全 文 ：Received 10 Dec. 2003 Accepted 16 Mar. 2004
Supported by the Knowledge Innovation Program of The Chinese Academy of Sciences (KSCX1-08-03) and the State Key Basic Research
and Development Plan of China (G2000018603).
* Author for correspondence. E-mail: .
http://www.chineseplantscience.com
Acta Botanica Sinica
植 物 学 报 2004, 46 (8): 889-895
Effects of Plant Sizes on the Nitrogen Use Strategy in an Annual
Herb, Helianthus annuus (Sunflower)
YUAN Zhi-You1, LI Ling-Hao1, HAN Xing-Guo1*, JIANG Feng-He2, ZHAO Ming-Xu2, LIN Guo-Hui2
(1. Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China;
2. Grassland Management Station of Duolun County, Duolun 027300, Nei Mongol, China)
Abstract: We analyzed the effects of plant sizes on nitrogen (N) uptake and use in a dense monospecific
stand of an annual herb, Helianthus annuus L. (sunflower) and evaluated the consequences of intraspecific
competition. Larger individuals obtained more N disproportionately to their sizes, suggesting that the
competition for soil N was asymmetric (one-sided) among individual plants in the stand. Nitrogen loss of
individuals also increased with plant size. N influx was greater in larger individuals, while N efflux was lower
in small individuals. Therefore, the relative rate of N increment was greater in larger individuals, while it was
around zero in the smallest individuals. N use efficiency (NUE) was separated into the N productivity (NP)
and the mean residence time of N (MRT). Both NP and MRT were positively related to plant size. Larger
individuals showed a higher NP and a longer MRT, while smaller ones displayed the reverse pattern.
Consequently, NUE (i.e. the product of NP and MRT), was higher for larger individuals. No trade-off between
NP and MRT was found among individuals. N resorption efficiency (NRE) was closely related to plant size.
The higher NUE at individual-level was partly a result of greater N resorption during senescence.
Asymmetric competition among individuals in this stand resulted mainly from lower efficiency in both N
uptake and N use by smaller individuals. This study shows that the concept of NUE defined by Berendse and
Aerts offers a powerful tool in studying plant strategies within species as well as among species.
Key words: intraspecific competition; mean residence time (MRT); nitrogen use efficiency (NUE);
nitrogen productivity (NP); plant strategies; size inequality
The size of individual plants within a stand can vary
greatly and competition for limited resources among indi-
viduals is an important factor responsible for the difference
in the size-specific growth (Weiner and Thomas, 1986; Wang
et al., 2004). Nitrogen (N) is the most limiting resource in
many growth environments and it is therefore of interest to
study the effect of plant size on the efficiency with which
plants use this resource for growth (Chapin, 1980; Aerts
and Chapin, 2000). N use efficiency (NUE) can be defined
as the total net production per unit N absorbed or lost
(Hirose, 1971; Vitousek, 1982). Berendse and Aerts (1987)
redefined NUE as the product of N productivity (NP, growth
rate per unit N in the plant) and the mean residence time
(MRT) of the N in the plant. The separation of NUE into NP
and MRT as defined in the concept of Berendse and Aerts
(1987) allows for a functional interpretation of NUE in terms
of different N economies (Garnier and Aronson, 1998;
Eckstein et al., 1999; Yuan et al., 2003b).
It appears that the NUE, NP and MRT of whole popula-
tions were the focus of most studies, while differences
among individuals have not been analyzed (Yuan et al.,
2003a). Furthermore, the NUE approach of Berendse and
Aerts (1987) is based on the assumption that the system is
at a “steady state” (Frissel, 1981). Each individual, however,
grows and dies inequablly in the population and can hardly
be considered at a steady state. At the level of the indi-
vidual plant, N uptake, use and loss occur during different
times of the season. Therefore, it is needed to reconsider
the changes of plants when growing at a non-steady state.
In this study, the concept of NP and MRT of Berendse and
Aerts (1987) was modified to calculate NUE of different
sized individuals in a Helianthus annuus stand. We tried to
apply the concept to individuals that were not at steady
state and analyze their N use strategies in relation to plant
growth during a short period of time in the growing season.
We suggested that larger individuals can receive strong
sun light, therefore, they should have higher NP than smaller
individuals. On the other hand, MRT is positively corre-
lated with leaf lifespan (Garnier and Aronson, 1998; Eckstein
et al., 1999). We propose that smaller, shaded individuals
may have a longer MRT, which would compensate for their
low NP.
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004890
In studying competition within monocultures, it has been
found useful to distinguish between two forms of
competition, i.e. symmetric competition and asymmetric
competition (Weiner, 1988; Freckleton and Watkinson, 2001).
However, it is still unclear that whether the competition for
soil N is symmetric or asymmetric among individuals in a
dense stand, where each individual grows in a different
light environment which may influence competition for
nutrients. Therefore, the second aim of the present study
was to examine whether or not the rate of N uptake by
individuals would be proportional to their sizes in a crowded
population and to analyze variations in N use strategies at
the individual plant level.
1 Materials and Methods
1.1 Study site and plant materials
The experiment was conducted in Duolun County
(115o50-116o55 E，41o46-42o36 N), which is located on
the southern edge of the Hunshandake Sandland in the
central part of Nei Mongol Autonomous Region, China.
This area is also a typical agro-pastoral ecotone. The ter-
rain is relatively flat. The climate belongs to semiarid mon-
soon climate of moderate temperature zone. Mean annual
precipitation is around 385.5 mm and mean annual tempera-
ture is 1.6 ℃, with mean monthly temperature ranging from
–18.3 ℃ in January to 18.5 ℃ in July. The soil types are
classified as chestnut and aeolian sandy soils, relatively
poor in nutrient availability.
Sunflower (Helianthus annuus L.), the species we se-
lected in the present study, was one of the major cultivated
species in this area. It was an erect fast-growing herba-
ceous annual with large and broad leaves. Therefore, it was
an ideal material for obtaining the initial parameter in study-
ing N uptake and use by plants, especially for plants which
were not at a steady state (Frissel, 1981).
1.2 Experimental design and measurement
On 10 August, 2002, a 10 m×10 m plot in a H. annuus
stand located in a relatively homogeneous soil was selected
for sampling. Pure H. annuus stand was obtained by fre-
quent weeding. The average density was about 600 plants
per m2. We chose 20 individual plants at random from the
plot and marked them with small square tags (2 cm in
breadth). Plant height from the base to the terminal shoot
apex, diameter of the stem below cotyledons, and leaf num-
ber were measured for the marked individuals. Plant height
was measured to the nearest centimeter. Stem diameter was
measured to the nearest 0.1 mm with a caliper. These mea-
surements were carried out carefully to minimize the distur-
bance of neighbouring plants. In addition, another 20
individual plants were chosen at random from the stand
and harvested by cutting at ground level to obtain regres-
sion among size, biomass and N concentration (Hikosaka
et al., 1999). Individuals marked on 10 August were har-
vested on 30 August, when the average stand height was
73.7 cm. In the laboratory, plant height and leaf number of
the harvested individuals were measured. The plants were
carefully separated into leaves and stems and then clipped
at every 5 cm from the base. All plant parts were oven-dried
at 70 ℃ for 48 h and weighed to the nearest 0.01 g. After
weighing, leaves and stems were ground and dried again
before the analysis of N concentration. Total Kjeldahl N
was analyzed with an Alpkem autoanalyzer.
1.3 Data analysis
We used aboveground biomass as a measure of the
plant size. Aboveground biomass, leaf N content, and stem
N content of the marked individuals on 10 August were
calculated from a regression of the harvested individuals
on that date (Hikosaka et al., 1999; Weih, 2001).
Aboveground biomass (y, in grams) of the marked indi-
viduals on 10 August was estimated from a linear regres-
sion against plant height× diameter× leaf number (x, m
×cm×n). The relationship between aboveground biom-
ass and plant height (m) × diameter (cm) × leaf number
were expressed as follows:
y = 0.882 6 x + 0.322 2 (r2 = 0.903)
N content of the individuals marked on 10 August was
calculated from a regression of the harvested individuals
on that date. Leaf N content (y, in milligrams) was calcu-
lated as a function of plant height and aboveground biom-
ass (x, in m×g):
y = 7.407 x2 –13.303 x + 23.241 (r2= 0.884)
The amount of stem N (y, in milligrams) was well corre-
lated with aboveground biomass (x, in grams):
y = 0.298 2 x2 + 5.928 7 x + 0.666 6 (r2= 0.981)
Thus we obtained the amount of N in the aboveground
part (stem and leaf) of marked individual on 10 August.
Because the H. annuus seedlings grew fast, the system
was not at a “steady state” (Frissel, 1981). Therefore we
calculated the mean aboveground biomass (Mmean) and the
mean N quantity (Nmean) of an individual between 10 and 30
August as follows (Eckstein and Karlsson, 2001):
Mmean= , Nmean=
Where Mi and Ni (i=1, 2) were the aboveground biomass
and the amount of aboveground N at time ti (i=1, 2),
respectively.
The N loss was calculated with the assumption that
there was no N loss from stems or leaves. The total N loss
M2-M1
lnM2-lnM1
N2-N1
lnN2-lnN1
YUAN Zhi-You et al.: Effect of Plant Size on the Nitrogen Use Strategy in an Annual Herb, Helianthus annuus (Sunflower) 891
from an individual was obtained by quantifying the N con-
tained in the senesced leaves. The rate of N uptake (Nuptake) and
the rate of N loss (Nloss) of an individual between 10 and 30
August were calculated respectively as follows (Hirose, 1971):
Nuptake= , Nloss=
Where LN was Nloss per individual plant. The “turnover”
rate of N was defined separately for the influx (rin, relative Nuptake)
and for the efflux (rout, relative Nloss) of N (Hirose, 1971):
rin= , rout=
The NUE approach of Berendse and Aerts (1987) is built
on the assumption that the system is at a steady state
(Frissel, 1981) with respect to biomass production and N
content (Garnier and Aronson, 1998). Since this was not
the case in our study, we calculated NP as the average NP
of shorter time intervals, as proposed by Vázquez de Aldana
and Berendse (1997). To calculate the NP of each individual
we applied the following equation adopted from Evans
(1972):
NP= × ＝
When Nloss=Nuptake, i.e. N1=N2, the N in the individual was
at a steady state. When Nloss≠ Nuptake, the MRT of an
individual was obtained by dividing Nmean by Nloss, i.e. the
inverse of rout:
MRT = =
Therefore, we obtained NUE, the product of NP and
MRT as follows:
NUE = NP×MRT = ×
=
N concentration in mature and senescing leaves was
used to calculate N resorption efficiency (NRE) (Killingbeck,
1996) on a mass basis as follows:
NRE (%) = ×100%
Where Ng and Ns were the concentration of N in mature
green leaves and senescing leaves, respectively.
The significance of regression coefficients was as-
sessed with SPSS10.0 for Windows.
2 Results
2.1 N concentrations of individual plants at two harvest-
ing times
On 10 August, smaller individuals tended to have higher
N concentrations, while larger ones tended to have lower N
concentrations (Fig.1a). In contrast, the decreasing ten-
dency of the N concentration with increasing plant size
was not observed on 30 August (Fig.1b). The average N
concentration of all individuals on 30 August (22.91 mg/g)
was lower than that on 10 August (33.97 mg/g), suggest-
ing that the N concentration in plant tissues decreased
during plant growth.
2.2 Aboveground N, N uptake and loss of individual
plants
The mean aboveground N (Nmean), the rate of N up-
take (Nuptake) and the rate of N loss (Nloss) for each indi-
vidual increased with the increasing aboveground bio-
mass (Fig.2). Larger individuals tended to contained more
N (Fig.2a). Larger individuals had greater N uptake rate
than smaller ones (Fig.2b). The N resource obtained by
taller plants was thus disproportionate to their sizes, in-
dicating that competition for soil N was asymmetric in
the stand. Similarly, the rate of N loss was also higher in
larger individuals (Fig.2c). The fact that the rate of N
uptake was not equal to the rate of N loss suggested
that the system in this study was not at a steady
state.
Fig.1. N concentration of individuals on 10 August (a) and 30 August (b). *, P < 0.05.
N2-N1+LN
t2-t1
LN
t2-t1
Nuptake
Nmean
Nloss
Nmean
M2-M1
t2-t1
lnN2-lnN1
N2-N1
M2-M1
(t2-t1) Nmean
Nmean
Nloss
1
rout
M2-M1
(t2-t1) Nmean
Nmean
Nloss
M2-M1
LN
Ng-Ns
Ng
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004892
2.3 N turnover of individual plants
The N turnover of individual plants changed with plant
size. N influx (rin, relative N uptake) increased with
aboveground biomass (Fig.3a), while N efflux (rout, relative
N loss) decreased with aboveground biomass (Fig.3b). Due
to the fact that rin was much higher than rout, the relative N
increment (rin-rout) was also higher in larger individuals
than smaller ones (Fig.3c).
2.4 NUE and resorption efficiency of individual plants
Figure 4 shows variations in NUE, NRE and its related
indices among individuals and the relationships between
different indices. Both the NP and MRT increased with plant
size (Fig.4a, b). Consequently NUE, i.e. the product of NP
and MRT, was higher for larger individuals (Fig.4c). NRE
was closely related to plant size (Fig.4d). NP increased, but
not significantly, with MRT (Fig.4e).We found a positive
correlation between NUE and NRE for all plants (Fig.4f).
3 Discussion
In studying competition for resources within
monocultures, it has been found useful to distinguish be-
tween two forms of competition in relation to resource allo-
cation among individuals: one is symmetric competition
and the other is asymmetric competition (Weiner and
Thomas, 1986). Competition for light is often considered to
be asymmetric while competition for soil nutrients is often
considered to be symmetric (Freckleton and Watkinson,
2001). In this study, however, larger dominant individuals
took up more N than the smaller ones (Fig.2), indicating
that the competition for soil N among individuals in this
monocultural stand was asymmetric. The lower demand for
N of the smaller subordinate plants than that of the domi-
nant ones (Anten and Hirose, 1998) may be responsible for
this asymmetric competition for soil nutrients.
Result from regressional analysis showed that individual
plant N concentration was related to plant biomass through
regression relationship (Fig.1). This indicated that the N
uptake rate was regulated not only by soil N availability
but also by the plant growth rate. This is important be-
cause crop N uptake has often been considered in relation
either to soil N availability (N supply approach), or to plant
growth (N demand approach), but rarely to both
simultaneously. Furthermore, as N uptake per unit biomass
decreased as plant biomass increased, it was suggested
that the dependence between N uptake and growth was
probably complex.
Our results showed that individuals were different in
their N use strategies. Larger individuals took up more N
Fig.2. Aboveground N (a), rate of N uptake (b) and rate of N loss (c) as a function of the mean aboveground biomass. *, P < 0.05; **,
P < 0.01.
Fig.3. The relative rate of N uptake (a), relative rate of N loss (b) and relative rate of N increment (c) as a function of the mean
aboveground biomass. **, P < 0.01.
YUAN Zhi-You et al.: Effect of Plant Size on the Nitrogen Use Strategy in an Annual Herb, Helianthus annuus (Sunflower) 893
from soil and lost more N than smaller ones (Fig.2). However,
larger individuals had higher N influx (Fig.3a) and lower N
efflux (Fig.3b). Therefore, larger individuals also had greater
N increment than small ones (Fig.3c). Both NP and MRT of
N increased with plant size (Fig.4a, b). Consequently NUE,
i.e. the product of NP and MRT (Berendse and Aerts, 1987),
was higher in larger individuals (Fig.4c). NP is related to
biomass production and depends on photosynthetic NUE
and N allocation (Garnier et al., 1995). Hikosaka et al. (1999)
found that leaf N content (per unit leaf area) of small plants
was much higher than the optimal N content. This would,
therefore, lead to lower NP of small individuals since NP is
negatively related to N content. It is impossible for small
plants to achieve higher NP than larger ones because larger
individuals have the “optimal” N content (Hikosaka et al.,
1999). Due to the evolutionary trade-off between NP and
MRT (Berendse and Aerts, 1987; Aerts and Chapin, 2000),
plants increase NUE either by increasing N productivity or
by increasing MRT of N. Therefore, subordinate small plants
are supposed to have a long MRT to maintain a high NUE
since NP is physiologically restricted. In our study,
however, MRT was found to be shorter in smaller individu-
als (Fig. 4b). These results suggest that, unlike shade-tol-
erant species, H. annuus was not able to increase their leaf
longevity under shade conditions.
Based on the NUE concept of Berendse and Aerts (1987),
it has been shown that MRT is a measure of N conserva-
tion and depends on the biomass loss rate (e) and on the
NRE, i.e. MRT =1/(e×(1-NRE)) (Garnier and Aronson,
1998; Eckstein et al., 1999; Yuan et al., 2003a). Higher N
resorption and extended leaf lifespan may contribute to an
increase in the MRT (Garnier and Aronson, 1998). In the H.
annuus stand, larger individuals had higher N resorption
efficiency (Fig.4d) which could have contributed to their
longer MRT. The biomass loss rate (e) is negatively related
to tissue lifespan (Garnier and Aronson, 1998).
Unfortunately, we had no data on the tissue lifespan of H.
annuus which would have been important for MRT accord-
ing to the equation. NUE increased with increased NRE
(Fig. 4f), indicating that the higher NUE of larger plants was
due, in part, to higher N resorption efficiency: Resorption
from senescing leaves may reduce N loss from the whole
pant and increase MRT of N (Eckstein et al., 1999; Yuan et
al., 2003a). Therefore, NUE of plants will increase with in-
creasing NRE.
In this study, no trade-off between NP and MRT was
found at the intraspecific level (Fig.4e). Empirical studies
dealing with the trade-off present inconsistent results with
respect to the relationship between nutrient productivity
and nutrient conservation (Garnier and Aronson, 1998). It
appears that studies focusing on interspecific comparisons
showed the proposed trade-off (Aerts, 1990; Eckstein and
Karlsson, 1997), while those dealing with congeneric or
intraspecific comparison did not (Aerts and de Caluwe,
1994). There may be several reasons: Firstly, NP, MRT and
related traits vary less within than among species (Aerts
Fig.4. The N productivity (NP) versus the mean aboveground biomass (a); The mean residence time (MRT) of N versus the mean
aboveground biomass (b); N use efficiency (NUE) versus the mean aboveground biomass (c); The N resorption efficiency (NRE) versus
the mean aboveground biomass (d); Correlation between NP and MRT (e); Correlation between NUE and NRE (f). **, P < 0.01.
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004894
and de Caluwe, 1994; Eckstein et al., 1999). Thus the varia-
tion in only one of the components of NUE may be too low
to detect patterns within the narrow intraspecific range
considered. Secondly, and probably most important, the
relation between NP and MRT is mediated through other
interrelated traits. MRT, for example, is positively related to
leaf lifespan (Eckstein et al., 1999). Thirdly, this way of
illustrating the relationship between NP and MRT may be
bound to some problems of autocorrelation (Knops et al.,
1997; Pastor and Bridgham, 1999), since the average nutri-
ent pool size is the denominator of NP and the numerator of
MRT. Therefore, the proposed trade-off between NP and
MRT may be found among life-forms or among species if
the variation in leaf lifespan is large. In contrast, within
species no such trade-off can be expected owing to the
small variation in biomass loss rate, leaf lifespan, MRT or
NP.
A proper evaluation of N use strategies requires data at
the whole-plant level, because patterns of aboveground
NUE are not necessarily similar to whole-plant NUE (Aerts
and Chapin, 2000). Unfortunately, the whole-plant NUE in
this study was not evaluated owing to the difficulty of
measuring belowground biomass and nutrient. Compared
with perennials, H. annuus, an annual herb in our study,
has no storage in root for growth in the next season and
consequently allocates smaller amounts of biomass to root.
Therefore, it is expected that the fraction of plant N in roots
should be minimal in annuals as compared with perennials.
The patterns of whole plant NUE in H. annuus would be
similar to the patterns of aboveground NUE.
In conclusion, individuals in the H. annuus stand
showed different plant strategies. Larger individuals had
higher NP and MRT of nitrogen, both of which contributed
to higher NUE, than the smaller individuals. Larger indi-
viduals obtained more N disproportionately to their sizes,
indicating that the competition for soil nitrogen was asym-
metric among individual plants in the stand. These results
suggested that different individual plants adapted to envi-
ronments by different N use strategies, which consisted in
different NP and MRT. We conclude that the concept of
NUE offers a powerful tool to study plant strategies within
species as well as among species.
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