Tree Physiology 26, 865–873
© 2006 Heron Publishing—Victoria, Canada
Changes in photosynthesis and leaf characteristics with tree height in
five dipterocarp species in a tropical rain forest
TANAKA KENZO,1,2,7 TOMOAKI ICHIE,3,4 YOKO WATANABE,5 REIJI YONEDA,2 IKUO
NINOMIYA6 and TAKAYOSHI KOIKE5
1
The United Graduate School of Agricultural Sciences, Ehime University, Matsuyama, 790-8566, Japan
2
Present address: Forestry and Forest Products Research Institute, Tsukuba, 305-8687, Japan
3
Center for Tropical Forest Science - Arnold Arboretum, Asia Program, NIE-NTU, 637616, Singapore
4
Present address: Faculty of Agriculture, Kochi University, Nankoku, 783-8502, Japan
5
Hokkaido University Forests, FSC, Sapporo, 060-0809, Japan
6
Faculty of Agriculture, Ehime University, Matsuyama, 790-8566, Japan
7
Corresponding author ([email protected])
Received April 11, 2005; accepted September 15, 2005; published online April 3, 2006
Summary Variations in leaf photosynthetic, morphological
and biochemical properties with increasing plant height from
seedlings to emergent trees were investigated in five dipterocarp species in a Malaysian tropical rain forest. Canopy
openness increased significantly with tree height. Photosynthetic properties, such as photosynthetic capacity at light saturation, light compensation point, maximum rate of carboxylation and maximum rate of photosynthetic electron
transport, all increased significantly with tree height. Leaf
morphological and biochemical traits, such as leaf mass per
area, palisade layer thickness, nitrogen concentration per unit
area, chlorophyll concentration per unit dry mass and chlorophyll to nitrogen ratio, also changed significantly with tree
height. Leaf properties had simple and significant relationships
with tree height, with few intra- and interspecies differences.
Our results therefore suggest that the photosynthetic capacity
of dipterocarp trees depends on tree height, and that the trees
adapt to the light environment by adjusting their leaf morphological and biochemical properties. These results should aid in
developing models that can accurately estimate carbon dioxide
flux and biomass production in tropical rain forests.
Keywords: Dipterocarpaceae, leaf morphology, nitrogen content, palisade layer, photosynthetic capacity, Sarawak.
Introduction
The vertical structure of a forest is complex and multilayered,
resulting in great variation in light availability with height
(Yoda 1978, Kimmins 1997). Most canopy trees experience
diverse light conditions during their lifetime, starting as seedlings on the poorly lit forest floor but gaining access to the
well-lit canopy layer at maturity. Many tree species have different photosynthetic capacities at light saturation (Amax) according to growth stage or light conditions, or both, as a result
of differences in leaf morphological and biochemical properties (Körner 1994, Larcher 2003). It is well known that sun
leaves have higher leaf nitrogen and leaf mass per area
(LMA), corresponding to higher Amax, than shade leaves.
Shade leaves have a higher leaf chlorophyll content and are
thinner and thus have a lower dark respiration rate and light
compensation point (I c) than sun leaves (Lambers et al. 1998).
However, there is little information on the variations in leaf
photosynthetic, morphological and biochemical traits in tropical rain forests, which account for a substantial fraction of
global primary production (Chapin et al. 2002, Kumagai et al.
2004). To guide development of models of carbon dioxide
(CO2) fixation in tropical rain forests (see review by
Ehleringer and Field 1993), there is a need for a detailed understanding of the changes in leaf physiological and morphological characteristics with depth in the forest profile.
Tropical rain forests have a particularly complex and multilayered vertical structure (Whitmore 1998). The crown surface
of emergent trees in tropical rain forests are exposed to high
solar irradiances (Chazdon et al. 1996), but less than 1% of the
solar radiation incident above the canopy typically reaches the
forest floor. Carswell et al. (2000) and Rijkers et al. (2000)
conducted studies to determine how tree leaves respond to the
drastic differences in light conditions at differing heights under the closed canopy of a tropical rain forest and reported that
Amax, LMA and leaf nitrogen content increased significantly
with tree height in some neotropical forest trees, though neither report gave much information about large canopy trees or
emergent trees.
Studies designed to determine if photosynthetic capacity of
canopy and emergent trees increases with height in the tropical
rain forest have shown that an age- or size-dependent decrease
in leaf nitrogen content and an increase in LMA parallel the
ontogenetic decrease in Amax in some canopy species (Yoder et
al. 1994, Fredericksen et al. 1996, Bond 2000, Thomas and
866
KENZO ET AL.
Winner 2002, Koch et al. 2004). In general, a decline in leaf nitrogen content causes a reduction in Amax in tall trees (Bond
2000, Niinemets 2002). Because Amax may also depend on
LMA (Thomas and Winner 2002), an increase in LMA with
tree size leads to an increase in resistance to CO2 diffusion
within the leaf and eventually, a decrease in Amax (Terashima et
al. 2001, Niinemets 2002). It is possible, however, that tropical
canopies and emergent trees achieve a high Amax by developing
a leaf mesophyll structure that is adjusted to the tropical forest
canopy environment. Kenzo et al. (2004) reported that, in
some canopy species with high Amax (~ 20 µmol m – 2 s – 1) in the
tropical rain forest of Southeast Asia, Amax had a higher positive correlation with leaf mesophyll structure, such as leaf palisade layer thickness and surface area of mesophyll cells per
unit leaf area (Ames /Aa), than with area-based leaf nitrogen concentration and LMA. We therefore hypothesized that tree
height of tropical canopy species does not limit Amax.
To test this hypothesis, we determined the effects of tree
height on leaf photosynthesis and on leaf morphological and
biochemical properties, in five dipterocarp species. We studied
specimens ranging from seedlings on the poorly lit forest floor
to mature canopy trees in the brightly lit canopy layer, which
we accessed with a canopy crane (Ozanne et al. 2003). We paid
particular attention to differences in photosynthetic capacity
and leaf traits with depth within the closed canopy, rather than
with crown position of each individual.
Materials and methods
Study site
The study was carried out in an experimental plot (200 ×
200 m) in an intact lowland mixed dipterocarp forest in
Lambir Hills National Park, Sarawak, Malaysia (4°20′ N,
113°50′ E, 150–250 m a.s.l.), in September 2002. Mean height
of the canopy was 30–40 m and some emergent trees reached
50 m. An 80-m tall canopy crane with a 75-m-long rotating jib
was constructed in the center of the plot to provide three-dimensional access, from close to the forest floor to the top of
the canopy (Sakai et al. 2002, Ozanne et al. 2003, Kumagai et
al. 2004).
The study area has a humid tropical climate, with weak seasonal changes in rainfall and temperature (Kato et al. 1995).
Annual precipitation at the study site averaged 2429 mm from
2000 to 2003. Mean annual temperature from 2000 to 2003
was 26.3 °C, with monthly means that varied from 25.6 °C in
February to 27.0 °C in May.
Plant material and canopy openness
We selected 65 individuals of five dipterocarp species, from
seedlings to mature trees (Table 1). The species were Dipterocarpus globosus Vesq. (DG), Dryobalanops aromatica
Gaertn. f. (DA), Shorea acuta Ashton (SA), S. beccariana
Burck (SB) and S. macroptera Dyer (SM). All are evergreen
trees that grow to the forest canopy layer. In particular, DG,
DA and SB are common emergent species at the study site
(Itoh et al. 1995, Lee et al. 2002).
Tree heights ranged from 0.6 to 53 m. The seedlings and
saplings (0.6–5m tall) were chosen from, or close to, gaps (n =
3 for each species) and from beneath a closed canopy (n = 3 for
each species). Canopy openness at the top of the trees studied
was estimated from hemispherical photographs (Coolpix
5000, Nikon; Fisheye Converter FC-E8, Nikon, Tokyo, Japan;
Yamamoto 2000).
Gas exchange measurements
Leaf gas exchange rate was measured with a portable photosynthesis apparatus (LI-6400, Li-Cor, Lincoln, NE). All measurements were made between 0800 and 1100 h to avoid the
midday depression in photosynthesis (Ishida et al. 1996,
Hiromi et al. 1999, Kenzo et al. 2003). We measured fully expanded and apparently non-senescing leaves taken from the
top of the crown (the same positions as the canopy openness
measurements). To ensure that leaf age was not a variable
within and across species, the age of the leaves of the study
species was estimated from position on the branch, leaf texture
and, particularly, leaf color (Sobrado and Medina 1980, Ishida
et al. 1996) measured with a chlorophyll meter (SPAD-502,
Konica Minolta Holdings, Tokyo, Japan). Gas exchange measurements were made on the third to fifth leaf from the shoot
apex, for which the SPAD values were fairly stable (Ishida et
al. 1996, Kenzo et al. 2004).
A–PPF curve measurements The relationship between photosynthetic photon flux (PPF) and carbon assimilation rate (A)
was determined for three leaves from each tree. Photosynthetic
photon flux, CO2 concentration and temperature in the chamber were controlled at 0 to 1800 µmol m – 2 s – 1, 360 ppm and
30 °C, respectively. Illumination was supplied by an internal
LED light source (Li-Cor, LI-640B). From the gas exchange
measurements, Amax and I c were estimated. Light compensation point, defined here as the instantaneous compensation
point, is the PPF at which photosynthesis just balances respiration (Ashton and Turner 1979).
A–Ci curve measurements The A–Ci curves were made with
the LI-6400 equipped with a CO2 injector (Li-Cor, LI6400–01). The PPF and temperature in the chamber were
maintained at 1000–1500 µmol m – 2 s – 1 and 30 °C, respectively. The leaf selection criteria were the same as for A–PPF
curve measurements. The A–Ci curves were analyzed by the
mechanistic model of CO2 assimilation proposed by Farquhar
et al. (1980) and modified by Sharkey (1985) and Harley and
Table1. Tree species, species code, number of individuals and maximum (Hmax ) and minimum (Hmin) tree heights.
Species
Code
Individual
Hmax (m) Hmin (m)
Dipterocarpus globosus
Dryobalanops aromatica
Shorea acuta
Shorea beccariana
Shorea macroptera
DG
DA
SA
SB
SM
13
12
15
11
12
46.0
49.4
39.5
52.5
27.5
TREE PHYSIOLOGY VOLUME 26, 2006
0.6
0.6
1.0
1.0
0.7
VERTICAL CHANGES IN PHOTOSYNTHESIS IN TROPICAL TREES
Sharkey (1991). From the A–Ci curve, maximum rate of
carboxylation (Vcmax, µmol m – 2 s –1) and maximum rate of photosynthetic electron transport (J max, µmol m – 2 s – 1) were estimated by nonlinear regression techniques (KaleidaGraph ver
3.52; Harley et al. 1992, Wullschleger 1993).
Following the gas exchange measurements, the leaves were
collected and their area, blade thickness and fresh mass measured. The leaves were then divided into three groups: one for
measuring dry mass and nitrogen content; one for chlorophyll
analysis; and one for observation of mesophyll structure.
Leaf nitrogen and chlorophyll determination
Leaf nitrogen and carbon contents were determined with an
NC analyzer (Sumigraph NC-900, Shimadzu, Kyoto, Japan)
after leaves had been dried at 60 °C for 3 days and their dry
mass measured. Chlorophyll was extracted with dimethyl
sulfoxide (DMSO) (Barnes et al. 1992, Shinano et al. 1996)
and absorbances at 664.9 and 648.2 nm were determined spectrophotometrically (UV-1400, Shimadzu, Kyoto, Japan).
Leaf mesophyll structure
Leaves selected for observation of mesophyll structure were
fixed in FAA (40% formaldehyde:acetic acid:70% ethanol;
2:1:17, v/v) and transverse slices prepared. The transverse
slices were frozen in a drop of distilled water and sectioned
with a sliding microtome. Transverse sections (about 150 to
530 µm thick) were observed and photographed with the aid of
a light microscope (BH-2, Olympus, Tokyo, Japan). Transmitted light images of transverse sections were also obtained with
a confocal laser scanning microscope (LSM-310, Carl Zeiss,
Oberkochen, Germany; Kitin et al. 1999). The thicknesses of
the leaf blade and palisade layer were determined from a micrograph at 200× magnification. The surface area of mesophyll cells per unit leaf area (Ames /Aa) was estimated by the
method of Nobel (1999).
867
Leaf photosynthetic properties and tree height
Photosynthetic rate at light saturation and I c increased significantly with tree height both within and across species (Figures 2A and 2B). There were no interspecific differences in
Amax and I c with tree height (ANCOVA; P > 0.05), except for
Amax of canopy individuals of SB. The I c value of understory
seedlings was relatively low, usually less than 10 µmol m – 2
s– 1.
Maximum rate of carboxylation by Rubisco (Vcmax) and
maximum rate of photosynthetic electron transport (J max) increased significantly with tree height (Figures 2C and 2D). No
interspecific differences in Vcmax or J max with tree height were
observed (ANCOVA; P > 0.05), except for DG where these parameters hardly changed with height. However, when gap
seedlings of DG were excluded from the regression, both Vcmax
and J max of DG increased significantly with tree height
(P < 0.05). A positive correlation between Vcmax and J max was
observed both within and across species (data not shown). The
slope of the regression line of J max versus Vcmax varied from
1.37 (SB) to 1.77 (DA), with r 2 varying from 0.50 to 0.81.
Leaf morphological and biochemical properties and tree
height
Leaf blade thickness and LMA increased significantly with
tree height (Figures 3A and 3B). Interspecific differences were
found between SA and the other species. Of the species studied, SA had the thickest leaf blade and highest LMA
(ANCOVA; P < 0.05). The thickness of the palisade layer and
Ames /Aa—both indicators of the degree of development of leaf
mesophyll structure—increased with tree height, and no inter-
Statistical analysis
Scatter plots of leaf morphological and physiological properties with tree height were analyzed by linear regression. Differences between leaf properties of species were tested by
analysis of covariance (ANCOVA; SPSS v.11.5), with species
as the main factor and tree height as a covariable (Sokal and
Rohlf 1995, Rijkers et al. 2000).
Results
Relationship between canopy openness and tree height
Canopy openness varied from 5–10% in the understory to
more than 90% at 40 m aboveground. Canopy openness increased roughly linearly with tree height up to 30 m, then increased more rapidly to 90% at 40 m (Figure 1). In gaps,
canopy openness was about 20%, and direct sunlight usually
reached the leaves. On sunny days, irradiances were around
5 to 20 µmol m – 2 s –1 in the forest understory and at least
1800 µmol m – 2 s –1 in the canopy layer.
Figure 1. Relationship between tree height and canopy openness. The
regression line is: y = –42.8 + 18.9 lnx; r 2 = 0.88, P < 0.001. Symbols:
zz = Dipterocarpus globosus; 䉫 = Dryobalanops aromatica; 䊊 =
Shorea acuta; ⵧ = Shorea beccariana; and 䉭 = Shorea macroptera.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
868
KENZO ET AL.
Figure 2. Relationships between tree height and:
light-saturated photosynthetic
rate (Amax; A); the light compensation point (I c; B); maximum rate of carboxylation
(Vcmax; C); and the maximum
rate of photosynthetic electron
transport (J max; D). Values are
means for each individual
across all replicate leaves. The
regression lines are: A, y =
4.69 + 0.16x; r 2 = 0.66, P <
0.001; B, y = 7.34 + 0.57x;
r 2 = 0.74, P < 0.001; C, y =
31.48 + 0.90x; r 2 = 0.39, P <
0.001; and D, y = 46.1 +
1.79x; r 2 = 0.47, P < 0.001.
Symbols: = = Dipterocarpus
globosus; 䉫 = Dryobalanops
aromatica; 䊊 = Shorea acuta;
ⵧ = Shorea beccariana; and
䉭 = Shorea macroptera.
specific differences were identified (Figures 3C and 3D). Leaf
density (LMA/leaf blade thickness) increased significantly
with tree height in all species (Figure 3E), with interspecific
differences only between DA and DG (ANCOVA; P < 0.05).
The relationship between area-based nitrogen concentration
(N area) and tree height was similar to the other traits and no significant interspecific difference was found (Figure 4A). Although area-based chlorophyll concentration did not vary with
tree height (data not shown), mass-based chlorophyll concentrationtent (Chlmass; Figure 4B) and the chlorophyll to nitrogen ratio (Chl/N ratio; Figure 4C) decreased with tree
height in all species, with no interspecific differences identified. However, Chlmass and the Chl/N ratio differed between
gap seedlings and seedlings beneath the closed canopy.
Relationship between light compensation point and leaf
characteristics
Negative correlations were found between I c and Chlmass (Figure 6A), and between I c and Chl/N (Figure 6B). There were
interspecific differences between I c and Chlmass. Two groups
could be distinguished: between DA, DG and SA, SB and SM
(ANCOVA; P < 0.05). The only interspecific difference in the
relationship between I c and Chl/N was between DG and SM
(ANCOVA; P < 0.05).
Discussion
Relationship between Amax and leaf characteristics
Changes in photosynthetic capacity and light compensation
point with tree height
Significant correlations were found between Amax and LMA
(Figure 5A; r 2 = 0.63, P < 0.001) and between Amax and N area
(Figure 5B; r 2 = 0.57, P < 0.001). Interspecific differences
were found between SB and the other species (ANCOVA;
P < 0.05). For all species, the highest correlation coefficients
were between Amax and properties of leaf mesophyll structures,
such as the thickness of the palisade cell layer (Figure 5C; r 2 =
0.76, P < 0.001) and Ames /Aa (Figure 5D; r 2 = 0.72, P < 0.001)
and no interspecific differences were found.
Photosynthetic capacity was not limited by tree height in the
studied tropical canopy tree species, supporting our hypothesis. For the five dipterocarp species studied, Amax had a simple
relationship with tree height (Figure 2A). Rijkers et al. (2000)
also found a significant relationship between Amax and tree
height in four neotropical species. The slope and intercept of
their linear regression line (0.16 and 4.08, respectively) corresponded closely with the values of 0.16 and 4.69 that we obtained. These findings may be important when developing
TREE PHYSIOLOGY VOLUME 26, 2006
VERTICAL CHANGES IN PHOTOSYNTHESIS IN TROPICAL TREES
869
Figure 3. Relationships between tree height and: leaf
thickness (A); leaf mass per
area (LMA; B); palisade layer
thickness (C); mesophyll cell
surface area per unit leaf area
(Ames /Aa; D); and leaf density
(E). Values are means for each
individual across all replicate
leaves. The regression lines
are: A, y = 206 + 4.76x; r 2 =
0.69, P < 0.001; B, y = 69.7 +
2.76x; r 2 = 0.84, P < 0.001; C,
y = 38.3 + 1.97x; r 2 = 0.83,
P < 0.001; D, y = 20.1 + 1.05x;
r 2 = 0.86, P < 0.001; and E,
y = 0.34 + 0.003x; r 2 = 0.53,
P < 0.001. Symbols: =
Dipterocarpus globosus; 䉫 =
Dryobalanops aromatica; 䊊 =
Shorea acuta; ⵧ = Shorea
beccariana; and 䉭 = Shorea
macroptera.
models for CO2 fixation in tropical forests, although further
studies are needed in diverse tropical forests.
The photosynthetic parameters Vcmax and J max increased significantly with tree height, as well as with Amax (Figures 2C
and 2D), indicating that leaves exposed to high irradiances
have high rates of carboxylation and electron transport capacity per unit area. Wullschleger (1993), who reviewed the
ranges of values of Vcmax and J max in tropical forest species (n =
22), based mostly on wild plants and experimental plants
growing in natural conditions or greenhouses, quoted values of
9–126 (for Vcmax) and 30–222 (for J max). Variations in Vcmax
and J max in our study are consistent with these ranges. The
highest values of Vcmax and J max in our study were about twice
the values found in the canopy of neotropical trees (Carswell et
al. 2000), indicating that dipterocarp species have a high photosynthetic capacity over a wide range of irradiances.
At the dimly lit forest floor, I c, although low, seemed
sufficient to maintain positive net gas exchange (Figure 2B).
The I c was below 10 µmol m – 2 s – 1 for most of the non-gap
seedlings we studied. Eschenbach et al. (1998) reported simi-
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
870
KENZO ET AL.
Figure 4. Relationships between tree height and: nitrogen
content per area (N area; A);
chlorophyll content per dry
mass (Chlmass; B); and chlorophyll to nitrogen ratio (Chl/N
ratio; C). Values are means for
each individual across all replicate leaves. The regression
lines are: A, y = 0.045 +
0.0013x; r 2 = 0.74, P < 0.001;
B, y = 3.48 + –0.05x; r 2 =
0.49, P < 0.001; and C, y =
5.4 + –0.06x; r 2 = 0.48, P <
0.001. Symbols: = Dipterocarpus globosus; 䉫 = Dryobalanops aromatica; 䊊 =
Shorea acuta; ⵧ = Shorea beccariana; and 䉭 = Shorea
macroptera.
larly low I c values for 11 woody species in the Malaysian rain
forest, but some pioneer species displayed higher values.
Many authors have reported that PPF beneath the canopy of
tropical rain forests ranges between 5 and 20 µmol m – 2 s – 1
(Pearcy 1983, Chazdon 1988, Barker et al. 1997, Eschenbach
et al. 1998). Thus, the low I c of the non-gap seedlings indicates
that our study species are well suited to the low light conditions beneath the closed canopy of tropical rain forests.
Leaf photosynthetic traits in relation to leaf morphological
and biochemical properties
Differences in photosynthetic characteristics such as Amax and
I c with tree height were closely related to leaf morphological
and biochemical traits. It is well known that Amax is strongly affected by various leaf characteristics, such as leaf thickness
(MacClendon 1962, Koike 1988), leaf mesophyll structure
(Ames /Aa; Nobel 1975, Koike 1988, Hanba et al. 1999, Kenzo et
al. 2004) and nitrogen content (Field and Moony 1986, Evans
1989, Reich et al. 1999). Generally, age- and size-dependent
declines in leaf nitrogen concentration seem to be reflected in
a reduction in Amax in tall trees (Bond 2000, Niinemets 2002);
however, we found that leaf nitrogen concentration increased
with tree height in these tropical canopy species. Although
high LMA may also limit Amax (Terashima et al. 2001,
Niinemets 2002), dipterocarp canopy trees have a well-developed leaf mesophyll structure, including a thick palisade layer
and high Ames /Aa, which is responsible for reduced leaf internal
resistance to CO2 diffusion, as well as a high LMA (Hanba et
al. 1999, Kenzo et al. 2004). Our results suggest that high leaf
nitrogen concentration and a well-developed mesophyll structure helps maintain high Amax in the upper-canopy leaves.
High foliar chlorophyll concentration (Chlmass) and Chl/N
ratio leaves were related to low I c, permitting better acclimation under poor light at the sapling stage (Figures 4B and 4C).
There was a negative correlation between Chlmass and I c (Figure 6A), indicating that high Chlmass contributes to light-harvesting efficiency at low irradiances (Lambers at al. 1998). In
the model of Hikosaka and Terashima (1995), increased allocation of leaf nitrogen to chlorophyll-protein complexes under shade increases the efficiency of incident light capture
(Björkman 1981). The Chl/N ratio therefore acts as an indicator of the allocation of leaf nitrogen to chlorophyll-protein
complexes of the light-harvesting component (Kimura et al.
1998, Kull and Niinemets 1998, Koike et al. 2001). In our
study, the Chl/N ratio of all species increased with decreasing
tree height (Figure 4C), and the ratio was negatively correlated
with I c (Figure 6B). These findings support the model of
Hikosaka and Terashima (1995) and suggest that the study
TREE PHYSIOLOGY VOLUME 26, 2006
VERTICAL CHANGES IN PHOTOSYNTHESIS IN TROPICAL TREES
871
Figure 5. Light-saturated photosynthetic rate (Amax) versus:
leaf mass per area (LMA; A);
nitrogen content per area
(N area; B); palisade layer thickness (C); and mesophyll cell
surface area per unit leaf area
(Ames /Aa; D). Values are means
for each individual across all
replicate leaves. The regression lines are: A, y = 1.11 +
0.05x; r 2 = 0.63, P < 0.001; B,
y = 0.67 + 102.9x; r 2 = 0.57,
P < 0.001; C, y = 1.67 + 0.08x;
r 2 = 0.76, P < 0.001; and D,
y = 1.85 + 0.15x; r 2 = 0.72, P
< 0.001. Symbols: = Dipterocarpus globosus; 䉫 =
Dryobalanops aromatica; 䊊 =
Shorea acuta; ⵧ = Shorea beccariana; and 䉭 = Shorea macroptera.
species are able to change their light-harvesting component,
allowing ready adaptation of photosynthetic capacity to the
variable light conditions encountered by seedlings in gaps and
beneath the closed canopy.
In conclusion, our results suggest that Amax is not limited by
tree height in tropical canopy tree species. We found simple
and significant linear relationships between tree height and
both leaf photosynthetic characteristics (e.g., Amax, I c, J max
and Vcmax) and leaf morphological and biochemical traits
(e.g., LMA, N area, Chlmass, Chl/N ratio), which in turn affect
photosynthetic traits, with some differences among the
dipterocarp species studied. These relationships, involving
leaf properties of forest understory seedlings up to mature canopy trees, may allow more accurate modeling of CO2 flux and
biomass production in tropical rain forests than hitherto. We
also obtained evidence that dipterocarp species can optimize
leaf anatomy and physiology to make the best use of the variable light encountered from the seedling stage to adulthood.
Figure 6. Light compensation
point (I c) versus: chlorophyll
content per unit dry mass
(Chlmass; A); and chlorophyll
to nitrogen ratio (Chl/N ratio;
B). The regression lines are:
A, y = 35.5 + –6.98x; r 2 =
0.51, P < 0.001; and B, y =
39.3 + –5.06x; r 2 = 0.43, P <
0.001. Symbols: = Dipterocarpus globosus; 䉫 = Dryobalanops aromatica; 䊊 =
Shorea acuta; ⵧ = Shorea beccariana; and 䉭 = Shorea macroptera.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
872
KENZO ET AL.
Acknowledgments
We are grateful to the Forest Department, Sarawak, and to Prof.
T. Nakashizuka and Mr. M. Yoshimura for their kind support of this
study. We thank Dr. R. Funada and his students for help in making microphotographs. Prof. M. Suzuki, Dr. K. Kuraji and Dr. T. Kumagai
gave us the climate data. We received valuable comments on the
manuscript from Dr. S. Kitaoka and Dr. T. Hiromi. This research was
partly supported by a grant from the Core Research for Environmental
Science and Technology program of the Japan Science and Technology Corporation (JST), by a Grant-in-Aid for Scientific Research
(No. 16310017) from the Ministry of Education, Science and Culture,
Japan, and by the Japan Society for Promotion of Science (JSPS) Research Fellowships for Young Scientists to T.I. and R.Y.
References
Ashton, D.H. and J.S. Turner. 1979. Studies on the light compensation point of Eucalyptus regnans F. Muell. Aust. J. Bot. 27:
589–607.
Barker, M.G., M.C. Press and N.D. Brown. 1997. Photosynthetic
characteristics of dipterocarp seedlings in three tropical rain forest
light environments: a basis for nich partitioning? Oecologia 112:
453–463.
Barnes, J.D., L. Balaguer, E. Manrique, S. Elvira and A.W. Davison.
1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophyll a and b in lichens and higher plants. Environ. Exp. Bot. 32:85–100.
Björkman, O. 1981. Responses to different quantum flux densities. In
Encyclopedia of Plant Physiology I. New Series, Vol. 12A. Eds.
O.L. Lange, P.S. Nobel., C.B. Osmond and H. Ziegler. SpringerVerlag, Berlin, pp 57–107.
Bond, B.J. 2000. Age-related changes in photosynthesis of woody
plants. Trends Plant Sci. 5:349–353.
Chapin, F.S., III, P.A. Matson and H.A. Mooney. 2002. Principles of
terrestrial ecosystem ecology. Springer-Verlag, Berlin, 436 p.
Carswell, F.E., P. Meir, E.V. Wandelli, L.C.M. Bonates, B. Kruijt,
E.M. Barbosa, A.D. Nobre, J. Grace and P.G. Jarvis. 2000. Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol.
20:179–186.
Chazdon, R.L. 1988. Sunflecks and their importance to forest understory plants. Adv. Ecol. Res. 18:1–63.
Chazdon, R.L., R.W. Pearcy, D.W. Lee and N. Fetcher. 1996. Photosynthetic responses of tropical forest plants to contrasting light environments. In Tropical Forest Plant Ecophysiology. Eds. S.S.
Mulkey, R.L. Chazdon and A.P. Smith. Chapman and Hall, New
York, pp 5–55.
Ehleringer, J.R and C.B. Field. 1993. Scaling physiological processes. Leaf to globe. Academic Press, New York, 385 p.
Eschenbach, C., R. Glauner, M. Kleine and L. Kappen. 1998. Photosynthesis rates of selected tree species in lowland dipterocarp rain
forest of Saba, Malaysia. Trees 12:356–365.
Evans, J.R. 1989. Photosynthesis and nitrogen relationships in leaves
of C3 plants. Oecologia 78:9–19.
Farquhar, G.D., von S. Caemmerer and J.A. Berry. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90.
Field, C. and H. Mooney 1986. The photosynthesis–nitrogen relationship in wild plants. In On the Economy of Form and Function. Ed.
T.J. Givnish. Cambridge University Press, Cambridge, pp 25–55.
Fredericksen, T.S., K.C. Steiner, J.M. Skelly, B.J. Joyce, T.E. Kolb,
K.B. Kouterick and J.R. Ferdinand. 1996. Diel and seasonal patterns of leaf gas exchange and xylem water potentials of different-sized Prunus serotina Ehrh. trees. For. Sci. 42:359–365.
Hanba, Y.T., S. Miyazawa and I. Terashima. 1999. The influence of
leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese
warm-temperate forests. Funct. Ecol. 13:632–639.
Harley, P.C. and T.D. Sharkey. 1991. An improved model of C3 photosynthesis at high CO2: Reversed O2 sensitively explained by lack
of glycerate re-entry into the chloroplast. Photosynth. Res. 27:
169–178.
Harley, P.C., R.B. Thomas, J.F. Reynolds and B.R. Strain. 1992. Modeling photosynthesis of cotton in elevated CO2. Plant Cell Environ.
15:271–282.
Hikosaka, K. and I. Terashima. 1995. A model of the acclimation of
photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ. 18:605–618.
Hiromi, H., I. Ninomiya, T. Koike and K. Ogino. 1999. Stomatal regulation of canopy trees in a tropical rain forest. Jpn. J. Ecol. 49:
68–76. In Japanese with English summary.
Ishida, A., T. Toma, Y. Matsumoto, S.K. Yap and Y. Maruyama. 1996.
Diurnal changes in leaf gas exchange characteristics in the uppermost canopy of a rain forest tree, Dryobalanops aromatica Gaertn.
f. Tree Physiol. 16:779–785.
Itoh, A., T. Yamakura, K. Ogino, H.S. Lee and P.S. Ashton. 1995.
Population structure and canopy dominance of two emergent dipterocarp species in a tropical rain forest of Sarawak, East Malaysia.
Tropics 4:133–141.
Kato, M., T. Inoue, A.A. Hamid, T. Nagamitsu, M.B. Merdek,
A.R. Nona, T. Itino, S. Yamane and T. Yumoto. 1995. Seasonality
and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Res. Popul. Ecol. 37:59–79.
Kenzo, T. T, Ichie, I. Ninomiya and T. Koike. 2003. Photosynthetic
activity in seed wings of Dipterocarpaceae in a masting year: does
wing photosynthesis contribute to reproduction? Photosynthetica
41:551–557.
Kenzo, T. T, Ichie, R. Yoneda, Y. Kitahashi, Y. Watanabe, I. Ninomiya
and T. Koike. 2004. Interspecific variation of photosynthesis and
leaf characteristics in five canopy trees of Dipterocarpaceae in a
tropical rain forest. Tree Physiol. 24:1187–1192.
Kimmins. J.P. 1997. Forest ecology. A foundation for sustainable
management. 2nd Edn. Prentice Hall, Upper Saddle River, NJ,
596 p.
Kimura, K., A. Ishida, A. Uemura, Y. Matsumoto and I. Terashima.
1998. Effect of current-year and previous-year PPFDs on shoot
gross morphology and leaf properties in Fagus japonica. Tree
Physiol. 18:459–466.
Kitin, P., R. Funada, Y. Sano, H. Beeckman and J. Ohtani. 1999. Variations in the lengths of fusiform cambial cells and vessel elements
in Kalopanax pixtus. Ann. Bot. 84:621–632.
Koch, G.W., S.C. Sillett, G.M. Jennings and S.D. Davis. 2004. The
limits to tree height. Nature 428:851–854.
Koike, T. 1988. Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant
Species Biol. 3:77–87.
Koike, T., M. Kitao, Y. Maruyama, S. Mori and T.T. Lei. 2001. Leaf
morphology and photosynthetic adjustments among deciduous
broad-leaved trees within the vertical canopy profiles. Tree
Physiol. 21:951–958.
Körner, C. 1994. Scaling from species to vegetation: the usefulness of
functional groups. In Biodiversity and Ecosystem Function.
Eds. E.-D. Schulze and H.A. Mooney. Springer-Verlag, Berlin,
pp 117–140.
Kumagai, T., T.M. Saitoh, Y. Sato, T. Morooka, O.J. Manfroi, K. Kuraji and M. Suzuki. 2004. Transpiration, canopy conductance and
the decoupling coefficient of a lowland mixed dipterocarp forest in
Sarawak, Borneo: dry spell effects. J. Hydrol. 287:237–251.
TREE PHYSIOLOGY VOLUME 26, 2006
VERTICAL CHANGES IN PHOTOSYNTHESIS IN TROPICAL TREES
Kull, O. and Ü. Niinemets. 1998. Distribution of leaf photosynthetic
properties in tree canopies: comparison of species with different
shade tolerance. Funct. Ecol. 12:472–479.
Lambers, H., F.S. Chapin, III, and T.L Pons. 1998. Plant physiological
ecology. Springer-Verlag, New York, 540 p.
Larcher, W. 2003. Physiological plant ecology. 4th Edn. SpringerVerlag, New York, 513 p.
Lee, H.S., P.S. Ashton, T. Yamakura, S. Tan, S.J. Davies, A. Itho,
E.O.K. Chai, T. Ohkubo and J.V. LaFrankie. 2002. The 52-hectare
forest research plot at Lambir Hills, Sarawak, Malaysia: tree distribution maps, diameter tables and species documentation. Forest
Department Sarawak, The Arnold Arboretum-CTFS Asia Program
and The Smithsonian Tropical Research Institute, Lee Miing Press,
Kuching, 621 p.
MacClendon, J.H. 1962. The relationship between the thickness of
deciduous leaves and their maximum photosynthetic rate. Am.
J. Bot. 49:320–322.
Niinemets, Ü. 2002. Stomatal conductance alone does not explain the
decline in foliar photosynthetic rate with increasing tree age and
size in Picea abies and Pinus sylvestris. Tree Physiol. 22:515–535.
Nobel, P.S. 1975. Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves
of Plectranthus parviflorus Henckel. Plant Physiol. 55:1067–1070
Nobel, P.S. 1999. Plant physiology 2nd. Edn. Academic Press, New
York, 474 p.
Ozanne, C.M.P., D. Anhuf, S.L. Boulter et al. 2003. Biodiversity
meets the atmosphere: a global view of forest canopies. Science
301:183–186.
Pearcy, R.W. 1983. The light environment and growth of C3 and C4
tree species in the understory of a Hawaian forest. Oecologia 58:
19–25.
Reich, P.B., D.S. Ellsworth, M.B. Walters, J.M. Vose, C. Gresham,
J.C. Volin and W.D. Bowman. 1999. Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969.
Rijkers, T., T.L. Pons and F. Bongers. 2000. The effect of tree height
and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct. Ecol. 14:77–86.
873
Sakai, S., T. Nakashizuka, T. Ichie, M. Nomura and L. Chong. 2002.
Lambir hills canopy crane, Malaysia. In The Global Canopy Handbook. Eds. A.W. Mitchell, K. Secoy and T. Jackson. Global Canopy Programme, Oxford, U.K., pp 77–79.
Sharkey, T.D. 1985. Photosynthesis in intact leaves of C3 plants:
physics, physiology and late limitations. Bot. Rev. 51:53–105.
Shinano, T., T. Lei., T. Kawamukai, M. Inoue, T. Koike and T. Tadano. 1996. Dimethyl sulfoxide method for the extraction of chlorophylls a and b from the leaves of wheat, field bean, dwarf
bamboo, and oak. Photosynthetica 32: 404–415.
Sokal, R.R. and F.J. Rohlf. 1995. Biometry. The principles and practice of statistics in biological research. 3rd Edn. W. H. Freeman,
New York, 887 p.
Sobrado, M.A. and E. Medina. 1980. General morphology, anatomical structure, and nutrient content of sclerophyllous leaves of the
‘Bana’ vegetation of Amazonas. Oecologia 45:341–345.
Terashima, I., S. Miyazawa and T.Y. Hanba. 2001. Why are sun leaves
thicker than shade leaves? Consideration based on analyses of CO2
diffusion in the leaf. J. Plant Res. 114:93–105.
Thomas, S.C. and W.E. Winner. 2002. Photosynthetic differences between saplings and adult trees: an integration of field results by
meta-analysis. Tree Physiol. 22:117–127.
Whitmore, T.C. 1998. An introduction to tropical rain forests. 2nd
Edn. Oxford University Press, Oxford, U.K., 282 p.
Wullschleger, S.D. 1993. Biochemical limitation to carbon assimilation in C3 plants—a retrospective analysis of the A/C i curves from
109 species. J. Exp. Bot. 44:907–920.
Yamamoto, S. 2000. Estimation of the canopy-gap size using two
photographs taken at different heights. Ecol. Res. 15:203–208.
Yoda, K. 1978. Three-dimensional distribution of light intensity in a
tropical rain forest of West Malaysia. Malay. Nat. J. 30:161–177.
Yoder, B.J., M.G. Ryan, R.H. Waring, A.W. Schoettle and M.R. Kaufmann. 1994. Evidence of reduced photosynthetic rates in old trees.
For. Sci. 40:513–527.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com