Effects of tillage and residue management on soil nematode communities in North China

Ecological Indicators 13 (2012) 75–81

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Effects of tillage and residue management on soil nematode communities in North China Xiaoke Zhang a,1 , Qi Li a,1 , Anning Zhu b , Wenju Liang a,∗ , Jiabao Zhang b , Yosef Steinberger c a

State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110164, China State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China c The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel b

a r t i c l e

i n f o

Article history: Received 10 March 2011 Received in revised form 7 May 2011 Accepted 8 May 2011 Keywords: Bioindication Descriptive indicator Evaluative indicator Soil nematodes Tillage Residue management

a b s t r a c t Soil nematode abundance, community composition and biomass were determined in the Fengqiu State Key Agro-Ecological Experimental Station, North China, in order to evaluate the effects of tillage system (conventional tillage and no-tillage) and residue management (0, 50% and 100% wheat residue incorporation/coverage) on the nematode communities. Two kinds of indicators (descriptive and evaluative) were categorized. Of the descriptive indicators, residue management had a significant effect on the total nematode abundance, biomass and trophic groups except for bacterivores. Of the evaluative indicators, Shannon diversity (H ), generic richness (GR), nematode channel ratio (NCR) and enrichment index (EI) significantly increased with increasing residue quantity, whereas dominance (), basal index (BI) and channel index (CI) exhibited an opposite trend. Significant tillage effects were observed on the trophic diversity (TD), EI, CI and carbon production (P). The responses of nematodes to tillage and residue were genus-dependent. Canonical correspondence analysis indicated that tillage explained 4.9% and 15.4%, and residue management explained 5.2% and 13.1% of the variations in soil nematode abundance and biomass, respectively. Different metabolic footprint characteristics of the food web were demonstrated graphically by enrichment and structure footprints. The evaluative indicators, such as EI and CI, were sensitive to both tillage and residue management. The descriptive indicators could be used to obtain an intuitive answer to the effect of residue management and the evaluative indicators were more comprehensive for interpreting the structure and function of the soil food web under different tillage and residue management regimes. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction In agroecosystems, tillage and residue management as main agricultural practices (Minoshima et al., 2007) could affect the surface residue accumulation, leading to changes in soil physiochemical properties, microbial activity and biomass, and further resulting in profound changes in the composition and function of soil biota (Ferris et al., 2004; Liebig et al., 2004). There were many soil properties to changes in management practices, some of which were highly sensitive, whereas others were more subtle (Bezdicek et al., 1996; Mendoza et al., 2008). The chemical or physical measures might therefore be not enough for detecting potential changes in an ecosystem (Suter II, 2001). Practical assessment of soil quality

∗ Corresponding author at: Institute of Applied Ecology, Chinese Academy of Sciences, P.O. Box 417, Shenyang 110016, China. Tel.: +86 24 83970359; fax: +86 24 83970300. E-mail address: [email protected] (W. Liang). 1 These authors contributed equally. 1470-160X/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecolind.2011.05.009

requires considering biological factors. More researchers have realized the need to measure environmental conditions using biological rather than physicochemical indicators (Goodsell et al., 2009). According to the definition of bioindicators, two kinds of indicators (descriptive and evaluative) can be categorized (Heink and Kowarik, 2010). Descriptive indicators were used to reflect attributes of the indicators and describe the state or analyze changes in agroecosystems (McGeoch, 1998; Walz, 2000). Evaluative indicators served mainly for evaluating ecosystem function and diagnosing the cause of an environmental problem (Dale and Beyeler, 2001). Soil nematode communities have been widely used as bioindicators of ecosystem conditions (Yeates, 2003; Ritz et al., 2009; Sánchez-Moreno et al., 2010), due to their key positions in soil food webs (Neher, 2001). The utilization of nematode community analysis for indicating soil food web dynamics in agroecosystems has been reported by many researches (Wardle et al., 1995; Ferris and Matute, 2003; Briar et al., 2007; SánchezMoreno et al., 2008; DuPont et al., 2009). As descriptive indicators, nematode abundance, body length and biomass are relatively easy to determine and their increase or decrease are usually directly

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X. Zhang et al. / Ecological Indicators 13 (2012) 75–81

Table 1 Total abundance and biomass of soil nematodes and abundance of trophic groups (mean ± SE) in the different tillage and residue treatments. Tillage

Residue

Total abundancea

Total biomassb

BFa

FFa

PPa

OPa

NT

0 50 100

2441.39 ± 264.03 2384.80 ± 144.34 2984.61 ± 350.51

66.65 ± 32.00 55.15 ± 19.24 116.50 ± 37.77

279.47 ± 27.99 341.28 ± 45.27 378.32 ± 58.82

240.72 ± 50.55 197.98 ± 31.23 252.00 ± 56.43

1773.38 ± 214.70 1682.11 ± 96.27 2083.17 ± 288.11

147.83 ± 18.85 163.44 ± 53.43 271.12 ± 104.11

CT

0 50 100

2450.86 ± 262.19 2476.88 ± 466.71 3431.26 ± 320.25

39.38 ± 21.41 64.87 ± 28.47 90.86 ± 22.82

369.76 ± 55.21 466.29 ± 105.34 478.09 ± 67.76

428.66 ± 87.52 170.13 ± 55.31 253.45 ± 55.71

1541.67 ± 134.90 1628.22 ± 308.19 2381.66 ± 260.24

110.78 ± 32.74 212.24 ± 43.84 318.07 ± 74.96

ns <0.05 ns

ns <0.01 ns

ns ns ns

ns <0.05 ns

ns <0.05 ns

ns <0.05 ns

Tillage Residue Tillage × Residue a b

Individuals per 100 g dry soil. ␮g per 100 g dry soil.

affected by tillage and cover crops (Fiscus and Neher, 2002; Ferris, 2010; Mills and Adl, 2011). Wardle (1995) summarized that there were different responses (stimulation or inhibition) of total nematode abundance to tillage in different studies and larger organisms were likely to be reduced by tillage. DuPont et al. (2009) found that plant parasites were increased and omnivores-predators did not vary significantly in cover crop treatments. Significant increase in the body length of nematode families such as Dorylaimidae, Monhysteridae and Cephalobidae were observed in an intensive management system (Mills and Adl, 2011). As evaluative indicators, some nematode ecological indices have been proven to be useful tools for evaluating soil conditions. Lenz and Eisenbeis (2000) found that nematode trophic diversity (TD) did not indicate the tillage disturbance, but the maturity index (MI) was suitable for indicating immediate tillage effects on the nematode community. Cover-cropped soils had a high enrichment index (EI) and low channel (CI) and basal (BI) indices, suggesting a bacterial-dominated food web under nutrient enrichment conditions (DuPont et al., 2009). Ferris et al. (2001) confirmed a more structured food web in a conventional management system by using nematode community structural indices. Using metabolic footprints, Ferris (2010) monitored the metabolic activity of different nematode guilds in the farming system with crop coverage, and found that the metabolic footprints provided more detailed interpretation on the structure and function of the soil food web. The objectives of our study were to determine the effects of tillage and residue management on the nematode communities and soil food webs, and to evaluate the bioindication validity of different nematode-based indicators to different tillage and residue management regimes. 2. Material and methods 2.1. Study site The experiment was set up in the Fengqiu State Key Agro-Ecological Experimental Station (35◦ 01 N, 114◦ 32 E), Henan province, located in the Huang-Huai-Hai Plain of China in 2007. The 30-year mean annual temperature in the area was 13.9 ◦ C, and the annual precipitation ranged from 355 mm to 800 mm (Ding et al., 2010). The rotation of summer maize (Zea mays L.) and winter wheat (Triticum aestivum L.) was practiced for at least 50 years before the experiment was established. The soil is calcareous (Fluvo-Aquic soil) with 11.13 g/kg organic matter, total nitrogen 1.39 g/kg, pH (H2 O) 8.24 and bulk density 1.16 g/cm2 (Cai and Qin, 2006; Zhu et al., 2009). 2.2. Experimental design and soil sampling The experiment was a split-plot design with six replicates. Tillage system was the main plot factor and residue management

the sub-plot factor. The tillage systems were conventional tillage (CT) and no-tillage (NT). Chopped wheat residues were incorporated into soil in the conventional tillage field and covered the soil surface in the no-tillage field. Three residue treatments were 0 (no wheat residue incorporation/coverage), 50% and 100% (7.5 t/ha) wheat residue incorporation/coverage. Individual plots were 4 m wide and 100 m long for convenient in-field agronomic operation. Thirty-six soil samples were collected from the 0 to 20 cm depth before harvesting wheat on June 10, 2010. Composite samples of 5 random sub-samples per plot were collected with a 2.5 cm diameter auger. The fresh samples were stored at 4 ◦ C until analysis. 2.3. Soil nematode determination Nematodes were extracted from 100 g of fresh soil by a modified cotton–wool filter method (Liang et al., 2009). Nematode abundance was expressed as individuals per 100 g dry soil and at least 100 nematodes from each sample were identified to genus level using an inverted compound microscope, according to Jairajpuri and Ahmad (1992) and Bongers (1994). Following identification, the nematode length (␮m) and maximum body diameter were determined using an ocular micrometer. The nematodes were assigned to the following trophic groups characterized by feeding habits: bacterivores (BF), fungivores (FF), plant parasites (PP) and omnivores-predators (OP) (Steinberger and Loboda, 1991; Yeates et al., 1993). 2.4. Data analysis The ecological indices for soil nematodes were calculated: trophic diversity (TD) for trophic groups (Wieser, 1953), Simpson’s dominance index () (Simpson, 1949), Shannon diversity (H ) (Shannon, 1948) and richness (GR) (Yeates and King, 1997) for genera, maturity index (MI) (Bongers and Ferris, 1999), and nematode channel ratio (NCR) (Yeates and Bongers, 1999). Enrichment (EI), structure (SI), basal (BI) and channel (CI) indices were calculated from weighted faunal components (Ferris et al., 2001). Nematode biomass was calculated by the formula W = (L3 /a2 )/(1.6 × 106 ), where W is the fresh weight (␮g) per individual, L is the nematode length (␮m), and a is the length to maximum body diameter ratio. Carbon respiration coefficient, R = 0.273(W0.75 ); carbon production, P = 0.1Wt /mt , where Wt and mt are the body weight and the cp class of taxon t. The metabolic footprint calculation, F = P + R. The enrichment (efoot) and structure footprint (sfoot) are the metabolic footprint of lower (cp1–2) and higher (cp3–5) trophic levels, respectively (Neher et al., 2004; Ferris, 2010). Canonical correspondence analysis (CCA) was performed to explore the nematode community in relation to tillage and residue ˇ management using the CANOCO software (ter Braak and Smilauer,

X. Zhang et al. / Ecological Indicators 13 (2012) 75–81

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Table 2 Nematode genera present in this study. Bacterivores

Abbr.

Fungivores

Abbr.

Plant parasites

Abbr.

Omnivores-predators

Abbr.

Acrobeles Acrobeloides Alaimus Cephalobus Chiloplacus Diploscapter Eucephalobus Mesorhabditis Prismatolaimus

Acro Acroi Alaim Cepha Chilo Diplo Euce Meso Prism

Aphelenchoides Aphelenchus Dorylaimoides Filenchus Paramphidelus Tylencholaimus

Apheoi Aphe Dory Filen Param Tylen

Coslenchus Geocenamus Helicotylenchus Malenchus Pratylenchus Tylenchorhynchus

Cosle Geoc Helico Malen Praty Tyley

Aporcelaimellus Discolaimium Discolaimus Dorydorella Dorylaimellus Epidorylaimus Thonus Thornenema

Apor Discom Discos Doryd Dorym Epi Thon Thorn

2002). Treatments (tillage and residue management) were treated as nominal (0, 1) environmental variables. A Monte Carlo permutation option was employed to determine the significance of first and second axes. Nematode abundances were ln(x + 1) transformed to normalize data prior to statistical analysis. All statistical analyses were performed by the SPSS statistical software (SPSS Inc., Chicago, IL). Nematode data were statistically analyzed using the genera linear model (GLM) procedure for a split-plot design. Differences at p < 0.05 were considered statistically significant. 3. Results 3.1. Nematode abundance and community composition The total nematode abundance was significantly higher in the 100% residue than in the no residue and 50% residue treatments (p < 0.05) for both NT and CT. Plant parasites were the most abundant groups, followed by bacterivores, fungivores and omnivores-predators (Table 1). The abundance of plant parasites and omnivores-predators increased with increasing residue quantity. Residue had significant effect on the abundance of total nematodes and trophic groups (p < 0.05), except for the bacterivores (p > 0.05). Twenty-nine nematode taxa were identified (Table 2). The most abundant genera were Pratylenchus and Tylenchorhynchus (relative abundance > 10%), and Pratylenchus responded obviously to the

residue management. A significant tillage effect was observed on the abundance of 7 genera (p < 0.05), and a residue effect on that of 6 genera (p < 0.05) (Table 3). Only the abundance of Acrobeloides responded significantly to both tillage and residue management. 3.2. Nematode biomass The overall effect of residue on the total biomass was significant (p < 0.05) (Table 1). The total biomass increased significantly in 100% residue compared to other residue treatments in both CT and NT (Table 1). Tillage effect on the biomass of 5 genera, and residue effect on the biomass of 12 genera were significant (p < 0.05) (Table 3). The responses of genus biomass to tillage and residue management were different, but the biomass of Dorylaimellus was responsive to both tillage (p < 0.05) and residue management (p < 0.01). Only Helicotylenchus showed a significant response of the average biomass to the interactions of tillage and residue management (p < 0.01). 3.3. Nematode ecological indices Tillage significantly influenced TD, EI and CI (p < 0.05) (Table 4). TD and EI decreased but CI increased in NT compared to CT (p < 0.05). Residue management affected all ecological indices except for TD and MI (p < 0.05) (Table 4). The values of H and GR increased, but those of  decreased with the increasing residue

Table 3 The statistical analysis on the effect of tillage and residue on abundance and biomass of nematode genera. Tillage

Abundance

Residue

Tillage

Residue

Tillage × Residue

Tillage

Residue

Tillage × Residue

<0.01 <0.05 <0.05 ns

ns <0.05 ns <0.05

ns <0.01 <0.01 ns

<0.01 ns ns ns

ns <0.01 <0.01 <0.01

ns ns ns ns

ns ns <0.01 ns ns

<0.05 <0.05 ns ns ns

ns ns ns ns <0.01

ns ns <0.05 ns ns

ns ns ns <0.01 <0.01

ns ns ns ns ns

<0.01 ns <0.05 ns ns

ns <0.01 ns <0.05 ns

ns <0.01 ns ns ns

ns ns ns ns ns

<0.01 <0.01 ns <0.01 <0.05

ns <0.01 ns ns ns

ns <0.05 ns ns ns ns

ns ns ns ns ns ns

ns ns ns <0.01 ns ns

ns <0.05 <0.05 ns <0.05 ns

<0.01 ns ns ns <0.01 <0.01

ns ns ns ns ns ns

Bacterivores Acrobeles Acrobeloides Eucephalobus Mesorhabditis Fungivores Aphelenchoides Aphelenchus Filenchus Paramphidelus Tylencholaimus Plant parasites Coslenchus Helicotylenchus Malenchus Pratylenchus Tylenchorhynchus Omnivores-predators Aporcelaimellus Discolaimium Discolaimus Dorydorella Dorylaimellus Thornenema

Biomass

Only the genera with significant responses to tillage or residue were listed.

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X. Zhang et al. / Ecological Indicators 13 (2012) 75–81

Table 4 Nematode ecological indices in the different tillage and residue treatments. Indices

NT

CT

0 TD  H MI GR NCR EI SI BI CI P R efoot sfoot

1.82 0.29 1.83 2.83 3.15 0.55 32.84 74.32 22.83 83.07 5.20 11.71 7.62 9.58

50 ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.15 0.06 0.14 0.15 0.33 0.14 12.30 6.48 5.60 26.54 2.55 4.06 6.79 6.44

1.88 0.25 1.97 2.82 3.29 0.63 48.04 78.90 17.31 43.23 6.73 14.72 6.79 6.40

100 ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.23 0.06 0.21 0.31 0.50 0.12 21.55 8.95 7.98 36.20 4.32 10.00 2.08 2.21

1.95 0.20 2.13 2.90 3.74 0.61 44.57 76.36 19.59 49.62 7.01 13.54 9.85 19.90

0 ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.22 0.05 0.17 0.42 0.21 0.09 15.22 13.50 10.61 30.55 3.23 4.93 1.95 8.78

2.16 0.26 1.84 2.58 2.57 0.47 38.36 62.84 30.08 74.63 4.95 8.84 6.14 4.44

50 ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.25 0.02 0.07 0.20 0.45 0.16 10.79 10.05 8.24 30.30 3.49 7.25 3.42 2.87

2.09 0.24 2.02 2.79 3.41 0.77 51.13 78.62 16.82 20.81 11.14 16.20 10.09 10.41

Tillage

Residue

Tillage × Residue

<0.05 ns ns ns ns ns <0.05 ns ns <0.05 <0.05 ns ns ns

ns <0.05 <0.01 ns <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 ns ns <0.05 <0.01

ns ns ns ns ns ns ns <0.05 ns ns ns ns ns ns

100 ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.27 0.05 0.24 0.31 0.56 0.13 17.08 8.90 6.44 14.60 8.39 10.66 3.84 6.08

1.95 0.21 2.09 2.87 3.56 0.65 66.97 84.79 11.48 13.30 11.47 17.21 12.02 25.33

± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.26 0.05 0.18 0.28 0.32 0.14 7.19 4.99 3.57 8.12 2.58 5.50 3.16 13.22

P and R, carbon production and respiration coefficients; efoot, enrichment footprint; sfoot, structure footprint.

NT

100

Enrichment index

quantity in both CT and NT. NCR values were higher in the presence than in the absence of residue (p < 0.05). BI and CI decreased but EI and SI increased significantly after the residue application (50% and 100% residue) (p < 0.01). Significant residue effect on enrichment and structure footprint (efoot and sfoot) was detected (p < 0.05) (Table 4). In NT, the efoot and sfoot were greater in 100% residue coverage than in other residue treatments (p < 0.05). In CT, the efoot and sfoot were lower in the absence of residue compared to 50% and 100% residue incorporation treatments (p < 0.05). Significant tillage effect on carbon production (P) was found, but no residue effect on carbon production (P) and respiration (R). The metabolic footprint characteristics of the food web were found to be different between NT and CT (Fig. 1). Most plots in NT were located in quadrat C, which indicated less disturbed or relatively undisturbed environments, whereas the food web for CT was moderately disturbed since most plots were clustered in quadrat B. The functional footprint is the total area of the enrichment and structure footprints as illustrated in Fig. 1. The total functional footprint of NT in 100% residue was greater than in other residue treatments. In CT, the total functional footprint increased as the residue quantity increased.

NT0 NT50 NT100

50

0 0

4. Discussion 4.1. Bioindication of descriptive indicators to tillage and residue Our study indicated that the total nematode abundance and biomass responded remarkably to the residue effect, but not to the tillage effect (Table 1). Similarly, Lenz and Eisenbeis (2000) and Mendoza et al. (2008) found that the short-term effects of different tillage management on total nematode communities were

B

D

C

50

100

Structure index

CT

100

CT0 CT50 CT100

Enrichment index

3.4. The relationship between abundance and biomass of nematodes and treatments Results from canonical correspondence analysis showed that eigenvalues were 0.069 (F = 3.43, P = 0.002), and 0.058 for the first and second axes (Fig. 2A), respectively, and the first two axes explained 67.1% of the total species-environment variation. In Fig. 2B, eigenvalues were 0.103 (F = 3.42, P = 0.002) and 0.052 for the first and second axes, respectively, and the first two axes explained 64.7% of the variation. Nematode genera between CT and NT were distinguished by the horizontal axis in Fig. 2A and the vertical axis in Fig. 2B. Tillage explained 4.9% and 15.4%, while residue explained 5.2% and 13.1% of the variations in soil nematode abundance and biomass, respectively.

A

50

0

0

50

100

Structure index Fig. 1. Functional metabolic footprint of nematodes subjected to tillage and residue management. The vertical axis of each footprint represents the enrichment footprint and the horizontal axis represents the structure footprint. The x-axis coordinates of the metabolic footprint are calculated as SI − 0.5Fs and SI + 0.5Fs , and the y-axis coordinates as EI − 0.5Fe and EI + 0.5Fe . The functional metabolic footprint is depicted by sequentially jointing points: SI − 0.5Fs , EI; SI, EI + 0.5Fe ; SI + 0.5Fs , EI; SI, EI − 0.5Fe ; and SI, EI. Fs is the sum of standardized C utilization by structure indicator genera (structure footprint) and Fe by enrichment indicator genera (enrichment footprint) (Ferris, 2010). The abbreviations of genera are as indicated in Table 2.

1.0

X. Zhang et al. / Ecological Indicators 13 (2012) 75–81

Diplo

A

Discom

NT0

Epi Dory

NT100 Filen Cepha

Helico

Geoc Discos Doryd

Thorn

CT100

Alaim Tyley Acroi Praty Aphe Thon Param Prism Euce Meso Malen Apheoi Dorym Chilo

NT50

Cosle

Apor

-0.6

AXIS2

Tylen

Acro

CT50

- 0 .8

CT0

0 .8

0.8

AXIS1

B

CT0 NT50

AXIS2

NT0 Diplo Aphe Thon Tyley Alaim Euce Tylen Praty Cepha Param Apheoi Malen Acroi Doryd Cosle

Acro Helico Dorym Geoc Thorn Chilo Filen CT100 Prism Meso

CT50

Discom

Discos

Apor

-0.8

Epi

Dory

- 0 .6

AXIS1

NT100

1 .0

Fig. 2. Canonical correspondence analysis bi-plot of the abundance and biomass of soil nematode and treatment variables (CT0, CT50 and CT100 were conventional tillage with no residue, 50% and 100% residue, respectively; NT0, NT50 and NT100 were no-tillage with no residue, 50% and 100% residue, respectively). A: Triangles represent abundance of soil nematodes; B: triangles represent biomass of soil nematodes.

not significant. Four-year no-tillage practices in our study did not affect the abundance and biomass of total nematodes and different trophic groups, which suggested that the no-tillage period in our study was not long enough to recover soil nematodes from the long-term tillage effect. In the different residue treatments, total nematode abundance and biomass were significantly greater in 100% residue treatments, due to abundant resources in the presence of cover crops (Okada and Harada, 2007). Similarly, Liebig et al. (2004) reported that inputs of organic materials from crop residue had a strong effect on soil nematode communities. The total abundance and biomass of soil nematode communities reflected the capacity of soil to perform essential ecosystem functions such as nutrient cycling (Yeates and Bongers, 1999; Overstreet et al., 2010). The abundance of bacterivores, plant parasites and omnivores-predators increased with the increasing

79

residue quantity, indicating that the residue quantity was an important driver of soil nematodes at the trophic level (Ferris and Matute, 2003; DuPont et al., 2009). However, no obvious responses of bacterivores to residue management were found. In the soil food web, plant parasites and omnivores-predators belonging to K-strategists with relatively higher cp values exhibited greater sensitivity to environmental disturbance compared to bacterivores belonging to r-strategists (Ferris et al., 2001). The responses of nematodes to tillage and residue were found to be genus-dependent. With the exception of Acrobeloides and Dorylaimellus, genera sensitive to tillage differed from those sensitive to residue, and the different effect mechanisms between tillage and residue might contribute to the discrepancy. Tillage affected soil nematode communities mainly through direct abrasion and changes to soil texture and residue through influencing nutrient cycling (Kladivko, 2001; Rahman et al., 2007). Yeates (2003) also suggested that using nematodes as indicators relies on the discrimination of nematodes at the genus level. In our study, the biomass of Dorylaimellus, a K-strategist located in the higher trophic level of the soil food web (Ferris et al., 2001; Farina and Belgrano, 2004) was sensitive to both tillage and residue management, indicating that the agricultural practice effect may be greater on the growth than on the reproduction (indicated by abundance) process of K-strategists (Sánchez-Moreno et al., 2006). Nematodes such as Acrobeloides, Pratylenchus and Helicotylenchus are abundant in agricultural fields (Briar et al., 2007; Liang et al., 2009), and in the present research, their abundance and biomass were sensitive to residue management. Relative to the sensitive genera, the dominant genus Tylenchorhynchus was tolerant to tillage disturbance. CCA analysis indicated that the tillage factor explained more variations than residue for nematode biomass, whereas opposite results were found for abundance (Fig. 2). These results are similar to the finding of Zhu et al. (2009), who found that straw cover explained more variation in soil fauna abundance than tillage, but tillage affected the distribution pattern of soil fauna through influencing the residue management. The genera positioning in approximately the same direction as the environmental arrows indicated a high positive correlation (the nearer the projected distance of a genus, the stronger the relationship) (Fig. 2). The position of genera distinguished nematode genera with distinctive responses to agricultural management from those with ambiguous responses. Rare genera, such as Discolaimium, were found only in the quadrant of NT (Fig. 2), representing the genera sensitive to tillage disturbance. Fiscus and Neher (2002) also found that the increase or decrease of dominant genera and the presence or absence of rare genera played important roles in the ordination. 4.2. Bioindication of evaluative indicators to tillage and residue The evaluative indicators involving functional changes in the soil food web reflected the composition of soil nematode communities (Sánchez-Moreno et al., 2010). The residue application increased the Shannon diversity index (H ) and the generic richness (GR), but decreased the Simpson index (), which was consistent with our previous findings (Liang et al., 2009). Li et al. (2009) also found that the application of residue had a significant effect on soil nematode diversity due to the increasing supply of resources to the soil food web. The significant tillage effect on TD suggested tillage treatments changed the soil community structure at the trophic level. The effects of no-tillage and residue application were not revealed by the MI. Yeates (2003) claimed that the maturity index actually relied on family level discrimination. However, feeding habits and reproduction potential varied within nematode families. The maturity index has been used successfully to distinguish heavily disturbed or stressed systems (Neher, 1999). In our study, only low to moderate change appeared in short-term agricultural

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X. Zhang et al. / Ecological Indicators 13 (2012) 75–81

Table 5 The indicators sensitive to tillage or residue.

Acknowledgements

Indicators

Tillage (NT)

Residue

Descriptive indicators

–

Evaluative indicators

↑CI ↓TD, EI

↑Total abundance, total biomass, abundance of PP and OP ↑H , GR, NCR, EI, SI, efoot, sfoot ↓␭, BI, CI

Only indicators with a consistent and significant response are listed; ↑ and ↓ indicate the increase or decrease of variables in the no-tillage field or with increasing residue quantity, respectively.

practices, and no response was therefore found in the MI. In both NT and CT treatments, the lowest values of NCR were found in the no residue treatments. The results suggested that the bacterial decomposition pathway were relatively more important in the presence than in the absence of residue, and that the abundant resources and fast nutrient turnover in the residue treatments might contribute to the changes in the NCR (Ferris et al., 2004). SI was significantly affected by an interaction effect of tillage and residue (p < 0.05). The sensitivity of SI is primarily determined by omnivorous and predatory nematode populations which need much more time to establish than the more rapidly growing fungivores and bacterivores (Liang et al., 2009). Relatively lower EI and higher CI in NT (Table 5) indicated that organic matter decomposition was achieved primarily through the fungal energy channel (Sánchez-Moreno et al., 2010; Mills and Adl, 2011). A relatively higher abundance of fungivores and lower abundance of bacterivores resulted in a higher BI in the treatments without residue (Table 5). Since the BI indicated the response of the soil food web to nutrient resources (Ferris et al., 2001), it was more sensitive to the residue effect. In the present study we attempted to utilize the metabolic footprint to validate the bioindication of soil nematodes to agricultural practices. P based on C utilization for production was larger in NT than in CT in the treatments without residue, but an opposite trend appeared after application of residues. Soil nematodes were regulators of residue decomposition through their high turnover rates and interaction with microbes (Fu et al., 2000). Tillage affected the distribution of residue and promoted their mixing with soil, which enhanced C used in production. Sánchez-Moreno et al. (2006) also proved that organic matter decomposition rates were slower in no-tillage. The different treatments had very different food web and metabolic footprint characteristics, which were clearly shown graphically (Fig. 1). The enrichment and structure footprint also increased significantly in the 100% residue, as also reported by Ferris (2010). A greater functional footprint in the 100% residue indicated higher C used in production and total rate of CO2 evolution for nematodes due to a large quantity of residue application. These changes might suggest a positive, bottom-up effect of residue on the soil food web. DuPont et al. (2009) also found that cover crop quantity was an important determinant of the nature and magnitude of soil food web services. 5. Conclusions In conclusion, nematode faunal analysis has been proposed as a useful tool for assessing tillage and residue effects. Our results indicated that the descriptive indicators (the abundance and biomass of total nematodes, and the abundance of plant parasites and omnivores-predators) could be used to obtain an intuitive answer to the effect of residue management, and the evaluative indicators such as CI and EI were comprehensive for interpreting the structure and function of the soil food web in both tillage and residue treatments. Soil nematodes were more sensitive to residue effect than no-tillage effect after short-term practices.

We thank Prof. Maihe Li, Swiss Federal Research Institute, and the two anonymous reviewers provided by the journal for insightful reviews of the manuscript. This research was supported by the National Basic Research Program of China (973 Program) (Nos. 2011CB100504 and 2011CB100506) and the Knowledge Innovation Programs of the Chinese Academy of Sciences (No. KZCX2-YW445).

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