Functional
Ecology 2001
15, 113 –123
Light-dependent changes in biomass allocation and
their importance for growth of rain forest tree species
Blackwell Science, Ltd
L. POORTER
Department of Plant Ecology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands,
and Programa Manejo de Bosques de la Amazonía Boliviana (PROMAB), Casilla 107, Riberalta, Bolivia
Summary
1. Sapling growth of six rain forest tree species was compared to evaluate whether
species respond in a similar way to a natural light gradient. Saplings were measured
non-destructively; production and loss of leaves, stem and branches were analysed in
detail.
2. Sapling height growth was positively related to light environment and leaf area. No
single descriptor of light environment explained sapling growth best. Direct or diffuse
light could explain plant growth, depending on species.
3. Seventeen percent of the saplings had negative relative biomass growth rates,
although they occurred in fairly bright conditions. Negative growth rates were caused
by leaf shedding and stem breakage. Sapling relative growth rate increased with irradiance, mainly because of an increase in net assimilation rate.
4. On a shoot basis, shaded plants had a smaller leaf mass fraction (LMF) and a larger
specific leaf area, resulting in similar leaf area ratios (LAR) to those of sun plants. This
contrasts with the results of seedling studies under controlled conditions, where LMF
and LAR increased with shade.
5. Biomass partitioning to leaf growth decreased with irradiance and relative growth
rate of the sapling. This leaf partitioning ratio was better correlated with RGR than
with irradiance.
6. Species differed in the effect of light-dependent changes in specific leaf area (SLA)
on growth. This underscores the importance of SLA in explaining differences in species
performance in a forest environment. Nevertheless, the effect of SLA was not related
to the shade tolerance of the species.
Key-words: Biomass partitioning, Bolivia, growth analysis, shade tolerance, tropical rain forest
Functional Ecology (2001) 15, 113–123
Introduction
In tropical rain forests, light is probably the most
important environmental factor affecting plant establishment, growth and survival. Plant performance is
enhanced through morphological and physiological
acclimation to the light environment. Growth analyses
of tree seedlings under controlled conditions indicate how such plants adjust to the light environment
(e.g. Popma & Bongers 1988; Osunkoya et al. 1994;
Veenendaal et al. 1996; Poorter 1999). At low irradiance, shade plants enhance interception of light by a
large biomass fraction in leaves (leaf mass fraction,
LMF). In combination with a large leaf area per unit
leaf biomass (specific leaf area, SLA), this leads to a
© 2001 British
Ecological Society
Present address: Silviculture and Forest Ecology, Department of Environmental Sciences, P.O. Box 342, 6700 AH
Wageningen, The Netherlands.
large interceptive leaf area per unit plant mass (leaf
area ratio, LAR). Shade leaves have slow respiration
and light-saturated photosynthetic rates (Langenheim
et al. 1984; Oberbauer & Strain 1985). Little physiological activity means smaller maintenance costs, and
in this way, carbon losses in the understorey are
reduced and potential relative growth rates (RGR)
enhanced (Lehto & Grace 1994; Sims, Gebauer &
Pearcy 1994). At high irradiance, nutrient and water
availability may limit plant growth. Accordingly, sun
plants invest relatively more biomass in roots (i.e. they
have a large root mass fraction, RMF). Carbon fixation is increased by the formation of thick leaves with
fast light-saturated photosynthetic rates, increasing
biomass growth per unit leaf area (net assimilation
rate, NAR) and potential RGR.
Plant growth in the understorey is limited by the
amount of light intercepted for photosynthesis.
Growth in the understorey may depend on the amount
113
114
L. Poorter
of incident radiation and the leaf area (Oberbauer
et al. 1988). Incident radiation is composed of direct
light and diffuse light. Because 50–80% of the total
daily radiation in the forest understorey may be as
sunflecks (Pearcy 1987; Chazdon 1988), direct light is
probably a more important determinant of plant growth
than diffuse light. However, this is not always supported
by field observations (Clark, Clark & Rich 1993).
A plant’s carbon balance is affected by the partitioning of fixed carbon to photosynthesizing tissue (leaf
partitioning ratio, LPR) and its longevity (i.e. the leaf
lifespan). At low irradiance, a greater biomass partitioning to leaves increases the leaf area. As carbon gain
in the understorey is slow, leaf longevity should be
increased to return the construction costs of the leaves
(Chabot & Hicks 1982; Williams, Field & Mooney
1989). Pioneer species have short-lived leaves (Bongers
& Popma 1990; Reich, Ellsworth & Uhl 1995). They
must therefore replace lost leaf area quickly to sustain
growth (King 1994), a prerequisite that is difficult to
meet in the forest understorey.
Plant growth analysis is useful to evaluate how plants
differ in growth rate, either inherently or dependent
on the environment (Lambers 1998). Few studies have
analysed growth of saplings in this way (but see King
1991, 1994). To evaluate whether (i) species differ in
their response to the light environment, and (ii) similar
patterns are found for large saplings in the field compared to small seedlings grown under controlled conditions, a field study was carried out on growth and
biomass partitioning of six rain forest tree species
differing in shade tolerance. Naturally established
saplings occurring along a light gradient were selected,
and the growth and turnover of shoots and their
components were analysed. The following questions
were addressed:
1. How is height growth related to light environment,
and what factors cause this relationship? It is
hypothesized that sapling growth depends on the
amount of incident radiation and leaf area, and that
direct light is a more important determinant for
plant growth than diffuse light.
2. How does RGR and its components (NAR, LAR,
LMF and SLA) vary with irradiance? Do species
differ in light-dependent changes in biomass allocation, and what is their effect on growth? It is
expected that NAR increases with irradiance, due
to faster photosynthetic rates, and that LMF, SLA
and LAR increase with shade to enhance light
interception.
3. How do LPR and leaf lifespan vary with light
environment? LPR and leaf longevity are postulated
to increase with shading. Because leaf turnover
of pioneer species exceed those of shade-tolerant
species, it is also expected that they will have a
larger leaf partitioning ratio.
Materials and methods
The field study was carried out in forest reserve ‘El
Tigre’ (10°59′ S, 65°43′ W). El Tigre is a research site
of the Programa Manejo de Bosques de la Amazonía
Boliviana (PROMAB), located 170 m above sea level
in the Amazon region of Bolivia. Mean annual temperature is 26 °C, and annual rainfall is about 1780 mm
with a distinct drier period (< 100 mm mo–1) from May
to September. Vegetation in the region can be classified
as a tropical lowland moist forest, with a canopy 25–35 m
high. Some of the canopy trees are deciduous during
the dry season.
Six tree species were selected based on their light
requirements for establishment and survival (Table 1).
Classification of the species – as pioneer, non-pioneer
light-demanding, and shade-tolerant – was based on
observations of the abundance of saplings in different
microhabitats. Cecropia ficifolia and Bellucia pentamera
are typical pioneer species, which establish soon after
disturbance. Tachigali vasquezii is a non-pioneer lightdemanding species with intermediate light requirements.
Table 1. The studied species and their characteristics, including strategy, adult height, seedling light compensation point (LCPNAR, see Poorter 1999),
mode of lateral crown expansion, sapling height and direct site factor. Mean values followed by a different letter were significantly different at P = 0·05
(Student Newman–Keuls test)
Species
Family
Cecropiaceae
Cecropia ficifolia Warb.
Bellucia pentamera Naud.
Melastomataceae
Tachigali vasquezii J.J. Pipeloy
Fabaceae
Cariniana micrantha Ducke
Lecythidaceae
Capirona decorticans Spruce
Rubiaceae
Theobroma speciosum Willd.
Sterculiaceae
ex Sprengel
© 2001 British
P = Pioneer.
Ecological
Society,
NPLD = Non-pioneer
light demander.
Functional
Ecology,
S =113–123
Shade-tolerant.
15,
Sapling height (m)
Direct site factor
Strategy
Adult
height
(m)
LCPNAR
(%)
Expansion
mode
Mean
Range
Mean
Range
n
P
P
NPLD
S
S
S
12
20 –25
25 –30
35
25 –30
15
2·0
1·8
1·2
0·3
–
0·1
petiole
branch
rachis
branch
branch
branch
1·6a
1·6a
1·7a
1·8a
1·6a
1·6a
(0·9–2·6)
(0·9–2·8)
(1·0–2·9)
(0·7–3·3)
(0·6–2·5)
(0·8–3·0)
25·4a
24·2a
7·0b
5·5b
9·2b
7·3b
(2·8–68·2)
(4·6–64·7)
(1·3–18·7)
(1·1–18·4)
(2·5–38·7)
(2·9–26·2)
16
14
14
16
15
15
115
Light, biomass
allocation and
growth
Cariniana micrantha, Capirona decorticans and Theobroma
speciosum are shade-tolerant species. The species differ
in adult stature, sapling architecture and whole-plant
light compensation point, i.e. the irradiance at which
net growth is zero (Table 1; Poorter & Werger 1999).
Henceforth, the species will be referred to by their generic
name.
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
Approximately 15 saplings per species were selected.
For each species, care was taken to select saplings
along the whole light gradient, including individuals in
large gaps, small gaps and understorey. All saplings
occurred on the same soil type (Ferrasols) and presumably experienced the same nutrient availability.
Saplings were 0·6–3·3 m tall (Table 1) and had no signs
of stem breakage or resprouting. Saplings were measured non-destructively to determine the production
and losses of stems, branches and leaves over the
growth interval. Saplings were first measured between
October and December 1996 and remeasured 11 months
later (mean interval 335 days, range 293–389 days).
Diameter was determined at three to five permanently
marked positions along the stem, including one at
10 cm from its base. The diameter of each branch was
measured 5 cm from its base. Stem and branch diameters were measured in two perpendicular directions,
using a caliper. Lengths of stem, branches and spacer
organs like petioles (Cecropia) and rachae (Tachigali)
were also determined. At the final measurement, stem
height was measured from the highest marked ring
onwards, to accurately estimate height growth.
Leaves at the terminal growing points were marked
to monitor leaf production and loss. For all species but
Cariniana (which has very small leaves), leaf lengths
and widths, plus the height of the insertion points of
petioles on the stem, were recorded. Leaf damage by
herbivory was estimated visually in 10% area interval
classes. For Cariniana, leaves were simply counted.
Crown width in two perpendicular directions and
length of each internode, from the lowest leaf onward,
were measured. After the second non-destructive measurement, three leaves per sapling were selected along
the stem and their areas determined with a portable
leaf area meter (CI-202, CID Inc., Vancouver, WA,
USA). These leaves were oven-dried for 48 h at 70 °C.
To estimate stem biomass and leaf area from the
non-destructive measurements, 10 additional, similarsized saplings per species were selected in the same
area. Five saplings were sampled in bright light and
five saplings in shade. Three leaves were sampled from
each sapling and a 10 cm section was taken from the
upper and lower part of the stem. Leaf area and length
and width of each leaf blade were measured. An allometric relation was established between ln(leaf area),
ln(leaf length) and ln(leaf width) for each species. In
this way, total leaf area per plant could be estimated
from individual non-destructive leaf measurements.
The mean coefficient of determination for the regression
equations was 0·96 (range 0·91–0·99). Volume of the
stem sections was determined and stem parts were ovendried for 48 h at 70 °C. Specific stem mass was calculated
as the stem mass per unit stem volume (SSM, in g cm–3).
For species-specific values of SSM, see Table 3 in
Poorter & Werger (1999).
Stem and branch volume of the monitored saplings
were calculated based on size measurements and
volume equations (see Poorter & Werger 1999). All areas
were measured in cm2, volumes in cm3 and masses in g.
Stem mass was obtained by multiplying stem volume
by SSM, branch mass by multiplying branch volume
by SSM, and leaf mass by dividing the leaf area by the
specific leaf area (SLA, the leaf area per unit leaf mass)
of the sapling.
The leaf mass fraction was calculated as leaf mass
per unit above-ground plant mass (LMF, g g–1), and
the net above-ground relative growth rate (RGRn, mg
g–1 d–1) as (lnM1 – lnM0)/t, in which M0 and M1 are the
total shoot masses at the beginning and end of the
experiment, respectively, and t is the time interval
(days). The RGRn can be factored into a morphological component, the leaf area ratio (LAR, leaf area per
unit above-ground mass, m2 kg–1), and a physiological
component, the net assimilation rate (NAR, the net
above-ground biomass growth per unit leaf area on
average present during that time interval, g m–2 d–1)
(Hunt 1978). Due to practical limitations, the growth
analysis in this study is restricted to the above-ground
plant parts. Biomass invested in roots is not taken into
account and the reported NAR will therefore be less
than the whole-plant NAR.
The LMF is a static descriptor of biomass allocation
to leaves. It describes the fraction of shoot biomass
present as leaves, and is the end result of the production and loss of leaf, stem and branch biomass. In contrast, the leaf partitioning ratio is a dynamic descriptor
of biomass allocation to leaves. It indicates the fraction
of newly produced, above-ground biomass allocated to
the production of new leaves (LPR, g g–1). The LPR is
an approximation of the real proportion of carbon
gain allocated to the leaves, as it is based on net biomass growth. Note that carbon costs for growth (i.e. to
convert fixed CO2 into dry matter) and maintenance
respiration are not included in the LPR.
Average leaf lifespan (days) was calculated as the
ratio of the mean leaf area present at the beginning and
the end of the study period (m2), to the mean of the leaf
area production and loss over the study period (m2 d–1)
(King 1994).
Hemispherical photographs were taken above the
saplings in December 1996. Photographs were taken
mainly around sunrise or sunset, and sometimes when
the sky was overcast. Photos were taken with a Canon
AE-1 camera with a 7·5 mm fish-eye lens using an
116
L. Poorter
Ilford 125 Asa black and white film. The camera was
mounted on a pole and kept horizontal using a levelling device. Negatives were scanned with a Sony XC77CE black and white CCD camera attached to a
VIDAS image analysis system (Kontron/Zeiss, Eching,
Germany) and analysed with Winphot 5 (Tropenbos
Foundation, Wageningen, The Netherlands; ter Steege
1997). With Winphot, the direct site factor (DSF) and
the indirect site factor (ISF) were calculated. They
indicate what proportion of radiation above the forest
canopy reaches the sapling in the form of direct radiation (i.e. sunflecks) and diffuse radiation, respectively
(Mitchell & Whitmore 1993).
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
Individuals should be of similar sizes and have experienced similar light conditions in order to make direct
comparisons between species’ morphology and growth
responses to light. Mean sapling height ranged from
1·6 to 1·8 m, and was similar for all species (Table 1,
one-way , F5,84 = 0·29, P > 0·05). The DSF differed considerably between species (Table 1, one-way
, F5,84 = 6·1, P < 0·001); the mean DSF of the
two pioneer species (24 –25%) was significantly greater
than the DSF of the other species (5·5 –9·2%). DSF
was similar for all species when individuals from large
gaps (DSF > 30%) were excluded from the analysis
(one-way , F5,73 = 1·4, P > 0·05). Therefore, two
types of analysis were performed. For intraspecific
comparisons, all saplings were included. For interspecific comparisons, only the restricted data set was used.
To analyse which plant features and abiotic factors
were associated with intraspecific differences in height
growth, a backward multiple regression was carried
out for each species, using plant growth as dependent
variable and DSF, ISF and initial plant height and leaf
area as independent variables. Initial plant height was
included as an independent variable because growth
rate may be size-dependent.
Height growth is a function of internode length and
production rate, both of which are probably influenced
by sapling size and the light environment. Therefore,
for each species, three regression analyses were carried
out: two multiple regressions with the internode production rate or mean internode length as dependent
variables and height and DSF as independent variables;
and one multiple regression of height growth against
internode length and internode production rate.
A growth response coefficient (GRC) was calculated
to evaluate how responses in biomass partitioning to
light affect the RGR of a plant. The GRC indicates
how intraspecific variation in RGR is associated with
variation in one if its components. If RGR is analysed
as the product of NAR and LAR, then the sum of the
GRCs of NAR and LAR should equal unity. Alternatively, RGR can be defined as the product of NAR,
LMF and SLA, and their three corresponding GRCs
should also sum to unity. A GRC value of 1 indicates
that a change in the growth parameter being considered
leads to a proportional change in RGR. GRCs can be
> 1 if the increase in growth parameter is stronger
than the increase in RGR, 0 if an increase in the growth
parameter does not lead to a change in RGR, and
negative if an increase in the growth parameter is
associated with a decrease in RGR (Poorter & Nagel
2000). The GRCs can be obtained by calculating the
regression slope of ln(NAR) or ln(LAR) against
ln(RGR) for each species. Saplings with a negative
RGR were excluded from this regression analysis. For
more information on GRCs see Poorter & Van der
Werf (1998) and Poorter & Nagel (2000). To evaluate
whether species differ in their GRC, an
was carried out in which the ln-transformed growth
parameter was used as dependent variable, species as a
factor and ln(RGR) as a covariate. A significant species–
covariate interaction indicates that species differ in their
GRC. To test whether species differ in the effect of lightdependent changes in allocation on growth, the speciesspecific GRC was correlated with the whole-plant
light compensation point (LCPNAR), estimated from an
independent growth experiment (Poorter 1999; Table 1).
The LCPNAR of Capirona is not known, but as this is
a highly shade-tolerant species, it was set to 0·1%. All
statistical analyses were carried out using SPSS 6·0
(SPSS Inc., Chicago, IL, USA; Norusis 1993).
Results
Seven of the 91 saplings died during the study period.
Cecropia had the poorest survival (69%), whereas
92–100% of the saplings of the other species survived.
Initial plant height or DSF had no effect on survival
probability when all species were pooled (logistic
regression, P > 0·05).
Height growth was positively related to light
environment, leaf area, or a combination of the two
(Table 2), whereas initial plant height had no effect.
The regression models explained 76% of the variation,
on average (range 27– 98%). Leaf area affected the
growth of all species but Theobroma. The light environment affected growth of all species but Cariniana. For
the other four species, the combined effects of light and
leaf area explained more than either alone. There was
no single measure of the light environment that best
explained height growth for all species; for some species,
height growth was more closely related to DSF, whereas
for other species it was more closely related to ISF.
An increased height growth at higher irradiance
was due to the combined effect of a greater internode
production rate and longer internodes (Table 3). For
some species, the enhanced height growth was largely
due to an increase in internode production rate (e.g.
Cariniana). For other species (e.g. Theobroma), it was
mainly due to increased internode length.
Fourteen of the 84 surviving individuals (17%) had
a net negative RGR, as a result of leaf shedding, branch
loss or stem breakage. Saplings which showed negative
117
Light, biomass
allocation and
growth
Table 2. Effect of direct site factor (DSF) indirect site factor (ISF), initial height and initial leaf area on height growth of six
rain forest tree species. A backward multiple regression was carried out, and standardized partial regression coefficients are
shown for those variables which contributed significantly to the model
Species
DSF (%)
ISF (%)
Height (cm)
Leaf area (m2)
r2
Cecropia
Bellucia
Tachigali
Cariniana
Capirona
Theobroma
0·46*
–
–
–
0·87***
0·52*
–
0·81***
0·77***
–
–
–
–
–
–
–
–
–
0·56*
0·24**
0·33*
0·78***
0·36***
–
0·84
0·98
0·85
0·60
0·92
0·27
– P > 0·05; * P < 0·05; ** P < 0·01; *** P < 0·001.
Table 3. Effect of initial plant height and light environment (DSF) on internode production rate (IPR) and internode length (IL)
of six rain forest tree species. Regression coefficients (b) indicate the effect of 1 cm change in height or 1% change in direct light
on the dependent variables. Light has an effect on height growth (expressed as cm change in height per year per percent change
in DSF) via the IPR and via the IL
Internode production rate (year−1)
Internode length (cm)
Height (cm)
DSF (%)
Height (cm)
DSF (%)
Species
b
P
b
P
r2
b
P
b
P
r2
Via IPR
Via IL
(cm year−1 %−1)
Cecropia
Bellucia
Tachigali
Cariniana
Capirona
Theobroma
0·06
0·00
0·04
–0·03
0·01
0·01
*
ns
*
ns
ns
ns
0·37
0·15
0·40
2·04
0·19
–0·03
***
***
*
**
***
ns
0·91
0·90
0·61
0·84
0·72
0·21
0·01
–0·02
0·00
0·00
0·02
0·01
ns
ns
ns
ns
ns
ns
0·06
0·46
0·65
0·18
0·29
0·87
*
***
***
ns
*
ns
0·52
0·95
0·67
0·46
0·36
0·29
2·1
1·4
3·5
5·3
1·7
–0·1
Effect DSF on
height growth
0·9
3·7
3·3
1·0
0·9
0·9
– P > 0·05; * P < 0·05; ** P < 0·01; *** P < 0·001.
Table 4. Relation between sapling light environment (direct site factor, %) and net RGR (RGRn ), NAR, LAR, LMF, SLA and
leaf lifespan. LAR and LMF are given for the initial measurement, SLA for the final measurement. Pearson’s correlation
coefficients are shown and significance levels are indicated by *
Species
RGRn (mg g–1 d–1)
NAR (g m–2 d–1)
LAR (m2 kg–1)
LMF (g g–1)
SLA (m2 kg–1)
Lifespan (yr)
Cecropia
Bellucia
Tachigali
Cariniana
Capirona
Theobroma
0·70*
0·95***
0·85***
–
0·89***
–
0·90***
0·95***
0·89***
–
0·90***
0·51*
–
–
–
–
–
–
0·64**
0·73**
–
–
0·74**
–
–0·79**
–0·81**
–0·58*
–
–0·70**
–0·66**
–0·74**
–
–0·70**
–
–
–
– P > 0·05; * P < 0·05; ** P < 0·01; *** P < 0·001.
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
growth rates were not confined to severely shaded
microsites; theywere also growing in relatively brighter
conditions (mean DSF = 5·0%, range 2·9 – 9·5). In
general, net RGR (RGRn ) and NAR were positively
correlated with DSF (Table 4, Fig. 1). Responses of
RGRn and NAR did not show a saturating response
to light over the light range evaluated here. There
was a striking lack of significant correlations between
LAR and light environment as LMF and SLA showed
opposite responses to irradiance. For three species, the
LMF increased with irradiance whereas for five species,
the SLA decreased.
An increase in RGR with irradiance was closely
paralleled by an increase in NAR (Fig. 1); the GRCNAR
of the species ranged from 0·88 to 1·23 (Fig. 2a), and
was significantly different from zero in all cases. For
four species, an increase in LMF with irradiance led
to an increase in RGR (and positive GRCLMF; Fig. 2c).
This was counterbalanced by a decrease in SLA with
irradiance and a negative GRCSLA. As a consequence,
adjustments in LAR had little effect on RGR, and
GRCLAR values were close to zero (Fig. 2b).
Species tended to differ in their GRCs, but this was
only significant for GRCSLA (GRCNAR, F = 2·0, P = 0·089;
GRCLAR, F = 2·1, P = 0·081; GRCLMF, F = 2·2, P = 0·071;
GRCSLA, F = 3·1, P = 0·016). The two pioneer species, Cecropia and Bellucia, had the largest GRCLMF
and GRCSLA (Fig. 2), but overall, the GRCs were
118
L. Poorter
Fig. 1. Relationship between above-ground RGRn, NAR, LAR, LMF, SLA and sapling light environment (DSF) for Cecropia
(d) and Bellucia (s) (a); Tachigali (d) and Cariniana (s) (b); and Capirona (d) and Theobroma (s) (c). LAR and LMF are
given for the initial measurement, SLA for the final measurement. Continuous regression lines refer to the filled symbols, and
broken regression lines to the open symbols. Regression lines are only shown if they are significant; + P < 0·054; * P < 0·05;
** P < 0·01; *** P < 0·001.
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
not correlated with the whole-plant light compensation point of the species (Spearman’s rank correlation
between GRCs and LCPNAR of the six species: GRCNAR,
r = – 0·17, P > 0·10; GRCLAR, r = 0·17, P > 0·10; GRCLMF,
r = 0·78, P = 0·066; GRCSLA, r = – 0·32, P > 0·10).
Species differed considerably in their LPR (one-way
, F5,64 = 4·74, P < 0·001). On average, Cecropia
had the greatest LPR (92%), and Theobroma had the
smallest (17%) (Fig. 3a). Species also had different
leaf lifespans (one-way , F5,63 = 5·6, P < 0·001),
from 0·4 years for Cecropia to 3·2 years for Tachigali
(Fig. 3b). LPR was negatively correlated with irradiance and RGRn, although correlations were stronger
with RGRn (three significant relationships) than with
DSF (two significant relationships) (Fig. 4, Table 5).
The leaf lifespan of Cecropia and Tachigali was
related negatively to light environment (Table 4);
plants in shade had leaf lifespans which were, on
119
Light, biomass
allocation and
growth
Fig. 3. Interspecific variation in leaf partitioning ratio
(LPR) and leaf lifespan for six rain forest tree species.
Back-transformed logarithmic means and corresponding
standard errors are shown. Bars with a different letter were
significantly different at P = 0·05 (Student Newman–Keuls
test). Species are ordered along the X-axis according to their
shade tolerance. Only saplings with a direct site factor < 30%
were included.
average, half (Cecropia) to three times (Tachigali)
longer than plants in a high-light environment (data
not shown).
Discussion
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
Fig. 2. Growth response coefficient (GRC) (mean ± SE) of
net assimilation rate (NAR) (a); leaf area ratio (LAR) (b);
leaf mass fraction (LMF) (c); and specific leaf area (SLA) (d)
for six rain forest tree species. LAR and LMF are taken as the
average over the growth interval. Species are ordered along
the X-axis according to their shade tolerance, with the most
shade-tolerant species on the right. * indicates whether the
GRC is significantly different from 0 (P < 0·05). Note that the
scaling of the Y-axis differs between graphs.
Despite careful selection of saplings on the basis of
their light environment, the average irradiance experienced by the pioneer species still exceeded those of the
non-pioneer species (Table 1). Unintentionally, this
reflects differences in microhabitat distribution between
pioneer and shade-tolerant species (cf. Hubbell & Foster
1986; Clark et al. 1993). When working with naturally
established populations in the field, it is difficult to
establish whether observed differences are caused by
inherent adaptations to the light environment or the
acclimation of plants to the contrasting environments
in which they occur. Interspecific comparisons should
120
L. Poorter
Table 5. Correlation between leaf partitioning ratio (LPR),
the light environment (DSF) and carbon balance (RGRn) of
saplings of six rain forest tree species. Pearson’s correlation
coefficient and significance levels are shown
LPR (g g–1)
Species
DSF (%)
RGRn (mg g–1 d–1)
Cecropia
Bellucia
Tachigali
Cariniana
Capirona
Theobroma
–0·94***
0·18 ns
–0·44 ns
–0·44 ns
–0·55*
–0·05 ns
–0·70*
0·19 ns
–0·49 ns
–0·63*
–0·70**
0·20 ns
ns P > 0·05; * P < 0·05; ** P < 0·01; *** P < 0·001.
Fig. 4. Leaf partitioning ratio (LPR) vs sapling RGRn for
Cecropia (d) and Bellucia (s) (a); Tachigali (d) and Cariniana
(s) (b); and Capirona (d) and Theobroma (s) (c). Continuous
regression lines belong to the filled symbols, and broken
regression lines belong to the open symbols. Regression lines
are only shown if they are significant; * P < 0·05; ** P < 0·01;
*** P < 0·001. Note that the scaling of the X-axis differs
between graphs.
therefore be made only in the shared light range in
which both species groups occur.
the findings of other studies (Oberbauer et al. 1988,
1989; Sterck et al. 1999) and supports the hypothesis
that sapling growth in a forest environment is limited
by the amount of light intercepted for photosynthesis.
Leaf loss due to herbivory or leaf shedding has, therefore, important repercussions for plant growth. Using
regression equations (data not shown), it can be calculated that for an average plant (leaf area = 0·5 m2,
DSF = 7·8), a 10% reduction in leaf area also implies
a 10% reduction in height growth.
In the forest understorey, 50–80% of the PPFD is in
the form of sunflecks (Pearcy 1987; Chazdon 1988).
Therefore, it was expected that sapling growth would
be most closely related to DSF. This hypothesis was
not confirmed by the results, however; for two species,
even ISF was a better predictor of sapling height
growth than DSF (Table 2). Few studies make an
explicit distinction between the effect of direct and diffuse radiation on plant growth (e.g. Canham 1988;
King 1991; Oberbauer et al. 1993; Clark et al. 1993),
and from these, no clear patterns emerge; if growth is
affected by light environment, then growth can be correlated with direct light, diffuse light, or both. In the
understorey, a close relation is found between direct
light and diffuse light. This relation becomes weaker at
stronger irradiances (Clark et al. 1993), and perhaps
there is sufficient uncoupling between the two light
descriptors to distinguish between the effects of direct
and diffuse light on plant growth. Gap studies (Sipe &
Bazzaz 1995; Poorter 1998) have shown that diffuse
light is a better predictor of plant growth than direct
light, probably because peak irradiances above the
photosynthetic light saturation point are not used for
carbon fixation (e.g. Wayne & Bazzaz 1993), and can
inhibit plant growth.
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
For all species but Theobroma, height growth was positively related to sapling leaf area, light environment,
or a combination of the two (Table 2). This agrees with
Most species reduced their internode length in the
shade (Table 3, cf. King 1994; Sterck 1999). In this
way, smaller masses of woody support tissue were
invested for the new production of a unit leaf tissue.
This is at the risk of an increased self-shading of the
121
Light, biomass
allocation and
growth
crown (Horn 1971). The advantage of smaller support
mass is that more biomass was available for new leaf
growth. This shift in biomass allocation from stem to
leaf mass is also reflected in the high LPR of understorey saplings (Table 5).
Morphologically, height growth is a function of the
length of the internodes and their rates of production.
Increased height growth in bright light was attained
mainly through an increase in internode production
rates, which were up to seven times higher in plants in
gaps compared to those in the understorey (Table 3).
For herbaceous stoloniferous plants, light quantity
mainly affects the production rate, and light quality
mainly affects the length of the modules (Stuefer &
Huber 1998). However, herbaceous plants increase
their module length with shade, whereas tree species
decrease their internode length with shade.
-
Eight percent of the saplings died. In addition, 17% of
the surviving saplings had a net negative RGR, mostly
because of leaf shedding and occasionally because
of branch loss or stem breakage. Interestingly, these
saplings occurred not only in severely shaded microsites
of the forest understorey, but also in brighter sites.
Although seedling experiments in controlled conditions have shown that whole-plant light compensation
points may occur at 0·5–2% of incident radiation
(Boot 1993; Poorter 1999), saplings growing in a forest
understorey respond differently. LCPs of forest-grown
saplings of several rain forest tree species are between
1% and 5% incident irradiance (King 1994). Differences
in LCP between seedling studies in controlled conditions
and saplings growing under natural conditions may be
partly because of size differences among the plants.
The whole-plant light compensation point increases
with plant size, due to a smaller LAR and smaller carbon
gain per unit plant mass (Givnish 1988; Veneklaas &
Poorter 1998). Another cause for the high LCP of
forest-grown plants is a stochastic one: under natural
conditions, plants lose biomass through herbivory
or falling debris. Leaf losses due to herbivory can be
considerable: in this study, herbivory accounted for
4% (Cecropia) to 23% (Bellucia) of the standing leaf
biomass. Falling debris from the canopy may also
damage saplings. In a Costa Rican rain forest, 25%
of understorey saplings are exposed annually to such
events (Clark & Clark 1989).
R G R n
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
Net RGR and NAR of saplings increased with irradiance (Fig. 1, Table 4), agreeing with other studies
describing above-ground sapling growth (King 1991,
1994; Moad 1992 cited in Ackerly 1996). Increases in
RGRn with light were largely due to increases in NAR
(cf. Poorter & Nagel 2000; Fig. 2a), because bright
light increases photosynthetic capacity (Rijkers et al.
2000) and rate. In general, pioneer species show a
stronger increase in photosynthetic capacity with irradiance than shade-tolerant species (Strauss-Debenedetti
& Bazzaz 1996). Therefore, it was expected that they
would also have a larger GRCNAR, yet this was not the case.
Sapling LMF increased and SLA decreased with
irradiance (Fig. 1, Table 4). LAR remained constant
over the light range regarded, as a result of opposing
influences of LMF and SLA. Similar results were
obtained by Sterck (1997) when studying whole-plant
allocation of understorey and clearing saplings of
three rain forest tree species. The LAR of Chlorocardium
saplings even increases with irradiance, mainly due
to an increase in LMF (ter Steege et al. 1994). The
greater standing leaf biomass of the sun plants can be
explained by their considerably faster leaf production
rates, and the similar or shorter leaf lifespan of sun
plants compared to shaded plants (Tables 3 and 4,
King 1994; Rijkers 2000).
The observed patterns are in sharp contrast with the
hypothesis. They do not corroborate the results from
seedling experiments stating that LMF and LAR of
shaded plants exceed those of sun plants (Popma &
Bongers 1988; Osunkoya et al. 1994; Poorter 1999).
Note that LMF is affected not only by the biomass
production, but also by the loss of the different shoot
components. In seedling studies, leaf shedding does
not occur to a significant extent because the experiments are often too short, and leaf cohorts of freshly
germinated seedlings are too young.
Species tended to differ in the effect of light-dependent
changes in their allocation on growth (Fig. 2), but this
was only significant for SLA. SLA is considered to be
a key factor in explaining growth differences between
species (Poorter & Van der Werf 1998), especially at
low irradiances (Poorter 1999). The two pioneer species
were most plastic in the response of LMF and SLA to
irradiance, and this had important repercussions for
their growth (cf. Veneklaas & Poorter 1998). Nevertheless,
GRCLMF and GRCSLA were not correlated consistently
with species’ shade tolerance, probably because of too
few data. Large plasticity in SLA has the potential to
increase sapling RGR in the shade. Pioneer species are
very plastic in their SLA, but shade-adapted species
are not likely to show such a plastic response; large
SLA increases the chances of herbivory, and lost leaf
material is difficult to replace in a light-limited environment (Kitajima 1996; Walters & Reich 1999).
Observed patterns in standing biomass fractions
(LMF, LAR) do not support the idea that shaded
plants respond to the light environment by investing
more biomass in leaf area for light interception. However, standing biomass fractions reflect the end result
of allocation, rather than the process of biomass
122
L. Poorter
allocation itself. If the LPR is considered, then it appears
that a larger proportion of the biomass growth of
shaded plants was allocated to leaves, although only
significantly for two out of six species (Table 5). LPR
correlated more strongly with RGRn than with DSF.
Similar trends in LPR were observed for other rain
forest saplings (King 1991, 1994). This suggests that
leaf partitioning is influenced by the carbon balance of
the plant rather than by the light environment, or that
RGRn is a better reflection of the actual light environment than DSF. The standing biomass fraction in
leaves is a poor indicator of the biomass partitioning
to leaves because the LPR was up to three times larger
than the LMF (compare Figs 1 and 3a). The actual LPR
may be considerably larger if maintenance respiration
is taken into account (Veneklaas & Poorter 1998).
Leaf longevity increased with shading for two out
of six species (Table 4). Similar results were obtained
for seedlings growing under controlled conditions
(Bongers & Popma 1990; Ackerly & Bazzaz 1995) and
for saplings growing in the field (Sterck 1999). At low
irradiance, carbon gain is limited. In theory, therefore,
leaf construction costs can be recovered only if leaves
live longer (cf. Williams et al. 1989; Rijkers 2000),
which is consistent with these observations.
Mean LPR ranged from 20% to 90% (Fig. 3a). It was
hypothesized that leaf partitioning rates of pioneer
species would exceed those of shade-tolerant species, because their greater leaf turnover rates require
more carbon partitioning to leaves in order to replace
those that are shed. This hypothesis does not hold
because there was neither a systematic difference in
leaf lifespan between pioneer and shade-tolerant
species (Fig. 3b), nor a significant correlation between
species’ LPR and leaf lifespan (Pearson’s r = – 0·60,
P > 0·05, n = 6). In a study on several moist forest
species in Panama (King 1994), such a negative relation
between LPR and leaf lifespan was found (Pearson’s
r = – 0·65, P < 0·05, n = 10), probably because more
species were included. Interspecific variation in LPR also
reflects interspecific variation in sapling architecture.
Species with the smallest LPR (Bellucia and Theobroma)
tend to form relatively heavy branches; species with the
largest LPR have lateral extension units that are cheap
to construct (Cecropia) or virtually absent (Capirona)
(Poorter & Werger 1999).
Conclusions
© 2001 British
Ecological Society,
Functional Ecology,
15, 113–123
Intraspecific variation in sapling growth is determined
by irradiance and leaf area per plant. Gap saplings
may have standing leaf areas similar to those of understorey saplings, because of a fast rate of leaf production. For understorey saplings, the formation of short
internodes, a large biomass partitioning to leaves, a
large SLA and long leaf lifespan may enhance light
interception and increase the chance of persistence
in shade. Species tend to differ in the effect of lightdependent changes in biomass allocation on sapling
growth, but this is not related to the shade tolerance of
the species.
Acknowledgements
Staff of Programa Manejo de Bosques de la Amazonía
Boliviana are acknowledged for their logistic support,
especially Don Nico Divico, Miguel Cuadiay, Rene
Aramayo and Luis Apaza. Maarten Terlou of the
Department of Image Analysis and Design facilitated
the scanning of the fish-eye photographs; John Grace,
Marielos Peña, Frank Sterck, Erik Veneklaas, Marinus
Werger, Pieter Zuidema and two anonymous reviewers
gave helpful comments on the manuscript. This
research was partly funded by grant BO 009701 from
the Netherlands Development Assistance.
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Received 15 May 2000; accepted 18 September 2000