Acta Oecologica 20 (5) (1999) 559570 / 1999 ditions scientifiques et mdicales Elsevier SAS. All rights reserved.

Relationships between leaf nitrogen and limitations

of photosynthesis in canopies of Solidago altissima
Philipp Egli a*, Bernhard Schmid b
a
b

Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), CH-8903 Birmensdorf, Switzerland.
Institut fr Umweltwissenschaften, University of Zurich, Winterthurerstr. 190, CH-8057 Zrich, Switzerland.
* Corresponding author (fax: +41 1 739 2215; e-mail: philipp.egli@wsl.ch)

Received January 4, 1999; revised May 14, 1999; accepted July 12, 1999

Abstract Vertical distribution patterns of light, leaf nitrogen, and leaf gas exchange through canopies of the clonal perennial Solidago
altissima were studied in response to mowing and fertilizer application in a field experiment. Consistent with the distribution of light, average
leaf nitrogen content followed a smooth exponential decline along the fertilized stands both in control and mown plots. The nitrogen profile
along the unfertilized stands in mown plots, however, was disrupted by high-nitrogen leaves at the top of shorter ramets that only reached
intermediate strata of the canopies. Hence, in these stands leaf nitrogen was significantly increased in short ramets compared with tall ramets
for a given light environment, suggesting suboptimal stand structure but not necessarily suboptimal single-ramet architecture. However, at least
under the climatic conditions observed during measurements, such disrupture had no substantial effect on stand productivity: model calculations
showed that vertical distribution patterns of leaf nitrogen along ramets only marginally influenced the photosynthetic performance of ramets and
stands. This is explained by the observed photosynthesis-nitrogen relationship: the rate of photosynthesis per unit amount of leaf nitrogen did
not increase with leaf nitrogen content even under saturating light levels indicating that leaf photosynthesis was not nitrogen limited during the
measurement periods. Nevertheless, our study indicates that consideration of how architecture(s) of adjacent individual plants interact could be
essential for a better understanding of the trade-offs between individual and canopy characteristics for maximizing carbon gain. Such trade-offs
may end up in a suboptimal canopy structure, which could not be predicted and understood by classical canopy optimization models. 1999
ditions scientifiques et mdicales Elsevier SAS
Canopy structure / carbon limitation / individual vs. stand optimization / light distribution / nitrogen limitation / photosynthesis

1. INTRODUCTION
Leaves within a canopy experience very different
light environments which is reflected by characteristic
distribution patterns of photosynthetic activity. Foliar
nitrogen content is another important factor linked
with photosynthesis. This is indicated by the well
known positive correlation between the nitrogen content of a leaf and its photosynthetic activity under
saturating photosynthetically active photon flux densities [6, 8, 9, 10, 11, 13, 29, 30]. If the nitrogen
allocation to leaves within a canopy were to match
their light interception, then foliar nitrogen content
should be higher in well illuminated leaves at the top
than in shaded leaves at the bottom of a canopy.
Generally, the overall productivity of a plant stand
should be optimized when the distribution of leaf
nitrogen ideally tracks that of light [7, 16, 18, 19, 20].

However, in stands where plants differ in height, the

upper (younger) leaves of shorter plants may occupy
the same position in the light gradient as the older
(lower) leaves of taller plants. Given the effect of leaf
age on leaf nitrogen content, with younger leaves
having higher nitrogen contents than older ones [16,
29], the smooth exponential decline in the vertical
distribution of leaf nitrogen may be disrupted by
high-nitrogen leaves at the top of shorter ramets in
such stands [5]. More generally, optimization at the
stand level may be in conflict with optimization at
the ramet level [23], an issue that has not been
considered in classical canopy optimization models
(e.g. [7, 12, 18, 19]).
To address this question, we studied height distributions of light and leaf nitrogen as well as correlations between leaf nitrogen and single-leaf gas exchange characteristics in a natural population of

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P. Egli, B. Schmid

Figure 1. Sketch of the study

site: blocks, plots (control and
mown; established in 1987) and
stands (unfertilized and fertilized; established in 1991) were
arranged in a split-plot design.
See text for further explanations.

Solidago altissima L., which shows considerable

variation in ramet height [28]. S. altissima is a clonal,
herbaceous perennial which forms unbranched, annual
above-ground ramets that grow out from short, overwintering rhizomes. The species has been introduced
from North America to Europe about 300 years
ago [33] and for the past 100 years has become highly
invasive. To better understand the relationship between leaf nitrogen and photosynthetic productivity,
we subjected the population of S. altissima to experimental manipulation which involved yearly mowing in
late summer and fertilizer addition. Mowing was
applied to manipulate the leaf area and the canopy
structure of the plant stands; fertilizer was added to
manipulate leaf nitrogen content. Based on the measurements made in the experimental part, we constructed a mechanistic model scaling up from singleleaf photosynthesis to daily carbon gain of individual
ramets of S. altissima. The model was used to assess
the effects of the changed plant architecture under
mowing on ramet productivity and to examine whether
there is a conflict between ramet and stand optimization in this species.
2. MATERIALS AND METHODS
2.1. Experimental design and measurements
Solidago altissima is native to North America and
has become one of the most successful plant invaders
in Central Europe in the course of the 20th century.
The study presented here was carried out at an
old-field site located near Basle, Switzerland
(4730 N, 736 E, altitude 280 m, see [28] for further
information). It was part of a project which examined

the invading potential of this species under different

experimental manipulations, i.e. yearly mowing and
nutrient addition. The experimental design had a
randomized block structure with three blocks containing two plots each (10 16 m; figure 1). From
19871991, one plot in each block was mown yearly
in late summer and the other one was left undisturbed
(referred to as mown and control plots in the following). Above-ground plant parts of Solidago altissima
and all co-occurring species were cut at a height of
5 cm and removed from the mown plots. In April 1991
in each plot, four stands of 2 2 m were randomly
selected (figure 1) and two of them fertilized with
liquid N-P-K fertilizer (0.8 g Nm2, 0.3 g Pm2,
0.7 g Km2) at monthly intervals from MarchMay
1991 and with slow release granular N-P-K
(8 g Nm2, 4 g Pm2, 8 g Km2) in June 1991. The
following three data sets were collected in 1990 and
1991.
2.1.1. Microclimatic measurements (data set 1)
Photosynthetically active photon flux density
(PPFD, mol quantam2s1) at the top of the canopy,
air temperature at 40 cm above ground, and soil
temperature and soil water potential at 10 cm below
the soil surface were measured at the field site
throughout the study period (figure 1). Soil water
potential was assessed with cylindrical soil moisture
blocks (Delmhorst 227, Campbell Scientific, Sutton
Bonington, England). Temperature probes and moisture blocks were placed in one mown and one adjacent
control plot outside the stands established in 1991
(see figure 1 for sensor locations). Microclimate measurements were taken every 30 s and the hourly means
were continuously stored on a data logger (CR10,
Campbell Scientific, Sutton Bonington, England).
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Nitrogen and photosynthesis in Solidago

In addition, on two cloudless days in August 1991,

a total of 72 height profiles (three profiles in each of
the 24 stands) of instantaneous PPFD were recorded
to assess the vertical and horizontal distribution of
PPFD within the canopies in each mowing-byfertilizer treatment combination. Ten quantum sensors
were attached on a bar from 13 to 130 cm above
ground (13-cm height intervals). For each light profile,
3-min means of PPFD of each sensor were recorded
and stored on a data logger (CR10).
2.1.2. Mowing-by-fertilizer data set 2 (1991)
During two sampling periods in July and August
1991, the light-saturated rate of net photosynthesis (A)
and stomatal conductance (g) of single leaves were
measured in the field in full sunlight between 10:00
and 16:00 hours (LI6200 photosynthesis measurement system, LI-COR, Lincoln, USA). Only unshaded
leaves were measured; shading was prevented by tying
back neighbouring ramets. In each stand, different
leaf cohorts of two randomly selected ramets had been
marked when their leaves unfolded (figure 1). On 23
July 1991, gas exchange was measured on these leaf
cohorts, then aged 22 and 43 d. The measurements
were repeated on the following 2 d. On 613 August
1991, the same leaf cohorts were measured again (now
aged 57 and 78 d on average) and a third cohort,
marked later and now aged 28 d, was additionally
measured. This time the measurements were not repeated. A total of 336 leaves were measured during the
two sampling periods. The absolute leaf insertion
height above ground and the ramet height were determined such that the relative position along the ramet,
ranging from 01 from the bottom up, could be
calculated for each sampled leaf. Immediately after
measurement the leaves were put into ice-cooled
plastic bags and their area was determined on the same
day. The sampled leaves were dried to constant mass at
60 C and their nitrogen content was determined
(CHN-analyzer LECO 900, LECO, St. Joseph, USA).
Nitrogen was expressed both in percent of leaf dry
mass (Nm) and on a leaf area basis (Na, g Nm2).
Daytime leaf dark respiration (Rd) was also assessed
directly in the field in August 1991. For the measurement, the sampled leaf was completely shaded by
covering the cuvette. The rates were measured on
sixteen leaves of each of the three marked cohorts.
Measurements were restricted to two ramets in each
fertilized and unfertilized stand in block 3 (figure 1).
Leaf respiration at night was measured on a few leaves
during one night in August 1991.
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2.1.3. Harvest data set 3 (1990)

In August 1990 (in the growing season before the
start of fertilizer application), two ramets, i.e. unbranched above-ground stem axis together with leaves,
were harvested randomly from each of the three mown
and three control plots. Each of these ramets was cut
into height sections of 10 cm from the bottom up.
Immediately after harvesting, the sampled leaves were
detached from the stem sections and put into icecooled plastic bags. The total leaf area of each height
section on each ramet was determined in the laboratory on the same day (LI-3000 leaf area meter,
LI-COR, Lincoln, USA). In addition, eight out of the
twelve ramets were randomly selected for nitrogen
analysis of the leaves of each height section (LECO
900).
The data sets 2 and 3 were used to construct a model
scaling up from instantaneous single-leaf photosynthesis to daily carbon gains of each harvested ramet under
the different daily light regimes that were observed in
August 1991 (data set 1); calculations are explained in
the appendix.
2.2. Statistical analyses
The leaf canopies in the different mowing-byfertilizer treatment combinations were tested for disruption in their nitrogen profile (see Introduction)
using the leaf nitrogen data collected in August 1991.
In each treatment, the average nitrogen distribution
along short sub-canopy ramets was compared with
that along taller canopy ramets. For the analysis, all
ramets shorter than the average ramet height in a given
treatment combination were assigned to a sub-canopy
group and the remainder to a canopy group. Leaf
nitrogen profiles were compared using analyses of
covariance with the dependent variable Na, the explanatory factor ramet size class (sub-canopy or
canopy group), and either the covariate leaf insertion
height or the covariate light interception (see figure 4
for a graphical illustration). The light interception of
each leaf was assessed using fitted height distributions
of PPFD. For the parameterization of these PPFD
profiles, the light-distribution data were first expressed
in percent of incoming PPFD, then log-transformed,
and finally analysed using analysis of covariance with
the covariate height above ground (i.e. sensor position along the bar) and the explanatory factors mowing
and fertilizer application; separate slopes and intercepts were fitted for each mowing-by-fertilizer combination (overall r2 = 0.46).
Effects of mowing and fertilizer application on
single-leaf nitrogen content and gas exchange as listed
in table I were analysed with split-plot analysis of

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P. Egli, B. Schmid

Table I. Split-plot analysis of variance for leaf nitrogen concentration (Nm, in % of leaf dry mass), leaf nitrogen content per unit leaf area (Na,
g Nm2), light-saturated rate of photosynthesis (A), and stomatal conductance (g). Photosynthesis and conductance were measured simultaneously
in each sampled leaf (n = 336). The nitrogen data were log-transformed for the analyses. Each term in the analyses (terms of interest in bold)
was tested at the relevant error level given by the hierarchic structure of the mowing-by-fertilizer experiment (see section 2.2). The relative
position of each leaf along the ramet was included as a covariate; nitrogen declined exponentially from the top downwards along the leaf
population of the ramets as shown by the linear decreases on the log-scale. Mean squares (MS) and F-probabilities are listed; levels of
significance: * P < 0.05; ** P < 0.01; *** P < 0.001.
df

Source of variation
Date (July or August 1991)
Block
Effect pooled across dates (main effect)
Separate effects for July and August
(interaction with time)
Mowing
Effect pooled across dates
Separate effects for July and August
Plot
Effect pooled across dates
Separate effects for July and August
Fertilizer
Effect pooled across dates
Separate effects for July and August
Mowing-by-fertilizer interaction
Effect pooled across dates
Separate effects for July and August
Stand
Effect pooled across dates
Separate effects for July and August
Ramet (separate effects for each of the three
replicated measurements per ramet)
Relative position of the leaf along the ramet
(ranging from 01 from the bottom up)
Residual
Total
1

Nm

Na

MS

Sign.

MS

Sign.

MS

Sign.

3.547

9.931

94.2

n.s.

1.726

n.s.

2
2

0.280
0.061

n.s.
n.s.

0.263
0.050

n.s.
n.s.

129.4
285.3

**
**

0.111
0.274

***
*

1
1

0.179
0.177

n.s.
n.s.

0.660
0.182

n.s.
n.s.

60.7
267.0

*
**1

0.120
0.126

***
n.s.

2
2

0.202
0.052

n.s.
n.s.

0.121
0.062

n.s.
n.s.

0.6
2.4

n.s.
n.s.

< 0.001
0.029

n.s.
n.s.

1
1

4.391
0.001

***
n.s.

3.388
0.069

**
n.s.

235.7
0.2

*
n.s.

< 0.001
0.007

n.s.
n.s.

1
1

0.011
0.628

n.s.
**

0.034
0.556

n.s.
*

130.1
10.9

n.s.
n.s.

0.328
0.088

*
n.s.

16
16
96

0.185
0.046
0.019

**
**
n.s.

0.232
0.073
0.066

*
n.s.
***

48.7
19.2
15.4

*
n.s.
***

0.069
0.039
0.015

n.s.
**
***

3.614

***

3.917

***

737.0

***

0.191

***

191
335

0.019
0.068

0.028
0.108

6.0
18.1

MS

Sign.

0.004
0.022

Positive effect of mowing in August (+35 %) but not in July.

variance. The nitrogen data were log-transformed for

the analyses because they were log-normally distributed; means predicted from analysis of variance were
back-transformed from log-scale. Statistical tests (Ftests) were made at the levels given by the hierarchical
structure of the experimental layout, e.g. mowing
effects were tested against plot effects, whereas fertilizer effects and mowing-by-fertilizer interactions were
tested against stand effects. The relative position of
each leaf along the ramet (ranging from 01 from the
bottom up) was included as a covariate in these
analyses in order to assess height variations of Nm, Na,
A, g and Rd. Finally, multiple linear regression was

used to assess the effects of Na and g on A. The above

analyses were used to parameterize the relationships
listed in step 1 in the appendix.
3. RESULTS
3.1. Microclimate at the study site
Thirty-day running means of air and soil temperature as recorded in one control and one mown plot
during the growing season 1991 are shown in figure 2a
and b, respectively. Air temperatures were similar in
the two plots, whereas soil temperature was higher in
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Nitrogen and photosynthesis in Solidago

Figure 2. Microclimate at the study site in 1991. (a) Thirty-d running means of air temperature (C) at 40 cm above ground (solid line). Air
temperatures as recorded in one control and one adjacent mown plot were pooled because differences were very small. The upper and lower
dashed line illustrate short-time fluctuation within each 30-d period calculated as the mean 1 standard error. (b) Thirty-d running means of soil
temperature (C) at 10 cm below surface level measured in one control plot (solid line) and in one mown plot (dashed line); horizontal lines
indicate periods of drought with soil water potential below 1 MPa at 10 cm below surface level. (c) Total daily PPFD arriving at the top of the
canopies during August 1991. (d) Observed daily courses of instantaneous PPFD on a cloudless day (solid line) and a rainy day (dashed line).

the mown plot than in the control plot. The sandy soil
at the study site dried completely during longer periods of drought. This is illustrated by the horizontal
lines in figure 2b which indicate periods with soil
water potential below 1 MPa at 10 cm below surface
level. Daily light regimes as observed in August 1991
are shown in figure 2c. During this period, the incoming daily PPFD ranged from 10.7 mol quantam2d1
(overcast conditions) to 46.3 mol quantam2d1
(cloudless day). The courses of instantaneous PPFD
during these two days are shown in figure 2d.
Vol. 20 (5) 1999

3.2. Light and nitrogen distributions through

the leaf canopies
Coincident with the differences in soil temperatures
mentioned above, the leaf canopies in control plots
absorbed/reflected a greater proportion of incoming
PPFD (P < 0.05, figure 3) than those in the mown
plots. Fertilizer application reduced percentage light
transmission through the leaf canopies in both mowing
treatments but these effects were not significant.

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P. Egli, B. Schmid

Figure 3. Vertical distribution of PPFD (in percent of incoming

PPFD, log-scale) along stands of Solidago altissima growing in
different mowing-by-fertilizer treatment combinations (August
1991). Light availability below 40 cm above ground is not shown
because all leaves inserting below this level had been shed by August.
Note that average canopy height was greater in the control than in the
mown plots.

The analysis of the mowing-by-fertilizer data set

(August data only) revealed that height profiles of leaf
nitrogen did not differ significantly either between the
sub-canopy and the canopy ramet group (see section 2.2) in the fertilized stands (both in control and
mown plots), or in the unfertilized stands located in the
control plots. The leaf nitrogen profile through the
unfertilized stands in the mown plots, however, was
disrupted by high-nitrogen leaves at the top of
shorter ramets that only reached intermediate strata of
the canopy: in these stands, leaf nitrogen was significantly increased in short ramets compared with tall
ramets for a given height above ground (P < 0.01, data
not shown) and hence level of light intercepted
(P < 0.01; figure 4).
3.3. Treatment effects on the nitrogen content
and gas exchange of single leaves
Foliar nitrogen content (Nm and Na) on average was
higher in August than in July 1991 (figure 6, table I):
Na of the youngest leaf cohort sampled in August
(aged 28 d) on average exceeded that of the youngest
cohort measured in July (aged 22 d) by 61 %. Na also
increased over time in the two leaf cohorts that were

Figure 4. Leaf nitrogen distribution along unfertilized stands and

fertilized stands located in mown plots. Each symbol shows the
nitrogen content of a single leaf in relation to the light intercepted by
that leaf (light decreased exponentially from the top downwards
through the canopies, figure 3). In the unfertilized stands (upper
panel), leaf nitrogen was significantly increased in shorter ramets
compared with taller ramets for a given light environment as
illustrated by the double-headed arrow. There was no such difference
in the fertilized stands (lower panel) and the stands located in control
plots (data not shown).

sampled at both dates (+28 % on average). Leaf

nitrogen contents did not significantly respond to the
mowing treatment but to fertilizer application
(figure 5a, b).
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Nitrogen and photosynthesis in Solidago

565

Figure 5. Nitrogen content (a, b) and gas exchange characteristics (ce) of single leaves of Solidago altissima growing in unfertilized (open bars)
or fertilized stands (hatched bars) located in control and mown plots. Values are pooled across the two sampling periods in July and August 1991.
Means are given together with their common standard error (standard error of the mowing-by-fertilizer interaction calculated from split-plot
analysis of variance); n = 84 leaves for each mowing-by-fertilizer treatment combination except day time dark respiration (n = 12). See table I
for significant treatment effects.

Light-saturated leaf photosynthesis (A) did not differ significantly between the two sampling dates (table I). Figure 5c illustrates the positive main effects
(pooled across sampling dates) of mowing and fertilizer on A as listed in table I; in fact, both were due to
the marked response of A to fertilizer application in
mown plots (although the mowing-by-fertilizer interaction was not significant). Average stomatal conductance (g) was reduced by 43 % in August compared
with July. Mowing interacted significantly with fertilizer application, when effects were pooled across both
sampling dates: g did not respond to mowing in
unfertilized stands but showed a positive response in
fertilized stands (figure 5d; note also the opposite
response of g to fertilizer application in control as
compared with mown plots).
Daytime leaf dark respiration (Rd) did not vary
significantly among the different treatment combinaVol. 20 (5) 1999

tions. Nevertheless, there was a trend towards increased Rd in fertilized stands (figure 5e). Similar to
what was observed for leaf nitrogen, A and g (table I),
Rd declined from the upper to the lower leaves along
the ramet (P < 0.01, linear regression). Respiration at
night was below 1 mol CO2m2s1.
3.4. Relationships between leaf nitrogen content
and gas exchange
A responded positively to Na (P < 0.001; r2 = 0.13,
linear regression). The explained variance increased
from 13 to 32 % if separate regression lines were fitted
to the July and August data (figure 6; P < 0.001 for the
date-by-nitrogen interaction). As noted above, A on
average was not increased in the August sample
despite higher leaf nitrogen contents. In consequence,
average instantaneous nitrogen-use efficiency (NUEi,
rate of photosynthesis per unit amount of leaf nitro-

566

Figure 6. Light-saturated leaf photosynthesis as function of leaf

nitrogen content measured under field conditions in July and August
1991, respectively. Separate regression lines are fitted to the July and
August data (overall r2 = 0.32).

gen) was lower in August (7.9 mol CO2g1 Ns1)

than in July (12.1 mol CO2g1 Ns1). The intercept
of the linear regression of A on Na did not differ
significantly from zero in July (figure 6) indicating no
systematic change of NUEi with increasing leaf nitrogen content at that time. In August, however, NUEi
was negatively correlated with Na as shown by the
positive intercept of the regression line.
A was also positively correlated with g (r2 = 0.51,
linear regression). Na and g together explained 67 %
of the total variation in A if both effects were pooled
across the two sampling periods. The two effects were
not purely additive since the proportion of explained
variance increased significantly (P < 0.001) when the
product of g and Na was added to the regression
model. This interaction means that the responsiveness
of A to foliar nitrogen content increased with increasing g. Hence, the difference in the nitrogen response of
photosynthesis between July and August coincided
with the difference in g between these two dates (see
above).
3.5. Model calculations of integrated ramet carbon
gain
The daily ramet carbon gain per ramet leaf area
(mol CO2m2day1, daily net photosynthesis in the
following) provides a measure of the efficiency of
daily ramet photosynthesis. Figure 7 shows plots of
calculated daily net photosynthesis versus average Na

P. Egli, B. Schmid

Figure 7. The relationship between the average leaf nitrogen content

per ramet and the estimated rate of daily net photosynthesis per
ramet. Rates were assessed for each of four unfertilized ramets from
control plots (closed symbols) and mown plots (open symbols; no
estimates for fertilized plants). Daily net photosynthesis was calculated for two different observed daily light regimes (see values for
daily PPFD and figure 2d). The slope of the dashed lines indicates
daily nitrogen-use efficiency (NUEd) expressed as mol CO2 assimilated per g leaf nitrogen and day (see text for further explanations).

per ramet at two different cumulated daily PPFDs as

observed in August 1991 (see figure 2d). The slopes of
the dashed lines in the figure (i.e. tangent ) equal
daily ramet nitrogen use efficiency (NUEd,
mol CO2g1 N per ramet and day) for a given daily
PPFD and average Na per ramet. The figure shows that
NUEd was negatively correlated with ramet Na even at
high daily PPFD, i.e. decreasing slopes of the dashed
lines with increasing foliar nitrogen contents. Estimated daily carbon gain per ramet ranged from 8.8 to
26.7 mmol CO2d1 (data not shown) and was very
closely correlated with the total foliage area per ramet
(r2 = 0.96, linear regression with n = 8 ramets), but
not significantly with daily net photosynthesis; the
latter two traits were not significantly correlated with
each other.
4. DISCUSSION
4.1. Limitations to photosynthesis
Nitrogen investments into the photosynthetic apparatus were paid back only in part by increased photosynthesis under field conditions during the sampling
periods in July and August 1991. This conclusion rests
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Nitrogen and photosynthesis in Solidago

on the negative correlation between the leaf nitrogen

content (Na) and the rate of photosynthesis per unit
leaf nitrogen (NUE) in August, both at the single-leaf
and the whole-ramet level. Returns were better in July
but, overall, NUEi still did not increase with increasing
Na at that time. Following the concept of nitrogen/
carbon limitation in photosynthetic performance presented by Hirose [17], photosynthesis was not
nitrogen-limited but carbon-limited in August,
whereas N- and C-limitation were approximately in
balance in July. This means that in August, CO2
assimilation was not limited by catalytic processes (i.e.
activity of RuBP-carboxylase-oxygenase and other
nitrogenous compounds linked with photosynthesis)
but primarily by a restricted supply of the substrate
CO2 through the stomata. The 43 % reduction in g in
August as compared with July may have been induced
by enhanced (+20 %) leaf-to-air water vapour mole
fraction differences (w, data not shown), but presumably was not attributable to increased water stress. Soil
water data did not indicate critical water supply during
the two sampling periods (see figure 2b), and the
decline in g with increasing w was not steeper in
August than in July.
4.1.1. Effects of mowing on productivity
in unfertilized stands
Despite lower self-shading (figure 3, open vs. closed
circles) and similar light-saturated single-leaf photosynthesis (compare open bars in figure 5c) in the
mown plots as compared with control plots, average
daily net photosynthesis per ramet did not respond to
mowing when rates were expressed on a whole-ramet
foliage area basis (figure 7, open vs. closed symbols).
Expressed as the amount of CO2 fixed per ramet and
day, however, the average productivity of the ramets
from mown plots was estimated to be reduced by 38 %
compared with that of the ramets from control plots
corresponding to an equal reduction in the average
foliage area per ramet (data not shown). These findings
indicate that primary carbon gain in Solidago altissima
should be more strongly controlled by the quantity
than the quality (efficiency) of photosynthetic processes. Similarly, other authors [26] reported that in
Eucalyptus grandis the amount of absorbed radiation
by the tree crown, which is a function of total leaf area,
was directly proportional to daily carbon gain, whereas
variation in single-leaf productivity was of minor
importance. This enforces the importance of assessing
the physiology of a particular organ and whole-plant
performance (i.e. physiological traits integrated over
the plant) to understand a plants primary carbon
gain [24].
Vol. 20 (5) 1999

4.2. Individual versus stand optimization

Using a stand-level approach, Hirose and
Werger [19] reported that in a population of S. altissima exponential decline of nitrogen along the leaf
canopy nearly optimized productivity in each stratum
of the canopy. However, their stand-based optimization model does not necessarily apply to stands with
large variation in ramet height as found in our study
population [4, 28]. In such a situation, the optimal
structure of the stand as a whole potentially conflicts
with the optimal design of individual ramets which
build up the stand: the photosynthetic performance of
the whole stand, in contrast to that of single shorter
ramets, might be increased when nitrogen was redistributed from high-nitrogen leaves at the top of the
shorter ramets to the upper leaf layers of the taller
ramets, because the modified nitrogen pattern would
match the distribution of PPFD through the canopy
better. On the other hand, preserving high nitrogen
contents in leaves at the top of shorter ramets should
be favourable for these ramets as long as their nitrogen
response of photosynthesis is not critically suppressed
through severe shading by taller neighbours.
Because the individual is the primary unit of natural
selection, such conflicts of individual- versus standoptimization may end up in optimal designs of individuals rather than the optimal structure of the stand as
a whole. Essentially, the architecture of a plant should
represent an evolutionary stable strategy (ESS; [27]),
i.e. there should exist no alternative architecture that
increases the fitness of a single plant (genotype) over
that achieved by the common architecture of all the
other plants (genotypes) building up the stand, irrespective whether this common architecture is optimal
with respect to the whole stand or not [21, 23].
In clonal plants like S. altissima, the genet and
therefore a group of ramets may be the key unit of
natural selection [31]. Thus in stands of clonal plants
natural selection may favour optimal designs of groups
of ramets rather than single ramets, but this may
critically depend on whether neighbouring ramets
belong to the same genet or not [32]. S. altissima has
a rather compact genet architecture, i.e. neighbouring
ramets usually belong to the same genet, and individual ramets are physiologically integrated within the
genet [1, 14, 15]. Therefore, the above conflict is
expected to be less pronounced in this species than in
clonal species with spreading genets or in annual
species. Nevertheless, in the unfertilized stands located in the mown plots but not in the other,
nutrient-richer, mowing-by-fertilizer combinations
the leaves of shorter ramets had higher nitrogen
contents than the leaves of taller ramets at the same
height above ground and hence light environment
(figure 4, upper panel). All shorter ramets sampled

568

were surrounded by taller neighbouring ramets of the

same genet which suggests that we did not compare
short high-nitrogen genets with tall low-nitrogen
genets.
In two studies with annual herbs, Na was also
reported to be higher in subordinate plants than in
dominant plants at the same height in the canopy [2,
3], but the consequences of such disrupture for singleplant and whole-stand productivity were not evaluated.
We also did not directly test this, because the eight
ramets used for the model calculations could not be
clearly assigned to the canopy or sub-canopy group
(such model calculations would have required detailed
leaf nitrogen distributions along a larger number of
ramets of different height). But model calculations for
ramets with either observed or a hypothetical uniform
nitrogen distribution (in which all leaves have a
nitrogen content equal to the mean across all height
sections on all ramets) indicated that the distribution of
leaf nitrogen along single ramets had virtually no
effect on their photosynthetic performance: average
daily CO2 gain per ramet calculated for a cloudless day
differed by only 0.3 % between ramets with observed
and uniform nitrogen distributions. Redistributing leaf
nitrogen in the unfertilized stands in mown plots in
order to bring the nitrogen profile along each ramet
into line with the resulting average foliar nitrogen
distribution along the stand (i.e. smoothing the leaf
nitrogen profile) does not change leaf nitrogen contents more profoundly than does the redistribution
uniforming the nitrogen profile. Therefore, we conclude that smoothing the leaf nitrogen profile along
these stands would not have considerably altered
single-ramet and whole-canopy productivity, at least
under the environmental conditions during the sampling periods in summer 1991. Nevertheless, such
conflicts of individual- versus stand-optimization
could be of more relevance in situations where leaf
nitrogen (rather than CO2 supply) becomes limiting
for photosynthesis. The climate actually was much
more humid and cooler from April to mid May 1991
indicating that photosynthetic productivity might have
been more closely related to foliar nitrogen during the
early phase of the annual ramet-growth cycle.
Small differences (< 5 %) between observed and
uniform nitrogen distributions were also reported for a
stand of Lepechinia calycina [7] and whole-crown
photosynthesis in Eucalyptus grandis [26]. These and
our findings contrast with the model outcomes of
Hirose and Werger [18]. In their population of S.
altissima, the observed nitrogen distribution increased
daily net photosynthesis by more than 20 % over a
canopy with uniform nitrogen distribution. This difference, in part, was based on the strong nitrogen
response of single-leaf photosynthesis underlying their

P. Egli, B. Schmid

model computations. Divergent from what was found

here and by Leuning et al. ([25]; see also the Discussion in [26]), photosynthesis was nitrogen limited
even in shaded strata in the canopy studied by Hirose
and Werger. The discrepancy between the findings of
these authors and our own may be attributable to
differing measurement techniques: Hirose and Werger
determined photosynthetic rates in the laboratory
(plants were harvested and then put into a water bottle
in the dark until measurement of photosynthesis the
next day), while we measured photosynthesis as
achieved under field conditions. The discrepancy may
also arise from differences in the canopy density
between the two populations. Hirose and Werger
reported that effects of nitrogen redistribution become
smaller in open canopies compared with dense canopies. In our population, the relative PPFD at the lowest
layer of the leaf canopy ranged from 1637 % of the
incoming radiation (figure 3), whereas it was below
10 % in the stand studied by Hirose and Werger. The
stand of L. calycina also had a relatively open canopy
structure with a relative PPFD of 2040 % at the
darkest microsites [7]. Similarly, lowest PPFDs within
the crown of E. grandis trees were found to be
3050 % of the levels at the top of the crown [26].
5. CONCLUSIONS
Our findings indicate that an emphasis on the
competitive environment of plants in particular data
on how architecture(s) of adjacent individuals may
interact and on the relatedness of these individuals
could be essential to detect trade-offs between singleplant and whole-stand characteristics for maximizing
carbon gain, an issue not considered in conventional
canopy optimization models. Such trade-offs could
become significant in situations where the architecture
of the individual plant representing an evolutionary
stable strategy contrasts with the optimal structure of
the stand as a whole and therefore could explain
potential discrepancies between real canopy structures and those predicted by canopy optimization
models. Consideration of the performance of individual plants is necessary if ecological processes at the
canopy or stand level are to be understood in an
evolutionary context.
Acknowledgments
We thank P. Heubschl for help with the field work, and M. Iseli
and H.P. Rusterholz for assistance with the nitrogen analyses.
Thanks to M. Diemer and A. Weis for their helpful comments on
earlier versions of the manuscript. The research was supported by
Swiss National Science Foundation grant No. 31-30041.90 to B.
Schmid.
Acta Oecologica

Nitrogen and photosynthesis in Solidago

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Appendix. Upscaling from single-leaf to wholeramet photosynthesis.

Daily carbon gains of unfertilized ramets taken from
control and mown plots (n = 4 ramets per treatment,
data set 3) were assessed in four steps. In essence, the
leaf population of each of these ramet was approximated by a series of horizontal sections of 10 cm, each
comprised of leaves of homogenous photosynthetic
characteristics.
Data set 2 was used to parameterize relationships
between leaf nitrogen content (Na), leaf gas exchange,
and leaf insertion height. Analyses were restricted to
the data from unfertilized stands (as mentioned above,
the modelled ramets were taken from unfertilized
stands), and the parameter estimates were pooled
across the two measurement periods in July and
August 1991. (i) The stomatal conductance (g) and the
daytime respiration (Rd) of a single leaf were expressed as functions of its relative position along the
ramet (i.e. leaf insertion height/ramet height). Following the outcomes of these statistical analyses, separate
intercepts were assessed for the control and mowing
treatment for g, while a common intercept was fitted
for Rd; for both traits a common slope parameter was
fitted to both mowing treatments. (ii) The rate of the
light-saturated net photosynthesis of a leaf (A) as
realized under field conditions was expressed as a
function of its Na and g using multiple linear regression (see also section 3.4).
The above functions were established to assess A
and Rd of each 10-cm height section on each harvested
ramet (data set 3): first, the relative position of each
height section along the ramet (i.e. height aboveground/ramet height) was used to estimate g and Rd for
each single section. Then calculated g was combined
with Na as determined for each section to assess A.
We used a non-rectangular hyperbolic function [22] to describe the response of leaf gross photosynthesis (Pg, mol CO2m2 leaf areas1) to PPFD (I,
mol quantam2s1):
Pg = @ uI + Ag $ ~ uI + Ag !2 4uhIAg % 1/2 # /~ 2h ! ~ 1 !

The shape of this function is determined by the

following parameters: light-saturated gross photosynthesis (Ag), quantum yield (, the initial slope of the
curve, mol CO2mol1 quanta), and a convexity

P. Egli, B. Schmid

parameter (, a dimensionless parameter indicating the

degree of curvature, 0 1). Ag was assessed
separately for each height section on each harvested
ramet as the sum of A plus Rd which were estimated in
the first step. However, common values of and
were used for all height sections and ramets. For
practical reasons, these values were not assessed
directly in the population investigated. Instead, and
were estimated by fitting hyperbolas to light response data from a garden experiment with cultivated
Solidago altissima [5]: = 0.056 mol CO2mol1
quanta, = 0.900.
The light response function as established specifically for each 10-cm height section on each ramet in
the second step was linked with horizontal variation of
PPFD within each height section (data set 1) to estimate the instantaneous rates of CO2 uptake of each of
these sections. Horizontal variation of PPFD within
each height section was assessed by calculating separate frequency distributions of PPFD for each height
section of the canopies (separately for control and
mown plots). For each of these distributions, the PPFD
values were first expressed in percent of incoming
PPFD (Io) and then classified into PPFD-classes with a
class-width of 10 %.
Given a specific value of Io, instantaneous net CO2
uptake (mols1) of each height section on each ramet
was obtained by the weighted mean of the rate of
photosynthesis realized over all PPFD classes:
@ 90100 % #

Pheight section =

@ 010 % #
I

~ fI* area !* PI*Io ,

~2!

where I is PPFD-class in percent of Io, fI the relative

frequency of each PPFD-class, area the total leaf area
of the specific height section (and ramet), and PI*Io the
rate of instantaneous net photosynthesis calculated for
each absolute value of PPFD (= [I/100]*Io) in the first
two steps. Integrating rates of instantaneous photosynthesis over all height sections yielded instantaneous
ramet carbon gains.
Finally, the microclimatic data on temporal variation of Io (hourly means) as recorded in August 1991
(figure 2c) were used to integrate hourly ramet carbon
gains over each day during this period. Leaf dark
respiration at night was set to 0.5 mol CO2m2s1
which is about the average value of the night time rates
measured in August 1991 (there were no significant
differences between treatments).

Acta Oecologica