Tree Physiology 20, 519–526
© 2000 Heron Publishing—Victoria, Canada
Leaf optical properties in Venezuelan cloud forest trees
LOURENS POORTER,1,2 R. KWANT,1 R. HERNÁNDEZ,3 E. MEDINA3 and M. J. A.
WERGER1
1
Department of Plant Ecology, Utrecht University, P.O. Box 800.84, 3508 TB Utrecht, The Netherlands
2
Present address: Department of Silviculture and Forest Ecology, Wageningen University, P.O. Box 342, 6700 AH Wageningen, The Netherlands
3
Centro de Ecología y Ciencias Ambientales, Instituto Venezolano de Investigaciones Cientificas, Aptdo 21827, Caracas 1020 A, Venezuela
Summary Leaf optical properties and related leaf characteristics were compared for thirteen cloud forest tree species differing in successional status. Sun leaves were sampled for the
eight pioneer species and sun and shade leaves were sampled
for the five climax species. Sun leaves had a slightly higher absorptance than shade leaves, although differences were small.
Sun leaves had a higher leaf mass per unit area (LMA) and a
lower chlorophyll concentration per unit leaf mass, resulting in
similar chlorophyll concentrations per unit leaf area and hence
similar light harvesting capacities as shade leaves. However,
shade leaves realized a higher efficiency of absorptance per
unit leaf biomass than sun leaves. There were few differences
in leaf characteristics of sun leaves between the climax and pioneer species. Absorptance values of cloud forest species were
comparable with values reported for rain forest and more seasonal forest species. Intraspecific variation in leaf absorptance
was largely the result of variation in LMA, whereas interspecific variation in leaf absorptance was largely a result of
variation in chlorophyll concentration per unit leaf area.
Keywords: carotenoids, chlorophyll, climax, cloud forest, leaf
absorptance, light, pioneer species.
Introduction
In tropical rain forests, light is an important environmental
factor affecting growth and survival of saplings and juvenile
trees (Fetcher et al. 1994, Zagt and Werger 1998). Trees adjust
their leaf morphological and physiological properties to the
light environment. In a low light environment, trees tend to
maximize foliar light interception while minimizing support
costs. Thus, shade plants have thin, horizontal leaves (Wallace
and Dunn 1980) with a low leaf mass per unit area (Bongers
and Popma 1988), and a high chlorophyll concentration per
unit leaf mass (Oberbauer and Strain 1985). As a result, shade
plants have capacities for light absorptance similar to sun
plants (Poorter et al. 1995). For plants growing in a high-light
environment, however, maximization of carbon gain per unit
leaf area is more important than efficiency of light capture.
Therefore, plants in high light produce thick leaves with high
leaf mass per unit area, multiple mesophyll cell layers (Ells-
worth and Reich 1993), a high N concentration per unit leaf
area and N investment in Calvin cycle enzymes rather than in
pigments, resulting in a low Chl/N ratio (Evans 1989, Evans
and Seemann 1989). In combination, these responses lead to a
high rate of light-saturated photosynthesis per unit leaf area
(Poorter and Oberbauer 1993, Raaimakers et al. 1995) and a
high carbon gain per unit nitrogen invested (Evans 1989).
Generally, mature green leaves absorb 80–90% of the incident photosynthetically active radiation (PAR) (Ehleringer
1988). It has been postulated that leaves of shaded plants have
a higher absorptance than leaves of sun plants, because light
limits carbon fixation in the shaded leaves. Similarly, it has
been suggested that climax species have a higher leaf absorptance than pioneer species, because pioneer species have to
cope with the high radiation load in their early successional
habitats. It has also been suggested that pioneers reduce the
heat load on their leaves by means of decreased absorptance.
Although few studies have investigated leaf spectral properties of species differing in successional status or shade tolerance, there are indications that leaves of sun and shade species
have similar reflectance and absorptance characteristics (Lee
and Graham 1986, Knapp and Carter 1998). However, these
studies included species from different life forms, growing in
different geographical locations, with their leaves being exposed to different environmental conditions. To separate the
effect of the environment and species-specific traits on leaf
optical properties, it would be more straightforward to compare species under similar environmental conditions.
There are several mechanisms by which enhanced absorptance by leaves can be achieved. Almost all PAR absorptance
is realized by chloroplast pigments such as chlorophylls and
carotenoids. Although it has been shown that absorptance increases with increasing chlorophyll concentration (Gabrielsen
1948, Evans and Seemann 1989, Agusti et al. 1994), little is
known about the role of carotenoid pigments, which consist of
lutein, α- and β-carotene and xanthophylls, in light absorptance. Besides chlorophyll and carotenoid concentrations, leaf
structure also affects absorptance. In the spongy mesophyll,
light is scattered at the cell-wall–air interface, because of the
different refractive indices of water and air. Leaves with many
intercellular airspaces have a higher probability of light absorptance by pigments, as a result of this path lengthening ef-
520
POORTER, KWANT, HERNÁNDEZ, MEDINA AND WERGER
fect (Lee et al. 1990, DeLucia et al. 1996, Vogelmann et al.
1996).
We analyzed leaf optical properties and related leaf characteristics for thirteen Venezuelan cloud forest tree species. One
might envisage that the distinct climatic conditions of the
cloud forest biome (high cloud cover and consequently a high
relative humidity and a low insolation, Richards 1996) have
led to specific adaptations at the leaf level. For example, the
relatively low insolation could be associated with a high leaf
absorptance without compromising the water balance of the
plant, because vapor pressure deficits are low. Our specific objectives were to determine: (1) how plants respond to light in
terms of leaf optical properties and related leaf characteristics;
(2) if trends in leaf characteristics of pioneer and climax species are comparable with those of sun and shade plants; (3)
whether cloud forest species have a higher absorptance than
woody species from other vegetation types; and (4) the functional relationships between light absorptance and leaf characteristics.
Materials and methods
Research was carried out in the tropical montane cloud forest
surrounding the Instituto Venezolano de Investigaciones
Científicas (10°20′ N, 66°55′ W) near Caracas, Venezuela. Elevation is about 1750 m and annual precipitation is about
1100 mm. Five climax and eight pioneer tree species were selected (Table 1). Leaf responses to growth light environment
were evaluated by comparing sun and shade leaves of the five
climax species. For each species, five trees with well-exposed
crowns were sampled for a pair of sun leaves and five trees in
the understory were sampled for a pair of shade leaves. Sun
leaves of eight pioneer species were sampled for comparison
with the climax species. For each pioneer species, five pairs of
sun leaves were selected from between two and five trees per
species. Leaves were sampled by removing leafy branches.
Table 1. Summary of the study species. Group refers to successional
status.
Species
Family
Group
Clethra fragifolia
Clusia minor
Clusia multiflora
Heliocarpus americanus
Hyeronima moritziana
Miconia dodecandra
Oyedaea verbesinoides
Vismia lindeniana
Aspidosperma fendlerii
Graffenrieda latifolia
Podocarpus pittierri
Richeria grandis
Tetrorchidium rubrivenium
Clethraceae
Clusiaceae
Clusiaceae
Tiliaceae
Euphorbiaceae
Melastomataceae
Asteraceae
Clusiaceae
Apocynaceae
Melastomataceae
Podocarpaceae
Euphorbiaceae
Euphorbiaceae
Pioneer
Pioneer
Pioneer
Pioneer
Pioneer
Pioneer
Pioneer
Pioneer
Climax
Climax
Climax
Climax
Climax
The excised branches were placed in water bottles and transported to the laboratory. Care was taken to sample fully
expanded mature leaves without damage. Epiphylls were
gently removed from the leaves as much as possible, with a
soft sponge. For species with compound leaves, two opposite
leaflets were selected, whereas for species with single leaves,
the nearest leaf next to the target leaf was selected. One
leaf(let) was used to measure leaf absorptance, and the other
was used to determine leaf chemical characteristics. Leaves
were analyzed for their spectral properties within 1 to 3 h after
the branch was removed from the tree. The leaf was placed in
an LI-1800-12 integrating sphere connected to an LI-1800
spectroradiometer (Li-Cor Inc., Lincoln, NE). For the adaxial
side of the leaves, reflectance and transmittance were determined at 2-nm intervals for the 400–700 nm wavelength
range. Absorptance (Abs) was calculated as: Absorptance =
(1 – reflectance – transmittance).
Subsequently, leaf area was measured with a leaf area meter
(Li-Cor LI-3100). Leaves were then oven-dried for 3 days at
70 °C and weighed, and leaf mass per unit leaf area (LMA)
calculated. Organic nitrogen content of leaf punches was determined with a continuous flow analyzer after Kjeldahl digestion. Chlorophyll a and b and carotenoids (xanthophylls
plus carotenes) were extracted, and pigment concentrations
were calculated according to the formulas given by
Lichtenthaler and Wellburn (1983). Henceforth chlorophyll
will be referred to as Chl, carotenoids as Car and nitrogen as
N. Subscripts “a” and “m” indicate whether concentrations are
expressed on an area or mass basis, respectively.
Statistical analysis was carried out with SPSS 6.0 (SPSS
Inc., Chicago, IL; 1993). A two-way ANOVA was used to
evaluate whether PAR absorptance and related leaf characteristics differed between light environments and between species. Absorptance data were arcsine-transformed before
analysis to meet the assumption of symmetrically distributed
data. Data were checked for homoscedasticity with the Bartlett-Box F-statistic. If necessary, variables were log-transformed to stabilize variances.
To compare the spectral properties of sun leaves of pioneer
and climax species, a two-way ANOVA was performed, with
species nested within successional status. A Student’s t-test
was applied for the other leaf variables, based on species’
means as data points. To compare the absorptance of cloud
forest species with published absorptance data for tree and
shrub species from other tropical vegetation types (arid shrub
land, forests with a seasonal aspect, evergreen rain forest), we
used a one-way ANOVA and a Student-Newman-Keuls test.
Two types of regression analysis were performed to evaluate how leaf characteristics (Chla, Cara, LMA) contribute to
intraspecific and interspecific variation in absorptance. Data
for sun and shade leaves of the five climax species were used
to explain intraspecific patterns in absorptance. A multiple regression analysis was carried out, with the leaf characteristic
of interest as the continuous variable and species as dummy
variables. To evaluate the relative importance of factors in explaining interspecific variation in absorptance, a multiple regression was carried out, with mean values for sun leaves of
climax and pioneer species as data points.
TREE PHYSIOLOGY VOLUME 20, 2000
LEAF OPTICAL PROPERTIES IN CLOUD FOREST TREES
521
higher Chl a to Chl b (Table 2) and carotenoid to chlorophyll
ratios than shade leaves (Figure 2b) (P < 0.001).
Results
Sun versus shade leaves
Mean values for the leaf characteristics measured and results
of statistical analysis are presented in Tables 2 and 3. Sun and
shade leaves differed in their spectral properties. Sun leaves
had similar reflectance (P > 0.05) and a lower transmittance
(P < 0.001) compared with shade leaves, resulting in a PAR
absorptance that was on average slightly higher for sun leaves
than for shade leaves (90.9 versus 90.0%; P < 0.001).
In all species, shade leaves had higher chlorophyll,
carotenoid, and nitrogen concentrations per unit biomass than
sun leaves (P < 0.05). However, sun leaves had a higher LMA,
resulting in a similar chlorophyll concentration per unit leaf
area (P > 0.05) and higher carotenoid and nitrogen concentrations per unit leaf area (P < 0.001) compared with shade
leaves.
Efficiency of absorptance can be defined as absorptance per
unit chlorophyll, carotenoid, or biomass invested. Compared
with sun leaves, shade leaves had a similar absorptance per
unit chlorophyll, but a higher efficiency per unit carotenoid or
biomass invested (P < 0.001, Figure 1, Table 3). Sun leaves
had a lower ratio of chlorophyll to nitrogen (Figure 2a), and
Pioneer versus climax species
Sun leaves of pioneer species had reflectance, transmittance
and absorptance properties that were comparable with those of
climax species (P > 0.05 in all cases; Table 4). However,
within the successional group, there were appreciable differences between species (P < 0.001 in all cases); absorptance
ranged from 84.7% for the pioneer Clethra to 93.1% for the pioneer Heliocarpus. Efficiencies of absorptance were similar
for both successional groups. Climax species had signifiantly
higher Na and Cara than pioneer species; however, the two
successional groups did not differ significantly for any of the
other leaf characteristics examined.
Cloud forest species versus species from other vegetation
types
Despite striking variation in microclimatic conditions, there
was little variation in leaf absorptance between woody species
from different vegetation types (P < 0.001). Although cloud
forest species had on average the highest absorptance (89.6%)
of the vegetation types examined, they only differed signifi-
Table 2. Leaf characteristics of sun and shade leaves of five cloud forest climax tree species. Means and standard errors of untransformed data are
shown (n = 5).
Species
Reflectance (%)
Transmittance (%)
Absorptance (%)
LMA (g m –2)
Abs/Chl (% mmol –1)
Abs/Car (% mg –1)
Abs/biomass (% g –1)
Chlm (µmol g –1 )
Chla (µmol m –2)
Carm (mg g –1)
Cara (mg m –2)
Nm (mmol g –1)
Na (mmol m –2)
Chl a/Chl b
Leaf type
Aspidosperma
Graffenrieda
Podocarpus
Richeria
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
Shade
Sun
7.7 ± 0.1
7.3 ± 0.3
1.7 ± 0.2
0.7 ± 0.2
90.6 ± 0.1
92.0 ± 0.5
76.2 ± 5.3
120.0 ± 1.4
144 ± 8
162 ± 18
1.00 ± 0.06
0.86 ± 0.09
1.21 ± 0.09
0.77 ± 0.01
8.4 ± 0.6
5.0 ± 0.6
638 ± 33
600 ± 71
1.14 ± 0.08
0.93 ± 0.10
92 ± 6
112 ± 12
1.40 ± 0.09
1.13 ± 0.07
105 ± 4
144 ± 8
3.27 ± 0.09
4.29 ± 0.12
7.8 ± 0.2
8.5 ± 0.2
4.7 ± 0.3
4.6 ± 0.6
87.5 ± 0.4
86.9 ± 0.7
39.4 ± 1.0
72.2 ± 1.0
227 ± 8
269 ± 16
1.87 ± 0.15
1.35 ± 0.12
2.23 ± 0.06
1.20 ± 0.01
9.6 ± 0.3
4.5 ± 0.3
386 ± 11
328 ± 20
1.20 ± 0.05
0.91 ± 0.06
48 ± 4
66 ± 5
1.59 ± 0.14
1.43 ± 0.05
63 ± 6
110 ± 6
2.87 ± 0.08
3.76 ± 0.10
6.6 ± 0.2
6.4 ± 0.2
1.7 ± 0.2
0.5 ± 0.1
91.7 ± 0.3
93.1 ± 0.3
87.4 ± 2.3
195.1 ± 12.0
145 ± 5
191 ± 28
1.22 ± 0.11
1.02 ± 0.11
1.05 ± 0.03
0.48 ± 0.03
7.5 ± 0.4
2.8 ± 0.5
636 ± 23
538 ± 91
0.94 ± 0.08
0.50 ± 0.06
78 ± 7
96 ± 11
0.94 ± 0.15
0.84 ± 0.10
81 ± 13
163 ± 23
2.95 ± 0.17
3.87 ± 0.27
6.4 ± 0.2
6.9 ± 0.2
2.2 ± 0.3
1.2 ± 0.1
91.5 ± 0.4
91.9 ± 0.3
60.5 ± 2.9
112.1 ± 1.3
139 ± 7
119 ± 3
1.25 ± 0.06
0.64 ± 0.02
1.53 ± 0.07
0.82 ± 0.01
11.2 ± 1.0
6.9 ± 0.2
666 ± 40
778 ± 22
1.28 ± 0.09
1.29 ± 0.04
74 ± 4
144 ± 5
1.72 ± 0.14
1.30 ± 0.06
102 ± 4
145 ± 6
2.93 ± 0.07
3.86 ± 0.11
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Tetrorchidium
6.9 ± 0.3
7.1 ± 0.1
4.6 ± 0.3
2.3 ± 0.1
88.5 ± 0.5
90.6 ± 0.1
36.9 ± 1.5
72.2 ± 4.3
169 ± 9
173 ± 4
2.12 ± 0.09
0.85 ± 0.11
2.42 ± 0.11
1.27 ± 0.07
11.1 ± 1.1
7.4 ± 0.4
528 ± 28
526 ± 13
1.14 ± 0.05
1.57 ± 0.20
42 ± 2
112 ± 11
2.55 ± 0.02
1.66 ± 0.04
94 ± 4
119 ± 6
3.25 ± 0.16
4.72 ± 0.18
All
7.1 ± 0.1
7.2 ± 0.2
3.0 ± 0.3
1.9 ± 0.3
90.0 ± 0.4
90.9 ± 0.5
60.0 ± 4.2
114.3 ± 9.5
165 ± 7
183 ± 12
1.49 ± 0.10
0.94 ± 0.06
1.69 ± 0.11
0.91 ± 0.06
9.6 ± 0.4
5.3 ± 0.4
571 ± 24
554 ± 37
1.14 ± 0.04
1.04 ± 0.09
67 ± 4
106 ± 6
1.64 ± 0.12
1.27 ± 0.06
89 ± 4
136 ± 6
3.05 ± 0.06
4.10 ± 0.10
522
POORTER, KWANT, HERNÁNDEZ, MEDINA AND WERGER
Table 3. Results of a two-way ANOVA for characteristics of sun and
shade leaves of five cloud forest tree species. Influence of growth
light environment, species and their interaction are shown. Significance of the factors and explained variance of the model are indicated
by asterisks (* = P < 0.01, ** = P < 0.05, and *** = P < 0.001) and the
coefficient of determination (r 2), respectively. The kind of transformation (Transform.) that was applied before analysis is indicated.
Variable
Transform. Light
Species
Interaction
r2
Reflectance
Transmittance
Absorptance
LMA
Chlm
Chla
Carm
Cara
Nm
Na
Chl a/Chl b
Chl/N
Car/Chl
Abs/Chl
Abs/Car
Abs/Biomass
Arcsine
Arcsine
Arcsine
Log
Log
Log
Log
Log
–
Log
–
Log
Log
Log
–
Log
***
***
***
***
***
***
***
***
***
***
***
ns
*
***
***
***
*
**
*
***
**
ns
***
***
**
ns
ns
ns
***
ns
***
*
0.72
0.91
0.87
0.97
0.85
0.73
0.75
0.83
0.85
0.67
0.80
0.54
0.79
0.71
0.84
0.97
ns
***
***
***
***
ns
**
***
***
***
***
***
***
ns
***
***
cantly from arid shrubland species (Figure 3).
Functional relationships
To explain intraspecific differences in absorptance, a regression analysis was carried out with species as dummy variables
and pigment concentrations or LMA as explanatory variables
(Table 5). In all cases, the models were highly significant, with
Figure 2. (a) Chlorophyll/nitrogen ratio and (b) carotenoid/chlorophyll ratio for shade (open bar) and sun (hatched bar) leaves of five
cloud forest climax tree species. Means and standard errors are shown
(n = 5).
coefficients of determination (r 2) ≥ 0.78. Species differed significantly in absorptance. Intraspecific differences in
absorptance were positively related to Chl a/Chl b, Cara and
LMA, but not to chlorophyll concentration. A multiple regression analysis with species, Chla, Cara and LMA as explanatory
variables showed that LMA was the only factor giving rise to
Table 4. Leaf characteristics of pioneer (n = 8) and climax (n = 5) tree
species. Means and standard errors, as well as results of a nested
ANOVA (for reflectance, transmittance and absorptance, n = 65) and
a Student’s t-test (for other leaf characteristics, n = 13) are shown.
Variable
Figure 1. Efficiencies of absorptance for shade (open bars) and sun
(hatched bars) leaves of five cloud forest climax tree species. Efficiencies are expressed as absorptance per unit (a) chlorophyll, (b)
carotenoid, and (c) leaf biomass. Grand means and standard errors for
pooled sun (n = 25) and shade leaves (n = 25) are shown. Asterisks indicate levels of significance: *** = P < 0.001; and ns = not significant.
Reflectance
Transmittance
Absorptance
LMA
Chlm
Chla
Carm
Cara
Nm
Na
Chl a/Chl b
Chl/N
Car/Chl
Abs/Chl
Abs/Car
Abs/LMA
Units
(%)
(%)
(%)
(g m –2)
(µmol g –1)
(µmol m –2)
(mg g –1)
(mg m –2)
(mmol g –1)
(mmol m –2)
(mmol mol –1)
(g mol –1)
(% mmol –1)
(% mg –1)
(% g –1)
TREE PHYSIOLOGY VOLUME 20, 2000
Climax
Pioneer
P
Mean
SE
Mean SE
7.23
1.86
90.91
114.3
5.33
554
1.04
106.0
1.27
136.5
4.10
4.24
196
183
0.94
0.91
0.35
0.76
1.08
22.5
0.83
72
0.18
12.7
0.14
9.5
0.18
0.38
5
25
0.12
0.15
7.70
3.52
88.78
89.3
4.94
423
0.9
77.8
1.19
101.9
3.71
4.33
193
221
1.16
1.04
0.25
0.89
1.01
7.4
0.61
38
0.12
3.9
0.15
8.5
0.32
0.57
16
19
0.05
0.1
ns
ns
ns
ns
ns
ns
ns
0.01
ns
0.01
ns
ns
ns
ns
ns
ns
LEAF OPTICAL PROPERTIES IN CLOUD FOREST TREES
523
Figure 3. Leaf absorptance (means and SE) of tropical shrub and tree
species from arid shrublands (AS, n = 8), forests with a seasonal aspect (SF, n = 12), rain forests (RF, n = 29) and cloud forests (CF, n =
13). Bars with a different letter are significantly different at P = 0.05.
Data were obtained from Langenheim et al. 1984, Lee and Graham
1986, Lee et al. 1986, Thompson et al. 1992, Poorter et al. 1995 and
the present study.
intraspecific variation in absorptance (n = 50, PLMA < 0.05;
Pspecies < 0.01; Pmodel < 0.001; r 2model =0.83).
Interspecific differences in absorptance could be related to
differences in chlorophyll concentration (P < 0.001) and Cara
(P < 0.01), but not to LMA (P > 0.05) (Figure 4; Table 5). Multiple regression with Chla, Cara and LMA as independent variables showed that chlorophyll concentration per unit leaf area
was the only factor contributing significantly to interspecific
differences in absorptance (n = 13, PChl < 0.01; Pmodel < 0.01;
r 2model = 0.81).
Discussion
Sun versus shade leaves
Sun leaves had a lower transmittance, similar reflectance, and
hence a slightly higher absorptance than shade leaves. This
finding contrasts with the hypothesis that shade leaves are
more light-limited than sun leaves and therefore should have a
leaf design that enables them to absorb a higher proportion of
the incident light. Enhanced absorptance in sun leaves was
mainly a result of a higher LMA. Although differences in
Table 5. Results of regressions of intraspecific (n = 50) and
interspecific (n = 13) variations in leaf absorptance against log-transformed LMA and pigment densities as independent variables. Significance (* = P < 0.01, ** = P < 0.05, and *** = P < 0.001) of LMA and
pigment density (variable), and species, and the coefficient of determination (r 2) of the model are shown.
Variable
Chla a
Chla b
Chla
Chl a/Chl b
Cara
LMA
Intraspecific
Interspecific
Variable Species
r2
Model
r2
Model
ns
ns
ns
**
**
**
0.79
0.78
0.78
0.81
0.81
0.81
***
***
***
***
***
***
0.72
0.62
0.74
0.01
0.34
0.30
***
**
***
ns
*
ns
***
***
***
***
***
***
Figure 4. Species-specific absorptance versus (a) chlorophyll concentration per unit area, (b) carotenoid concentration per unit area, and
(c) LMA, for sun leaves of five climax (䊉) and eight pioneer (䊊) species.
spectral properties of sun and shade leaves were small, the avenues by which absorptances were realized were strikingly
different. Shade leaves had a lower LMA and a higher chlorophyll concentration per unit biomass than sun leaves, leading
to a chlorophyll concentration on an area basis that was similar
for sun and shade leaves. Because of equivalent absorptance
efficiencies per unit chlorophyll (Figure 1a), the sun and shade
leaves had comparable light harvesting capacities.
Although sun and shade leaves had a similar absorptance,
the shade leaves were 60–120% more efficient in light capture
per unit biomass (Figure 1c). Efficient use of biomass for light
harvesting would provide an advantage in the forest
understory, where carbon fixation limits plant growth. Similar
patterns in PAR absorptance, LMA, and chlorophyll concentrations were found by Poorter et al. (1995) for leaves of four
rain forest tree species along a height gradient in the canopy.
Understory leaves were more efficient in light capture per unit
biomass than canopy leaves, with mid-canopy leaves realizing
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524
POORTER, KWANT, HERNÁNDEZ, MEDINA AND WERGER
intermediate values.
Nitrogen is another scarce resource that can limit photosynthetic capacity and whole-plant carbon gain (Field and Mooney 1986, Anten et al. 1995). Under shade conditions,
relatively more N was invested in chlorophyll as indicated by a
high Chl/N ratio (Figure 2a) (cf. Evans 1996, Niinemets
1997). Under high-light conditions, the Chl/N ratio declined
(Figure 2a) as relatively more nitrogen was invested in
carboxylation enzymes at the expense of nitrogen investment
in light harvesting components (Evans and Seemann 1989).
Both a higher nitrogen concentration per unit area (Table 2)
and an altered nitrogen partitioning within the leaf may lead to
a higher light-saturated photosynthetic rate for sun leaves
compared with shade leaves (Raaimakers et al. 1995).
Concentrations of Cara were on average 60% higher for sun
leaves than for shade leaves (Table 2), possibly because carotenoids have a dual function in the pigment–protein complex.
Carotenoids not only intercept light (Figure 3b) (Siefermann-Harms 1987) but the xanthophyll carotenoids also allow for effective heat dissipation when excess light is
absorbed. At high irradiances, xanthophyll cycle carotenoids
like violaxanthin and antheraxanthin are converted to zeaxanthin. The latter two pigments may accept excess energy
from the excited singlet chlorophyll and lose it in the form of
heat, thereby preventing photo-oxidative damage to the leaf
(Demmig-Adams and Adams 1996a). A higher probability of
excess light might be the reason for an increased carotenoid to
chlorophyll ratio in sun leaves (Figure 2b). Similar patterns
were found for sun and shade leaves of a temperate shrub
(Demmig-Adams and Adams 1996b), for Australian rain forest plants occurring along a light gradient from a gap to
understory (Logan et al. 1996) and for leaves occurring in the
canopy and the understory (Königer et al. 1995). In these studies, there was not only an increase in carotenoid to chlorophyll
ratio in high-light leaves, but also an increase in the percentage
of carotenoids involved in the xanthophyll cycle.
The Chl a/Chl b ratio was lower in shade leaves than in sun
leaves (Table 2). A decreased Chl a/Chl b ratio in shade is
thought to maintain the energy balance between photosystems
I and II, by capturing the deficient red light in the forest shade
more efficiently (Björkman 1981). This contention is not always supported by direct absorptance measurements. In a Japanese forest, it was shown that, for 12 out of 16 species, a
decreased Chl a/Chl b ratio led to an increased absorptance of
red light over far-red light; however, for the other four species
the reverse was the case (Lei et al. 1996).
Pioneer versus climax species
There were few differences in leaf characteristics between pioneer and climax species (Table 4) compared with the many
differences between sun and shade leaves (Table 3). This
might be because sun leaves of climax and pioneer species
were exposed to the same environmental constraints, giving
rise to similar leaf characteristics.
Pioneer and climax species had similar leaf optical properties (Table 4). This finding contrasts with the hypothesis that
pioneer species, adapted to the high radiation load in their
early successional habitats, will reduce the heat load on their
leaves by an increased reflectance and a decreased absorptance. However, our results corroborate the findings of Lee
and Graham (1986) and Knapp and Carter (1998).
Climax and pioneer species differed only in Na and Cara
(Table 4), with climax species having a higher Na and Cara
than pioneer species. This difference does not support the suggestion that high Na and Cara provide an advantage in early
successional habitats, where a high Na gives rise to a high photosynthetic capacity, and a high Cara protects the photosynthetic apparatus. In an extensive study on leaf characteristics
of Mexican rain forest species, Popma et al. (1992) also found
that pioneers had a lower N concentration per unit area than
gap-dependent species. They reported that pioneers and
late-successional species differed mainly in LMA and leaf
size, with pioneers having a lower LMA and larger leaves.
Cloud forest species versus species from other vegetation
types
Leaf absorptance increased slightly with the humidity of the
habitat (Figure 3) (cf. Ehleringer and Werk 1984). Yet, despite
the large variation in microclimatic conditions, there was little
variation in leaf absorptance among species from different
vegetation types. This strong convergence in optical properties is in line with the findings for sun and shade leaves, and
for pioneer and climax species.
Functional relationships
We related Chla, Cara, and LMA separately to intra- and
interspecific differences in leaf absorptance (Table 5;
Figure 4). Multiple regression showed that intraspecific differences were the result of changes in LMA, whereas interspecific differences were largely the result of changes in Chla.
Relationships between absorptance and Cara were weak, perhaps because of the dual role of carotenoids in light absorptance and energy dissipation.
A higher LMA led to higher absorptances as a result of increased chlorophyll and carotenoid concentrations per unit
area; however, LMA was also an important factor in itself. A
high LMA reflects thick leaves with an increased number of
cell layers (Lee et al. 1990, Lambers and Poorter 1992). A
light beam penetrating such a leaf will have to pass more
cell-wall–air interfaces, with a higher probability of being
scattered. An increased path-length will in turn lead to an enhanced absorptance, especially in the green wavelength range.
The roles of pigments and LMA in leaf absorptance remain
controversial. Interspecific variation in absorptance has been
found to correlate with leaf thickness (Gausman and Allen
1973, Knapp and Carter 1998) and chlorophyll a concentration on an area basis (Agusti et al. 1994). Based on a literature
review, Evans (1998) concluded that interspecific differences
in absorptance were caused by differences in chlorophyll concentration on an area basis, rather than differences in LMA.
However, in a study on absorptance of rain-forest herb and
tree species, no relationship was found between absorptance
and LMA, or between absorptance and Chla (Lee et al. 1990).
Because interspecific differences in absorptance of Venezuelan cloud forest species could be predicted from chlorophyll concentrations alone, we determined whether this
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LEAF OPTICAL PROPERTIES IN CLOUD FOREST TREES
525
expense of rapidly diminishing returns per unit chlorophyll invested; however, such an expense is worthwhile for plants
growing in deep shade (cf. Evans and Seemann 1989).
Acknowledgments
We thank staff and personnel of IVIC for their logistic support during
this study.
References
Figure 5. Relationship between absorptance and chlorophyll concentration for sun and shade leaves of 76 herb, shrub, and tree species. An
asymptotic light response curve was fitted through the data; Abs =
97.8 × 2068[Chl]/(97.7 + 2068[Chl]) (n = 77, P < 0.001, r 2 = 0.89).
The thick curve shows the predicted in vitro PAR absorptance, based
on the Lambert-Beer equation; A = 100(1–e–2240[Chl]/903), in which
903 is the mean molecular mass of chlorophyll and [Chl] is the chlorophyll concentration in g m –2. The curve with the broken line indicates the difference between the two lines. If various observations
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