Seasonal changes in the relationship between species richness and community biomass in grassland under grazing and exclosure,Horqin Sandy Land,northern China

XiaoAn Zuo ,XueYong Zhao,TongHui Zhang,ShaoKun Wang,YaYong Luo,Xin Zhou

Naiman Desertification Research Station,Cold and Arid Regions Environmental and Engineering Research Institute,Chinese Academy of Sciences,Lanzhou,Gansu 730000,China

1 Introduction

Research on the relationship between species diversity and productivity has emerged as a hot issue in ecology over the last decades (e.g.,Aarssen,1997;Loreauet al.,2001;Hooperet al.,2005;Zuoand Knopset al.,2012).The nature of the relationships between species diversity and productivity,as well as the underlying mechanisms forming these relationships,are still debated due to differences in ecosystems and measurement scales (Tilmanet al.,2001;Kahmenet al.,2005;van Ruijven and Berendse,2005).Graphic depictions of the three primary diversity-productivity relationships are either linear (positive or negative),hump-shaped,or indicate no relationship (Tilmanet al.,2001;Baiet al.,2007;Hectoret al.,2010;Maet al.,2010;Zuoand Knopset al.,2012).Numerous studies have shown that many factors influence the variation observed in relationships between productivity and diversity at different spatial and temporal scales in all kinds of ecosystems,including climate change (De Boecket al.,2007;Laughlin and Moore,2009),disturbance regime (Grosset al.,2009),resource heterogeneity (Baiet al.,2007;Zuoand Knopsetal.,2012),and community competition (Peltzeret al.,1998).

Many studies have suggested that livestock grazing is one of most important drivers affecting changes in the composition and structure of plant communities in grassland ecosystems (Wang,1992;Osemet al.,2002;Zhaoet al.,2005;Socheret al.,2012;Zuo and Wanget al.,2012).It has also been demonstrated that long-term grazing has resulted in obvious declines in species diversity and ecosystem function (Zhenget al.,2010;Baiet al.,2012),but the temporal dynamics under grazing disturbance have rarely been studied in this context.A study by Zuoand Zhaoet al.(2012)showed that species richness and productivity changed simultaneously and that the shape of the correlation curve depends on the vegetation succession stage of dune stabilization.However,the seasonal dynamics of the relationship between species richness and biomass under grazing influence is not clear.Thus,understanding how grazing and time interactions affect species diversity,productivity,and their relationship is very important to provide guidance for sustainable management practices in grassland ecosystems.

The Horqin Sandy Land has become one of the most severely desertified regions in northern China in the last century due to the strong influence of harmful anthropogenic activities such as fuelwood gathering,heavy livestock grazing,and reclamation (Zhaoet al.,2005;Zhaoet al.,2009;Zuo and Zhaoet al.,2012).However,because the annual precipitation in this area is 350-500 mm,some degraded sandy grassland could be gradually and naturally restored after excluding destructive land uses (Suet al.,2006;Zuoet al.,2009).In recent years,many studies on the influence of grazing and exclosure on vegetation and soil in sandy grassland ecosystems have been carried out in this region (Zhanget al.,2005;Suet al.,2006;Liet al.,2011;Zuo and Wanget al.,2012).Nevertheless,there is still limited information on how the relationship between species richness and community biomass responds to grazing and exclosure during the whole plant growth season.Here,two hypotheses are tested:(1) the relationship between species richness and community biomass in grassland under grazing and exclosure varies with seasonal changes;and (2)changes of dominant plants species in grasslands which are determined by grazing and exclosure affect the relationship between species richness and community biomass during the whole plant growth season.

2 Materials and methods

2.1 Site description

This study was undertaken in the Horqin Sandy Land(42°55′N,120°42′E;360 m a.s.l.elevation),Inner Mongolia,northern China.The climate in this area is temperate,semi-arid,continental,and monsoonal,receiving an annual average precipitation of 360 mm,75% of which falls during the growing season of June to September.The annual mean open-pan evaporation is about 1,935 mm.The annual mean temperature is about 6.4 °C,with the minimum monthly mean temperature of-13.1 °C occurring in January and the maximum of 23.7 °C in July.The annual mean wind velocity is in the range of 3.2 to 4.1 m/s,and the prevailing wind direction is northwest in winter and spring.

The pattern of natural vegetation is characterized by a mosaic of grasslands and sand dunes,including lowland grasslands,meadows,fixed dunes,semi-fixed dunes,and mobile dunes (Zuo and Knopset al.,2012).Sand lands are covered with various native plants,including grasses (e.g.,Cleistogenes squarrosa,Setaria viridis,Phragmites australis,Digitaria ciliaris),forbs (e.g.,Mellissitus ruthenicus,Salsola collina,Agriophyllum squarrosum,Artemisia scoparia),subshrubs (e.g.,Lespedeza davurica),and shrubs(e.g.,Artemisia halodendron,Artemisia frigida).

2.2 Experiment design

In April of 2007,we selected a fenced grassland (exclosure) and an adjacent area outside the exclosure for sampling.In the fenced grassland,the Naiman Station of Desertification Research (Chinese Academy of Sciences) had excluded grazing for 11 years to assess the potential for restoring degraded vegetation.Local herdsmen had used the areas outside the exclosure for free,continuous grazing by cattle and sheep since 1980.As a result,the vegetation covers in the exclosure and outside the exclosure were ＞70% and ＜30%,respectively.The same plant species,Artemisia scoparia,Setaria viridis,Cleistogenes squarrosa,andLesredeza davurica,were dominant in both the exclosure and outside the exclosure.

Three typical 30m×30m plots with similar topography(slope 0°-5°),60 m apart,were chosen in each of the two parts of the study site.During the entire plant growing season,10 random 1m×1m quadrats at each sampling plot were established to survey the vegetation characteristics in April,June,and August.In each quadrat the number of plant species,plant density,and plant cover percentage were recorded,and the aboveground biomass was also estimated by the harvest method.The aboveground biomass materials were dried at 60 °C in a hot-air oven for 48 h and weighed in a lab.

2.3 Data analysis

The effects of grazing and seasonal changes (different harvest dates) on vegetation characteristics were examined using two-way analysis of variance (ANOVA) procedures and multiple comparisons.The results of multiple mean comparisons were checked by Tukey’s test (P＜0.01).The descriptive statistical parameters and significance tests were performed with SPSS (version 16.0).

3 Results

3.1 Effects of grazing and seasonal changes on vegetation characteristics in grassland

In sandy grassland,long-term grazing had the most significant effect on vegetation cover,plant density,and biomass(P＜0.01) (Table 1),followed by the effect of seasonal changes (P＜0.01).The interaction of grazing and seasonal changes also had a significant effect on vegetation cover,plant density,and biomass (P＜0.01).

Regarding seasonal changes,the vegetation cover,species number,and biomass in August were higher than those in April (P＜0.01),whereas plant density showed a reverse trend (P＜0.01) (Figure 1).During the whole growing season,vegetation cover in the grazed grassland was less than in the fenced grassland (P＜0.05).Species numbers were similar between the grazing grassland and the fenced grassland(P＞0.05).Biomass in June and August in the fenced grassland was higher than in the grazed grassland (P＜0.05),whereas plant density in April and June in the grazed grassland was higher than in the fenced grassland (P＜0.05) (Figure 1).

Table 1 Results from two-way ANOVA testing of the effects of grazing and harvest date on vegetation cover,species number,density,and biomass

Figure 1 Seasonal changes of vegetation cover,species number,density,and aboveground biomass in the grassland under grazing and exclosure (* or ** indicates statistical significance of P＜0.05 and P＜0.01,respectively)

3.2 Seasonal changes of relationships between vegetation cover,species number,plant density,and biomass undergrazing and exclosure

Correlation analysis showed that the relationship between vegetation cover,species number,plant density,and biomass varied obviously with seasonal changes in the grazed and fenced grasslands (Table 2,Figure 2).As in Figure 2,a positive relationship between vegetation cover and biomass was found in April and June in the grazed grassland,as well as in June and August in the fenced grassland (P＜0.05).A negative relationship between species number and biomass was found in August in the fenced grassland (P＜0.01),whereas no relationship was found in April and June in the fenced grassland and during the whole growing season in the grazed grassland(P＞0.05).In the grazed grassland,the relationship between plant density and biomass changed from positive in April to negative in August (P＜0.01),whereas no relationship was found in June in the grazed grassland and during the whole growing season in the fenced grassland (P＞0.05).

Table 2 Regression analyses of the relationship between vegetation cover,species number,density,and total biomass in the grazed and fenced grasslands

Figure 2 Regression lines and results of regression analyses are presented separately for each harvest date in the grasslands under (a) grazing and (b) exclosure

3.3 Seasonal changes in density of dominant plant species and total biomass under grazing and exclosure

Our regression analysis also showed that the relationship between the density of the dominant plant species and the total biomass varied obviously with seasonal changes in the grazed and fenced grasslands (Table 3).In the grazed grassland,the relationship between the density ofCleistogenes squarrosaand the total biomass changed from positive in April to negative in August (P＜0.01);the relationship between the density ofArtemisia scopariaand the total biomass was negative in August (P＜0.01);the relationship between the density ofSalsola collinaand the total biomass was positive in April and June (P＜0.01);and the relationship between the density ofSetaria viridisand the total biomass was negative in August(P＜0.01).In the fenced grassland,the relationship between the density ofLespedeza davuricaand the total biomass was positive in April and August (P＜0.01),and the relationship between the density ofSalsola collinaand the total biomass was positive in August (P＜0.01).

Table 3 The relationship between density of the dominant plant species and the total biomass in grazed and fenced grasslands

4 Discussion

Our analysis of vegetation characteristics in grasslands under grazing and exclosure during a whole growing season demonstrated that they varied significantly with seasonal changes.During the periods of plant germination in April and seedling emergence in June,vegetation cover and biomass in the grazed grasslands increased slowly due to the effects of livestock.As the peak of the growing season approached,increasing precipitation and abundant light favored plant growth and accumulation of photosynthates in grasslands.However,livestock grazing results in compensative plant growth,so the vegetation cover and biomass of the grazed grassland showed an increasing trend from April to August.Nevertheless,the vegetation cover and biomass in June and August were still lower in the grazed grassland than in the fenced grassland.These results suggest that long-term grazing during the growing season has an important negative influence on vegetation characteristics,resulting in a sharp decline of vegetation cover and standing biomass in grassland,which is consistent with the findings of other studies (e.g.,Wang,1992;Liuet al.,2005;Luoet al.,2008;Yanet al.,2012).

In addition,plant density in April was higher than that in August in the grazed grassland,and plant density in April and June in the grazed grassland was also higher than that in the fenced grassland.These results suggest that in order to adapt to long-term grazing,plants in grazed grasslands increase their reproduction ability,which results in an increase of soil seed bank as well as an increase of plant density early in the growth season.A study by Wang and Li (1999) also showed that grazing may favor the branch sprouting of rhizome plants and increase the plant density of bunch grass in grasslands.Some studies also suggest that grazing may directly or indirectly affect the reproduction strategies,energy allocation,community structure,seed density,and aboveground and belowground biomass in grasslands by livestock ingestion,trampling,and excrement (Liuet al.,2005;Zhanget al.,2009;Baiet al.,2012;Yanet al.,2012).

Our study suggests that seasonal changes and land use(exclosure and grazing) have an influence on the relationship between species diversity and ecosystem functions in grasslands.Bischoffet al.(2005) found that during the early succession of vegetation,species richness decreased because of the strong competition among plant species in the peak of the growing season,which results in the relationship between species richness and biomass changing from a positive correlation at the beginning of the growing season to no relationship at the peak of the growing season.That result is not agreement with our finding that the relationship between species richness and biomass changes from no relationship at the beginning of the growing season to a negative correlation at the peak of the growing season.This may be explained by the competition among plant species in the fenced grassland in our study,which caused a very weak increase of species richness and a high increase of biomass at the peak of the growing season.In addition,we found no relationship between species richness and biomass during the whole growing season in the grazed grassland,whereas the relationship between plant density and biomass changed from positive in April to negative in August.These results suggest that long-term grazing significantly affects the vegetation cover,species richness,plant density,and biomass in grasslands (Osemet al.,2002;Zhanget al.,2004;Sunet al.,2006).

A previous study showed that the effects of land use on biomass in grassland are mediated by the variation of species richness (Grosset al.,2009).Our results suggest that land use (exclosure and grazing) also significantly affects relationships between plant density and biomass by mediating changes in the dominant plant species in grasslands.We found that long-term grazing greatly decreased the biomass of palatable grass (Cleistogenes squarrosaandSetaria viridis) and the Compositae family (Artemisia scoparia),resulting in a negative relationship between the density of the dominant plant species and the total biomass from the three dominant species at the peak of the growing season.However,the high density of the dominant plant species,Lespedeza davuricaandSalsola collina,maintained the high biomass in the fenced grassland.Thus,the relationship between density of the dominant plant species and the total biomass in grazed and fenced grasslands varies with seasonal changes,which also supports the ecological theory of"interspecific competitive exclusion" (Bischoffet al.,2005).

5 Conclusions

Our study demonstrated the importance of temporal dynamics and land use in understanding the relationship between species richness and productivity in grassland ecosystems.In our study,relationships between species richness,plant density,density of the dominant plant species,and biomass varied with seasonal changes and land use (exclosure and grazing).Long-term grazing resulted in a decrease of vegetation cover and standing biomass,an increase of plant density in April,no relationship between species richness and biomass during the whole growing season,and seasonal changes in the relationship between density of the dominant plant species and the total biomass.In fenced grassland,species competition resulted in a negative correlation between species richness and biomass.Changes in the dominant plant species and their density which were determined by temporal dynamics and land use,influenced the relationships between species richness,plant density,and biomass.Therefore,developing proper strategies of grazing management is very necessary to maintain the function,stability,and sustainability of grassland ecosystems.

The authors thank all the members of the Naiman Desertification Research Station,Chinese Academy of Sciences(CAS),for their help in field work.We also wish to thank the reviewers for their valuable comments and language revisions.This paper was financially supported by the Knowledge Innovation Program of the Chinese Academy of Sciences (No.KZCX2-EW-QN313),the National Natural Science Foundation of China (No.41171414,41071185),the Key Project of Scientific and Technical Supporting Programs (No.2011BAC07B02-09),and the West Light Foundation of the Chinese Academy of Sciences (No.O928711001).

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