Agricultural and Forest Meteorology 134 (2005) 3959

www.elsevier.com/locate/agrformet

Photosynthetic and structural characteristics of canopy and shrub

trees in a cool-temperate deciduous broadleaved forest:
Implication to the ecosystem carbon gain
Hiroyuki Muraoka *, Hiroshi Koizumi
Institute for Basin Ecosystem Studies, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan
Received 6 April 2004; accepted 4 August 2005

Abstract
To reveal the seasonal change of leaf ecophysiological and canopy characteristics and to evaluate the functional role of canopy
and shrub tree species in forest CO2 uptake, we measured forest canopy leaf area index (LAI) using a hemispherical canopy
photography technique, leaf CO2 gas exchange and shoot architecture for canopy (Betula ermanii and Quercus crispula) and shrub
(Hydrangea paniculata and Viburnum furcatum) tree species in a deciduous broadleaved forest in a cool-temperate region in central
Japan. Canopy LAI and photosynthetic capacity of canopy tree leaves increased rapidly with leaf expansion. LAI reached its
maximum in early summer but photosynthetic capacity reached its maximum in late summer. Development of photosynthetic
capacity was dependent on the changes of leaf mass per area and leaf chlorophyll content (evaluated by SPAD). The seasonal
maximum photosynthetic capacity of the leaves at the forest canopy top (B. ermanii and sun leaves of Q. crispula) was about more
than double of the leaves in the shrub layer (H. paniculata, shade leaves of Q. crispula and V. furcatum). Light interception and
photosynthetic carbon gain at a shoot level were simulated under three air temperature conditions by a three-dimensional canopy
photosynthesis model (Y-plant) involving the combined leaf photosynthesis and stomatal conductance responses and shoot
architecture. Results showed that (1) calculations without considering the heterogeneous light distribution in a foliage made by
geometrical feature of plants would overestimate the photosynthetic carbon gain by +40% even at the canopy surface, and (2) the
steep leaf angle in B. ermanii avoided midday depression of photosynthesis while the rather horizontal leaves in Q. crispula received
excess light and heat load which led larger midday depression of photosynthesis. In addition to the large capacity of photosynthetic
productivity of the canopy top foliage, our model also suggests the functional role of shrub species in forest ecosystem carbon gain,
due to their high photosynthetic utilization efficiency of low light incidence available in the forest understory.
# 2005 Elsevier B.V. All rights reserved.
Keywords: AsiaFlux network; Cool-temperate deciduous forest; Leaf area index; Photosynthesis; Phenology; Shoot architecture; Takayama
Experimental Forest

1. Introduction
The net carbon gain of a terrestrial ecosystem is
composed from complex consequences of leaf area,

* Corresponding author. Tel.: +81 58 293 2064;

fax: +81 58 293 2062.
E-mail address: muraoka@green.gifu-u.ac.jp (H. Muraoka).
0168-1923/$ see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.agrformet.2005.08.013

carbon dioxide (CO2) exchange capacity and activity of

photosynthetic (leaves) and non-photosynthetic (stems
and roots) organs, canopy architecture, stand biomass of
plant species involved, and meteorological conditions
including light incidence, air temperature, air humidity,
wind speed and air CO2 concentration (Ehleringer and
Field, 1993; Baldocchi and Meyers, 1998; Baldocchi
and Wilson, 2001; Baldocchi et al., 2002). As well as
these instantaneous consequences of plants and their

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

environments, spatial and temporal variations of both

biotic and abiotic factors throughout the growing season
control the ecosystem behavior. Due to these multiple
relationships of factors governing the ecosystem
function, the ecophysiological mechanisms underlying
the functional role of the vegetation are always
fundamental knowledge since they provide mechanistic
explanations and/or parameters to the meteorological
observation, satellite remote sensing and modeling
prediction of the ecosystem carbon cycling which
enable us to evaluate larger scale behavior of the
ecosystems (Ehleringer and Field, 1993; Baldocchi and
Meyers, 1998; Wilson et al., 2001). The overall
objective of this study is to reveal the seasonal change
(phenology) of foliage properties of canopy tree species
and to evaluate the functional role of canopy and shrub
species in ecosystem CO2 uptake in a cool-temperature
deciduous broadleaved forest in central Japan. Investigations were made for canopy leaf area, single leaf gas
exchange and photosynthetic productivity at a shoot
scale. The investigated forest, whose canopy is
dominated by birch and oak and has several shrub tree
species in its understory, has been a research forest for
AsiaFlux network study, and meteorological CO2 flux
observation (Yamamoto et al., 1999; Saigusa et al.,
2002; Murayama et al., 2003) and ecological observations such as tree biomass accumulation (Ohtsuka et al.,
in press) and soil respiration (Lee et al., 2003; Mo et al.,
2006) have been conducted since 1993. Considering the
fact that an ecosystem behavior is the integration of
individual leaves, shoots, plants and species composing
the ecosystem, revealing small scale ecophysiological
behavior created by leaf photosynthesis and shoot level
properties in the present study (started in 2003) would
provide us basic but important characteristics of part of
the ecosystem, which are necessary to estimate or
analyze the whole ecosystem CO2 flux by scaling
techniques (e.g., process-based models, eddy covariance and satellite remote sensing).
Deciduous forest ecosystems in cool-temperate
region can be characterized by the rapid temporal
change of leaf biomass and gas exchange characteristics
(photosynthesis and respiration) of the plant species
composing the forest. Among the ecological parameters
that describe the potential of carbon fixation at the
ecosystem scale, leaf area index (LAI) has been the
central one and measurements of its seasonality have
been conducted intensively (e.g., Gond et al., 1999;
Wythers et al., 2003; Jonckheere et al., 2004). However,
as the expansion of leaf area tends to cease earlier than
the maturation of leaf photosynthetic capacity (Miyazawa et al., 1998), evaluation of carbon budget without

considering the seasonality of leaf photosynthetic

capacity would lead to a considerable overestimation
of carbon fixation (Wilson et al., 2000; Morecroft et al.,
2003). Therefore, ecophysiological observation at the
single leaf scale, in addition to the spatial and seasonal
distribution of biomass, is required for understanding
the consequences between ecological characteristics
and the photosynthetic productivity of a given
ecosystem (e.g., Reich et al., 1991; Wilson et al.,
2000, 2001; Muraoka et al., 2002; Kosugi et al., 2003).
Among the ecophysiological parameters, those for the
leaf photosynthesis model (Farquhar et al., 1980) and
stomatal conductance model (Ball et al., 1987; Leuning,
1995) are useful because they provide mechanistic
model to predict leaf photosynthetic activity, involving
the interactive effects of light, temperature and
humidity on photosynthetic and stomatal responses
that cannot be ignored in natural environment especially
under open sky, sunlit conditions (Harley and Baldocchi, 1995; Beyschlag and Ryel, 1999; Xu and
Baldocchi, 2003).
Photosynthetic carbon gain of a plant does not
depend only on the single leaf photosynthetic characteristics, but also on the architectural (geometrical)
characteristics of shoots (branch), which is an
aggregation of the leaves (Pearcy and Valladares,
1999; Valladares, 1999). A model estimation of leaf
photosynthesis at any level of organ (single leaf, shoot,
branch and stand) without considering the plant
structural (geometrical) characteristics would mislead
our understanding of canopy photosynthesis via over- or
underestimation of light interception. Recent canopy
photosynthesis models emphasize the importance of
leaf area and angle distribution within a canopy, since
they affect the light interception of the leaves and
penetration into the canopy (Caldwell et al., 1986;
Anten, 1997; de Pury and Farquhar, 1997; Raulier et al.,
1999). In addition, leaf orientation affects the photosynthetic activity in midday hours under sunny open sky
via the interactive effects of incident light, temperature
and vapor pressure deficit on stomatal and photosynthetic responses (Muraoka et al., 1998; Ishida et al.,
1999; Valladares and Pearcy, 1999; Werner et al., 2001).
Species-specific shoot architectural characteristics
would play a significant role in ecosystem behavior
in a case that a given forest canopy is composed by some
species having similar photosynthetic capacity but
different leaf orientation. The forest canopy of our study
site is composed of birch (Betula platyphylla Sukatchev
var. japonica Hara and Betula ermanii Cham) and oak
(Quercus crispula Blume). These species have different
leaf orientations at their canopy top; leaves of birch are

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

41

2. Materials and methods

reaches to the shrub layer in the forest. All these

deciduous tree species flush their leaves after snowmelt,
while second flush (in early summer) can be found in
birch with smaller leaf area than the first one.
In the experimental forest, a canopy access tower
(10 m
10 m
18 m height) was established in winter
of 2001 to access the foliage of dominant canopy trees;
three B. ermanii (ca. 1720 m tall) and two Q. crispula
(1215 m). Leaf gas exchange and shoot architectural
measurements were conducted for several shoots of
these canopy species throughout the growing season
from late May to late October 2003. Photosynthetically
active photon flux density (PPFD, 400700 nm) around
the canopy tower was measured continuously above
(20 m above the ground) and within (15, 10 and 2 m) the
forest canopy with quantum sensors (PAR-01L, Prede
Co. Ltd., Japan, and IKS-27, Koito Industry Co. Ltd.,
Japan). Air temperature and relative humidity were also
measured throughout the growing season by a platinum
thermometer and a relative humidity sensor (HMP-45,
Vaisala, Finland). All sensors were connected to a datalogger (Thermodac-EF, Eto-Denki Co. Ltd., Japan) and
the readings were recorded at 5 min intervals.

2.1. Study site and plant species

2.2. Evaluation of forest canopy leaf area index

Field study was taken in a cool-temperate deciduous

broadleaved forest (368080 N, 1378250 E, 1420 m asl) on
the north-western slope of Mt. Norikura, Japan. In this
forest, a 1-ha study plot is situated as the Takayama
Experimental Forest of Institute for Basin Ecosystem
Studies, Gifu University. Annual mean air temperature
and precipitation from 1980 to 2002 measured at the
field station (500 m apart from the study site) are 7.2 8C
and 2275 mm, respectively. The forest canopy is
dominated by Q. crispula Blume, B. platyphylla
Sukatchev var. japonica Hara and B. ermanii Cham.,
and sub-canopy and shrub layers are dominated by Acer
rufinerve Sieb. et Zucc., Acer distylum Sieb. et Zucc.,
Hydrangea paniculata Sieb and Viburnum furcatum
Blume ex Maxim. (Ohtsuka et al., in press). The
understory is dominated by an evergreen dwarf bamboo
Sasa senanensis (Fr. Et Sav.) Rehder. Part of understory
without S. senanensis are dominated by seedlings of Q.
crispula, A. distylum, A. rufinerve, H. paniculata, V.
furcatum and some perennial herbaceous species. B.
ermanii, Q. crispula, H. paniculata and V. furcatum
were selected for the material species due to their
representativeness of this forest. B. ermanii is a pioneer
species and has thin crown in the present multi-species
deciduous forest, while Q. crispula is a late-successional species and has multi-layered crown which often

Forest canopy leaf area index (LAI) was estimated

using hemispherical canopy photographs taken in the
forest understory (2 m above the ground) at 14 locations
covering the 1-ha plot. Photographs were taken by a
digital camera (CoolPix 910, Nikon, Japan) equipped
with a fish-eye lens (FC-E8, Nikon, Japan) mounted on
a monopod. The camera was carefully leveled by
referring to a bubble level. A thin wire was used to
indicate south on the photographs. All photographs
were taken while the skies were overcast in midday or in
late afternoon. The photographs were analyzed with a
commercially available software program, HemiView
2.1 (Delta-T Devices, UK). Gap fraction was determined for 160 specific sky sectors on the photographs
and sectors within 308 from the zenith were used for the
estimation of LAI. Data analyses for thus selected area
avoided the influence of trunk shadow and surrounding
understory vegetation on upper slope of the observation
points, which cover a significant area of the photographs. We did not calibrate thus estimated LAI using
the branch area (which can be recognized before canopy
leaf expansion). Therefore, our value can be called as
plant area index or vegetation area index (reviewed by
Jonckheere et al., 2004).
In addition to this LAI estimation, we measured the
growth of individual leaf area for the canopy species.

largely inclined downwards while leaves of oak are

rather horizontal or slightly inclined. The geometrical
feature would affect the estimated photosynthetic CO2
uptake when one scales from single leaf gas exchange
characteristics to foliage, since leaf orientation and leaf
overlap (self-shading) affect the light interception of
each leaf remarkably. In this study, we tested the effect
of shoot architecture on the carbon gain by using a
three-dimensional canopy photosynthesis model Yplant (Pearcy and Yang, 1996). Although this model
does not treat ecosystem scale but a single leaf and
shoot scale, the plantenvironment consequences at
these scale would show us important plant ecophysiological functions of the species in a given ecosystem.
The objectives of this study are: (1) to reveal the
seasonal properties of leaf gas exchange characteristics
and LAI of canopy tree species, and (2) to examine the
possible effects of shoot architecture on the estimation
of light interception and photosynthesis in canopy and
shrub species in mid summer, in a cool-temperate
deciduous broadleaved forest in central Japan.

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

Leaf length of three branches (each has 2030 leaves)

for the canopy top of B. ermanii and Q. crispula, and for
inner-canopy of Q. crispula were measured periodically
from leaf emergence to mid summer.
3. Measurements of leaf gas exchange
Gas exchange measurements were conducted intensively for sunlit leaves of the canopy species (B. ermanii
and Q. crispula) due to their great responsiveness to the
potential carbon gain of the forest, while leaves of innercanopy were also investigated for Q. crispula having
multi-layer canopy. In mid summer, measurements
were also conducted for the dominant shrub species (H.
paniculata and V. furcatum) to examine their photosynthetic productivity.
Relationship between net photosynthetic rate (A) and
leaf intercellular CO2 concentration (Ci), and dark
respiration rate (R) were measured to obtain the leaf
gas exchange characteristics. Measurements for the
canopy species were taken in about 2 week intervals but
once in mid summer for the shrub species, using a
portable photosynthesis measuring system (LI-6400, LiCor, Inc., USA). Measurements were conducted for the
intact three to seven leaves, but due to frequent rain,
measurements in mid June for B. ermanii and in late
October for B. ermanii and Q. crispula leaves were taken
for shoots cut under water and taken to the laboratory
within 10 min. Care was taken for the cut shoots to
experience in situ temperature by well ventilation of the
laboratory during the measurements, and data were used
for further analyses if the stomatal conductance for water
vapor (gsw) reached the level of in situ measurements
considering the possibility of water stress effect on A due
to cutting. The ACi curves were obtained under constant
PPFD, air temperature and leaf to air vapor pressure
deficit (VPD, <1 kPa), and the CO2 concentration
entering the leaf chamber (Ca) was changed from 0,
100, 200, 300, 370, 600, 800 and 1000 mmol CO2 mol1
air. About 23 min were taken to obtain the readings at
each Ca. R was measured under the same air temperature
and VPD conditions with ACi curves but under Ca of
370 mmol mol1. Measurements at the canopy top were
taken in morning hours (08:0012:00 h) to avoid possible
effects of photo-inhibition, heat load and water stress.
Material branches and LI-6400 were covered by shade
cloth to avoid direct irradiance. PPFD (provided by RedBlue LED of LI-6400) and air temperature for the ACi
measurements were changed seasonally by considering
the leaf phenology (i.e., degree of maturation of
photosynthetic capacity to avoid photo-inhibition and
rising leaf temperature). For the leaves of B. ermanii and

leaves at the canopy top (sun leaves) of Q. crispula

(both at about 15 m above the ground), PPFD of
was
given
in
May,
800 mmol m2 s1
1000 mmol m2 s1 in June, 1200 mmol m2 s1 in July
and 1500 mmol m2 s1 afterwards. For the innercanopy leaves (shade leaves) of Q. crispula (at about
7 m above the ground), PPFD of 800 mmol m2 s1 was
given in May and June and 1000 mmol m2 s1 afterwards. Air temperature of the leaf chamber was adjusted
to mean daytime air temperature of about 1 week before
each measurement day. Immediately after the gas
exchange measurements, index of leaf chlorophyll
content (SPAD) was measured (SPAD-502, Minolta,
Japan; Markwell et al., 1995), and the leaves were
collected to obtain leaf mass per area (LMA) for which
leaf area was measured with a leaf area meter (LI-3100,
Li-Cor, Inc., USA) and weighed after drying at 80 8C for
48 h. These measurements were taken on the same
branch or branches at similar heights of each species
throughout the season. Gas exchange measurements for
leaves of shrub species were taken in branches at 2 m
above the ground, while the tree height was 2.53 m.
Light availability of the shade shoots of Q. crispula and
material branches of shrub species were evaluated by
hemispherical canopy photographs taken under diffuse
light conditions. Indirect site factor (ISF), which is
proportional to the diffuse light transmittance, was
calculated by using HemiView 2.1 software.
Using thus obtained gas exchange data, maximum
carboxylation rate (Vcmax) and maximum electron
transport rate (Jmax) were calculated by using the
equations by Lambers et al. (1998) and Xu and Baldocchi
(2003). Vcmax was calculated using the data of
RuBP (ribulose bisphosphate) saturated range
(Ci < 300 mmol mol1), while Jmax was calculated using
the data of RuBP regeneration limited range (Ci of 540
900 mmol mol1 depending on the sample leaves). In
these calculations, day (non-photorespiratory) respiration (Rd) was assumed to be 40% of R considering the
light inhibition of mitochondrial respiration (Apel and
Peisker, 1995; Viller et al., 1995). CO2 compensation
point (G *) was calculated by a linear regression between
Ci and [A + Rd] at a range of low Ci (<200 mmol mol1).
Thus calculated Vcmax and Jmax were converted to the
values at 25 8C using the temperature dependence
equations (Lambers et al., 1998).
3.1. Measurements of shoot architecture and
photosynthesis modeling
Light capture and photosynthesis at the shoot scale
of the forest canopy species (B. ermanii and sun and

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

shade shoots of Q. crispula) and of the shrubs (H.

paniculata and V. furcatum) were simulated with a
three-dimensional canopy architecture model, Y-plant
(Pearcy and Yang, 1996). Y-plant simulates light
interception and photosynthesis at leaf and shoot levels
to study the interactive effects of leaf ecophysiological
properties and shoot architecture on plant carbon gain
and growth (e.g., Pearcy and Valladares, 1999;
Valladares, 1999; Muraoka et al., 2003; Pearcy et al.,
2005). In this study, we utilized Y-plant to gain an
implication of the possible effects of leaf ecophysiology
and shoot architecture specific to each species on
foliage CO2 fixation in summer (late August), since the
shoot architectural properties (leaf angle, relative
position of the leaves on a shoot and self-shading)
affect the photosynthesis at shoot level considerably and
hence would affect photosynthetic behavior in individual trees. The calculations of light interception and
photosynthesis include the effects of environmental
conditions around the shoots, ecophysiological properties of the leaves specific to species and local light
environment, and the structural characteristics (size,
orientation and position of single leaves and hence
mutual shading of the leaves). Y-plant requires inputs of
the angles, azimuths and length of stems (internodes),
petioles and leaves which construct a shoot. These
structural measurements were made in late August.
Angles and azimuths were measured by a compass
protractor (Norman and Campbell, 1989). Coordinates
for leaf-blade shape were obtained by tracing representative leaves onto graph paper and then recording the
x- and y-coordinates for points on the leaf margins
starting at x = 0 and y = 0 at the point of attachment of
the petiole. The details of the model and architecture
inputs can be found in previous papers (Pearcy and
Yang, 1996, 1998). For Q. crispula, due to its very small
petiole, the petiole length was set at 1.0 mm and the
orientation was assumed to be the same as that of the
leaf midrib. Measurements of shoot geometrical
characteristics were taken for three shoots for each
species.
Calculation of light incidence were performed
assuming open sky for the shoots of B. ermanii and
sun shoots of Q. crispula, while hemispherical
photographs were used for the shade shoots of Q.
crispula and shrubs H. paniculata and V. furcatum. The
measured shoots of B. ermanii and Q. crispula were
rotated in azimuth angle of +908, +1808 and +2708 by
Y-plant to simulate the different azimuth of whole
shoot and treated as replications to examine the
possible range of light interception for the shoots
(i.e., three measured shoots
four azimuth for each

43

species). Hemispherical photographs were taken at

3.5 m height above the ground on September 4 at the 14
locations where forest canopy LAI was estimated. The
shoots of shrub species were not rotated like the canopy
species, but the 14 hemispherical photographs allowed
us to estimate the shoot photosynthetic productivity in a
range of light environment available in the forest. For
the shade shoots of Q. crispula, light interception and
photosynthesis were estimated for rotated 12 shoots
under a hemispherical photograph taken for one of the
measured shoots, and three shoots (not rotated) under
the above 14 hemispherical photographs. These
hemispherical photographs were analyzed with HemiView 2.1 software. The photographs having 160 sky
sections were used to estimate diffuse and direct PPFD
on the individual leaves in Y-plant. We used the
standard overcast sky (SOC) algorithm (Moon and
Spencer, 1942) to calculate the distribution of light over
the sky. In the computation of absorbed PPFD by the
leaves, we assumed a leaf absorptance and transmittance of 0.85 and 0.10, respectively, for all species
studied. The below calculation of photosynthesis is
based on this absorbed PPFD Other detailed explanations for the calculation of light incidence can be found
in Pearcy and Yang (1996).
Y-plant contains photosynthesis (Farquhar et al.,
1980), stomatal conductance for CO2 (gsc) (Leuning,
1995) and leaf energy balance models to calculate the
leaf CO2 gas exchange, stomatal conductance and
transpiration rate by incorporating the interactive
effects of irradiance, temperature and relative
humidity/vapor pressure deficit (Valladares and
Pearcy, 1999). Calculation of photosynthetic rate
requires light-saturated rate of gross photosynthesis
(Agmax), dark respiration (R), apparent quantum yield
(a) and convexity factor (u, set at 0.8) of lightphotosynthetic curve, Vcmax25 and Jmax25. Agmax for
each species (shoots) was given as [light saturated net
photosynthetic rate (Amax) + R] obtained by the ACi
measurements at Ca of 370 mmol mol1, and a for B.
ermanii and Q. crispula was set at 0.05 calculated by
the relationship between PPFD and net photosynthetic
rate (A) obtained from the in situ leaf gas exchange
measurements conducted for the same shoots (T.
Sakai, personal communication), while a of 0.05 was
also given to H. paniculata and V. furcatum assuming
that there is little difference in a between the species
nor local light environment. Stomatal conductance
(gsc) was determined as [gsc = g0 + mA/{(Cs  G *)

(1 + Ds/Do)}] (Leuning, 1995), where Cs is the CO2
concentration at the leaf surface, Ds the leafair vapor
pressure deficit and Do is a constant. The slope (m)

44

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

and g0 for B. ermanii and Q. crispula were obtained

from in situ gas exchange measurements made under
constant Ca of 370 mmol mol1 (data not shown) and
those for H. paniculata and V. furcatum were obtained
from the measurements of ACi relationships, by a
linear regression between observed gsc (=gsw/1.6) and
[A/{(Cs  G *)
(1 + Ds/Do)}]. In addition, we calculated the parameter (slope: a) of the stomatal
conductance model by Ball et al. (1987) as
[gsw = g0 + aAhs/Cs] (hs is the relative humidity at
leaf surface) which enables one to simulate the
photosynthetic productivity with our data in processbased ecosystem CO2 flux models. Maximum PPFD
in open sky, maximum and minimum air temperatures
and water vapor pressure for the simulations were
determined referring to the meteorological data
obtained at the canopy tower. Ambient CO2 concentration was set at 370 mmol mol1. The photosynthesis and stomatal conductance submodels of Yplant output the net photosynthetic rate and stomatal
conductance at the sunlit and shade parts of a single
leaf, then the values were integrated with sunlit and
shade leaf area for net photosynthetic rate of an entire
single leaf. The light interception and net photosynthesis of the shoots were obtained by integrating
the values for single leaves, and divided by total leaf
area for each shoot.
4. Results
4.1. Meteorological conditions and forest canopy
LAI
Meteorological conditions in year 2003 (Fig. 1) were
characterized by less irradiance in summer, lower
temperature and prolonged rainy season as compared to
the other years. Fig. 1c shows the seasonal change of
single leaf growth, forest canopy LAI and light
availability (ISF) in the forest understory. LAI and
ISF values in early May (just after snowmelt) reflect the
branch and trunk of the canopy trees. In late May, leaves
started to expand rapidly and matured in late June. The
single leaf area and LAI reached their peak almost
simultaneously. The maximum LAI was 4.0  1.0 for
the 14 locations in the studied forest. The value was
close to that estimated by light transmittance measurements in this forest (Saigusa et al., 2002). ISF at the
forest understory decreased with increasing leaf area of
the forest canopy and reached minimum (about 0.12)
when LAI reached maximum. LAI started to decrease
and ISF started to increase in early October until the
defoliation completed in early November.

Fig. 1. Seasonal change of daily PPFD (a), precipitation and air

temperature (b), canopy LAI (open square), single leaf growth at
the canopy (gray triangle for B. ermanii., open and closed circles for
sun and shade leaves of Q. crispula, respectively: open circles were
hidden behind the closed circles on the figure) and light availability
(ISF, closed square) in the understory (c). Mean  S.D. are shown.

4.2. Seasonal change of leaf characteristics

We observed remarkable seasonal changes in single
leaf characteristics related to photosynthetic capacity
(Fig. 2). Amax, Vcmax25 and Jmax25 increased rapidly until
mid June, and were stable until late July (early
summer). The values in B. ermanii and Q. crispula
sun leaves then increased again and reached peak in late
August, with mean Amax of 16.2 mmol m2 s1 for B.
ermanii, 13.4 mmol m2 s1 for sun leaves and
6.7 mmol m2 s1 for shade leaves of Q. crispula,
respectively (Table 1). The ratio of Jmax25 to Vcmax25
was the highest (ca. 3.2) at the initial stage of leaf

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

45

Fig. 2. Seasonal changes of single leaf characteristics of canopy trees; light saturated rate of photosynthesis (Amax) (a), maximum carboxylation
efficiency at 25 8C (Vcmax25) (b), maximum electron transport rate at 25 8C (Jmax25) (c), the ratio of Jmax25 to Vcmax25 (d), stomatal conductance for
water vapor at light saturation (gsw) (e), dark respiration rate (R) (f), leaf mass per area (LMA) (g) and SPAD value as an index of leaf chlorophyll
content (h). Mean  S.D. are shown for B. ermanii (gray triangle), sun (open circle) and shade (closed circle) leaves of Q. crispula.

development, staying around 1.52.4 until late summer,

and increased again to about 3.2 in autumn. Stomatal
conductance for water vapor (gsw) changed concomitantly with Amax. Dark respiration rate (R) was the
highest when the leaves emerged and decreased rapidly
until late June when the photosynthetic capacity

reached the high values (but not the maximum). In

mid summer (early August), R of B. ermanii and Q.
crispula sun leaves increased once but was due to the
higher temperature condition for this measurement day
than the others. R continued to decrease until leaf
yellowing in autumn. LMA of both species reached

Light saturated rate of net photosynthesis (Amax), dark respiration rate (R), stomatal conductance for water vapor (gsw), maximum carboxyration rate at 25 8C (Vcmax25), maximum electron transport
rate at 25 8C (Jmax25), leaf mass per area (LMA) and SPAD value as an index of chlorophyll content are shown (mean  S.D., n = 5). Amax, R and gsw were measured at leaf temperature of ca. 23.0 8C
and VPD of <1 kPa. Parameters for the Leuning (1995) stomatal conductance model (m and g0) and slope (a) for the Ball et al. (1987) stomatal conductance model are also shown.

0.106
0.047
0.047
0.19
0.05
10.23
10.01
10.01
3.1
9.7
76.1  6.9
99.2  3.1
63.2  3.2
28.6  4.9
42.6  6.0
0.62  0.14
1.30  0.24
0.59  0.15
0.28  0.09
0.27  0.07
Open
Open
0.159
0.142  0.019
0.137  0.090
Betula
Quercus-sun
Quercus-shade
Hydrangea
Viburnum

16.2  1.9
13.4  0.8
6.7  0.8
7.9  1.7
5.7  1.4

0.681  0.216
0.385  0.083
0.193  0.054
0.332  0.070
0.225  0.063

69.1  7.5
57.8  4.4
29.2  3.2
32.8  7.6
24.2  5.9

162.7  22.7
122.1  12.9
54.9  8.0
67.9  23.6
60.5  9.3

41.9  1.2
43.2  1.7
43.2  0.6
37.4  1.9
36.0  3.8

g0
m
SPAD
LMA
(g m2)
Jmax25
(mmol m2 s1)
Vcmax25
(mmol m2 s1)
gsw
(mol m2 s1)
R
(mmol m2 s1)
Amax
(mmol m2 s1)
ISF
Species

Table 1
Summary of single leaf characteristics for two canopy (Betual and Quercus) and two shrub (Hydrangea and Viburnum) species in summer (August 22, 2003)

9.35
10.41
10.41
4.21
12.23

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

46

maximum in late August when the photosynthetic

capacity reached maximum. SPAD value, which
represents leaf chlorophyll content, increased rapidly
with increasing LMA and photosynthetic capacity, and
reached maximum in early summer (late June).
Fig. 3 shows the relationships between the single leaf
characteristics throughout the growing season to find
any consequence between leaf morphological and
physiological development. Amax and Vcmax25 were
highly dependent on LMA and SPAD. Between the two
determinant factors of the photosynthetic capacity,
SPAD had larger effect than LMA. Amax and gsw were
highly correlated throughout the season (Fig. 3c). There
was no remarkable relationship between R and Amax or
Vcmax (data not shown). Fig. 3f shows the relationship
between R and leaf temperature. Although R at the early
stage of the leaf development showed remarkably
higher values at given leaf temperatures due to
construction respiration, R increased exponentially
with increasing leaf temperature when the relationship
was examined for data in summer and autumn.
4.3. Leaf characteristics of canopy and shrub
species in mid summer
Leaf gas exchange characteristics of canopy and
shrub species were compared for the data obtained in
mid summer (Fig. 4 and Table 1). Among the four
species, B. ermanii showed the highest photosynthetic
capacity (Amax, Vcmax25 and Jmax25) and gsw. In Q.
crispula, Amax, R and gsw in sun leaves were about
double of those in shade leaves, while LMA was about
30% higher in sun leaves and SPAD was similar
between sun and shade leaves. Mean Amax of H.
paniculata was slightly higher than that in shade leaves
of Q. crispula and V. furcatum.
Leaves of H. paniculata and V. furcatum showed a
small but an expectable effect of microsite light
availability on the ACi curves (Fig. 4) and other leaf
properties. Although we pooled the data of ISF and leaf
characteristics for each species on Table 1, leaves in
both shrub species had slightly higher Amax under higher
light availability in the forest understory ranging from
ISF of 0.12 to 0.16 (r = 0.976 in H. paniculata and
r = 0.581 in V. furcatum, data not shown). LMA was also
highly correlated to ISF in H. paniculata (r = 0.961) and
V. furcatum (r = 0.499). In mid summer, relationship
between SPAD and Amax was not remarkable but LMA
showed a highly positive correlation with Amax in Q.
crispula (r = 0.9675: for sun and shade leaves), H.
paniculata (r = 0.908) and V. furcatum (r = 0.647), but
not in B. ermanii.

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

47

Fig. 3. Relationships between the single leaf properties (Amax, Vcmax25, LMA, SPAD, gsw) during the seasonal leaf development, and relationship
between leaf temperature (Tleaf) and R for B. ermanii (gray triangle), sun (open circle) and shade (closed circle) leaves of Q. crispula. Correlation
coefficient (r) is shown for linear correlation (ae). The equations between leaf temperature and R (f) fitted for the data obtained after leaf maturation
(during late June to October) are: R = 0.10328 exp(0.098083Tleaf) for B. ermanii, R = 0.11422 exp(0.10348Tleaf) for sun and
R = 0.32287 exp(0.024822Tleaf) for shade leaves of Q. crispula.

4.4. Shoot architecture

Fig. 5 shows the sample images of the canopy and
shrub shoots reconstructed by Y-plant. B. ermanii
exhibits distichous phyllotaxy and the shoots are
characterized by the steep leaf angle (mean 658) and
long petiole (2530 mm), while leaves in sun shoots of
Q. crispula (spiral phyllotaxy) have smaller inclination
angle (31.58) with small petiole and the shade shoots
were arranged rather flat than the sun shoots with
smaller leaf angle (24.58). H. paniculata (17.88) and V.
furcatum (28.68), both exhibits opposite decussate
phyllotaxy, were similar to that in shade shoots of Q.

crispula, but leaves are arranged so as to be less

overlapped.
We examined the effects of leaf arrangement along
the shoot and leaf angle on the efficiency of leaf display
for light interception (Fig. 6). Here, we calculated the
projection efficiency (PE) and the display efficiency
(DE) by Y-plant (Pearcy and Yang, 1996; Pearcy et al.,
2005). PE is the leaf area of a shoot projected in a
particular direction divided by the actual leaf area on the
shoot. For a given direction, PE is equal to the average
cosine of incidence, ranging from one if the leaf
surfaces are all perpendicular to the beam direction to
zero if the leaf surfaces are all parallel to the beam

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

Fig. 4. Relationship between net photosynthetic rate (A) and intercellular CO2 concentration (Ci) for B. ermanii (at canopy top), Q. crispula (canopy
top, open circle; inner-canopy, closed circle), H. paniculata and V. furcatum. For H. paniculata and V. furcatum, samples obtained under small gap
were represented by open symbols (see text).

Fig. 5. Sample images of shoots of B. ermanii, Q. crispula, H. paniculata and V. furcatum reconstructed in Y-plant. Bar represents 10 cm.
Mean  S.D. for total leaf area (m2) of the measured shoots and leaf angle are also shown with their sample numbers in parentheses.

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

49

Fig. 6. Simulated diurnal changes of projection efficiency (PE), display efficiency (DE), fraction of self-shading in a shoot (upper plates) and fraction
of sunlit and shaded leaf area of the shoots (lower plates) for B. ermanii and sun shoots of Q. crispula. Symbols in upper plates are: artificialhorizontal leaves (PE:
; DE: +), measured and rotated shoots (PE: open triangle; DE: open circle; fraction of self-shading: closed circle). In lower
plates open circle and closed circle represent fraction of sunlit and shaded leaf area, respectively. Mean  S.D. of 12 samples are shown for the
measured and rotated shoots.

direction. DE is the leaf area displayed in a particular

direction relative to the actual leaf area on the shoot, and
is equal to PE minus the fraction of leaf area that is
overlapped by other leaves in the plane perpendicular to
the beam; DE includes both the effect of leaf angles and
the spatial distribution of leaves that influences their
self-shading. Hence, the fraction of leaf area that is selfshaded is [PE  DE].
Fig. 6 shows the diurnal changes of PE, DE and
fraction of self-shading for shoots of B. ermanii and sun
shoots of Q. crispula, calculated assuming clear open sky
of August 20. For comparison, those for an artificial shoot
having four horizontal leaves with no overlap are also
calculated. In a case leaves are horizontal and not selfshaded, PE equals DE and changed from 0.02 at dawn to
0.904 at solar noon and then declined. In B. ermanii
shoots having steep leaf angles, PE was high in morning
and evening (ca. 0.54), and lowest at solar noon (0.38).
DE was rather constant throughout the day (0.30.4) due
to the change in the fraction of leaf overlap (0.080.14) in
a similar pattern to PE. In sun shoots of Q. crispula, whose
stems are relatively erect and leaves have much smaller

angle and shorter petiole than B. ermanii, PE, DE and the

fraction of leaf overlap was lowest in morning and
evening (0.35, 0.25 and 0.1, respectively), and highest at
solar noon (0.75, 0.5 and 0.25). Reflecting these diurnal
changes of leaf display characteristics, fraction of sunlit
and shaded leaf area for the whole shoots changed
diurnally (Fig. 6b and d). The steep leaf angles of B.
ermanii allowed a high fraction of sunlit leaf area under
high solar angle at noon (ca. 85%), while small leaf
angles and short petioles of Q. crispula reduced sunlit
leaf area in midday hours (ca. 65%).
4.5. Estimation of shoot light interception and
photosynthesis
Using the above leaf gas exchange characteristics
(Table 1) and shoot geometrical characteristics (Fig. 5),
we simulated light interception and photosynthesis of the
shoots. Calculations were taken for the solar condition of
August 20, which is in the period of maximum
photosynthetic activity for the studied forest, with
maximum incident PPFD of ca. 2400 mmol m2 s1 at

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

horizontal plane. Three air temperature (Tair) conditions

were applied: minimum and maximum (13:00 h) of 10
15, 1520 and 1828 8C. These three temperature
regimes were determined referring to the available

conditions in summer. Relative humidity at the leaf

surface was 6070%.
Fig. 7 shows the simulated diurnal courses of
absorbed PPFD, leaf temperature (Tleaf), photosynthetic

Fig. 7. Simulated diurnal courses of absorbed PPFD, leaf temperature (Tleaf), net photosynthetic rate (Asim) and stomatal conductance for CO2 (gsc)
for artificial shoots with horizontal leaves (left column) and measured shoots (right column, mean  S.D. for 12 shoots) of B. ermanii. Different
symbols for Tleaf, Asim and gsc represent different air temperature regimes; 1015 8C (open triangle), 1520 8C (gray) and 1828 8C (closed).

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

rate (Asim) and stomatal conductance to CO2 (gsc, equals

gsw/1.6) for an artificial shoot having four horizontal
leaves with no overlap and for the 12 measured and
rotated shoots for B. ermanii. Absorbed PPFD and Asim
are shown for the whole shoots expressed on leaf area
basis (averaged for total leaf area), but Tleaf and gsc are
for the sunlit parts. In the artificial-horizontal leaves
(Fig. 7ad), absorbed PPFD reached maximum of about
2000 mmol m2 s1 at noon, and Tleaf reached about 19,
23 and 30 8C for the three Tair regimes, respectively.
Maximum values and diurnal patterns of Asim and gsc
were affected by the different Tair regimes. The middle
and highest Tair regimes allowed Asim to reach the
highest values of about 18 mmol m2 s1 (close to the
highest value in situ), but the lowest Tair regime led
lower maximum Asim in morning hours. In contrast, the
lowest and middle Tair regimes resulted in the highest gsc
in morning hours while gsc under the highest Tair
condition was reduced especially in midday hours. Due
to this remarkable midday depression of gsc, Asim also
showed a midday depression.
Simulations for measured shoots (Fig. 7eh) showed
lower values in absorbed PPFD and Asim than those for
artificial-horizontal leaves. Tleaf in the sunlit part was
lower than in the horizontal leaves by about 2 8C (i.e.,
close to the daily maximum Tair for each temperature
regime). Depending on the individual shoot architecture
(characterized by its leaf angles), Asim was also
decreased by 20% than the horizontal leaves
(Fig. 7g). In the measured shoot simulations, although
Asim of the sunlit parts showed a small midday
depression (data not shown) like the case in horizontal
leaves, Asim of the whole shoot was rather constant in
midday hours. This constant Asim was achieved by the
relatively high photosynthetic rate on leaf area basis at
the shaded part (about 1530% of sunlit part) due to
relatively high light incidence at midday even under the
other leaves.
Results for the sun shoots of Q. crispula are shown in
Fig. 8. Diurnal pattern of absorbed PPFD in the
measured shoots followed that in artificial-horizontal
leaves by the small inclination angle of the actual
leaves, but the level was reduced by shaded lower leaves
in the shoots. Tleaf of Q. crispula leaves was higher than
B. ermanii and reached about 20, 25 and 32 8C for
respective Tair regimes (i.e., higher than maximum Tair
by about 5 8C). Maximum Tleaf for horizontal leaves and
for sunlit part of the measured shoots were similar. The
magnitude of midday depression of gsc and hence Asim
in the highest Tair regime was larger in Q. crispula for
both artificial-horizontal leaves (Fig. 8ad) and for
measured shoots (Fig. 8eh) than those in B. ermanii. In

51

the highest Tair regime, the large midday depression of

photosynthetic rate in sunlit part (data not shown but
refer to Fig. 8c) induced the midday depression of Asim
(Fig. 8g) irrespective the relatively high photosynthetic
rate on the leaf area basis in the shaded part (about 27
57% of sunlit part).
Examples of the simulations of PPFD and photosynthetic rate are also shown for the shrub species
(Fig. 9). Diurnal changes of absorbed PPFD and Asim in
the forest understory were characterized by the
incidence of sunflecks depending on the forest canopy
conditions (geometrical distribution and density of
foliage) covering a plant. The effect of leaf display was
less for shrub species as compared to the canopy
species, due to the sparse arrangement of leaves along
the stem (Fig. 5).
The above simulation results are summarized in
Table 2. Simulations showed that measured shoots at the
forest canopy top have about 6-fold of daily light
absorption (DayPPFD) of those in inner-canopy and
understory. In all species, simulated daily photosynthesis (DayA) was the smallest under Tair of 1015 8C
among the three temperature regimes. The highest
DayA of B. ermanii and H. paniculata, both have high
stomatal conductance, was found in the highest
temperature regime. In sun shoots of Q. crispula,
DayA was maximized in mid temperature regime. Shade
shoots of Q. crispula and V. furcatum reached similar
DayA between the highest and mid temperature
regimes.
Under any temperature condition, DayA was the
highest in B. ermanii and then sun shoots of Q. crispula
followed; B. ermanii was estimated to assimilate CO2
about 1.2-fold of Q. crispula. This difference was
enhanced to about 1.5-fold if DayA was expressed on the
leaf mass basis converted by LMA (7.0 mmol g1 day1
for B. ermanii and 4.8 mmol g1 day1 for Q. crispula in
1520 8C regime). In the light environment of forest
understory, H. paniculata was estimated to assimilate
CO2 about 1.5-fold of shade shoots of Q. crispula and V.
furcatum, and the productivity was enhanced to about
double when DayA was expressed on leaf mass basis.
Light utilization efficiency (LUE), the ratio of DayA to
DayPPFD was the highest in B. ermanii (17.2
18.7 mmol CO2 mol1 photons) due to its highest
photosynthetic capacity, while those of sun and shade
shoots of Q. crispula, H. paniculata and V. furcatum were
similar (12.614.9 mmol CO2 mol1 photons) irrespective of the difference in DayPPFD and photosynthetic
capacity among these species.
The simulation results also showed the possibility of
large overestimation of DayPPFD and DayA if the shoot

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

Fig. 8. Simulated diurnal courses of absorbed PPFD, leaf temperature (Tleaf), net photosynthetic rate (Asim) and stomatal conductance for CO2 (gsc)
for artificial shoots with horizontal leaves (left column) and measured shoots (right column, mean  S.D. for 12 shoots) of sun shoots of Q. crispula.
Different symbols for Tleaf, Asim and gsc represent different air temperature regimes; 1015 8C (open circle), 1520 8C (gray) and 1828 8C (closed).

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

53

Fig. 9. Simulated diurnal courses of absorbed PPFD and net photosynthetic rate (Asim) for H. paniculata (left column) and V. furcatum (right
column). Thick and thin lines represent simulations for measured shoots and artificial-horizontal leaves, respectively. Tair is 1520 8C.

Table 2
Summary of simulated results of daily light absorption, photosynthesis and light utilization efficiency for the shoots of canopy (Betula and Quercus)
and shrub (Hydrangea and Viburnum) species
Species

DayPPFD (mol m2 day1)

Estimation for measured shoots

Betula
29.61  4.63
Quercus-sun
33.36  3.17
Quercus-shade
5.38  2.00
Hydrangea
8.14  3.05
Viburnum
6.78  2.51

(12)
(12)
(54)
(42)
(42)

DayA (mmol m2 day1)

Light utilization efficiency

(mmol CO2 mol1 photons)

1015 8C

1520 8C

1828 8C

1015 8C

1520 8C

1828 8C

501.1  37.9
449.2  30.4
73.7  18.5
105.2  22.2
80.9  16.8

533.6  40.0
471.3  32.5
77.1  19.7
111.7  23.9
85.3  17.8

543.4  36.7
459.2  31.5
76.1  19.8
114.3  24.0
85.5  17.6

17.2  2.3
12.8  0.4
14.2  2.2
13.6  2.6
12.6  2.6

18.4  2.5
14.2  0.7
14.9  2.3
14.5  2.7
13.3  2.7

18.7  2.8
13.8  0.8
14.7  2.5
14.9  3.0
13.4  3.0

leaf overlap
725.5
624.2
110.4  24.6
116.5  25.1
96.9  19.9

716.5
587.9
108.6  25.2
119.4  25.3
96.8  19.7

12.2
10.9
13.3  2.4
13.7  2.8
11.5  2.5

13.0
11.4
14.1  2.6
14.6  2.9
12.2  2.6

12.8
10.8
13.9  2.9
15.0  3.2
12.2  2.9

Estimations for artificial shoots with horizontal four leaves a and no

Betula
55.80(1)
680.8
Quercus-sun
54.41 (1)
595.5
Quercus-shade
8.23  3.03 (15)
104.8  23.1
Hydrangea
8.44  3.20 (14)
109.5  23.4
Viburnum
8.44  3.16 (14)
91.9  18.8

Results are shown for measured shoot architecture (Fig. 5) and artificial model shoots having four horizontal leaves with no leaf overlap. Simulations
for canopy species (Betula and sun shoots of Quercus) were conducted under clear open sky condition and those for shade shoots of Quercus and
shrubs were conducted using hemispherical canopy photographs, under three air temperature conditions (minimummaximum; 1015, 1520 and
1828 8C). Replications (in parentheses) for each species were created by rotating the measured shoots architecture (Betula and Quercus; three
shoots
four azimuth) or hemispherical photographs (1 for rotated 3 shoots
4 azimuth and 14 for measured 3 Q. crispula-shade shoots, and 14 for
3 Hydrangea and Viburnum shoots).

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H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

architecture was not taken into account, especially for

the canopy tree species (Table 2). In a case that light
absorption and photosynthesis were estimated assuming
horizontal leaf and no self-shading for B. ermanii and Q.
crispula, light absorption can be overestimated by
double and DayA to be +40%. In contrast, shrub species
showed similar DayPPFD and DayA between those
estimated for measured shoot architectures and artificial-horizontal leaves.
5. Discussion
5.1. Seasonal changes of single leaf and forest
canopy characteristics
Periodical measurements of single leaf area and leaf
photosynthetic/respiratory characteristics for the
canopy tree species and forest canopy LAI revealed
different patterns of seasonal change in these factors
responsible for forest CO2 uptake (Figs. 1 and 2). Leaf
area (and canopy LAI) matured much earlier than the
photosynthetic capacity (Amax, Vcmax) and respiration
rate (R). The time-lag of these two factors was about 2
months, while the growing season for these canopy trees
are about 5 months. Observations on leaf area,
anatomical and biochemical characteristics with leaf
ontogeny revealed such time-lag (Miyazawa et al.,
1998). Another possible reason for the long time-lag in
the present study would be the shortage of irradiance
due to the irregularly prolonged rainy season of this year
(2003); usually the rainy season of the present region
ceases in late July. Since the development of photosynthetic capacity in a sunny environment (i.e., canopy
top) requires high light incidence (e.g., Niinemets et al.,
2004), the prolonged rainy/cloudy sky should have
suppressed the physiological development at the canopy
top until mid August (Figs. 1 and 2).
These results strongly indicate that the photosynthetic productivity (capacity of CO2 uptake) of the
deciduous forest canopy should be evaluated by
considering the different patterns of seasonal changes
in leaf area (LAI) and leaf gas exchange characteristics.
Studies suggesting the significant influences of seasonal
changes in LAI and photosynthetic capacity have shown
a remarkable overestimation of photosynthetic productivity at the forest canopy level if the evaluation was
performed assuming constant photosynthetic capacity
(Wilson et al., 2001; Morecroft et al., 2003; Xu and
Baldocchi, 2003), which can be expected easily by
comparing the canopy photosynthetic productivity
between [LAI
Amax (or Vcmax) maintaining the
maximum level for entire season] and [LAI
Amax

(or Vcmax) with seasonal change] for full season. In

addition, the phenological changes in leaf area and
photosynthetic capacity are species-specific. It is no
doubt that such species-specific phenological features
affect ecosystem photosynthetic productivity in a forest
whose canopy includes several species like our
deciduous forest. Phenology of LAI and leaf gas
exchange characteristics should be investigated continuously for a few years since year-to-year variation of
meteorological conditions affects leaf development and
photosynthetic productivity (Abrams et al., 1994;
Muraoka et al., 1997; Wilson et al., 2000) and hence
probably ecosystem CO2 flux (Yamamoto et al., 1999;
Saigusa et al., 2002). Accumulation of these data would
provide us the ecological consequences between
seasonal meteorology and foliage ecophysiological
properties, which would enable us to analyze the past
and future CO2 flux by introducing a process-based
model (Ito and Oikawa, 2002; Ito et al., 2006).
The seasonal development of photosynthetic capacity was dependent on the ontogenetic changes in leaf
anatomical (thickness) and biochemical (photochemistry and Calvin cycle) component (LMA and SPAD)
and stomatal conductance (Fig. 3). Although the
relationship between LMA and Amax (or Vcmax25) was
weak in our observation, SPAD value was found to be an
index of the relative change of photosynthetic capacity
for a given species under a given light environment (see
also Kosugi et al., 2003). However, SPAD value may not
be used for the comparison of photosynthetic capacity
between leaves in different light environment for a
given species as we showed for sun and shade leaves of
Q. crispula (Table 1). For Q. crispula in mid summer,
LMA and microsite light availability (ISF) were the
determinant to explain the difference of photosynthetic
capacity. If one would estimate the seasonal photosynthetic capacity of leaves for different species and
different light environment without measuring leaf gas
exchange, combined model of leaf chlorophyll content
(or SPAD value), nitrogen content, LMA and local light
environment should be developed (Niinemets and
Tenhunen, 1997; Wilson et al., 2000; Larocque,
2002) by an intensive measurements of these parameters across season and vertical profile of the forest
canopy.
In addition to the above phenological changes of LAI
and photosynthetic capacity, we found a remarkable
seasonal change in R and in Jmax25/Vcmax25 (Fig. 2). The
very high R at the initial phase of leaf phenology can be
attributed to the construction cost of leaf expansion
involving leaf anatomical and biochemical development as can be found in the changes of LMA, SPAD and

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

Amax. The seasonal change of R affects the CO2 balance

of the whole ecosystem since it directly scales with
entire leaf biomass and its seasonal change. The rapid
increase of canopy leaf area and the high R would cause
a rapid increase and high rate of ecosystem CO2 efflux
during a period of leaf expansion (S. Murayama, N.
Saigusa, C. Takamura, personal communication).
Seasonal change in Jmax/Vcmax would be also
responsible for the photosynthetic productivity in the
foliage under variable temperature conditions (Hikosaka, 1997; Hikosaka et al., 1999; Xu and Baldocchi,
2003). Since the photosynthetic rate at low temperature
tends to be limited by the RuBP regeneration capacity,
which is expressed by Jmax, higher allocation of
nitrogen to the responsible component would maintain
photosynthetic production under low temperature
conditions such as in spring and autumn (cf. Berry
and Bjorkman, 1980). The opposite would be also true
since the photosynthetic rate under higher temperature
conditions in summer is limited by RuBP carboxylation
capacity (Vcmax) (see also Hikosaka et al., 1999). If
plants change Jmax/Vcmax responding to the seasonal
change of temperature condition (i.e., temperature
acclimation), simple scaling from Vcmax to Jmax
(Wullschleger, 1993) assuming their constant ratio
would underestimate Jmax in low temperature seasons.
We were not able to test these effects since our present
data on Jmax and Vcmax at 25 8C (and thus Jmax25/
Vcmax25) are calculated but not obtained by measuring
temperature dependency of ACi curves. Future
measurements of temperature dependency for each
species throughout the season are needed for accurate
scaling from leaf level ecophysiology to canopy scale
behavior over the season.
5.2. Effects of leaf properties and shoot
architecture on productivity at the canopy top
Our calculation of light interception and photosynthetic carbon gain showed two aspects in model study:
one is the effectiveness of the use of combined model of
leaf photosynthesis (Farquhar et al., 1980) and stomatal
conductance (Leuning, 1995), and the another is the
responsibility of the plant geometrical characteristics in
canopy light interception and photosynthesis.
The combined model of leaf photosynthesis and
stomatal conductance has been used widely and now is a
fundamental component of canopy photosynthesis
model (Baldocchi and Meyers, 1998; Wilson et al.,
2001; Xu and Baldocchi, 2003). The most remarkable
effect of the combined model on the estimation of daily
photosynthesis in our study was shown in artificial-

55

horizontal leaves of B. ermanii and Q. crispula

conducted under the highest Tair condition (Figs. 7a
d and 8ad). Under the high midday Tair of 28 8C, which
is close to the highest temperature condition observable
in the forest, intrinsically high gsc (g0 = 0.106) of B.
ermanii worked efficiently in regulating Tleaf and hence
induced little midday depression of Asim, while
intrinsically low gsc (g0 = 0.047) of Q. crispula led
rising Tleaf and hence larger midday depression of
photosynthesis.
Our model incorporating the shoot architectural
property showed striking effects of leaf orientation and
self-shading on the estimation of canopy photosynthesis. Recent canopy photosynthesis models objected for
ecosystem CO2 uptake have emphasized the importance
of heterogeneous light distribution in a canopy such as
sunlit and shaded leaves since spatial and temporal
distribution of PPFD have considerable influence on the
photosynthesis under a sunny condition (Leuning et al.,
1995; Anten, 1997; de Pury and Farquhar, 1997;
Baldocchi and Meyers, 1998). In contrast, light
distribution under a cloudy sky is less heterogeneous
due to the diffuse light condition and therefore light
incidence at a given strata can be described by Monsi
Saeki law (Monsi and Saeki, 1953). Beside these one- or
two-dimensional models, recent development of threedimensional models for an individual plant (Pearcy and
Yang, 1996; Takenaka et al., 1998; Valladares, 1999) or
canopy (Takenaka, 1994a,b; Beyschlag and Ryel, 1999;
Werner et al., 2001) have shown the significant effects
of leaf position and orientation on the light interception
and photosynthetic carbon gain at a single leaf, shoot
and whole plant. Our simulations of light interception
and photosynthesis using Y-plant, which was developed
to study the effect of crown architecture on light
interception and carbon gain in relatively small scale
(Pearcy and Valladares, 1999; Valladares et al., 2002;
Muraoka et al., 2003; Pearcy et al., 2005), suggested
that model estimations without considering heterogeneous light distribution created by orientations and
positions of the leaves would overestimate the photosynthetic CO2 uptake remarkably even at the small scale
of our shoots with length of about 0.5 m (Figs. 7 and 8;
Table 2).
Light interception and resulting photosynthetic
carbon gains at the shoot scale are determined by the
geometrical relationships between leaf angle, leaf
position and solar beam. The most remarkable effect
was found for the canopy species, which have many
leaves along a given length of shoot stem (Fig. 5). The
long petiole and downward lamina of B. ermanii
allowed efficient light penetration into lower leaves,

56

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

resulting in higher fraction of sunlit leaf area throughout

a day (Fig. 6). In contrast, the rather horizontal lamina
and small petiole with spiral phyllotaxy of Q. crispula
led considerable self-shading of lower leaves in sun
shoots (Fig. 6). Although the calculated DayPPFD for
B. ermanii was smaller than that for sun shoots of Q.
crispula, the non-linear response of single leaf
photosynthetic rate to incident light does not require
full irradiance (A saturates at PPFD of about
1000 mmol m2 s1). Therefore, larger fraction of
sunlit leaf area (but not receiving full irradiance;
Fig. 7e) in B. ermanii contributed effectively for whole
shoot carbon gain. Again, the above-mentioned high gsc
of B. ermanii also worked for regulation of Tleaf and
high photosynthetic activity in the sunlit parts. Thus,
DayA of B. ermanii was not affected by the highest Tair
regime (Table 2). In contrast in sun shoots of Q.
crispula, the larger DayPPFD in midday hours than B.
ermanii was mostly attained by surface leaves of the
shoots that receive excessive high light (i.e., PPFD over
light saturation of photosynthesis) in midday with their
small inclination angle (data not shown but refer to
Fig. 8a). This excessive light in the sunlit parts led rising
Tleaf and VPD, and hence large midday depression in gsc
and photosynthetic rate. Thus, DayA was reduced in the
highest Tair regime (Table 2). These consequences of
single leaf properties and shoot architecture at the
canopy top under sunny and high temperature conditions would be highly responsible to the entire forest
CO2 uptake, though the contribution of photosynthesis
by inner-canopy leaves, stem respiration and soil
respiration are remained to be examined to explain
the dynamics of forest CO2 balance (Ito et al., 2006).
5.3. Possible contribution of understory species to
forest ecosystem carbon gain
Comparison of light interception and photosynthetic
carbon gain between canopy and shrub species
suggested important contribution of shrub species on
the CO2 uptake of whole forest ecosystem (Table 2).
Low R provides a high photosynthetic utilization
efficiency of low light at the single leaf scale and the
small self-shading enables the species to intercept light
effectively for photosynthesis. These characteristics in
shrub species led higher photosynthetic carbon gain
than the shade shoots of Q. crispula. Shrub species
inhabiting forest understory have been shown to
construct a crown, which is effective for light
interception by arranging branch architecture and leaf
display (AcKerly and Bazzaz, 1995; Valladares et al.,
2002; Pearcy et al., 2005). There is also evidence that

understory leaves can utilize sunflecks efficiently for

photosynthesis (Pearcy et al., 1994). These characteristics are no doubt to provide shrub species a significant
functional role in ecosystem CO2 uptake.
Previous studies on the forest ecosystem carbon gain
have been rarely focusing on the contribution of shrub
species or understory vegetation, partly because of the
low light availability in a forest understory. However, in
addition to their effective interception and utilization of
low light, the earlier leaf emergence and probably
photosynthetic maturation in shrub species than in the
canopy species (Kawamura et al., 2001) would enable
the shrub species to have a significant effect on the
forest CO2 uptake throughout a season in a forest (see
also Gill et al., 1998). Indeed, the understory herbaceous vegetation (evergreen dwarf bamboo, S. senanensis) has been shown to have a considerable contribution
to whole forest carbon gain especially in spring when
the forest canopy has no leaves (Sakai and Akiyama,
2006; Kondo et al., 2006; Nishimura et al., 2004).
Thus, photosynthetic productivity (or CO2 uptake) of
a forest ecosystem should be evaluated by taking the
role of different species in different strata of the forest
into account. There should be specific contribution
(role) in forest CO2 uptake depending on the species life
form, leaf ecophysiology and shoot architecture of each
species and available light, i.e., the canopy species
utilize the high light at the canopy top with their high
photosynthetic capacity, while understory species
utilize low light environment with no other environmental stress like rising temperature. Measurements of
seasonal change and spatial distribution of leaf area and
gas exchange properties for canopy species, shrub
species and understory vegetation, and further quantitative evaluation of their functional role in forest CO2
exchange are our ongoing research.
Acknowledgements
We deeply thank R.W. Pearcy of UC Davis (USA)
for his kind permission and technical support for our use
of Y-plant, and Y. Onoda of the Tohoku University
(Japan) for his advice in interpreting the seasonal
change of photosynthetic characteristics. We thank S.
Yamamoto, S. Murayama, N. Saigusa, K. Muto and C.
Takamura of National Institute of Advanced Industrial
Science and Technology and W. Mo of the University of
Tsukuba for their support in meteorological observation. Thanks are also due to K. Nishida of the University
of Tsukuba, M. Uchida of National Institute for Polar
Research and H. Hirota of Tokyo Metropolitan
University, K. Kurumado, M. Ohno, T. Sakai, M.

H. Muraoka, H. Koizumi / Agricultural and Forest Meteorology 134 (2005) 3959

Kondo and T. Akiyama of Institute for Basin Ecosystem

Studies, Gifu University, for their support in field
observation. This study was supported by the Ministry
of Environment, Japan, as Global Environment
Research Fund (S-1: Integrated Study for Terrestrial
Carbon Management of Asia in the 21st Century Based
on Scientific Advancement).

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