Tree Physiology 26, 1173–1184
© 2006 Heron Publishing—Victoria, Canada
Seasonal fluctuations and temperature dependence of leaf gas
exchange parameters of co-occurring evergreen and deciduous trees in
a temperate broad-leaved forest
YOSHIKO KOSUGI
1,2
and NAOKO MATSUO1
1
Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
2
Corresponding author ([email protected])
Received March 21, 2005; accepted September 22, 2005; published online June 1, 2006
Summary Seasonal fluctuations in leaf gas exchange parameters were investigated in three evergreen (Quercus glauca
Thunb., Cinnamomum camphora Sieb. and Castanopsis cuspidata Schottky) and one deciduous (Quercus serrata Thunb.)
co-occurring, dominant tree species in a temperate broadleaved forest. Dark respiration rate (R n ), maximum carboxylation rate (Vcmax ) and stomatal coefficient (m), the ratio of
stomatal conductance to net assimilation rate after adjustment
to the vapor pressure deficit and internal carbon dioxide (CO2)
concentration, were derived inversely from instantaneous field
gas exchange data (one-point method). The normalized values of R n and Vcmax at the reference temperature of 25 °C
(R n25 , Vcmax25 ) and their temperature dependencies (ΔH a (R n ),
ΔH a (Vcmax )) were analyzed. Parameter Vcmax25 ranged from
24.0–40.3 µmol m – 2 s – 1 and ΔH a (Vcmax ) ranged from 29.1–
67.0 kJ mol – 1. Parameter R n25 ranged from 0.6–1.4 µmol m – 2
s – 1 and ΔH a (R n ) ranged from 47.4–95.4 kJ mol – 1. The stomatal coefficient ranged from 7.2–8.2. For the three evergreen
trees, a single set of Vcmax25 and R n25 parameters and temperature dependence curves produced satisfactory estimates of carbon uptake throughout the year, except during the period of
simultaneous leaf fall and leaf expansion, which occurs in
April and May. In the deciduous oak, declines in Vcmax25 were
observed after summer, along with changes in Vcmax25 and R n25
during the leaf expansion period. In all species, variation in m
during periods of leaf expansion and drought should be considered in modeling studies. We conclude that the changes in normalized gas exchange parameters during periods of leaf
expansion and drought need to be considered when modeling
carbon uptake of evergreen broad-leaved species.
Keywords: dark respiration rate, maximum carboxylation
rate, photosynthesis, stomatal conductance, temperate broadleaved forest.
Introduction
Leaf gas exchange characteristics must have an important
bearing on forest carbon uptake (e.g., Baldocchi and Meyers
1998, Wilson et al. 2001, Lai et al. 2002), yet, to date, studies
of leaf-scale gas exchange have yielded few results applicable
to modeling long-term canopy or landscape carbon exchange
(Xu and Baldocchi 2003, Kosugi et al. 2003). It is still unclear
how gas exchange parameters differ among species, seasons,
locations and environmental conditions in the field, although it
has recently been recognized that it is essential to include seasonal changes in gas exchange characteristics to model accurately the carbon uptake of deciduous broad-leaved forests.
This requirement was confirmed by Wilson et al. (2001) who
showed that modeled net ecosystem exchange of carbon better
matched eddy covariance measurements when seasonal variation in maximum carboxylation rate (Vcmax ; Wilson et al. 2000)
was taken into account.
Kosugi et al. (2003) used field gas exchange data to demonstrate that accurate modeling of gas exchange in deciduous
broad-leaved trees across seasons requires information on seasonal changes in Vcmax, dark respiration rate (R n ) at a reference
temperature and stomatal coefficient (m), the ratio of stomatal
conductance to net assimilation rate after adjustment for
the vapor pressure deficit and internal carbon dioxide (CO2)
concentration in the Ball-type stomatal conductance model,
during leaf expansion. Spatial variations in gas exchange parameters have also been reported in a deciduous and an evergreen broad-leaved tree (Dungan et al. 2003) and a pine tree
(Han et al. 2003). Seasonal and spatial variations in gas exchange parameters can be explained, in part, by changes in leaf
nitrogen content, although the relationship with leaf nitrogen
is not necessarily constant. Thus, gas exchange parameters and
their temporal and spatial variations cannot be described simply as a constant function of leaf nitrogen content. The influences of nitrogen allocation, acclimation, enzyme activity and
other factors on leaf gas exchange parameters need, therefore,
to be quantified if the relationship between gas exchange at the
leaf scale and at the canopy scale, is to be understood.
There is a need for information, based on long-term field observations, about which parameter set should be used for
long-term and larger scale simulations of each forest type. Although several studies have clarified seasonal changes in gas
exchange parameters in temperate deciduous broad-leaved
forest, there is little information about seasonal fluctuations in
1174
KOSUGI AND MATSUO
gas exchange characteristics in other types of forests such as
temperate evergreen broad-leaved forests (Tenhunen et al.
1990). Consequently, most larger scale simulation models,
which are now one of the main tools for evaluating carbon uptake by forests, use limited sets of published leaf gas exchange
parameters. Detailed information on the seasonal variation in
the value of these parameters in evergreen forests would allow
us to determine if we can evaluate carbon uptake for all seasons with one set of leaf gas exchange parameters.
We chose to study three evergreen and one deciduous tree
species co-occurring and dominant in a temperate evergreen
broad-leaved forest in western Japan. We investigated seasonal fluctuations in three major gas exchange parameters (Rn ,
Vcmax and stomatal coefficient of the improved Ball-type stomatal conductance modelt (m) (Leuning 1995)) to obtain primary information for a canopy-scale long-term estimate of gas
exchange with a process-based multi-layer model based on
field observations (e.g., Tanaka et al. 2002).
Few studies have examined the temperature dependencies
of major gas exchange parameters of canopy leaves in the forest based on in situ field observation, especially in temperate
evergreen broad-leaved forests. The objectives of our study
were: (1) to develop a practical method for determining the
magnitude and seasonal fluctuations in leaf gas exchange parameters of the study species as a basis for modeling forest gas
exchange; and (2) to determine if it is possible to evaluate the
carbon uptake of a temperate evergreen broad-leaved forest in
all seasons with a single set of leaf gas exchange parameters.
Li-Cor, Lincoln, NE) under light-saturated conditions in three
sunlit current-year or previous-year leaves in the canopy of
each tree studied. Measurements were made in the morning
(between 0830 and 1300 h) on April 27, May 10, 17, 24,
June 7, 26, July 12, August 30 and October 16 in 2001 and on
January 23 and March 6 in 2002. Measurements were made
once on each leaf with an irradiance of 1000 µmol m – 2 s – 1 supplied by a red/blue LED (Li-Cor, LI-6400-02) under ambient
temperature, humidity and CO2 concentration. Previous studies of gas exchange in leaves of these trees indicated that maximum gas exchange rates were usually reached at a photosynthetic photon flux (PPF) of 1000 µmol m – 2 s – 1, at which
irradiance there was neither a sharp increase in leaf temperature nor a depression in photosynthesis. After the gas exchange measurements in the light, dark gas exchange rates of
the same leaves were measured with the LI-6400 by placing
the leaves in a dark chamber under ambient conditions.
Environmental conditions were measured at a meteorological observation tower close to the gas exchange observation
tower. Air temperature and relative humidity above the canopy
were measured with a Visala-type hygrothermometer (HMP35C, Campbell Scientific), downward solar radiation was
measured with a four-component radiometer (MR-40, Eiko,
Japan), rainfall data were provided from a fire station located
approximately 1 km from the plantation, soil capillary pressure was measured with tensiometers buried at depths of 10,
20, 30 and 40 cm and volumetric soil water content was measured with a water content reflectometer (CS615, Campbell
Scientific) buried in the soil beside the tower at depths of
0–30 cm.
Materials and methods
Parameterization procedure
Observations
Field observations were made in a forest plantation established
in 1987 at 34°44′ N, 134°22′ E in Akou, Hyogo prefecture on
the east coast of Japan. The plantation includes 12 temperate
evergreen trees species and four deciduous broad-leaved tree
species (Kosugi et al. 2005). Three-year-old seedlings were
planted in 1987 at a density of 1–2 stems m – 2. In January
2002, trees had a mean height of 5.3 m (including small shaded
trees) and a mean basal area of 34 m – 2 ha – 1. Tree density was
11,150 stems ha – 1. We made leaf gas exchange measurements
from April 2001 to March 2002 on one tree of each of three evergreen broad-leaved species (Quercus glauca Thunb., Cinnamomum camphora Sieb. and Castanopsis cuspidata Schottky)
and one co-occurring deciduous oak species (Quercus serrata
Thunb.) growing near a gas exchange observation tower in the
center of the forest. In the evergreen trees, simultaneous leaf
fall and leaf expansion occur in April and May, when the majority of previous-year leaves abscise and most current-year
leaves expand. Expansion occurs from mid-April in Q. glauca
and C. camphora and from early May in C. cuspidata.
C. camphora also expands some leaves in July and August. In
the deciduous oak (Q. serrata), expansion of new leaves occurs from mid-April and leaf senescence occurs in November.
Gas exchange measurements were made with a portable
steady-state photosynthesis measurement system (LI-6400,
We derived three major gas exchange parameters: normalized
dark respiration rate (R n25 ), normalized maximum carboxylation rate (Vcmax25 ) and m. The model used for the analysis was
a modified Farquhar et al. (1980) biochemical model of photosynthesis for C3 plants. Net CO2 assimilation rate is described
by:
⎛
p ( Γ* ) ⎞
A = Vc ⎜1 –
⎟ – Rd
p ( C c )⎠
⎝
(1)
p (O)
2τ
(2)
p ( Γ* ) =
where A is net assimilation rate (µmol m – 2 s – 1 ), Vc is rate of
carboxylation in the PCR cycle (µmol m – 2 s – 1 ), R d is day
(non-photorespiratory) respiration rate (µmol m – 2 s – 1 ), p(Γ* )
is the CO2 compensation point without non-photorespiraory respiration (Pa), τ the specificity factor of Rubisco and
p(C c ) (Pa) and p(O) (21,000 Pa) are the partial pressures of
CO2 and oxygen (O2) at the sites of carboxylation and oxygenation, respectively. The lower value between the ribulosebisphosphate (RuBP) regeneration or electron-transport limited rate of carboxylation (Wj ; µmol m – 2 s – 1) and the RuBP
saturated rate of carboxylation (Wc ; µmol m – 2 s – 1 ) is taken as
the velocity of carboxylation (Vc ), with Wc expressed as:
TREE PHYSIOLOGY VOLUME 26, 2006
SEASONAL FLUCTUATIONS IN LEAF GAS EXCHANGE
Wc = Vcmax
p (C c )
⎛
p (O) ⎞
p ( C c ) + K c ⎜1 +
⎟
Ko ⎠
⎝
(3)
where K c and K o (Pa) are the Rubisco Michaelis-Menten constants for CO2 and O2 , respectively. Parameter Vcmax (µmol
m – 2 s – 1 ) was estimated by the one-point method as described
by Kosugi et al. (2003). Briefly, Vcmax was derived from any
point within the low intercellular carbon dioxide concentration
(Ci ) range of the A–C i relationship after determining R d. Thus,
after excluding the points at which Wc is not the limiting factor
(under field conditions, this usually occurs at low PAR and
ambient CO2 concentration), each CO2 and H2O gas exchange
data point includes information on Vcmax if we know R d. This
method can reveal more information than the analysis of an
A–C i curve obtained with a controlled chamber in the field.
Values of K c and K o , τ and their activation energies used to
calculate temperature dependence were taken from Harley et
al. (1992). The Arrhenius function was used to determine the
temperature dependencies of parameters K c , K o , τ and R n as:
⎛ ⎡ T ⎤ ΔHa ⎞
f (T1. k ) = f (T ref ) exp ⎜ ⎢1 – ref ⎥
⎟
⎝ ⎣ T l. k ⎦ RT ref ⎠
(4)
A simplified equation from Sharpe and DeMichele (1977)
was used to determine the temperature dependence of Vcmax:
⎛ ⎡ T ⎤ ΔHa ⎞
f (T ref ) exp ⎜ ⎢1 – ref ⎥
⎟
⎝ ⎣ T1. k ⎦ RT ref ⎠
f ( T1. k ) =
⎛ Δ ST1. k – Δ H d ⎞
1 + exp ⎜
⎟
RT1. k
⎝
⎠
(5)
where f (Tl.k ) is the value of a given parameter at leaf temperature Tl.k (K), f (Tref ) is the reference value of that parameter at
25 °C (K c25 , K o25 , R n25 , τ 25 and Vcmax25 ), ΔH a is the activation
energy (J mol –1 ), ΔH d is the deactivation energy (J mol –1 ) and
ΔS is an entropy term (J K –1 mol –1 ).
First, we determined R n at the reference temperature and its
temperature dependence (Equation 4). Here, net assimilation
rate measured in the dark chamber was used to derive R n25 and
ΔH a (R n ) for each species. During the leaf expansion and leaf
fall periods, R n25 was optimized with a nonlinear least squares
optimization procedure separately for each species based on
the same activation energy as used in the other periods. Day
respiration rate (R d ) was scaled using the relationship with R n
(Lloyd et al. 1995) based on the results of Brooks and Farquhar
(1985):
R d = R n , when 0 < Q < 10 µmol m – 2 s – 1
1175
Next, we obtained the instantaneous Vcmax for each value
measured under light-saturated conditions by the one point
method. Temperature dependence and seasonal fluctuations in
Vcmax are discussed based on these data.
An improved Ball et al. (1987)-type model (Leuning 1995)
was used to estimate stomatal conductance:
g sw = m
f (D) =
A f (D)
+ g sw min
Cs – Γ
1
1+
(7)
D
D0
where g sw is stomatal conductance of H2O (mol H2O m – 2 s – 1 ),
A is net assimilation rate (µmol m – 2 s – 1 ), f (D) is the nonlinear
function of the vapor pressure deficit, m is the slope of the relationship between the stomatal index (Af (D)/(C s – Γ)) and
stomatal conductance, C s is CO2 concentration at the leaf surface (µmol mol – 1 ), Γ is the CO2 compensation point
( µmol mol – 1 ) and g swmin is minimum stomatal conductance.
A Lohammer-type (Lohammer et al. 1980) hyperbolic form
function is used for f (D), where D is vapor pressure deficit
(kPa) of air and D 0 is the empirical value at which f (D) halves.
The CO2 concentration at the leaf surface (Cs ) was calculated
based on the CO2 concentration of air in the chamber, a constant boundary layer conductance and net assimilation rate.
An important advantage of this improved model of Leuning
(1995) for long-term analyses is that it can describe stomatal
response to vapor pressure deficit with one curve over a wide
temperature range. If we use relative humidity for f (D), as in
the original version of Ball-type model (Ball et al. 1987),
stomatal response to vapor pressure deficit becomes too large
in winter and also differs from the summer curve, making the
analysis of the meaning of m obscure.
Results
Environmental conditions
Seasonal fluctuations in daily total solar radiation, daily mean,
maximum and minimum air temperatures, daily mean and
maximum vapor pressure deficits, daily total precipitation,
volumetric soil water content at 0–30 cm and soil capillary
pressure at 10, 20, 30 and 40 cm are shown in Figure 1. Summer droughts at the study site varied across years and the influence of severe drought on gas exchange processes has been detected (Tanaka et al. 2002). The year 2001 was moderate in
terms of precipitation (annual precipitation was 788 mm in
2000; 1078 mm in 2001; 578 mm in 2002; and 1230 mm in
2003).
Dark respiration rate
R d = ( 0.5 – 0.05 ln (Q ))R n , when Q > 10 μmol m – 2 s – 1
(6)
where Q is the incident PPF (µmol m – 2 s – 1 ).
Dark respiration rates are plotted against simultaneously measured leaf temperatures in Figure 2. Here we defined expanding leaves and old leaves as leaves having different R n characteristics compared with mature leaves of the same species. For
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1176
KOSUGI AND MATSUO
Figure 1. Seasonal fluctuations
in daily total solar radiation,
daily mean, maximum and
minimum air temperatures,
daily mean and maximum vapor pressure deficits (VPD),
daily total precipitation, volumetric soil water content at
0–30 cm and soil capillary
pressure at depths of 10, 20,
30 and 40 cm.
Figure 2. Dark respiration rate
(R n ) observed in three leaves
of each tree and on each observation day, plotted against
leaf temperature. Circles indicate mean values for three
leaves (䊊 = expanding leaves;
䊉 = mature leaves; and 䊉 =
old leaves). Error bars are ± 1
standard deviation.
all species, R n values were significantly higher for expanding
leaves than for mature and old leaves (cf. Xu and Baldocchi
2003, Kosugi et al. 2003). In old leaves (about one month before abscission) of the evergreen trees, R n values were lower
than expected based on the temperature dependence curve of
mature leaves. After excluding values obtained when leaves
were expanding or old, seasonal changes in R n could be explained by one temperature dependence curve for each species. Values of R n25 and ΔH a (R n ) used in the temperature dependence curve for each species (Equation 4) are shown in
Table 1. The dark respiration rate at 25°C ranged between
0.6–1.4 µmol m – 2 s – 1 and ΔH a (R n ) ranged between 47.4–
95.4 kJ mol – 1.
Maximum carboxylation rate
Maximum carboxylation rates are plotted against leaf temperature in Figure 3. We assumed that expanding leaves and old
leaves have different Vcmax characteristics compared with mature leaves of the same species. Thus, the data for expanding
and old leaves were excluded from the line fitting process. The
shift in observed Vcmax from expanding to mature leaves occurred earlier than the shift in R n (May 24 for Q. glauca, June 6
for C. camphora, May 10 for Q. serrata; cf. Figures 2 and 3).
The post-summer decline in Vcmax that was detected in the deciduous oak (August 29 and October 16 for Q. serrata) was
also considered a characteristic of old leaves. Apart from the
TREE PHYSIOLOGY VOLUME 26, 2006
SEASONAL FLUCTUATIONS IN LEAF GAS EXCHANGE
1177
Table 1. Dark respiration rates at the reference temperature (R n25 ), the activation energy (ΔH a (R d )), maximum carboxylation rate at the reference
temperature (Vcmax25 ), the activation energy (ΔH a (Vcmax )), the deactivation energy (ΔH d (Vcmax )) and the entropy term (ΔS) in mature leaves of
each tree species.
Species
Rn25
(µmol m – 2 s – 1 )
ΔH a (R n )
(kJ mol – 1 )
Vcmax25
(µmol m – 2 s – 1 )
ΔH a (Vcmax )
(kJ mol – 1 )
ΔH d (Vcmax )
(kJ mol – 1)
ΔS
(J K – 1 mol – 1 )
Q. glauca Thunb.
C. camphora Sieb.
C. cuspidata Schottky
Q. serrata Thunb.
1.3
1.4
1.0
0.6
47.4
48.0
60.0
95.4
24.0
40.3
33.1(27.8) 3
32.9
59.5
54.9
29.1(56.2) 3
67.0
250.0 1
250.0 1
250.0 1
204.62
600 1
600 1
600 1
650 2
1
2
3
Tenhunen et al. 1990.
Kosugi et al. 2003.
Values in parentheses in Castanopsis cuspidata are optimized based on summer and autumn data only (June 7–October 16, 2001).
leaf expansion and leaf fall periods, seasonal fluctuations in
Vcmax for the three evergreen broad-leaved trees could be explained by one temperature dependence curve for each species. A post-summer decline in normalized Vcmax needs to be
incorporated into models involving deciduous trees because
our results for the deciduous oak corroborate those reported
for several other temperate deciduous tree species (Wilson et
al. 2001, Xu and Baldocchi 2003, Dungan et al. 2003, Kosugi
et al. 2003). Moreover, similar seasonal fluctuations in Vcmax
have been observed in wheat (Grossman-Clarke et al. 1999),
Sphagnum and Pleurozium (Williams and Flanagan 1998), although Falge et al. (1996) reported no obvious seasonality in
normalized Vcmax of an evergreen conifer (Picea abies (L.)
Karst.) growing in a forest. Although more field results are
necessary to clarify the relationships between seasonality and
plant lifestyle, we found that normalized Vcmax in our temperate evergreen broad-leaved trees changed significantly from
the year-round value only during the leaf expansion and leaf
fall periods.
Values of Vcmax25 and ΔH a (Vcmax ) used in the temperature dependence curve (Equation 5) are shown in Table 1. The deacti-
vation energy (ΔH d (Vcmax )) and the entropy term (ΔS) were
fixed as constant values in the optimization procedure because
the data we used provided insufficient information about the
behavior of Vcmax at high temperature to evaluate these parameters, except to conclude that there was no obvious decline in
Vcmax at temperatures above 30 °C. The constant values used
were 250,000 for ΔH d (Vcmax ) and 600 for ΔS, following the results obtained for the evergreen oak Quercus coccifera L. by
Tenhunen et al. (1990). For calculations involving the deciduous oak, we used 204, 600 for ΔH d (Vcmax ) and 650 for ΔS (cf.
Kosugi et al. (2003). Parameter Vcmax25 ranged among species
from 24.0 to 40.3 µmol m – 2 s – 1 and ΔH a (Vcmax ) ranged from
29.1 to 67.0 kJ mol – 1.
Stomatal conductance
The relationship between stomatal index (defined as
Af (D)/(C s – Γ)) and stomatal conductance is shown in Figure 4. The linear relationship between these parameters and
the constant m (estimated at between 7.2 and 8.2) appeared to
be more or less maintained through all seasons. A more detailed examination of the data showed that there were differ-
Figure 3. Maximum carboxylation rate
(Vcmax ) observed in three leaves of
each tree on each observation day,
against leaf temperature. Circles indicate mean values for three leaves (䊊 =
expanding leaves; 䊉 = mature leaves;
and 䊉 = old leaves). Error bars are ±
1 standard deviation.
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1178
KOSUGI AND MATSUO
ences in the slope m on each observation day. A time series for
m (optimized for each tree species and each observation day)
against volumetric soil water content is shown in Figure 5. The
value of m was large during the leaf expansion period and then
gradually settled into a narrow range following leaf maturation, with fluctuations in response to changes in soil water content.
Discussion
Dark respiration rate
The activation energy (ΔH a (R n )) values of three evergreen
species obtained in our analyses, based on the assumption of
one temperature dependence curve for most of the year, were
in the moderate range compared to previously published results (Table 2). Parameter ΔH a (R n ) of the deciduous oak was
higher than that reported in other studies listed in Table 2.
However, this difference may be unimportant, reflecting only
a lack of data at low temperatures. Mixing the effects of acclimation and physiological seasonality with the temperature dependence response curve could pose problems for the analysis
of field data. However, Falge et al. (1996) found no obvious
differences in ΔH a (R n ) for P. abies across four seasons of the
year. Xu and Baldocchi (2003) reported that the normalized
R n25 of deciduous Quercus douglasii Hook. & Arn. (blue oak)
Figure 4. Relationship between
stomatal index (Af(D)/(C s – Γ)) and
stomatal conductance observed in three
leaves of each tree, on each observation day. Circles indicate mean values
for three leaves (䊊 = expanding leaves;
䊉 = mature leaves; and 䊉 = old
leaves). Error bars are ± 1 standard deviation.
Figure 5. Time series showing changes
in stomatal coefficient m (optimized
for each tree and each observation day)
in relation to volumetric soil water
content at 0–30 cm depth.
TREE PHYSIOLOGY VOLUME 26, 2006
SEASONAL FLUCTUATIONS IN LEAF GAS EXCHANGE
1179
Table 2. Activation energies of dark respiration (ΔH a (Rd )) and maximum carboxylation rate (ΔH a (Vcmax )), and deactivation energy (ΔH d (Vcmax ))
and entropy (ΔS) of maximum carboxylation rate in mature leaves of each tree species investigated in this study and for other species reported in
the literature.
Species
ΔH a (R d )
(J mol – 1 )
Evergreen trees
Quercus glauca Thunb.
47400
Cinnamomum camphora Sieb. 48000
Castanopsis cuspidata Schottky 60000
Quercus coccifera L.
Arbutus unedo L.
Eucalyptus pauciflora
Sieber ex. A. Spreng.
Macadamia integrifolia Maiden
& Betche and Litchi chinensis
Senn.
Aristotelia serrata
Deciduous trees
Quercus serrata Thunb.
Quercus alba L. White
Acer saccharum Marsh.
Acer pseudoplatanus L.
Betula pendula Roth
Fagus sylvatica L.
Quercus petraea L. ex Liebl.
Quercus robur L.
Fraxinus excelsior L.
Juglans regia L.
Juglans regia L.
Fuchsia excorticata J.R. Forst
& G. Forst.
Conifer
Picea abies (L.) Karst.
Pinus sylvestris L.
Pinus radiata D.
ΔH a (Vcmax )
(J mol – 1 )
ΔH d (Vcmax )
(J mol – 1 )
(250000) 1
(250000) 1
(250000) 1
This study
This study
This study
600
–
–
Tenhunen et al. 1990
Harley et al. 1986
Kirschbaum and Farquhar 1984
–
–
Lloyd et al. 1995
–
–
Dungan et al. 2003
41500
22260
no data
–
–
53000
(53000) 2
26200–47400
43300
95400
38700
42000
67000
55000
74000
60800
69700
75400
67600
61100
88000
89000
109500
39100
62500–64500
32290–42580
9593–10315
75750
52550–53050
52762–45027
no data
65000
Others
Atriplex glabriuscula Edmonston (C4)
Spinach?
Spinach
Cotton
Tobacco
Mountain grassland 29 species
66405
no data
84450
46390
no data
Averaged curve
59 dataset average
7 deciduous trees
–
–
Evergreen trees (n = 7)
Deciduous trees (n = 13)
Conifers (n = 3)
–
–
–
58520
53000
116300
65330
51300–149061
Source
(600) 1
(600) 1
(600) 1
59500
54900
29100
56200
65000
59780
45000
21100
24950
36500
27950
41550
36500
37950
(84450) 4
32900
ΔS
(J K – 1 mol – 1)
250000
(204600) 3
(200000)
203000
401000
404000
175000
144000
247000
90000
265000
199500
–
(650) 4
656
645
1285
1285
559
451
778
293
851
(650) 4
–
(200000) 5
202600–203100
206083–203594
(656) 5
665–669
(650) 4
This study
Harley and Baldocchi 1995
Ninemets and Tenhunen 1997
Weber et al. 1985
Dreyer et al. 2001
Dreyer et al. 2001
Dreyer et al. 2001
Dreyer et al. 2001
Dreyer et al. 2001
Dreyer et al. 2001
Dreyer et al. 2001
Le Roux et al. 1999
Dungan et al. 2003
Falge et al. 1996
Wang et al. 1996
Walcroft et al. 1997
–
–
Badger and Collatz 1977
–
–
–
–
194800–204000
656
Farquhar et al. 1980
Jordan and Ogren 1984
Harley et al. 1992
Bernacchi et al. 2001
Wohfahrt et al. 1999
73637
67600
149252
204600
486
(650) 4
Leuning 2002
Kosugi et al. 2003
55200
65900
56100
> 220000
204000
199500
(650)4
(650) 4
(650) 4
Estimated in this study
Estimated in this study
Estimated in this study
202900
–
650
–
Values in parentheses are assumed to apply, but are not directly determined for the respective species.
1
Tenhunen et al. 1990.
2
Kirschbaum and Farquhar 1984.
3
Kosugi et al. 2003.
4
Harley et al. 1992.
5
Harley and Baldocchi 1995.
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KOSUGI AND MATSUO
remained stable through most of the growing season, except
during the leaf expansion period, suggesting that ΔH a (R n ) is
constant for several months. Wang et al. (1996) reported that
there was no significant difference in ΔH a (R n ) between ambient and elevated temperature treatments. Conversely, Dungan et al. (2003) showed that ΔH a (R n ) in Aristotelia serrata
Hook. f. (evergreen wineberry) was slightly lower in winter
than in summer, indicating that dark respiration at low temperatures was higher in leaves in winter than in mature leaves in
summer. We found no obvious hysteresis in the relationship
between temperature and R n in three evergreen broad-leaved
trees during summer and autumn (Figure 2). Dark respiration
rates increased with increasing temperatures in early spring
(March) and dropped below the temperature dependence
curve just before leaf fall in April–May (Figure 2). Consequently, we consider that expression and parameterization
based on one temperature dependence curve is acceptable for
temperate evergreen species, except during the leaf expansion
and leaf fall periods.
Seasonal fluctuations in observed R n and simulated R n (with
the parameter sets listed in Table 1) are compared in Figure 6.
At the study site, R n can safely be estimated with one set of parameters, except during the period of simultaneous leaf expansion and leaf fall in April and May in the case of the evergreen
trees and during the leaf expansion period in the case of the deciduous oak.
by Kosugi et al. (2003) from published data for seven deciduous broad-leaved tree species (67.6 kJ mol – 1 ). These
deciduous-tree values also correspond closely to results obtained for tobacco in laboratory experiments (Bernacchi et al.
2001) and are a little larger than the values we obtained for our
three evergreen species. For comparison, we derived mean
normalized temperature dependence curves based on the data
in Table 2, for seven evergreen broad-leaved trees, 13 deciduous broad-leaved trees and three conifers (Figure 7).
Leuning’s (2002) mean curve for 59 datasets and the temperature dependence curve for cotton (Harley et al. 1992) and tobacco (Bernacchi et al. 2001), which are often used as examples of typical temperature dependence of Vcmax , are also
shown in Figure 7. The entropy term (ΔS) was fixed at 650 for
simplicity because no dataset enabling precise optimization of
ΔS exists. The result of the comparison based on these limited
datasets suggests that the activation energy is lower in evergreen broad-leaved trees and conifers than in deciduous
broad-leaved trees, cotton or tobacco. This might result from
acclimation of leaves growing at low temperatures. In practice
this means that Vcmax of evergreen trees and conifers tends to be
high at low temperatures. These tendencies suggest that spe-
Maximum carboxylation rate
Mean Vcmax25 of the three evergreen trees (mean and SD of
32.5 ± 8.2) was slightly lower than mean Vcmax25 (39.9 ± 10.7)
of the four deciduous tree species investigated by Kosugi et al.
(2003). However, there were no significant differences between the Vcmax25 of the co-occurring deciduous oak and the
evergreen trees. Differences in normalized Vcmax could be associated with environmental conditions at each site. The lack of a
dataset for evergreen tree species grown under various environmental conditions and the lack of information on potential species-specific differences in the kinetic parameters of
Rubisco make it difficult to explain the differences between
our estimated Vcmax and those of previous studies.
We compared our temperature dependence curve parameters for mature leaves with those reported in previous studies
(Table 2). The ΔH a (Vcmax ) of the three evergreen species
ranged from 29.1 to 67.0 kJ mol – 1. The ΔH a (Vcmax ) of C. cuspidata was significantly lower than the values obtained for the
other two species, perhaps indicating winter acclimation. Consequently, we constructed another temperature curve based on
summer and autumn data only (June 7–October 16, 2001)
(Figure 3; gray line). Estimated ΔH a (Vcmax ) then closely approximated the results obtained for the other species
(56.2 kJ mol –1 ). With our experimental design, we could
not distinguish between the simple temperature dependence
of Rubisco activity from acclimation effects, although “apparent” temperature dependence obtained from long-term
field observations would improve prediction accuracy. The
ΔH a (Vcmax ) of the deciduous oak was optimized to 67.0 kJ
mol – 1, which is close to the value of the average curve derived
Figure 6. Comparison of seasonal fluctuations in observed and simulated dark respiration rate (R n ) based on the parameter sets in Table 1.
Values are means for three leaves. Symbols: 䊊 = previous year leaves;
䊉 = current year leaves; and 䊉 = simulated value using a constant
R n25 . Error bars are ± 1 standard deviation.
TREE PHYSIOLOGY VOLUME 26, 2006
SEASONAL FLUCTUATIONS IN LEAF GAS EXCHANGE
1181
Figure 7. Mean normalized temperature dependence curve based on the
data in Table 2 for seven evergreen
broad-leaved trees, 13 deciduous
broad-leaved trees and three conifers.
The mean curve for 59 datasets by
Leuning (2002) and the temperature
dependence curves for cotton (Harley
et al. 1992) and tobacco (Bernacchi et
al. 2001) are shown for comparison.
cies of similar life type and biome have similar temperature
dependence curves as a result of adaptation to the environmental conditions of their habitat. When there is insufficient information available to fully describe actual temperature dependence, we propose that parameters associated with an averaged
temperature dependence curve for each life style or species
(Figure 7; Table 2) can be used with relatively little error.
However, the parameters in Table 2 for conifers may result in
substantial errors because they are based on only three data
sets.
Seasonal fluctuations in observed Vcmax and simulated Vcmax
based on the parameter sets listed in Table 1 are shown in Figure 8 (29,100 was used for C. cuspidata). For the three evergreen broad-leaved trees at this site, Vcmax could be estimated
for a whole year based on a single set of parameters, except
during the periods of leaf expansion and leaf fall in April and
May. Deciduous broad-leaved trees, however, showed a postsummer decline in Vcmax at the reference temperature, as well
as differences during the leaf expansion period and both of
these fluctuations would need to be incorporated into models.
In situ field data measured in the forest canopy under natural
conditions are most reliable for revealing the exchanges in
canopy leaves and hence, represent the most suitable data for
the parameterization of leaf gas exchange models. However,
the values, range and behavior of Vcmax detected in the field
should be considered apparent rather than actual because Vcmax
is determined by Rubisco activity which is directly related to
the amount of Rubisco and leaf nitrogen content through complex mechanisms of nitrogen allocation (e.g., Field 1983, Evans 1987, Evans 1993, Hikosaka and Terashima 1995, Niinemets and Tenhunen 1997, Takashima et al. 2004). In addition,
there are many other factors that may influence Vcmax. For example, most studies investigating gas exchange parameters ignore internal (mesophyll) conductance, even though many isotope studies have determined that Cc of tree species is around
0.1 to 0.2 CO2 mol m – 2 s – 1 or lower (e.g., von Caemmerer and
Evans 1991, Loreto et al. 1992, Epron et al. 1995, Hanba et al.
1999, 2001), which means that Cc may be a major factor determining the range of apparent Vcmax for each species (Loreto
1992). The influence on apparent Vcmax and photoinhibition of
patchy stomatal closure should also be considered in some sit-
uations. We observed neither marked patchiness in stomatal
closure, which causes severe decreases in apparent Vcmax (Takanashi et al. 2006) nor depression of electron transport rate
except during the severe summer drought in 2001 (Kosugi and
Matsuo, unpublished data). To evaluate the possible influences
of internal conductance (g i ) and error in the estimation of R d
on the estimation of apparent Vcmax , we calculated seasonal
Figure 8. Comparison of seasonal fluctuations in observed and simulated maximum carboxylation rate (Vcmax ) based on the parameter sets
listed in Table 1. Values are means for three leaves. Symbols: 䊊 = previous year leaves; 䊉 = current year leaves; and 䊉 = simulated value
using a constant Vcmax25. Error bars are ± 1 standard deviation.
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1182
KOSUGI AND MATSUO
fluctuations in Vcmax by several methods (Figure 9). The possible influence of the error in the estimation of R d is shown on
the left side of Figure 9. There were differences between apparent Vcmax calculated by Equation 3 and calculated assuming
that R d = R n and this assumption has been questioned in several other studies (e.g., Brooks and Farquhar 1985, Kirschbaum and Farquhar 1987, Villar et al.1994, 1995). The differences in apparent Vcmax were smaller when it was assumed that
R d = 0.5R n (e.g., Niinemets and Tenhunen1997). In several
other studies reporting R d derived from the A–C i curve and
where R n was measured in a dark chamber (e.g., Harley et al.
1992, Dungan et al. 2003), it was suggested that a scaling ratio
of about 0.5 or lower is adequate. The possible influence of gi
was quite large as shown on the right side of Figure 9 (cf.
Loreto et al. 1992). Values of gi of ~ 0.1 CO2 mol m – 2 s – 1 were
reported for several Japanese evergreen (Hanba et al. 1999)
and deciduous (Hanba et al. 2001) broad-leaved tree species.
Although Vcmax is generally calculated assuming that g i = ∞.
The possible influence of changing g i with leaf age might be
important in our study because lower values of g i have been reported for both expanding leaves (Hanba et al. 2001) and old
leaves (Loreto et al. 1994). However, Figure 9 shows that differences in g i associated with leaf age within the range reported by Hanba et al. (2001) do not explain the low Vcmax during leaf expansion and leaf fall.
Stomatal conductance
Figure 10 shows seasonal fluctuations in parameter m compared with the constant values optimized for each tree. Parameter m has a significant physiological meaning related to
intrinsic water-use efficiency, indicating species-dependent
Figure 10. Comparison of seasonal fluctuations in observed and constant stomatal coefficient (m) (䊊 = previous-year leaves; 䊉 = current-year leaves; and 䊉 = simulated values).
Figure 9. Effects of daytime
respiration rate (R d ) and internal conductance (g i ) on the estimation of “apparent” maximum carboxylation rate
(Vcmax ). Seasonal fluctuations
in Vcmax calculated by several
methods are shown. Left side:
䊉 = Vcmax estimated with R d =
Equation 3; 䊉 = R d = R n; and
䊊 = R d = 0.5R n. Right side:
䊉 = g i = ∞; 䊉 = g i = 0.2
CO2 mol m –2 s –1; and 䊊 =
gi = 0.1 CO2 mol m –2 s –1.
TREE PHYSIOLOGY VOLUME 26, 2006
SEASONAL FLUCTUATIONS IN LEAF GAS EXCHANGE
regulation of water fluxes; slight fluctuations in parameter m
are therefore important. Some studies have reported that m decreases in response to drought (Sala and Tenhunen 1996) and
in old trees (Falge et al. 1996). The evidence suggests that different m values should be applied during periods of leaf expansion and during drought in the long-term simulation of gas exchange for all of our study species.
Conclusions
Seasonal fluctuations in three major leaf gas exchange parameters (R n , Vcmax and m) were investigated in co-occurring evergreen and a deciduous tree species in a temperate broad-leaved
forest. For the three evergreen trees, one set of the parameters
Vcmax25 and R n25 and temperature dependence curves satisfactorily estimated fluctuations in gas exchange throughout the
year, except during the period of simultaneous leaf fall and leaf
expansion in April and May. In the deciduous oak, post-summer declines in Vcmax25 were observed as well as changes in
Vcmax25 and R n25 during the leaf expansion period. The period
of leaf expansion, when leaf gas exchange characteristics differ from those of mature leaves, was shorter in the deciduous
oak than in the evergreen species. The temperature dependence of the activation energy of Vcmax was investigated using
both our data and data from previously published studies and
was found to be smaller in evergreen broad-leaved trees than in
deciduous broad-leaved trees. For all of our study species, the
difference in m should be considered during periods of leaf expansion and drought. Canopy-scale flux observations at this
site demonstrated changes in the photosynthetic ability and
stomatal behavior characteristics of the whole canopy during
periods of leaf expansion and drought (Kosugi et al. 2005).
These results strongly suggest that the changes in the normalized gas exchange parameters, and thus, the impact of leaf
physiology on seasonal fluctuations in gas exchange, should
be incorporated in models of carbon uptake of evergreen
broad-leaved forests.
Acknowledgments
We thank the Kansai Electric Power Co. and Kansai Environmental
Engineering Co. (KANSO) for help with our field observation at
Akou Power Station. We also thank Dr. Tsunahide Shidei, Dr. Makoto
Tani and Dr. Shozo Shibata for their support with the project on this
site and Ms. Motoko Higuchi, Dr. Satoru Takanashi, Dr. Hiroki
Tanaka, Ms. Noriko Hama and Dr. Nobuhito Ohte for collecting field
data.
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