Journal of
Plant Ecology
VOLUME 9, NUMBER 5,
PAGES 508–519
October 2016
doi:10.1093/jpe/rtv083
Advance Access publication
5 January 2016
available online at
www.jpe.oxfordjournals.org
Effects of grazing and precipitation
variability on vegetation dynamics
in a Mongolian dry steppe
Tserenpurev Bat-Oyun1,2,*, Masato Shinoda3, Yunxiang Cheng4
and Yadamjav Purevdorj5
1
Arid Land Research Center, Tottori University, Hamasaka, Tottori 680-0001, Japan
Information and Research Institute of Meteorology, Hydrology and Environment, Ulaanbaatar 15160, Mongolia
3
Graduate School of Environmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
4
College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
5
Department of Food Science and Human Wellness, Rakuno Gakuen University, Ebetsu, Hokkaido 069-8501, Japan
*Correspondence address. Arid Land Research Center, Tottori University, Hamasaka, Tottori 680-0001, Japan.
Tel/Fax: +81-857-21-7030; E-mail: [email protected]
2
Abstract
Aims
Grazing and water availability are the primary drivers of vegetation dynamics in grazing-dominated regions of Mongolia with a
semi-arid climate and frequent droughts. Nomadic animal husbandry still plays a large part in the economy of Mongolia, but
more variable precipitation regime and increase in livestock
number have severely affected grassland ecosystems through
overgrazing, leading to pasture degradation. This study aimed to
examine the effects of grazing exclusion, interannual variation
of plant-available precipitation (PAP) and their interaction on the
aboveground biomass (AGB) of each dominant species, the AGB
of annual species and the total AGB in a Mongolian dry steppe,
using long-term field data.
Methods
To detect the effect of grazing on vegetation dynamics, vegetation
surveys were conducted in a non-grazed exclosure zone and a fully
grazed area outside the exclosure. We assessed the effects of grazing, PAP and their interaction on AGB parameters using a generalized linear model. A detrended correspondence analysis (DCA)
was used to visualize the effects of grazing and PAP on the AGB of
each species.
Important Findings
Grazing, PAP and their interaction had significant effects on AGB. The
effect of grazing on AGB was larger with higher precipitation and higher
amounts of AGB (i.e. forage) while AGB was strongly limited in drought
years, which resulted in a smaller grazing effect. The current year PAP
had the highest impact (r = 0.88, P < 0.01) on AGB. The dominance of
annual species was characterized by the amount of PAP in the current
and preceding years: annuals dominated in wet years that followed consecutive dry years. The DCA Axis 1 reflected the variation of AGB with
interannual variation of PAP while the DCA Axis 2 differentiated the grazing effect. The DCA scatter diagram based on species score illustrated
that Artemisia adamsii (an unpalatable herb) was clearly linked to grazing
disturbance whereas palatable perennials such as Agropyron cristatum,
Stipa krylovii and Cleistogenes squarrosa were related to grazing abandonment and wetter conditions. In brief, number of livestock, hence the
grazing impacts on vegetation dynamic in this region could have driven
by forage availability, which is mainly controlled by current-year PAP.
Keywords: aboveground biomass, annual species, drought,
grazing, plant-available precipitation
Received: 23 December 2014, Revised: 29 September 2015,
Accepted: 29 December 2015
INTRODUCTION
For several thousand years, Mongolian pastoral nomads have
developed traditional grazing lifestyle adapted to the country’s cold, dry climate. Mongolia is one of the few countries
where nomadic animal husbandry still plays a large part in
the economy. This industry accounts for 16.5% of GDP, and
27.8% of the population relies on it as a source of food and
income (National Statistical Office of Mongolia 2014). Natural
grassland covers 80% of the country, and the Mongolian
steppe comprises a major portion of the East Asian grasslands (Batima and Dagvadorj 2000). This grassland is a major
source of forage for livestock. The frequencies of extreme
events such as drought and dzud (severe winter) have been
© The Author 2016. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
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Bat-Oyun et al. | Effects of grazing and precipitation on vegetation509
increased due to human induced climate change, especially in
the last two decades (Batima and Dagvadorj 2000). This condition has led to more threats in livestock farming and pasture
management, increasing their vulnerability. In 1992, there
was an abrupt change in social and economic systems, from
a centrally planned socialist economy (state-owned livestock
and pasture land with systematic control by state on pasture
use) to a free market economy (livestock was privatized but
pasture land remained state-owned). Herders became entirely
responsible for their own herding management, leading to
increases in herd number (Chuluun and Ojima 2001). The
number of livestock increased by 49.5% from 25.7 million
in 1992 to 51.9 million in 2014 (National Statistical Office
of Mongolia 2014). Such increases in livestock have severely
affected grassland ecosystems through overgrazing, leading to
pasture degradation (Hilker et al. 2013).
Previous studies have revealed that grazing is a key anthropogenic disturbance on natural grasslands in arid and semiarid ecosystems, and plays an important role in shaping the
structure and functions of plant communities (Cingolani et al.
2005; Milchunas et al. 1989). Increased grazing has been
tended to increase plant mortality and ultimately decrease
species richness especially in water- and nutrient-limited
environments (Fynn and O’Connor 2000; Proulx and
Mazumder 1998). Grazing also reduces the abundance and
biomass of palatable species and increases the proportion of
unpalatable and grazing-resistant species (Adler and Morales
1999; Hickman and Hartnett 2002). Other studies have demonstrated that while overgrazing can result in grassland degradation (Cooper et al. 2005), moderate grazing can promote
plant growth and increase species diversity (Huston 1979;
Sasaki et al. 2008).
Drought and grazing interact closely to affect ecosystems
in grazed grasslands (Milchunas et al. 1989). In the arid and
semi-arid regions of Mongolia, frequent drought events are
the key factor driving livestock dynamics by limiting forage
availability, which may further exacerbate dzud conditions
(Begzsuren et al. 2004). In Mongolia, grazing land is stateowned and free for public use. When drought occurs, herders move their herds in search of better forage and water to
build up the condition of their livestock and increase their
chances of surviving harsh winter conditions. Variability in
precipitation and drought have substantial impacts not only
on the quantitative aspect (biomass, Lauenroth and Sala
1992; Le Houérou et al. 1988; Yang et al. 2008) but also qualitative aspects such as phenology (Shinoda et al. 2007); species composition (Bai et al. 2004; Cheng et al. 2011; Kinugasa
et al. 2012; Ni 2003); plant life cycles (Le Houèrou 1996; Li
et al. 2011, Loeser et al. 2007; Tilman and El Haddi 1992); and
radiation-use efficiency (Bat-Oyun et al. 2012).
Vegetation dynamics can be studied using equilibrium and
non-equilibrium models, although the debate on which to
use has not been adequately resolved (Díaz et al. 1999). The
equilibrium model suggests a tight coupling of plant–herbivore systems, with grazing being important in ecosystem
modification. In non-equilibrium models, abiotic factors
such as precipitation have a greater influence on vegetation
dynamics than grazing (Sullivan and Rohde 2002). Wiens
(1984) suggested that drier environments are affected by
unpredictable abiotically driven dynamics to a greater extent
than wetter environments. Therefore, the effects of grazing
and climate would be more complex in the environments
characterized by low and erratic rainfall. Previous research
indicated that environments with less than 250 mm of annual
precipitation and a coefficient of variation (CV) greater than
33% in interannual precipitation are better described by nonequilibrium model (Ellis 1995; Illius and O’Connor 1999).
Based on these thresholds, we expected that the interannual
variation of precipitation in the Mongolian semi-arid ecosystem would have a greater effect on vegetation than grazing,
and we ascribed vegetation changes mainly to interannual
variation of precipitation rather than grazing, reflecting nonequilibrium dynamics.
This study aimed to investigate the effects of year-round
grazing (hereinafter referred to as grazing) and precipitation
variability on vegetation dynamics in a Mongolian dry steppe
with 9 years of species-specific, systematically observed datasets under naturally grazed and grazing-excluded conditions.
The response variables are the aboveground biomass (AGB)
of each dominant species, the AGB of annual species (annuals) and total AGB.
MATERIALS AND METHODS
The present study was conducted in Bayan-Unjuul county
(47°02′37.2″N, 105°57′04.9″E, 1200 m asl), in a moderately
dry steppe (Vostokova and Gunin 2005), with steppe vegetation as described by Yunatov (1976). The region’s climate is
semi-arid, with an aridity index ranging between 0.2 and 0.5
(UNEP 1992). The site is characterized by low annual precipitation, with high inter- and intra-seasonal variability, frequent
droughts and sandy, nutrient-poor soils (Shinoda et al. 2010).
Meteorological observations were collected ~400 m southeast
of the center of the observation site by the monitoring station
of the Information and Research Institute of Meteorology,
Hydrology and Environment (IRIMHE) of Mongolia. Data
from the IRIMHE station showed that the long-term (1995–
2012) annual mean temperature was 0.1°C (16.8°C during
the growing season, May–Aug) with a minimum of −24.2°C
in January and a maximum of 20.4°C in July. Annual precipitation averaged from 1995 to 2012 was 165.8 mm with high
interannual variation (CV = 29%), and precipitation was concentrated in the growing season (131.0 mm, CV = 30%). Over
past decades, the site has experienced droughts in 1999, 2000
and 2002 [<100 mm of plant-available precipitation (PAP)],
with the most severe drought (<72 mm of PAP) in 2005–2007.
In this study, PAP is the accumulated precipitation from 1
May through the earlier dates of biomass sampling as defined
by Shinoda et al. (2014). The long-term average (1995–2012)
of PAP was 122.5 mm (Fig. 1a). For the years when we did not
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Journal of Plant Ecology
Figure 1: interannual variations of (a) PAP (1999–2012) and the long-term average (1995–2012) of PAP (b) aboveground biomass in the
grazed (G) and non-grazed (NG) plots (2003–2012, except in 2003 for NG plots and in 2009 both plots). *P < 0.05, **P < 0.01, ***P < 0.001.
measure AGB (1999–2002 and 2009), we considered a period
from 1 May to 25 Aug as the growth period. It is noted that
four high precipitation events (one large event at 21.2 mm/
day in 2003 and three large events at 14.2–25.7 mm/day
within a few days in 2008) were recorded early in the growing season, which was exceptional.
The soil at the site was classified as a Kastanozem (FAO/
ISRIC 1998), which is widely distributed in the plain steppes
of Mongolia (Dorjgotov 2003). The soil has a low water-holding capacity, and the vegetation cover is sparse. Year-round
free grazing occurs of large livestock herds dominated by goats
and sheep, with some horses and cattle. A 300 × 300 m area
at the study site has been surrounded by a fence since June
2004, to protect this area from grazing by livestock. The exclosure was established to detect the effect of long-term grazing
exclusion on natural grassland (Shinoda et al. 2010). Before
the exclosure was constructed, livestock grazing had long been
experienced in the area. The Bayan-Unjuul, including our site,
was grazed with a stocking rate of ~0.4 sheep equivalent ha−1
for 4 years (2000–2003) before establishing the exclosure.
This stocking rate was classified as light to moderate grazing
in a similar steppe region of Mongolia (Shinoda et al. 2010).
The study area was homogeneous before the exclosure was
established.
Data collection
The AGB of each species was collected and measured once
at the end of August or September each year between 2003
and 2008 and between 2010 and 2012, which coincides with
the period of peak plant growth. Exceptions to this were in
2007, when the AGB was sampled and measured in July, and
in 2009 for which data are missing. No data were available in
2003 for the non-grazed area since the fence was not erected
until 2004. The experimental layout was a fully randomized
design. To detect the effect of grazing on vegetation dynamics,
the vegetation survey was conducted in two types of areas:
a non-grazed area located inside the exclosure, and a fully
grazed area outside the exclosure. Sampling with quadrats
is commonly used for most plant communities (Cox 1990).
During each annual survey 1 × 1 m quadrats for this sparse
grassland ecosystem were randomly placed in the grazed area
outside the exclosure (G plot) and non-grazed area inside
the large exclosure (NG plot). Each G and NG plot included
four random replications (quadrats) at the four corners of
the outside and inside of the exclosure. The aboveground
parts of each species were clipped at ground level in four 1
m2 quadrats of the G and NG plots, respectively. Wide buffer
zones were used for both G and NG plots to avoid edge effects
from the fence. Each year the sampled plots were marked to
Bat-Oyun et al. | Effects of grazing and precipitation on vegetation511
avoid re-sampling in the subsequent years. All collected plant
materials were oven-dried at 80°C for 3 days and were then
weighed to determine their dry weights.
NG plots for each year was tested by t test with Bonferroni’s
adjustment.
RESULTS
Data analysis
Detrended correspondence analysis (DCA; Hill and Gauch
1980) was used to visualize the effects of grazing and PAP on
the AGB of each species. DCA assumes that the most important environmental gradient causes the largest variation in
the species composition. DCA applies detrending to avoid an
arch effect by dividing the first axis into several segments and
then centering the second axis on zero within each of those
segments (Gauch 1982). Ordination diagrams were plotted
for the first and second axes, which had considerably higher
eigenvalues than the lower order axes. To evaluate the relationship between the DCA axes and environmental factors, a
regression analysis was conducted.
We evaluated the effects of grazing, interannual variation
of PAP and their interaction on the AGB of each dominant
species, the AGB of annuals and total AGB using a generalized linear model with normal distribution and an identity
link function.
Simple regression analysis and Pearson’s correlation were
used to determine the impacts of PAP parameters on the AGB
parameters. First, we tested for effects of the current year (t),
then combinations of first to fifth preceding years (e.g. (t−1),
(t−1) + (t−2), (t−1) + (t−2) + (t−3), etc.). Finally, we measured
the association effect of the current and preceding years’ (e.g.
(t) + (t−1), (t) + (t−1) + (t−2), (t) + (t−1) + (t−2) + (t−3), etc.)
total PAP on the current year’s total AGB and the proportional
AGB of annuals in the NG plots. Statistical analysis was performed with JMP 12 (SAS Institute, Cary, NC, USA) statistical software and R software (version 2.8.0, R Development
Core Team 2008). The difference in AGB between G and
Effects of grazing, PAP and their interaction
on AGB
Analysis of the generalized linear model demonstrated that
AGB was significantly affected (P < 0.001) by grazing, interannual variations in PAP and their interaction during the
study period (Table 1).
In general, grazing resulted in a significantly lower AGB
± standard error (72.0 ± 12.6 g/m2) than in the NG areas
(123.1 ± 29.6 g/m2) during the study period. On an interannual basis, grazing significantly reduced AGB in 2005, 2011
and 2012. This pattern was not consistent in the driest years
of 2006 and 2007, when AGB was slightly higher in the G
plots than in the NG plots (Fig. 1).
The current-year AGB was significantly related to the current-year PAP during the study period. In general, greater
AGB was characterized by wet conditions, whereas the consecutive dry years of 2005–2007 resulted in reductions in
AGB (Fig. 1). However, the results conducted for the NG plots
revealed that the current-year PAP was similar in the two wet
years (137.6 mm in 2004 and 139.6 mm in 2008) and in the
two dry years (69.8 mm in 2005 and 72 mm in 2006), but different AGB were recorded. The AGB was higher but not significantly (P < 0.1) in 2008 (147.5 ± 26.5 g/m2) than in 2004
(93.0 ± 11.9 g/m2); and significantly higher (P < 0.05) in 2005
(87.1 ± 9.0 g/m2) than in 2006 (44.9 ± 6.2 g/m2). To improve
understanding of interannual variations in AGB, we modeled
the current-year AGB in the NG plots against the PAP parameters in the current year, in sequential combinations of the
first to fifth preceding years and in sequential combinations of
Table 1: results of the generalized linear model for the effects of grazing, interannual variation of PAP and their interaction on the AGB
of each dominant species, the AGB of annuals and total AGB during the study period
Grazing (G)
Source
Degrees of freedom (df)
P value
PAP
Sig. level
1
P value
G x PAP
Sig. level
7
P value
Sig. level
7
Agropyron cristatum
0.01
*
0.31
ns
0.46
ns
Stipa krylovii
0.00
***
0.00
***
0.00
***
Cleistogenes squarrosa
0.01
*
0.22
ns
0.74
ns
Elymus chinensis
0.61
ns
0.59
ns
0.56
ns
Carex spp
0.28
ns
0.01
*
0.94
ns
Caragana spp
0.04
*
0.04
*
0.15
ns
Artemisia adamsii
0.03
*
0.00
***
0.12
ns
Chenopodium spp
0.64
ns
0.006
**
1.00
ns
Salsola spp
0.15
ns
0.38
ns
0.86
ns
Annual species
0.06
†
0.02
*
0.41
ns
Total AGB
0.00
***
0.00
***
0.00
***
Here, the AGB of each variable is based on a normal distribution. ns: not significant.
†
P < 0.1, *P < 0.05, **P < 0.01, ***P < 0.001.
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Journal of Plant Ecology
the current and first to fifth preceding years. This allowed us
to test for a possible time lag effect of PAP. The result of this
analysis demonstrated that the current-year PAP had a significant positive impact (r = 0.88, P < 0.01) on AGB. In terms
of the combined effects of PAP over time, PAP in the current
and first preceding year (r = 0.62, P < 0.1) and current and
first two preceding years (r = 0.65, P < 0.1) best explained the
current-year AGB variation (Table 2).
The interactive effect of grazing and PAP on AGB, depicted
by an interaction plot, showed that the differences in AGB
between the G and NG plots increased with higher PAP values
while this difference was strongly limited in drier conditions
(top right corner, Fig. 2k). In the wettest year (164.1 mm of
PAP in 2011), AGB increased sharply from the G plot to the
NG plot, while in the driest year (48.8 mm of PAP in 2007),
AGB is slightly decreased from the G plot to the NG plot (bottom left corner, Fig. 2k). These findings suggest that the grazing effect expressed by AGB differences between the G and
NG plots is enhancing with an increase in PAP.
Effects of grazing, PAP and their interaction on
the AGB of dominant species
In total, 42 species, including 12 annuals, 1 biennial and 29
perennials, were recorded during the study period. As shown
in Fig. 3, the AGB was formed mainly by nine species including the palatable perennial grasses (Agropyron cristatum, Stipa
krylovii, Cleistogenes squarrosa and Elymus chinensis), palatable perennial herbs [Carex duriuscula and Carex korshinskii
(Carex spp.)], an unpalatable perennial herb (Artemisia adamsii), palatable perennial small shrubs [Caragana microphylla
and Caragana stenophylla (Caragana spp.)] and unpalatable
annual herbs [Chenopodium album, Chenopodium aristatum,
and Chenopodium acuminatum (Chenopodium spp.); and Salsola
collina and Salsola ruthenica (Salsola spp.)]. Here, species
Table 2: relationships between AGB, proportional AGB of
annuals (AAGB) for NG plots and different sets of plant-available
precipitation
Possible variables (x)
Response variables (y)
df
r
P
RR (t)
AGB
7
0.88**
<0.01
RR (t) + (t−1)
AGB
7
0.62†
<0.1
RR (t) + (t−1) + (t−2)
AGB
7
0.65†
<0.1
RR (t)
AAGB
8
0.57†
<0.1
RR (t−1) + (t−2) + (t−3)
AAGB
8
−0.74*
<0.05
RR (t−1) + (t−2) + (t−3) + (t−4)
AAGB
8
−0.86**
<0.01
The correlations with high (P < 0.1) or significant impacts (P < 0.05
and P < 0.01) were included in the table, in which RR (t), RR (t−1),
RR (t−2), RR (t−3) and RR (t−4) indicate the PAP amount in the current
and first to fourth preceding years, respectively. For the missing observation year in 2009, only the proportions of annuals were obtained
from the agrometeorological station of IRIMHE, which has observation plots inside and outside the 300 × 300 m enclosure. Significant
correlation coefficients are highlighted in bold.
†
P < 0.1, *P < 0.05, **P < 0.01.
palatability and life cycle was defined based on previous literature (Undarmaa et al. 2015).
The generalized linear model predicting the effects of
grazing on the AGB of each dominant species during the
study period demonstrated that significantly higher AGB for
A. cristatum, S. krylovii, C. squarrosa and Caragana spp. higher,
although not statistically significant, AGB for E. chinensis,
Carex spp. and Chenopodium spp. were found in the NG plots
compared with the G plots. In contrast, significantly higher
AGB for A. adamsii (P < 0.05) and higher (but not significant)
AGB for Salsola. spp. were estimated in the G plots compared
with the NG plots (Table 1). On an interannual basis, in 2005,
2011 and 2012, the years with significant grazing impacts
on AGB, perennial palatable species including A. cristatum,
S. krylovii and C. squarrosa contributed high proportions to the
total biomass in the NG plots. Meanwhile, the proportions of
unpalatable species of A. adamsii, Chenopodium spp. and Salsola
spp. in the G plots were higher relative to the palatable species (Fig. 3).
A significant positive effect of PAP on individual species can
be seen for the AGB of S. krylovii, Carex spp., Caragana spp.,
A. adamsii and Chenopodium spp. during the study period. No
significant effect of PAP was found for the other dominant
species (Table 1).
The interactive effect of grazing and PAP on each species
was illustrated through interaction plots (Fig. 2). The clear differences in AGB between the G and NG plots for A. cristatum,
S. krylovii, C. squarrosa, Caragana spp. and A. adamsii were
associated with increases of PAP (top right corner, Fig. 2a–c,
f and g). This difference was fairly consistent for E. chinensis,
Carex spp., Chenopodium spp. and Salsola spp. (top right corner,
Fig. 2d, e, h and i). With regard to the AGB changes from the
G plot to the NG plot in the wettest and driest years, the most
pronounced changes were for S. krylovii and A. adamsii (bottom left corner, Fig. 2b and g). In the wettest year, the AGB
for S. krylovii increased sharply from the G plot to the NG plot,
while in contrast the AGB of A. adamsii decreased markedly
from the G plot to the NG plot (bottom left corner, Fig. 2b and
g). Statistically significant interactive effects of grazing and
PAP were detected only for S. krylovii (Table 1).
Effects of grazing, PAP and their interaction on
annuals
Strong (P < 0.1) and significant (P < 0.05) effects of grazing
and interannual variation of PAP were found on the AGB
of annuals (Table 1). No significant interactive effect was
found. Grazing resulted in higher AGB for annuals than
in the non-grazed area during the study period. Statistical
tests implemented year by year demonstrated that the proportion of annuals was clearly higher (P < 0.1) in the G
plots relative to the NG plots in both 2010 (dry year) and
2011 (wet year).
Annuals dominated in the wet years (2003 and 2008),
which followed three sequential dry years. In the wettest
post-droughts year of 2003, two Salsola species (annuals)
Bat-Oyun et al. | Effects of grazing and precipitation on vegetation513
Figure 2: interaction plots obtained from the generalized linear model showing interactive effect of PAP and grazing on the AGB of each
dominant species (a–i), the AGB of annual species (j) and total AGB (k). Here 164.1 and 48.8 is corresponding to the PAP in the wettest (2011)
and driest (2007) year during the study period. G and NG denote the grazed and non-grazed plots. Lines in the top right corner indicate that
changes of AGB along PAP variation for the G and NG plots. Lines in the bottom left corner represent that change of AGB from G to NG plot
for the wettest and driest years.
accounted for 79% of the total AGB for the G plots (no data
for NG plot), after recovery from multiple droughts in 1999,
2000 and 2002. Similarly, in the wet year of 2008, which was
preceded by consecutive dry years in 2005–2007, the AGB of
the three Chenopodium species (annuals) contributed the highest portion to the total AGB for the G (62%) and NG (67%)
plots (Fig. 3).
To comprehensively understand the response of annuals to
PAP, the current-year proportional AGB of annuals measured
in the NG plots and precipitation parameters from the PAP of
the current year, sequential combinations of the first to fifth
preceding years and sequential combinations of the current
and first to fifth preceding years were proposed as predictive
parameters during the study period. A positive and high
correlation (r = 0.57, P < 0.1) was found between the current-year PAP and current-year proportional AGB of annuals. In contrast to the current year, negative and significant
time-lagged effects were obtained between the current-year
proportional AGB of annuals and PAP amount in the three
(r = −0.74, P < 0.05) and four (r = −0.86, P < 0.01) sequential
preceding years (Table 2).
The interaction plots of grazing and PAP for annuals showed
that trends in the AGB of annuals in the G plots mirrored those
in the NG plots and increased consistently with increases of
PAP, indicating that AGB for annuals was driven more strongly
by PAP than grazing (top right corner, Fig. 2j). The AGB of
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Journal of Plant Ecology
Figure 3: relative AGB composition of dominant species in (a) NG and (b) G plots.
Figure 4: DCA based on AGB at the G (open circles) and NG (black circles) plots in different years. Here, the smallest circle corresponds with
the driest year, whereas the largest circle represents the wettest year.
Bat-Oyun et al. | Effects of grazing and precipitation on vegetation515
Figure 5: DCA scatter diagram of the nine dominant species (based on species scores).
annuals was slightly higher in the G plots than in the NG plots
in both the wettest and driest years (bottom left corner, Fig. 2j).
DCA
The majority of the variation along the DCA axes 1 and 2
explained interannual variation of precipitation and differences in AGB between the G and NG plots. The gradient
along axis 1 generally reflected the variation of AGB with
interannual variation of PAP (eigenvalue = 0.62). The AGB
measured in years with relatively more precipitation were
positioned near the lower score on the left (bigger circles),
and those measured in years with less precipitation had the
higher scores on the right (smaller circles) along axis 1. The
years 2003 and 2008 were noteworthy. In these years, cases
of the annuals dominated and were the main contributors to
total AGB, which was controlled by not only the current year
but also the preceding year’s PAP as described above (Table 2,
Fig. 4). The axis 2 scores were related to the effect of grazing
on AGB along the y-axis, with the G plots (open circles) at the
top and the NG plots (black circles) towards the bottom (eigenvalue = 0.35). The regression analysis on the DCA axes scores
and environmental factors indicates that variation in AGB
that was expressed on axis 1 had a negative and significant
correlation (r = −0.56, P < 0.05) with the current-year PAP,
excluding the noteworthy cases of the annuals dominated.
Meanwhile, scores on the DCA axis 2 were significantly correlated (r = −0.31, P < 0.05) with AGB in the G and NG plots.
Ordination of the dominant species by the DCA is depicted
in Fig. 5. The species scores tended to reflect the effect of grazing and the interannual variation of PAP, which supports the
results previously presented in this study. The most palatable
plant species (such as A. cristatum, S. krylovii and C. squarrosa)
were positioned at the lower negative scores under wet and
non-grazed conditions, and an unpalatable species, A. adamsii
was clearly separated from the other species at the highest
positive score along the y-axis under grazing.
DISCUSSION
We expected that grazing would have a smaller effect than
interannual variation of precipitation on vegetation dynamics in the dry steppe (a non-equilibrium model). However, our
findings over an 9-year indicated that vegetation dynamics in
this area are characterized by both equilibrium and non-equilibrium systems. Grassland AGB and species composition were
strongly defined by the interannual precipitation as characteristics of a non-equilibrium model. However, there were also evidences supporting an equilibrium model, including significant
differences in AGB under grazing and grazing-excluded conditions, significant effects of grazing on some species, increases in
the amount of unpalatable annuals and decreases in palatable
species in the G plots relative to the NG plots.
This result supports the findings of several other researchers who have adopted an intermediate pattern that recognizes
516
ecosystems possess characteristics of both equilibrium and nonequilibrium systems (Ho 2001; Oba et al. 2003). Studies conducted on vegetation dynamics in different vegetation zones of
the Mongolian grasslands indicate that these respond differently
to equilibrium and non-equilibrium models. In relation to biomass, species cover and richness, vegetation in the desert steppe
conformed to the non-equilibrium model, whereas the steppe
zone was characterized by an equilibrium model (Cheng et al.
2011; Fernandez-Gimenez and Allen-Diaz 1999). At a regional
scale, ecosystems in dry environments mostly corresponded to
the non-equilibrium model (Sullivan and Rohde 2002), while in
other studies on a larger scale, dry ecosystems often experienced
equilibrium dynamics (Illius and O’Connor 1999, Oba et al.
2003). Wesche and Retzer (2005) proposed that equilibrium and
non-equilibrium conditions depend on the variables examined.
A worldwide study by Milchunas and Lauenroth (1993)
suggested that site history also matters in regard to the magnitude of grazing impact, and this is likely to be important in the
Mongolian steppes where nomadic pastoralism has formed
the principal land use over centuries.
In Mongolia, the livestock population has increased over
recent decades because of privatization of livestock to herders
and public use of pastoral land, mainly driven by institutional
change. On a local scale, livestock densities are not stable and
are driven largely by forage availability, which in turn affects
grazing impact. For example, under nomadic herding strategies, animals are moved from drought-affected areas into
areas that have recently had high rainfall, and thus have good
forage availability. These areas then experience significant
grazing impact. This was discussed in the next section.
Both this research and previous studies suggest that allocation of vegetation dynamics to an equilibrium and non-equilibrium system is complex and can depend on a broad range
of factors including eco-climatological conditions, choice of
variables, grazing pressure and management, site history, and
spatial and temporal scales.
Effects of grazing, PAP and their interaction
on AGB
A significant positive impact of precipitation on AGB in this
study was consistent with the findings of previous studies
(Bat-Oyun et al. 2010; Fernandez-Gimenez and Allen-Diaz
1999; Munkhtsetseg et al. 2007; Shinoda et al. 2010). Grazing
significantly reduced the AGB relative to the NG area in the
wet years (2005, 2011 and 2012), while the opposite trend
(but not significant) occurred in the dry years (2006 and
2007), showing that there was little or no consumption of
AGB in the grazed plots. It is, therefore, believed that the
number of livestock, and hence the grazing effect, is controlled by forage (i.e. biomass) availability to livestock. From
a practical point of view, in the dry years livestock numbers
may collapse owing to limited availability of forage and water.
Nomadic pastoralists, therefore, reduce the risk for livestock
associated with drought by moving their livestock to places
where more pasture and water is available.
Journal of Plant Ecology
In wet years, grazing significantly reduced AGB mainly
owing to the reduction of palatable species. This could be
explained by the increases in livestock numbers with an
influx of livestock from places where drought had previously
occurred. Previous research supports our finding that livestock numbers are driven by forage availability, which is controlled by precipitation during a given summer (Gillson and
Hoffman 2007; Retzer 2004).
Examining the relationship with PAP parameters, the AGB is
primarily controlled by the current-year PAP (r = 0.88, P < 0.01)
and also combinations of the current and first preceding year
(r = 0.62, P < 0.1) and current, first and second preceding years’
(r = 0.65, P < 0.1) PAP. A number of studies have documented
that the current and preceding year’s precipitation have a strong
influence on the Normalized Difference Vegetation Index of the
current year in some regions of the world (North America, Wang
et al. 2003; Africa, Wiegand et al. 2004; Mongolia, Nandintsetseg
et al. 2010). In this study, dry years receiving similar precipitation resulted in significantly different AGB in the NG plots (PAP
were 69.8 and 72.0 mm, AGB were 87.1 and 44.9 g/m2 for 2005
and 2006, respectively). We suggest a possible reason for greater
AGB in 2005 was due to high soil moisture and greater AGB
mainly from perennial species in a preceding wet year in 2004.
High AGB in 2004 produced a substantial amount of leaf litter
and this litter accumulation helped to maintain high soil moisture owing to shading of the soil surface (Goldberg and Werner
1983; Kinugasa et al. 2012), and remained in the frozen soil until
the following season. In contrast, less AGB was produced in
2006, which followed the dry year of 2005. Another example
is shown in the wet years (137.6 mm of PAP in 2004 which followed a wet year dominated by annuals (79% of Salsola spp.)
and 139.6 mm of PAP in 2008 which followed consecutive dry
years dominated by perennials). In these years, different but not
significant AGB was produced (93.0 g/m2 in 2004 and 147.5 g/
m2 in 2008). The probable reason underlying this pattern is a
difference in species composition in the current and preceding
years: in 2004 perennial species were dominant, while in 2008
annuals (Chenopodium spp. and Salsola spp.) were dominant.
Annuals can result in more allocation to AGB and less allocation
to belowground biomass. We believe that high litter accumulation produced by Salsola spp. in preceding year of 2003 could not
maintain soil moisture through soil shading process as the way
above mentioned, because Salsola collina is a species that senesces
into a ball of dried branches. This ball is easily uprooted owing to
its shallow root system, and then blows away in the wind (personal observation). Moreover, less accumulation of belowground
biomass from annuals in 2003 may cause negative feedback
on AGB in the following year through the coupled interaction
between aboveground and belowground components (Wardle
et al. 2004). To confirm this, systematic research is required on
dynamics of the aboveground and belowground parts of ecosystems over the long term. We expected that in 2008, AGB experienced more by the current-year species composition than PAP
in the preceding dry years. The greater AGB in 2008 possibly
attributed by the dominance of annuals (Chenopodium spp. and
Bat-Oyun et al. | Effects of grazing and precipitation on vegetation517
Salsola spp.), which are high in aboveground part in comparison
to perennial grasses. Therefore, species composition in the preceding and current seasons may also contribute to the biomass
-precipitation relationship in this grassland, which is consistent
with the findings of a previous study in the Inner Mongolian
grassland (Bai et al. 2008).
Effects of grazing, PAP and interaction on species
composition
It is well known that livestock selectively graze on plants
because of the quantity of plant production and the nutritional quality of the plant species (Wilson and Harrington,
1984). Such dynamics are also evident in the present study. In
the years of 2005, 2011 and 2012, AGB significantly decreased
under grazing. We expect that selective grazing by livestock is a
possible cause for such differences, decreasing the abundance
of palatable perennial grasses such as A. cristatum, S. krylovii
and C. squarrosa (Ronnenberg et al. 2011; Sergelenkhuu and
Oyuntsetseg 2008) and increasing the dominance of unpalatable herbs and annuals such as A. adamsii, Chenopodium spp.
and Salsola spp. (Jigjidsuren and Johnson 2003). Consistent
with our results, previous research has found that most palatable and nutritious plants were removed under grazing (Adler
and Morales 1999; Fernandez-Gimenez and Allen-Diaz 1999;
Hickman and Hartnett 2002; Sasaki et al. 2005, Tsubo et al.
2012). There is evidence that the domination of A. adamsii
under grazing disturbance (Hilbig 1995) is an indicator of pasture degradation (Sergelenkhuu and Oyuntsetseg 2008).
In summary, both the quantitative aspects (grassland biomass) and the qualitative aspects of vegetation (species composition) are important diagnostic signs of grassland condition
under grazing.
Effects of grazing, PAP and their interaction on
annuals
The proportion of annuals were clearly higher in the G plots
relative to the NG plots in 2010 (dry year) and 2011 (wet year).
Possible reason for that not only selective grazing on grassland
discussed above, but also compaction and erosion of soil under
livestock trampling, which may form another key disturbance
relating to loss of grassland quality through the increase of
unpalatable annuals. This result was corroborated by previous
research revealing that the abundance and rate of recovery
of annuals are influenced by high animal density (FernandezGimenez and Allen-Diaz 2001; Metzger et al. 2005).
Annuals appear to be ordered along the PAP variation of the
current and preceding seasons, with domination of annuals in
the wetter years (Salsola spp. in 2003 and Chenopodium spp. in
2008) that followed three or four consecutive dry years (Figs
1a and 3). Correlation analysis demonstrated that there are
strong and positive effect (r = 0.57, P < 0.1) of PAP in current
year and significant negative effects of PAP in preceding three
(r = −0.74, P < 0.05) and four (r = −0.86, P < 0.01) years on the
proportional AGB of annuals in the current year. This indicates
that in dry years annuals are dormant and perennial species
contribute a major role in the ecosystem, whereas when wet
weather conditions return after multiyear droughts, the annuals resume their role in the ecosystem, germinating from the
seed bank in soil that has not been depleted or exhausted.
Such shifts in the domination of annuals during post-drought
recovery have also been observed in grassland ecosystems in
Minnesota, USA (Tilman and El Haddi 1992), in Nevada, USA
(Lei 1999), in Arizona, USA (Loeser et al. 2007) and in Mongolia
(Cheng et al. 2011; Natsagdorj and Sanjid 2005). General and
possible mechanisms for the abundant propagation and depletion of annuals include the following. (1) Annuals escape
droughts by remaining dormant in the seed bank for several
years (up to 20 years, Natsagdorj and Sanjid 2005), and then
abundantly propagate when soil moisture is favorable again,
leading to nutrient pulses. (2) Annuals commence their life
cycle each year from seeds, which experience a greater mortality rate than perennials in dry years. (3) Perennials have a
relative advantage over annuals when water is limited, as perennials can access stored soil water in deeper soil through their
extensive root system, while annual grasses have shallow roots
and utilize soil water in the upper soil that is dependent on
precipitation pulses. (4) The present study demonstrated that
annuals are associated with the timing and amount of precipitation, especially during the early-growing season to germinate
seeds. The years 2003 and 2008, when annuals germinated in
large numbers, were characterized by not only the precipitation amount during the current and preceding growing seasons
but also by larger amount of precipitation occurred early in the
season (in the materials and methods section).
On the basis of our results, we obtained the following conclusions. (1) In general, grazing exclusion improved total
grassland AGB. However, high interannual variation in PAP
and drought events may modify the effect of grazing exclusion, because livestock numbers fluctuate in response to vegetation availability in such climate-dependent nomadic pastoral
ecosystem. We suggest that maintaining livestock populations
within carrying capacity is important to allow sustainable
management of the rangeland. (2) Under grazing disturbance, the AGB of palatable species decreased while unpalatable weeds and annual forbs increased, suggesting that some
palatable perennial species are susceptible to heavy grazing.
(3) The current-year PAP had a significant positive impact
on AGB, while current- and multiple preceding-year PAP
had profound effects on the interannual variation in annuals. The present study provides fundamental knowledge on
the complex interactions between climate-vegetation-grazing
systems, which will usefully underpin efficient planning and
management options in arid and semi-arid grasslands.
FUNDING
Grants-in-Aid from the Japanese Ministry of Education,
Culture, Sports, Science and Technology (16405002, 20255001
and 25220201); National Natural Science Foundation of
China (31402118).
518
ACKNOWLEDGEMENTS
We are very grateful to Dr. G.U. Nachinshonhor for his expert advice
and kind help with vegetation surveys. We also thank Dr. Toshihiko
Kinugasa for his advice with the analysis. This article benefited from
constructive comments by the editor of the journal, and three anonymous reviewers.
Conflict of interest statement. None declared.
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