Download Changes in nitrogen resorption traits of six temperate grassland

Plant Soil (2008) 306:149–158
DOI 10.1007/s11104-008-9565-9
REGULAR ARTICLE
Changes in nitrogen resorption traits of six temperate
grassland species along a multi-level N addition gradient
Ju-Ying Huang & Xiao-Guang Zhu &
Zhi-You Yuan & Shi-Huan Song & Xin Li &
Ling-Hao Li
Received: 25 April 2007 / Accepted: 28 January 2008 / Published online: 22 February 2008
# Springer Science + Business Media B.V. 2008
Abstract Nitrogen (N) resorption from senescing
leaves is an important mechanism of N conservation
for terrestrial plant species, but changes in Nresorption traits over wide-range and multi-level N
addition gradients have not been well characterized.
Here, a 3-year N addition experiment was conducted
to determine the effects of N addition on N resorption
of six temperate grassland species belonging to three
different life-forms: Stipa krylovii Roshev. (grass),
Cleistogenes squarrosa (T.) Keng (grass), Artemisia
frigida Willd. (semishrub), Melissitus ruthenica C.W.
Wang (semishrub and N-fixer), Potentilla acaulis L.
(forb) and Allium bidentatum Fisch.ex Prokh. (forb).
Generally, N concentrations in green leaves increased
asymptotically for all species. N concentrations in
senescent leaves for most species (5/6) also increased
asymptotically, except that the N concentration in
Responsible Editor: Alfonso Escudero.
J.-Y. Huang : X.-G. Zhu : Z.-Y. Yuan : S.-H. Song : X. Li :
L.-H. Li (*)
Key Laboratory of Vegetation and Climate Change,
Institute of Botany, the Chinese Academy of Sciences,
Xiangshan,
Beijing 100093, People’s Republic of China
e-mail: [email protected]
J.-Y. Huang : X.-G. Zhu
Graduate University of the Chinese Academy of Sciences,
Yuquanlu,
Beijing 100049, People’s Republic of China
senescent leaves of A. bidentatum was independent of
N addition. N-resorption efficiency decreased with
increasing N addition level only for S. krylovii and A.
frigida, while no clear responses were found for other
species. These results suggest that long-term N
fertilization increased N uptake and decreased Nresorption proficiency, but the effects on N-resorption
efficiency were species-specific for different temperate grassland species in northern China. These interspecific differences in N resorption may influence the
positive feedback between species dominance and N
availability and thus soil N cycling in the grassland
ecosystem in this region.
Keywords Leaf N concentration . N cycling .
N fertilization . N-resorption efficiency
and proficiency . Semi-arid grassland ecosystem .
Species composition
Introduction
Nitrogen (N) resorption from senescing leaves is an
important mechanism of N conservation, which
minimizes the dependence of terrestrial plants on N
uptake from soils and increases N-use efficiency
(Aerts 1996; Killingbeck 1996). Previous studies on
N resorption focused mainly on whether species from
N-poor habitats have higher N-resorption efficiency
(the proportional N withdrawn from senescent leaves
prior to abscission, NRE) or N-resorption proficiency
150
(the terminal N concentration in senescent leaves,
NRP) (Cote et al. 2002; Oleksyn et al. 2003;
Richardson et al. 2005). It has been shown that there
is no clear nutritional control on NRE, and NRE does
not explain the distribution of growth-forms over
habitats differing in soil N availability (Aerts 1996;
Aerts and Chapin 2000). Killingbeck (1996) alleged
that NRP is more responsive to changes in N
availability. This allegation is supported by a number
of recent studies (e.g., Cordell et al. 2001; Kobe et al.
2005; van Heerwaarden et al. 2003a; Wright and
Westoby 2003). In contrast to NRE, there are
significant differences in NRP between growth-forms
(Aerts 1996). In temperate grasslands, Yuan et al.
(2005a) found that the herbs and shrubs were more
proficient at N resorbing than the N-fixing species,
but less proficient than graminoids. N-resorption
responses to changes in soil N availability have been
found in previous studies. However, most of these
studies were conducted along natural nutrient gradients or within a narrow range of N fertilization.
Studies on the changes in N resorption of plants along
wide-range and multi-level N availability gradients
are almost completely lacking, and it is not clear
whether or not these changes are life-form-specific.
The temperate grasslands of Inner Mongolia cover
a total area of about 0.6 million km2 and constitute a
major part of the Eurasian grasslands (Li et al. 1998).
It has been noted that some grass species in this
region are highly dependent on internal N cycling
(Yuan et al. 2004, 2006). However, for plant species
of other life-forms, it is not clear whether this
mechanism still holds true. If the responses of
different species to changing soil N supply are
species- or life-form-specific, there will be significant
changes in dominant species composition of grasslands where N supply has been increasingly altered
by human activities in the region. In this study, we
conducted a 3-year experiment of N fertilization in a
temperate grassland community to address the following questions: (1) how do N-resorption traits in
plant species with different life-forms respond to a
wide range of N addition levels? (2) What are the
major N-conserving mechanisms for species of
different life-forms in terms of N-resorption traits?
(3) What are the differential effects of N addition on
the dominance of these species in the community and
the N-resorption-related mechanisms?
Plant Soil (2008) 306:149–158
Materials and methods
Study site and experiment design
The study was conducted in a long-term N fertilization experiment started in 2002 in a grassland at
Duolun County (42°02′N, 116°41′E, 1,380 m a.s.l),
Inner Mongolian Autonomous Region, China. The
climate is temperate and semiarid with a dry spring
and wet summer. Mean annual precipitation is about
385 mm. Mean annual temperature amounts to 1.6°C,
ranging from −18.3°C in January to 18.5°C in July.
The major soil type of the study site is chestnut soil
(Chinese classification), which is equivalent to Calcisorthic Aridisol in United States Soil Taxonomy
classification (Yuan et al. 2005b). The vegetation
was a degraded typical steppe dominated by Artemisia frigida Willd., Stipa krylovii Roshev. and Allium
bidentatum Fisch.ex Prokh.
In July 2002, 40 sub-plots measuring 15×10 m
were selected on a well-conserved (fenced and free
from animal disturbance) and very flat ground in a
S. krylovii community. These plots were separated
by buffer zones of about 4 m in width. Since 2002,
five replication plots have been N fertilized at one of
8 N levels (N levels were 0, 1, 2, 4, 8, 16, 32 and
64 g N m−2 year−1). N fertilizer (NH4NO3) was
added in mid-July annually. The sub-plots were
aligned randomly in the total plot (150×70 m). In
early August 2005, soil properties were investigated
(X.L. Zhang et al. unpublished data, Table 1).
Field sampling
Six perennial plant species in the community belonging to three different life-forms were selected: two
grasses (S. krylovii and Cleistogenes squarrosa (T.)
Keng); two forbs (Potentilla acaulis L. and A.
bidentatum), and two semi-shrubs [A. frigida and
Melissitus ruthenica C.W.Wang (also N-fixer)]. From
early May to mid-June in 2005, six typical individuals
(three for measuring N concentration in green leaves
and three for senescent leaves) of each species with
similar morphology were selected and tagged in each
sub-plot. In early August (peak growth period), fully
expanded mature leaves (free from disease and insect
damage) were collected from the tagged species, and
attached senescent leaves (yellow and ready to drop)
Plant Soil (2008) 306:149–158
Table 1 Changes in soil
chemical properties for each
N addition treatment after
3-year N fertilization
151
N fertilization gradient
(g N m−2 year−1)
Soil properties
Organic C
(g kg−1)
pH
Total N
(g kg−1)
AmmoniaN (mg kg−1)
Nitrate-N
(mg kg−1)
0
1
2
4
8
16
32
64
22.42±1.72
22.37±1.77
22.88±1.53
22.89±1.27
24.50±0.66
24.35±1.01
25.57±1.01
24.57±2.43
7.30±0.05
7.31±0.06
7.25±0.04
6.97±0.06
7.03±0.22
6.38±0.19
5.85±0.15
5.79±0.16
2.14±0.15
2.32±0.19
2.30±0.13
2.17±0.16
2.25±0.09
2.46±0.12
2.58±0.11
2.65±0.20
2.60±0.24
2.39±0.23
2.42±0.11
3.23±0.55
2.67±0.35
2.92±0.89
9.60±0.39
15.72±5.26
2.08±0.47
1.48±0.21
1.21±0.30
1.48±0.24
1.71±0.46
2.69±1.54
15.15±2.88
25.46±3.56
were collected by gently clipping in mid-October (Aerts
et al. 2007; Güsewell 2005). In early August, live
aboveground biomass was sampled by harvesting the
standing biomass within 1×1 m2 quadrats and separated according to species. All plant samples were
oven-dried at 65°C and weighed. N concentrations in
leaves were analyzed colorimetrically by the Kjeldahl
acid-digestion method with an Alpkem auto-analyzer
(Kjektec System 1026 Distilling Unit, Sweden).
NRE was estimated as the percentage of N
withdrawn from green leaves before leaf abscission.
The formula is:
NRE ¼ 100%½ðNgr NsenÞ=Ngr;
where Ngr and Nsen are the N concentrations in green
and senescent leaves, respectively. NRE is expressed
on the basis of leaf mass rather than leaf area or leaf
cohorts because the leaves of grass species are
relatively small and needle-shaped, making it difficult
to determine changes in leaf area or to collect leaf
cohorts.
Dominance value was calculated as the proportion
of canopy biomass of a certain species in the total
canopy biomass in the community.
Data were analyzed by SPSS version13.0 (SPSS,
Chicago, IL). Regression analysis was used to
describe the relationships between the variables
(Ngr, Nsen, NRE, and Dominance value) and N
levels, and two-way ANOVA was used to test for the
effects of N levels and species on the variables. Data
used in the regression analyses were the means of the
variables for each treatment.
Results
Effects of N addition on N concentration in green
leaves
As shown in Table 2, both N addition and species had
significant effects on the N concentrations in green
leaves of the six species (P<0.0001) whereas the
effects of their interaction were minor (P=0.4800).
Among the three life-forms, semi-shrubs had the
highest green leaf N concentrations, and grasses had
the lowest, while forbs displayed intermediate N
concentrations. Among all the species, M. ruthenica
(a N-fixer) had the highest N concentration, while the
lowest N concentration occurred in S. krylovii. The
values follow the order M. ruthenica > A. frigida > P.
acaulis > A. bidentatum > C. squarrosa > S. krylovii.
Table 2 Effects of species and N addition and their interaction
on N concentrations in green (Ngr) and senescent leaves (Nsen)
and on N-resorption efficiency (NRE) of six temperate
grassland species
Ngr
Nsen
NRE
Source
d.f.
F
P
N addition
Species
N addition× species
N addition
Species
N addition× species
N addition
Species
N addition×species
7
5
35
7
5
35
7
5
35
37.200
51.799
0.998
21.849
90.569
1.967
3.335
41.604
4.012
<0.0001
<0.0001
0.4800
<0.0001
<0.0001
0.0040
0.0020
<0.0001
<0.0001
152
N concentration in green leaves increased asymptotically and significantly with N addition for all
species (Fig. 1). The N concentrations in leaves
reached a maximum at N levels ranging from 8 to
32 g m−2 year−1 of N application for the different
species examined (Fig. 1).
Effects of N addition on N concentration in senescent
leaves
N addition, species and their interaction had significant effects on the N concentration in senescent
leaves of the six species (P<0.01, Table 2). In
cantrast to the situation in green leaves, concentrations in senescent leaves differed more among species
but less among life-forms (Fig. 2). However, semishrubs still held the highest values. Among species, N
concentration in senescent leaves in M. ruthenica was
highest, while that in S. krylovii leaves was lowest.
Altogether, N concentrations in senescent leaves
follow the sequence M. ruthenica > A. frigida > P.
acaulis > C. squarrosa > A. bidentatum > S. krylovii,
generally similar to that for green leaves.
The same asymptotic patterns between N concentrations in senescent leaves and N addition were
found for the two grasses, the two semi-shrubs and
one of the forbs (P. acaulis), with breakpoints
appearing at a range between 8 and 32 g m−2 year−1
of N application, while no clear pattern was found in
A. bidentatum (Fig. 2).
Effects of N addition on N-resorption efficiency
N addition species and their interaction had significant effects on the NRE of the six species (P<0.01,
Table 2). Among the six species, the two semi-shrubs
showed the lowest NRE while the remaining species
displayed comparable efficiency.
Regression analysis revealed that NRE decreased
linearly and significantly with increasing N addition
in A. frigida and S. krylovii, whereas no significant
changes in the rest four species were detected (Fig. 3).
Effects of N addition on species dominance
Dominance values of the six species had changed
substantially after 3 years of N fertilization (Fig. 4).
The response patterns were less species-specific but
were more life-form dependent. Two changing pat-
Plant Soil (2008) 306:149–158
terns in dominance values of the six species were
detected with increasing N addition, namely, (1)
values decreased linearly and sharply at lower N
addition (between N8 and N32), and changed slightly
at higher N addition in the two forbs and the two
semi-shrubs; (2) bell-shaped patterns in the two
grasses, with an initial increase at lower N addition,
followed by a slight decline after the peak value at
intermediate N addition levels (between N16 and N32).
Discussion
Relationships between N availability
and N-resorption traits
It has been suggested that NRE is similar among
habitats but that NRP is higher in N-limited habitats.
In the present study, N concentrations, both in green
leaves and in senescent leaves, increased with
increasing N availability whereas NRE showed a
decreasing trend in two species (A. frigida and S.
krylovii) and no responses in the remaining species.
Our results show that NRP was more sensitive to
N addition than NRE, consistent with previous
results based on fertilization experiments (Feller et
al. 2003; van Heerwaarden et al. 2003a; Vitousek
1998) and natural communities (Rejmankova 2005;
Wright and Westoby 2003; Yuan et al. 2005b). These
increased N concentrations indicate that N fertilization increased the dependence of N acquirement on
soil N pool rather than on leaf N resorption.
Increased green leaves N and unchanged or reduced
NRE may lead to a decrease in NRP, as reported by
Soudzilovskaia et al. (2007).
It is worth noting that, to obtain more accurate
relations between N-resorption traits and N fertilization experimentally, a multi-level and wide-range N
addition gradient is extremely important. For example, in the present study, NRE and NRP values were
rather variable and irregular at lower N addition rates
(Figs. 2 and 3), but our broad range of N fertilization
rates ensured a full view of changes in N-resorption
traits. The highest N addition rates in most other
studies have been about 10 g N m−2 year−1, thus we
speculate that one reason for the varying responses of
nutrient resorption to nutrient addition in different
experiments could be differences in N addition
amounts and ranges.
Plant Soil (2008) 306:149–158
153
Fig. 1 Relationships between N concentrations in
green leaves of six species
and N addition. Data were
fitted with piecewise regression (mean ± SE, n=5)
A. frigida
r 2=0.962, P=0.003
M. ruthenica
2
40 r =0.916, P=0.013
30
20
10
0
S. krylovii
2
40 r =0.942, P=0.006
C. squarrosa
r 2=0.959, P=0.003
-1
[Ngr] (mg g )
30
20
10
0
A. bidentatum
r 2=0.960, P=0.011
P. acaulis
2
40 r =0.955, P=0.014
30
20
10
0
0
10
20
30
40
50
60
0
10
-2
20
30
40
50
60
-1
N addition gradients (g m yr )
In the present study, NRE was expressed on the
basis of leaf mass, which might bias the estimation of
NRE to a certain extent if considerable leaf mass loss
occurred due to mass resorption (van Heerwaarden et
al. 2003b; Vernescu et al. 2005). As a major mass
resorption pathway, reallocation of carbohydrates
from canopy to basal tillers and root crowns in
grassland species has been well documented (Xu et
al. 1995). Substantial increases in the total carbohy-
drate content of root crowns and basal tillers from the
leaf-mature stage to leaf-senescent period were
reported in the two forbs (about 10%) (Xu et al.
1995), and minor increases (below 5%) were observed in the two semi-shrubs and in C. squarrosa
(about 2%), whereas a decrease was observed in A.
frigida (about 4%) in the same area (Xu and Bai
1994), suggesting that leaf losses due to mass
resorption may be relatively large only in the two
154
Plant Soil (2008) 306:149–158
Fig. 2 Relationships between N concentrations in
senescent leaves of six species and N addition. Data
were fitted by piecewise regression (mean ± SE, n=5)
M. ruthenica
r 2=0.974, P=0.001
A. frigida
r 2=0.981, P=0.001
S. krylovii
r 2=0.989, P<0.001
C. squarrosa
r 2=0.986, P<0.001
P. acaulis
r 2=0.955, P=0.004
A. bidentatum
20
10
0
-1
[Nsen] (mg g )
20
10
0
20
10
0
0
10
20
30
40
50
60
0
10
-2
20
30
40
50
60
-1
N addition gradients (g m yr )
forbs, which possibly led to an underestimation of
their NRE in the study.
Soil characteristics changed greatly with the
increase in N supply. For example, soil pH decreased from 7.3 in the control plot to 5.8 in the
high N addition plot (Table 1), which might also
affect NRP. It has been proposed that, in natural
habitats, NRP of grasses was negatively correlated to
soil pH whereas NRE was independent of soil pH
(Yuan et al. 2005b).
Life form-specific mechanisms in N resorption
N concentrations in senescent leaves were considerably lower than those in green leaves for all species
(cf. Figs. 1 and 2), indicating the widespread
existence of N resorption as an N-conserving mechanism in the temperate ecosystem of the study area.
Our findings show that N concentrations in green
leaves were highly dependent on life-form but less
species-specific within life-form. Aerts (1996) also
Plant Soil (2008) 306:149–158
155
Fig. 3 Relationships between N-resorption efficiency in six species and N
addition. Data were fitted by
linear regression (mean ±
SE, n=5)
A. frigida
r 2=0.785, P=0.004
M. ruthenica
100
80
60
40
20
0
S. krylovii
100 r 2=0.770, P=0.004
C. squarrosa
NRE (%)
80
60
40
20
0
P. acaulis
A. bidentatum
100
80
60
40
20
0
0
10
20
30
40
50
60
0
10
-2
20
30
40
50
60
-1
N addition gradients (g m yr )
found that N concentrations in mature leaves of
shrubs and forbs were consistently higher than in
grasses. However, in his analysis, N concentrations in
green leaves within growth-forms were quite speciesspecific. Yuan et al. (2005a) reported similar results.
The six plant species in our study displayed high
NRE. NRE values for the two forbs were much higher
than the average NRE value (about 41.4%), while
those for the two grasses were comparable to those
reported worldwide (Aerts 1996). N concentration in
green leaves reflects the ability of plant species to
acquire N. On the other hand, low N concentration in
green leaves is considered an efficient mechanism to
conserve and utilize N (Carrera et al. 2000). In light
of these arguments, it can be concluded that the semishrubs were most capable of acquiring N, and the
grasses conserved more N by absorbing less N in
leaves, while the forbs adopted both methods in their
156
Plant Soil (2008) 306:149–158
A. frigida
M. ruthenica
10 r 2=0.803, P=0.068
r 2=0.937, P=0.007
8
40
6
30
4
20
2
10
0
S. krylovii
100 r 2=0.974, P=0.001
Dominance value (%)
50
0
C. squarrosa
r 2=0.670, P=0.180
10
80
8
60
6
40
4
20
2
0
P. acaulis
50 r 2=0.890, P=0.022
Dominance value (%)
Fig. 4 Changes in species
dominance along the N addition gradient. Data were
fitted by piecewise regression (mean ± SE, n=5)
0
A. bidentatum
r 2=0.896, P=0.019
50
40
40
30
30
20
20
10
10
0
0
0
10
20
30
40
50
60
0
10
20
30
40
50
60
N addition gradients (g m-2 yr-1)
competition for limited N supply from the habitat.
There were only small differences in NRE values
among life-forms, implying that the grasses contributed more to N conservation via their low N
concentrations in green leaves than via N resorption.
Effects of N-resorption changes on species
composition
After 3 years of N fertilization, species composition in
the community changed from multi-species-dominant
to S. krylovii-dominant. In the control plots, A.
frigida, S. krylovii and A. bidentatum co-dominated
the community, accounting for 26.6%, 25.8% and
22.6% of the total canopy biomass, respectively. The
situation did not change significantly at the lower N
addition rates until N4, which is understandable
because soil N regimes did not change either (Table 1).
Species dominance in the community changed substantially at the higher N addition rates, with grasses
(specifically S. krylovii) increasing significantly while
other life-forms decreased greatly (Fig. 4). N concen-
Plant Soil (2008) 306:149–158
tration in senescent leaves was lowest and NRE was
highest for S. krylovii in the control sub-plots,
suggesting that S. krylovii is better adapted to the
relatively N-poor habitat than the other species. On
the other hand, NRE in S. krylovii was most sensitive
to changes in soil N regime, which explains its
success over other species at a wide range of soil N
availability.
Our results show that, with increases in soil N
availability, plant growth became less dependent on N
resorption for the dominant species (i.e., S. krylovii
and A. frigida, see Fig. 3), while other nutrients (e.g.,
P) or resources (e.g., water and light) could become
limiting factors for plant growth. Life-forms might
have played a very important role in determining the
species dominance in the community. Grasses are
more favored by their clonal growth-form and high
competitiveness for light over forbs and semi-shrubs,
which is especially true for S. krylovii over A. frigida
in this study. Increased dominance in grass species
resulting from long-term fertilization has also been
reported in other studies (Press et al. 1998; van
Heerwaarden et al. 2003a). Güsewell (2005)
explained that this could be attributed to their high
resorption proficiency. Additionally, P became limiting due to 3-year N fertilization. Rejmankova (2005)
noted that grasses may be more dominant in P-poor
habitats.
Implications for N cycling in the ecosystem
N concentrations in green leaves increased for all
species, while NRE decreased for the two mostdominant species (S. krylovii and A. frigida) with
increased N fertilization, implying that the community
as a whole will absorb more N from the soil and
become less N-resorption dependent in the N economy in regions where N supply has increased greatly
via N atmospheric deposition due to rapid industrialization and urbanization. N concentrations in senescent leaves increased for most species with increased
N fertilization, indicating that litter N content in the
community as a whole became higher. Thus, the
amount of N returned to the soil via leaf litter production
would also increase. The decomposition rate of plant
litter is controlled largely by litter quality (N concentration) (Knorr et al. 2005), with N-high litter being more
easily decomposed (Quested et al. 2003). It has been
reported that increased N availability can exert indirect
157
effects on N cycling via shifts in species composition
of vegetation (Cornelissen and Thompson 1997;
Shaver and Chapin 1991). Our findings suggest that
shifts in species composition will change the N cycling
rate to a certain extent in the studied community. As S.
krylovii becomes the most dominant species with
increased N fertilization, the community will absorb
more N from soils. On the other hand, the higher N in
canopy litter would speed up decomposition, thus
leading to more rapid N returns to soils. All these
mechanisms will eventually facilitate N cycling in the
plant–soil system.
Acknowledgments We thank the staff of Duolun Restoration
Ecology Research Station, the Chinese Academy of Sciences
(CAS) for providing meteorological data, Mr. G.J. Wang for the
maintenance of the field experimental plot. We also thank
Stephen Hart for kindly correcting the English language of the
manuscript. This study was supported by the State Key Basic
Research Development Program of China (2007CB106800),
two general grants (30600076, 30670347) from the National
Natural Science Foundation of China, the Knowledge Innovation Major Project of CAS (KZCX2-XB2-01) and the State
Science & Technology Promotion Program (2006bad16b01).
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