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Effects of Litter Leachate on Plant Community Characteristics of Alpine Grassland in Qinghai Tibetan Plateau
Rangeland Ecology & Management 73 (2020) 147e155
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Rangeland Ecology & Management journal homepage: http://www.elsevier.com/locate/rama
Effects of Litter Leachate on Plant Community Characteristics of Alpine Grassland in Qinghai Tibetan Plateau* Zhouwen Ma a, Yingxin Wang a, Yongchao Gu a, Saman Bowatte a, Qingping Zhou b, Fujiang Hou a, * a
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, China Institute of Qinghai-Tibet Plateau, Southwest University for Nationalities, Chengdu, 610041, China
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 January 2019 Received in revised form 29 September 2019 Accepted 11 October 2019
Plant litter dynamics are sensitive to grassland productivity and the spatial heterogeneity of plant community. In this study, we investigated the effects of litter leachates on plant community characteristics using three plant species that represent different successional stages of alpine grasslands located on the Qinghai-Tibetan Plateau (QTP). We tested four concentrations of leachates (0, 50, 100, and 200 g L1) from Kobresia setchwanensis, Elymus nutans, and Ligularia virgaurea. The leachates from the three plant species generally responded similarly, but the responses to the varying concentrations were significantly different. Addition of litter leachates negatively impacted the aboveground biomass and species richness. The Shannon-Wiener diversity index was positively correlated with the litter leachate addition. The effects of the litter leachate’s addition on plant functional groups varieddgrasses were inhibited, forbs and legumes were promoted, and sedges were not significantly affected. This study demonstrates that litter leachates are a critical determinant of species diversity, grassland productivity, and community structure in QTP alpine grasslands. © 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Key Words: Alpine meadow community structure plant functional group grassland litter leachates species diversity
Introduction Climate change and unreasonable grazing can alter grassland plant community structure in Qinghai-Tibetan Plateau (QTP) (Lu et al. 2016; Dong et al. 2019), resulting in spatially heterogeneous litter accumulation. These compositional changes can result in variation in litter turnover, thereby altering ecosystem processes such as nutrient cycling (Hobbie and Sarah 2015) and plant community characteristics, as well as plant functional traits (Makkonen et al. 2012; Yuan et al. 2015; Dai et al. 2016). The heterogeneity introduced by the patchy accumulation of litter can also affect the plant community structure (Elgersma et al. 2012; Loydi et al. 2015), but the mechanisms driving such impacts in QTP grasslands have rarely been investigated and therefore are poorly understood.
* This study was supported by the Project of the Second Tibetan Plateau Scientific Expedition (2019QZKK0302), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20100102), the National Natural Science Foundation of China (31672472), the program for Changjiang Scholars and Innovative Research Team in University (IRT_17R50) and the 111 project (B12002). * Correspondence: Professor Fujiang Hou, Lanzhou University, Lanzhou, 730000, Gansu, China. E-mail address: [email protected] (F. Hou).
Litter plays an important role in plant growth and soil properties (Chapman and Newman 2010; Bradford et al. 2016; Harrop-Archibald et al. 2016). Decomposition of litter can impact nutrient cycling (Meier and Bowman 2008), as well as seed germination (Zhang et al. 2017) and establishment of seedlings (Yuan et al. 2015). Furthermore, litter contributes to interspecific competition of grassland community structure and succession (Donath and Eckstein 2010; Hobbie and Sarah 2015; Xiao et al. 2015). Litter can also provide favorable sites and energy for the life activities of microorganisms, soil fauna, and small herbivores. It also affects the structure and function of grassland ecosystems, which drives the progressive succession of plant communities (Hou et al. 2004; Bork et al. 2012; Hang 2014; Ma et al. 2017). Although the effects of physical changes induced by litter on grassland communities are well documented, the mechanisms of grassland community responses to chemical changes are not. Plant litter can influence establishment of seedlings and germination by allelopathy effects of litter leachates (Rice 1979; Samedani et al. 2013; Dai et al. 2016). Allelochemicals can also play a role in regulating ecosystem functions, including herbivory, decomposition, and nutrient mineralization (Hou et al. 2013; Li et al. 2014; Malenke et al. 2014). The strength of the allelopathy can be different between plant species where the chemical properties
https://doi.org/10.1016/j.rama.2019.10.003 1550-7424/© 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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of the litter leachates depend on substances accumulated in plant organs before senescence and biochemical transformations during decomposition. Most previous studies have investigated the responses of individual species to litter leachate addition (Olson and Wallander 2002; Tian and Hou 2009; Mudr ak and Frouz 2012; Samedani et al. 2013), but the responses to individual species may not reflect the combined response of plant communities composed of various functional groups such as in the natural grasslands in the QTP. The plant community responses to litter leachates of grassland species in the QTP have never been investigated, and such information is vital for developing the best management strategies for healthy grasslands in the QTP that are experiencing constant changes in vegetation composition (Zhou et al. 2012). Here we report a 2-yr field experiment conducted in alpine meadow grassland in the QTP to investigate the impacts of litter leachates on grassland species composition and functional traits. We investigated the effects of litter leachates from three grassland species dominant during early, mid, and late stages of succession in alpine meadow grasslands of QTP. The litter leachates were obtained from 1) Kobresia setchwanensis, a perennial sedge belonging to the Cyperaceae family; 2) Elymus nutans, a perennial grass belonging to the Gramineae family; and 3) Ligularia virgaurea, a perennial noxious forb belonging to the Asteraceae family. In natural conditions, leachates of litter consist of materials leached by washings from rainwater falling through litter or from chemical compounds released during the decomposition of litter. In our study, we used water extracts of pulverized dried litter as a means to examine maximum potential effects of chemical composition of litter leachates. We hypothesized that litter leachates from plant species representing three different successional stages would affect the grassland community composition and functional traits differently due to the differences in the chemical composition of the litter for the three species. We also tested the effects of different concentrations of litter leachate because under natural conditions, the concentration of litter leachate released to the soil can vary spatially and temporally. The objective of our study was to investigate the effects of litter leachates from three representative plant species of different successional stages in alpine grasslands in the QTP on aboveground biomass and plant community diversity. Materials and Methods
tartaricus, and Ligularia virgaurea. Legumes included Tibetia himalaica and Oxytropis.
Litter Collection and Leachate Preparation Plant litter of Elymus nutans (En), Kobresia setchwanensis (Ks), and Ligularia virgaurea (Lv) was collected from the QTP Research Base of Southwest Minzu University, after the grass withered and turned yellow in late October of 2014 and 2015. The litter was air dried at room temperature. The litter was then pulverized into powder and packed in polyethylene bags and stored 4 mo at room temperature. Pulverized dry powder (200 g) of three types of litter was steeped in 1 L of distilled water for 48 h at room temperature (15 C) and filtered through a double layer of nylon gauze (Yuan 2009). The leachate was then diluted with distilled water to obtain concentrations of 50, 100, and 200 g L1. Distilled water was used as the control (0 g L1).
Experimental Design The experimental area at the study site is a moderately degraded grassland. Since 2014, yak have grazed the site from late November to February. The randomized complete block design was used in the experiment. We established a concentration gradient using litter collected from three different species. Each plot was 2 2 m, arranged in three blocks. The buffer of each plot was 1 m, and blocks were separated by a 2-m strip. Each treatment had 3 replications. In early May 2015 and 2016, all aboveground plant materials were removed from all plots by cutting 2-cm aboveground herbage and removing litter by hand. We added four concentrations of leachate (0, 50, 100, and 200 g L1) of each litter type by hand sprayer in early May, June, and July in each yr. Each plot received 4 L of leachate. The volume of leachate application (4 L) was based on an estimation, assuming leachate incorporation of 100 g litter L1 (Yuan 2009) over 3 mo in a grassland where average litter accumulation of 300 g m2 (Yuan et al. 2015) was occurring. The litter leachate concentration treatments were adjusted (half and double) by the quantity of litter used to prepare the leachate, and the volume of leachate application was kept constant.
Study Site This experiment was conducted in 2015 and 2016 at the QTP Research Base of Southwest Minzu University, located in Hongyuan (3147'34”N, 102 33'07”E), on the northeastern boundary of the QTP in China (3485 m above sea level). The mean annual temperature is 1.4 C, ranging from 9.5 C in January to 11 C in July, the temperature varies greatly between day and night, where average relative humidity is 6070%. Mean annual sunshine duration is 2 159 hours, and mean annual precipitation is 791.95 mmd80% of which occurs from May to September. The study area belongs to the continental alpine temperate monsoon climate zone. The soil type is classified as Mat Cry-gelic Cambisols (Chinese Soil Taxonomy 1995). The annual growth season of the vegetation at the study site is from April to the end of September (Fig. 1). The return to the green period is mainly concentrated in April to May, reaching peak growth in mid August, with vegetation average coverage of > 80%. The plant community comprises of 53% forbs, 26% grasses, 17% sedges, and 4% legumes. All the grasses, sedges, and legumes were perennials. Of the forbs present in this study, 5% were annuals. Dominant grasses included Elymus nutans and Poa pratensis. Dominant sedges included kobresia setchwanensis and Kobresia Pygmaea. Dominant perennial forbs included Saussurea purpurea, Anemone trullifolia, Anaphalis lactea, Potentilla fragarioides, Aster
Field Sampling and Measurements In August (peak of growing season) of each yr, plant community species richness, plant density, plant height, and aboveground biomass were measured for each species by harvesting 0. 5 0.5 m quadrats at 2-cm height above in a randomly selected area within each plot. Plant community species richness was estimated by counting the number of all species in the quadrat. Plant density was estimated by summation of all the number of individuals in the quadrat. Plant height was measured using ruler measures for absolute height of each plant. The aboveground biomass was harvested, separated by species, oven dried at 65 C for 48 h, and weighed. All plant species were classified according to life form (annual and perennials) and four plant functional groups (PFGs) (grasses, sedges, legumes, and forbs).
Data Analysis Calculation of plant community species diversity was used for analysis of the ShannoneWiener diversity index (H0 ) and important value (IV) (Smith and Wilson 1996; Liu and Nie 2012; Pizzio et al. 2016), with the following equations:
Litter Leachate Effects on Plant Functional Groups The responses of plant functional groups (PFGs) to the addition of litter leachates were estimated by the importance value; an index to indicate relative dominance of a species in a plant community. The responses of PFGs to three litter leachate types were similar (Table 1). The effects of litter leachates addition on PFGs varied. Compared with the control, addition of litter leachates increased the legumes and forbs, decreased grasses, and had no
P
0.629 0.701 0.569 0.999 0.183 0.557 0.944 0.899 0.672 0.744 0.489 0.27 0.338 0.652 0.711 0.414 0.73 0.635 0.809 0.068 1.582 0.827 0.277 0.361 0.673 0.581 0.92 1.313 1.178 0.699 0.623 1.043 0.479 0.9 0.362 0.597 0.113 0.589 0.862 0.76 0.543 0.333 0.666 0.185 0.32 0.347 0.889 0.503 0.939 0.36 1.133 0.771 1.879 0.782 0.418 0.559 0.844 1.181 0.68 1.544 1.214 1.162 0.379 0.904 0.251 0.239 0.226 0.144 0.922 0.187 0.388 0.263 0.031 0.544 0.056 0.005 0.161 0.388 0.092 0.752 1.424 1.461 1.514 1.901 0.161 1.683 1.034 1.386 3.223 0.722 2.712 4.788 1.808 1.035 2.272 0.402 0.294 0.111 0.377 0.923 0.399 0.231 0.755 0.93 0.147 0.243 0.385 0.426 0.842 0.77 0.451 0.826 1.263 2.323 1.002 0.08 0.945 1.523 0.283 0.073 1.996 1.458 0.975 0.868 0.173 0.263 0.809 0.192 0.253 0.111 0.346 0.002 0.74 0.001 0.002 0.379 0.070 0.022 0.002 0.79 < 0.0001 0.359 0.188 < 0.0001 1.347 2.653 0.911 11.19 0.112 14.01 11.21 0.795 3.432 5.633 10.25 3.226 65.88 0.864 1.782 30.54 < 0.0001 < 0.0001 < 0.0001 < 0.0001 0.104 0.318 < 0.0001 0.487 0.604 0.019 0.887 0.001 0.002 0.313 < 0.001 0.009 111.82 8.356 110.93 27.043 2.219 1.182 45.121 0.827 0.623 3.656 0.213 6.219 5.670 1.226 6.536 4.495 0.414 0.546 0.471 0.813 0.151 0.103 0.870 0.668 0.540 0.595 0.795 0.068 0.618 0.187 0.428 0.747
Concentration
F P F P F P F
Yr Litter type
Litter type Concentration
P F P
0.903 0.614 0.769 0.208 2.002 2.209 0.140 0.408 0.625 0.525 0.230 2.854 0.487 1.752 0.863 0.293
The response of litter leachate addition on plant species richness and Shannon-Weiner index were similar for all three litter types (Table 1). The plant species richness of total community decreased with increasing concentration of added leachate in 2015 (Fig. 3A), annual species richness was decreased in both 2015 and 2016 (Fig. 3B), and had no impact on perennial species (Fig. 3C). The Shannon-Weiner index was significantly higher in treatment plots than the control in 2016 (P < 0.05) but not affected in 2015 (Fig. 3D).
Community aboveground biomass Annual species aboveground biomass Perennial species aboveground biomass Grasses aboveground biomass Sedges aboveground biomass Legumes aboveground biomass Forbs aboveground biomass Litter aboveground biomass Community species richness Annual species richness Perennial species richness Shannon-Wiener diversity index Important value of grasses Important value of sedges Important value of legumes Important value of forbs
Litter Leachate Effects on Plant Species Diversity
F
The plant community aboveground biomass response to the addition of litter leachate was similar in both years and for all three litter types (Table 1). In both years, irrespective of litter type, the aboveground biomass of community, grasses, forbs, perennial, and annual species significantly decreased with increasing concentration of the added litter leachate (P < 0.0001) (Figs. 2E, 2A, 2D, 2H, and 2G) and had no impact on sedges, legumes, and litter (Figs. 2B, 2C, 2F). The aboveground biomasses of the grasses and legumes were significantly lower in 2015 than in 2016, but forbs showed an opposite trend (Table 1).
P
Litter Leachate Effects on Plant Community Aboveground Biomass
F
Results
Yr Concentration
Where rd is the relative density, rh is the relative height, and rb is the relative aboveground biomass. Pi is the proportion of species i based on percent biomass data. We used structural equation modeling (SEM) to estimate the contributions of litter leachate to aboveground biomass and community diversity (Grace 2006). In the model, we assumed that litter leachate addition had the potential to alter aboveground biomass directly, as well as indirectly changing community diversity. The standard path coefficients were estimated to indicate the strengths of these multiple effects. We used the chi-square test, Akaike information criteria, and the root mean square error of approximation to evaluate the fit of model. The SEM analyses was performed using AMOS 17.0 (Amos Development Company, Greene, ME) for Windows (SPSS Inc., Chicago, IL). The effects of litter leachate type, leachate concentration, yr, and their interactions on plant community characteristics were analyzed using the analysis of variance procedure, and means were separated by the LSD test at the 5% probability level, using Statistical Product and Service Solutions software version 17.0 (SPSS Inc., Chicago, IL). Principal component analysis (PCA) was carried out using the vegan package of R program (R Core Team 2013) to illustrate the plant community composition variation responses to the leachate addition.
Yr Litter type
[2]
Yr
Pi ln ðPiÞ
Concentration
X
Litter type
H0 ¼
[1]
Variable
IV ¼ ð rd þ rh þ rb Þ = 3
Table 1 Statistical summary of the effects (P values) of litter leachate concentrations, litter type, yr, and interactions on aboveground biomass, species diversity, functional groups. Significant effects (P < 0.05) are highlighted in bold.
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Figure 1. Monthly mean precipitation and temperature from 2014 to 2016 at the study site located in Hongyuan (3147'34”N, 102 33'07”E) at the Qinghai Tibetan Plateau, China.
impact on sedges (Fig. 4). These responses were consistent in both yrs (Table 1). The grasses and forbs composition in the plant community was significantly lower in 2016 than in 2015 (Table 1), which may have been due to the lower rainfall during the plant growing season in 2016 (Fig. 1). Variation in Plant Community Composition by Litter Leachate Addition The first two axes of the PCA accounted for 61.8% of the total variance, which can reflect the characteristics of community composition. There was no discernible pattern in the distribution of litter types in the principal component ordination space (Fig. 5). Axis 1 accounted for 47.9% of the variance and illustrated the plant community structure changes with the decreasing of concentration of litter leachate. No separation of these groups was evident on axis 2. Relationships Between Litter Leachate Addition and Plant Community Characteristics The structural equation model (SEM) (Fig. 6) was used to evaluate casual relationships between the litter leachate and the plant community characteristics to understand how litter leachate would affect the grassland plant community. There were significant direct negative effects of litter leachate on aboveground biomass, which further indirectly affected plant species richness and species diversity estimated by the Shannon-Weiner index. Discussion The results of our study contribute to the numerous previous research that demonstrates the profound effect litter can have on grassland productivity (Fig. 2) and botanical composition of plant community structure (Figs. 4 and 5). More importantly, it provides new evidence for a potential mechanism driving such impacts, through litter leachates in an alpine grassland in QTP (Fig. 6). Contrary to our hypothesis, the responses of leachates from the tested plant species were generally similar, but the responses to the concentrations of the litter leachate were significant. Structural equation modeling (Fig. 6) indicated the addition of litter leachates affected grassland plant community through strong effects on aboveground biomass, plant species richness, and community species diversity. This result is consistent with Xiong et al.’s (1999) general view, established from a meta-analysis using the data from 35 studies worldwide, that plant litter has a significant effect on vegetation. Their meta-analysis indicated overall litter effects were
stronger on species richness than on aboveground biomass. In our study, which considered litter leachate effects only, the effects on aboveground biomass were much stronger than the species diversity effects (Fig. 6). The strong direct negative effect of litter leachate on aboveground biomass (Fig. 2) was possibly through the effects of allelopathy. The different secondary compounds contained in the litter leachates could have inhibited plant growth (Ma et al. 2005; Liu et al. 2017). Other studies, including research on Leymus chinensis grassland and the Canadian savannah, similarly reported that increasing concentrations of litter leachate decreased plant community biomass (Wang 2011; Nyanumba and Cahill 2012). Furthermore, it is possible that higher concentrations of litter leachate impacted carbon and nitrogen cycle processes (Meier and Bowman 2008), soil organic matter decomposition, nitrification and mineralization (Zhang et al. 2014), and soil microorganism activity (Makkonen et al. 2013; Li et al. 2016; Yahdjian et al. 2017), resulting in a decrease in plant available nutrients, which would have an effect on plant growth and contribute to the reduction in aboveground biomass. We found that increased litter leachate concentration changed the proportion of different plant families, affected vertical (grasses) and rhizomatous (forbs) plant growth (Fig. 2A and 2D), and may have increased spatial variation in plant growth, resulting in reduced aboveground biomass as suggested by Wen et al. (2013). The loss of dominant PFGs from grassland ecosystems can result in significant aboveground biomass reduction as observed by Pan et al. (2016) in an Inner Mongolian grassland. In our study, increased inhibition of the grasses (Fig. 4A) indicates that such a mechanism may be involved. We found that plant species richness, an important indicator of species diversity and species competitive coexistence (Liu et al. 2016; Tredennick et al. 2017), decreased with increasing concentration of added leachate (Fig. 3A and B); however, the ShannonWeiner index estimates indicated that the addition of leachate significantly increased plant community diversity in 2016 (Fig. 3D). The Shannon-Weiner diversity index is a measure of the degree of diversity and heterogeneity at the species level, which comprehensively reflects the species richness and evenness of the community. So, it is somewhat different from the results of species richness (Chen et al. 2013). Part of this effect may be due to litter phytotoxins leaching into the soil and impeding seedling recruitment (Vellend et al. 2000; Yu 2012). Alpine plants have low levels of seedling establishment from seed (Yuan et al. 2015), but most annual plants (Scrophulariaceae, Gentianaceae, Caryophyllaceae) and some perennial plants (grasses, Asteraceae ect.) are primarily established from seed. High concentrations of litter leachate
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Figure 2. The response of aboveground biomass to the addition of litter leachates. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level.
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Figure 3. The response of litter leachate addition on plant species diversity. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level in the same year.
consequently inhibited the annual plant seed germination, thus reducing annual plant species richness. Perennials can be multiplied by other means (Zhao et al. 2006), so there was less of an impact on the species richness of perennials. However, this possibility should be considered cautiously as we do not have long-term data on annual and perennial plant recruitment and seedling establishment within these plots. High-concentration litter leachate weakened the relative importance of the dominant species such as grasses (Fig. 4A) and indirectly enhanced the relative importance and development of other species such as legumes and forbs (Fig. 4C and 4D) in the community, which is an important cause of the increase in plant diversity. Zhang et al. (2015) suggested that allelopathy may be an important mechanism of plant dominance that allows certain plants to modify community diversity by affecting the seedling establishment of co-occurring species. In addition, litter leachate can affect plant community indirectly through their effects on soil fauna that are known to affect the composition of natural vegetation strongly (De Deyn et al. 2003). Different PFGs’ important values were inhibited, promoted, or unaffected by litter leachate (Table 1, Fig. 4). Grasses were inhibited by the addition of litter leachate (Fig. 4A), while legumes and forbs were promoted by leachate addition (Fig. 4C and D). The sedges were not significantly affected by litter leachate addition (Fig. 4B). Part of this impact may be through different species of functional groups having different requirements for seedling emergence and survival (Yuan 2009; Rayamajhi et al. 2012). In addition, growth mechanisms may play a role, with the varying growth mechanisms of different genera and plants being
impacted differently by litter leachate type and concentration. For example, similar to our study, sedges did not respond to litter in Wang et al’s (2010) study and speculated the neutral responses to litter was due to crowd-short rhizomatous growth form and inherent developmental constraints. In comparison, the positive response of forbs to the leachate addition was due to the competitive advantage of negative response by grasses (Chamane et al 2017). The positive responses by forbs to leachate is important for vegetation dynamics, especially in grasslands like our experimental site in which forbs contribute to 53% of the plant community. Forbs contribute to much of the plant diversity in grasslands, enrich the seed bank (Laforgia et al. 2018), and often show considerable trait plasticity in response to changes in species richness and composition (Lipowsky et al. 2015). Therefore, forbs are important for both convergence and divergence between species for specific traits (Mitchell et al. 2016). Chemical, physical, and biological feedback from litter varies with functional groups (Ma et al. 2017), and so litter can regulate the structure and function (Fig. 5) of grassland ecosystem in many ways. Litter of Ligularia virgaurea has been previously shown to affect the composition of plant communities (Shi et al. 2011; Xie et al. 2014). However, its effect is concerning, as it is a noxious weed that indicates severe degradation of grasslands. In other studies, invasive plant species have increased their impact on the existing plant community through the litter they produce, as in the case of sage brush-steppe plant communities being altered by the invasion of annual grasses (Bansal et al. 2014). This impact can be through general impacts on soil nutrient cycling, as well as production of alleochemicals.
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Figure 4. The responses of plant functional groups (PFGs) to the addition of litter leachates. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level.
The SEM (Fig. 6) demonstrated that leachate-driven changes to forbs and grass biomass influenced plant community diversity. Such PFGs or plant species changes can add further feedbacks to the plant community in future years through variable levels of litter accumulation, spatially and in time (Li 2014). Plant species provide a strong source of variation in standing litter mass and litter chemistry (Ren et al. 2014,) and any factors that affect plant community composition (Fig. 5) would therefore influence litter mass accumulation and hence litter leachate dynamics. It is well recognized that grazing regimes and environmental factors can substantially influence the plant community composition (Garibaldi et al. 2007; Shen et al. 2016). Semmartin et al. (2004) showed evidence that grazing, rainfall, and their interactions induced plant community changes and altered litter quality, causing major changes in ecosystem functions such as in nutrient cycling. The
importance of grazing-induced plant composition changes on litter chemistry was also highlighted by Campanella and Bisigato (2010). Our study showed such litter quality impacts are possibly through litter leachates. Li et al. (2015) reported that in a desert step grassland the green-up dates can be advanced up to 7 d when litter accumulation reaches 300400 g m2, benefiting healthy grassland systems by maintaining community stability. Identifying such critical levels for litter leachate accumulation under varying grazing management regimes would be beneficial for developing best practices for sustainable grassland management. In the QTP, climate change and intensive animal grazing has been attributed to plant community changes and grassland degradation (Hautier et al. 2015). Therefore, future studies are warranted for the environmental and grazing effects of litter leachate feedbacks and their impact on plant community changes.
Figure 5. Principal component analysis illustrating the variation in plant community composition by litter leachate addition.
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Figure 6. A structural equation model of treatment effects on above-ground biomass and community diversity. The structural equation model considered all plausible pathways through which experimental treatments influence community aboveground biomass and diversity. Solid and dashed line arrows represent significant and nonsignificant pathways, respectively. Numbers indicate the standard path coefficients. Arrow width is proportional to the strength of the relationship. R2 represents the proportion of variance explained for each dependent variable in the model. *P < 0.05, **P < 0.01, ***P < 0.001; (a)c2 ¼ 1.241, df ¼ 2, P ¼ 0.538; root mean square error of approximation (RMSEA) ¼ 0.000.
In summary, we found litter leachate additions to a native mixed-grass alpine grassland community generated a strong response to the aboveground biomass and plant community diversity, highlighting the importance of litter leachate in maintaining grassland community structure and ecosystem functions.
Acknowledgments The authors are grateful to the Qinghai-Tibet Plateau Research Base of Southwest Minzu University for supporting the field work.
References Implications An important implication of our study is improved understanding of the link between litter feedbacks on plant community composition through litter leachates. Such understanding is important for the management of natural grasslands. We found that at higher leachate concentrations, there were significant changes in herbage biomass, species richness, and composition of PFGs, indicating potential impacts on grassland community stability. These feedbacks can also have broader implications on spatial variability, biodiversity, and ecosystem processes. Our results also indicate that litter dynamics may have the potential to shift vegetation succession of the plant community, as species availability, species functional characteristics, and site availability are three primary causes of succession (Krueger-Mangold et al. 2006), and litter leachate can have an impact on all three of these. In our study, the impact of leachate concentration was much stronger than the litter identity. As litter mass is one of the key factors that would influence leachate concentration, standing total litter mass can be considered as a critical factor influencing litter leachate feedback effects on grassland community. In addition, environmental factors such as temperature, rainfall, and snow melting can also be important for the concentration of litter leachates. Our approach and findings pave way for wider empirical evaluation of spatial heterogeneity in a range of systems, highlighting feedback links between plant spatial heterogeneity and litter dynamics. This study reports only a short-term response of litter leachate addition to enclosed grassland during two plant growing seasons. Future studies should explore long-term effects of litter leachates on animal-grazed grasslands.
Bansal, S., Sheley, R.L., Blank, B., Vasquez, E.A., 2014. Plant litter effects on soil nutrient availability and vegetation dynamics: changes that occur when annual grasses invade shrub-steppe communities. Plant Ecology 215, 367e378. Bork, E., Willms, W., Alexander, T.M., 2012. Seasonal patterns of forage availability in the fescue grasslands under contrasting grazing histories. Rangeland Ecology & Management 65, 47e55. Bradford, M.A., Berg, B., Maynard, D.S., Wieder, W.R., Wood, S.A., Cornwell, W., 2016. Understanding the dominant controls on litter decomposition. Journal of Ecology 104, 229e238. Campanella, M.V., Bisigato, A.J., 2010. What causes changes in plant litter quality and quantity as consequence of grazing in the Patagonian Monte: plant cover reduction or changes in species composition? Australian Ecology 35, 787e793. Chamane, S., Kirkman, K.P., Morris, C., O’Connor, T., 2017. Does high-density stocking affect perennial forbs in mesic grassland? African Journal of Rangeland Forestry Science 34, 133e142. Chapman, S.K., Newman, G.S., 2010. Biodiversity at the plantesoil interface: microbial abundance and community structure respond to litter mixing. Oecologia 162, 763e769. Chen, F.R., Cheng, J.M., Liu, W., Zhu, R.B., Yang, X.M., Zhao, X.Y., Su, J.S., 2013. Effects of different disturbances on diversity and biomass of communities in the typical steppe of loess region. Acta Ecologica Sinica 33, 2856e2866. Dai, Z.C., Wang, X.Y., Qi, S.S., Cai, H.H., Sun, J.F., Huang, P., Du, D.L., 2016. Effects of leaf litter on inter-specific competitive ability of the invasive plant Wedelia trilobata. Ecological Engineering 31, 367e374. De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R., Berg, M.P., de Ruiter, P.C., Verhoef, H.A., Bezemer, T.M., Putten, W.H., 2003. Soil invertebrate fauna enhances grassland succession and diversity. Nature 422, 711e713. Donath, T.W., Eckstein, R.L., 2010. Effects of bryophytes and grass litter on seedling emergence vary by vertical seed position and seed size. Plant Ecology 207, 257e268. Dong, S.K., Sha, W., Su, X.K., Zhang, Y., Li, S., Gao, X.X., 2019. The impacts of geographic, soil and climatic factors on plant diversity, biomass and their relationships of the alpine dry ecosystems: cases from the Aerjin Mountain Nature Reserve, China. Ecol Eng 127, 170e177. Elgersma, K.J., Yu, S., Vor, T., Ehrenfeld, J.G., 2012. Microbial-mediated feedbacks of leaf litter on invasive plant growth and interspecific competition. Plant Soil 356, 341e355. Garibaldi, L.A., Semmartin, M., Chaneton, E.J., 2007. Grazing-induced changes in plant composition affect litter quality and nutrient cycling in flooding Pampa grasslands. Oecologia 151, 650e662.
Z. Ma et al. / Rangeland Ecology & Management 73 (2020) 147e155 Grace, J.B., 2006. Structural equation modeling and natural systems. Cambridge University Press, Cambridge, UK, p. 348. Hang, J., 2014. Study on landscape pattern of vegetation and variation of composition and spatial distribution of ground-dwelling beetles (Coieoptera) community in Hilly and Gully Loess Regions, Ningxia. Ningxia University, Ningxia, China, p. 87. Harrop-Archibald, H., Didham, R.K., Standish, R.J., Tibbett, M., Hobbs, R.J., 2016. Mechanisms linking fungal conditioning of leaf litter to detritivore feeding activity. Soil Biology Biochemistry 93, 119e130. Hautier, Y., Tilman, D., Isbell, F., Seabloom, E.W., Borer, E.T., Reich, P.B., 2015. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336e340. Hobbie, S.E., 2015. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends in Ecology and Evolution 30, 357e363. Hou, F.J., Chang, S.H., Yu, Y.W., Ling, H.L., 2004. A review on trampling by grazed livestock. Acta Ecologica Sinica 24, 784e789. Hou, Y.P., Liu, L., Wang, X., Yan, X.Y., Men, H., Li, W.J., Xu, W.M., 2013. Allelopathic effects of aqueous extract of exotic plant Rhus typhina L. on soil microecosystem. Acta Ecologica Sinica 11, 592e595. Krueger-Mangold, J.M., Sheley, R.L., Svejcar, T.J., 2006. Toward ecologically-based invasive plant management on rangeland. Weed Science 54, 597e605. Laforgia, M.L., Spasojevic, M.J., Case, E.J., Latimer, A.M., Harrison, S.P., 2018. Seed banks of native forbs, but not exotic grasses, increase during extreme drought. Ecology 99, 896e903. Li, Q., 2014. The study on litter effects during old-field succession in Songnen plain. University of Chinese Academy of Sciences, Changchun, China, p. 99. Li, X.B., Liu, B.R., Chen, L., Song, N.P., 2015. Effects of litter accumulation on plant communities in fenced desert steppe. Polish Journal of Ecology 63, 333e340. Li, Y.L., Ning, Z.Y., Cui, D., Mao, W., Bi, J.D., Zhao, X.Y., 2016. Litter decomposition in a semiarid dune grassland: neutral effect of water supply and inhibitory effect of nitrogen addition. PLoS One 11, e0162663. Lipowsky, A., Roscher, C., Schumacher, J., Michalski, S.G., Gubsch, M., Buchmann, N., Schmid, B., 2015. Plasticity of functional traits of forb species in response to biodiversity. Perspectives in Plant Ecology 17, 66e77. Liu, Q., Wu, C.H., Peng, A.F., Gao, K., Chen, J.J., Li, Y., Fu, H., 2017. Flavonolignans from Elymus natans L. and phytotoxic activities. Journal of Agricultural Food Chemistry 65, 1320e1327. Liu, X.M., Nie, X.M., 2012. Effects of enclosure on the quantitative characteristics of alpine vegetation. Prataculture Science 29, 112e116. Loydi, A., Donath, T.W., Otte, A., Eckstein, R.L., Rennenberg, H., 2015. Negative and positive interactions among plants: effects of competitors and litter on seedling emergence and growth of forest and grassland species. Plant Biology 17, 667e675. Makkonen, M., Berg, M.P., Handa, I.T., Ttenschwiler, S., Ruijven, J.V., Bodegom, P.M., Aerts, R., 2012. Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecology Letters 15, 1033e1041. Makkonen, M., Berg, M.P., Van Logtestijn, R.S.P., Van Hal, J.R., Aerts, R., 2013. Do physical plant litter traits explain non-additivity in litter mixtures? A test of the improved microenvironmental conditions theory. Oikos 122, 987e997. Malenke, J.R., Skopec, M.M., Dearing, M.D., 2014. Evidence for functional convergence in genes upregulated by herbivores ingesting plant secondary compounds. BMC Ecology 14, 1e16. Ma, R.J., Wang, M.L., Zhu, X.T., Lu, X.W., Sun, K., 2005. Allelopathy and chemical constituents of Ligularia virgaurea volatile. Chinese Journal of Applied Ecology 16, 18e26. Ma, Z.W., Wang, Y.X., Wang, H., A, B.M., Zhang, Z.M., Hou, F.J., 2017. Litter and its functions in grazing ecosystems. Acta Pratacult Sinica 26, 201e212. Meier, C.L., Bowman, W.D., 2008. Links between plant litter chemistry, species diversity, and below-ground ecosystem function. PNAS 105, 19780e19785. Mitchell, R.M., Bakker, J.D., 2016. Grass abundance shapes trait distributions of forbs in an experimental grassland. Journal of Vegetation Science 27, 557e567. Mudr ak, O., Frouz, J., 2012. Allelopathic effect of Salix caprea litter on late successional plants at different substrates of post-mining sites: pot experiment studies. Botany 90 (4), 311e318. Nyanumba, S.M., Cahill, J.F.J., 2012. Effect of aboveground litter on belowground plant interactions in a native rough fescue grassland. Basic Applied Ecology 13, 615e622. Olson, B.E., Wallander, R.T., 2002. Effects of invasive forb litter on seed germination, seedling growth and survival. Basic Applied Ecology 3, 309e317. Pan, Q.M., Tian, D.S., Naeem, S., Auerswald, K., Elser, J.J., Bai, Y.F., Huang, J.H., Wang, Q.B., Wang, H., Wu, J.G., Han, X.G., 2016. Effects of functional diversity loss on ecosystem functions are influenced by compensation. Ecology 97, 2293e2302. uregui, C., Pizzio, M., Oesterheld, M., Acosta, A., 2016. Impact of Pizzio, R., Herrero-Ja stocking rate on species diversity and composition of a subtropical grassland in Argentina. Applied Vegetation Science 19, 454e461.
155
Rayamajhi, M.B., Pratt, P.D., Tipping, P.W., Center, T.D., 2012. Litter cover of the invasive tree Melaleuca quinquenervia influences seedling emergence and survival. Open Journal of Ecology 2, 131e140. R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https:// www.r-project.org. Accessed 16 July 2018. Ren, Y.D., Shang, Z.H., Long, R.J., 2014. Progress of allelopathy in grassland ecosystem of China. Pratacult Science 31, 993e1002. Rice, E.L., 1979. Allelopathy: an update. Botanical Review 45, 15e109. Samedani, B., Juraimi, A.S., Rafii, M.Y., Anuar, A.R., Sheikh, A.S.A., Anwar, M.P., 2013. Allelopathic effects of litter Axonopus compressus against two weedy species and its persistence in soil. Science World Journal, 2013:695404. Semmartin, M., Aguiar, M.R., Distel, R.A., Moretto, A.S., Ghersa, C.M., 2004. Litter quality and nutrient cycling affected by grazing-induced species replacements along a precipitation gradient. Oikos 107, 148e160. Shen, Y., Chen, W.Q., Yang, G.W., Yang, X., Liu, N., Sun, X., Chen, J.S., Zhang, Y.J., 2016. Can litter addition mediate plant productivity responses to increased precipitation and nitrogen deposition in a typical steppe? Ecological Research 31 (4), 579e587. Shi, X.M., Li, X.G., Wu, R.M., Yang, Y.H., Long, R.J., 2011. Changes in soil biochemical properties associated with Ligularia virgaurea spreading in grazed alpine meadows. Plant Soil 347, 65e78. Smith, B., Wilson, J.B., 1996. A consumer's guide to evenness indices. Oikos 76, 70e82. Tian, M., Hou, F.J., 2009. Responses of Lespedeza davurica seedling growth to residue aqueous extract of three forages. Pratacult Science 26, 45e49. Tredennick, A.T., Adler, P.B., Adler, F.R., Vasseur, D., 2017. The relationship between species richness and ecosystem variability is shaped by the mechanism of coexistence. Ecology Letters 20, 958e968. Vellend, M., Lechowicz, M.J., Waterway, M.J., 2000. Germination and establishment of forest sedges (Carex, Cyperaceae): tests for home-site advantage and effects of leaf litter. American Journal of Botany 87, 1517e1525. Wang, Q.Q., 2011. Effects of litter on seedling establishment of herb species in Leymus Chinensis grassland. Hebei University, Baoding, China, p. 43. Wang, C.T., Long, R.J., Wang, Q.L., Liu, W., Jing, Z.C., Zhang, L., 2010. Fertilization and litter effects on the functional group biomass, species diversity of plants, microbial biomass, and enzyme activity of two alpine meadow communities. Plant Soil 331, 377e389. Wen, L., Dong, S.K., Li, Y.Y., Sherman, R., Shi, J.J., Liu, D.M., 2013. The effects of biotic and abiotic factors on the spatial heterogeneity of alpine grassland vegetation at a small scale on the Qinghai-Tibet Plateau (QTP), China. Environment Monit Assess 185, 8051e8064. Xiao, C.W., Janssens, I.A., Zhou, Y., Su, J.Q., Liang, Y., Guenet, B., 2015. Strong stoichiometric resilience after litter manipulation experiments; a case study in a Chinese grassland. Biogeosciences 11, 757e767. Xie, T.P., Zhang, G.F., Zhao, Z.G., Du, G.Z., He, G.Y., 2014. Intraspecific competition and light effect on reproduction of Ligularia virgaurea an invasive native alpine grassland clonal herb. Ecology & Evolution 4, 827e835. Xiong, S.J., Nilsson, C., 1999. The effects of plant litter on vegetation: a meta-analysis. Journal of Ecology 87, 984e994. Yahdjian, L., Tognetti, P.M., Chaneton, E.J., 2017. Plant functional composition affects soil processes in novel successional grasslands. Functional Ecology 31, 1813e1823. Yu, L.N., 2012. Allelopathy effect of composite pant litters on Stipa seeds in loess region. Northwest Agriculture and Forestry University, Yangling, China, p. 65. Yuan, H., 2009. Responses of plant population and community to residue aqueous extract to main species of eastern Gansu province. Lanzhou University, Lanzhou, China, p. 83. Yuan, J.L., Liang, D.F., Zhang, S.T., 2015. Litter and its interaction with standing vegetation affect seedling recruitment in Tibetan alpine grasslands. Plant Ecology Diversity 9, 89e95. Zhang, L., Zhang, Y.J., Zou, J.W., Siemann, E., 2014. Decomposition of Phragmites australis litter retarded by invasive Solidago canadensis in mixtures: an antagonistic non-additive effect. Science Report 4, 5488. Zhang, R., Hu, X.W., Baskin, J.M., Baskin, C.C., Wang, Y.R., 2017. Effects of litter on seedling emergence and seed persistence of three common species on the Loess Plateau in Northwestern China. Front Plant Science 8, 103. Zhang, Y.J., Tang, S.M., Liu, K.S., Li, X.F., Huang, D., Wang, K., 2015. The allelopathic effect of Potentilla acaulis, on the changes of plant community in grassland, northern China. Ecol Res 30, 41e47. Zhao, Z.G., Du, G.Z., Zhou, X.H., Wang, M.T., Ren, Q.J., 2006. Variations with altitude in reproductive traits and resource allocation of three Tibetan species of Ranunculaceae. Australian Journal of Botany 54, 691e700. Zhou, H.K., Zhao, X.Q., Wen, J., Chen, Z., Yao, B.Q., Yang, Y.W., Xu, W.X., Duan, J.C., 2012. The characteristics of soil and vegetation of degenerated alpine steppe in the Yellow River source region. Acta Pratacult Sinitra 21, 1e11.
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Rangeland Ecology & Management journal homepage: http://www.elsevier.com/locate/rama
Effects of Litter Leachate on Plant Community Characteristics of Alpine Grassland in Qinghai Tibetan Plateau* Zhouwen Ma a, Yingxin Wang a, Yongchao Gu a, Saman Bowatte a, Qingping Zhou b, Fujiang Hou a, * a
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, China Institute of Qinghai-Tibet Plateau, Southwest University for Nationalities, Chengdu, 610041, China
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 January 2019 Received in revised form 29 September 2019 Accepted 11 October 2019
Plant litter dynamics are sensitive to grassland productivity and the spatial heterogeneity of plant community. In this study, we investigated the effects of litter leachates on plant community characteristics using three plant species that represent different successional stages of alpine grasslands located on the Qinghai-Tibetan Plateau (QTP). We tested four concentrations of leachates (0, 50, 100, and 200 g L1) from Kobresia setchwanensis, Elymus nutans, and Ligularia virgaurea. The leachates from the three plant species generally responded similarly, but the responses to the varying concentrations were significantly different. Addition of litter leachates negatively impacted the aboveground biomass and species richness. The Shannon-Wiener diversity index was positively correlated with the litter leachate addition. The effects of the litter leachate’s addition on plant functional groups varieddgrasses were inhibited, forbs and legumes were promoted, and sedges were not significantly affected. This study demonstrates that litter leachates are a critical determinant of species diversity, grassland productivity, and community structure in QTP alpine grasslands. © 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Key Words: Alpine meadow community structure plant functional group grassland litter leachates species diversity
Introduction Climate change and unreasonable grazing can alter grassland plant community structure in Qinghai-Tibetan Plateau (QTP) (Lu et al. 2016; Dong et al. 2019), resulting in spatially heterogeneous litter accumulation. These compositional changes can result in variation in litter turnover, thereby altering ecosystem processes such as nutrient cycling (Hobbie and Sarah 2015) and plant community characteristics, as well as plant functional traits (Makkonen et al. 2012; Yuan et al. 2015; Dai et al. 2016). The heterogeneity introduced by the patchy accumulation of litter can also affect the plant community structure (Elgersma et al. 2012; Loydi et al. 2015), but the mechanisms driving such impacts in QTP grasslands have rarely been investigated and therefore are poorly understood.
* This study was supported by the Project of the Second Tibetan Plateau Scientific Expedition (2019QZKK0302), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20100102), the National Natural Science Foundation of China (31672472), the program for Changjiang Scholars and Innovative Research Team in University (IRT_17R50) and the 111 project (B12002). * Correspondence: Professor Fujiang Hou, Lanzhou University, Lanzhou, 730000, Gansu, China. E-mail address: [email protected] (F. Hou).
Litter plays an important role in plant growth and soil properties (Chapman and Newman 2010; Bradford et al. 2016; Harrop-Archibald et al. 2016). Decomposition of litter can impact nutrient cycling (Meier and Bowman 2008), as well as seed germination (Zhang et al. 2017) and establishment of seedlings (Yuan et al. 2015). Furthermore, litter contributes to interspecific competition of grassland community structure and succession (Donath and Eckstein 2010; Hobbie and Sarah 2015; Xiao et al. 2015). Litter can also provide favorable sites and energy for the life activities of microorganisms, soil fauna, and small herbivores. It also affects the structure and function of grassland ecosystems, which drives the progressive succession of plant communities (Hou et al. 2004; Bork et al. 2012; Hang 2014; Ma et al. 2017). Although the effects of physical changes induced by litter on grassland communities are well documented, the mechanisms of grassland community responses to chemical changes are not. Plant litter can influence establishment of seedlings and germination by allelopathy effects of litter leachates (Rice 1979; Samedani et al. 2013; Dai et al. 2016). Allelochemicals can also play a role in regulating ecosystem functions, including herbivory, decomposition, and nutrient mineralization (Hou et al. 2013; Li et al. 2014; Malenke et al. 2014). The strength of the allelopathy can be different between plant species where the chemical properties
https://doi.org/10.1016/j.rama.2019.10.003 1550-7424/© 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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of the litter leachates depend on substances accumulated in plant organs before senescence and biochemical transformations during decomposition. Most previous studies have investigated the responses of individual species to litter leachate addition (Olson and Wallander 2002; Tian and Hou 2009; Mudr ak and Frouz 2012; Samedani et al. 2013), but the responses to individual species may not reflect the combined response of plant communities composed of various functional groups such as in the natural grasslands in the QTP. The plant community responses to litter leachates of grassland species in the QTP have never been investigated, and such information is vital for developing the best management strategies for healthy grasslands in the QTP that are experiencing constant changes in vegetation composition (Zhou et al. 2012). Here we report a 2-yr field experiment conducted in alpine meadow grassland in the QTP to investigate the impacts of litter leachates on grassland species composition and functional traits. We investigated the effects of litter leachates from three grassland species dominant during early, mid, and late stages of succession in alpine meadow grasslands of QTP. The litter leachates were obtained from 1) Kobresia setchwanensis, a perennial sedge belonging to the Cyperaceae family; 2) Elymus nutans, a perennial grass belonging to the Gramineae family; and 3) Ligularia virgaurea, a perennial noxious forb belonging to the Asteraceae family. In natural conditions, leachates of litter consist of materials leached by washings from rainwater falling through litter or from chemical compounds released during the decomposition of litter. In our study, we used water extracts of pulverized dried litter as a means to examine maximum potential effects of chemical composition of litter leachates. We hypothesized that litter leachates from plant species representing three different successional stages would affect the grassland community composition and functional traits differently due to the differences in the chemical composition of the litter for the three species. We also tested the effects of different concentrations of litter leachate because under natural conditions, the concentration of litter leachate released to the soil can vary spatially and temporally. The objective of our study was to investigate the effects of litter leachates from three representative plant species of different successional stages in alpine grasslands in the QTP on aboveground biomass and plant community diversity. Materials and Methods
tartaricus, and Ligularia virgaurea. Legumes included Tibetia himalaica and Oxytropis.
Litter Collection and Leachate Preparation Plant litter of Elymus nutans (En), Kobresia setchwanensis (Ks), and Ligularia virgaurea (Lv) was collected from the QTP Research Base of Southwest Minzu University, after the grass withered and turned yellow in late October of 2014 and 2015. The litter was air dried at room temperature. The litter was then pulverized into powder and packed in polyethylene bags and stored 4 mo at room temperature. Pulverized dry powder (200 g) of three types of litter was steeped in 1 L of distilled water for 48 h at room temperature (15 C) and filtered through a double layer of nylon gauze (Yuan 2009). The leachate was then diluted with distilled water to obtain concentrations of 50, 100, and 200 g L1. Distilled water was used as the control (0 g L1).
Experimental Design The experimental area at the study site is a moderately degraded grassland. Since 2014, yak have grazed the site from late November to February. The randomized complete block design was used in the experiment. We established a concentration gradient using litter collected from three different species. Each plot was 2 2 m, arranged in three blocks. The buffer of each plot was 1 m, and blocks were separated by a 2-m strip. Each treatment had 3 replications. In early May 2015 and 2016, all aboveground plant materials were removed from all plots by cutting 2-cm aboveground herbage and removing litter by hand. We added four concentrations of leachate (0, 50, 100, and 200 g L1) of each litter type by hand sprayer in early May, June, and July in each yr. Each plot received 4 L of leachate. The volume of leachate application (4 L) was based on an estimation, assuming leachate incorporation of 100 g litter L1 (Yuan 2009) over 3 mo in a grassland where average litter accumulation of 300 g m2 (Yuan et al. 2015) was occurring. The litter leachate concentration treatments were adjusted (half and double) by the quantity of litter used to prepare the leachate, and the volume of leachate application was kept constant.
Study Site This experiment was conducted in 2015 and 2016 at the QTP Research Base of Southwest Minzu University, located in Hongyuan (3147'34”N, 102 33'07”E), on the northeastern boundary of the QTP in China (3485 m above sea level). The mean annual temperature is 1.4 C, ranging from 9.5 C in January to 11 C in July, the temperature varies greatly between day and night, where average relative humidity is 6070%. Mean annual sunshine duration is 2 159 hours, and mean annual precipitation is 791.95 mmd80% of which occurs from May to September. The study area belongs to the continental alpine temperate monsoon climate zone. The soil type is classified as Mat Cry-gelic Cambisols (Chinese Soil Taxonomy 1995). The annual growth season of the vegetation at the study site is from April to the end of September (Fig. 1). The return to the green period is mainly concentrated in April to May, reaching peak growth in mid August, with vegetation average coverage of > 80%. The plant community comprises of 53% forbs, 26% grasses, 17% sedges, and 4% legumes. All the grasses, sedges, and legumes were perennials. Of the forbs present in this study, 5% were annuals. Dominant grasses included Elymus nutans and Poa pratensis. Dominant sedges included kobresia setchwanensis and Kobresia Pygmaea. Dominant perennial forbs included Saussurea purpurea, Anemone trullifolia, Anaphalis lactea, Potentilla fragarioides, Aster
Field Sampling and Measurements In August (peak of growing season) of each yr, plant community species richness, plant density, plant height, and aboveground biomass were measured for each species by harvesting 0. 5 0.5 m quadrats at 2-cm height above in a randomly selected area within each plot. Plant community species richness was estimated by counting the number of all species in the quadrat. Plant density was estimated by summation of all the number of individuals in the quadrat. Plant height was measured using ruler measures for absolute height of each plant. The aboveground biomass was harvested, separated by species, oven dried at 65 C for 48 h, and weighed. All plant species were classified according to life form (annual and perennials) and four plant functional groups (PFGs) (grasses, sedges, legumes, and forbs).
Data Analysis Calculation of plant community species diversity was used for analysis of the ShannoneWiener diversity index (H0 ) and important value (IV) (Smith and Wilson 1996; Liu and Nie 2012; Pizzio et al. 2016), with the following equations:
Litter Leachate Effects on Plant Functional Groups The responses of plant functional groups (PFGs) to the addition of litter leachates were estimated by the importance value; an index to indicate relative dominance of a species in a plant community. The responses of PFGs to three litter leachate types were similar (Table 1). The effects of litter leachates addition on PFGs varied. Compared with the control, addition of litter leachates increased the legumes and forbs, decreased grasses, and had no
P
0.629 0.701 0.569 0.999 0.183 0.557 0.944 0.899 0.672 0.744 0.489 0.27 0.338 0.652 0.711 0.414 0.73 0.635 0.809 0.068 1.582 0.827 0.277 0.361 0.673 0.581 0.92 1.313 1.178 0.699 0.623 1.043 0.479 0.9 0.362 0.597 0.113 0.589 0.862 0.76 0.543 0.333 0.666 0.185 0.32 0.347 0.889 0.503 0.939 0.36 1.133 0.771 1.879 0.782 0.418 0.559 0.844 1.181 0.68 1.544 1.214 1.162 0.379 0.904 0.251 0.239 0.226 0.144 0.922 0.187 0.388 0.263 0.031 0.544 0.056 0.005 0.161 0.388 0.092 0.752 1.424 1.461 1.514 1.901 0.161 1.683 1.034 1.386 3.223 0.722 2.712 4.788 1.808 1.035 2.272 0.402 0.294 0.111 0.377 0.923 0.399 0.231 0.755 0.93 0.147 0.243 0.385 0.426 0.842 0.77 0.451 0.826 1.263 2.323 1.002 0.08 0.945 1.523 0.283 0.073 1.996 1.458 0.975 0.868 0.173 0.263 0.809 0.192 0.253 0.111 0.346 0.002 0.74 0.001 0.002 0.379 0.070 0.022 0.002 0.79 < 0.0001 0.359 0.188 < 0.0001 1.347 2.653 0.911 11.19 0.112 14.01 11.21 0.795 3.432 5.633 10.25 3.226 65.88 0.864 1.782 30.54 < 0.0001 < 0.0001 < 0.0001 < 0.0001 0.104 0.318 < 0.0001 0.487 0.604 0.019 0.887 0.001 0.002 0.313 < 0.001 0.009 111.82 8.356 110.93 27.043 2.219 1.182 45.121 0.827 0.623 3.656 0.213 6.219 5.670 1.226 6.536 4.495 0.414 0.546 0.471 0.813 0.151 0.103 0.870 0.668 0.540 0.595 0.795 0.068 0.618 0.187 0.428 0.747
Concentration
F P F P F P F
Yr Litter type
Litter type Concentration
P F P
0.903 0.614 0.769 0.208 2.002 2.209 0.140 0.408 0.625 0.525 0.230 2.854 0.487 1.752 0.863 0.293
The response of litter leachate addition on plant species richness and Shannon-Weiner index were similar for all three litter types (Table 1). The plant species richness of total community decreased with increasing concentration of added leachate in 2015 (Fig. 3A), annual species richness was decreased in both 2015 and 2016 (Fig. 3B), and had no impact on perennial species (Fig. 3C). The Shannon-Weiner index was significantly higher in treatment plots than the control in 2016 (P < 0.05) but not affected in 2015 (Fig. 3D).
Community aboveground biomass Annual species aboveground biomass Perennial species aboveground biomass Grasses aboveground biomass Sedges aboveground biomass Legumes aboveground biomass Forbs aboveground biomass Litter aboveground biomass Community species richness Annual species richness Perennial species richness Shannon-Wiener diversity index Important value of grasses Important value of sedges Important value of legumes Important value of forbs
Litter Leachate Effects on Plant Species Diversity
F
The plant community aboveground biomass response to the addition of litter leachate was similar in both years and for all three litter types (Table 1). In both years, irrespective of litter type, the aboveground biomass of community, grasses, forbs, perennial, and annual species significantly decreased with increasing concentration of the added litter leachate (P < 0.0001) (Figs. 2E, 2A, 2D, 2H, and 2G) and had no impact on sedges, legumes, and litter (Figs. 2B, 2C, 2F). The aboveground biomasses of the grasses and legumes were significantly lower in 2015 than in 2016, but forbs showed an opposite trend (Table 1).
P
Litter Leachate Effects on Plant Community Aboveground Biomass
F
Results
Yr Concentration
Where rd is the relative density, rh is the relative height, and rb is the relative aboveground biomass. Pi is the proportion of species i based on percent biomass data. We used structural equation modeling (SEM) to estimate the contributions of litter leachate to aboveground biomass and community diversity (Grace 2006). In the model, we assumed that litter leachate addition had the potential to alter aboveground biomass directly, as well as indirectly changing community diversity. The standard path coefficients were estimated to indicate the strengths of these multiple effects. We used the chi-square test, Akaike information criteria, and the root mean square error of approximation to evaluate the fit of model. The SEM analyses was performed using AMOS 17.0 (Amos Development Company, Greene, ME) for Windows (SPSS Inc., Chicago, IL). The effects of litter leachate type, leachate concentration, yr, and their interactions on plant community characteristics were analyzed using the analysis of variance procedure, and means were separated by the LSD test at the 5% probability level, using Statistical Product and Service Solutions software version 17.0 (SPSS Inc., Chicago, IL). Principal component analysis (PCA) was carried out using the vegan package of R program (R Core Team 2013) to illustrate the plant community composition variation responses to the leachate addition.
Yr Litter type
[2]
Yr
Pi ln ðPiÞ
Concentration
X
Litter type
H0 ¼
[1]
Variable
IV ¼ ð rd þ rh þ rb Þ = 3
Table 1 Statistical summary of the effects (P values) of litter leachate concentrations, litter type, yr, and interactions on aboveground biomass, species diversity, functional groups. Significant effects (P < 0.05) are highlighted in bold.
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Figure 1. Monthly mean precipitation and temperature from 2014 to 2016 at the study site located in Hongyuan (3147'34”N, 102 33'07”E) at the Qinghai Tibetan Plateau, China.
impact on sedges (Fig. 4). These responses were consistent in both yrs (Table 1). The grasses and forbs composition in the plant community was significantly lower in 2016 than in 2015 (Table 1), which may have been due to the lower rainfall during the plant growing season in 2016 (Fig. 1). Variation in Plant Community Composition by Litter Leachate Addition The first two axes of the PCA accounted for 61.8% of the total variance, which can reflect the characteristics of community composition. There was no discernible pattern in the distribution of litter types in the principal component ordination space (Fig. 5). Axis 1 accounted for 47.9% of the variance and illustrated the plant community structure changes with the decreasing of concentration of litter leachate. No separation of these groups was evident on axis 2. Relationships Between Litter Leachate Addition and Plant Community Characteristics The structural equation model (SEM) (Fig. 6) was used to evaluate casual relationships between the litter leachate and the plant community characteristics to understand how litter leachate would affect the grassland plant community. There were significant direct negative effects of litter leachate on aboveground biomass, which further indirectly affected plant species richness and species diversity estimated by the Shannon-Weiner index. Discussion The results of our study contribute to the numerous previous research that demonstrates the profound effect litter can have on grassland productivity (Fig. 2) and botanical composition of plant community structure (Figs. 4 and 5). More importantly, it provides new evidence for a potential mechanism driving such impacts, through litter leachates in an alpine grassland in QTP (Fig. 6). Contrary to our hypothesis, the responses of leachates from the tested plant species were generally similar, but the responses to the concentrations of the litter leachate were significant. Structural equation modeling (Fig. 6) indicated the addition of litter leachates affected grassland plant community through strong effects on aboveground biomass, plant species richness, and community species diversity. This result is consistent with Xiong et al.’s (1999) general view, established from a meta-analysis using the data from 35 studies worldwide, that plant litter has a significant effect on vegetation. Their meta-analysis indicated overall litter effects were
stronger on species richness than on aboveground biomass. In our study, which considered litter leachate effects only, the effects on aboveground biomass were much stronger than the species diversity effects (Fig. 6). The strong direct negative effect of litter leachate on aboveground biomass (Fig. 2) was possibly through the effects of allelopathy. The different secondary compounds contained in the litter leachates could have inhibited plant growth (Ma et al. 2005; Liu et al. 2017). Other studies, including research on Leymus chinensis grassland and the Canadian savannah, similarly reported that increasing concentrations of litter leachate decreased plant community biomass (Wang 2011; Nyanumba and Cahill 2012). Furthermore, it is possible that higher concentrations of litter leachate impacted carbon and nitrogen cycle processes (Meier and Bowman 2008), soil organic matter decomposition, nitrification and mineralization (Zhang et al. 2014), and soil microorganism activity (Makkonen et al. 2013; Li et al. 2016; Yahdjian et al. 2017), resulting in a decrease in plant available nutrients, which would have an effect on plant growth and contribute to the reduction in aboveground biomass. We found that increased litter leachate concentration changed the proportion of different plant families, affected vertical (grasses) and rhizomatous (forbs) plant growth (Fig. 2A and 2D), and may have increased spatial variation in plant growth, resulting in reduced aboveground biomass as suggested by Wen et al. (2013). The loss of dominant PFGs from grassland ecosystems can result in significant aboveground biomass reduction as observed by Pan et al. (2016) in an Inner Mongolian grassland. In our study, increased inhibition of the grasses (Fig. 4A) indicates that such a mechanism may be involved. We found that plant species richness, an important indicator of species diversity and species competitive coexistence (Liu et al. 2016; Tredennick et al. 2017), decreased with increasing concentration of added leachate (Fig. 3A and B); however, the ShannonWeiner index estimates indicated that the addition of leachate significantly increased plant community diversity in 2016 (Fig. 3D). The Shannon-Weiner diversity index is a measure of the degree of diversity and heterogeneity at the species level, which comprehensively reflects the species richness and evenness of the community. So, it is somewhat different from the results of species richness (Chen et al. 2013). Part of this effect may be due to litter phytotoxins leaching into the soil and impeding seedling recruitment (Vellend et al. 2000; Yu 2012). Alpine plants have low levels of seedling establishment from seed (Yuan et al. 2015), but most annual plants (Scrophulariaceae, Gentianaceae, Caryophyllaceae) and some perennial plants (grasses, Asteraceae ect.) are primarily established from seed. High concentrations of litter leachate
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Figure 2. The response of aboveground biomass to the addition of litter leachates. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level.
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Figure 3. The response of litter leachate addition on plant species diversity. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level in the same year.
consequently inhibited the annual plant seed germination, thus reducing annual plant species richness. Perennials can be multiplied by other means (Zhao et al. 2006), so there was less of an impact on the species richness of perennials. However, this possibility should be considered cautiously as we do not have long-term data on annual and perennial plant recruitment and seedling establishment within these plots. High-concentration litter leachate weakened the relative importance of the dominant species such as grasses (Fig. 4A) and indirectly enhanced the relative importance and development of other species such as legumes and forbs (Fig. 4C and 4D) in the community, which is an important cause of the increase in plant diversity. Zhang et al. (2015) suggested that allelopathy may be an important mechanism of plant dominance that allows certain plants to modify community diversity by affecting the seedling establishment of co-occurring species. In addition, litter leachate can affect plant community indirectly through their effects on soil fauna that are known to affect the composition of natural vegetation strongly (De Deyn et al. 2003). Different PFGs’ important values were inhibited, promoted, or unaffected by litter leachate (Table 1, Fig. 4). Grasses were inhibited by the addition of litter leachate (Fig. 4A), while legumes and forbs were promoted by leachate addition (Fig. 4C and D). The sedges were not significantly affected by litter leachate addition (Fig. 4B). Part of this impact may be through different species of functional groups having different requirements for seedling emergence and survival (Yuan 2009; Rayamajhi et al. 2012). In addition, growth mechanisms may play a role, with the varying growth mechanisms of different genera and plants being
impacted differently by litter leachate type and concentration. For example, similar to our study, sedges did not respond to litter in Wang et al’s (2010) study and speculated the neutral responses to litter was due to crowd-short rhizomatous growth form and inherent developmental constraints. In comparison, the positive response of forbs to the leachate addition was due to the competitive advantage of negative response by grasses (Chamane et al 2017). The positive responses by forbs to leachate is important for vegetation dynamics, especially in grasslands like our experimental site in which forbs contribute to 53% of the plant community. Forbs contribute to much of the plant diversity in grasslands, enrich the seed bank (Laforgia et al. 2018), and often show considerable trait plasticity in response to changes in species richness and composition (Lipowsky et al. 2015). Therefore, forbs are important for both convergence and divergence between species for specific traits (Mitchell et al. 2016). Chemical, physical, and biological feedback from litter varies with functional groups (Ma et al. 2017), and so litter can regulate the structure and function (Fig. 5) of grassland ecosystem in many ways. Litter of Ligularia virgaurea has been previously shown to affect the composition of plant communities (Shi et al. 2011; Xie et al. 2014). However, its effect is concerning, as it is a noxious weed that indicates severe degradation of grasslands. In other studies, invasive plant species have increased their impact on the existing plant community through the litter they produce, as in the case of sage brush-steppe plant communities being altered by the invasion of annual grasses (Bansal et al. 2014). This impact can be through general impacts on soil nutrient cycling, as well as production of alleochemicals.
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Figure 4. The responses of plant functional groups (PFGs) to the addition of litter leachates. Different letters for mean values indicate significant difference among litter leachate treatments at P < 0.05 level.
The SEM (Fig. 6) demonstrated that leachate-driven changes to forbs and grass biomass influenced plant community diversity. Such PFGs or plant species changes can add further feedbacks to the plant community in future years through variable levels of litter accumulation, spatially and in time (Li 2014). Plant species provide a strong source of variation in standing litter mass and litter chemistry (Ren et al. 2014,) and any factors that affect plant community composition (Fig. 5) would therefore influence litter mass accumulation and hence litter leachate dynamics. It is well recognized that grazing regimes and environmental factors can substantially influence the plant community composition (Garibaldi et al. 2007; Shen et al. 2016). Semmartin et al. (2004) showed evidence that grazing, rainfall, and their interactions induced plant community changes and altered litter quality, causing major changes in ecosystem functions such as in nutrient cycling. The
importance of grazing-induced plant composition changes on litter chemistry was also highlighted by Campanella and Bisigato (2010). Our study showed such litter quality impacts are possibly through litter leachates. Li et al. (2015) reported that in a desert step grassland the green-up dates can be advanced up to 7 d when litter accumulation reaches 300400 g m2, benefiting healthy grassland systems by maintaining community stability. Identifying such critical levels for litter leachate accumulation under varying grazing management regimes would be beneficial for developing best practices for sustainable grassland management. In the QTP, climate change and intensive animal grazing has been attributed to plant community changes and grassland degradation (Hautier et al. 2015). Therefore, future studies are warranted for the environmental and grazing effects of litter leachate feedbacks and their impact on plant community changes.
Figure 5. Principal component analysis illustrating the variation in plant community composition by litter leachate addition.
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Figure 6. A structural equation model of treatment effects on above-ground biomass and community diversity. The structural equation model considered all plausible pathways through which experimental treatments influence community aboveground biomass and diversity. Solid and dashed line arrows represent significant and nonsignificant pathways, respectively. Numbers indicate the standard path coefficients. Arrow width is proportional to the strength of the relationship. R2 represents the proportion of variance explained for each dependent variable in the model. *P < 0.05, **P < 0.01, ***P < 0.001; (a)c2 ¼ 1.241, df ¼ 2, P ¼ 0.538; root mean square error of approximation (RMSEA) ¼ 0.000.
In summary, we found litter leachate additions to a native mixed-grass alpine grassland community generated a strong response to the aboveground biomass and plant community diversity, highlighting the importance of litter leachate in maintaining grassland community structure and ecosystem functions.
Acknowledgments The authors are grateful to the Qinghai-Tibet Plateau Research Base of Southwest Minzu University for supporting the field work.
References Implications An important implication of our study is improved understanding of the link between litter feedbacks on plant community composition through litter leachates. Such understanding is important for the management of natural grasslands. We found that at higher leachate concentrations, there were significant changes in herbage biomass, species richness, and composition of PFGs, indicating potential impacts on grassland community stability. These feedbacks can also have broader implications on spatial variability, biodiversity, and ecosystem processes. Our results also indicate that litter dynamics may have the potential to shift vegetation succession of the plant community, as species availability, species functional characteristics, and site availability are three primary causes of succession (Krueger-Mangold et al. 2006), and litter leachate can have an impact on all three of these. In our study, the impact of leachate concentration was much stronger than the litter identity. As litter mass is one of the key factors that would influence leachate concentration, standing total litter mass can be considered as a critical factor influencing litter leachate feedback effects on grassland community. In addition, environmental factors such as temperature, rainfall, and snow melting can also be important for the concentration of litter leachates. Our approach and findings pave way for wider empirical evaluation of spatial heterogeneity in a range of systems, highlighting feedback links between plant spatial heterogeneity and litter dynamics. This study reports only a short-term response of litter leachate addition to enclosed grassland during two plant growing seasons. Future studies should explore long-term effects of litter leachates on animal-grazed grasslands.
Bansal, S., Sheley, R.L., Blank, B., Vasquez, E.A., 2014. Plant litter effects on soil nutrient availability and vegetation dynamics: changes that occur when annual grasses invade shrub-steppe communities. Plant Ecology 215, 367e378. Bork, E., Willms, W., Alexander, T.M., 2012. Seasonal patterns of forage availability in the fescue grasslands under contrasting grazing histories. Rangeland Ecology & Management 65, 47e55. Bradford, M.A., Berg, B., Maynard, D.S., Wieder, W.R., Wood, S.A., Cornwell, W., 2016. Understanding the dominant controls on litter decomposition. Journal of Ecology 104, 229e238. Campanella, M.V., Bisigato, A.J., 2010. What causes changes in plant litter quality and quantity as consequence of grazing in the Patagonian Monte: plant cover reduction or changes in species composition? Australian Ecology 35, 787e793. Chamane, S., Kirkman, K.P., Morris, C., O’Connor, T., 2017. Does high-density stocking affect perennial forbs in mesic grassland? African Journal of Rangeland Forestry Science 34, 133e142. Chapman, S.K., Newman, G.S., 2010. Biodiversity at the plantesoil interface: microbial abundance and community structure respond to litter mixing. Oecologia 162, 763e769. Chen, F.R., Cheng, J.M., Liu, W., Zhu, R.B., Yang, X.M., Zhao, X.Y., Su, J.S., 2013. Effects of different disturbances on diversity and biomass of communities in the typical steppe of loess region. Acta Ecologica Sinica 33, 2856e2866. Dai, Z.C., Wang, X.Y., Qi, S.S., Cai, H.H., Sun, J.F., Huang, P., Du, D.L., 2016. Effects of leaf litter on inter-specific competitive ability of the invasive plant Wedelia trilobata. Ecological Engineering 31, 367e374. De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R., Berg, M.P., de Ruiter, P.C., Verhoef, H.A., Bezemer, T.M., Putten, W.H., 2003. Soil invertebrate fauna enhances grassland succession and diversity. Nature 422, 711e713. Donath, T.W., Eckstein, R.L., 2010. Effects of bryophytes and grass litter on seedling emergence vary by vertical seed position and seed size. Plant Ecology 207, 257e268. Dong, S.K., Sha, W., Su, X.K., Zhang, Y., Li, S., Gao, X.X., 2019. The impacts of geographic, soil and climatic factors on plant diversity, biomass and their relationships of the alpine dry ecosystems: cases from the Aerjin Mountain Nature Reserve, China. Ecol Eng 127, 170e177. Elgersma, K.J., Yu, S., Vor, T., Ehrenfeld, J.G., 2012. Microbial-mediated feedbacks of leaf litter on invasive plant growth and interspecific competition. Plant Soil 356, 341e355. Garibaldi, L.A., Semmartin, M., Chaneton, E.J., 2007. Grazing-induced changes in plant composition affect litter quality and nutrient cycling in flooding Pampa grasslands. Oecologia 151, 650e662.
Z. Ma et al. / Rangeland Ecology & Management 73 (2020) 147e155 Grace, J.B., 2006. Structural equation modeling and natural systems. Cambridge University Press, Cambridge, UK, p. 348. Hang, J., 2014. Study on landscape pattern of vegetation and variation of composition and spatial distribution of ground-dwelling beetles (Coieoptera) community in Hilly and Gully Loess Regions, Ningxia. Ningxia University, Ningxia, China, p. 87. Harrop-Archibald, H., Didham, R.K., Standish, R.J., Tibbett, M., Hobbs, R.J., 2016. Mechanisms linking fungal conditioning of leaf litter to detritivore feeding activity. Soil Biology Biochemistry 93, 119e130. Hautier, Y., Tilman, D., Isbell, F., Seabloom, E.W., Borer, E.T., Reich, P.B., 2015. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336e340. Hobbie, S.E., 2015. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends in Ecology and Evolution 30, 357e363. Hou, F.J., Chang, S.H., Yu, Y.W., Ling, H.L., 2004. A review on trampling by grazed livestock. Acta Ecologica Sinica 24, 784e789. Hou, Y.P., Liu, L., Wang, X., Yan, X.Y., Men, H., Li, W.J., Xu, W.M., 2013. Allelopathic effects of aqueous extract of exotic plant Rhus typhina L. on soil microecosystem. Acta Ecologica Sinica 11, 592e595. Krueger-Mangold, J.M., Sheley, R.L., Svejcar, T.J., 2006. Toward ecologically-based invasive plant management on rangeland. Weed Science 54, 597e605. Laforgia, M.L., Spasojevic, M.J., Case, E.J., Latimer, A.M., Harrison, S.P., 2018. Seed banks of native forbs, but not exotic grasses, increase during extreme drought. Ecology 99, 896e903. Li, Q., 2014. The study on litter effects during old-field succession in Songnen plain. University of Chinese Academy of Sciences, Changchun, China, p. 99. Li, X.B., Liu, B.R., Chen, L., Song, N.P., 2015. Effects of litter accumulation on plant communities in fenced desert steppe. Polish Journal of Ecology 63, 333e340. Li, Y.L., Ning, Z.Y., Cui, D., Mao, W., Bi, J.D., Zhao, X.Y., 2016. Litter decomposition in a semiarid dune grassland: neutral effect of water supply and inhibitory effect of nitrogen addition. PLoS One 11, e0162663. Lipowsky, A., Roscher, C., Schumacher, J., Michalski, S.G., Gubsch, M., Buchmann, N., Schmid, B., 2015. Plasticity of functional traits of forb species in response to biodiversity. Perspectives in Plant Ecology 17, 66e77. Liu, Q., Wu, C.H., Peng, A.F., Gao, K., Chen, J.J., Li, Y., Fu, H., 2017. Flavonolignans from Elymus natans L. and phytotoxic activities. Journal of Agricultural Food Chemistry 65, 1320e1327. Liu, X.M., Nie, X.M., 2012. Effects of enclosure on the quantitative characteristics of alpine vegetation. Prataculture Science 29, 112e116. Loydi, A., Donath, T.W., Otte, A., Eckstein, R.L., Rennenberg, H., 2015. Negative and positive interactions among plants: effects of competitors and litter on seedling emergence and growth of forest and grassland species. Plant Biology 17, 667e675. Makkonen, M., Berg, M.P., Handa, I.T., Ttenschwiler, S., Ruijven, J.V., Bodegom, P.M., Aerts, R., 2012. Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecology Letters 15, 1033e1041. Makkonen, M., Berg, M.P., Van Logtestijn, R.S.P., Van Hal, J.R., Aerts, R., 2013. Do physical plant litter traits explain non-additivity in litter mixtures? A test of the improved microenvironmental conditions theory. Oikos 122, 987e997. Malenke, J.R., Skopec, M.M., Dearing, M.D., 2014. Evidence for functional convergence in genes upregulated by herbivores ingesting plant secondary compounds. BMC Ecology 14, 1e16. Ma, R.J., Wang, M.L., Zhu, X.T., Lu, X.W., Sun, K., 2005. Allelopathy and chemical constituents of Ligularia virgaurea volatile. Chinese Journal of Applied Ecology 16, 18e26. Ma, Z.W., Wang, Y.X., Wang, H., A, B.M., Zhang, Z.M., Hou, F.J., 2017. Litter and its functions in grazing ecosystems. Acta Pratacult Sinica 26, 201e212. Meier, C.L., Bowman, W.D., 2008. Links between plant litter chemistry, species diversity, and below-ground ecosystem function. PNAS 105, 19780e19785. Mitchell, R.M., Bakker, J.D., 2016. Grass abundance shapes trait distributions of forbs in an experimental grassland. Journal of Vegetation Science 27, 557e567. Mudr ak, O., Frouz, J., 2012. Allelopathic effect of Salix caprea litter on late successional plants at different substrates of post-mining sites: pot experiment studies. Botany 90 (4), 311e318. Nyanumba, S.M., Cahill, J.F.J., 2012. Effect of aboveground litter on belowground plant interactions in a native rough fescue grassland. Basic Applied Ecology 13, 615e622. Olson, B.E., Wallander, R.T., 2002. Effects of invasive forb litter on seed germination, seedling growth and survival. Basic Applied Ecology 3, 309e317. Pan, Q.M., Tian, D.S., Naeem, S., Auerswald, K., Elser, J.J., Bai, Y.F., Huang, J.H., Wang, Q.B., Wang, H., Wu, J.G., Han, X.G., 2016. Effects of functional diversity loss on ecosystem functions are influenced by compensation. Ecology 97, 2293e2302. uregui, C., Pizzio, M., Oesterheld, M., Acosta, A., 2016. Impact of Pizzio, R., Herrero-Ja stocking rate on species diversity and composition of a subtropical grassland in Argentina. Applied Vegetation Science 19, 454e461.
155
Rayamajhi, M.B., Pratt, P.D., Tipping, P.W., Center, T.D., 2012. Litter cover of the invasive tree Melaleuca quinquenervia influences seedling emergence and survival. Open Journal of Ecology 2, 131e140. R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https:// www.r-project.org. Accessed 16 July 2018. Ren, Y.D., Shang, Z.H., Long, R.J., 2014. Progress of allelopathy in grassland ecosystem of China. Pratacult Science 31, 993e1002. Rice, E.L., 1979. Allelopathy: an update. Botanical Review 45, 15e109. Samedani, B., Juraimi, A.S., Rafii, M.Y., Anuar, A.R., Sheikh, A.S.A., Anwar, M.P., 2013. Allelopathic effects of litter Axonopus compressus against two weedy species and its persistence in soil. Science World Journal, 2013:695404. Semmartin, M., Aguiar, M.R., Distel, R.A., Moretto, A.S., Ghersa, C.M., 2004. Litter quality and nutrient cycling affected by grazing-induced species replacements along a precipitation gradient. Oikos 107, 148e160. Shen, Y., Chen, W.Q., Yang, G.W., Yang, X., Liu, N., Sun, X., Chen, J.S., Zhang, Y.J., 2016. Can litter addition mediate plant productivity responses to increased precipitation and nitrogen deposition in a typical steppe? Ecological Research 31 (4), 579e587. Shi, X.M., Li, X.G., Wu, R.M., Yang, Y.H., Long, R.J., 2011. Changes in soil biochemical properties associated with Ligularia virgaurea spreading in grazed alpine meadows. Plant Soil 347, 65e78. Smith, B., Wilson, J.B., 1996. A consumer's guide to evenness indices. Oikos 76, 70e82. Tian, M., Hou, F.J., 2009. Responses of Lespedeza davurica seedling growth to residue aqueous extract of three forages. Pratacult Science 26, 45e49. Tredennick, A.T., Adler, P.B., Adler, F.R., Vasseur, D., 2017. The relationship between species richness and ecosystem variability is shaped by the mechanism of coexistence. Ecology Letters 20, 958e968. Vellend, M., Lechowicz, M.J., Waterway, M.J., 2000. Germination and establishment of forest sedges (Carex, Cyperaceae): tests for home-site advantage and effects of leaf litter. American Journal of Botany 87, 1517e1525. Wang, Q.Q., 2011. Effects of litter on seedling establishment of herb species in Leymus Chinensis grassland. Hebei University, Baoding, China, p. 43. Wang, C.T., Long, R.J., Wang, Q.L., Liu, W., Jing, Z.C., Zhang, L., 2010. Fertilization and litter effects on the functional group biomass, species diversity of plants, microbial biomass, and enzyme activity of two alpine meadow communities. Plant Soil 331, 377e389. Wen, L., Dong, S.K., Li, Y.Y., Sherman, R., Shi, J.J., Liu, D.M., 2013. The effects of biotic and abiotic factors on the spatial heterogeneity of alpine grassland vegetation at a small scale on the Qinghai-Tibet Plateau (QTP), China. Environment Monit Assess 185, 8051e8064. Xiao, C.W., Janssens, I.A., Zhou, Y., Su, J.Q., Liang, Y., Guenet, B., 2015. Strong stoichiometric resilience after litter manipulation experiments; a case study in a Chinese grassland. Biogeosciences 11, 757e767. Xie, T.P., Zhang, G.F., Zhao, Z.G., Du, G.Z., He, G.Y., 2014. Intraspecific competition and light effect on reproduction of Ligularia virgaurea an invasive native alpine grassland clonal herb. Ecology & Evolution 4, 827e835. Xiong, S.J., Nilsson, C., 1999. The effects of plant litter on vegetation: a meta-analysis. Journal of Ecology 87, 984e994. Yahdjian, L., Tognetti, P.M., Chaneton, E.J., 2017. Plant functional composition affects soil processes in novel successional grasslands. Functional Ecology 31, 1813e1823. Yu, L.N., 2012. Allelopathy effect of composite pant litters on Stipa seeds in loess region. Northwest Agriculture and Forestry University, Yangling, China, p. 65. Yuan, H., 2009. Responses of plant population and community to residue aqueous extract to main species of eastern Gansu province. Lanzhou University, Lanzhou, China, p. 83. Yuan, J.L., Liang, D.F., Zhang, S.T., 2015. Litter and its interaction with standing vegetation affect seedling recruitment in Tibetan alpine grasslands. Plant Ecology Diversity 9, 89e95. Zhang, L., Zhang, Y.J., Zou, J.W., Siemann, E., 2014. Decomposition of Phragmites australis litter retarded by invasive Solidago canadensis in mixtures: an antagonistic non-additive effect. Science Report 4, 5488. Zhang, R., Hu, X.W., Baskin, J.M., Baskin, C.C., Wang, Y.R., 2017. Effects of litter on seedling emergence and seed persistence of three common species on the Loess Plateau in Northwestern China. Front Plant Science 8, 103. Zhang, Y.J., Tang, S.M., Liu, K.S., Li, X.F., Huang, D., Wang, K., 2015. The allelopathic effect of Potentilla acaulis, on the changes of plant community in grassland, northern China. Ecol Res 30, 41e47. Zhao, Z.G., Du, G.Z., Zhou, X.H., Wang, M.T., Ren, Q.J., 2006. Variations with altitude in reproductive traits and resource allocation of three Tibetan species of Ranunculaceae. Australian Journal of Botany 54, 691e700. Zhou, H.K., Zhao, X.Q., Wen, J., Chen, Z., Yao, B.Q., Yang, Y.W., Xu, W.X., Duan, J.C., 2012. The characteristics of soil and vegetation of degenerated alpine steppe in the Yellow River source region. Acta Pratacult Sinitra 21, 1e11.