Plant Communities Soil Carbon and Soil N
Environmental Management (2009) 44:755–765
DOI 10.1007/s00267-009-9361-1
Plant Communities, Soil Carbon, and Soil Nitrogen Properties
in a Successional Gradient of Sub-Alpine Meadows on the Eastern
Tibetan Plateau of China
Wen-Jin Li Æ Jin-Hua Li Æ Johannes M. H. Knops Æ
Gang Wang Æ Ju-Jie Jia Æ Yan-Yan Qin
Received: 29 February 2008 / Accepted: 26 July 2009 / Published online: 25 August 2009
Ó Springer Science+Business Media, LLC 2009
Abstract To assess the recovery trajectory and selfmaintenance of restored ecosystems, a successional gradient (1, 3, 5, 15, and 30 years after abandonment) was
established in a sub-alpine meadow of the eastern Tibetan
Plateau in China. Plant communities and soil carbon and
nitrogen properties were investigated and analyzed.
Regression analyses were used to assess the models (linear
or quadratic) relating measures of species richness, soil
carbon and nitrogen properties to fallow time. We found
that species richness (S) increased over the first 20 years
but decreased thereafter, and aboveground biomass showed
a linear increase along the fallow time gradient. The richness of different functional groups (forb, grass and legume)
changed little along the fallow time gradient, but their
corresponding above ground biomass showed the
U-shaped, humped or linear pattern. Soil microbial carbon
(MBC) and nitrogen (MBN) in the upper 20 cm showed a
U-shaped pattern along the fallow time gradient. However,
soil organic carbon (Corg) and total nitrogen (TN) in the
soil at depth greater than 20 cm showed significant patterns
of linear decline along the fallow time gradient. The
threshold models of species richness reflected best the
recovery over the 15 year fallow period. These results
indicated that fallow time had a greater influence on
development of the plant community than soil processes in
W.-J. Li J.-H. Li (&) G. Wang J.-J. Jia Y.-Y. Qin
Key Laboratory of Arid and Grassland Agroecology, Lanzhou
University, Lanzhou 730000, People’s Republic of China
e-mail: lijinhuap@sohu.com
W.-J. Li
e-mail: wenjinli@yahoo.com.cn
J. M. H. Knops
School of Biological Sciences, University of Nebraska,
348 Manter Hall, Lincoln, NE 68588-0118, USA
abandoned fields in sub-alpine meadow ecosystem. These
results also suggested that although the succession process
did not significantly increase soil C, an increase in
microbial biomass at the latter stage of succession could
promote the decomposability of plant litter. Therefore,
abandoned fields in sub-alpine meadow ecosystem may
have a high resilience and strong rehabilitating capability
under natural recovery condition.
Keywords Fallow time gradient Species richness
Soil carbon Soil nitrogen Sub-alpine meadow
Introduction
Many grasslands worldwide are degraded through overgrazing, lowering their productivity and resilience (Li and
Zhou 1998; Landsberg and others 1999). Within the
Tibetan plateau of China, overgrazing has degraded 42.51
million ha and severely degraded 7.03 million ha of
grasslands (Wang 1997). Therefore, developing rehabilitation strategies for severely degraded grasslands is
important. Degraded grasslands may have a capacity for
self-recovery if the disturbance is ceased for an extended
time and undergo a natural succession. Several studies have
documented that such as cessation of disturbance results in
a natural succession and that this has the potential to be a
successful conservation strategy that restores the diversity,
functioning and resilience in degraded grasslands worldwide (Burel and Baundry 1995; Jordan and others 1988;
Palik and others 2000).
Restoration studies have traditionally determined the rate
and direction of secondary succession of plant communities
(Pickett 1982; Asefa and others 2003; Abebe and others
2006; Ruprecht 2006). Studies of succession in abandoned
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fields have shown different patterns for the vegetation and
soil carbon and nitrogen pools. Several studies have shown
a linear positive increase in plant diversity with time indicating that plant species diversity may recover over periods
of less than 10 years after abandonment of disturbance
(Abebe and others 2006). However, other studies showed
that the restoration of plant species diversity in response to
fallow time is ‘humped-back model’ (Peet and Christensen
1978; Asefa and others 2003). In contrast to vegetation
changes, most studies have shown that soil does not
improve significantly over time periods less than 10 years
(Odum 1960; Aweto 1981; Odum and others 1984; Lee
2002), and that soil improves only over much longer periods
(Aweto 1981; Juo and Lal 1977; Hamburg 1984; Robertson
and Vitousek 1981; Landgraf and others 2003; Knops and
Tilman 2000; Brye and Kucharik 2003). However, to gain a
better understanding of ecosystem changes of fallow lands
it might be essential to study vegetation and soil changes
simultaneously (Potthoff and others 2005), because both
vegetation and soil changes are associated with an increase
in below-ground plant biomass (Potthoff and others 2005).
Ecological restoration procedures can directly affect both
vegetation and ecosystem functions such as nutrient cycling
and carbon (C) accrual (Cione and others 2002; De Deyn
and others 2003). However, how vegetation and soil
recovery are linked in restored ecosystems is unclear (Palmer and others 1997). Understanding the relationships
among plant species diversity, plant productivity and
resource availability in restored ecosystems are important to
the management, preservation, and restoration of native
communities and may also be key for successfully restoring
species-rich ecosystem.
We used a chronosequence of successional fields and
studied both the vegetation and soil changes during secondary succession in a sub-alpine meadow region with the
goal of determining appropriate management activities to
restore plant diversity, increase plant cover, biomass and
increase soil fertility. We evaluated the vegetation structure,
species diversity, and ecological processes in order to
determine the recovery trajectory and self-maintenance of a
restored sub-alpine meadow ecosystems. We used a
chronosequence with space-for-time substitutions that may
allow us to forecast recovery trajectories of plant and soil
parameters. If consistent patterns of vegetation and soil
change exist along successional gradient, using a fallow
period could be a useful strategy and a major step forward in
providing a way for managers and policy-makers to develop
a sustainable management of these sub-alpine meadow
ecosystems. The major objectives of this study were: (1) to
quantify species richness over time under natural recovery
conditions; (2) to examine whether different functional
group (forbs, grasses and legumes) showed different
recovery trajectories; and (3) to examine if soil carbon and
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Environmental Management (2009) 44:755–765
nitrogen properties were correlated with plant changes over
time. We propose the following specific hypothesis:
(1)
(2)
(3)
(4)
(5)
Plant diversity and functional group and their corresponding biomass increase during a fallow period
because of the cessation of grazing.
The humped pattern on species richness over time
may reflect threshold recovery model, which can be
apply to decision making and management over
relatively short timescales (Suding and Hobbs 2008).
Soil carbon increases during a fallow period because
of increased plant productivity.
Soil nitrogen increases during a fallow period, if
legume abundance increases, because legumes might
increase activity of soil microbes involved in mineralization (Spehn and others 2000).
Soil recovery is much slower than vegetation changes
during a fallow period (Knops and Tilman 2000; Brye
and Kucharik 2003).
Materials and Methods
Study Area
A chronosequence of abandoned fields was established in
the Research Station of Alpine Meadow and Wetland
Ecosystems of Lanzhou University in the eastern part of the
Qing-Hai Tibetan Plateau, China (N3455°, E10253°) in
2003. The region has an elevation of 2,900–3,000 m above
sea level. Based on meteorological data provided by
Hezuo’s Institute of Meteorology, the area belongs to
sub-alpine meadow with mean annual precipitation of
546.6 mm from 1958 to 2007, and about 85% of that rainfall
is concentrated within the growing season from June
through September. Annual mean temperature is 2.4°C from
-9.9°C in January to 12.8°C in July. The coldest months are
December, January, and February with an average temperature of -8.9°C and the warmest months are June, July, and
August, of which the average temperature is 11.5°C. The
soil texture is sandy loam with gravel, slightly alkaline and
classified as a sub-alpine meadow soil (Gong 1999).
Agricultural practices in this region include rain-fed
farming with main two crops of short growing season: oat
(Avena sativa) and rape (Brassica napus) in an oat–fallow–
rape rotation.
Study Design
We used fallow time as the successional gradient. Despite
the existence of several methodological problems using
chronosequences (Bonet 2004), most of the predictions
made with a space-for-time substitution have been
Environmental Management (2009) 44:755–765
validated by revisiting and resampling the studied communities (Foster and Tilman 2000).
We established the sampling fields in Hezuo in 2003.
The fields used in this study were set aside from agriculture
in 2001, 1999, 1997, 1987, and 1972 and had an age since
abandonment at sampling time of 1, 3, 5, 15, and 30 years.
All fields are located within an area of 10 km2, had the
same orientation, facing south and slope with 15–25°. All
fields were fenced to exclude large herbivores (mainly
sheep and cattle), but not small herbivores, such as rabbit,
plateau pika and plateau zokor, which were found occasionally at low densities.
In each field, 10 (50 9 50 cm) permanent sampling
quadrats were placed using a systematic sampling design
along two transects. Quadrats in each field were set 3.5 m
apart from each other and field margins (about 2 m from
the edge). In August 2006 and 2007, during the peak of the
growing season, cover (%) was visually estimated in each
quadrat. After these measurements, the aboveground biomass of each species was cut, dried at 80°C to constant
weight and weighed.
Species richness (S) was expressed as the average
number of species per quadrat (n = 10) in each field, and
aboveground biomass was also expressed as the average
biomass per quadrat in each field. All species were classified into three functional groups: i.e., grass, legume and
forb. No natural woody plants were found in any fields.
The grass group included graminoids and sedges, and the
forb group included all other species except grass and
legumes.
Soil Sampling
Eight 0–20 cm, 20–40 cm soil samples were collected at
random in August 2006 and 2007 in each field, and composited by field and depth, for a total of 8 samples per field
per depth. After removing larger gravel stones and plant
fragments and roots, each sample was divided into two
parts. One part of each soil sample was air-dried for the
estimation of soil physicochemical parameters and the
other part was sieved through a 2 mm screen and adjusted
to 50% of water holding capacity and then incubated at
25°C for 2 weeks to permit uniform rewetting and to stabilize the microbial activity after the initial disturbances.
0.1 g dry soil samples for each field was used to measure
soil organic carbon (Corg) by the dichromate oxidation
method (Kalembasa and Jenkinson 1973), and 1 g dry soil
samples for each field was used to measure soil total
nitrogen (TN) by the Kjeldahl method (Jackson 1958).
Microbial biomass carbon (MBC) and nitrogen (MBN)
in soil were estimated by fumigation extraction (Brookes
and others 1985). Six portions equivalent to 25 g of dry
weight soil were taken from each soil sample per field.
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Three portions were fumigated for 24 h at 25°C with
CHCl3 (ethanol-free). Following fumigant removal, the soil
was extracted with 100 ml of 0.5 M K2SO4 by shaking for
1 h at 200 rpm and then filtered (membrane mesh size is
0.4 lm). The other three non-fumigated portions were
extracted simultaneously at the time fumigation commenced. Organic carbon in the extracts was measured
using dichromate oxidation method. Microbial biomass C
was calculated as follows:
Microbial biomass carbon ¼ ðCorg ðfumÞ Corg ðnonÞÞ=0:38;
Total nitrogen in the extracts was measured using the
Kjeldahl method (Brookes and others 1985). Microbial
biomass nitrogen was calculated as follows:
Microbial biomass N ¼ ðTN (fum) TN(non)Þ=0:45
Statistical Analyses
Linear or quadratic regression models were used to evaluate changes in plant and soil properties over time and
were fitted to the data based on the best fit. Analyses were
performed using Origin 7.0.
Results
Plant Community
Total vascular plant cover increased from 12.5 to 85.2%
over time. During the first 8 years of succession, the vegetation changed from annual and biannual weeds to
perennial grasses (Table 1). After 18 years of fallow, the
vegetation was dominated by Elymus nutans, Roegneria
nutans, Koeleria cristata, Kobresia bellardii, Kobresia
humilis and Thermopsis lanceolata (Table 1).
Plant species richness in the five fields ranged from 13.7
to 28.1 per 0.25 m2 and increased over the first 20 years but
decreased thereafter (Fig. 1a, b). Most of species richness
was comprised of forbs (Fig. 1c, d) and forb richness
increased over the first 20 years but decreased thereafter.
The aboveground biomass of forb group exhibited significant U-shape curve (decreased over the first 10 years but
increased thereafter) responding to fallow time gradient in
2006 (Fig. 2a; Table 2). Aboveground biomass of forb
showed an inverse trend in 2007 which was correlated with a
significantly higher aboveground biomass of legumes and
grasses (Fig. 2b; Table 2). Legume group richness and their
corresponding biomass increased significantly over fallow
time (Figs. 1c, d, 2a, b; Table 2). We also found that
aboveground biomass along the fallow time gradient
increased significantly linearly (Fig. 2c, d; Table 2). The
aboveground biomass in 2006 varied from 112 to 412 g m-2
and increased from 142 to 347 g m-2 in 2007.
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Table 1 Changes in plant
across fallow time gradients
Environmental Management (2009) 44:755–765
Site
Dominant species
Total cover in
community (%)
Cover in
FFG (%)
Cover in
LFG (%)
Cover in
GFG (%)
Nature meadow
Kobresia humilis (35.9%)
98.0
34.15
8.17
65.68
12.5
9.34
0.24
2.93
21.6
16.33
2.51
2.76
32.5
20.66
7.0
16.82
56.8
29.84
8.17
48.79
85.2
18.67
23.45
63.08
Roegneria nutans (12.3%)
Elymus nutan (19.5%)
Poa annua (3.5%)
Stipa aliena (2.9%)
Agrostis var. (4.9%)
1-year old site
Aconitum gymnandrum (3.5%)
Chenopodium glaucum (1.0%)
Galium aparine (0.8%)
Artemisia hedinii (1.3%)
3-year old site
Elymus nutans (3.3%)
Aster flaccidus (3.6%)
Elephantopus mollis (9.6%)
5-year old site
Elymus nutans (6.3%)
Roegneria nutans (8.3%)
Poa annua (2.8%)
Thermopsis lanceolata (13.4%)
15-year old site
Elymus nutans (19.2%)
Roegneria nutans (11.3%)
Koeleria cristata (3.5%)
Kobresia humilis (6.5%)
The mean covers are shown for
the years of 2006 and 2007.
FFG Forb functional group,
LFG Legume functional group,
GFG Grass functional group
30-year old site
Kobresia humilis (13.9%)
Kobresia bellardii (20.0%)
Thermopsis lanceolata (22.3%)
Astragalus polycladus (4.5%)
Soil Carbon and Nitrogen Properties
Soil organic C in the upper 20 cm differed among the two
sampling years. In 2006 we found a linear decrease, whereas
in 2007 we found no significant change with fallow time.
The soil organic C in the 20–40 cm depth showed the same
linear decrease with fallow time in both years (Fig. 3a, b;
Table 3). Soil microbial C (MBC) and the percent of
microbial carbon to soil organic carbon (MBC/Corg) in the
upper 20 cm along fallow time gradient decreased over the
first 20 years but increased thereafter (Fig. 3c–f; Table 3).
The response pattern of the soil microbial N (MBN) in
relation to the fallow time gradient showed a U-shaped
curve (decreased over the first 10 years but increased
thereafter) in the upper 20 cm in 2006, and the decrease of
MBN was larger in the upper 20 cm as compared to 20–
40 cm in the first years of fallow (Fig. 4a; Table 3). At the
fallow of 18 years, MBN in the upper 20 cm began to
increase markedly again and reached the peak in the fallow
of 33 years, whereas the 20–40 cm MBN increasing but
less so in 2006 (Fig. 4a). There was significant linear
decrease in TN over fallow time except in the upper 20 cm
in 2007 (Fig. 4c, d; Table 3).
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The percent of microbial carbon to soil organic nitrogen
(MBC/TN) in the upper 20 cm showed a U-shaped curve
(decreased over the first 20 years but increased thereafter) in
2006, while the 20–40 cm showed a more significant Ushaped increase in 2007. MBC/TN in the upper 20 cm was
always larger than in the under 20 cm (Fig. 5a, b). The ratio
of soil organic carbon and soil total nitrogen (C/N) showed
the same trend at both soil depths in 2006, with the 20–40 cm
depth showing a U-shaped curve in both years (Fig. 5c, d).
Discussion
Changes in Plant Communities Over Time
In the early succession stage (1–4 years) annual and perennial weeds and herbs with high reproductive capacities and
ecological, morphological and genetic plasticity dominated.
In the later successional stage(1–30 years) the annual plants
and short-lived perennials were displaced by the slowgrowing, long-lived, and highly resilient perennial grasses
with clonal reproduction (Egler 1954; Pickett 1982) such as
Elymus nutans, Roegneria nutans and Kobresia humilis.
Environmental Management (2009) 44:755–765
759
Fig. 1 Changes in species and
functional group richness over
time. Each data point is the
average of 10 quadrats with
standard error in 2006 (left) and
2007 (right). See Table 2 for
significance of all variables
Fig. 2 Aboveground biomass
changes in species and
functional group richness over
time. Each data point is the
average of 10 quadrats with
standard error in 2006 (left) and
2007 (right). See Table 2 for
significance of all variables
We also found a significantly increase in legume functional richness and biomass over time. Forb functional
richness increased at the earlier stage, then decreased
gradually at the medium stage. The aboveground biomass
showed a linear-increase with fallow time gradient. These
indicate that the cessation of grazing favors the functional
group richness and their corresponding biomass during a
fallow period and supports the first hypothesis. The abovementioned correlations suggest that the relationship
between aboveground biomass and species richness did not
always increase linearly over time. Our results disagree
with the hypothesis that increasing productivity was a
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Table 2 The characteristics of fitted curve between fallow time and
several variables describing the plant at this sites
Variables
Regression
2006
df R
2007
2
P
df R2
0.302
2 0.711
0.288
P
Forb functional, group
richness (0.25 m2)
2
0.697
Legume functional, group
richness (0.25 m2)
2
0.939a 0.060
2 0.949b
0.050
Grass functional, group
richness (0.25 m2)
2
0.466
0.534
2 0.783
0.216
Forb functional, group
biomass (g m-2)
2
0.992b 0.010
2 0.651
0.353
Legume functional, group
biomass (g m-2)
2
0.951b 0.047
2 0.357
0.642
Grass functional, group
biomass (g m-2)
2
0.620
2 0.500
0.500
Aboveground biomass
(g m-2)
1
1.000c 0.0001 1 0.987c \0.0001
Species richness (0.25 m2) 1
0.846
0.373
0.153
1 0.823
0.177
R2 values from regression analyses testing for first and second order
polynomial
a
Statistical significant differences at P B 0.1
b
Statistical significant differences at P B 0.05
c
Statistical significant differences at P B 0.001
direct result of higher species diversity, as has been shown
in experimental grassland plant communities (Tilman and
others 1996; Hector and others 1999).
In general, species richness increased in a ‘humpshaped’ pattern over fallow time. This indicates that species richness does not always increase over longer fallow
time. Abebe and others (2006) also reported that the trends
of plant species richness and diversity after restoration
changed in a positive-linear way, and declined when the
fallow times were doubled. Bonet and Juli (2004) investigated a 60-year chronosequence study of semi-arid oldfields and indicated that species richness varied in a nonlinear relation as a result of the coexistence of different
functional groups. Species richness increased quickly during the first decade of abandonment and the maximum total
richness was found at 18 years following fallow, with a
decrease after that. Annuals and perennial forbs reached
their maximum richness during the first 10 years of abandonment. Asefa and others (2003) assessed the restoration
of biodiversity in highly degraded areas in eastern Tigray,
northern Ethiopia using enclosures, and found that herbaceous species richness increased with time of restoration,
reaching a maximum after 3 years of rest, followed by a
decline.
During the early stages of succession, the gradual colonization and reestablishment of a soil seed bank may lead
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to an increase in species richness (Huston 1979), and
subsequently, species richness may decrease in later successional stages as a result of competitive interactions
(Tilman 1982). Thus, the ‘‘humped-back model’’ (unimodal response curve) of species richness may be a general
pattern that occurs in the vegetation diversity over fallow
time gradients (Peet and Christensen 1978). This pattern,
although the underlying factors may be different, can also
be applied to nutrient and productive gradients (Grime
1973; Tilman 1982; Wisheu and Keddy 1989), and disturbance frequency gradients (Connell 1978; Lubchenco
1978; Huston 1979; Wilson and Keddy 1988). In total the
hump shaved curve suggests that there may be a threshold
along fallow time, nutrient and productive and disturbance
frequency gradient. Critical thresholds occur when the
response of a species or ecological process to disturbance is
not linear, but instead changes abruptly at some threshold
level (Sasaki and others 2008). Exceeding this threshold
leads to a loss of ecosystem functions and biodiversity;
change in the opposite direction can instead lead to
recovery if the threshold change can be reversed (Sasaki
and others 2008). The threshold models of species richness
matches the recovery that we found following 15 years of
fallow and supports our second hypothesis. This threshold,
to some degree, may depend also depend on other factors,
such as land use history, previous crop practices (Bonet
2004), soil seed bank (Baskin and Baskin 1998), plant
dispersal type, soil moisture content and nutrient (Bonet
2004) and current management. However, the mechanism
causing this threshold is unclear.
Changes in Soil Carbon and Soil Nitrogen
Properties Over Time
If soil processes are influenced by plant community, then
soil processes should correlate with successional plant
dynamics (Amiotti and others 2000; Woods 2000). It is
generally accepted that organic carbon increase over successional time (Aweto 1981; Juo and Lal 1977; Hamburg
1984; Landgraf and others 2003; Potter and others 1999;
Richter and others 1999; Knops and Tilman 2000; Brye
and Kucharik 2003), although a few studies have shown
limited change (Robles and Burke 1998; Bonet 2004).
In our study we found a significant decline in soil
organic carbon with fallow time. This is not consistent with
many other studies and our third hypothesis that soil carbon
would increase with increased plant productivity. We
hypothesize that in the absent of disturbance the biomass
accumulation was mainly in aboveground plant biomass
and litter and not in belowground biomass, which led to
lower belowground carbon input. In addition, the higher
plant cover and increased aboveground biomass may have
immobilized more nutrients in the later stages of
Environmental Management (2009) 44:755–765
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Fig. 3 Changes in soil carbon across fallow time gradients. The mean
and standard error are shown for years 2006 (left) and 2007 (right).
See Table 3 for significance of all variables. All abbreviations: Corg
soil organic carbon, MBC soil microbial carbon, MBC/Corg (%) the
percent of microbial carbon to soil organic carbon
succession. An alternative explanation of the slower
decomposition and nutrient mineralization, may be the
recalcitrant nature of belowground litter at high latitudes
(Flanagan and Veum 1974; Van Cleve and Yarie 1986).
The establishment of native species may lead to an increase
in undecomposed belowground litter that may take longer
than our time series to become incorporated into soil
organic matter. These two mechanisms may in combination
have caused the significant decline in soil organic carbon
over fallow time.
Our study also showed a significant decline in soil
nitrogen with fallow time. This isn’t consistent with many
other studies and also does not correspond with the
increased legume abundance. Other studies have shown
that soil N content in the top 25 cm did not significantly
correlated with ecosystem age in the restored prairies (Brye
and Kucharik 2003). Total soil N content in the top 30 cm
increased significantly from year to year, however, total
soil N content in the 30–60 cm depth interval did not differ
significantly (Brye and others 2002). Knops and Tilman
(2000) found that soil total carbon, nitrogen, and the carbon
to nitrogen ratio (C:N) all were significantly positively
correlated with field age since abandonment and soil
nitrogen in the 0–10 cm depth increased with field age, but
there was no change in the 10–60 cm depth horizon.
Therefore, it is necessary to consider soil depth when
studying soil nutrient accumulation. We hypothesized that
soil nitrogen increases during a fallow period, if legume
abundance increases, because legumes might increase
activity of soil microbes involved in mineralization (Spehn
and others 2000). Our results have shown that the legume
cover and aboveground biomass increased over fallow
time, but similarly to the soil carbon decline, the decrease
in soil nitrogen might be caused by a redistribution of soil
nitrogen into the plant or litter nitrogen.
Soil microbial biomass is sensitive to the changes in
soil function over the time scale of secondary succession
(Schmidt and others 2007). Manlay and others (2000)
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Table 3 The characteristics of fitted curve between fallow time and several variables describing the soil at these sites
Variables
Depth (cm)
Regression
2006
df
Corg
MBC
MBC/Corg (%)
MBC/MBN
MBC/TN (%)
C/N
MBN
TN
2007
R2
P
df
R2
P
b
0–20
1
0.868
0.021
1
0.010
0.916
20–40
1
0.806b
0.038
1
0.978c
0.001
0–20
20–40
2
2
0.400
0.126
0.598
0.874
2
2
0.316
0.528
0.648
0.471
0.841
0–20
2
0.525
0.475
2
0.159
20–40
2
0.271
0.729
2
0.925a
0.075
0–20
1
0.248
0.392
1
0.151
0.849
20–40
1
0.009
0.879
\
\
\
0–20
2
0.533
0.467
2
0.273
0.728
20–40
2
0.807
0.193
2
0.971b
0.029
0–20
2
0.647
0.352
2
0.102
0.897
20–40
2
0.793
0.206
2
0.783
0.216
0.991
0–20
2
0.751
0.249
2
0.010
20–40
2
0.434
0.565
\
\
\
0–20
1
0.822b
0.034
1
0.002
0.941
20–40
1
0.884b
0.015
1
0.848b
0.026
2
R values from regression analyses testing for first and second order polynomial
a
Statistical significant differences at the P B 0.1
b
Statistical significant differences at the P B 0.05
c
Statistical significant differences at the P B 0.001
‘‘\’’ = indicates not applicable; Corg soil organic carbon, MBC soil microbial carbon, MBN soil microbial nitrogen, TN soil total nitrogen, C/N the
ratio of soil organic carbon and soil total nitrogen, MBC/Corg (%) the percent of microbial carbon to soil organic carbon, MBC/TN (%) the
percent of microbial carbon to soil organic nitrogen
Fig. 4 Changes in soil nitrogen
across the fallow time gradient.
The mean and standard error are
shown for years 2006 (left) and
2007 (right). See Table 3 for
significance of all variables. All
abbreviations: MBN soil
microbial nitrogen, TN soil total
nitrogen
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Fig. 5 Changes in the ratios of soil carbon and nitrogen across the
fallow time gradient. The mean and standard error are shown for years
2006 (left) and 2007 (right). See Table 3 for significance of all
variables. All abbreviations: Corg soil organic carbon, MBC soil
microbial carbon, MBN soil microbial nitrogen, TN soil total nitrogen,
C/N the ratio of soil organic carbon and soil total nitrogen, MBC/Corg
(%) the percent of microbial carbon to soil organic carbon, MBC/TN
(%) the percent of microbial carbon to soil organic nitrogen
reported that microbial biomass showed no clear variation
in sampled 0–10 cm soil along fallow time (\30 years).
Landgraf (2001) found that microbial biomass carbon and
MBC/Corg ratios increased along fallow time (\3 years),
but microbial biomass N decreased. Jia and others (2005)
found that microbial biomass carbon and MBC/Corg
readily decreased but microbial biomass nitrogen exhibited no trend along fallow time (\15 years). However, our
study is inconsistent with these patterns. We found that
microbial biomass carbon and MBC/Corg in the upper
20 cm increased in the former stage of fallow(\6 years),
and declined from 8 to 18 years, and after 18 years
increased again. This suggests that changes in microbial
biomass along fallow time gradients are different among
ecosystems. MBC/Corg reflects the link and interaction
between microbial biomass and soil organic C (Insam and
Domsch 1988) and can serve as an index for monitoring
soil perturbation (Smith and Paul 1990). The percent of
microbial C to soil organic C was significantly greater,
which indicates that microbial biomass potentially plays a
greater role in soil C turnover than the plant detrital
matter in alpine meadow We found that the microbial
biomass N in the upper 20 cm decreased sharply during
the early stage of fallow (\8 years), followed by an
increase in later stages. We hypothesize that the increasing plant cover and aboveground biomass over time
increased the plant litter pool, which may have led to a
decrease in soil temperature, which resulted in slower
decomposition and nutrient mineralization and a slower N
cycling leading to lower soil available nitrogen levels
(Tilman and others 1996; Knops and others 2001).
Diversity, vegetation structure, and ecological processes
can be regarded as the criteria of restoration success
(Ruiz-Jaen and Aide 2005). Our results indicated that
fallow time had a great influence on development of plant
community and soil process in this ecosystem and
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764
supported our hypothesis that soil recovery is slower than
the vegetation recovery during succession.
We found that during natural restoration succession, the
vegetation developed faster than soil processes, which
suggest that fallow would not significantly improve the soil
(Odum 1960; Aweto 1981; Odum and others 1984; Lee
2002).
Conclusions
Our results suggest that fallow time had a greater influence
on development of plant community than soil process in
abandoned fields in sub-alpine meadow ecosystem. The
species richness of different functional group (forb, grass
and legume species) showed the same hump-shaped patterns along fallow time gradient, but the corresponding
biomass exhibited no trend. Soil organic carbon and total
nitrogen showed the more significant linear-declined
models except in the upper 20 cm in 2007 along fallow
time gradient. MBC (0–20 cm), MBC/Corg (%) (0–20 cm),
MBC/TN (0–20 cm), C/N (20–40 cm) and MBN
(0–20 cm) showed the U-shaped model along fallow time
gradient. These results indicate that the development of
plant community may lead to nutrient limitation at the
latter stage of succession. However, the increased microbial biomass at the latter successional stage may promote
increased decomposition of plant litter. Therefore, abandoned fields in sub-alpine meadow ecosystem have a high
resilience and stronger rehabilitating capability under the
natural recovery condition. These results support a
‘‘humped-shaped model’’ of recovery, suggesting that
15 years of fallow leads to the best restoration of these
degraded fields.
Acknowledgments This research was supported by a grant (No.
30871823) from the Natural Science Foundation of China and the
Research Station of Alpine Meadow and Wetland Ecosystems of
Lanzhou University. We are very grateful to professor Guozhen Du,
Shiting Zhang and Xianhui Zhou for helping in field investigation and
two anonymous reviewers for the constructive suggestions on our
manuscript.
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DOI 10.1007/s00267-009-9361-1
Plant Communities, Soil Carbon, and Soil Nitrogen Properties
in a Successional Gradient of Sub-Alpine Meadows on the Eastern
Tibetan Plateau of China
Wen-Jin Li Æ Jin-Hua Li Æ Johannes M. H. Knops Æ
Gang Wang Æ Ju-Jie Jia Æ Yan-Yan Qin
Received: 29 February 2008 / Accepted: 26 July 2009 / Published online: 25 August 2009
Ó Springer Science+Business Media, LLC 2009
Abstract To assess the recovery trajectory and selfmaintenance of restored ecosystems, a successional gradient (1, 3, 5, 15, and 30 years after abandonment) was
established in a sub-alpine meadow of the eastern Tibetan
Plateau in China. Plant communities and soil carbon and
nitrogen properties were investigated and analyzed.
Regression analyses were used to assess the models (linear
or quadratic) relating measures of species richness, soil
carbon and nitrogen properties to fallow time. We found
that species richness (S) increased over the first 20 years
but decreased thereafter, and aboveground biomass showed
a linear increase along the fallow time gradient. The richness of different functional groups (forb, grass and legume)
changed little along the fallow time gradient, but their
corresponding above ground biomass showed the
U-shaped, humped or linear pattern. Soil microbial carbon
(MBC) and nitrogen (MBN) in the upper 20 cm showed a
U-shaped pattern along the fallow time gradient. However,
soil organic carbon (Corg) and total nitrogen (TN) in the
soil at depth greater than 20 cm showed significant patterns
of linear decline along the fallow time gradient. The
threshold models of species richness reflected best the
recovery over the 15 year fallow period. These results
indicated that fallow time had a greater influence on
development of the plant community than soil processes in
W.-J. Li J.-H. Li (&) G. Wang J.-J. Jia Y.-Y. Qin
Key Laboratory of Arid and Grassland Agroecology, Lanzhou
University, Lanzhou 730000, People’s Republic of China
e-mail: lijinhuap@sohu.com
W.-J. Li
e-mail: wenjinli@yahoo.com.cn
J. M. H. Knops
School of Biological Sciences, University of Nebraska,
348 Manter Hall, Lincoln, NE 68588-0118, USA
abandoned fields in sub-alpine meadow ecosystem. These
results also suggested that although the succession process
did not significantly increase soil C, an increase in
microbial biomass at the latter stage of succession could
promote the decomposability of plant litter. Therefore,
abandoned fields in sub-alpine meadow ecosystem may
have a high resilience and strong rehabilitating capability
under natural recovery condition.
Keywords Fallow time gradient Species richness
Soil carbon Soil nitrogen Sub-alpine meadow
Introduction
Many grasslands worldwide are degraded through overgrazing, lowering their productivity and resilience (Li and
Zhou 1998; Landsberg and others 1999). Within the
Tibetan plateau of China, overgrazing has degraded 42.51
million ha and severely degraded 7.03 million ha of
grasslands (Wang 1997). Therefore, developing rehabilitation strategies for severely degraded grasslands is
important. Degraded grasslands may have a capacity for
self-recovery if the disturbance is ceased for an extended
time and undergo a natural succession. Several studies have
documented that such as cessation of disturbance results in
a natural succession and that this has the potential to be a
successful conservation strategy that restores the diversity,
functioning and resilience in degraded grasslands worldwide (Burel and Baundry 1995; Jordan and others 1988;
Palik and others 2000).
Restoration studies have traditionally determined the rate
and direction of secondary succession of plant communities
(Pickett 1982; Asefa and others 2003; Abebe and others
2006; Ruprecht 2006). Studies of succession in abandoned
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fields have shown different patterns for the vegetation and
soil carbon and nitrogen pools. Several studies have shown
a linear positive increase in plant diversity with time indicating that plant species diversity may recover over periods
of less than 10 years after abandonment of disturbance
(Abebe and others 2006). However, other studies showed
that the restoration of plant species diversity in response to
fallow time is ‘humped-back model’ (Peet and Christensen
1978; Asefa and others 2003). In contrast to vegetation
changes, most studies have shown that soil does not
improve significantly over time periods less than 10 years
(Odum 1960; Aweto 1981; Odum and others 1984; Lee
2002), and that soil improves only over much longer periods
(Aweto 1981; Juo and Lal 1977; Hamburg 1984; Robertson
and Vitousek 1981; Landgraf and others 2003; Knops and
Tilman 2000; Brye and Kucharik 2003). However, to gain a
better understanding of ecosystem changes of fallow lands
it might be essential to study vegetation and soil changes
simultaneously (Potthoff and others 2005), because both
vegetation and soil changes are associated with an increase
in below-ground plant biomass (Potthoff and others 2005).
Ecological restoration procedures can directly affect both
vegetation and ecosystem functions such as nutrient cycling
and carbon (C) accrual (Cione and others 2002; De Deyn
and others 2003). However, how vegetation and soil
recovery are linked in restored ecosystems is unclear (Palmer and others 1997). Understanding the relationships
among plant species diversity, plant productivity and
resource availability in restored ecosystems are important to
the management, preservation, and restoration of native
communities and may also be key for successfully restoring
species-rich ecosystem.
We used a chronosequence of successional fields and
studied both the vegetation and soil changes during secondary succession in a sub-alpine meadow region with the
goal of determining appropriate management activities to
restore plant diversity, increase plant cover, biomass and
increase soil fertility. We evaluated the vegetation structure,
species diversity, and ecological processes in order to
determine the recovery trajectory and self-maintenance of a
restored sub-alpine meadow ecosystems. We used a
chronosequence with space-for-time substitutions that may
allow us to forecast recovery trajectories of plant and soil
parameters. If consistent patterns of vegetation and soil
change exist along successional gradient, using a fallow
period could be a useful strategy and a major step forward in
providing a way for managers and policy-makers to develop
a sustainable management of these sub-alpine meadow
ecosystems. The major objectives of this study were: (1) to
quantify species richness over time under natural recovery
conditions; (2) to examine whether different functional
group (forbs, grasses and legumes) showed different
recovery trajectories; and (3) to examine if soil carbon and
123
Environmental Management (2009) 44:755–765
nitrogen properties were correlated with plant changes over
time. We propose the following specific hypothesis:
(1)
(2)
(3)
(4)
(5)
Plant diversity and functional group and their corresponding biomass increase during a fallow period
because of the cessation of grazing.
The humped pattern on species richness over time
may reflect threshold recovery model, which can be
apply to decision making and management over
relatively short timescales (Suding and Hobbs 2008).
Soil carbon increases during a fallow period because
of increased plant productivity.
Soil nitrogen increases during a fallow period, if
legume abundance increases, because legumes might
increase activity of soil microbes involved in mineralization (Spehn and others 2000).
Soil recovery is much slower than vegetation changes
during a fallow period (Knops and Tilman 2000; Brye
and Kucharik 2003).
Materials and Methods
Study Area
A chronosequence of abandoned fields was established in
the Research Station of Alpine Meadow and Wetland
Ecosystems of Lanzhou University in the eastern part of the
Qing-Hai Tibetan Plateau, China (N3455°, E10253°) in
2003. The region has an elevation of 2,900–3,000 m above
sea level. Based on meteorological data provided by
Hezuo’s Institute of Meteorology, the area belongs to
sub-alpine meadow with mean annual precipitation of
546.6 mm from 1958 to 2007, and about 85% of that rainfall
is concentrated within the growing season from June
through September. Annual mean temperature is 2.4°C from
-9.9°C in January to 12.8°C in July. The coldest months are
December, January, and February with an average temperature of -8.9°C and the warmest months are June, July, and
August, of which the average temperature is 11.5°C. The
soil texture is sandy loam with gravel, slightly alkaline and
classified as a sub-alpine meadow soil (Gong 1999).
Agricultural practices in this region include rain-fed
farming with main two crops of short growing season: oat
(Avena sativa) and rape (Brassica napus) in an oat–fallow–
rape rotation.
Study Design
We used fallow time as the successional gradient. Despite
the existence of several methodological problems using
chronosequences (Bonet 2004), most of the predictions
made with a space-for-time substitution have been
Environmental Management (2009) 44:755–765
validated by revisiting and resampling the studied communities (Foster and Tilman 2000).
We established the sampling fields in Hezuo in 2003.
The fields used in this study were set aside from agriculture
in 2001, 1999, 1997, 1987, and 1972 and had an age since
abandonment at sampling time of 1, 3, 5, 15, and 30 years.
All fields are located within an area of 10 km2, had the
same orientation, facing south and slope with 15–25°. All
fields were fenced to exclude large herbivores (mainly
sheep and cattle), but not small herbivores, such as rabbit,
plateau pika and plateau zokor, which were found occasionally at low densities.
In each field, 10 (50 9 50 cm) permanent sampling
quadrats were placed using a systematic sampling design
along two transects. Quadrats in each field were set 3.5 m
apart from each other and field margins (about 2 m from
the edge). In August 2006 and 2007, during the peak of the
growing season, cover (%) was visually estimated in each
quadrat. After these measurements, the aboveground biomass of each species was cut, dried at 80°C to constant
weight and weighed.
Species richness (S) was expressed as the average
number of species per quadrat (n = 10) in each field, and
aboveground biomass was also expressed as the average
biomass per quadrat in each field. All species were classified into three functional groups: i.e., grass, legume and
forb. No natural woody plants were found in any fields.
The grass group included graminoids and sedges, and the
forb group included all other species except grass and
legumes.
Soil Sampling
Eight 0–20 cm, 20–40 cm soil samples were collected at
random in August 2006 and 2007 in each field, and composited by field and depth, for a total of 8 samples per field
per depth. After removing larger gravel stones and plant
fragments and roots, each sample was divided into two
parts. One part of each soil sample was air-dried for the
estimation of soil physicochemical parameters and the
other part was sieved through a 2 mm screen and adjusted
to 50% of water holding capacity and then incubated at
25°C for 2 weeks to permit uniform rewetting and to stabilize the microbial activity after the initial disturbances.
0.1 g dry soil samples for each field was used to measure
soil organic carbon (Corg) by the dichromate oxidation
method (Kalembasa and Jenkinson 1973), and 1 g dry soil
samples for each field was used to measure soil total
nitrogen (TN) by the Kjeldahl method (Jackson 1958).
Microbial biomass carbon (MBC) and nitrogen (MBN)
in soil were estimated by fumigation extraction (Brookes
and others 1985). Six portions equivalent to 25 g of dry
weight soil were taken from each soil sample per field.
757
Three portions were fumigated for 24 h at 25°C with
CHCl3 (ethanol-free). Following fumigant removal, the soil
was extracted with 100 ml of 0.5 M K2SO4 by shaking for
1 h at 200 rpm and then filtered (membrane mesh size is
0.4 lm). The other three non-fumigated portions were
extracted simultaneously at the time fumigation commenced. Organic carbon in the extracts was measured
using dichromate oxidation method. Microbial biomass C
was calculated as follows:
Microbial biomass carbon ¼ ðCorg ðfumÞ Corg ðnonÞÞ=0:38;
Total nitrogen in the extracts was measured using the
Kjeldahl method (Brookes and others 1985). Microbial
biomass nitrogen was calculated as follows:
Microbial biomass N ¼ ðTN (fum) TN(non)Þ=0:45
Statistical Analyses
Linear or quadratic regression models were used to evaluate changes in plant and soil properties over time and
were fitted to the data based on the best fit. Analyses were
performed using Origin 7.0.
Results
Plant Community
Total vascular plant cover increased from 12.5 to 85.2%
over time. During the first 8 years of succession, the vegetation changed from annual and biannual weeds to
perennial grasses (Table 1). After 18 years of fallow, the
vegetation was dominated by Elymus nutans, Roegneria
nutans, Koeleria cristata, Kobresia bellardii, Kobresia
humilis and Thermopsis lanceolata (Table 1).
Plant species richness in the five fields ranged from 13.7
to 28.1 per 0.25 m2 and increased over the first 20 years but
decreased thereafter (Fig. 1a, b). Most of species richness
was comprised of forbs (Fig. 1c, d) and forb richness
increased over the first 20 years but decreased thereafter.
The aboveground biomass of forb group exhibited significant U-shape curve (decreased over the first 10 years but
increased thereafter) responding to fallow time gradient in
2006 (Fig. 2a; Table 2). Aboveground biomass of forb
showed an inverse trend in 2007 which was correlated with a
significantly higher aboveground biomass of legumes and
grasses (Fig. 2b; Table 2). Legume group richness and their
corresponding biomass increased significantly over fallow
time (Figs. 1c, d, 2a, b; Table 2). We also found that
aboveground biomass along the fallow time gradient
increased significantly linearly (Fig. 2c, d; Table 2). The
aboveground biomass in 2006 varied from 112 to 412 g m-2
and increased from 142 to 347 g m-2 in 2007.
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Table 1 Changes in plant
across fallow time gradients
Environmental Management (2009) 44:755–765
Site
Dominant species
Total cover in
community (%)
Cover in
FFG (%)
Cover in
LFG (%)
Cover in
GFG (%)
Nature meadow
Kobresia humilis (35.9%)
98.0
34.15
8.17
65.68
12.5
9.34
0.24
2.93
21.6
16.33
2.51
2.76
32.5
20.66
7.0
16.82
56.8
29.84
8.17
48.79
85.2
18.67
23.45
63.08
Roegneria nutans (12.3%)
Elymus nutan (19.5%)
Poa annua (3.5%)
Stipa aliena (2.9%)
Agrostis var. (4.9%)
1-year old site
Aconitum gymnandrum (3.5%)
Chenopodium glaucum (1.0%)
Galium aparine (0.8%)
Artemisia hedinii (1.3%)
3-year old site
Elymus nutans (3.3%)
Aster flaccidus (3.6%)
Elephantopus mollis (9.6%)
5-year old site
Elymus nutans (6.3%)
Roegneria nutans (8.3%)
Poa annua (2.8%)
Thermopsis lanceolata (13.4%)
15-year old site
Elymus nutans (19.2%)
Roegneria nutans (11.3%)
Koeleria cristata (3.5%)
Kobresia humilis (6.5%)
The mean covers are shown for
the years of 2006 and 2007.
FFG Forb functional group,
LFG Legume functional group,
GFG Grass functional group
30-year old site
Kobresia humilis (13.9%)
Kobresia bellardii (20.0%)
Thermopsis lanceolata (22.3%)
Astragalus polycladus (4.5%)
Soil Carbon and Nitrogen Properties
Soil organic C in the upper 20 cm differed among the two
sampling years. In 2006 we found a linear decrease, whereas
in 2007 we found no significant change with fallow time.
The soil organic C in the 20–40 cm depth showed the same
linear decrease with fallow time in both years (Fig. 3a, b;
Table 3). Soil microbial C (MBC) and the percent of
microbial carbon to soil organic carbon (MBC/Corg) in the
upper 20 cm along fallow time gradient decreased over the
first 20 years but increased thereafter (Fig. 3c–f; Table 3).
The response pattern of the soil microbial N (MBN) in
relation to the fallow time gradient showed a U-shaped
curve (decreased over the first 10 years but increased
thereafter) in the upper 20 cm in 2006, and the decrease of
MBN was larger in the upper 20 cm as compared to 20–
40 cm in the first years of fallow (Fig. 4a; Table 3). At the
fallow of 18 years, MBN in the upper 20 cm began to
increase markedly again and reached the peak in the fallow
of 33 years, whereas the 20–40 cm MBN increasing but
less so in 2006 (Fig. 4a). There was significant linear
decrease in TN over fallow time except in the upper 20 cm
in 2007 (Fig. 4c, d; Table 3).
123
The percent of microbial carbon to soil organic nitrogen
(MBC/TN) in the upper 20 cm showed a U-shaped curve
(decreased over the first 20 years but increased thereafter) in
2006, while the 20–40 cm showed a more significant Ushaped increase in 2007. MBC/TN in the upper 20 cm was
always larger than in the under 20 cm (Fig. 5a, b). The ratio
of soil organic carbon and soil total nitrogen (C/N) showed
the same trend at both soil depths in 2006, with the 20–40 cm
depth showing a U-shaped curve in both years (Fig. 5c, d).
Discussion
Changes in Plant Communities Over Time
In the early succession stage (1–4 years) annual and perennial weeds and herbs with high reproductive capacities and
ecological, morphological and genetic plasticity dominated.
In the later successional stage(1–30 years) the annual plants
and short-lived perennials were displaced by the slowgrowing, long-lived, and highly resilient perennial grasses
with clonal reproduction (Egler 1954; Pickett 1982) such as
Elymus nutans, Roegneria nutans and Kobresia humilis.
Environmental Management (2009) 44:755–765
759
Fig. 1 Changes in species and
functional group richness over
time. Each data point is the
average of 10 quadrats with
standard error in 2006 (left) and
2007 (right). See Table 2 for
significance of all variables
Fig. 2 Aboveground biomass
changes in species and
functional group richness over
time. Each data point is the
average of 10 quadrats with
standard error in 2006 (left) and
2007 (right). See Table 2 for
significance of all variables
We also found a significantly increase in legume functional richness and biomass over time. Forb functional
richness increased at the earlier stage, then decreased
gradually at the medium stage. The aboveground biomass
showed a linear-increase with fallow time gradient. These
indicate that the cessation of grazing favors the functional
group richness and their corresponding biomass during a
fallow period and supports the first hypothesis. The abovementioned correlations suggest that the relationship
between aboveground biomass and species richness did not
always increase linearly over time. Our results disagree
with the hypothesis that increasing productivity was a
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760
Environmental Management (2009) 44:755–765
Table 2 The characteristics of fitted curve between fallow time and
several variables describing the plant at this sites
Variables
Regression
2006
df R
2007
2
P
df R2
0.302
2 0.711
0.288
P
Forb functional, group
richness (0.25 m2)
2
0.697
Legume functional, group
richness (0.25 m2)
2
0.939a 0.060
2 0.949b
0.050
Grass functional, group
richness (0.25 m2)
2
0.466
0.534
2 0.783
0.216
Forb functional, group
biomass (g m-2)
2
0.992b 0.010
2 0.651
0.353
Legume functional, group
biomass (g m-2)
2
0.951b 0.047
2 0.357
0.642
Grass functional, group
biomass (g m-2)
2
0.620
2 0.500
0.500
Aboveground biomass
(g m-2)
1
1.000c 0.0001 1 0.987c \0.0001
Species richness (0.25 m2) 1
0.846
0.373
0.153
1 0.823
0.177
R2 values from regression analyses testing for first and second order
polynomial
a
Statistical significant differences at P B 0.1
b
Statistical significant differences at P B 0.05
c
Statistical significant differences at P B 0.001
direct result of higher species diversity, as has been shown
in experimental grassland plant communities (Tilman and
others 1996; Hector and others 1999).
In general, species richness increased in a ‘humpshaped’ pattern over fallow time. This indicates that species richness does not always increase over longer fallow
time. Abebe and others (2006) also reported that the trends
of plant species richness and diversity after restoration
changed in a positive-linear way, and declined when the
fallow times were doubled. Bonet and Juli (2004) investigated a 60-year chronosequence study of semi-arid oldfields and indicated that species richness varied in a nonlinear relation as a result of the coexistence of different
functional groups. Species richness increased quickly during the first decade of abandonment and the maximum total
richness was found at 18 years following fallow, with a
decrease after that. Annuals and perennial forbs reached
their maximum richness during the first 10 years of abandonment. Asefa and others (2003) assessed the restoration
of biodiversity in highly degraded areas in eastern Tigray,
northern Ethiopia using enclosures, and found that herbaceous species richness increased with time of restoration,
reaching a maximum after 3 years of rest, followed by a
decline.
During the early stages of succession, the gradual colonization and reestablishment of a soil seed bank may lead
123
to an increase in species richness (Huston 1979), and
subsequently, species richness may decrease in later successional stages as a result of competitive interactions
(Tilman 1982). Thus, the ‘‘humped-back model’’ (unimodal response curve) of species richness may be a general
pattern that occurs in the vegetation diversity over fallow
time gradients (Peet and Christensen 1978). This pattern,
although the underlying factors may be different, can also
be applied to nutrient and productive gradients (Grime
1973; Tilman 1982; Wisheu and Keddy 1989), and disturbance frequency gradients (Connell 1978; Lubchenco
1978; Huston 1979; Wilson and Keddy 1988). In total the
hump shaved curve suggests that there may be a threshold
along fallow time, nutrient and productive and disturbance
frequency gradient. Critical thresholds occur when the
response of a species or ecological process to disturbance is
not linear, but instead changes abruptly at some threshold
level (Sasaki and others 2008). Exceeding this threshold
leads to a loss of ecosystem functions and biodiversity;
change in the opposite direction can instead lead to
recovery if the threshold change can be reversed (Sasaki
and others 2008). The threshold models of species richness
matches the recovery that we found following 15 years of
fallow and supports our second hypothesis. This threshold,
to some degree, may depend also depend on other factors,
such as land use history, previous crop practices (Bonet
2004), soil seed bank (Baskin and Baskin 1998), plant
dispersal type, soil moisture content and nutrient (Bonet
2004) and current management. However, the mechanism
causing this threshold is unclear.
Changes in Soil Carbon and Soil Nitrogen
Properties Over Time
If soil processes are influenced by plant community, then
soil processes should correlate with successional plant
dynamics (Amiotti and others 2000; Woods 2000). It is
generally accepted that organic carbon increase over successional time (Aweto 1981; Juo and Lal 1977; Hamburg
1984; Landgraf and others 2003; Potter and others 1999;
Richter and others 1999; Knops and Tilman 2000; Brye
and Kucharik 2003), although a few studies have shown
limited change (Robles and Burke 1998; Bonet 2004).
In our study we found a significant decline in soil
organic carbon with fallow time. This is not consistent with
many other studies and our third hypothesis that soil carbon
would increase with increased plant productivity. We
hypothesize that in the absent of disturbance the biomass
accumulation was mainly in aboveground plant biomass
and litter and not in belowground biomass, which led to
lower belowground carbon input. In addition, the higher
plant cover and increased aboveground biomass may have
immobilized more nutrients in the later stages of
Environmental Management (2009) 44:755–765
761
Fig. 3 Changes in soil carbon across fallow time gradients. The mean
and standard error are shown for years 2006 (left) and 2007 (right).
See Table 3 for significance of all variables. All abbreviations: Corg
soil organic carbon, MBC soil microbial carbon, MBC/Corg (%) the
percent of microbial carbon to soil organic carbon
succession. An alternative explanation of the slower
decomposition and nutrient mineralization, may be the
recalcitrant nature of belowground litter at high latitudes
(Flanagan and Veum 1974; Van Cleve and Yarie 1986).
The establishment of native species may lead to an increase
in undecomposed belowground litter that may take longer
than our time series to become incorporated into soil
organic matter. These two mechanisms may in combination
have caused the significant decline in soil organic carbon
over fallow time.
Our study also showed a significant decline in soil
nitrogen with fallow time. This isn’t consistent with many
other studies and also does not correspond with the
increased legume abundance. Other studies have shown
that soil N content in the top 25 cm did not significantly
correlated with ecosystem age in the restored prairies (Brye
and Kucharik 2003). Total soil N content in the top 30 cm
increased significantly from year to year, however, total
soil N content in the 30–60 cm depth interval did not differ
significantly (Brye and others 2002). Knops and Tilman
(2000) found that soil total carbon, nitrogen, and the carbon
to nitrogen ratio (C:N) all were significantly positively
correlated with field age since abandonment and soil
nitrogen in the 0–10 cm depth increased with field age, but
there was no change in the 10–60 cm depth horizon.
Therefore, it is necessary to consider soil depth when
studying soil nutrient accumulation. We hypothesized that
soil nitrogen increases during a fallow period, if legume
abundance increases, because legumes might increase
activity of soil microbes involved in mineralization (Spehn
and others 2000). Our results have shown that the legume
cover and aboveground biomass increased over fallow
time, but similarly to the soil carbon decline, the decrease
in soil nitrogen might be caused by a redistribution of soil
nitrogen into the plant or litter nitrogen.
Soil microbial biomass is sensitive to the changes in
soil function over the time scale of secondary succession
(Schmidt and others 2007). Manlay and others (2000)
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762
Environmental Management (2009) 44:755–765
Table 3 The characteristics of fitted curve between fallow time and several variables describing the soil at these sites
Variables
Depth (cm)
Regression
2006
df
Corg
MBC
MBC/Corg (%)
MBC/MBN
MBC/TN (%)
C/N
MBN
TN
2007
R2
P
df
R2
P
b
0–20
1
0.868
0.021
1
0.010
0.916
20–40
1
0.806b
0.038
1
0.978c
0.001
0–20
20–40
2
2
0.400
0.126
0.598
0.874
2
2
0.316
0.528
0.648
0.471
0.841
0–20
2
0.525
0.475
2
0.159
20–40
2
0.271
0.729
2
0.925a
0.075
0–20
1
0.248
0.392
1
0.151
0.849
20–40
1
0.009
0.879
\
\
\
0–20
2
0.533
0.467
2
0.273
0.728
20–40
2
0.807
0.193
2
0.971b
0.029
0–20
2
0.647
0.352
2
0.102
0.897
20–40
2
0.793
0.206
2
0.783
0.216
0.991
0–20
2
0.751
0.249
2
0.010
20–40
2
0.434
0.565
\
\
\
0–20
1
0.822b
0.034
1
0.002
0.941
20–40
1
0.884b
0.015
1
0.848b
0.026
2
R values from regression analyses testing for first and second order polynomial
a
Statistical significant differences at the P B 0.1
b
Statistical significant differences at the P B 0.05
c
Statistical significant differences at the P B 0.001
‘‘\’’ = indicates not applicable; Corg soil organic carbon, MBC soil microbial carbon, MBN soil microbial nitrogen, TN soil total nitrogen, C/N the
ratio of soil organic carbon and soil total nitrogen, MBC/Corg (%) the percent of microbial carbon to soil organic carbon, MBC/TN (%) the
percent of microbial carbon to soil organic nitrogen
Fig. 4 Changes in soil nitrogen
across the fallow time gradient.
The mean and standard error are
shown for years 2006 (left) and
2007 (right). See Table 3 for
significance of all variables. All
abbreviations: MBN soil
microbial nitrogen, TN soil total
nitrogen
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Environmental Management (2009) 44:755–765
763
Fig. 5 Changes in the ratios of soil carbon and nitrogen across the
fallow time gradient. The mean and standard error are shown for years
2006 (left) and 2007 (right). See Table 3 for significance of all
variables. All abbreviations: Corg soil organic carbon, MBC soil
microbial carbon, MBN soil microbial nitrogen, TN soil total nitrogen,
C/N the ratio of soil organic carbon and soil total nitrogen, MBC/Corg
(%) the percent of microbial carbon to soil organic carbon, MBC/TN
(%) the percent of microbial carbon to soil organic nitrogen
reported that microbial biomass showed no clear variation
in sampled 0–10 cm soil along fallow time (\30 years).
Landgraf (2001) found that microbial biomass carbon and
MBC/Corg ratios increased along fallow time (\3 years),
but microbial biomass N decreased. Jia and others (2005)
found that microbial biomass carbon and MBC/Corg
readily decreased but microbial biomass nitrogen exhibited no trend along fallow time (\15 years). However, our
study is inconsistent with these patterns. We found that
microbial biomass carbon and MBC/Corg in the upper
20 cm increased in the former stage of fallow(\6 years),
and declined from 8 to 18 years, and after 18 years
increased again. This suggests that changes in microbial
biomass along fallow time gradients are different among
ecosystems. MBC/Corg reflects the link and interaction
between microbial biomass and soil organic C (Insam and
Domsch 1988) and can serve as an index for monitoring
soil perturbation (Smith and Paul 1990). The percent of
microbial C to soil organic C was significantly greater,
which indicates that microbial biomass potentially plays a
greater role in soil C turnover than the plant detrital
matter in alpine meadow We found that the microbial
biomass N in the upper 20 cm decreased sharply during
the early stage of fallow (\8 years), followed by an
increase in later stages. We hypothesize that the increasing plant cover and aboveground biomass over time
increased the plant litter pool, which may have led to a
decrease in soil temperature, which resulted in slower
decomposition and nutrient mineralization and a slower N
cycling leading to lower soil available nitrogen levels
(Tilman and others 1996; Knops and others 2001).
Diversity, vegetation structure, and ecological processes
can be regarded as the criteria of restoration success
(Ruiz-Jaen and Aide 2005). Our results indicated that
fallow time had a great influence on development of plant
community and soil process in this ecosystem and
123
764
supported our hypothesis that soil recovery is slower than
the vegetation recovery during succession.
We found that during natural restoration succession, the
vegetation developed faster than soil processes, which
suggest that fallow would not significantly improve the soil
(Odum 1960; Aweto 1981; Odum and others 1984; Lee
2002).
Conclusions
Our results suggest that fallow time had a greater influence
on development of plant community than soil process in
abandoned fields in sub-alpine meadow ecosystem. The
species richness of different functional group (forb, grass
and legume species) showed the same hump-shaped patterns along fallow time gradient, but the corresponding
biomass exhibited no trend. Soil organic carbon and total
nitrogen showed the more significant linear-declined
models except in the upper 20 cm in 2007 along fallow
time gradient. MBC (0–20 cm), MBC/Corg (%) (0–20 cm),
MBC/TN (0–20 cm), C/N (20–40 cm) and MBN
(0–20 cm) showed the U-shaped model along fallow time
gradient. These results indicate that the development of
plant community may lead to nutrient limitation at the
latter stage of succession. However, the increased microbial biomass at the latter successional stage may promote
increased decomposition of plant litter. Therefore, abandoned fields in sub-alpine meadow ecosystem have a high
resilience and stronger rehabilitating capability under the
natural recovery condition. These results support a
‘‘humped-shaped model’’ of recovery, suggesting that
15 years of fallow leads to the best restoration of these
degraded fields.
Acknowledgments This research was supported by a grant (No.
30871823) from the Natural Science Foundation of China and the
Research Station of Alpine Meadow and Wetland Ecosystems of
Lanzhou University. We are very grateful to professor Guozhen Du,
Shiting Zhang and Xianhui Zhou for helping in field investigation and
two anonymous reviewers for the constructive suggestions on our
manuscript.
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