JEC525.fm Page 1 Monday, March 12, 2001 4:08 PM
Journal of
Ecology 2001
89, 1–13
Crown development in tropical rain forest trees:
patterns with tree height and light availability
Blackwell Science, Ltd
FRANK J. STERCK and FRANS BONGERS
Silviculture and Forest Ecology Group, Department of Environmental Sciences, Wageningen University, PO Box 342,
6700 AH Wageningen, The Netherlands, tel.: 31 317478008, fax: 31 317478078
Summary
1 Monitoring of two canopy species Dicorynia guianensis and Vouacapoua americana
(Caesalpiniaceae) in a tropical rain forest in French Guiana was used to investigate
vegetative crown development at five organizational levels: leaf, metamer, extension
unit, sympodial unit and whole crown. The effects of light availability and tree height on
different traits were evaluated in trees < 25 m in height and compared with taller
individuals (25–37 m). Path-analysis is used to illustrate the consequences of trait
changes at multiple levels of organization for the whole crown level.
2 Tree height and canopy openness influenced crown development at each organizational
level. Crowns in higher light levels had lower specific leaf area, greater leaf spacing,
greater extension of all branches, and greater extension of the leader shoot. With
increasing tree height, crowns had a lower specific leaf area, greater leaf area index and
greater relative crown depth.
3 Vouacapoua showed some responses to light not seen in Dicorynia. In particular,
Vouacapoua increased meristem activity with light, but the lack of response in Dicorynia
may be due to moderate light levels rather than inability to respond.
4 Low leaf-display costs at low light availability may enable trees to survive light suppression.
5 Light availability cannot explain trait changes with tree height. Alternative explanations for trait changes with tree height are discussed.
6 Several of the relationships between plant traits and tree height or canopy openness
became non-linear when taller trees (25–37 m) were included. In these taller trees,
vegetative growth was reduced at all organizational levels, particularly in Vouacapoua,
which does not grow as tall as Dicorynia.
7 Qualitatively, plant responses to light did not differ between trees of different height,
and were similar to seedling and sapling data in the literature. Responses were, however,
quantitatively different, suggesting that small saplings cannot serve as model organisms
for crown development in taller trees.
Key-words: canopy, crown structure, Dicorynia guianensis, French Guiana, ontogeny,
rain forest trees, tree architecture, Vouacapoua americana.
Journal of Ecology (2001) 89, 1–13
Introduction
Trees growing through a tropical rain forest understorey
encounter different light environments (e.g. Chazdon
& Fetcher 1984; Terborgh 1985; Clark et al. 1996).
Generally, they will occupy sites with more light as they
get taller (e.g. Yoda 1974; Clark & Clark 1992; Bongers
© 2001 British
Ecological Society
Correspondence: Frank J. Sterck, Utrecht University, Section
Plant Ecology, Postbox 80084, 3508 TB Utrecht, The Netherlands (e-mail [email protected]).
& Sterck 1998), until they reach the canopy and no
longer compete with neighbours for light. If pioneer
trees are to survive, they must expand their crowns
quickly, shading their neighbours, and grow to maturity
in the high light conditions associated with canopy gaps
(e.g. Alvarez-Buylla & Martinez-Ramos 1992; Ackerly
1996). Slower growing, shade-tolerant trees cannot
monopolize canopy gaps and need to survive periods
of light suppression, expanding during periods when
sufficient light is available, until they reach maturity
(e.g. Hartshorn 1978). Vegetative crown development
plays an important role in the shade-tolerant strategy
1
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F. J. Sterck &
F. Bongers
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Table 1 Plant components in order of increasing size (partly adapted from Bell 1991; Room et al. 1994) and representing the
various organizational levels in the crown
Name
Definition
Meristem
Region of active cell division and enlargement. There is typically a meristematic zone at the apex (apical
meristem) and each node (axillary meristem) along every axis. Axillary meristems become apical meristems
once they become active and produce a new shoot.
Leaf
Photosynthetic structure.
Metamer
An internode with axillary bud(s) at its proximal end and one or more leaves at its distal end, but without
shoots resulting from growth of axillary buds.
Extension unit
The vegetative axis, displayed by one period of activity of a meristem (‘flush’), either of apical or axillary
origin. It consists of a sequence of metamers.
Sympodial unit
The total sequence of metamers and /or extension units produced by one meristem (also referred to as module,
Prévost 1967; Hallé et al. 1978).
Crown
The assemblage of leaf-supporting branches, including portions of the stem that support leaves or leafsupporting branches.
(e.g. Canham 1988; Küppers 1989; Kohyama & Hotta
1990; King 1994; Aiba & Kohyama 1997).
Our approach to the process in structurally complex
rain forest trees defines vegetative crown development
as the production, positioning and morphological
properties of the various components listed in Table 1
(see also White 1979; Barthélémy 1991; Bell 1991; Room
et al. 1994). These plant components characterize the
different levels of organization in the crown hierarchy,
and are produced and spaced according to an inherited
pattern ( Hallé & Oldeman 1970; Hallé et al. 1978). This
hierarchy remains the same as trees get taller or respond
to environmental conditions, and can be used to integrate
development at different organizational levels and to
compare crown development among trees in different
light environments and in different ontogenetic phases.
Components at each of the various organizational
levels are well known to respond to light, i.e. they are
located at different positions and produced at different
rates (King 1994), and have different sizes or architectures (Fisher 1986; Shukla & Ramakrishnan 1986).
Theoretical predictions that crown development at
low light availability will favour survival if it is associated with slow growth rates (Veneklaas & Poorter
1998), if bifurcation ratios are low and crowns are
flatter (Leopold 1971), if there is reduced self-shading
of the leaves (Horn 1971) and if there is higher allocation
of mass to leaves relative to wood (Givnish 1988) are
generally supported by empirical studies of seedlings
and small saplings (e.g. Canham 1988; King 1994).
The influence of ontogeny on vegetative development
is less well known and, although it has been described
for some rain forest trees (Hallé et al. 1978; Edelin
1990), information on the effects on bifurcation ratios,
crown allometry, leaf self-shading and leaf allocation
remains anecdotal and ambiguous. Trees often become
more exposed as they grow taller and crown development may therefore change with tree height, just as
it does with increasing light availability. This would
parallel physiological leaf traits where assimilation and
respiration rates are reported to increase as either tree
height or light increased (Kitajima 1996; Rijkers et al.
2000). Yet some trees become less exposed with increasing tree height (e.g. Clark & Clark 1992). Moreover,
trees become increasingly woody and have to be maintained by relatively low light interception (or leaf ) areas.
We would therefore expect any change in vegetative
crown development with tree height to parallel that
with declining light levels. Most of the available data
relates to the pioneer species that monopolize light gaps
(e.g. Alvarez-Buylla & Martinez-Ramos 1992; Ackerly
1996), rather than the shade-tolerant trees that grow
in variable light conditions (Strauss-Debenedetti &
Bazzaz 1996).
Ontogenetic stage and light environment are likely to
influence crown development simultaneously. Although
the effects of both tree size and light level have been
considered for leaf morphology (Niinemets & Kull
1995; Niinemets 1997; Rijkers et al. 2000), such joint
investigations on crown development are rare and
usually focus on smaller individuals and few organizational levels (e.g. Canham 1988). The combined effects
of development at the various organizational levels for
the whole crown are also poorly understood.
We explicitly distinguished between the effects of
tree height and light availability on each of the plant
traits in Table 2 (i.e. at the various organizational
levels) to evaluate their influence on crown growth, leaf
display and leaf display costs. We studied individuals of
two shade-tolerant species in French Guiana, ranging
in size from small saplings to canopy trees, to test two
hypotheses: (i) plant traits will vary with light availability such that trees will have slower crown growth,
wider crowns, less self-shading, smaller leaf display
cost, smaller leaf spacing and larger specific leaf area at
lower light levels; and (ii) because an increase in tree
height is accompanied by a gradual increase in light
availability, trait changes with increasing tree height
(up to 25 m) will parallel those seen under conditions
of increasing light.
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Crown development
in tropical trees
Table 2 Plant traits, ordered by organizational level. Metamer is equivalent to extension unit in Vouacapoua
Crown level
Relative crown depth
Total branch extension
Leader extension
Crown area
Total leaf area
Leaf area index
Number of meristems
=
=
=
=
=
=
=
Crown depth /mean crown width
Total branch length produced per year
Total leader length produced per year
Ground projection of the crown area
Mean leaf area × total number of leaves
Total leaf area /crown area
Number of apical meristems
(m m–1)
(m year–1)
(m year–1)
(m2)
(m2)
(m2 m–2)
Sympodial unit level
Metamer production
Leader metamer production
Sympodial unit survival
Sympodial unit production
=
=
=
=
Number of metamers produced per sympodial unit per year
Number of leader metamers produced per year
Percentage of sympodial units surviving per year
Percentage of sympodial units that is produced in preceding year
(year –1)
(year –1)
(% year –1)
(% year –1)
Metamer level
Metamer length
Leader metamer length
Leaf production
Leaf fall
Leaf spacing
Relative leaf spacing
=
=
=
=
=
=
Mean length of metamer
Mean length of leader metamer
Number of leaves produced per metamer per year
Number of fallen leaves per metamer per year
Mean length between leaves
Leaf spacing /√leaf area
(cm)
(cm)
(year–1)
(year–1)
(cm)
(cm cm–1)
Leaf level
Leaf area
Specific leaf area
=
=
Mean surface area of individual leaf
Leaf area /leaf mass
(cm2)
(cm2 g–1)
Materials and methods
  
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Field work was carried out in a pristine lowland
tropical rain forest at the biological field station ‘les
Nouragues’ (4°05′ N, 52°40′ W), French Guiana. Annual
rainfall is approximately 3000 mm, with dry seasons
(< 100 mm month–1) in September and October, and
sometimes in March. The forest is dominated by species
of Lecythidaceae, Leguminosae, Sapotaceae, Chrysobalanaceae and Burseraceae (Sabatier & Prévost 1989).
The area is covered with well-drained, clayey to sandyclayey soils on weathered granite parent material.
Dicorynia guianensis Amshoff. and Vouacapoua
americana Aubl., hereafter referred to by their generic
names alone, are abundant in the canopy. Such
Caesalpiniaceae or other leguminous species are
(co-)dominant in many neo-tropical forests and most
are characterized as shade-tolerant (e.g. Schulz 1960)
and as conforming either to Troll’s model of canopy
architecture or to other mixed plagiotropic models
(Oldeman 1974; Hallé et al. 1978; Oldeman 1989).
Thus, the stem leans over to support a horizontal spray
of distichously arranged leaves and the process is
repeated at different positions in the crown as a result of
relays sprouting from the bends. Stem and branches cannot be distinguished from one another at early stages
of crown development, but one branch subsequently
straightens towards the vertical and continues secondary
thickening growth and thus becomes the stem, while
the other branches fall or develop in a more horizontal
direction. Both study species are known for their commercial timber value in French Guiana and Surinam.
Figure 1 shows how different components (leaves,
metamers, extension units and sympodial units, Table 1)
contribute to crown development in the study species.
For Vouacapoua, metamers were not considered because
they are structurally variable: those at the bottom of an
extension unit support scale leaves, and the ones at the
top support compound leaves. For Dicorynia, however,
metamers are structurally equivalent, with each producing
one compound leaf, and therefore extension units
cannot always be unambiguously distinguished (but
see Drénou 1994).
    
Populations of both species were inventoried in
October 1992 as part of a long-term study of tree growth
(Sterck 1997). A 12-ha plot was mapped for trees with a
stem diameter ≥ 10 cm at 1.30 m above ground level (d.b.h.),
and a central 1.5-ha plot was mapped for trees with a stem
diameter < 10 cm, but with a height greater than 0.50 m.
For each species, we selected 20 of the inventoried
individuals that were less than 4 m tall, ensuring that
the full range of light levels within the site was represented. Their crown development was measured from
the ground, either by bending the stem over or using
natural elevations within the forest. The crowns of taller
individuals could only be studied from neighbouring
trees (climbed using spikes or alpinist ropes). Because
only a few of the inventoried individuals were accessible
in this way, we included a selection of the accessible
4–25 m trees (13 Dicorynia and 20 Vouacapoua) and all
five accessible > 25 m trees (Vouacapoua, 25, 35 and
37 m, and Dicorynia, 26 and 37 m) from the adjacent
area outside the plots. Measurements were made in
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4
F. J. Sterck &
F. Bongers
Fig. 1 Plant component architecture of Dicorynia guianensis and Vouacapoua americana, two shade-tolerant canopy tree species of
tropical rain forest in French Guiana. For definitions of plant components see Table 1. Figure adapted from Sterck (1999).
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
November 1992, November 1993, and November 1994
for all individuals.
The light environment was recorded using hemispherical photographs, taken in November 1993. A
Canon Ti 70 body and Canon 7.5 mm/5.6 lens was
mounted in a leveller and telescopic poles (up to 6 m long)
were used to position the camera just above the top of
each individual. The light environment of taller individuals
was also measured by climbing neighbouring trees with
ropes or spikes. Black-and-white prints were scanned
using a Hewlett Packard Desk Scan II and canopy openness (the percentage of open sky) was calculated using
the programme Winphot 5 (Ter Steege 1996). Canopy
openness is used as an estimate of light availability.
Trees were marked and drawn to scale in 1992. All
branches and apical meristems of individuals < 4 m were
tagged and coded, as was a selection of branches plus
their apical meristems (n = 10–45) within the top of the
crown of taller individuals. In later censuses (1993 and
1994), we measured size, structure and production rate
of each plant component (for details see below).
Production was assessed by counting leaves, leaf scars,
metamers (Dicorynia), extension units (Vouacapoua)
and apical meristems (or active sympodial units) that
had been produced by 1994 on top of apical meristems
tagged in 1992. For Vouacapoua, the number of leaves
and scars included photosynthetic but not scale leaves.
Although for trees taller than 4 m detailed counts were
made only for the selected apical meristems, we
assessed the total number of leaves and apical meristems
by climbing carefully along the length of these individuals.
In each individual, the axis (linear sequence of metamers
or extension units) that supported the uppermost apical
meristem of the crown in 1994 was defined as the leader.
Leaf area was determined (Delta Image Analysis
System, Eijkelkamp 1991) as the mean value for 20 leaves
taken from random positions in the crown. Lengths
were measured for all metamers (Dicorynia) or extension units (Vouacapoua) produced distal to monitored
meristems. Mean metamer length and extension unit
length were calculated for both the whole crown and
the leader separately. Lengths of sympodial units are
not reported because they may have continued length
growth after the last census in November 1994. We also
measured the greatest crown width, the crown width
perpendicular to this, and crown depth, i.e. the vertical
distance between the uppermost and the bottom leaves.
Plant traits were categorized into various organizational levels (as detailed in Table 2). At crown level
we used the measurements to calculate relative crown
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5
Crown development
in tropical trees
Fig. 2 Model presenting the expected influences of tree
height and light availability on plant traits at the crown level
after two successive steps. Initially, light availability and tree
height act on different plant traits, which then influence a
plant trait at the specific (usually the whole crown) level.
Single-headed arrows indicate causal relationships; doubleheaded arrows indicate correlations.
because it is harder to get a coefficient that differs
significantly from 0 (Petraitis et al. 1996). In our analysis,
we had to deal with collinearity between tree height
and canopy openness, as well as among plant traits.
We did not evaluate the magnitudes of significant effects
since the coefficient values cannot be accurately estimated.
We realise that by only distinguishing between effects that
are significant and those that are not, we may erroneously
have rejected actual effects (increased type II errors).
Results
depth, total branch extension, leader extension, crown
area, total leaf area, leaf area index and number of meristems. At sympodial unit level we calculated metamer
(or extension unit) production, leader metamer production, sympodial unit survival and sympodial unit production. At metamer (or extension unit, in the case of
Vouacapoua) level we calculated metamer length, leader
metamer length, leaf production, leaf fall, leaf spacing (a
measure for the average distance between leaves) and
relative leaf spacing (a measure for the leaf spacing
per unit area). At leaf level we calculated leaf area and
specific leaf area.
 
Multiple linear regression was used to assess the relative importance of tree height and canopy openness in
determining plant traits. Trees taller than 25 m were
excluded because their inclusion caused relationships
between plant traits and tree height to become nonlinear in 11 out of 36 cases. In some cases, plant trait
values were transformed if this improved the linearity
among variables and/or the homogeneity of variances.
The following regression model was used:
Plant trait = c + (b1 × height) + (b2 × openness)
+ (b3 × height × openness) + e
eqn 1
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Here, c is the constant (intercept), the b1, b2, b3 are the
regression coefficients and e is the error term.
We used path-analysis (e.g. Wright 1934; Kingsolver
& Schemske 1991) to integrate the effects of tree height
and canopy openness on plant traits and to show the
consequences of these plant traits for the whole crown
(Fig. 2). Path-analysis shows direct (or causal) effects
as path-coefficients, and relations without causal effect
as Pearson product moment correlation coefficients.
The analysis distinguishes direct, indirect and total effects
(e.g. Sokal & Rohlf 1981). In general, path-analysis
indicates the change in a criterion variable (expressed
in SD units) as a result of a change of 1 SD in each of
its predictors, both direct and indirect. Correlation
among predictors (collinearity) inflates both the pathcoefficients and their confidence intervals. Consequently,
the effect of a predictor on a criterion variable is either
overestimated with respect to its magnitude, or neglected
  .  
Canopy openness of individuals < 25 m tall ranged
from 0.8% to 30% (Fig. 3). For the five taller individuals it
ranged from 12% to 80%. Tree height and canopy
openness were correlated (Pearson’s product moment
coefficient of 0.54 in Dicorynia and 0.74 in Vouacapoua,
P < 0.001). Although canopy openness tended to be
higher above taller trees, there was a wide range of
canopy openness values for any particular tree height.
In our multiple regression analyses and path-analyses
we concentrated on how crown development is affected
by canopy openness independent of tree height, and by
tree height independent of canopy openness.
     
  
Multiple regression analysis was used to evaluate changes
in plant traits with tree height and canopy openness
(Table 3) for trees < 25 m high. For clarity, the plant trait
changes are described for each organizational level.
Crown level: In both species, total branch extension
increased with both tree height and canopy openness,
and leader extension increased with canopy openness
independent of tree height. All other traits in Dicorynia
increased with height alone, whereas in the case of
Vouacapoua they increased with both tree height and
canopy openness, except for crown area (height only)
and leaf area index (interaction only).
Fig. 3 Canopy openness vs. tree height for sampled trees. s,
Dicorynia guianensis; d, Vouacapoua americana.
Dicorynia
Vouacapoua
Level
Plant traits
R2
Height
Openness
Interaction
R2
Height
Openness
Interaction
Crown
Relative crown depth
Total branch extensiona
Leader extension
Crown area
Total leaf areaa
Leaf area index
No. of meristemsa
0.62***
0.84***
0.24**
0.71***
0.77***
0.32***
0.82***
0.76***
0.73***
/
0.82***
0.84***
0.56**
0.89***
/
0.24*
0.41**
/
/
/
/
/
/
/
/
/
/
/
0.67***
0.84***
0.20**
0.70***
0.90***
0.52***
0.94***
0.75***
0.68***
/
0.70***
0.79***
/
0.84***
0.20*
0.29**
0.45**
/
0.21*
/
0.17*
/
/
/
/
/
0.33***
/
Sympodial unit
Metamer production
Sympodial unit survival
Sympodial unit production
NS
NS
0.24*
/
/
– 0.65**
/
/
/
/
/
/
0.25**
NS
0.17*
– 0.12*
/
/
/
/
0.40*
/
/
/
Metamer
Metamer lengthc
Leaf productionb
No. of leaves
Leaf fall
Leaf spacingc
Relative leaf spacing
0.16*
–
NS
NS
0.16*
0.26**
/
0.39*
/
/
/
/
/
/
/
0.39*
0.51**
/
/
/
/
0.34***
0.44***
0.50***
NS
0.16*
0.13*
/
0.66***
0.57**
/
/
/
0.58***
/
/
/
0.45*
0.46*
/
/
/
/
/
/
Leaf area
Specific leaf area
NS
0.63***
/
– 0.64***
/
– 0.18*
/
/
NS
0.40***
/
/
/
/
/
–0.15***
Leaf
a
Data log transformed. bNot relevant for Dicorynia as leaf production is 1 by definition. cMetamer length is synonymous with leaf spacing in the case of Dicorynia.
JEC525.fm Page 6 Monday, March 12, 2001 4:08 PM
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F. J. Sterck &
F. Bongers
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Table 3 Regression of plant traits (see Table 2) on tree height (m), canopy openness (%), and their interaction for trees (0.5– 25 m high) of Dicorynia guianensis (n = 33) and Vouacapoua americana (n = 40).
Standardized regression coefficients are presented. When interaction effects were not significant, regressions were calculated with only height and openness. In the case of Vouacapoua, metamers are equivalent to
extension units (see methods section). *** P < 0.001, ** P < 0.01, * P < 0.05, NS = model not significant. / = coefficient not significant
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Crown development
in tropical trees
Fig. 4 Path-diagrams presenting the effects of tree height and canopy openness on total branch extension for the canopy tree species
Dicorynia guianensis and Vouacapoua americana in a tropical rain forest in French Guiana. The effects are split into the effects of
canopy openness and tree height on plant traits at various organizational levels and the subsequent effects of these traits on total
branch extension (whole crown level). Significant (P < 0.05) correlations and direct effects are indicated by double- and single-headed
arrows, respectively. Relationships were usually positive; instances of negative relationship are shown by a negative (–) sign.
Sympodial unit level: Extension unit production
decreased with tree height in Vouacapoua. Sympodial
unit production decreased with tree height in Dicorynia
and increased with canopy openness in Vouacapoua.
Metamer level (only for Dicorynia): Metamer length
(and thus also leaf spacing) and relative leaf spacing increased with canopy openness independent of tree height.
Extension unit level (only for Vouacapoua): Extension
unit length, leaf spacing and relative leaf spacing
increased with canopy openness independent of tree
height. Leaf production and the number of leaves
increased with tree height.
Leaf level: In Dicorynia, specific leaf area decreased
with tree height and canopy openness. In Vouacapoua,
the decrease in specific leaf area required increases with
both tree height and canopy openness, as illustrated by
the highly significant interaction term.
    
 
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
The path-analysis shows how tree height and canopy
openness influence plant traits at a higher level through
their effects on plant traits at lower organizational
levels (Figs 4 – 7). Path-analysis does not account for
interactions between tree height and canopy openness,
nor for non-linear relationships, and is therefore restricted
to trees shorter than 25 m.
Total branch extension depends on the number of
meristems, metamer (or extension unit) production
per meristem, and metamer (or extension unit) length
(Fig. 4). In both species tree height contributed to the
increase in total branch extension because of the greater
number of meristems. In Vouacapoua, extension unit
production was also affected (in this case negatively) by
tree height, but the effect on total branch extension was
minor, compared to the strong positive effect of the
number of meristems (values of effects not shown).
Canopy openness increased total branch extension in
Vouacapoua due to both increased numbers of meristems
and greater extension unit length. In turn, the greater
number of meristems resulted from a greater sympodial unit production (Table 3). In Dicorynia, however,
the increase in total branch extension with canopy
openness resulted only from the positive effect on
metamer length. Thus, only one organizational level
contributed to the more rapid crown growth of Dicorynia
with both greater tree height and with greater canopy
openness, whereas two levels were involved in Vouacapoua.
Leader extension depends on leader metamer (or
extension unit) production, and on the length of these
plant components (Fig. 5). The increase in leader
extension in Dicorynia with greater canopy openness
was mainly due to increases in metamer length. Vouacapoua showed the same tendency, although the effect
of canopy openness on leader extension unit length
was not significant (P = 0.07).
Total leaf area depends on the number of meristems,
metamer (or extension unit) production per meristem,
leaf production and leaf fall per metamer (or extension
unit), and leaf area (Fig. 6). The increase in total
leaf area with tree height resulted primarily from an increasing number of meristems. Although extension unit
production in Vouacapoua decreased with tree height,
its effect was minor compared to the strong positive
effect of the number of meristems. Only in Vouacapoua
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F. J. Sterck &
F. Bongers
Fig. 5 Path-diagrams of the effects of canopy openness and tree height on plant traits which in turn affect leader extension.
Conventions as in Fig. 4.
Fig. 6 Path-diagrams of the effects of canopy openness and tree height on plant traits affecting total leaf area (whole plant level) and,
in turn, of total leaf area and crown area on leaf area index (also whole crown level). Conventions as in Fig. 4.
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
did total leaf area increase with greater canopy openness
and this was also due to an increasing number of meristems.
Ultimately, leaf area index was strongly influenced by
total leaf area rather than by crown area (although
this had a minor negative effect in Vouacapoua).
At the metamer (or extension unit) level, we analysed how leaf spacing (equal to metamer length in
Dicorynia) and relative leaf spacing depended on
other plant traits (Fig. 7). Both measures were governed
by canopy openness (see also Table 3) via increased
unit length. These patterns indicate shorter woody
support structures per unit leaf area at lower canopy
openness, and thus lower costs for producing a unit of
leaf area.
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Crown development
in tropical trees
Fig. 7 Path-diagrams of the effects of canopy openness and tree height on plant traits which in turn affect leaf spacing (metamer
level). Conventions as in Fig. 4.
Fig. 8 Plant traits showing significant non-linear relationships with tree height for trees up to 37 m tall in a French Guianan
tropical rain forest. (a – d) crown level; (e –g) metamer/extension unit level; (h) leaf level. s, Dicorynia guianensis; d, Vouacapoua
americana. Non-linearity was tested by adding quadratic terms to a linear regression model: plant trait = constant + coefficient
× height + coefficient × height2. Significance level was set at P = 0.05. For plant traits and their units see Table 2.
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13

≥ 25
  
When trees taller than 25 m were included, regressions
of several plant traits on tree height were non-linear
(Fig. 8). We were unable to distinguish between the
effects of tree height and canopy openness on crown
development in these tall trees, and can only compare
their development with shorter (and generally less
JEC525.fm Page 10 Monday, March 12, 2001 4:08 PM
10
F. J. Sterck &
F. Bongers
exposed) trees. At the crown level, non-linear relationships became apparent generally for both species
between tree height and relative crown depth, total
leaf area, number of meristems, and leader extension
(Fig. 8a–d). There were no non-linear relationships at
the sympodial unit level, neither were there for Dicorynia at the metamer level, whereas extension unit length,
leaf production and leaf spacing in Vouacapoua
showed maximal values around 25 m (Fig. 8e–g). At
the leaf level, leaf area decreased above 25 m, particularly in Vouacapoua (Fig. 8h).
Discussion
 
Total crown growth and leader growth (which is correlated with height growth) increased with canopy openness, independently of height in the latter. Only one or
two organizational levels contributed to these crown
growth responses, in contrast with another study of
these species (Sterck 1999) where both measures of
crown growth of juveniles (4–18 m) were higher in gaps
than in the understorey because of changes at all possible levels. It may be that some traits respond only to
the high light levels characteristic of gaps and these are
rarely experienced by trees shorter than 25 m. Alternatively, gradual changes may become significant only
when well-separated light levels are compared.
The influence of light availability on leader extension
has been shown for seedlings (e.g. Popma & Bongers
1988), saplings (e.g. King 1991) and taller juveniles
(Sterck 1999). The increase in height growth with size
in eight Costa Rican tree species (Clark & Clark 1992)
might also be due to light availability rather than size
itself. Leader growth therefore generally seems to
be controlled by light in trees up to at least 25 m,
whereas total branch extension (which has rarely been
studied explicitly) is more affected by tree height
(Table 3).
 
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Total leaf area and leaf area index increased with tree
height in Dicorynia. In Vouacapoua, total leaf area
increased with both tree height and canopy openness,
but leaf area index was affected only by their interaction.
An increasing number of meristems explained most of
each effect.
Small individuals (< 10 m) of the pioneer tree Cecropia
obtusifolia (Alvarez-Buylla & Martinez-Ramos 1992)
show a similar increase in total leaf area with height
but as a result of a more than 100-fold increase in leaf
area, rather than meristem activation. Dicorynia and
Vouacapoua typically have c. 20 apical meristems by
the time they reach 10 m in height, and larger individuals continued to increase total leaf area by producing
more apical meristems, as is the case with Cecropia
individuals > 10 m in height. Similar changes may
therefore be the result of different plant traits in each
species.
The early branching of Dicorynia and Vouacapoua
follows Troll’s model, while Cecropia persists for longer
as a single pole axis and its subsequent branching pattern is described by Rauh’s model (Alvarez-Buylla &
Martinez-Ramos 1992). Below 10 m, Cecropia (still in
pole phase) may have a higher leaf area index than the
branched Dicorynia and Vouacapoua, but self-shading
is reduced by the positioning (Ashton 1978; Orians
1982) and by wider spacing of its leaves (King 1994).
The higher sympodial unit production in Vouacapoua
with greater canopy openness indicates both an increased
branching rate and a higher bifurcation ratio (an index
of the degree of branching from one branching order to
the next) with greater canopy openness (Canham 1988)
and was associated with narrower crowns. Leopold
(1971) and Whitney (1976 ) argued that such high bifurcation ratios are more efficient (in terms of stem tissue
used for leaf display) for narrower crowns in higher
light environments, while low bifurcation ratios are
more efficient for planar crowns (which have less leaf
self-shading) at lower light levels. Similar increases in
bifurcation ratios at higher light availability have also
been found in other studies (Steingraeber et al. 1979;
Shukla & Ramakrishnan 1986).
Although juveniles of both species had larger total leaf
area, higher leaf area index, and longer and relatively
narrower crowns in gaps than in the darker understorey
(Sterck 1999), the lack of such effects in Dicorynia in
the present study may (as with crown growth) reflect
the moderate light levels. Similar differences in results
were found between studies of small saplings of the
temperate species Acer saccharum, which showed a
response only when fully exposed sites (highest light
levels) were included (Steingraeber et al. 1979; Canham
1988; Bonser & Aarssen 1994).
      
Leaf display costs can be defined as the amount of
carbon invested to produce one unit of leaf area, and
depend on the relative amounts, densities and construction costs of leaf and wood material. Such costs
must be reduced at low light levels if light interception
is to increase, but only the size components show significant plasticity (e.g. King 1991, 1994). Leaf spacing,
relative leaf spacing and specific leaf area reflect the
(relative) amounts of wood and leaves along new
shoots, although the impacts of secondary thickening
and root growth are not considered.
Specific leaf area (a leaf area trait) is negatively
related to both tree height and light availability in
Dicorynia, but only to their interaction in Vouacapoua,
similar to patterns observed for other species (Jurik
1986; Oberbauer & Strain 1986; Poorter et al. 1995;
Rijkers et al. 2000). Everything else being equal, a higher
specific leaf area at lower light levels and/or tree height
will result in a greater light interception area per leaf
JEC525.fm Page 11 Monday, March 12, 2001 4:08 PM
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Crown development
in tropical trees
mass, and thus contribute to reduced leaf display
costs. However, morphological information alone may
be misleading because many other leaf-level factors,
including content of expensive metabolites such as
chlorophyll, may vary (Boardman 1977; Pearcy 1987;
Ellsworth & Reich 1993) and contribute to reducing
costs in higher, more open canopies.
Leaf area was unaffected by either factor, but leaf
spacing and relative leaf spacing both decreased when
canopy openness is less; this decrease was due to shorter
metamers (Dicorynia) or extension units (Vouacapoua).
Leaf spacing also decreased at lower light in other
tropical trees (King 1991, 1993, 1994), but there is as far
as we know no comparable data on relative leaf spacing.
All three traits considered appear to contribute to a
reduction in the leaf display costs at lower light availability, which may enable trees to lower their whole-plant
compensation point and thus survive light suppression.
   
© 2001 British
Ecological Society,
Journal of Ecology,
89, 1–13
Regressions of plant traits against tree height showed
linear relationships in trees under 25 m in height, while
several regressions became non-linear if larger trees
were also included. This apparent switch in crown
development might be triggered at a certain height,
greater exposure or some other environmental factor.
On attaining the canopy, branching patterns may change
drastically (King & Maindonald 1999) and even multiple tree-like structures (trunk-like branches, each with
its own subcrown) may develop in a process referred to
as reiteration or metamorphosis (Hallé et al. 1978;
Edelin 1990); however, no data are available on associated quantitative changes in crown development traits.
Many crown-level traits in both species lost their
linear increase with tree heights above 25 m. The
changes in relative crown depth and leader extension
suggest that crowns which have been narrowing with
increasing height then widen above 25 m, as seen for
taller trees in other tropical forests (Bongers & Sterck
1998; Bongers et al. 1988; King 1996). This is probably
due to the higher light levels in the upper open canopy
because the change occurs at the height where light
levels increased sharply (Koop & Sterck 1994) and
juvenile plantation-grown trees of Dicorynia and
Vouacapoua had wider crowns than forest-grown trees
of the same height (F.J. Sterck, unpublished data). In
the open upper canopy, where there is little chance of
being over-topped, increasing crown width may enable
trees to shade and thus out-compete their smaller
neighbours.
In Vouacapoua, changes with tree height and canopy
openness also became non-linear above 25 m for some
traits at the extension unit level, indicating a reduction
in vegetative crown growth; this observation is expected
because maximum height is about 35 m for this species.
No such effects were seen in Dicorynia where the largest
trees (25 and 37 m) were still below the 45–50 m height
of full-grown adults.
At the leaf level, leaf area decreased above 25 m
for Vouacapoua and this may reflect adaptations to
physiological drought in the open upper canopy, but
there was no effect in Dicorynia. In general, adults of
canopy tree species have smaller leaves than juveniles
of the same species (Thomas & Ickes, 1995).
General conclusions
Traits generally responded to light in the same ways as
previously reported for smaller saplings. Returning to
our first hypothesis, under conditions of decreasing
light availability, trees were (as expected) found to be
characterized by slower crown growth rates, relatively
wide crowns, fewer leaf layers, smaller leaf display costs,
lower sympodial unit production, smaller leaf spacing
and larger specific leaf areas. The absence of some
responses in Dicorynia probably reflected the general
absence of light levels able to induce an effect, rather
than an inherent inability to respond.
Our second hypothesis, that increasing tree height
and increasing light availability influence tree characteristics in a similar way, was supported by parallel
responses in some traits at the crown and the leaf level.
However, even in these cases changes with height may
not be due to the higher light levels: at the leaf level,
effects on specific leaf area are more likely to reflect
physiological drought, and effects at the whole crown
level were due to the influence of height on the number of
apices. At the three intermediate levels (metamer, extension unit and sympodial unit), the changes in plant traits
with tree height never paralleled the patterns with light
availability. The decrease in the proportion of productive (leaves) to unproductive (wood) biomass with increasing tree height may counterbalance the positive effects
of increasing light availability. Overall, light availability
cannot be said to have been an important selection force
acting on architectural changes with tree height.
Our approach also suggests that small saplings
cannot serve as model organisms for the study of crown
development in trees of other sizes. While the directions
of responses of saplings and larger trees to light are
similar, no quantitative predictions can be made. As
well as changing with tree height per se, many trait
responses to light show changes in magnitude, or even
in direction (for trees above 25 m in height), as the tree
grows. Furthermore, responses to light at the crown
level are predominantly driven at intermediate
organizational levels (sympodial unit, extension unit
and metamer), which rarely receive attention in small
saplings. The modelling of crown development in trees
therefore requires data from trees of a range of sizes.
In addition, even closely related species such as those
studied here (same plant family and similar general
branching pattern) may differ in responses of some
traits. This may have far reaching consequences for
modelling forest canopy dynamics on the basis of
crown development of individual trees, particularly in
species-rich habitats such as tropical rain forests.
JEC525.fm Page 12 Monday, March 12, 2001 4:08 PM
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F. Bongers
Acknowledgements
We thank L. Poorter, T. Rijkers and M. Smeenge for
giving field support; D. Ackerly, C.D. Canham, P.A.
Jansen, D. King, E. Leigh Jr., J. den Ouden, L. Poorter,
H.H.T. Prins, S. Wijdeven and J. Wright for giving comments on earlier drafts of the manuscript; M.G. Born
for drawing Fig. 1. This study was supported by grant
W 85-239 of the Netherlands Foundation for the
Advancement of Tropical Research (WOTRO).
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