Research
Leaf lifespan and lifetime carbon balance of individual
leaves in a stand of an annual herb, Xanthium canadense
Blackwell Publishing Ltd
Shimpei Oikawa, Kouki Hikosaka and Tadaki Hirose
Graduate School of Life Sciences, Tohoku University, 6 – 3 Aoba, Sendai 980–8578, Japan
Summary
Author for correspondence:
Shimpei Oikawa
Tel: +81 22 7956698
Fax: +81 22 7956699
Email: [email protected]
Received: 6 March 2006
Accepted: 8 May 2006
• Leaf lifespan in response to resource availability has been documented in many
studies, but it still remains uncertain what determines the timing of leaf shedding.
Here, we evaluate the lifetime carbon (C) balance of a leaf in a canopy as influenced
by nitrogen (N) availability.
• Stands of Xanthium canadense were established with high-nitrogen (HN) and
low-nitrogen (LN) treatments and temporal changes of C gain of individual leaves
were investigated with a canopy photosynthesis model.
• Daily C gain of a leaf was maximal early in its development and subsequently
declined. Daily C gain at shedding was nearly zero in HN, while it was still positive
in LN. Sensitivity analyses showed that the decline in the daily C gain resulted
primarily from the reduction in light level in HN and by the reduction in leaf N in LN.
Smaller leaf size in LN than in HN led to higher light levels in the canopy, which
helped leaves of the LN stand maintain for a longer period.
• These results suggest that the mechanism by which leaf lifespan is determined
changes depending on the availability of the resource that is most limiting to plant
growth.
Key words: leaf longevity, photosynthesis, respiration, leaf nitrogen, light availability, leaf construction cost, sensitivity analysis.
New Phytologist (2006) 172: 104–116
© The Authors (2006). Journal compilation © New Phytologist (2006)
doi: 10.1111/j.1469-8137.2006.01813.x
Introduction
Leaf lifespan has been discussed in relation to carbon (C)
balance, defined as photosynthetic C gain minus respiratory
C loss for constructing and maintaining leaves (Chabot &
Hicks, 1982). Many studies have shown that leaf lifespan of
species growing at low nitrogen ( N) availabilities is longer
than that of species growing at higher N availabilities
(Monk, 1966; Moore, 1980; Aerts & Chapin, 2000).
Instantaneous C gain is generally high in species growing at
high N availabilities ( Wright et al., 2001; Osone & Tateno,
2005) and it is inversely correlated with leaf lifespan (Reich
et al., 1999; Hikosaka & Hirose, 2000; Wright et al., 2004).
Owing to the inverse correlation, lifetime C balance of a leaf
was comparable for species growing at low and high N
availabilities (Mediavilla & Escudero, 2003). Also, in a single
species, leaf lifespan was longer at lower N availabilities
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(Noble et al., 1979; Reader, 1980; Shaver, 1983; Aerts, 1989;
Ackerly & Bazzaz, 1995; Cordell et al., 2001; Reich et al.,
2004). But other studies showed that it was shorter at low
than at high N availabilities (Turner & Olson, 1976; Bazzaz
& Harper, 1977) or was not significantly different among
environmental conditions (Aerts & de Caluwe, 1995).
Carbon gain of a leaf is usually highest at full leaf expansion and then declines to the end of the lifespan as the leaf is
shaded by new leaves that are produced overhead (Mooney &
Gulmon, 1982; Kikuzawa, 2003). The leaf may be shed when the
light intensity reaches the compensation point of photosynthesis
(Monsi & Saeki, 1953). In some fast-growing pioneer trees, the
daily photosynthetic rate of the leaves at shedding was not
significantly different from zero (Ackerly, 1999). However, in
Ipomoea vines, the N content of old leaves decreased at low N
supply even when they received full sunlight (Hikosaka et al.,
1994). Thus, old leaves may be shed even when they receive
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relatively high irradiance with which they can attain a positive
C gain. This may be caused by N retranslocation from old
leaves to meet N demand in new leaf growth (Ono et al., 1996).
In monospecific stands of an annual herb, Xanthium
canadense, the turnover rate of leaves was faster in a high-(HN)
than a low-(LN) N availability, i.e. the leaf lifespan was longer
in the LN than the HN stand (Oikawa et al., 2005). Nitrogen
content per unit leaf area of a fully expanded leaf tended to be
lower in the LN than the HN stand. The instantaneous C
gain of a leaf might be lower in the LN than the HN stand
since leaf N content is positively correlated with photosynthetic rate (Field & Mooney, 1986; Evans, 1989). Thus we may
hypothesize that the lower instantaneous C gain is compensated
by a longer leaf lifespan in the LN stand. In the present study,
we address the following questions: (1) To what extent is C gain
of a leaf in the LN stand compensated by the longer leaf lifespan?
(2) Is the C gain zero in the leaf that is going to be shed under
LN and HN conditions? (3) How do light and N availability
influence the decline in C gain with leaf age? We applied a
canopy photosynthesis model (Hirose & Werger, 1987b) to
estimate the daily C gain of individual leaves from emergence
to shedding in stands of X. canadense. The influences of light
and N on C gain were evaluated with a sensitivity analysis.
(LI-185; Li-Cor, Lincoln, NE, USA) and recorded at 1-min
intervals with a data-logger (LI-1000; Li-Cor). Air temperature at the study site was measured with copper-constantan
thermocouples and recorded at 30-min intervals with a datalogger (Thermodac-EF, Eto Denki, Tokyo, Japan). PPFD was
low from late June to mid-July and mid- to late August
caused by high rainfall and dense cloud cover that obstructed
light in these periods. Mean daily air temperature was
13.7°C in May, 17.9°C in June, 23.1°C in July and 24.1°C
in August.
Materials and Methods
A L = 1.17 + 0.62 × L ×W
Growth conditions
The study was conducted at the experimental garden of
Tohoku University, Sendai, Japan (38°30 ′ N, 140°57 ′ E).
Xanthium canadense Mill. has an erect growth habit and often
forms dense monospecific stands (Anten & Hirose, 1998).
Seeds were collected from plants growing in the experimental
garden. They were germinated in a Petri dish with water and
seedlings were transplanted into plastic pots filled with
washed river sand (depth 20 cm, diameter 13 cm) on 22 May
2002. These pots were arranged tightly (59.2 plants m−2
ground area) to establish two stands with HN and LN
treatments. A total of 150 pots were allotted to each stand.
Both stands were enclosed by shade-cloth with 70% light
transmission to reduce solar radiation penetrating the sides of
the stands. The top of the shade-cloth was elevated to track
height growth. Each pot was supplied with 0.35 (HN) or
0.10 ml (LN) HYPONeX (5% nitrogen with other nutrients
being contained proportionately; HYPONeX Japan, Osaka,
Japan) at 10-d intervals (2.98 mg N per pot d−1 in HN and
0.85 mg N per pot d−1 in LN). Water was added every day.
Pots in each stand were rotated every 10 d. The experiment
continued until the onset of flowering (31 August 2002).
Microclimate
Photosynthetic photon flux density (PPFD; µmol photons
m−2 s−1) above the canopy was measured with a point sensor
Canopy structure and light climate
Nine plants were selected randomly in each stand for nondestructive monitoring of the area of individual leaves from
emergence to death at c. 10-d intervals. Leaf emergence was
defined at the time when the leaf length reached to 2 cm.
Numbered tags were placed around the petioles to identify the
time of leaf emergence. Leaf death was defined as the time
when > 90% of the surface area browned. Leaf lifespan was
determined as the difference between the day of emergence
and of death. Leaf area (A L, in cm2) was estimated with the
following regression equation:
(n = 222, r 2 = 0.98, P < 0.0001)
Eqn 1
(L is the leaf length in cm; W the leaf width in cm). This
equation was obtained from destructive sampling of plants
different from those for nondestructive monitoring. Leaf
position as a depth from the canopy top (h) was measured for
all leaves from emergence to death at c. 10-d intervals.
Vertical distribution of PPFD in the canopy was determined on 12 July, 20 July, 28 July and 11 August. The PPFD
on a horizontal plane within the canopy was measured at 10cm intervals from ground level with a line sensor (AccuPAR
Linear PAR Ceptometer, Model PAR-80; Decagon Devices,
Inc., Pullman, WA, USA). Relative PPFD was calculated
against reference PPFD measured on a horizontal plane above
the canopy with a point sensor (LI-185; Li-Cor), which was
calibrated with the line sensor.
Leaf gas exchange and construction cost
Photosynthesis and dark respiration were measured with a
portable photosynthetic measurement system (LI-6400; LiCor) on 29 June, 30 July and 30 August in 2002. For the
measurements of photosynthetic rate, PPFD at the leaf
surface was reduced in 10 steps (2000, 1500, 1000, 500, 200,
100, 50, 20, 10 and 0 µmol photons m−2 s−1). Leaf temperature was set at the mean day temperature in June (25.1°C),
July (27.3°C) and August (23.5°C) observed from 1999 to
2001 at the study site. Dark respiration rate was measured
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org
New Phytologist (2006) 172: 104–116
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3 h after sunset. Leaf temperature was set at the mean night
temperature in June (16.9°C), July (21.2°C) and August
(19.5°C). After measurements, the leaf portion included in
the chamber (2 cm × 3 cm) was separated, and dried in an
oven at 70°C for 48 h. Nitrogen content was determined with
an NC analyser (Sumigraph NC-900; Sumika-Bunseki
Center, Osaka, Japan).
Four plants were harvested in each stand at c. 10-d intervals. Leaves were separated from other organs and dry mass
and N content per unit leaf mass (Nmass) were determined for
every leaf after drying in an oven at 70°C for 48 h. Heat of
combustion per unit leaf mass (Hmass) was determined with a
calorimeter (CA-4PJ; Shimadzu Corporation, Tokyo, Japan),
and ash content per unit mass (Amass) was determined with a
muffle furnace (Model FA-21; Yamato, Himeji, Japan). Leaf
construction cost per unit leaf mass (Cmass; glucose equivalent,
g glucose g−1), defined as the amount of glucose needed for C
skeletons, reductant and ATP to synthesize the leaf tissues was
estimated for fully expanded leaves after Williams et al.
(1987):
C mass = [(0.06968H mass − 0.065)(1 − A mass)
+ (kN mass /14.0067)(180.15/24)]/0.89
Eqn 2
(Nmass is organic N per unit mass; k is the oxidation state of
N (5 for nitrate N and −3 for ammonium N)). As the major
form of applied N was ammonium, we calculated the
construction cost on k = −3. We used total N for Nmass
because no accumulation of nitrate was found in leaves
developed on soils with little nitrate (Oikawa et al., 2004). For
the measurement of Cmass, we used the leaf that attained a
maximum leaf area. Leaf construction cost per unit leaf area
(Carea) was calculated as the product of Cmass and leaf dry mass
per unit leaf area (LMA).
Model
Distribution of PPFD within the canopy was described by
Beer’s law (Monsi & Saeki, 1953):
I = I 0 exp(−K LF h)
Eqn 3
(I is PPFD within the canopy on a horizontal plane at depth
h; I 0 is PPFD above the canopy; K L is the light extinction
coefficient; F h is the leaf area cumulated from top of the
canopy to depth h). The mean PPFD incident on a leaf at
depth h (IL) is:
IL =
I 0K L
exp(−K L F h )
1 − tL
Eqn 4
(t L is the transmission coefficient of the leaf; Saeki, 1960).
For Fh, values obtained from the study plants were used. K L
New Phytologist (2006) 172: 104–116
was estimated from the slope in the linear regression of logtransformed relative PPFD (I/I 0) against the total cumulative
leaf area (F h). t L was assumed to be 0.086 (Hirose & Werger,
1987b).
A nonrectangular hyperbola was used to fit the light
response curve of net leaf photosynthesis per unit leaf area
(Pn) (Hirose & Werger, 1987a).
Pn =
[ϕI L + Pmax − {(ϕI L + Pmax )2 − 4ϕθI L Pmax }0.5 ]
− Rd
2θ
Eqn 5
(Pmax is the light-saturated photosynthetic rate per unit leaf
area; ϕ is the initial slope of the curve; θ is the curvature factor;
R d is the dark respiration rate per unit leaf area). Pma x , ϕ, θ
and R d are assumed to be a linear function of the N content
per unit leaf area (Narea) (Hirose & Werger, 1987a).
Pmax = am + bmNarea
ϕ = ap + bpNarea
θ = at + btNarea
Eqn 6
Rd = ar + brNarea
(a and b are regression coefficients) We determined
coefficients every month, assuming that coefficients were
constant across the HN and the LN treatments.
Daily C gain is cumulative daytime photosynthesis minus
cumulative night-time dark respiration. It was calculated with
IL monitored every minute and Narea obtained from the plants
for harvest. Narea was assumed to be constant between successive harvests.
The lifetime C balance per unit leaf area (EB) was defined
as:
EB = EG − EC
Eqn 7
(EG is the lifetime C gain (i.e. daily C gain cumulated from
emergence to shedding); EC is the CO2 equivalent of Carea).
EG was calculated with the seasonal course of I 0 and Narea of
the leaves harvested at c. 10-d intervals. EC is converted from
Carea, assuming that all substrates for respiration are glucose.
Statistics
Data on leaf lifespan and daily C gain were analysed with a
split-plot analysis of variance (ANOVA) with the N treatment as
a main effect and the leaf order as a split-plot effect. Simple
linear regression was used to test for the relationships between
leaf area cumulated from the canopy top and the relative
PPFD after log-transformation, and for the relationships
between leaf N content (Narea) and photosynthetic characteristics (Pmax, ϕ, θ and R d). A Mann–Whitney U-test was
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Table 1 Summary of linear regressions for the relationships between
light-saturated photosynthetic rate (Pmax), initial slope of the light
response curve (ϕ), curvature factor (θ), dark respiration rate (Rd) of
light response curve of photosynthesis and leaf nitrogen content per
unit area (Narea)
Date of measurements Relationship
June 29
July 30
Fig. 1 Lifespan of Xanthium canadense leaves with different leaf
order (numbered from the earliest) in the high-nitrogen (HN, squares)
and the low-nitrogen (LN, circles) stands. Each point represents the
mean from nine plants in the each stand and bars represents ± 1 SE.
used to test whether leaf construction cost was significantly
different between N treatments. The difference in Pmax, ϕ, θ
and R d between months and between N treatments was
examined with a multiple analysis of covariance (MANCOVA)
using Narea as the covariate. The difference in lifetime C
balance between the two N treatments was examined with an
analysis of covariance (ANCOVA), using mean leaf lifespan as
the covariate. These calculations were performed with R (R
Development Core Team, 2006).
Results
Plants increased their height without lateral branch formation during the experimental period. At the end of the
experiment (31 August), the height was 168 ± 3 cm in HN
and 86 ± 2 cm in LN. Leaves were produced continuously at
the top of the stem through the experimental period, with a
mean production rate of 0.22 leaves d−1 in HN and
0.19 leaves d−1 in LN (Oikawa et al., 2005). Leaf shedding
started in mid-July and continued through to the end of the
experiment, with a mean loss rate of 0.15 leaves d−1 in HN
and 0.11 leaves d−1 in LN. Leaf lifespan was significantly
longer in LN than in HN (Fig. 1). It tended to be shorter in
leaves emerging later (i.e. leaves with a higher leaf order)
than those emerging earlier particularly in HN but the
interaction between the N treatment and the leaf order was
not significant.
The relationships between the vertical distribution of relative PPFD (I/I0) in the canopy and the total cumulative leaf
area (F h) showed no significant difference among measurements. An average value of light extinction coefficient
(K L = 0.89) was applied to all estimations of the seasonal
course of the mean PPFD incident on a leaf (I L, Eqn 4). The
IL of a leaf was high in the early stage of its lifespan and
declined with growth of new leaves through the lifespan in
August 30
Pmax = 6.1 + 16.4 × Narea
ϕ = 0.04 + 0.007 × Narea
θ = 0.96 − 0.09 × Narea
Rd = 0.68 + 0.86 × Narea
Pmax = − 5.2 + 26.0 × Narea
ϕ = 0.03 + 0.012 × Narea
θ = 0.95 − 0.11 × Narea
Rd = 0.42 + 0.73 × Narea
Pmax = − 0.6 + 15.0 × Narea
ϕ = 0.04 + 0.001 × Narea
θ = 0.94 − 0.08 × Narea
Rd = 0.08 + 0.33 × Narea
r2
P
0.38
0.13
0.2
0.18
0.89
0.28
0.2
0.35
0.79
0.01
0.31
0.51
< 0.001
0.07
< 0.05
< 0.05
< 0.001
< 0.01
< 0.01
< 0.001
< 0.001
0.73
< 0.01
< 0.001
Data from the high-nitrogen (HN) and the low-nitrogen (LN)
stands were pooled.
both stands (Fig. 2). When leaves of the same order were compared, IL was similar between the two stands in the early stage
of its lifespan, while in the late stage, it was lower in HN than
in LN, especially in leaves emerging later.
Leaf N per unit leaf area (Narea) was high in the earliest stage
of the lifespan and declined in the later stage in both stands
(Fig. 3). Narea was slightly higher in HN than in LN at full leaf
expansion and was not significantly different at preshedding.
The light-saturated photosynthetic rate (Pmax) was positively correlated with Narea (Table 1). The slope was significantly different between months (P < 0.01) and Pmax at a
common Narea tended to be lower in August than in June and
July. The initial slope of light-photosynthesis curve (ϕ) was
positively correlated with Narea in July but it was independent
of Narea in June and August (Table 1). The slope was significantly different between months (P < 0.05). The curvature
factor (θ) was negatively correlated with Narea (Table 1) and
the intercept was significantly different between months
(P < 0.01). The dark respiration rate (R d) was positively
related to Narea (Table 1). The intercept was significantly
different between months (P < 0.01). Rd at a common Narea
decreased through the season. The slope of all regressions
was not significantly different between N treatments. The
relationships measured in June, July and August were used to
calculate Pn in May to June, July and August, respectively
(Eqn 5). Since ϕ was independent of Narea in June and August,
the averaged values (0.05 and 0.04 mol CO2 mol−1 photons,
respectively) were used in calculating Pn. In these measurements, the leaves from various orders (Leaf Order 1–20) with
different ages were used to obtain a wide variation in Narea.
The leaves that were shed before the onset of flowering (Leaf
Order 1–10) were used for further analysis.
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Fig. 2 Seasonal course of daily
photosynthetic photon flux density (PPFD)
incident on each Xanthium canadense leaf (IL)
with different leaf order (numbered from the
earliest) from emergence to shedding in the
high-nitrogen (HN, left panels) and the
low-nitrogen (LN, right panels) stands.
Daily C gain of a leaf was higher in the early stage of
the lifespan (Fig. 4), owing to higher IL (Fig. 2) and higher
Narea (Fig. 3). In the early stage, it was slightly higher in HN
than in LN. In the late stage of the lifespan, a high C gain was
attained on sunny days, when high PPFD penetrated into
New Phytologist (2006) 172: 104–116
lower layers in the canopy. The daily C gain of a leaf at
preshedding was around zero in the HN stand, whereas it
was higher than zero in the LN stand. The daily C gain averaged
over the later part of the lifespan was significantly higher in
the LN than the HN stand (P < 0.01).
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Fig. 3 Seasonal course of nitrogen content
per unit area (Narea) of Xanthium canadense
leaves with different leaf order from emergence to shedding in the high-nitrogen (HN,
left panels) and the low-nitrogen (LN, right
panels) stand. Data are mean ± 1 SE.
Leaf construction cost per unit leaf mass (Cmass) was significantly higher in the HN than the LN stand (Fig. 5a; P < 0.01).
Leaf construction cost per unit leaf area (Carea) tended to be higher
in the LN than the HN stand, although the difference was not
statistically significant (Fig. 5b; P = 0.11). The higher Carea in the
LN stand was caused by the higher LMA (Oikawa et al., 2005).
Owing to the cost for leaf construction, C balance of a leaf
(i.e. C gain minus leaf construction cost; Eqn 7) expressed on
a leaf-area basis was negative at emergence (Fig. 6a,b). The
rate of C gain was high in the early stage of its lifespan and the
construction cost was amortized within 4 d. Cumulative C
balance levelled off by the time of leaf shedding in the HN
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New Phytologist (2006) 172: 104–116
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Fig. 4 Seasonal course of daily carbon gain of
Xanthium canadense leaves with different
leaf order from emergence through shedding
in the high-nitrogen (HN, left panels) and the
low-nitrogen (LN, right panels) stands.
stand, while it continued to increase through to the end of
lifespan in the LN stand. Lifetime C balance expressed on a
leaf-area basis was higher in LN than in HN when compared
at a common leaf order. However, as the surface area of
individual leaves was larger in HN than in LN, especially in
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leaves emerging later in the growing season (Oikawa et al.,
2005), the lifetime C balance was greater in HN than in LN
when expressed on a single-leaf basis (Table 2).
Lifetime C gain per unit leaf area was positively correlated
with leaf lifespan (Fig. 7). The slope and intercept were not
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incident PPFD or Narea being kept constant at the initial values
(i.e. no decline in PPFD or Narea during the lifespan was assumed).
In the HN stand, if no decline in the relative PPFD was
assumed while Narea declined according to the pattern shown
in Fig. 3, the cumulative C balance of a leaf did not level off
in the late stage (Fig. 8a). The reduction in Narea had a small
effect on net daily C gain because Rd as well as Pmax decreased
with reduction in Narea. On the other hand, if no reduction in
Narea was assumed while PPFD decreased according to the
pattern in Fig. 2, the decline in the rate of C gain was similar
to the observed pattern. In contrast, the effects of PPFD and
Narea were reversed in the LN stand. If no reduction in Narea
was assumed with change in PPFD, the cumulative C gain
continued to increase, maintaining nearly the same slope as in
the earlier stage (Fig. 8b). Constant PPFD also increased daily
C gain, but to a smaller extent. Thus, N rather than light availability was more limiting to C gain of leaves in the LN stand.
Discussion
Fig. 5 (a) Leaf construction cost per unit leaf mass (Cmass) and (b) per
unit leaf area (Carea) of fully expanded Xanthium canadense leaves
with different leaf order in the high-nitrogen (HN, squares) and the
low-nitrogen (LN, circles) stands. The CO2 equivalent values
corresponding to glucose are given on the right y-axis of (b).
significantly different between treatments (P = 0.53 and
P = 0.26, respectively). In both stands, the leaves emerging
later had a lower lifetime C balance and a shorter leaf lifespan
than those emerging earlier.
The influence of light and N on C gain was evaluated with
a sensitivity analysis. The C balance of a leaf was calculated with
Leaf N content and photosynthetic capacity were lower in the
LN than the HN stand. However, smaller leaf area production
in the LN than the HN stand led to a lower rate of light
attenuation and thus greater light interception by leaves in the
late stage of the lifespan. This enabled the leaves in the LN
stand to assimilate C for a longer period and the leaves
achieved a higher lifetime C balance on a leaf-area basis.
There was a positive correlation between leaf lifespan
and lifetime C balance. Such positive correlation has been
reported in alpine herbs (Diemer & Körner, 1996) and in
tropical trees (Hiremath, 2000), whereas no correlation was
found in Mediterranean trees (Mediavilla & Escudero, 2003).
Our results supported the hypothesis that a longer leaf
lifespan is important for C gain of plants growing in infertile
soils (Orians & Solbrig, 1977; Chabot & Hicks, 1982; Kikuzawa, 1991; Reich et al., 1992). However, some studies
showed that within a species, leaf lifespan was shorter at low
than at high N availabilities (Turner & Olson, 1976; Bazzaz
& Harper, 1977). With a mathematical model, Hikosaka
Fig. 6 Seasonal course of cumulative carbon
balance of Xanthium canadense leaves with
different leaf order from emergence through
shedding in (a) the high-nitrogen (HN) and
(b) the low-nitrogen (LN) stands. Numbers
next to the lines indicate the leaf order.
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New Phytologist (2006) 172: 104–116
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Fig. 7 Lifetime carbon balance per unit leaf area as a function of leaf
lifespan. Closed squares and circles, respectively, early (leaf order
1–5) and late Xanthium canadense leaves (leaf order 6–10) in the
high-nitrogen (HN) stand; open squares and circles, respectively, early
and late leaves in the low-nitrogen (LN) stand.
(2003) examined the responses of leaf lifespan to changes in
environmental factors such as light and N. The model predicted that leaf lifespan is elongated when the plant is exposed
to chronic N deficiency while it is decreased when exposed to
a sudden decrease in N availability.
The elongation of leaf lifespan with higher incident PPFD
in the LN stand resulted in a greater C gain on a leaf-area basis
than that in the HN stand. However, leaves were smaller in
the LN than the HN stand (Table 2). When compared on a
single-leaf basis, lifetime C gain was higher in the HN than
the LN stand (Table 2). Whole-plant C gain was strongly
constrained by the limited leaf area production when N availability was low, but the limited leaf area was compensated by
the low rate of light attenuation (i.e. the high incident PPFD)
and longer leaf lifespan. Conversely, when N availability was
high, whole-plant C gain was more limited by light.
The lifetime C balance per unit leaf area was smaller in
leaves emerging later than those emerging earlier in both
stands (Fig. 6). There are several possible explanations for the
difference. First, PPFD incident on the stands was lower in
the period during which the late leaves were produced. Second, N content (Narea) of the late leaves at full expansion was
lower than that of the early leaves (Fig. 3). Third, the photosynthetic rate per unit leaf N was lower in the period
(Table 1). This is discussed in detail later. Fourth, leaf lifespan
was shorter in the later than the early leaves (Fig. 1). The surface area was much larger in the later than the early leaves in
each stand (Table 2), leading to the greater mutual shading
with the higher rate of light attenuation in the later leaves.
Owing to the larger surface area, the lifetime C balance on a
single-leaf basis was higher in the later than the early leaves
(Table 2).
In the HN stand, the daily C gain at shedding was around
zero (Fig. 4). Even if the leaf continued to live longer, it would
not contribute to growth of the plant. This result supports the
hypothesis that the leaf will be shed at the time when it
attained the maximum lifetime C balance. Near-zero C gain
at shedding was also observed in pioneer tree species with
continuous leaf production (Ackerly, 1999). Our sensitivity
analysis demonstrated that the decline in daily C gain was
caused primarily by the decline in incident PPFD rather than
in N content of the leaf (Fig. 8a). The rate of leaf area production and the LAI (total leaf area per unit ground area) in these
stands were high in HN (Oikawa et al., 2005), leading to a
large decline in light climate in the HN stand (Fig. 2). Owing
to the decline in incident PPFD (Fig. 2) as well as in Narea
(Fig. 3), the daily C gain decreased faster in the HN stand
(Fig. 4). Thus, leaves were shed when they were unable to
attain a positive C gain.
In the LN stand, incident PPFD at shedding was higher
than that of the leaves in HN (Fig. 2) and daily C gain maintained positive values until shedding (Fig. 4). A positive daily
C gain at shedding as well as a relatively higher incident PPFD
(20–30% of full sunlight) was also found in a stand of Helianthus annuus (Kobayashi, 1975). Why were those leaves shed
even when they had a positive daily C gain? The sensitivity
analysis showed that in the LN stand the decline in C gain of
a leaf was caused mainly by the decline in Narea, rather than in
the light climate of the leaf (Fig. 8b). One possible explanation
Fig. 8 Sensitivity analysis. Cumulative carbon
(C) balance was calculated by keeping leaf
nitrogen content per unit area (Narea) constant
with actual photosynthetic photon flux
density (PPFD) received by a Xanthium
canadense leaf (IL) (broken line) or by keeping
IL constant with actual Narea (dotted line).
Solid line indicates the actual cumulative C
balance. Examples of leaf order 6 in (a) the
high-nitrogen (HN) and (b) the low-nitrogen
(LN, b) stands are shown.
New Phytologist (2006) 172: 104–116
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Research
Table 2 Lifetime carbon balance of leaves with different leaf order (numbered from the earliest) in the high- (HN) and the low nitrogen (LN) stand
Lifetime carbon gain
(a)
Construction cost
(b)
(mol CO2 leaf–1)
Lifetime carbon balance
(a) – (b)
0.00046
0.00080
0.00118
0.00262
0.00340
0.00685
0.00697
0.00853
0.00948
0.00980
0.0107
0.0124
0.0275
0.0323
0.0413
0.0457
0.0435
0.0582
0.0596
0.0815
0.0014
0.0015
0.0041
0.0054
0.0077
0.0099
0.0076
0.0087
0.0096
0.0129
0.0093
0.0109
0.0234
0.0269
0.0337
0.0358
0.0359
0.0495
0.0500
0.0686
0.00040
0.00069
0.00091
0.00178
0.00285
0.00337
0.00512
0.00528
0.00579
0.00645
0.0097
0.0100
0.0222
0.0298
0.0245
0.0394
0.0406
0.0491
0.0580
0.0617
0.0010
0.0011
0.0026
0.0037
0.0045
0.0066
0.0056
0.0059
0.0061
0.0079
0.0087
0.0089
0.0196
0.0260
0.0200
0.0328
0.0350
0.0432
0.0519
0.0538
Nitrogen
treatment
Leaf
order
Size of fully expanded
leaves (m2 leaf–1)
HN
1
2
3
4
5
6
7
8
9
10
LN
1
2
3
4
5
6
7
8
9
10
is that N demand for new leaf growth caused N retranslocation before old leaves were heavily shaded (Oikawa et al.,
2005). It has been reported that N demand in sink organs
such as new leaves, stems and the reproductive part causes
senescence of old leaves (Thomas & Stoddart, 1980; Wittenbach, 1983; Hikosaka, 2005a; Hirose et al., 2005; Milla et al.,
2005). Retranslocation of N from older to new leaves would
maximize whole-canopy C gain. The optimal LAI that maximizes C gain of the canopy is small when N in the canopy
is limited (Anten et al., 1995; Hirose et al., 1997). This is
because an increase in leaf area with constant canopy-level N
dilutes N in individual leaves, leading to a decrease in photosynthetic rate (Hirose, 1984). Thus, leaves in the lowest layer
might be shed even when they receive an irradiance much
higher than the light compensation point of photosynthesis.
In our calculation of lifetime C gain, K L was assumed to be
constant in the leaf canopy. K L depends on the leaf angle such
that a larger leaf angle from the horizontal plane lowers K L
(Monsi & Saeki, 1953). If leaves were more vertical in the
upper part of the canopy, C gain would have been overestimated when leaves were young and underestimated when
leaves were old in the lower part of the canopy. Also, it was
assumed that PPFD at a given height in the canopy consisted
of diffuse light that had a horizontally uniform distribution.
On sunny days, however, some leaf areas receive diffuse light
and direct light that penetrates into the canopy (i.e. sunfleck)
while others receive diffuse light only. Spitters (1986) compared the daily C gain calculated by assuming that PPFD consisted of diffuse light only, with that calculated by assuming
that PPFD incident on leaves at a given height consisted of
direct and diffuse light. He showed that daily C gain was
slightly higher (on average, 4%) when all light was assumed to
be diffuse. This overestimation resulted from the shape of the
light–photosynthesis relationship: since photosynthetic rates
increase with increasing light with diminishing returns, the
photosynthetic rate estimated by the averaged light intensity
is higher than that estimated by high and low light intensity.
In his calculation, Spitters (1986) assumed that light-saturated
photosynthesis of individual leaves was the same among leaves
in the canopy. This assumption could cause an overestimation
of canopy C gain by up to 20% (Anten, 1997). In addition,
the fraction of direct light incident on leaves at shedding is
smaller because these leaves were located at the bottom of the
canopy where most light has been scattered. Therefore, our
assumption about the distribution of incident light should
have small effects on the estimation of C gain.
Our calculations of lifetime C gain assumed no decline in
photosynthesis resulting from water deficiency. It has been
shown that the decreased water supply from the soil and the
increased vapour pressure deficit between the leaf and the air
can cause mid-day depressions of photosynthesis (Bates &
Hall, 1982; Jones & Muthuri, 1984; Kikuzawa, 2004). However, no reduction in leaf conductance under high light intensity was found throughout the measurements of photosynthesis
(data not shown), probably owing to sufficient water supplies.
Thus, our assumption of no mid-day depression is unlikely to
affect the estimation of C gain significantly.
The light-saturated photosynthetic rate (Pmax), initial slope
(ϕ), curvature factor (θ) and dark respiration rate (Rd) were
linear functions of leaf N content per unit leaf area (Narea)
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org
New Phytologist (2006) 172: 104–116
113
114 Research
except for ϕ in June and August (Table 1). The Pmax at a given
Narea was lower in August than in June and July. Decline in
Pmax with time at a given Narea has been reported in Solidago
altissima (Schieving et al., 1992) and in Oryza sativa (Borjigidai et al. 2006). The maximum rate of carboxylation and the
maximum rate of electron transport that regulate photosynthetic rates also declined with time at a given Narea (Wilson
et al., 2000; Dungan et al., 2003). These differences might be
caused by a change in N allocation in a leaf (Wilson et al.,
2000; Hikosaka, 2005b), a decline in Rubisco activity (Warren & Adams, 2001) and a reduction in leaf conductance
(Evans & Loreto, 2000). Rd at a given Narea also decreased
through the growing season (Table 1). This trend has been
reported in S. altissima (Schieving et al., 1992).
The relationships between Pmax, ϕ, θ, R d and Narea
(Table 1) were determined at 1-month intervals at the averaged air temperature of the month of measurement, which
was calculated from the 3-yr record at the study site (see the
Materials and Methods). In the calculation of lifetime C gain,
these relationships were assumed to be constant between
two successive measurements. However, Pmax, ϕ and R d are
strongly affected by air temperature (Berry & Björkman,
1980; Sage & Sharkey, 1987; Criddle et al., 1994; von Caemmerer, 2000). We evaluated the influence of change in air
temperature on the lifetime C balance for Leaf Order 6 by
comparing the lifetime C gain neglecting the temperature
dependencies of Pmax, ϕ and Rd (EB) with that taking the
temperature dependence into consideration (E BT). For the
temperature dependence of Pmax, the empirical data for eight
herbaceous species (Bunce, 2000) were used. The temperature
dependence of ϕ was calculated according to von Caemmerer
(2000) and Bernacchi et al. (2001). Rd was calculated assuming that the temperature coefficient (Q10) was 2.7 (Kinugasa
et al., 2005). Our results were little affected by the change in
air temperature. EBT was 94.3–100.2% of EB in the HN stand
and was 94.6–98.1% of EB in the LN stand. The small effect
of temperature on lifetime C balance resulted from the narrow
range of day and night air temperature that may affect photosynthesis and the night respiration.
The results described in this paper suggest that the mechanism with which leaf lifespan is determined differs depending
on the availability of N. When N availability was high, a leaf
was discarded when it no longer contributed to plant growth.
The decline in C gain was caused primarily by a decrease in
light availability and less by a decrease in leaf N. The decrease
in light was caused by a larger leaf area development. When
N availability was low, a leaf was discarded even when the C
gain was positive. The smaller leaf size and thus the lower rate
of light attenuation resulted in the higher C gain on leaf-area
basis. Old leaves might be shed when part of N was retranslocated for growth of new leaves (Oikawa et al., 2005). The
timing of leaf shedding changed depending on the availability of the resource which was most limiting to plant
growth.
New Phytologist (2006) 172: 104–116
Acknowledgements
We thank Ken-ichi Sato for advice on the experimental
set-up. We also thank David Ackerly, Niels Anten, Almaz
Borjigidai, Tomoyuki Itagaki, Toshihiko Kinugasa, Onno
Muller, Riichi Oguchi, Michio Oguro, Yusuke Onoda,
Noriyuki Osada, Yukinori Shitaka, Yuka Suzuki, Masaki
Tateno, Hisashi Tsujisawa and two anonymous reviewers for
helpful comments. This work was supported in part by
Grant-in-aid from the Japan Ministry of Education, Science
and Culture.
References
Ackerly DD. 1999. Self-shading, carbon gain and leaf dynamics: a test of
alternative optimality models. Oecologia 119: 300–310.
Ackerly DD, Bazzaz FA. 1995. Leaf dynamics, self-shading and carbon gain
in seedlings of a tropical pioneer tree. Oecologia 101: 289–298.
Aerts R. 1989. The effect of increased nutrient availability on leaf turnover
and above-ground productivity of two evergreen ericaceous shrubs. Oecologia
78: 115–120.
Aerts R, Chapin FS III. 2000. The mineral nutrition of wild plants revised:
a re-evaluation of processes and patterns. Advances in Ecological Research
30: 1–67.
Aerts R, de Caluwe H. 1995. Interspecific and intraspecific differences in
shoot and leaf lifespan of four Carex species which differ in maximum dry
matter production. Oecologia 102: 467–477.
Anten NPR. 1997. Modelling canopy photosynthesis using parameters
determined from simple non-destructive measurements. Ecological
Research 12: 77–88.
Anten NPR, Hirose T. 1998. Biomass allocation and light partitioning
among dominant and subordinate individuals in Xanthium canadense
stands. Annals of Botany 82: 665–673.
Anten NPR, Schieving F, Werger MJA. 1995. Patterns of light and nitrogen
distribution in relation to whole canopy carbon gain in C3 and C4 monoand dicotyledonous species. Oecologia 101: 504–513.
Bates LM, Hall AE. 1982. Diurnal and seasonal response of stomatal
conductance for cowpea plants subjected to different levels of
environmental drought. Oecologia 54: 304–308.
Bazzaz FA, Harper JL. 1977. Demographic analysis of the growth of Linum
usitatissimum. New Phytologist 78: 193–208.
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP. 2001.
Improved temperature response functions for models of Rubisco-limited
photosynthesis. Plant, Cell & Environment 24: 253–259.
Berry JA, Björkman O. 1980. Photosynthetic response and adaptation to
temperature in higher plants. Annual Review of Plant Physiology 31: 491–
543.
Borjigidai A, Hikosaka K, Hirose T, Hasegawa T, Okada M, Kobayashi K.
2006. Seasonal changes in temperature dependence of photosynthetic rate
in rice under free-air CO2 enrichment. Annals of Botany 97: 549–557.
Bunce JA. 2000. Acclimation of photosynthesis to temperature in eight cool
and warm climate herbaceous C3 species: Temperature dependence of
parameters of a biochemical photosynthesis model. Photosynthesis Research
63: 59–67.
von Caemmerer S. 2000. Biochemical models of leaf photosynthesis.
Collingwood, Australia: CSIRO Publishing.
Chabot BF, Hicks DJ. 1982. The ecology of leaf life spans. Annual Review
of Ecology and Systematics 13: 229–259.
Cordell S, Goldstein G, Meinzer FC, Vitousek PM. 2001. Regulation of
leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees
at two extremes of a long chronosequence in Hawaii. Oecologia 127: 198 –
206.
www.newphytologist.org © The Authors (2006). Journal compilation © New Phytologist (2006)
Research
Criddle RS, Hopkin MS, McArthur ED, Hanse LD. 1994. Plant
distribution and the temperature coefficient of metabolism. Plant, Cell
& Environment 17: 233 –243.
Diemer M, Körner Ch. 1996. Lifetime leaf carbon balances of herbaceous
perennial plants from low and high altitudes in the central Alps. Functional
Ecology 10: 33–43.
Dungan RJ, Whitehead D, Duncan RP. 2003. Seasonal and temperature
dependence of photosynthesis and respiration for two co-occurring broadleaved tree species with contrasting leaf phenology. Tree Physiology 23:
561–568.
Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3
plants. Oecologia 78: 9 –19.
Evans JR, Loreto F. 2000. Acquisition and diffusion of CO2 in higher plant
leaves. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosyntheiss: physiology and metabolism. Dordrecht, The Netherlands: Kluwer,
321–351.
Field CB, Mooney HA. 1986. The photosynthesis–nitrogen relationships in
wild plants. In: Givnish TJ, ed. On the economy of plant form and function.
Cambridge, UK: Cambridge University Press, 25 –55.
Hikosaka K. 2003. A model of dynamics of leaves and nitrogen in a plant
canopy: an integration of canopy photosynthesis, leaf life span, and
nitrogen use efficiency. American Naturalist 162: 149 –164.
Hikosaka K. 2005a. Leaf canopy as a dynamic system: ecophysiology and
optimality in leaf turnover. Annals of Botany 95: 521–533.
Hikosaka K. 2005b. Nitrogen partitioning in the photosynthetic apparatus
of Plantago asiatica leaves grown under different temperature and light
conditions: similarities and differences between temperature and light
acclimation. Plant Cell Physiology 46: 1283 –1290.
Hikosaka K, Hirose T. 2000. Photosynthetic nitrogen-use efficiency in
evergreen broad-leaved woody species coexisting in a warm-temperate
forest. Tree Physiology 20: 1249 –1254.
Hikosaka K, Terashima I, Katoh S. 1994. Effects of leaf age, nitrogen
nutrition and photon flux density on the distribution of nitrogen among
leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual
shading of leaves. Oecologia 97: 451– 457.
Hiremath AJ. 2000. Photosynthetic nutrient-use efficiency in three fastgrowing tropical trees with differing leaf longevities. Tree Physiology 20:
937–944.
Hirose T. 1984. Nitrogen use efficiency in growth of Polygonum cuspidatum
Sieb. et Zucc. Annals of Botany 54: 695 –704.
Hirose T, Werger MJA. 1987a. Nitrogen use efficiency in instantaneous and
daily photosynthesis of leaves in the canopy of Solidago altissima stand.
Physiologia Plantarum 70: 215 –222.
Hirose T, Werger MJA. 1987b. Maximizing daily canopy photosynthesis
with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia
72: 520–526.
Hirose T, Ackerly DD, Traw MB, Ramseier D, Bazzaz FA. 1997. CO2
elevation, canopy photosynthesis, and optimal leaf area index. Ecology
78: 2339–2350.
Hirose T, Kinugasa T, Shitaka Y. 2005. Time of flowering, costs of
reproduction, and reproductive output in annuals. In: Reekie E, Bazzaz
FA, eds. Reproductive allocation in plants. San Diego, CA, USA: Elsevier,
159–188.
Jones MB, Muthuri FM. 1984. The diurnal course of plant water potential,
stomatal conductance and transpiration in papyrus (Cyperus papyrus L.)
canopy. Oecologia 63: 252–255.
Kikuzawa K. 1991. A cost-benefit analysis of leaf habit and leaf longevity of
trees and their geographical pattern. American Naturalist 138: 1250–1263.
Kikuzawa K. 2003. Phenological and morphological adaptations to the light
environment in two woody and two herbaceous plant species. Functional
Ecology 17: 29–38.
Kikuzawa K. 2004. Mean labor time of a leaf. Ecological Research 19: 365–
374.
Kinugasa T, Hikosaka K, Hirose T. 2005. Respiration and reproductive
effort in Xanthium canadense. Annals of Botany 96: 81– 89.
Kobayashi S. 1975. Growth analysis of plant as an assemblage of internodal
segments – a case of sunflower plants in pure stands. Japanese Journal of
Ecology 25: 61–70.
Mediavilla S, Escudero A. 2003. Photosynthetic capacity, integrated over the
lifetime of a leaf, is predicted to be independent of leaf longevity in some
tree species. New Phytologist 159: 203–211.
Milla R, Castro-Diez P, Maestro-Martinez M, Monserrat-Marti G.
2005. Relationships between nitrogen, phosphorus and potassium in
branches of eight Mediterranean evergreens. New Phytologist 168: 167–
178.
Monk CD. 1966. An ecological significance of evergreeness. Ecology 47:
504–505.
Monsi M, Saeki T. 1953. Über den Lichtfaktor in den Pflanzengesellschaften
und seine Bedeutung für die Stoffproduktion. Japanese Journal of
Botany 14: 22–52.
Mooney HA, Gulmon SL. 1982. Constraints on leaf structure and function
in reference to herbivory. Bioscience 32: 198–206.
Moore P. 1980. The advantages of being evergreen. Nature 285: 535.
Noble JC, Bell AD, Harper JL. 1979. The population biology of plants with
clonal growth. I. The morphology and structural demography of Carex
arenaria. Journal of Ecology 67: 983–1008.
Oikawa S, Hikosaka K, Hirose T, Shiyomi M, Takahashi S, Hori Y. 2004.
Cost–benefit relationships in fronds emerging at different times in a
deciduous fern, Pteridium aquilinum. Canadian Journal of Botany 82:
521–527.
Oikawa S, Hikosaka K, Hirose T. 2005. Dynamics of leaf area and nitrogen
in a canopy of an annual herb, Xanthium canadense. Oecologia 143: 517–
526.
Ono K, Terashima I, Watanabe A. 1996. Interaction between nitrogen
deficit of a plant and nitrogen content in the old leaves. Plant and Cell
Physiology 37: 1083–1089.
Orians GH, Solbrig OT. 1977. A cost-income model of leaves and roots
with special reference to arid and semiarid areas. American Naturalist 111:
677–690.
Osone Y, Tateno M. 2005. Nitrogen absorption by roots as a cause of
interspecific variations in leaf nitrogen concentration and photosynthetic
capacity. Functional Ecology 19: 460–470.
R Development Core Team. 2006. R: a language and environment for
statistical computing. Vienna, Austria: Royal Foundation for Statistical
Computing, http://www.R-project.org
Reader RJ. 1980. Effects of nitrogen fertilizer, shade and removal of new
growth on longevity of overwintering bog ericad leaves. Canadian Journal
of Botany 58: 1737–1743.
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC,
Bowman WD. 1999. Generality of leaf trait relationships: a test across six
biomes. Ecology 80: 1955–1969.
Reich PB, Uhl C, Walters MB, Prugh L, Ellsworth DS. 2004.
Leaf demography and phenology in Amazonian rain forest:
a census of 40000 leaves of 23 tree species. Ecological Monographs
74: 3–23.
Reich PB, Walters MB, Ellsworth DS. 1992. Leaf life span in relation to
leaf, plant and stand characteristics among diverse ecosystems. Ecological
Monographs 62: 365–392.
Saeki T. 1960. Interrelationships between leaf amount, light distribution and
total photosynthesis in a plant community. Botanical Magazine, Tokyo 73:
55–63.
Sage RF, Sharkey TD. 1987. The effect of temperature on the occurrence
of O2 and CO2 insensitive photosynthesis in field grown plants. Plant
Physiology 84: 658–664.
Schieving F, Weger MJA, Hirose T. 1992. Canopy structure, nitrogen
distribution and whole canopy photosynthetic carbon gain in growing
and flowering stands of tall herbs. Vegetatio 102: 173–181.
Shaver GR. 1983. Mineral nutrition and leaf longevity in Ledum palustre :
the role of individual nutrients and the timing of leaf mortality. Oecologia
56: 160–165.
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org
New Phytologist (2006) 172: 104–116
115
116 Research
Spitters CJT. 1986. Separating the diffuse and direct component of global
radiation and its implications for modeling canopy photosynthesis. Part II.
Calculation of canopy photosynthesis. Agricultural and Forest Meteorology
38: 231–242.
Thomas H, Stoddart JL. 1980. Leaf senescence. Annual Review of Plant
Physiology 31: 83–111.
Turner J, Olson PR. 1976. Nitrogen relations in a Douglas-fir plantation.
Annals of Botany 40: 1185 –1193.
Warren CR, Adams MA. 2001. Distribution of N, Rubisco and photosynthesis
in Pinus pinaster and acclimation to light. Plant, Cell & Environment 24:
597–609.
Williams K, Percival F, Merino J, Mooney HA. 1987. Estimation of tissue
construction cost from heat of combustion and organic nitrogen content.
Plant, Cell & Environment 10: 725 –734.
Wilson EB, Baldocchi DD, Hanson PJ. 2000. Spatial and seasonal variability
of photosynthetic parameters and their relationship to leaf nitrogen in a
deciduous forest. Tree Physiology 20: 565–578.
Wittenbach VA. 1983. Effects of pod removal on leaf photosynthesis and
soluble protein composition of field-grown soybeans. Plant Physiology
73: 121–124.
Wright IJ, Reich PB, Westoby M. 2001. Strategy shifts in leaf physiology,
structure and nutrient content between species of high- and low-rainfall
and high- and low-nutrient habitats. Functional Ecology 15: 423–434.
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F,
Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J,
Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W,
Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N,
Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC,
Tjoelker MG, Veneklaas EJ, Villar R. 2004. The worldwide leaf
economics spectrum. Nature 428: 821–827.
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