Effects of Grazing Regimes on Plant Traits and Soil Nutrients in an Alpine Steppe, Northern Tibetan Plateau
Plateau. PLoS ONE 9(9): e108821. doi:10.1371/journal.pone.0108821
Effects of Grazing Regimes on Plant Traits and Soil Nutrients in an Alpine Steppe, Northern Tibetan Plateau
Jian Sun 0
Xiaodan Wang 0
Genwei Cheng 0
Jianbo Wu 0
Jiangtao Hong 0
Shuli Niu 0
Cheng-Sen Li, Institute of Botany, China
0 1 Synthesis Research Centre of Chinese Ecosystem Research Network, Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences , Beijing , China , 2 The key laboratory of mountain surface processes and eco-regulation, Institute of Mountain Hazard and Environment, Chinese Academy of Sciences , Chengdu , China
Understanding the impact of grazing intensity on grassland production and soil fertility is of fundamental importance for grassland conservation and management. We thus compared three types of alpine steppe management by studying vegetation traits and soil properties in response to three levels of grazing pressure: permanent grazing (M1), seasonal grazing (M2), and grazing exclusion (M3) in the alpine steppe in Xainza County, Tibetan Plateau. The results showed that community biomass allocation did not support the isometric hypothesis under different grassland management types. Plants in M1 had less aboveground biomass but more belowground biomass in the top soil layer than those in M2 and M3, which was largely due to that root/shoot ratios of dominant plants in M1 were far greater than those in M2 and M3. The interramet distance and the tiller size of the dominant clonal plants were greater in M3 than in M1 and M2, while the resprouting from rhizome buds did not differ significantly among the three greezing regimes. Both soil bulk density and soil available nitrogen in M3 were greater than in M1 at the 15-30 cm soil depth (P = 0.05). Soil organic carbon and soil total nitrogen were greater in M3 than in M1 and M2 (P = 0.05). We conclude that the isometric hypothesis is not supported in this study and fencing is a helpful grassland management in terms of plant growth and soil nutrient retention in alpine steppe. The extreme cold, scarce precipitation and short growing period may be the causation of the unique plant and soil responses to different management regimes.
Funding: This research was jointly funded by the Knowledge Innovation Program of the Chinese Academy of Sciences (KZCX2-XB3-08), CAS Strategic Priority
Research Program (XDA05050602), and the Open Fund of Key Laboratory of Ecosystem Network Observation and Modelling (110301A1PA). The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Alpine grasslands make up the dominant ecosystem occupying
approximately 94% of Northern Tibet . The natural
environment of the region is extremely harsh, and the alpine steppe, a
fragile ecosystem, is extremely susceptible to the impacts of human
activities . It suffers from overgrazing, deforestation, and the
harvesting of numerous herbs commonly used in traditional
medicines . Studies examining the response of above- and
belowground biomass, the root/shoot ratio, the morphological
characteristics of dominant plants, and the soil properties to
human disturbance offer important insights that can contribute to
adopting the most effective approach to grassland management in
an alpine steppe, in which it is particularly difficult to recover from
ecosystem degradation due to the regions long period of frost and
relatively short growing season [3,6].
Although grazing and fencing, both of which have a substantial
affect on vegetation traits and soil properties , are the most
prevalent management regimes for grasslands worldwide, and
although the effects of herbivores on soil properties in (sub)alpine
ecosystems have recently been reported [10,11], knowledge about
plants and soils in response to grassland management regimes (i.e.,
fencing and grazing) in the Tibetan Plateau remains limited due to
an extremely difficult geographic situation [9,12]. With regard to
soil properties, it has been documented that grazing depresses soil
carbon storage by changing the plant biomass and composition of
a Tibetan alpine meadow . In contrast, Shi et al.  found
grazing exclusion to decrease soil organic carbon storage in an
alpine grassland of the Tibetan Plateau, while another report
suggested that seasonal grazing might enrich soil nutrients .
Such conflicting results indicate that different grazing intensities
may have varying impacts on soil properties.
Understanding the influence of different management types on
grassland production is essential for improving grassland
conservation and management . Previous studies have yielded
varying results for aboveground biomass changes. Grazing thus
increased  or decreased  aboveground production in
different cases. The fencing optimization hypothesis posits that
fencing significantly enhances above- and belowground biomass
by means of carbon reallocation to plant growth and promotes
increases in soil nutrient concentrations [19,20]. Belowground
biomass has also been shown to be affected by grazing, with some
studies indicating that plants reduce the proportion of
aboveground parts and allocate more biomass to belowground parts, so
as to geminate and resist environmental stress (i.e., grazing
pressure) . Conversely, more belowground biomass was
Figure 1. The experiment sites in alpine steppe, northern Tibetan Plateau.
allocated to the surface layer than the subsurface of the soil
profile with increasing grazing pressure . For instance, the
root to shoot ratio in the grazing pattern was significantly higher
than for the mowing and fencing patterns in temperate grassland
The root:shoot ratio provides the basis for understanding the
response or adaptive strategies of plants to environmental stress
[24,25], and reflects how plants respond to different selection
pressures [26,27]. Theory predicts the ratio of roots to shoots to
respond isometrically across different individuals and community
types under varying environmental conditions . While
biomass allocation has been widely examined from individual to
community to ecosystem levels , few studies compare the
biomass partitioning of dominant alpine species under different
grassland management types.
Aside from biomass, the morphological characteristics of clonal
plants are also regarded as a sensitive index for assessing the
possible effect of grazing pressure [36,37]. The traditional theory is
that a clone with a guerrilla-like foraging strategy should be able to
locate and exploit favorable patches in which competitors are
absent. In a habitat in which potential competitors are more
homogeneously distributed, a phalanx clone exhibits a
consolidation strategy and may be able to persist and monopolize locally
available resources . However, we know little about the
responses of the morphological characteristics of clonal plants to
grazing pressure in alpine steppes.
In this study, we examined plant traits and soil properties in
response to different grassland management strategies in the
Northern Tibetan Plateau. The specific aims are: (1) to reveal
the impact of different grassland managements on plant traits
and soil properties and to test the grazing optimization
hypothesis; (2) to test the isometric partitioning theory on
different alpine species under varying grassland management
patterns; and (3) to explore the effects of grazing stress on
Materials and Methods
Our study was conducted in the Alpine Steppe Experiment
Station (N 30u579, E 88u429, 4675 m a.s.l.) in Xainza County,
Northern Tibet (Fig. 1). The annual mean air temperature of this
region is 0uC, while the mean air temperature ranges from 2
10.1uC in January and 9.6uC in July. The average annual
precipitation is 300 mm. There is no absolute frost-free season,
and the frosty period can last up to 279.1 days . The regions
soil is classified as steppe soil with sandy loam . Vegetation
coverage of the alpine steppe is approximately 20% and is
dominated by Stipa purpurea (Bunch grass) and Carex moorcrofii
(sedge family, creeping rhizomes) (Fig. 2A). Other common species
include Stellera chamaejasme Linn. (Bunch weeds), Oxytropis
glacialis (Bunch weeds), and Leontopodium alpinum (Fig. 2B). All
of these plants are perennial herbs.
Grazing treatments and experimental plots
There were three grazing treatments in this study. i.e, M1
(grazing): The pasture is always used for grazing. M2 (seasonal
grazing): The pasture has been used for grazing in the
nongrowing seasons but not in the growing season (from May to
September) since 2007. M3 (grazing exclusion): Herbivores have
been excluded from the pasture since 2010.
The study area was divided into three blocks. Each block
contained three plots, the eastern plot having a grazing intensity of
M2, the middle plot a grazing intensity of M3, and the western
plot a grazing intensity of M1 (Fig. 1). The dimensions of each M3
fenced plot were 666 m; the dimensions for each M2 plot were
2006500 m. Three M1 plots were located outside of the fenced
area in each block, with each plot having dimensions of
2006500 m. In each plot, a quadrat (30 cm630 cm) was used
to measure biomass and take samples. The estimated average
livestock density in both M1 and M2 was approximately 120 sheep
units per km2. (The sheep unit is the most frequently used unit
of measurement for evaluating the carrying capacity of pasture
areas in China and includes figures for cattle, which are converted
to sheep; thus, e.g., one cow is equivalent to five sheep based on
the average weight of a cow) .
No specific permits were required for the samples collected from
any of the sites, and the field studies did not involve endangered or
Biomass measure and sample taking
We established a 30 cm630 cm quadrat in each of the sampling
plots to harvest aboveground biomass (AGB) in late August of
2012. After harvesting the aboveground biomass, we took soil
samples by auger with a 5-cm core diameter at two depths (0
15 cm and 1530 cm) to estimate belowground biomass (BGB).
According to previous research, most belowground biomass is
located in the top 30 cm layer . Soil samples were also taken at
depths of 015 cm and 1530 cm in order to measure soil
elements. After being air-dried and sieved (2 mm mesh), the soil
samples were carefully handpicked to extract the surface organic
materials and fine roots for an analysis of soil chemical properties.
Soil nutrients (including soil organic carbon, soil total nitrogen
content, available nitrogen, total phosphorus and available
phosphorus) were determined using standard protocol .
In order to estimate the root:shoot ratio of the dominant species
(S. purpurea, C. moorcrofii, O. glacialis, and L. alpinum), we took
three soil blocks in each sampling plot of different management
regimes. The patch was excavated with a spade with a diameter of
20 cm to a depth of 30 cm, which was selected based on the root
morphological traits of the species . The root samples obtained
from the sites were immediately placed in a cloth bag and then
soaked in water to remove the residual soil by means of a 0.5 mm
sieve. The roots of each sample were carefully separated from soil
and other belowground materials first. Then individuals of the all
species were carefully separated from other plant roots. Finally, we
separated the roots and shoots of each individual. Individual
biomass (shoots and roots) and community biomass (AGB and
BGB) was oven-dried at 65uC until a constant weight was
achieved. Individual biomass data were used to analyze allometric
functions under different management regimes (with a total of 40,
45, and 68 individuals in M1, M2, and M3, respectively).
The plant morphology of C. moorcrofii is regarded as a fairly
good indicator that reflects the different grassland management
regimes . We thus sampled C. moorcrofii. from other
30 cm630 cm quadrats at each of the 9 plots. The samples were
then taken back to the laboratory, where the morphological
characteristics (plant height, interramet distance, number of
rhizome buds, and tillering number) were immediately measured.
Special attention was paid to avoid destroying the structural
integrity of the plant throughout this process.
We performed a standardized major axis (SRMA) regression to
examine whether AGB and BGB scale isometrically at an
individual level across all samples, and then explored their
relationships under different management types. The regression
relationship of the form LogAGB = a+bLogBGB was used to
describe the allometric relationship between AGB and BGB,
where x is BGB, y is AGB, a is the intercept, and b is the scaling
slope [25,28,45,46]. The scaling slope and y-intercept of the
allometric function were determined using the software package
titled Standardized Major Axis Tests & Routines Version 2.0
. If a 95% confidence interval of the scaling slope covered 1.0,
the relationship between AGB and BGB was considered to be
One-way ANOVA was used to test differences in soil properties
and biomes (AGB, BGB, and R/S) among the different
treatments, and the Tukey test was used to distinguish differences
at a P = 0.05 level.
The relationship between BGB and AGB under different
grazing pressures was characterized by the linear function
LogAGB = a+bLogBGB (Fig. 3). The slopes of the allometric
relationship were 0.751 (for M1), 0.797 (for M2), 0.671 (for M3),
and 0.815 (for all samples at an individual level), respectively. All
of the slopes differed significantly from 1 at P = 0.05.
Responses of AGB, BGB, and R/S to different
AGB in M1 was slightly but not significantly lower than in M2
and M3 (Table 1). In contrast, BGB of M1, M2, and M3
amounted to 324.87, 244.84, and 261.88 g?m22, respectively. The
ratio of root to shoot in M1 was also higher than in M2 and M3.
The root biomass was mainly distributed in a soil depth of 0
15 cm, while the root biomass in a soil depth of 1530 cm only
accounted for 2.775.62% of total BGB. The ratios of BGB in the
015 cm-layer to BGB in the 1530 cm-layer of M1, M2, and M3
were 26.19, 35.17, and 16.79, respectively.
To investigate the characteristics of biomass allocation further,
we analyzed the dry matter fraction of M1, M2, and M3 in the
Tibetan Plateau (Fig. 4). The results indicated that the roots of
total plants in the Tibetan Plateau amounted to 88.05% (in M1),
85.27% (in M2), and 80.77% (in M3).
Traits of clonal plants under different management types
C. moocroftii was tallest in M3 and shortest in M1 (P,0.05,
Fig. 5A). Both interramet distance (Fig. 5C) and the tiller number
(Fig. 5D) in M3 were significantly larger than in M1 and M2. No
significant differences were found in the number of rhizome buds
among M1, M2, and M3 treatments (P,0.05, Fig. 5B).
Soil properties in response to management types
At a soil depth of 015 cm, soil bulk density, soil organic
carbon, total nitrogen, and available nitrogen were non-significant
among M1, M2, and M3 (Table 2). At a soil depth of 1530 cm,
both soil bulk densiy and soil available nitrogen in M3 were
greater than in M1 at a P = 0.05 level. Soil organic carbon and soil
total nitrogen in M3 were greater than in M1, and M2 (P = 0.05).
Based on the results of our SMA analysis, biomass allocation at
the community level did not agree with the isometric hypothesis
under different grassland management types. Plants consistently
sense changes in their environment and often allocate a greater
proportion of their biomass to the root system when water or
mineral elements are scarce . Moreover, roots have also been
found to store carbohydrates in alpine grasslands . In the
alpine steppe, greater plant biomass allocation to belowground
reflects the plants response to the harsh alpine environment
(limited precipitation and low temperatures) for survival. Another
reason may be the relatively narrow variation in plant size in that
region. Moreover, many species in the Tibetan alpine grasslands
do not have typical hierarchical branching structures , which
did not meet the assumption that stem length scales isometrically
with respect to root length. This characteristic is clearly reflected in
the root morphology structure shown in Fig. 2B and Fig. 5.
Biomass allocation in these areas may thus support the allometric
biomass partitioning hypothesis, rather than the isometric
Responses of AGB, BGB, and R/S to different
AGB in the grazing plots was found to be lower than in the
nongrazing plots, which is in agreement with the findings of
MedinaRoldan et al. . We suggested that alpine grassland production
might be decreased to some degree by grazing as a result of the
consumption effect of the livestock. The higher BGB in M1 than
M2 and M3 in our alpine steppe conflict with the results of Cheng
et al. , who found grazing to significantly decrease
belowground biomass in the Loess Plateau. Gao et al.  also reported
significantly less belowground biomass under conditions of heavy
grazing in comparison with a non-grazing site in Inner Mongolia.
The conflicting results between our study and previous studies in
other areas probably stem from differences in environmental
conditions. In the extreme cold region of alpine grassland, plants
reduce the proportion of aboveground parts and allocate larger
amounts of biomass to belowground parts in order to germinate
and resist grazing pressures . More BGB in the top soil layer of
M1 than M2 and M3 suggests that grazing results in more
belowground biomass being allocated to the topsoil , possibly
due to the alpine environment inhibiting root growth in ungrazed
plots. We did not find an ameliorating effect of reduced grazing
(M2) or grazer exclusion (M3), suggesting that the effects of
grazing cessation may only be detectable in the long term, as
proposed by Steffens et al. .
The root:shoot ratio (R/S) in M1 was much larger than in M2
and M3, suggesting that plants allocate more to BGB than AGB in
order to maximize resources for optimal growth in the grazed
environment . We compared the dry matter fraction of M1,
M2, and M3 in the Tibetan Plateau (Fig. 4) with dry matter
fractions in Argentina, Bolivia, Ecuador, the Arctic, and the Alps
, and we found that the proportion of BGB was much higher
in our study sites than for plants in a semi-arid grassland ecosystem
(Bolivia), mountain grassland ecosystem (Argentina), and a humid
mountain grassland ecosystem (Ecuadorian Andes). The main
reason may be associated with the comparatively slow depletion of
carbohydrates in roots, resulting from low respiration rates in the
extremely cold winter, and the slower root turnover in colder
environments . Meanwhile, long-term grazing results in a
higher BGB fraction in the Tibetan Plateau than for plants in
other cold alpine environments and the Arctic.
The clonal plant in response to different management
Clonal plants defend against large herbivores by regulating their
morphological characteristics . Clonal plant C. moocroftii in
M3 was notably taller than in M1 and M2 because it was not
bitten by livestock, and they can plastically respond to
environmental heterogeneity by placing ramets and changing tiller size in
favorable sites [57,58]. We found the interramet distance and tiller
number in M3 to be greater than for plants in M1 and M2. Tillers
may produce more daughter tillers as a result of increased nutrient
availability in grazing exclusion. C. moocroftii thus responds to
grazing by decreasing the tiller number . The results also
indicate that C. moocroftii may have both phalanx and guerrilla
strategies. The phalanx strategy involves the production of a
compact structure of closely spaced ramets (i.e., M1), and the
guerrilla strategy involves the production of loosely arranged and
more widely spaced ramets in order to seek out more soil nutrients
in a relatively suitable habitat (i.e., M3).
Clonal growth by means of lateral roots is regarded as a typical
trait of opportunistic species growing in disturbed habitats, as such
growth potentially produces a large number of buds on lateral
roots . However, our results implied that different grassland
management systems did not affect resprouting from rhizome
buds, which suggests that reprouting from rhizome buds is not a
major adjustment stragegy in response to grazing intensity. This
finding is probably due to the short time period since the
implementation of fencing and seasonal grazing.
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Soil properties in response to different management
Grazing intensity is one of the most important factors
influencing soil properties [50,60]. It has been documented that
the trampling action of grazing animals impacts the soil by
increasing bulk density  and mechanical resistance, and
reducing porosity, water infiltration, and aggregate stability ,
and native perennial cover and litter cover, with the consequence
of changing the soil nutrient concentrations . In our study,
bulk density was found to increase with increasing grazing
intensity, and all soil organic carbon, total nitrogen, and available
nitrogen contents in M3 were slightly higher than in M1 and M2.
We thus report that grazing exclusion may improve soil N
availability. Arevalo et al.  found an increase in soil
phosphorus content in response to increased goat grazing pressure
in pastures. In contrast, our results indicated that soil total
phosphorous and available phosphorous contents in M1 did not
differ significantly from those of M2 and M3. The extreme cold,
limited precipitation and short growing period may lead to no
obvious change in phosphorus content.
By studying plant traits and soil nutrients in response to grazing
intensity in an alpine steppe, we found that the isometric
hypothesis is not supported in this particular region. The extreme
cold, limited amount of precipitation and short growing period
may lead to the plants and soils unique to different management
types. Overall, the study suggests that the implementation of
grazing exclusion played a positive role in the sustainable
development of the alpine steppe region.
The authors are grateful to two anonymous reviewers all gave very helpful
Conceived and designed the experiments: XDW GWC. Performed the
experiments: JS JBW JTH. Analyzed the data: JS. Contributed reagents/
materials/analysis tools: JS GWC JTH. Wrote the paper: JS SLN.
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