large seedlings
% canopy openness
Leaf mass fraction
Specific leaf area*
No. of leaves*
Leaf length*
Leaf angle
Self-shading
LARd*
Species
[lineage(site)]
(d.f. ¼ 9)
F
P
F
P
F
P
11.590
4.533
12.695
72.226
46.155
29.855
40.183
24.060
,0.001
0.002
,0.001
,0.001
,0.001
,0.001
,0.001
,0.001
1.333
9.172
26.464
76.000
16.165
20.898
40.087
64.444
0.261
0.000
0.000
0.000
0.000
0.000
0.000
0.000
6.943
6.671
17.097
9.684
23.675
4.120
28.385
6.385
,0.001
,0.001
,0.001
,0.001
,0.001
0.001
,0.001
,0.001
12.488
6.513
7.377
57.398
96.215
10.861
23.264
34.212
,0.001
,0.001
,0.001
,0.001
,0.001
,0.001
,0.001
,0.001
1.500
4.381
15.706
75.130
29.940
10.008
53.985
37.837
0.205
0.002
0.000
0.000
0.000
0.000
0.000
0.000
2.782
2.760
13.214
6.014
47.132
1.868
7.998
2.381
0.005
0.005
,0.001
,0.001
,0.001
0.061
,0.001
0.015
*Variables that were log-transformed before analysis.
Specific leaf area (cm–2 g–1)
400
200
100
0·8
0·7
0·6
0·5
0·4
0·3
0·2
60
Leaf angle (°)
Leaf mass fraction
0·3
50
40
30
50
20
128
30
64
25
32
16
8
Self-shading (%)
Site (d.f. ¼ 4)
Lineage(site)
(d.f. ¼ 4)
0·4
20
15
10
4
5
2
0
64
32
16
8
Displayed leaf area ratio (cm2 g–1)
Source of variation
0·5
0·2
Number of leaves per plant
TA B L E 2. Summary of nested ANOVA testing for trait differences
between sites, lineages (conifer vs. angiosperm) and species, as
well as differences in mean light environments occupied by
seedlings
0·6
Leaf length (mm)
In both size classes, conifer and angiosperm seedlings significantly differed in all measured leaf, crown and biomass distribution traits (Table 2; Figs 2 and 3). Angiosperm leaves were
on average longer than those of conifers, and their widest points
were displaced proportionally further away from the stem.
Angiosperms developed larger SLAs and allocated more
biomass to leaves, although the latter difference was less
pronounced in larger seedlings (Figs 2 and 3). Angiosperm
seedlings had shallower leaf angles and less self-shading than
those of conifers. The result of these differences in leaf,
crown and biomass distribution traits was that angiosperms displayed about twice as much foliage area per unit plant biomass
as conifers: LARd of small seedlings showed minimal overlap
between the two lineages (Fig. 2), and that of large seedlings,
no overlap at all (Fig. 3).
Although there was significant interspecific variation in
the mean light environments occupied by seedlings, there
was no significant difference between conifers and angiosperms overall (Table 2).
Position of widest point of leaf
Differences between conifers and angiosperms
80
40
20
10
5
Conifers Angiosperms
Conifers Angiosperms
F I G . 2. Leaf and whole-plant traits of small seedlings (50– 149 mm tall) of
temperate rainforest conifers (n ¼ 6) and angiosperms (n ¼ 12). Box plots
show the range, upper and lower quartiles, and median.
Lusk et al. — Leaf display by conifer and angiosperm seedlings
0·5
0·4
0·3
0·2
60
0·6
50
0·5
0·4
0·3
0·2
20
320
50
Self-shading (%)
40
20
40
30
5
0
64
32
16
8
Conifers Angiosperms
B
30
20
R2 = 0·89
10
15
20
128
64
All species
Angiosperms
0
20
25
30
Soil C:N ratio
10
10
R2 = 0·89
20
40
60
80
30
40
30
160
40
0
50
Average LARd (cm2 g–1)
Leaf angle (°)
120
A
10
60
Displayed leaf area ratio (cm2 g–1)
Leaf length (mm)
Number of leaves per plant
Specific leaf area (cm–2 g–1)
240
0·7
Average LARd (cm2 g–1)
Position of widest point of leaf
Leaf mass fraction
0·6
183
F I G . 4. Relationships of displayed leaf area ratio (LARd) to soil
carbon-to-nitrogen ratio, at five temperate rainforest sites. (A) Small seedlings
(50– 149 mm tall); (B) large seedlings (50–149 mm tall). Triangles show
means of all species studied at each site, with lines showing significant fits
at P ¼ 0.05. Circles show means of angiosperm species only (no significant fit).
32
16
8
Conifers Angiosperms
F I G . 3. Leaf and whole-plant traits of large seedlings (150–349 mm tall) of
temperate rainforest conifers (n ¼ 6) and angiosperms (n ¼ 12). Box plots
show the range, upper and lower quartiles, and median.
(Los Mallines, Pino Huacho and Miranda) from those where
conifers 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 crossspecies data well (x2 ¼ 40.7, d.f. ¼ 12, P ¼ 0.0001). After
removing leaf shape from the model, and adding pathways
from leaf angle to self-shading and from leaf number to
LARd, 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 evaluate phylogenetically independent contrasts, a good fit was
again 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 by
biomass distribution traits (Fig. 5A, C). Although self-shading
was strongly negatively influenced by leaf length, species differences in self-shading contributed very little to variation in
LARd, which was driven primarily by SLA, and to a lesser
extent by leaf mass fraction (Fig. 5). As a result, none of the
traits we studied appeared to influence LARd of small seedlings indirectly through the mediating effects of self-shading.
Cross-species correlations and independent contrasts yielded
very similar results, suggesting that the traits responsible for
differences in self-shading and leaf area display between conifers and angiosperms were essentially the same as those
shaping patterns across more recent divergences (Fig. 5A, C).
Self-shading of large seedlings was determined mainly by
leaf number and angle, rather than lamina length (Fig. 5B).
Species differences in self-shading were in turn a major determinant of variation in LARd of large seedlings; SLA exerted a
184
Lusk et al. — Leaf display by conifer and angiosperm seedlings
Small seedlings
Large seedlings
c2 = 6·8, d.f. = 6, P = 0·34
Whole-plant traits
Whole-plant traits
A
Leaf number
LMF
–0·27
B
Leaf number
LMF
–0·06
0·40
0·27
1·10
0·38
Across
species
Self-shading
LARd
0·03
R2 = 0·71
–0·50
Self-shading
R2 = 0·98
–0·20
Leaf length
–0·37
LARd
R2 = 0·98
–0·53
–0·37
–0·15
Leaf angle
–0·47
0·56
0·64
Leaf length
R2 = 0·73
Leaf angle
SLA
SLA
Leaf traits
Leaf traits
c2 = 13·5, d.f. = 10, P = 0·20
Whole-plant traits
Whole-plant traits
C
Leaf number
LMF
–0·25
Leaf number
D
LMF
0·07
0·39
0·57
0·54
0·29
Independent
contrasts
Self-shading
–0·01
–0·55
R2 = 0·68
Self-shading
LARd
–0·68
R2 = 0·96
–0·16
0·75
Leaf length
Leaf length
–0·20
R2 = 0·67
R2 = 0·96
0·67
–0·41
–0·41
–0·28
Leaf angle
LARd
SLA
Leaf traits
Leaf angle
SLA
Leaf traits
F I G . 5. Final structural equation models illustrating how leaf and whole-plant traits influence self-shading and leaf area display (LARd) in 18 temperate rainforest
tree 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) and
the 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 coefficients
indicate 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.
similarly strong influence, and leaf angle and leaf mass fraction
made lesser but nevertheless significant contributions (Fig. 5).
In large seedlings, leaf number and angle therefore indirectly
influenced 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 again
yielded very similar results (Fig. 5B, D).
DISCUSSION
In agreement with our hypothesis, conifer seedlings on average
self-shaded more than angiosperms (Table 2), despite considerable overlap between the two lineages (Figs 2 and 3). As predicted, in small seedlings this pattern was shaped mainly by
differences in leaf length (Fig. 5). This result corresponds
well with Falster and Westoby (2003), who reported that leaf
size was the most important determinant of interspecific
variation in self-shading of woody angiosperms in Australian
sclerophyll forest. In large seedlings, in contrast, the lesser
self-shading of angiosperms was primarily the result of their
having far fewer leaves on average than conifers (Fig. 5). In
both size classes, the similarity of results from phylogenetically independent contrasts and cross-species analyses suggests
that the traits underlying interspecific variation in self-shading
across the data set were essentially the same as those determining differences between the two lineages (Fig. 5). The
increased influence of leaf number on self-shading in the
larger size class in part reflects the manifestation of species
differences in leaf life span. Although leaf life span was not
measured in the present study, data collated from previous
work on 16 of the 18 species (Lusk and Contreras, 1999;
Lusk, 2001; Lusk et al., 2003, 2011) confirm that leaf life
spans are much more strongly correlated with self-shading of
large seedlings (r ¼ 0.71, P ¼ 0.002) than with that of small
Lusk et al. — Leaf display by conifer and angiosperm seedlings
185
TA B L E 3. Mean light environments, leaf, biomass distribution and crown traits of seedling conifers and angiosperms from Chilean
and New Zealand temperate rainforests
Species
Canopy
openness (%)
Small seedlings (50–149 mm tall)
Agathis australis
5.7
Araucaria araucana
6.2
Phyllocladus
11.5
trichomanoides
Saxegothaea conspicua
6.0
Podocarpus nubigena
3.5
P. saligna
11.2
Drimys winteri
6.1
Laureliopsis philippiana
3.3
Persea lingue
7.3
Knightia excelsa
3.5
Lomatia hirsuta
11.8
3.7
Aextoxicon punctatum
Amomyrtus luma
2.8
Myrceugenia planipes
3.0
Eucryphia cordifolia
4.4
Nothofagus truncata
9.8
N. dombeyi
8.2
N. nitida
9.1
Large seedlings (150–349 mm tall)
Agathis australis
6.9
Araucaria araucana
7.5
Phyllocladus
8.7
trichomanoides
Saxegothaea conspicua
4.1
Podocarpus nubigena
3.5
P. saligna
12.0
Drimys winteri
6.2
Laureliopsis
3.6
philippiana
Persea lingue
9.1
Knightia excelsa
6.7
Lomatia hirsuta
9.5
Aextoxicon punctatum
3.8
Amomyrtus luma
2.8
Myrceugenia planipes
3.5
Eucryphia cordifolia
4.2
Nothofagus truncata
11.2
N. dombeyi
9.5
N. nitida
11.3
LMF
SLA
(cm2 g21)
No. of
leaves
Leaf length
(mm)
Widest point
of leaf
Leaf
angle (8)
Self-shading
(%)
LARd
(cm2 g21)
0.39
0.29
0.41
85
80
86
14.7
77.7
16.0
26.5
11.9
12.3
0.40
0.23
0.55
45.5
46.5
38.4
7.8
32.1
26.6
18.4
8.3
22.3
0.33
0.27
0.38
0.49
0.32
0.33
0.47
0.57
0.37
0.30
0.43
0.43
0.48
0.42
0.49
119
117
175
101
163
203
102
111
158
237
165
171
270
187
123
45.2
45.0
16.4
10.0
11.0
3.1
8.6
9.8
5.6
15.0
10.4
9.9
12.2
17.4
11.4
13.1
12.1
29.5
45.8
34.0
42.8
56.2
50.5
37.5
15.9
22.4
18.8
24.3
16.5
17.9
0.49
0.37
0.46
0.62
0.52
0.57
0.60
0.53
0.61
0.45
0.74
0.56
0.47
0.44
0.30
48.0
45.2
55.1
42.7
29.6
40.9
38.9
46.0
32.0
32.8
23.6
27.2
28.5
31.3
27.0
14.9
16.6
4.6
3.4
16.4
2.0
4.4
13.0
7.9
17.4
15.8
14.3
14.6
19.1
15.5
17.8
14.9
30.7
30.7
36.9
42.7
30.3
36.5
39.5
39.6
43.2
50.1
78.9
43.9
37.8
0.38
0.32
0.38
80.3
97.1
77.1
45.4
211.6
71.7
39.8
14.1
16.2
0.40
0.23
0.52
42.5
44.3
42.2
15.4
42.7
21.4
15.1
6.7
16.1
0.31
0.31
0.34
0.41
0.36
80.9
83.5
124.5
83.9
160.3
163.7
114.0
32.1
12.3
19.4
13.2
19.5
55.0
77.6
61.7
0.49
0.37
0.46
0.62
0.52
47.5
42.5
55.8
46.5
32.3
18.3
27.4
7.4
5.9
17.4
10.0
9.6
18.5
18.9
36.6
0.36
0.42
0.52
0.44
0.38
0.46
0.43
0.27
0.33
0.38
171.9
93.8
89.1
113.5
140.3
126.9
123.6
198.3
141.1
96.2
7.1
13.0
11.8
13.1
28.7
15.8
19.0
36.4
47.0
33.5
53.7
100.0
66.1
74.1
28.8
43.7
45.7
21.4
17.4
20.0
0.57
0.60
0.54
0.53
0.45
0.48
0.61
0.47
0.44
0.30
41.5
37.7
32.8
36.7
37.9
30.2
28.6
35.3
36.3
40.9
7.9
7.4
17.7
14.5
14.1
18.4
20.2
16.4
18.8
15.8
38.0
24.2
27.0
28.2
28.7
35.3
33.9
42.2
23.9
19.9
‘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 mass
fraction; SLA, specific leaf area; LARd, displayed leaf area.
seedlings (r ¼ 0.40, P ¼ 0.13). Overlap in self-shading
between the two lineages in our study reflects overlap in leaf
length and number (Figs 2 and 3); notably, self-shading of
the conifer Podocarpus saligna, which deployed relatively
few, but long, leaves (Fig. 1), was slight enough to rival that
of large-leaved angiosperms such as Drimys winteri and
Persea lingue (Table 3).
Seedling size modulated the relative importance of selfshading and other traits in determining the effective leaf area
displayed by plants at a given size. Although LARd of small
seedlings was largely a function of biomass distribution
traits, self-shading vied with SLA as the main control on
LARd of large seedlings. Again, phylogenetic relationships
had little bearing on this pattern (Fig. 5), indicating that the
main traits underlying interspecific variation in LARd across
the 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 trees
tend 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 previous
work comparing self-shading in these two lineages.
Unexpectedly, differences in leaf angles also contributed to
angiosperms displaying larger effective leaf areas than conifers
(Figs 2, 3 and 5). Although leaf angles are known to differ
widely across plant species (e.g. Barclay, 2001; Falster and
Westoby, 2003), we are unaware of previous studies showing
differences between conifers and angiosperms.
The reported differences in LARd suggest a 2-fold angiosperm advantage in average light interception per unit wholeplant biomass. Despite our relatively small sample sizes, there
are several grounds for believing that this pattern is likely to
186
Lusk et al. — Leaf display by conifer and angiosperm seedlings
hold across temperate rainforests in general: the wide ranges of
leaf number and size encompassed by our data set (Figs 2 and
3), the categorical differences in LARd between the two
lineages (Figs 2 and 3) and the very weak influence of phylogenetic relationships on results (Fig. 5). The 3-D technology
we used for describing architecture and modelling leaf display
does not accommodate species with scale-like leaves, which
make up .40 % of the coniferous flora of the humid temperate
forests of the southern hemisphere (Enright and Hill, 1995).
However, data obtained using a simpler 2-D approach show
that the average shoot LARd of three temperate rainforest conifers with small scale-like leaves (Dacrycarpus dacrydioides,
Dacrydium cupressinum and Halocarpus biformis) was slightly lower than the average of six laminate-leaved conifers
(Leverenz et al., 2000), providing further evidence that the differences in LARd reported in our study may be representative
of temperate rainforests in general.
Allied to differences in leaf vascularization and assimilation
rates (Brodribb and Feild, 2000; Lusk et al., 2003; Brodribb
et al., 2005), an advantage in LARd may explain angiosperm
dominance on productive sites in temperate forests. In this
respect it is noteworthy that the angiosperms with the largest
LARd occurred on sites where low soil C:N ratios suggest
rapid decomposition rates and relatively high nutrient availability (Fig. 4). These were sites where conifers were either
absent (Anticura) or else a sub-ordinate component of the
vegetation (El Manzano) (Table 1). The presence of coniferdominant or mixed stands on harsher sites reflects the fact
that the superior net carbon gain potential of angiosperms
will not be realized under all conditions. Under cold conditions, greater susceptibility to freeze – thaw embolism will
reduce or nullify the potential carbon gain advantages of
vessel-bearing angiosperms (Feild and Brodribb, 2001), and
in nutrient-poor habitats some angiosperms may struggle to
obtain enough nutrients to sustain their more rapid foliage
turnover (Escudero et al., 1992). Those angiosperms that do
coexist with conifers on harsh sites tend to have more conservative functional traits than their counterparts native to more
productive sites, e.g. small conduits on cold sites (Feild and
Brodribb, 2001), and low specific leaf areas on nutrient-poor
sites (Midgley et al., 1995).
We found no significant effect of leaf shape on self-shading
or leaf area display. Work elsewhere has supported the expectation that obovate or oblanceolate leaves should intercept light
more efficiently than leaves that are widest near the base
(Pearcy et al., 2004). In our study, however, leaf shape – as
indexed by the position of the widest point – did not have
any significant explanatory power once leaf length and leaf
number were taken into account (Fig. 5). This reflects the collinearity of leaf shape with both these other variables in our
data set (Supplementary Data Table S1). It is also possible
that other, unquantified, aspects of leaf shape influenced interspecific variation in self-shading and leaf area display in our
data set.
Our study complements recent advances in leaf hydraulics
by showing for the first time that the ability to deploy
foliage in relatively few, large leaves has important consequences for the light interception potential of juvenile trees.
The advantage of vessels over tracheids in productive environments has been well established (Zimmerman and Brown,
1971; Sperry et al., 2006), but the evolution of hydraulic
systems capable of adequately irrigating broad laminas may
be of comparable importance. The single-veined condition of
most conifer leaves imposes a severe constraint on lamina
width (Brodribb et al., 2007); this also appears to constrain
leaf length in conifers indirectly, presumably because the disproportionate increase in support requirements with the length
of cantilevered structures (Gere and Timoshenko, 1997;
Niinemets et al., 2007) outweighs the increase in light interception if lamina width cannot be increased (Brodribb et al.,
2010). Podocarpus saligna is an example of a conifer that is
able to develop quite large leaves that minimize self-shading
(Fig. 1, Tables 2 and 3), because of the abundant development
of accessory transfusion tracheids that conduct water to mesophyll tissues distant from the midvein. Accessory transfusion
tissue is well developed in large-leaved podocarps from warmtemperate to tropical regions (Buchholz and Gray, 1948;
Brodribb et al., 2007) but scarce or absent in small-leaved
species from colder regions, such as Saxegothaea conspicua
(T.J. Brodribb, pers. comm.), suggesting some type of climatic
constraint on the viability of this system. Some lowland tropical and sub-tropical podocarps have much larger leaves than
P. saligna, possibly enabling more efficient leaf display
than that reported for any conifer in the present study. For
reasons that are not well understood, angiosperm leaves also
tend to be larger in tropical forests (Webb, 1968); a tropical
counterpart of the present study would be very informative,
to determine whether angiosperm advantages in light interception potential extend to warmer climates. The performance of
the angiosperm D. winteri is another potent demonstration of
the importance of leaf hydraulics for light interception and
carbon gain potential of seedlings. Despite lacking vessels,
D. winteri has reticulate venation, enabling the deployment
of large leaves that conferred one of the lowest levels of
self-shading in both size classes (Table 3).
Although YPLANT assumes parallel solar beam geometry
and therefore ignores penumbral effects, this omission is unlikely to have much impact on calculations of self-shading
by plants of the sizes we studied. Stenberg (1995) simulated
the impact of penumbral effects on light interception and
photosynthesis of Pinus sylvestris L. shoots. She found that although the shading of one shoot by another .250 mm away
was dominated by penumbra, the assumption of parallel
solar beam geometry within a shoot ,250 mm long did not
lead to serious underestimates of the rate of carbon gain.
Umbral lengths within canopies are proportional to leaf
width (Horn, 1971) and, as leaves of all of the species in the
present study are broader than those of P. sylvestris, penumbral
effects should not be a significant influence on light interception and carbon gain over the range of seedling sizes that we
studied. Penumbral effects will increasingly dominate light
environments within crowns of small-leaved species as they
grow taller (Stenberg, 1995), and probably explain the high
leaf area indices and/or deep crowns developed by adult
trees of some conifers (e.g. Gower et al., 1993; Whitehead
et al., 2004). Stenberg (1995) showed that the shade cast by
a 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 of
shaded foliage within conifer canopies can thus be
Lusk et al. — Leaf display by conifer and angiosperm seedlings
considerably higher than that predicted by models assuming
parallel solar beam geometry, i.e. assuming that all foliage
obscured by other leaves is in umbra (Stenberg, 1995).
Although the first explanations of the rise of the angiosperms emphasized their reproductive innovations (Raven,
1977; Regal, 1977), our data support the more recent proposal
that features of angiosperm vegetative form and function may
be at least as important (Bond, 1989). This study adds significantly to evidence for the paramount importance of vascular
innovations in determining the outcome of plant competition
in productive habitats (Zimmerman and Brown, 1971;
Brodribb et al., 2010), by influencing the efficiency of light
capture – and presumably carbon gain – per unit of plant
biomass.
S U P P L E M E N TARY D ATA
Supplementary data are available online at www.aob.oxfordjournals.org and consist of the following. Figure S1: phylogenetic tree showing inferred evolutionary relationships among 18
conifer and angiosperm tree species from temperate rainforests
in Chile and New Zealand. Table S1: correlations among light
environment, leaf, biomass distribution and crown traits of
temperate rainforest conifer and angiosperms, for small and
large seedlings. Table S2: structural equations with unstandardized coefficients using the cross-species dataset.
ACK N OW L E DG E M E N T S
We thank FONDECYT for funding through grant 1030811, the
Australian Research Council for Discovery grant 1094606,
CONAF for permission to work in Parque Nacional
Puyehue, and the New Zealand Department of Conservation
for permission to work in the Miranda Scientific Reserve.
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