One-year grazing exclusion remarkably restores degraded alpine meadow at Zoige, eastern Tibetan Plateau

Global Ecology and Conservation 22 (2020) e00951

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Original Research Article

One-year grazing exclusion remarkably restores degraded alpine meadow at Zoige, eastern Tibetan Plateau Miao Liu a, b, 1, Zhenchao Zhang a, c, 1, Jian Sun a, *, Yi Wang a, Jinniu Wang d, Atsushi Tsunekawa b, Mesenbet Yibeltal e, f, Ming Xu a, g, Youjun Chen h a

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, 100101, China b Arid Land Research Center, Tottori University, Tottori, 6800001, Japan c School of Soil and Water Conservation, Beijing Forestry University, Beijing, 100083, China d Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, China e The United Graduate School of Agricultural Sciences, Tottori University, 1390 Hamasaka, Tottori, 680-8553, Japan f Faculty of Civil and Water Resource Engineering, Bahir Dar Institute of Technology, Bahir Dar University, Bahir Dar, Ethiopia g Department of Ecology, Evolution, and Natural Resources, School Environmental and Biological Sciences, Rutgers University, New Brunswick, NJ, 08901, USA h The Southwest University for Nationalities, Chengdu, 610041, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 14 December 2019 Received in revised form 31 January 2020 Accepted 31 January 2020

Understanding the influences of grazing exclusion (GE) on soil properties and vegetation characteristics is essential for the assessment of grassland restoration. The objectives of this study are exploring the efficiency of short-term GE in restoring alpine meadow in the Zoige region, eastern Tibetan Plateau, with high rainfall amount. We conducted sampling surveys before and after one-year GE in alpine meadows with seven sequent degraded degrees. The results showed that one-year GE significantly increased soil organic carbon (SOC), soil total nitrogen (STN), soil water content (SWC), and plant biomass, while decreased soil bulk density (SBD) regardless of the degradation degree. These findings suggest that short-term GE may be an effective way to restore degraded alpine meadow. Aboveground and belowground biomass was significantly positively associated with SWC, SOC, STN, soil total phosphorus, and soil available nitrogen, but presented negative relationship with SBD. This shows the complicated interaction between vegetation and soil physiochemical properties that regulates the grassland recovery process. The degraded alpine meadow in this rainfall-rich region could rapidly recover once grazing disturbance was excluded. This study can provide technical support for restoration and sustainable management of alpine meadows on the Tibetan Plateau. © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Keywords: Tibetan Plateau Short-term grazing exclusion Grassland restoration Alpine meadow Humid region

* Corresponding author. Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences (CAS), 11A, Datun Road, Chaoyang District, Beijing, 100101, China. E-mail addresses: [email protected] (M. Liu), [email protected] (Z. Zhang), [email protected] (J. Sun), [email protected] (Y. Wang), [email protected] (J. Wang), [email protected] (A. Tsunekawa), [email protected] (M. Yibeltal), [email protected] (M. Xu), [email protected] (Y. Chen). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.gecco.2020.e00951 2351-9894/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4. 0/).

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1. Introduction The Tibetan Plateau covers 2.5
108 ha, approximately 26% of China’s total area coverage (Sun et al., 2012). Alpine grassland is the main ecosystem and covers 50.9% of the total area of the Tibetan Plateau (Piao et al., 2012), which plays an important role in not only the development of livestock husbandry, but also multiple ecological service functions such as water and soil conservation, biodiversity maintenance, and carbon sequestration (Feng et al., 2010; Qin et al., 2018; Seuring and Muller, 2008). Due to the harsh environmental conditions, the alpine grassland ecosystem is very vulnerable (Sun and Wang, 2016). Recently, climate change and anthropogenic activities caused considerable degradation on the alpine grassland (Zhang et al., 2019; Wang et al., 2007). There are approximately 5.0
105 km2 areas experiencing various degrees of degradation across the Tibetan Plateau, whose 16% are considered severely degraded (Cui and Graf, 2009), seriously threatening local ecological security and the sustainable development of alpine grassland ecosystems (Sun et al., 2019). Enclosure has been extensively reported as an effective and very widely used approach for grassland restoration worldwide (Lu et al., 2015a,b; Wang et al., 2015; Zhao et al., 2011). In recent years, many studies concerning the evaluation of restoring degraded grasslands with grazing exclusion (GE) have been conducted (Hu et al., 2016; Jing et al., 2013; Zhao et al., 2016). However, there is continuous controversy on the effects of fencing on grassland restoration. Gao et al. (2011) and Yuan et al. (2012) reported that GE improved the soil water holding capacity as the result of eliminating grazers that trample the soil. Similar studies indicated that enclosure decreased soil water content (SWC) due to higher plant evapotranspiration and uptake by shallow roots (Li and Shao, 2006; Zhang et al., 2015; Zuo et al., 2009). As a result of the increase in organic matter input, GE could remarkably increase the concentration of soil carbon (C) and nitrogen (N) (Gao et al., 2011; Jing et al., 2014). Nevertheless, it exerted an indistinct or even negative influence on soil C and N according to the local climate, soil or vegetation type, grazing intensities before GE (Liu et al., 2012; Shi et al., 2013; Shrestha and Stahl, 2008; Wang et al., 2014). For effects of GE on plant, recent studies have proven that enclosure had significant positive impacts on plant biomass, because it improved soil nutrient and water availability and removed consumption from grazers (Gao et al., 2011; Liu et al., 2014); whereas it did not alter plant belowground biomass (BGB), due to short duration of enclosure (Niu et al., 2011; Reeder et al., 2004). As well, GE might increase species diversity (Zhu et al., 2016), or have little influence on species diversity (Lunt et al., 2010), or even negatively affect species diversity (Su et al., 2015), depending on the competitive ability of different plant species, environmental conditions, and duration of enclosure. The inconsistency of enclosures’ effects on grasslands might be related to a variety of factors, such as the degree of degradation before enclosure (Sun et al., 2019), duration of enclosure (Cheng et al., 2011), grassland type (Cao et al., 2019) and local climatic conditions (Wu et al., 2009). The study area (Zoige Plateau) has a cold and wet climate with average annual temperature and precipitation of approximately 1  C and 700 mm, respectively (Chen et al., 2016; Zhang et al., 2017), and most rain falls during the growing season providing abundant water resources for plant physiological activities (Zhang et al., 2017). Up to now, the response mechanisms of edaphic and vegetation characteristics to GE have not been thoroughly elucidated in this region that experiences relatively high rainfall. To fill this gap, we examined changes in soil physicochemical properties and vegetation characteristics after one-year GE in alpine meadows with seven sequent degraded degrees in the Zoige region, eastern Tibetan Plateau. The main aim of this study is to explore the responses of soil physicochemical properties and vegetation characteristics to short-term GE. The results could provide technical support for restoration and management practice of alpine meadows in humid areas. 2. Materials and methods 2.1. Study area Study area located in Zoige region (32 200 -34 000 N, 101300 -103 300 E), eastern Tibetan Plateau (Fig. 1), with an area of 6180 km2 and a mean altitude of 3500 m (Chen et al., 2016). The main ecosystem is alpine meadows and wetland vegetation, dominated by three plant species, i.e., Kobresia tibetica, Stipa capillata, and Carex lasiocarpa (Bai et al., 2008). The rainfall mostly occurs in the plant growing season from May to August (Su et al., 2015). The main soil category is Cambisols according to soil classifications WRB, and Inceptisols based on USDA soil taxonomy (Hu et al., 2015). 2.2. Sampling analysis The typical degraded grasslands were chosen after wide field surveys in Waqie village of Hongyuan county belonging to the Zoige Plateau (Fig. 1). According to Ma et al. (2002), we sampled nine sequent degradation gradients in 2017 and 2018 based on vegetation coverage and plant community structure. To elaborate the efficiency of fence, seven corresponding obvious degradation gradients were chosen, and the detailed information was introduced in Table 1. These grasslands were in free grazing conditions with the main livestock of yaks and horses until 2017 when fences were carried out. The sampling surveys were conducted in August of 2017 (before GE) and 2018 (after one-year GE). In every degraded gradient, we selected three representative sampling areas (about 50 m
20 m) as replicates where three quadrats (1 m
1 m) were randomly arranged to collect plant and soil samples. For eliminating the effects of rainfall, there was 5 days without rain before our sampling. Within each quadrat, plant information such as species and coverage were recorded. The aboveground biomass (AGB) was determined by clipping aboveground parts of the plants with scissors at

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Fig. 1. The location of sampled site in Zoige Region on the Tibetan Plateau (Graph a). Graph b and c presented the landscape of sampled site in 2017 (before GE) and 2018 (after one-year GE).

ground level. Belowground biomass was collected via 3 soil cores with 5 cm diameter from 0 to 30 cm soil layer. The plant samples were oven-dried at 65  C until the weight was constant. Three replicate samples for soil bulk density (SBD) measurements were obtained at 0e30 cm layer using 200 cm3 cutting ring. SWC was determined via oven-drying soil samples at 105  C. Soil samples for chemical property were obtained from 3 replicate soil profiles at 0e30 cm depth using 5 cm diameter soil cores and sieved (2 mm mesh) after they were air-dried and removed roots, stones and other debris. The detection methods of soil chemical properties are shown in Table 2. 2.3. Statistical method Species diversity indices were calculated by the following methods (Ma et al., 1995). Simpson dominance index:

C¼

X

Pi2

Shannon diversity index:

H¼ 

X

Pi lnPi

Pielou evenness index:

E ¼ H=ln S where N represents the total number of plants in the plot, Pi represents the relative importance value of species i, C is the Simpson dominance index, H is the Shannon diversity index, and E represents the Pielou evenness index, S represents the total number of species.

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Table 1 Information of 7 degradation gradients in our study. Degradation Coordinate Gradient 33 130 37.5300 N 102 360 51.2600 E 33 130 37.4400 N 102 360 51.6900 E 33 130 37.1100 N 102 360 50.8700 E 33 130 36.9300 N 102 360 51.4600 E 33 130 37.8400 N 102 360 51.1100 E 33 130 37.6200 N 102 360 50.9700 E 33 130 37.3900 N 102 360 51.2500 E

1 2 3 4 5 6 7

Altitude Main species (m)

Coverage Coverage before GE (%) after GE (%)

3678

77

89

65

78

56

67

44

50

31

38

22

29

13

17

3695 3702 3721 3725 3736 3740

Taraxacum mongolicum, Euphrasia pectinata, Anaphalis sinica, Anemone rivularis, Potentilla fragarioides, Carex tristachya Artemisia desertorum, Gueldenstaedtia verna, Oxytropis kansuensis, Anaphalis sinica, Commelina diffusa, Stipa capillata Artemisia desertorum, Lancea tibetica, Carex tristachya, Commelina diffusa, Gueldenstaedtia verna, Deschampsia caespitosa, Stipa capillata Carex tristachya, Artemisia desertorum, Lancea tibetica, Oxytropis kansuensis, Gueldenstaedtia verna, Anemone rivularis Carex tristachya, Artemisia desertorum, Oxytropis kansuensis, Pedicularis spicata, Deschampsia caespitosa Carex tristachya, Agrostis matsumurae, Artemisia desertorum, Stipa capillata, Oxytropis kansuensis Carex tristachya, Artemisia desertorum, Stipa capillata

Note: GE represents grazing exclusion.

The trade-off of above- and below-ground biomass was quantified by root average square error of single benefits (Sun and Wang, 2016). The one-way ANOVA was performed with SPSS 19.0 software (SPSS Inc., Chicago, IL, USA) to detect the differences in soil properties and vegetation characteristics between free grazing (FG) and GE grasslands. Correlation and regression analyses in SigmaPlot 14.0 software (Systat Software, Inc., Chicago, IL, USA) were used to explore changes in soil physicochemical properties and vegetation variables along degradation gradients before and after GE. Principal Component Analysis (PCA) was carried out with the soil physicochemical property data to explore the explanatory powers of variance in soil physiochemical properties between FG and GE grasslands, by using the packages of FactoMineR, and factoextra packages (CoreTeam, 2016). Besides, the heatmap was graphed by corrplot package in software R (CoreTeam, 2016).

3. Results 3.1. Variations of soil physicochemical properties before and after GE The PCA results revealed that the soil physicochemical properties accounted for 84.5% of the total variance explained in the two first axes, where the first axis (54%) was highly correlated with SOC and SBD, and the second axis (30.5%) was highly correlated with STN, STP, SAN, SAP and SWC (Fig. 2). The plots in the FG grassland were ordinated in a group with higher SAN, SAP, STP and SBD than the GE plots, which were ordinated in areas with more STN and SWC (Fig. 2). The soil physicochemical properties in the 0e30 cm soil profiles of the degraded sites in FG and GE are shown in Fig. 3. Soil physical and chemical properties in GE exhibited similar tendencies with those in FG along degradation gradients. Soil organic carbon (SOC), soil total nitrogen (STN) and SWC were remarkably higher in GE than those in FG (Fig. 3a, b and f). Conversely, soil total phosphorus (STP), soil available nitrogen (SAN) and soil available phosphorus (SAP) were distinctly lower in GE than those in FG (Fig. 3c, d and e), and SBD was slightly lower in GE than that in FG (Fig. 3g).

3.2. Variations of vegetation characteristics before and after GE According to Fig. 4a and b, AGB and BGB both decreased continuously with increasing degradation (P < 0.05) and were significantly higher in GE than those in FG. Notably, AGB and BGB were more sensitive to degradation gradients in GE (slope ¼ 22.38 and 52.25, respectively) than in FG (slope ¼ 14.59 and 5.63, respectively). The trade-off of above- and below-ground biomass favoured AGB and was 0.12 in FG grasslands, which was lower than 0.17 in GE grasslands (Fig. 5). The species diversity indices displayed decreasing trends except for the Pielou evenness index (Pielou), which remained essentially unchanged with increasing degradation (Fig. 4c, d, e and f). The species richness (SR) and Shannon diversity index

Table 2 Abbreviations and detection methods of soil chemical properties. Soil chemical property

Abbreviation

Detection method

Soil Soil Soil Soil Soil

SOC STN STP SAN SAP

External heating method (the K2Cr2O7 volumetric method) (Bao, 2000) Vario MACRO cube elemental analyser (Elementar Analysensysteme GmbH, Germany) (Bao, 2000) NaHCO3 alkali digestion method and molybdenum antimony colorimetry (Bao, 2000) Continuous alkali-hydrolysed reduction-diffusion method (Bao, 2000) The Olsen method (Bao, 2000; Olsen et al., 1954)

organic carbon total nitrogen total phosphorus available nitrogen available phosphorus

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Fig. 2. Principal component analyses (PCA) based on the data of soil physicochemical properties that includes soil organic carbon (SOC), soil total nitrogen (STN), soil total phosphorus (STP), soil available nitrogen (SAN), and soil available phosphorus (SAP). Blue dots and yellow triangles represent free grazing (FG) and grazing exclusion (GE), respectively. The cumulative percentage of variance explained by the two axes were 84.5%. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

(Shannon) were lower in GE than those in FG in lightly or moderately degraded grassland, while these values showed inverse results in the heavily and severely degraded plots (Fig. 4c and e). 3.3. Relationships between soil physicochemical properties and vegetation characteristics Fig. 6 indicated that AGB was remarkably associated with most soil properties, including SOC, STN, STP, SAN, SWC, and SBD with R square were 0.85, 0.78, 0.86, 0.92, 0.90, and 0.90, respectively. Similarly, BGB was distinctly associated with SOC, STN, STP, SAN, SWC, and SBD, with R square were 0.69, 0.79, 0.77, 0.73, 0.82, and 0.86, respectively (Fig. 6). Interestingly, the SR plot showed remarkable negative correlations with SOC (R2 ¼ 0.66), STN (R2 ¼ 0.56), STP (R2 ¼ 0.55), SAN (R2 ¼ 0.74), and SWC (R2 ¼ 0.63) (Fig. 6). 4. Discussion Grazing exclusion (GE) is the most widely used method for restoring grassland throughout the world (Wang et al., 2015, 2018b). In our study, one-year GE considerably improved SOC, STN, SWC, and AGB and BGB in a degraded alpine meadow with high rainfall. These findings proved that GE was an effective measure to restore grasslands in this humid region. The primary

Fig. 3. Changes of soil physicochemical properties at 0e30 cm depth along degradation gradients in free grazing (FG) and grazing exclusion (GE). Red and blue dots and lines stand for free grazing and grazing exclusion, respectively. (a: soil organic carbon (SOC); b: soil total nitrogen (STN); c: soil total phosphorus (STP); d: soil available nitrogen (SAN); e: soil available phosphorus (SAP); f: soil water content (SWC); g: soil bulk density (SBD).). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

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Fig. 4. Variations of plant biomass and diversity indices along degradation gradients in free grazing (FG) and grazing exclusion (GE). Red and blue dots and lines represented GF and GE, respectively. (a: aboveground biomass (AGB); b: belowground biomass (BGB); c: species richness (SR); d: Simpson dominance index (Simpson); e: Shannon diversity index (Shannon); f: Pielou evenness index (Pielou). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

regulating mechanism might be a combination of soil physicochemical properties and vegetation characteristic interactions in their natural state. 4.1. Effects of one-year GE on soil physiochemical properties Soil conditions could be significantly altered by the removal of livestock disturbance (Chen et al., 2012). Fig. 2 indicates that the soil physicochemical properties greatly explains the variance in the alpine meadow under the FG and GE conditions, with the two first axes explaining 84.5% of the variance. The one-year fencing distinctly improves SOC and STN (Fig. 3a and b, Table 3), which well agrees with the previous findings that enclosures had positive effects on soil nutrients (Mekuria and Aynekulu, 2013; Zhang and Zhao, 2015; Zhou et al., 2011b). During the time of no grazing, there is no matter and energy flowing from the plant-soil system to livestock and the input of organic matter through litter and roots improve, which directly enhances the turnover and accumulation of SOC and STN (Lozano et al., 2014; Zeng et al., 2017). Meanwhile, the improvement in soil fertility benefits plant growth (Zhang et al., 2019; Qiu et al., 2013), which is supported by the apparent positive relationships of AGB and BGB with soil nutrients (Fig. 6). An increase vegetation cover in GE promotes soil physical protection that reduces soil erosion and enhances soil aggregation preventing SOC and STN losses (Chen et al., 2012; Wiesmeier et al., 2012). Besides, the increased abundance of soil microorganisms due to plant restoration might be also responsible for the increases in microbial biomass carbon C and N (Zhang et al., 2016). By contrast, the closure of a degraded grassland causes a decrease in STP (Fig. 3c, Table 3). This observation could be explained as that soil P is primarily derived from rock weathering (Chen et al., 2013), while the vegetation restoration caused by fencing reduces the weathering of parent materials. We also observe significant decreases in SAN and SAP after GE (Fig. 3d and e, Table 3), which are consistent with other researchers who revealed that the absorption by shallow roots contributed to decreases in available nutrients during the process of vegetation restoration (Zhang and Zhao, 2015). Our results indicate that SAN which is significantly and positively related to AGB and BGB (Fig. 6) might be the limiting factor for plant growth in GE grasslands. Another important reason for the higher concentration of SAN and SAP in FG grasslands is that grazing has a fertilization effect on soils via faeces and urine (Bardgett and Wardle, 2003; Yan et al., 2013). SWC displays a significant increase after one-year fencing (Fig. 3f, Table 3), in contrast to the findings of other scholars who demonstrated that vegetation development in fenced areas decreased SWC in semiarid sandy grassland ecosystems due to plant evapotranspiration and uptake by shallow roots (Li and Shao, 2006; Zhang and Zhao, 2015; Zuo et al., 2009). The different results might be because our study area is located in a humid zone with relatively more rainfall. The vegetation restoration caused by fencing reduces the strong solar radiation via increased plant cover (Wang et al., 2009), and the absence of soil trampling by livestock and higher SOC content improve water infiltration rates and water holding capacities in GE grassland (Climo and Richardson, 1984; Wu et al., 2011), leading to the significant increase in SWC after fencing. SBD shows a slight decrease in GE grasslands (Fig. 3f, Table 3), which agrees with previous studies (Gao et al., 2011; Yuan et al., 2012). This observation may be due to the lack of trampling by animals in GE or that the soil is relatively loose (Sun et al., 2018);

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Fig. 5. The trade-off relationship between aboveground (AGB) and belowground biomass (BGB) in alpine meadow with free grazing and grazing exclusion. FG and GE represented free grazing and grazing exclusion, respectively.

additionally, SBD shows predominantly negative correlations with AGB, BGB, and soil nutrients (Fig. 6), indicating that the increases in plant biomass and soil organic matter accumulation under GE conditions also result in the reduction of SBD (Yuan et al., 2012). 4.2. Effects of one-year GE on plant characteristics In our study, there is a higher benefit for AGB than BGB in both FG and GE (Fig. 5), which conflicts with Sun et al. (2018). The inconsistent results might be due to discrepancies in grazing intensity, duration of enclosure, original vegetation, as well as edaphic and climatic conditions in the different studies (Lu et al., 2015a,b; Wu et al., 2014a). Plants allocate more biomass to belowground roots to better acquire resources from deeper soils in arid and infertile soil conditions (Zeng et al., 2015). On the contrary, our study site is located in a humid zone with sufficient precipitation, and plants in the presence of water and with an abundance of nutrients could invest more biomass in leaves for photosynthesis in the growing season (Zhou et al., 2011a). The degree of overall benefit for AGB increases following GE (Fig. 5), indicating that GE has a greater positive effect on AGB than on BGB, probably because the fence eliminates the removal of AGB by grazing.

Fig. 6. Relationships between soil properties (SOC, STN, SAN, SAP, STP, SWC and SBD represent soil organic carbon, soil total nitrogen, soil available nitrogen, soil available phosphorus, soil total phosphorus, soil water content, and soil bulk density, respectively) and vegetation characteristics (AGB, BGB, SR, Simpson, Shannon, and Pielou represent aboveground biomass, belowground biomass, species richness, Simpson dominance index, Shannon diversity index, Pielou evenness index, respectively), according to the documents obtained from grassland with grazing exclusion (2018). The highlighted color solid circles indicated the significant correlations between variables at 0.05 level. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

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Gradient SOC(g/kg)

1 2 3 4 5 6 7

STN(g/kg)

FG

GE

FG

12.03 ± 0.82a 9.20 ± 0.65a 6.46 ± 0.33a 5.64 ± 0.69a 7.29 ± 0.59a 5.17 ± 2.23a 2.88 ± 0.88a

12.50 ± 1.00a 11.13 ± 0.78b 9.00 ± 0.78b 3.95 ± 0.16a 6.07 ± 0.55a 6.69 ± 1.43a 2.62 ± 0.28a

0.59 0.52 0.57 0.38 0.45 0.38 0.22

STP(g/kg) GE

± ± ± ± ± ± ±

0.08a 0.04a 0.08a 0.02a 0.04a 0.15a 0.05a

0.97 1.11 1.12 0.76 0.75 0.78 0.46

FG ± ± ± ± ± ± ±

0.15b 0.29b 0.21b 0.24b 0.11b 0.09b 0.05b

0.38 0.35 0.35 0.36 0.35 0.33 0.32

SAN(mg/kg) GE

± ± ± ± ± ± ±

0.02a 0.02a 0.02a 0.02a 0.01a 0.03a 0.01a

0.33 0.33 0.30 0.26 0.27 0.29 0.27

± ± ± ± ± ± ±

0.02b 0.04b 0.02b 0.01b 0.01b 0.01a 0.01b

SAP(mg/kg)

FG

GE

190.50 ± 64.27a 175.04 ± 21.96a 133.51 ± 8.89a 77.25 ± 19.15a 92.11 ± 15.98a 57.76 ± 21.72a 37.02 ± 7.13a

42.00 44.14 38.11 20.37 32.67 24.50 11.28

FG ± ± ± ± ± ± ±

0.49b 1.40b 0.09b 0.67b 0.48b 0.72b 0.75b

9.21 8.60 8.32 8.59 7.19 7.94 6.64

GE ± ± ± ± ± ± ±

1.76a 0.94a 0.50a 1.69a 0.50a 0.54a 0.98a

SBD(g/cm3)

SWC(%)

3.68 3.40 2.66 3.54 2.54 2.91 3.19

FG ± ± ± ± ± ± ±

1.02b 0.57b 0.42b 0.26b 0.41b 0.09b 0.43b

8.61 6.37 7.57 5.57 6.73 7.14 6.53

± ± ± ± ± ± ±

0.23a 0.55a 0.34a 0.09a 1.25a 0.23a 0.70a

GE

FG

13.92 ± 1.63b 14.63 ± 2.61b 12.17 ± 1.04b 9.84 ± 1.28b 10.44 ± 0.37b 10.91 ± 0.86b 8.64 ± 0.38b

1.27 1.35 1.39 1.45 1.50 1.50 1.45

GE ± ± ± ± ± ± ±

0.13a 0.03a 0.05a 0.04a 0.02a 0.03a 0.08a

1.28 1.21 1.30 1.40 1.37 1.38 1.38

± ± ± ± ± ± ±

0.09a 0.08b 0.10a 0.10a 0.09b 0.02b 0.08a

Note: SOC, STN, SAN, SAP, STP, SWC and SBD represent soil organic carbon, soil total nitrogen, soil available nitrogen, soil available phosphorus, soil total phosphorus, soil water content, and soil bulk density, respectively. The different letters represent significant difference at the 0.05 level.

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Table 3 Soil properties along the degraded gradients before and after the fence (mean ± s.e.).

Gradient

1 2 3 4 5 6 7

AGB(g/m2)

BGB(g/m2)

FG

GE

106.33 ± 35.00a 92.09 ± 39.56a 90.36 ± 27.29a 93.64 ± 14.60a 58.35 ± 20.66a 32.77 ± 3.69a 20.28 ± 20.28a

271.75 317.63 231.93 184.80 239.12 170.16 158.75

± ± ± ± ± ± ±

38.68b 64.85b 40.83b 22.61b 57.56b 34.90b 49.68b

SR

Simpson

FG

GE

FG

GE

FG

35.31 ± 20.01a 20.19 ± 12.60a 17.58 ± 2.01a 4.36 ± 0.66a 2.17 ± 0.83a 0.59 ± 0.21a 1.01 ± 0.62a

263.05 ± 55.92b 469.76 ± 135.59b 264.09 ± 73.42b 226.47 ± 38.53b 117.91 ± 21.11b 78.22 ± 34.25b 85.14 ± 14.77b

6.33 ± 1.53a 9.00 ± 2.36a 7.33 ± 2.51a 8.33 ± 1.52a 8.33 ± 3.51a 8.00 ± 2.65a 11.67 ± 2.51a

4.67 ± 0.58b 8.67 ± 0.58b 11.33 ± 1.15b 9.33 ± 2.08a 7.67 ± 0.58a 15.00 ± 1.00b 16.67 ± 0.58b

0.75 0.75 0.69 0.75 0.76 0.77 0.78

Shannon GE

± ± ± ± ± ± ±

0.04a 0.06a 0.12a 0.06a 0.12a 0.02a 0.05a

0.66 0.78 0.83 0.79 0.58 0.83 0.83

FG ± ± ± ± ± ± ±

0.14a 0.02b 0.05b 0.04a 0.09b 0.01a 0.03b

1.56 1.63 1.47 1.62 1.69 1.68 1.85

Pielou GE

± ± ± ± ± ± ±

0.15a 0.35a 0.44a 0.26a 0.24a 0.12a 0.27a

1.27 1.77 2.01 1.77 1.14 2.13 2.21

FG ± ± ± ± ± ± ±

0.27a 0.01b 0.21b 0.22a 0.16b 0.10b 0.13b

0.32 0.29 0.30 0.33 0.33 0.31 0.34

GE ± ± ± ± ± ± ±

0.04a 0.03a 0.08a 0.06a 0.08a 0.04a 0.07a

0.30 0.38 0.40 0.34 0.19 0.37 0.38

± ± ± ± ± ± ±

0.07a 0.01b 0.04b 0.02a 0.06b 0.01b 0.02a

Note: AGB, BGB, SR, Simpson, Shannon, and Pielou represent aboveground biomass, belowground biomass, species richness, Simpson dominance index, Shannon diversity index, Pielou evenness index, respectively. The different letters represent significant difference at the 0.05 level.

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Table 4 Vegetation characteristics along the degraded gradients before and after the fence (mean ± s.e.).

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Additionally, we found that the SR, Simpson dominance index, and Shannon diversity index decreased from potentially to severely degraded grasslands (Fig. 4c, d and e), similar to previous reports (Wang et al., 2008; Yang et al., 2013). The logic is that the worsened soil conditions caused by degradation constrains plant survival and contributes to the loss of some associated species (Wang et al., 2008). Previous studies revealed that short-term GE could significantly increase SR (Jing et al., 2013; Xiong et al., 2016), which is consistent with our results in the heavily and severely degraded plots. However, the SR and Shannon diversity index decrease in the lightly and moderately degraded areas after one-year GE (Fig. 4c and e, Table 4). This result could be due to the gramineous and sedge functional groups that are more competitive than other species in the relatively humid and nutrient-rich soils (Diaz et al., 2007); their dominant roles become more significant once the grazing disturbance is eliminated, which was partly proven by the negative associations of SR with soil nutrients and water content (Fig. 6). GE has important effects on degraded grassland ecosystems (Lu et al., 2015a,b; Zhang et al., 2015). As expected, our study shows that one-year fencing significantly improves AGB and BGB (Fig. 4a and b, Table 4), because of the elimination of ingestion and soil trampling by domestic animals in GE (Niu et al., 2010; Wang et al., 2018a). This result is in agreement with previous studies which have reported that closure is a feasible measure for restoring degraded grasslands (Mekuria and Aynekulu, 2013; Shang et al., 2013; Sun et al., 2014). Our findings imply that short-time fencing could effectively restore vegetation and improve grassland production of degraded alpine meadow in this region. 4.3. Suitable enclosure duration for restoring degraded alpine meadows in humid regions Plant growth is influenced by many factors such as climatic and edaphic conditions as well as disturbance, and plants might respond differently under different conditions (Hu et al., 2013). Precipitation is a dominant environmental factor driving grassland restoration by providing suitable moisture condition for plant growth (Jia et al., 2015; Yan et al., 2013). Wang et al. (2018b) demonstrated that precipitation exhibited greater effects on alpine grassland than grazing. Growing season precipitation greatly controls SR (Wu et al., 2012) and promotes grassland productivity in alpine grasslands (Hu et al., 2010; Yang et al., 2010). We did not quantitatively assess the relationship between precipitation and the efficiency of enclosure for grassland restoration in the present study, but previous studies have shown that response patterns of alpine grasslands to GE are significantly related to precipitation in the Tibetan Plateau, where most of the grasslands are located in arid or semiarid regions (Wu et al., 2014b, 2017), because plant growth relies more upon rainfall as a main water source when water is lacked (Jia et al., 2017; Hu et al., 2013). The Zoige Plateau has a humid climate with an average annual precipitation of approximately 700 mm, which mostly occurs in plant growing season, providing abundant water for plant growth (Chen et al., 2016). In this study, we observed notable improvements in degraded alpine meadows by short-term GE in this humid region. Additionally, numerous studies have addressed long-term GE does not effectively recover degraded alpine grasslands on the Tibetan Plateau (Cao et al., 2019). What’s more, considering the dependency of the local economy on animal husbandry, it is unrealistic to completely protect grasslands from grazing (Liu et al., 2003). Therefore, a short-term GE which has effective impact on grassland rehabilitation can be used to restore humid alpine meadow towards a desirable state. Lower stocking rates than currently applied will be needed for grassland sustainable management after a period of exclusion. 5. Conclusion We concluded that one-year GE had remarkable positive effects on soil physicochemical properties and grassland productivity in a humid alpine meadow, and the findings can support that short-term enclosure may be an effective method for degraded alpine meadow restoration in regions with rich rainfall. Nevertheless, this study only analysed the impacts of GE for one year. To provide more evidence for a scientific assessment of grazing enclosure efficiency, a long-term continued monitoring should be carried out in the future. In general, our study can help take an ecological and food security oriented strategic standpoint to develop short-term enclosure as a flexible rangeland management tactic, and thereby balance the demand of grassland conservation and utilization in humid areas.

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements We thank Dr. Xiaoxu Jia help us to review the draft. This research was supported by the State Key Research Development Program of China (Grant No. 2016YFC0501802 and 2016YFC0501803), the China Postdoctoral Science Foundation (No. 2017M620889), and the National Natural Science Foundation of China (No. 41871040 and 41501057).

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