CC BY
93Russian Journal of Nematology, 2017, 25 (1), 37 - 50
The impact of herbivore grazing intensity on soil nematode communities and microbial biomass on
the Tibetan Plateau
Hu Jing1, 2 and Wail M. Hassan3
'College of Forestry and Life Science, Chongqing University of Arts and Sciences, 402160, Chongqing, China 2School of Life Science, Lanzhou University, Lanzhou, 730000, China 3Department of Biomedical Sciences, University of Wisconsin, 53211, Milwaukee, WI, USA
e-mail: [email protected]
Accepted for publication 9 June 2017
Summary. This study focuses on the efficacy of herbivore grazing intensity in preserving soil nematode biodiversity and microbial biomass in the alpine grasslands of the Tibetan Plateau. Grazing intensities of lightly (LG), medially (MG) and heavily grazed (HG) treatments were compared in terms of their influence on microbial biomass carbon (MBC) and nitrogen (MBN) and nematode diversity in May, July and September, 2014. We show that MG was associated with the highest MBC, MBN, and nematode diversity indices in July. We also show that grazing had different effects on various nematode trophic groups. HG decreased the density of bacterivores of coloniser-persister 3 (Ba3) guild and predators of coloniser-persister 4 guild (Pr4), but increased the plant feeders of coloniser-persister 2 (Pf2) guild over all sampling times. The overall densities of predators and omnivores were low in HG resulting in a low free-living nematode maturity index (MI) and the structure index (SI) across all sampling times. The higher density of bacterivores led to the higher value of the nematode channel ratio (NCR) in LG in May and September. The value of the enrichment index (EI) was highest on MG across all the sampling times. The research suggested that medially grazed intensity is conducive to biodiversity of soil fauna and belowground biomass in the middle plant growth period.
Key words: grazed intensities, microbial biomass C and N, medially grazed treatment.
The Tibetan Plateau is mainly composed of grassland ecosystems. Grasslands support diverse species of plants and animals and regulate the storage of carbon and nitrogen (Genxu et al., 2002; Guo et al., 2003; Yang et al., 2008; Liu et al., 2012; Yang et al., 2013). However, their ability to regenerate has often been overestimated. Grassland degradation on the Tibetan Plateau due to overgrazing has become a serious issue (Cai et al., 2015). To protect grassland biodiversity and its associated ecosystem functions, it is necessary to implement major reversion strategies for severely degraded land, followed by adequate and sustainable grazing intensity. Previous studies have addressed the effects of grazing on plant communities (Wu et al., 2009) and soil respiration (Cui et al., 2014) in the Tibetan Plateau. However, how herbivore grazing intensity impact soil biodiversity and food web quality in this area remains poorly understood (Yang et al., 2013; Hu et al., 2015).
Many studies that focused on the effects of grazing on soil nematode were carried out on different ecological systems. For example, in subtropical pastures, the effects of grazing have been found to differ among nematode genera. Grazing could decrease coloniser bacterivores and some herbivores such as Criconematidae and increase persistent bacterivores such as Euteratocephalus and Prismatolaimus. At the same time, grazing also resulted in a more structured nematode community (Wang et al., 2006). Grazing might show little or no effect on nematode community parameters, but total abundance was higher on ungrazed semi-natural steppe grassland (Zolda, 2006). In a semiarid steppe, abundance of soil nematodes increased with increasing grazing intensity (Qi et al., 2011). The variable results obtained on different grassland types make it difficult to predict the impacts of grazing on soil nematode communities in alpine grasslands, thus
underscoring the urgent need for more research in this area.
Ungrazed management on Tibetan Plateau grassland has been reported to improve forage production (Wang et al., 2012). However, the long-term lack of livestock grazing will likely depress the abundance or activity of soil biota (Bardgett et al., 2001) and reduce microbial biomass carbon (MBC) and nitrogen (MBN) (Wang et al., 2006). Livestock grazing improves seed density (Ma et al., 2013); plant nitrogen uptake and nitrogen mineralisation rates (Bagchi & Ritchie, 2010). By contrast, continuous intensive grazing may decrease above-and below-ground biomass, lead to deterioration of soil structure and fertility, and alter soil and sediment biodiversity (Bagchi & Ritchie, 2010; Bardgett & Wardle, 2010). This lead ecologists and farmers to postulate that moderate grazing intensity might be the best way to recover soil physical and chemical properties, plant production, and soil biological processes (Wang et al., 2006; Yang et al., 2013). This study is designed to test this hypothesis.
Investigations in the alpine grasslands of the Tibetan Plateau were performed: i) to evaluate the response of soil microbial biomass and soil nematode communities to different grazing intensity; ii) to examine the different effect of grazing on groups of nematodes and whether these effects could be linked to changes in soil organic matter and microbial biomass, and iii) to evaluate the efficacy of different grazing management strategies in the area.
MATERIALS AND METHODS
Experimental site. The study was carried out at the Alpine Meadow and Wetland Ecosystem Research Station of Lanzhou University, located on Maqu, Gansu, China on the eastern Tibetan Plateau (N 35°58', E 101°53', 3500 m. a.s.l.). The local climate is characterised by strong solar radiation with short, cool summers and long, cold winters. The area has more than 270 frost days and 2580 h of sunshine per year. The mean annual temperature and precipitation are 1.2°C (range from 11.7°C in July to -10°C in January) and 620 mm per year (over the last 35 years), respectively. The soil type is alpine meadow soil, and parent materials are from a variety of sources including glacial, alluvial, residual, and residual slope deposits. The plant community is mainly Tibetan alpine meadow type and is dominated by sedges, grasses and other forbs species.
Three replicate blocks were arranged in our study site. Each block was separated by 1000 m
distance to avoid edge effects. In each block, three plots with different grazing intensities and times were investigated: (1) light grazing treatment (LG), (2) medium grazing treatment (MG) and (3) heavy grazing treatment (HG) (see below for definition) (Fig. 1). In 1999, three plots were fenced out at the centre of each block (the first rectangular fence, 600 m x 400 m; the second rectangular fence, 450 m * 250 m; the third rectangular fence, 200 m * 100 m) that had a uniform vegetation cover, plant species composition and soil properties. Our interviews with local people revealed that this alpine meadow has been managed by the same herders with similar grazing intensity for at least 15 years. The lightly grazed treatment covered 2 ha and was grazed by approximately 2 yaks only during winter from 1999 to 2014. The effects of livestock only removed the dead biomass, and the live biomass was not affected. The plant community was dominated by graminoids, and its height and biomass was obviously higher than medially disturbed and seriously disturbed plots. The medially grazed treatment covered 9 ha with no grazing from April to October and approximately 10 yaks grazed during the hay-stage from 1999 to 2014. The disturbance intensity on this plot was higher than low disturbed plot and less than that on seriously disturbed plot. The heavily grazed treatment covered 13 ha. It was exposed to long-term continuous overgrazing and trampling throughout the year by approximately 20 yaks from 1999. Plant biomass was lowest on this plot, and vegetation was seriously degraded. In some patches there were holes dug by Tibetan Pika (Ochotona curzoniae) and marmot (Marmota himalayana). For further details, see Hu et al. (2015).
Six samples were collected from each of the rectangular plots, four along each of the long sides and two along the short sides (Fig. 1). Overall, eighteen samples were collected from each plot per sampling event. A total of 162 composite soil samples were collected at the end of the experiment. Random sampling in a large area showing homogeneous topography and soil texture was expected to reflect accurately the changes in soil biota induced by different grazing intensities. Soil samples were collected in May (early growth period (EP)), July (intermediate growth period (IP)), and September (late growth period (LP)), 2014. Changes induced by grazing in the Tibetan alpine meadow soil ecosystem occur mainly in the top 15 cm soil depth (Sun et al., 2011; Shi et al., 2013); hence, soil samples were taken within this depth. Each soil sample was divided into three parts to be used for soil characteristics analyses, soil microbial carbon
and nitrogen biomass analyses, and nematode community analyses. Soil samples were placed in a plastic bag and stored at 4°C for 1 day before soil analysis.
Soil characteristics, carbon and nitrogen
analysis. To determine soil moisture, 10 g from each soil sample was dried at 105°C to constant weight. Soil extractable organic carbon was estimated by equilibrating 20.0 g moist soil with a 50 ml of 0.5 M K2SO4 solution (Hu et al., 1997). The concentration of carbon in the solution was measured using the Total Organic Carbon Analyzer (TOC-5000A, Shimadzu Corporation, Kyoto, Japan). To estimate extractable nitrogen in soil, 20.0 g moist soil was shaken with 100 ml of 1 N KCl solution (Hart et al., 1994). The concentration of total nitrogen in the extract was measured using a San++ Continuous Flow Analyzer (Skalar, Breda, The Netherlands).
MBC and MBN were measured in field moist soil using a chloroform fumigation incubation method (Vance et al., 1987; Ross, 1992). Moist soil
(20.0 g) was fumigated with ethanol-free chloroform for 48 h. Both fumigated and non-fumigated soils were extracted with 50 ml of 0.5 M K2SO4 by shaking for 30 min on an end-to-end shaker. Organic carbon (Corg) in the extract was determined by TOC analyser. MBC was calculated as follows: MBC = (Corg in fumigated soil - Corg in non-fumigated soil) / kec, where kec is a factor used to convert extracted Corg to MBC. In the current study, we used kec = 0.33 as previously described (Sparling & West, 1988). The MBN was calculated using the equation: MBN = (total nitrogen in fumigated soil -total nitrogen in non-fumigated soil) / ken, where ken is the factor used to convert the extracted organic nitrogen to MBN and is equal to 0.45 (Jenkinson, 1988).
Nematodes extraction and identification. 50
ml portions were removed from one of the divided three parts. Soils were hand-mixed to make sure the sample for nematode extraction was thoroughly mixed. Nematodes were extracted for 48 h using the modified Baermann wet funnel. All nematodes were
Table 1. Changes in soil moisture, microbial biomass N and C, soil total nitrogen (N) and organic carbon (C) among different grazing intensities at each sampling time, expressed as mean ± S.E.
Items Sampling Grazing intensities Effects
time Lightly grazed treatment Medially grazed treatment Heavily grazed treatment Intensity Time
May 166±11a 162 ± 39a 75 ± 7b * *
SM (%) July 157±14a 131±25a 75 ± 2b
September 185±15a 176 ± 29a 98 ± 15b
May 405.22 ± 19.16a 438.99 ± 15.51a 278.90 ± 17.36b * ns
MBN (mg Kg-1) July 322.41 ± 13.15b 368.62 ± 9.31a 255.21 ± 5.32c
September 399.87 ± 9.30a 428.14 ± 15.08a 248.37 ± 12.37b
May 2539.48 ± 83.51a 2715.61 ± 183.3a 1964.24 ± 38.51b * ns
MBC (mg Kg-1) July 2329.80 ± 57.73a 2666.73 ± 71.22a 2044.10 ± 52.19b
September 2331.02 ± 36.61b 2543.37 ± 73.18a 2116.88 ± 31.56c
May 9.77 ± 0.68ns 8.77 ± 1.64ns 6.49 ± 0.90ns * *
TN (g kg-1) July 11.89 ± 0.95a 9.89 ± 0.88a 7.07 ± 0.27b
September 12.34 ± 0.53a 12.17 ± 1.33a 8.79 ± 0.84b
May 157.63 ± 13.22a 149.7 ± 27.64a 87.49 ± 8.39b * ns
OC (g kg-1) July 157.08 ± 12.08a 136.98 ± 20.05a 88.64 ± 4.81b
September 165.22 ± 8.26a 143.56 ± 22.38a 90.65 ± 17.54b
Abbreviations: SM - soil moisture; MBC - microbial biomass carbon; MBN - microbial biomass nitrogen; TN -soil total N; OC - organic C. Letters after each value indicate results of pairwise comparisons. Different lowercase letters (a, b, c) indicate significant differences between grazing intensities for each sampling time as ranked by least square means (P < 0.05); ns = non-significant (P > 0.05).
Results of repeated measures ANOVA for the effects of grazing intensity and sampling time on soil moisture, microbial C and N biomass, and soil nitrogen (N) and carbon (C). Significant levels: * P < 0.05.
Table 2. Proportional genus contribution (%) to the nematode community under different grazing intensities averaged
over all sampling times.
Genus Guild" Lightly grazed treatment Medially grazed treatment Heavily grazed treatment
Tylenchus Pf2 3.6 ± 0.4b 6.8 ± 0.9b 15.6 ± 1.8a
Helicotylenchus Pf3 1.8 ± 0.8ns 3.9 ± 1.0ns 4.8 ± 0.6ns
Hirschmanniella Pf3 3.1 ± 0.6a 0.1 ± 0.0b 0.1 ± 0.0b
Rotylenchus Pf3 0.1 ± 0.1b 0.2 ± 0.1b 0.8 ± 0.3a
Tylenchorhynchus Pf3 3.8 ± 0.6a 0.7 ± 0.0b 3.1 ± 1.0a
Axonchium Pf5 0.7 ± 0.1a 0.0 ± 0.0b 0.0 ± 0.0b
Aphelenchoides Fu2 0.7 ± 0.3b 2.5 ± 0.8a 3.3 ± 0.8a
Aphelenchus Fu2 0.2 ± 0.0ns 0.5 ± 0.2ns 0.7 ± 0.1ns
Ditylenchus Fu2 0.8 ± 0.3ns 1.2 ± 0.5ns 1.1 ± 0.3ns
Filenchus Fu2 3.0 ± 0.4ns 4.5 ± 0.6ns 4.7 ± 0.9ns
Dorylaimoides Fu4 1.0 ± 0.2b 1.8 ± 0.6b 3.2 ± 0.5a
Leptonchus Fu4 0.3 ± 0.0b 0.9 ± 0.1a 0.7 ± 0.3a
Caenorhabditis Ba1 0.0 ± 0.0ns 0.2 ± 0.1ns 0.1 ± 0.0ns
Diploscapter Ba1 0.1 ± 0.0ns 0.0 ± 0.0ns 0.0 ± 0.0ns
Mesorhabditis Ba1 0.4 ± 0.1b 1.3 ± 0.3a 0.2 ± 0.1b
Protorhabditis Ba1 1.7 ± 0.2ns 2.5 ± 0.9ns 2.2 ± 0.9ns
Acrobeles Ba2 0.0 ± 0.0ns 0.3 ± 0.1ns 0.0 ± 0.0ns
Acrobeloides Ba2 0.3 ± 0.0c 4.3 ± 0.8b 11.6 ± 1.0a
Anaplectus Ba2 6.8 ± 1.6ns 4.4 ± 1.1ns 2.1 ± 1.3ns
Cephalobus Ba2 1.1 ± 0.6b 4.7 ± 0.6a 6.4 ± 0.5a
Chiloplacus Ba2 0.1 ± 0.0ns 0.2 ± 0.1ns 0.3 ± 0.0ns
Chiloplectus Ba2 0.2 ± 0.0ns 0.0 ± 0.0ns 0.3 ± 0.1ns
Monhystera Ba2 6.8 ± 1.9a 1.2 ± 0.5b 1.1 ± 0.3b
Plectus Ba2 6.3 ± 1.0ns 4.2 ± 1.3ns 3.1 ± 0.9ns
Tylocephalus Ba2 0.4 ± 0.2ns 1.1 ± 0.3ns 1.6 ± 0.9ns
Bastiania Ba3 0.1 ± 0.0ns 0.1 ± 0.1ns 0.4 ± 0.2ns
Cylindrolaimus Ba3 2.6 ± 0.8a 0.2 ± 0.1b 1.2 ± 0.9a
Prismatolaimus Ba3 13.3 ± 0.9a 6.6 ± 0.8b 4.3 ± 0.3b
Rhabdolaimus Ba3 1.3 ± 0.5a 0.4 ± 0.1b 0.5 ± 0.1b
Teratocephalus Ba3 8.1 ± 0.6a 7.3 ± 0.9a 4.2 ± 0.5b
Alaimus Ba4 0.6 ± 0.0b 2.5 ± 0.3a 1.0 ± 0.2b
Tripyla Pr3 0.3 ± 0.1ns 0.0 ± 0.0ns 0.0 ± 0.0ns
Coomansus Pr4 1.4 ± 0.5a 0.6 ± 0.3a 0.0 ± 0.0b
Iotonchus Pr4 0.5 ± 0.1ns 0.4 ± 0.2ns 0.6 ± 0.1ns
Nygolaimus Pr5 0.3 ± 0.1a 0.0 ± 0.0b 0.4 ± 0.2a
Allodorylaimus Om4 2.0 ± 0.3b 3.7 ± 0.9a 4.4 ± 0.8a
Enchodelus Om4 16.1 ± 0.7a 10.0 ± 0.9b 6.1 ± 0.3c
Epidorylaimus Om4 3.2 ± 0.9ns 3.8 ± 1.3ns 2.7 ± 1.0ns
Labronema Om4 0.3 ± 0.1b 1.3 ± 0.2a 1.3 ± 0.1a
Mesodorylaimus Om4 6.4 ± 0.6b 14.6 ± 0.9a 5.1 ± 0.3b
Aporcelaimus Om5 0.0 ± 0.0b 0.5 ± 0.3a 0.0 ± 0.0b
Abbreviations: a - functional guilds of soil nematodes characterised by feeding habits and life history characters. Pf - plant feeders; Fu - fungivores; Ba - bacterivores; Pr - predators; Om - omnivores; numbers following the functional groups indicate the cp values (Bongers & Bongers, 1998; Ferris et al., 2001).
Different lowercase letters (a, b, c) indicate significant differences between grazing intensities as ranked by least square means (P < 0.05); ns indicates non-significant (P > 0.05).
identified in samples containing 150 or fewer individuals per sample, while in samples containing larger numbers, the first 150 individuals encountered were identified. Identification was done to the genus level.
In addition, nematodes were classified into five trophic groups using a method modified from that described by Yeates et al. (1993). The trophic groups were plant feeders (Pf), fungivores (Fu), bacterivores (Ba), predators (Pr), and omnivores (Om) (Yeates et al., 1993). Moreover, nematodes were allocated to coloniser-persister (cp) classes following the methods described by Bongers (1990). PfX, FuX, BaX, PrX and OmX represent the functional guilds of nematodes, where the guilds have the character indicated by X on the cp-scale (15) according to their r- and ^-characteristics (Ferris et al., 2001).
Data analyses. The species richness (S), Shannon-Wiener index (H'), Simpson index for dominance (2) and Pielou species evenness index (J) were used as measures of the diversity of nematode communities. Species richness: S = the number of nematode genera; Shannon-Wiener index: H' = -£pi lnp; Simpson index for dominance: 2 = Yp2u Pielou species evenness index: J = H' / ln S. Whichpi is the proportion of individuals in the ith taxon.
The free-living nematode maturity index (MI) was used to reflect soil condition, and was calculated according to the method described by Bongers (1990). The enrichment index (EI) and structure index (SI) were calculated to assess food web response to availability of resources and to indicate whether the soil community is basal (typical for example of disturbed systems) or structured (typical of more stable systems). EI and SI were calculated according to the method developed by Ferris et al. (2001). The nematode channel ratio (NCR) can be a powerful tool in assessing the soil decomposition processes and analysing the nematode communities. NCR is constrained to have values between 1 (totally bacterial-mediated) and 0 (totally fungal-mediated). NCR was calculated following the method developed by Yeates (2003).
The effects of grazing disturbance intensities were analysed by ANOVA. Pairwise comparisons among sampling treatments were made based on least square means. Analyses across sampling times were performed using repeated measures ANOVA for three replicate blocks. Mauchly's sphericity test was used to test for multivariate significance, using sampling time and grazing intensity as effects. Pearson's correlation coefficient was used to test correlation between nematode community structure and soil carbon and nitrogen content, and abiotic factors. Data were ln (x + 1) transformed before analysis to meet the rules of homogeneity of variance and normal distribution. All statistical analyses were performed by SPSS 19.0. Differences were regarded as significant at P < 0.05.
RESULTS
Fig. 1. Schematic diagram of one of the three blocks. On the heavily grazed plots, soil samples were taken between the first rectangular fence and the second rectangular fence. On the medially grazed plots, soil samples were taken between the second rectangular fence and the third rectangular fence. On the lightly grazed plots, soil samples were taken inside the third rectangular fence and 10 m away from the fence.6 points "oooooo" means the replications of soil samples.
Impact of grazing on soil properties and microbial biomass. During the study period, significant grazing intensity and/or sampling time effects were observed in soil moisture, MBC, MBN and soil nitrogen and carbon (Table 1). The soil moisture and organic carbon contents were highest with LG and lowest with HG across all the sampling times. Soil total nitrogen content was also highest with LG and lowest with HG, and the EP was non-
significant. MBC and MBN were highest on MG across all sampling times.
Impact of grazing on nematode communities.
Forty-one genera of nematodes were identified during the course of the study (Table 2). Significant grazing intensity and/or sampling time effects were observed in the numbers of different functional guilds (Table 3), except the Pf3, Ba2 and Pr3 guilds. At the EP and LP, the highest density of nematode communities appeared on LG. Pf2 guild was higher on HG than on LG and MG. Ba3 and Pr4 on LG had the highest abundance. MG had the highest abundance of Om5.
Significant grazing intensity and/or sampling time effects were observed in the diversity of nematode communities and ecological indices (Table 4). H', X, S, and J were significantly higher
on MG at IP (Fig. 2). Lower value of MI was observed on HG across all sampling times (Fig. 3A). At IP and LP, NCR was highest on LG and lowest on HG (Fig. 3B). The value of EI was highest on MG (Fig. 3C), and the value of SI was lowest on HG across all sampling times (Fig. 3D).
Correlations of nematode functional guilds and ecological indices with soil carbon and nitrogen. During the study period, most of the correlations of nematode functional guilds, ecological indices with soil moisture, microbial biomass N and C, and soil N and C were statistically significant. Especially, soil moisture value, MBN and MBC value, and soil contents of organic carbon were positively correlated with the number of Om4 (Table 5).
Fig. 2. Difference in the diversity of nematode communities among different grazing intensities at each sampling time. Error-bars represent the standard error. (a) H', Shannon-Wiener index; (b) 1, Simpson index for dominance; (c) S, Species richness; (d) J, Pielou species evenness index. Different lowercase letters (a, b, c) indicate significant differences between grazing intensities for each sampling time as ranked by least square means (p < 0.05), 'ns' indicates non-significant (p > 0.05) differences. Abbreviations of grazing intensities: L - lightly grazed treatment; M - medially grazed treatment; H - heavily grazed treatment.
Fig. 3. Difference in the ecological indices of nematode communities among different grazing intensities at each sampling time. (a) MI, The free living nematode maturity index; (b) NCR, Nematode channel ratio; (c) EI, Enrichment index; (d) SI, Structure index. Different lowercase letters (a, b, c) indicate significant differences between grazing intensities for each sampling time as ranked by least square means (P < 0.05), 'ns' indicates non-significant (P > 0.05) differences. Abbreviations of grazing intensities: L - lightly grazed treatment; M - medially grazed treatment; H -heavily grazed treatment.
DISCUSSION
Impact of grazing on soil carbon and nitrogen.
Our study results showed that belowground microbial biomass was maximal under intermediate grazing intensity by Yaks in the Tibetan alpine grassland ecosystem. Although we have not measured microbial process rates, these are normally contingent upon microbial biomass. Therefore, our prediction is that nutrients' mineralisation rate, soil respiration and plant nutrients uptake also peaked under intermediate grazing pressure (McNaughton, 1985; Bardgett & Cook, 1998). Our results are consistent with the 'intermediate disturbance hypothesis' that dictates
that ecosystem productivity, especially primary productivity, reaches a maximum at moderate levels of grazing disturbance (Huston, 1979). The consistently strong response of microbial biomass to grazing in this alpine grassland is consistent with observations made in hill pasture. A previous study (Bardgett et al., 2001) reported that an intermediate level of sheep grazing had resulted in maximal soil microbial biomass. Mikola et al. ( 2009) considered that returning dung and urine to mowed plots would be beneficial for soil microbes. Other researchers also found that clipping of grazing-tolerant grass stimulated root exudation of carbon, which was quickly assimilated into the microbial populations in the rhizosphere (Hamilton III & Frank, 2001). It has also been suggested that microbial biomass activity
Table 3. Changes in the density (103 individuals m 3) of nematode functional guilds among different grazing intensities
at each sampling time, expressed as mean ± S.E.
Guild" Sampling time Grazing intensities Effects
Lightly grazed treatment Medially grazed treatment Heavily grazed treatment Intensity Time
Pf2 May July September 10.69 ± 1.19b 1.48 ± 0.23b 3.85 ± 1.14b 9.14 ± 2.35b 4.83 ± 0.60b 5.81 ± 1.58b 17.50 ± 1.96a 11.74 ± 2.06a 9.82 ± 3.74a * *
Pf3 May July September 9.80 ± 2.24ns 13.82 ± 4.62b 7.42 ± 2.31ns 7.47 ± 1.85ns 3.02 ± 0.56a 3.59 ± 0.60ns 6.57 ± 0.81ns 9.04 ± 1.19ab 3.75 ± 0.92ns ns ns
Pf5 May July September 1.82 ± 0.87a 0 ± 0ns 1.61 ± 0.74a 0 ± 0b 0 ± 0ns 0.31 ± 0.30b 0 ± 0b 0 ± 0ns 0.09 ± 0.06b * *
Fu2 May July September 12.10 ± 2.13b 1.16 ± 0.30b 7.31 ± 1.75ns 4.13 ± 1.27a 6.46 ± 1.36a 10.36 ± 1.57ns 3.28 ± 0.53a 4.37 ± 1.16a 14.08 ± 3.43ns ns *
Fu4 May July September 3.99 ± 1.25b 0.66 ± 0.21b 1.11 ± 0.52b 1.23 ± 0.70a 5.62 ± 1.39a 0 ± 0a 1.47 ± 0.64ab 6.49 ± 0.20a 0 ± 0a * *
Ba1 May July September 5.98 ± 1.51ns 1.64 ± 0.69a 1.85 ± 0.78ns 5.88 ± 1.20ns 3.68 ± 0.84b 2.19 ± 0.61ns 2.73 ± 0.68ns 1.00 ± 0.37a 1.65 ± 0.61ns ns *
Ba2 May July September 25.70 ± 3.48ns 17.29 ± 5.66ns 39.90 ± 5.72b 23.84 ± 1.91ns 15.02 ± 2.35ns 17.25 ± 3.24a 24.70 ± 1.91ns 20.14 ± 2.48ns 17.30 ± 4.99a ns ns
Ba3 May July September 63.19 ± 15.44b 17.80 ± 4.89b 26.59 ± 2.92b 10.39 ± 1.28a 5.31 ± 0.76a 21.89 ± 4.62b 20.57 ± 2.20a 1.50 ± 0.77a 7.08 ± 1.90a * ns
Ba4 May July September 3.50 ± 0.93ab 0 ± 0b 0 ± 0ns 4.81 ± 0.59b 2.17 ± 0.8a 0.44 ± 0.29ns 1.45 ± 0.78a 0.81 ± 0.30ab 0.23 ± 0.17ns * *
Pr3 May July September 0.31 ± 0.20ns 0.67 ± 0.50ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns ns ns
Pr4 May July September 2.35 ± 2.13a 2.48 ± 1.08a 2.09 ± 0.71b 0.58 ± 0.23b 0.99 ± 0.25b 0.95 ± 0.49ab 0 ± 0b 0.85 ± 0.32b 0.17 ± 0.17a * ns
Pr5 May July September 1.46 ± 0.79ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0 ± 0ns 0.65 ± 0.32ns 0.36 ± 0.22ns 0 ± 0ns ns *
Om4 May July September 40.93 ± 3.62b 32.13 ±3.17b 27.44 ± 3.25b 48.34 ± 2.94b 32.29 ± 3.07b 13.42 ± 3.08a 25.09 ± 1.36a 9.75 ± 2.15a 13.81 ± 3.11a * ns
Om5 May July September 0 ± 0a 0 ± 0a 0 ± 0a 0.54 ± 0.24b 0.31 ± 0.31b 0.59 ± 0.28b 0 ± 0a 0.18 ± 0.18a 0 ± 0a * ns
TN May July September 181.81 ± 15.15a 89.13 ± 10.07ns 119.17 ± 13.90a 116.35 ± 9.95a 79.71 ± 3.41ns 77.48 ± 14.28ab 103.99 ± 5.93b 66.22 ± 5.56ns 69.22 ± 14.44b * ns
Abbreviations: a = functional guilds of soil nematodes characterised by feeding habits and life history characters. Pf - plant feeders; Fu - fungivores; Ba - bacterivores; Pr - predators; Om - omnivores; numbers following the functional groups indicate the cp values (Bongers & Bongers, 1998; Ferris et al., 2001). TN represents total number of nematode community. Letters after each value indicate results of pairwise comparisons. Different lowercase letters (a, b, c) indicate significant differences between grazing intensities for each sampling time as ranked by least square means (P < 0.05); ns indicates non-significant (P > 0.05) differences. Results of repeated measures ANOVA for the effects of grazing intensity and sampling time on the abundance of nematode functional guilds and total number of nematode community. Significant levels: * P < 0.05.
increases under moderate grazing intensity due to increased root exudation (Holland et al., 1996; Mawdsley & Bardgett, 1997).
Impact of grazing on nematodes communities. Although there was no significant difference between grazing intensities in July of 2014, the total density of nematode communities showed a downward tendency with increased grazing intensity. Wang et al. (2006) found that the density of nematode communities on the ungrazed plot was 615 individuals 100 cm-3 (data is mean of 3 samples). In our research, density on the grazed plot is lower than this ungrazed plot. The decrease of the density of nematode communities was largely due to the decrease of structure bacterivores (Ba3). These results are consistent with other studies (King & Hutchinson, 1983; Mulder et al., 2003). Our results indicated that the change of nematode communities' abundance was different from the change of microbial biomass. Some other studies also found that increases in microbial productivity do not always result in increases in the nematode abundance (Bardgett et al., 1997; Mikola, 1998). According to our results, the absence of consistent effects of grazing on the density of nematode communities with MBC and MBN may be due mainly that the different trophic groups respond differently to grazing intensities. On the LG, the density of nematode communities was higher than previously found in 2013 (Hu et al., 2015). These differences may be due to climate change. Both studies found that nematode abundance is related to the soil moisture.
Nematode trophic groups and life-history strategy provide a basis for using nematode faunal analyses in an integrative assessment of soil food web condition (Bongers, 1990; Ferris et al., 2001). In our study, the density of Pf2 increased with increased grazing intensity. A similar result was obtained by Smolik & Dodd (1983) in a study conducted on short-grass prairies. Our results
supported the notion that large herbivores increase the supply of resources for the more r-selected plant feeding nematodes (Ferris & Bongers, 2006). By contrast, our observation that plant feeders in guild Pf3 and Pf5 tend to be more abundant in lightly grazed areas was inconsistent with the results reported in other studies. One study reported that the abundance of k-selected plant feeders was lower on grazed grasslands (Wang et al., 2006), suggesting that heavy grazing intensity was detrimental to k-selected plant feeding nematodes. Our results are in agreement with the viewpoint that the decreased tendency of k-selected plant feeders induced by intensive grazing could be due to their inability to search for new feeding roots after plants and roots were impacted from grazing (Bongers & Bongers, 1998). Plant species identity and density have profoundly influenced plant feeders nematodes (De Deyn et al., 2004), and plant feeders are possibly more responsive to the host plant than they are to the type of grazing intensity (Veen et al., 2010; Chen et al., 2013). In this study, Ba3 on LG had the highest abundance across all sampling times. Mulder et al. (2003) also found similar results by showing that the increase in grazing intensities decreased the abundance of most bacterivores in Dutch dairy farms with grasslands on sandy soils. It is possible that plant litter assured a stable supply of nutrient and food sources for maintenance of Ba3 in lightly grazed areas (Mikola et al., 2001). In our observation, the proportional contribution of Acrobeloides and Cephalobus, which belonged to Ba2 guilds, showed an upward trend with increased grazing intensity. Similar results have also been found by Mulder et al. (2003), who showed that Chiloplacus numbers increased with the increased grazing intensity. This was probably due to the heavy aboveground herbivore grazing that accumulated large quantities of animal waste, which could have been used as a food resource for these nematodes.
Table 4. Results of repeated measures ANOVA for the effects of grazing intensity, sampling time on the ecological
indices of nematode communities.
Items Term H' X S J MI NCR EI SI
Df 2 2 2 2 2 2 2 2
Intensity F 2.962 2.148 3.010 1.658 6.170 15.499 7.749 16.172
p 0.047 0.151 0.049 0.224 0.012 0.0001 0.005 0.0001
Df 2 2 2 2 2 2 2 2
Time F 1.536 3.816 7.023 9.623 35.991 6.790 2.613 18.521
p 0.223 0.033 0.003 0.001 0.0001 0.004 0.090 0.0001
Abbreviations: H' = Shannon-Wiener index; X = Simpson index for dominance; S = the species richness; J = Pielou species evenness index; MI = free-living nematode maturity index; NCR = nematode channel ratio; EI = Enrichment index; SI = Structure index.
Differences shown in bold were statistically significant (P < 0.05).
Table 5. Correlations of nematode functional guilds, ecological indices with soil moisture, microbial biomass N and C,
soil total nitrogen (N) and organic carbon (C).
Nematode community8 Soil moisture Microbial biomass N Microbial biomass C Soil total N Soil organic C
Total number 0.242* 0.431** 0.312** 0.076 0.252*
Pf2 -0.288** -0.244* -0.138 -0.355** -0.254*
Pf3 -0.023 -0.141 -0.143 -0.018 -0.003
Pf5 0.115 0.201 0.088 0.155 0.184
Fu2 0.057 0.110 0.051 0.131 0.157
Fu4 -0.214 -0.187 0.000 -0.233* -0.193
Ba1 0.026 0.424** 0.298** -0.102 0.054
Ba2 0.147 0.163 0.042 0.096 0.158
Ba3 0.253* 0.392** 0.226 0.160 0.253*
Ba4 0.169 0.386** 0.454** -0.209 0.009
Pr3 0.122 -0.082 -0.064 0.137 0.067
Pr4 0.223 0.188 0.135 0.227* 0.233*
Pr5 0.004 0.045 0.109 -0.183 -0.063
Om4 0.303** 0.533** 0.494** 0.070 0.271**
Om5 -0.009 0.266* 0.254* 0.013 0.026
H' -0.185 0.022 0.154 -0.191 -0.128
X -0.212 -0.033 0.047 -0.184 -0.172
S -0.070 0.160 0.248* -0.135 0.010
J -0.225 -0.124 -0.068 -0.141 -0.211
EI -0.013 0.295** 0.258* -0.034 0.065
SI 0.215 0.412** 0.385** 0.046 0.166
NCR 0.281** 0.341** 0.143 0.146 0.193
MI 0.427** 0.581** 0.483** 0.272** 0.358**
Abbreviations: a - functional guilds of soil nematodes characterised by feeding habits and life-history strategy. Pf -plant feeders; Fu - fungivores; Ba - bacterivores; Pr - predators; Om - omnivores; numbers following the functional groups indicate the cp values (Bongers & Bongers, 1998; Ferris et al., 2001). H' - Shannon-Wiener index; X - Simpson index for dominance; S - Species richness; J - Pielou species evenness index; EI - Enrichment index; SI - Structure index; NCR - nematode channel ratio; MI - the free-living nematode maturity index. Significant levels: ** P < 0.01; * P < 0.05.
The value of EI was highest on MG, which indicated that the medium herbivore grazing could provide a large labile nutrient pool for the soil food web during the plant-growing season by stimulating root and/or microbial growth. Positive correlations were observed between the MBC and MBN and the values of EI. It was expected that EI would increase with increased disturbance intensity (Mills & Adl, 2011). At EP and IP, EI was lower in HG. The possible reason was that the effects of dung and urine were weak because a substantial part of total
nitrogen disappeared as volatilised ammonia (NH3) before reaching the soil (Mikola et al., 2009). Landscape-scale constraints on soil organic matter content and plant production can have a greater effect than grazer on soil fauna (Sankaran & Augustine, 2004); thus, it is possible that organic inputs confounded the influence of grazing on the Tibetan Plateau grassland ecosystems. The lowest density of predators and omnivores in HG caused the lower value of SI across all sampling times, which suggested fewer linkages in the food web
(Ferris et al., 2001). Some other studies also observed that SI is lower under intensive grazing disturbance (Zolda, 2006) and higher under intermediate level of land-use in grassland ecosystems (Mills & Adl, 2011).
The decrease values of MI were mainly due to the significantly decreased Pr4 and Om4 with HG. The increased predators and omnivores, especially Om5, contributed to the increase of MI with MG. Other studies have found that intensive grazing could result in lower MI (Mills & Adl, 2011; Chen et al., 2013). In our study, MI had a significant relationship with soil moisture, MBC and MBN, total nitrogen and organic carbon, which indicated the responsiveness of nematode communities' structure to environmental changes (Yeates & Bongers, 1999).
The higher density of Ba3 in LG led to a higher NCR, which reflected organic matter decomposition that was achieved primarily through the bacterial energy channel under this grassland treatment (Yeates, 2003). NCR was significantly correlated with soil moisture suggesting that drier locations could result in fungal-based channels (Briar et al., 2012). Our results were inconsistent with previous studies that showed a shift in the decomposition pathway from a slow-cycling, fungally-dominated system to a fast-cycling, bacterially-dominated system under heavy herbivore grazing (Briar et al., 2012). Differences in climate and soil conditions may explain these discrepancies between our results and published data.
We found that the densities of Pr4 and Om4 were consistent with their bacterivore prey under our conditions. The lowest density of predators or omnivores in HG caused the lower value of MI and SI across the sampling period, which suggested less structured nematode communities and unstable soil conditions induced by herbivore grazing (Ferris et al., 2001). The significant relationships between Om4 and MBC and MBN further support the theory that these nematode trophic groups accelerate nutrient flow by feeding on bacterivores or fungivores that could have otherwise immobilised nutrients (Yeates & Wardle, 1996).
In our study, the diversity indices of nematode communities were significantly higher on MG in July (P < 0.05), implying that medially grazed intensity strategies may enhance nematode biodiversity. Our results support the hypothesis that an intermediate level of disturbance may result in the highest level of species diversity in the soil (Huston, 1979). The reason for changing nematode community structure is the changes of some specific genera for example, Anaplectus, Monhystera,
Plectus, Cylindrolaimus, Prismatolaimus, Teratocephalus, Tripyla and Mesodorylaimus in heavily grazed treatment. It is known that for these taxa soil humidity is the main ecological factor (Gagarin, 1992). Monhystera is common representative of freshwater bodies. Anaplectus, Cylindrolaimus and Mesodorylaimus are species inhabiting both the coastal zone of water bodies and in moss and wet soil of terrestrial ecosystems. By contrast, the abundance of typical inhabitants of the soil increases Tylenchus, Aphelenchoides and members of the family Cephalobidae (Cephalobus and Acrobeloides).
CONCLUSIONS
The current study demonstrated the importance of examining different grazing intensity strategies and their effects on soil biological communities. Our results are consistent with the 'intermediate disturbance hypothesis' that states that ecosystem productivity, especially primary productivity, reaches a maximum at moderate levels of grazing disturbance. Heavily grazed intensity was likely to induce less structured soil fauna community.
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