Responses of Soil Nematode Abundance and Diversity to Long-Term Crop Rotations in Tropical China

Responses of Soil Nematode Abundance and Diversity to Long-Term Crop Rotations in Tropical China

Pedosphere 25(6): 844–852, 2015 ISSN 1002-0160/CN 32-1315/P c 2015 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press Respo...

159KB Sizes 0 Downloads 21 Views

Pedosphere 25(6): 844–852, 2015 ISSN 1002-0160/CN 32-1315/P c 2015 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press

Responses of Soil Nematode Abundance and Diversity to Long-Term Crop Rotations in Tropical China ZHONG Shuang1,2,∗ , ZENG Huicai3 and JIN Zhiqiang1 1 Haikou

Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102 (China) Key Laboratory of Banana Genetic Improvement, Haikou 570102 (China) 3 Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102 (China) 2 Hainan

(Received August 15, 2014; revised May 14, 2015)

ABSTRACT A field experiment was carried out from 2003 to 2013 in the Wanzhong Farm of the Hainan Island, China, to determine the effects of two long-term banana rotations on the abundance and trophic groups of soil nematode communities in the island. The experiment was set out as a randomized complete block design with three replications of three treatments: banana-pineapple rotation (AB), banana-papaya rotation (BB) and banana monoculture (CK) in a conventional tillage system. Soil samples were taken at depths of 0–10, 10–20 and 20–30 cm, and nematodes were extracted by a modified cotton-wool filter method and identified to the genus level. Nematode ecological indices of Shannon-Weaver diversity (H ′ ), dominance index (λ), maturity index (MI), plant parasite index (PPI), structure index (SI), enrichment index (EI), and channel index (CI) were calculated. A total of 28 nematode genera with relative abundance over 0.1% were identified, among which Tylenchus and Paratylenchus in the AB, Thonus in the BB, Tylenchus and Helicotylenchus in the CK were the dominant genera. The rotation soils favored bacterivores, fungivores and omnivores-predators with high colonizer-persister (c-p) values. Soil food web in the rotation systems was highly structured, mature and enriched as indicated by SI, MI and EI values, respectively. Higher abundance of bacterivores and lower values of CI suggested that the soil food web was dominated by a bacterial decomposition pathway in rotation soils. Nematode diversity was much higher after a decade of rotation. Soil depth had significant effects on the abundance of soil nematodes, but only on two nematode ecological indices (λ and MI). Key Words:

banana, ecological index, nematode community, rotation system, taxon, trophic group

Citation: Zhong S, Zeng H C, Jin Z Q. 2015. Responses of soil nematode abundance and diversity to long-term crop rotations in tropical China. Pedosphere. 25(6): 844–852.

INTRODUCTION Abundance and diversity of nematode fauna in agricultural soils are receiving increasing attention because of the possibility of using them as a sensitive indicator of performance of farming systems or soil health (Neher, 2001). Nematodes in soils are classified as plant parasites, bacterivores, fungivores and omnivores-predators based on their feeding habits. Each trophic group has the potential of reflecting a different aspect of changes in soil conditions (Yeates et al., 1993). Bacterivores and fungivores are closely related to decomposition of soil organic matter, and the ratio of numbers of these two trophic groups re∗ Corresponding

author. E-mail: [email protected]

flects the decomposition of organic matter and mineralization of N and C (Zhang et al., 2009). Omnivorespredators are most sensitive to environmental disturbances resulting from changes in land use, which are higher in a natural land than in a disturbed agricultural land (Viketoft et al., 2011). Plant parasites attack many field crops and cause serious economical damage (Waweru et al., 2014). Population density and structure of nematodes should be widely used as a powerful ecological tool to assess soil condition as they respond to changes in the soil environment caused by land use or agricultural management. It is well documented that rotation exerts a great influence on important soil quality attributes such as

RESPONSE OF SOIL NEMATODES TO CROP ROTATIONS

845

soil biota structure, organic matter content and moisture retention capacity (Ponge et al., 2013). At the same time, there are plenty of evidences that the abundance and composition of different nematode trophic groups are affected by rotation systems (Stirling et al., 2011; Matute and Anders, 2012). For example, Pan et al. (2010) demonstrated that the abundance and population density of fungivores and omnivores-predators are significantly higher in a 5-year soybean-wheat-corn rotation than in a 5-year soybean monoculture under fertilizer application. DuPont et al. (2014) also found that the abundance of free-living nematodes is significantly greater in a perennial meadow-wheat rotation than that in a wheat monoculture associated with notillage and residue management. In contrast, a greater population of plant parasites was recorded from plots with a wheat monoculture than a perennial meadowwheat rotation. In terms of pest control, Damour et al. (2014) suggested that the percentage of the aggregate plant parasites sharply declines after rotation with the nematode-suppressive crops. Therefore, soil nematodes are considered potential bio-indicators of rotation management (Pan et al., 2012). However, more information is needed, particularly over a range of cropping systems and environments, to demonstrate the effects of rotation management on the abundance and diversity of nematodes in cultivated soils. Banana is the main agricultural crop in South China. Plant pathogenic nematode disease caused by a long-term monoculture is recognized as the major factor limiting banana production. Zhong et al. (2013, 2014) reported that a banana monoculture provided preferential food resources for specific plant parasites, such as Meloidogyne, Pratylenchus and Rotylenchulus, which increased the competitive advantages of plant pathogenic nematodes over beneficial free-living forms, resulting in more than 70% yield losses. Rotation systems provide an effective control of root pathogens, improve banana growth, increase banana yield, and sustain soil quality (Qu´en´eherv´e et al., 2011). However, there has been a lack of characterization of soil nematode communities under the banana rotations, especially in a southern, tropical monsoon climate area. Therefore, the objective of this investigation was to determine the effects of two long-term banana rotations on the abundance and trophic groups of soil

nematode communities in the Hainan Island, Tropical China. MATERIALS AND METHODS Site description A field experiment was carried out in the Wanzhong Farm in Ledong (18◦ 37′ –18◦ 38′ N, 108◦ 46′ – 108◦ 48′ E), Hainan Province, China. The region has a tropical monsoon climate with a mean annual temperature of 25.8 ◦ C and a mean annual precipitation of 2 065 mm. The test soil was classified as sandy loam according to the U.S. Department of Agriculture (USDA) texture classification system, with 6.86 g kg−1 total organic C, 0.69 g kg−1 total N, 0.62 g kg−1 total P, 1.13 g kg−1 total K and pH 6.4. The total contents of clay, silt and sand were 140.5, 205.6 and 653.9 g kg−1 , respectively. The field experiment was divided into nine plots (170 m2 each), distributed in a completely randomized block design, and combined in the following three treatments (three replicates per treatment): banana (Musa nana cv. Baxijiao AAA)-pineapple (Ananas cv. Comte de paris) rotation (AB), banana-papaya (Carica cv. Sunrise solo) rotation (BB) and banana monoculture (CK) in a conventional tillage system. The chemical N (urea), P (superphosphate) and K fertilizers (sulphate) were applied at the rates of 960.0 kg N ha−1 , 576 kg P ha−1 and 2 880 kg K ha−1 to a depth of 0–20 cm after transplanting every year. The manure used was cow manure compost (14.4 t ha−1 ), with 533 g kg−1 soil water content, containing 145 g C kg−1 , 3.2 g N kg−1 , 2.5 g P2 O5 kg−1 , 1.6 g K2 O kg−1 on a dry-weight basis, which was basally applied before transplanting (June 25) to a depth of 0–20 cm every year. Lime was used (125 kg ha−1 ) together with cow manure compost for increasing soil pH. The experiment was conducted from 2003 to 2013, with one crop season in each year. Soil was mouldboard ploughed (30 cm deep) at the end of May, the crops were sown at the end of June, and the residues were left on the surface after crops harvest in mid-May of next year. Soil sampling All soil samples were collected together at the last growing season. After the removal of aboveground plant debris, soil samples were extracted using a soil

S. ZHONG et al.

846

corer (3.0 cm diameter) at depths of 0–10, 10–20 and 20–30 cm below the soil surface at the booting stage (March 20, 2014) within the rows of banana plants, 50 cm from the base of the banana plant. For each sample, five random cores were combined to form one composite sample. The fresh soil samples were stored in individual plastic bags and then immediately stored in a 4 ◦ C cold room. A subsample of 100 g soil (fresh weight) was used for nematode extraction. Subsamples were first elutriated and sieved (mesh size 38 and 250 µm) with water. Nematodes from the suspensions were then extracted using a modified cotton-wool filter method (Liang et al., 2009). The abundance of nematodes was expressed as individuals per g dry soil. Nematodes were identified to genus level using an inverted compound microscope. The classification of trophic groups is assigned to bacterivores, fungivores, plant parasites and omnivores-predators (Yeates and Bongers, 1999). Calculation of ecological indices Nematode taxonomic and functional diversity was analyzed by the following approaches. The ShannonWeaver diversity (H ′ , Shannon, 1948) was calculated as H ′ = −ΣPi (lnPi ), where Pi is the proportion of individuals in the i taxon. The Simpson index (λ) was calculated to determine effects of plant species on nematode taxonomic diversity (De Deyn et al., 2004; Liang et al., 2007). The maturity index (MI) was calculated as ΣPi Ci , where Ci is the colonizer-persister (c-p) value of the i taxon according to the 1–5 c-p scale of Bongers and Bongers (1998). The plant parasite index (PPI) was determined in a similar manner for plant parasitic genera (Yeates and Bongers, 1999). The structure index (SI), enrichment index (EI) and channel index (CI), indicators for the structure and function of soil food web (Ferris et al., 2001; De Deyn et al., 2004; Liang et al., 2007), were calculated according to the method of Ferris et al. (2001), and the c-p values of taxa are adopted from Bongers (1990) and Bongers and Bongers (1998). Statistical analysis Results were statistically analyzed with the analysis of variance (ANOVA) procedure using the SPSS 10.0 software package for Windows. Means were compared between treatments and soil depths by Fisher’s

least significant difference (LSD) test. Two-way ANOVA was applied to test the effects of rotation and soil depth as main effects and their two-way interaction on soil nematode abundances and ecological indices. Differences at P < 0.05 and P < 0.01 were considered as statistically significant. RESULTS Abundance and diversity of soil nematode The number of total nematode genera identified was 28 for the three treatments, with the highest value in the BB (27 nematode genera) at 0–10 cm and the lowest in the CK (18 nematode genera) at 20–30 cm (Table I). Among the identified 28 nematode genera in soil at 0–30 cm, Thonus in the BB, Paratylenchus in the AB, Tylenchus in the AB and CK, Helicotylenchus in the CK, and Boleodors in the three treatments were the dominant genera (relative abundance > 10%, Table I). The proportion contribution of individuals in bacterivores to total soil nematodes varied in a range of 0%–6.73%, with the highest proportion in the AB at 10–20 cm and the lowest proportion in CK at 20– 30 cm. The contribution of individuals in fungivores to total soil nematodes varied in a range of 0%–4.25%, with the highest proportion in the BB at 0–10 cm and the lowest proportion in CK at 20–30 cm. The contribution of individuals in plant parasites to total soil nematodes varied in a range of 0%–20.47%, with the highest proportion in the BB at 20–30 cm and the lowest proportion in the CK at 10–20 cm. The contribution of individuals in omnivores-predators to total soil nematodes varied in a range of 0%–10.60%, with the highest proportion in the BB at 10–20 cm and the lowest proportion in the CK at 0–10 cm. Significant effects of treatment and soil depth on total nematode abundance were observed (P < 0.05, Table II). The highest abundance of total nematodes (5.40 individuals g−1 dry soil) was observed in the AB at 0–10 cm. The lowest abundance of total nematodes (4.17 individuals g−1 dry soil) was observed in the CK at 20–30 cm. The abundance of total nematodes was significantly higher (P < 0.05) in the AB and BB than in the CK at 0–30 cm (Table II). The abundance of total nematodes decreased sharply (P < 0.05) with the increase of soil depth under the AB, BB and CK. Significant treatment effect was observed on the

RESPONSE OF SOIL NEMATODES TO CROP ROTATIONS

847

TABLE I Contributions of different nematode trophic groups and genera to total soil nematodes averaged under different rotation treatments at three soil depths of 0–10, 10–20 and 20–30 cm Group and genus

Treatmenta)

Guildsb)

AB

BB

0–10 cm 10–20 cm 20–30 cm

0–10 cm 10–20 cm

30.67 5.50 6.67 0.00 2.68 0.00 4.03 0.00 3.15 0.00 3.70 4.94

34.22 6.40 6.55 0.00 3.27 0.00 4.67 0.00 3.00 0.00 4.30 4.03

29.97 6.73 5.67 0.00 3.05 0.00 5.44 0.00 2.52 0.00 2.40 4.16

25.61 4.22 5.28 0.59 2.37 1.58 2.50 0.64 1.61 0.57 2.32 3.93

5.73 2.16 2.64 0.93

5.61 1.98 2.65 0.98

5.33 2.63 2.70 0.00

49.10 10.27 9.70 10.33 10.50 4.00 4.30 0.00

45.67 11.69 9.00 10.00 11.66 0.00 3.33 0.00

Omnivore-predators 12.50 Mononchus 3.00 Thonusd) 3.60 Eudorylaimus 0.00 Epidorylaimus 2.50 Prodorylaimus 0.00 Aporcelaimellus 3.40 Discolaimus 0.00

14.50 3.66 3.68 0.00 2.33 1.75 3.08 0.00

Bacterivores Mesorhabditisc) Protorhabditisc) Monhystera Heterocephalobus Acrobeles Acrobeloidesc) Cervidellus Plectus Odontolaimus Prismatolaimus Alaimus Fungivores Aphelenchus Aphelenchoides Tylencholaimus Plant parasites Boleodorsd) Malenchusc) Tylenchusd) Paratylenchusd) Helicotylenchusc) Rotylenchusc) Trichodorus

CK 20–30 cm 0–10 cm 10–20 cm

20–30 cm

% 24.51 2.63 4.52 0.96 3.92 0.00 2.00 0.67 0.96 0.65 3.00 4.50

25.57 2.88 4.55 1.64 3.18 1.61 2.29 0.00 1.64 1.27 2.66 4.20

27.88 0.00 0.60 0.00 2.79 2.30 6.55 0.79 0.00 2.65 0.98 3.56

18.94 0.60 0.00 0.00 3.46 4.04 6.01 0.00 0.00 0.00 2.06 2.77

17.48 0.00 0.00 0.00 3.15 2.39 6.13 0.00 0.00 0.00 0.00 2.91

Ba1 Ba1 Ba1 Ba2 Ba2 Ba2 Ba2 Ba2 Ba3 Ba3 Ba4

7.51 4.25 2.30 0.96

5.55 2.58 2.06 0.91

4.69 3.20 1.49 0.00

4.35 2.63 1.72 0.00

4.70 2.36 2.01 0.33

3.89 2.01 1.88 0.00

Fu2 Fu2 Fu4

46.00 12.30 4.00 10.00 11.34 6.36 2.00 0.00

47.26 10.05 7.62 9.29 8.65 8.16 3.09 0.00

45.99 10.35 2.83 9.25 8.53 9.22 5.16 0.65

44.72 10.11 3.86 8.04 7.46 8.74 5.84 0.67

57.74 13.43 9.00 12.96 5.19 12.64 4.48 0.00

62.49 20.47 4.00 10.25 6.29 13.83 7.65 0.00

60.81 16.37 4.81 10.75 7.32 13.21 8.35 0.00

PP2 PP2 PP2 PP2 PP3 PP3 PP4

18.70 3.50 4.33 0.00 3.80 2.40 4.67 0.00

20.02 1.27 10.03 1.44 0.61 2.04 4.23 0.40

23.95 2.30 10.60 1.61 0.00 2.82 4.24 2.38

25.02 2.01 10.52 2.33 0.65 2.97 4.58 1.96

10.03 0.00 4.21 0.00 0.00 3.84 1.98 0.00

13.87 0.00 4.33 0.00 3.04 3.69 2.20 0.61

17.82 1.45 5.21 0.00 3.09 4.10 2.40 1.57

Ca4 Om4 Om4 Om4 Ca5 Om5 Om5

a) AB

= banana-pineapple rotation; BB = banana-papaya rotation; CK = banana monoculture. guilds of soil nematodes characterized by feeding habits and life-history characters, and the subscript numbers indicate the colonizer-persister (c-p) values (Bongers and Bongers, 1998; Ferris et al., 2001). c) Dominant genera (> 5%). d) Dominant genera (> 10%). b) Functional

abundance of fungivores, plant parasites, and omnivores-predators (P < 0.01) and significant soil depth effect was observed on the abundance of plant parasites and omnivores-predators (P < 0.05, Table II). The highest abundance of bacterivores and fungivores (1.55 and 0.36 individuals g−1 dry soil) was observed in

the AB at 0–10 cm. The lowest abundance of bacterivores and fungivores (0.75 and 0.09 individuals g−1 dry soil) was observed in the CK at 20–30 cm. The highest abundance of plant parasites (3.42 individuals g−1 dry soil) and the lowest abundance of omnivores-predators (0.29 individuals g−1 dry soil) were both observed in

S. ZHONG et al.

848

TABLE II Abundance of nematode trophic groups under different rotation treatments at three soil depths and the results of two-way analysis of variance (ANOVA) Soil nematode

Treatmenta)

Soil depth (cm) 0–10

Total nematodes

Bacterivores

Fungivores

Plant parasites

Omnivore-predators

AB BB CK AB BB CK AB BB CK AB BB CK AB BB CK

5.40 5.25 4.83 1.55 1.38 0.96 0.36 0.32 0.17 3.04 2.71 3.42 0.45 0.84 0.29

P value 10–20

± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

individuals 0.58b) ac) 5.07 0.52a 4.82 0.50b 4.62 0.32a 1.25 0.30a 1.09 0.25b 0.79 0.10a 0.24 0.07a 0.29 0.07b 0.13 0.30b 2.84 0.21b 2.53 0.34a 3.32 0.10a 0.74 0.15a 0.92 0.04b 0.37

Treatment Soil depth Treatment × soil depth

20–30

g−1 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

dry soil 0.48a 4.75 0.46a 4.69 0.42b 4.17 0.31a 1.11 0.22a 1.06 0.24b 0.75 0.09a 0.21 0.06a 0.17 0.04b 0.09 0.26b 2.32 0.17b 2.21 0.30a 2.93 0.13a 1.11 0.19a 1.25 0.07b 0.39

± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.44a 0.43a 0.41b 0.24a 0.21a 0.15b 0.06a 0.04a 0.03b 0.19b 0.16b 0.24a 0.22a 0.24a 0.08b

0.049

0.029

nsd)

0.043

ns

0.018

< 0.01

ns

0.012

< 0.01

0.034

ns

< 0.01

0.018

ns

a) AB

= banana-pineapple rotation; BB = banana-papaya rotation; CK = banana monoculture. ± standard error (n = 3). c) Means followed by the same letter(s), within the same soil depth, are not significantly different (P < 0.05) among different treatments. d) Not significant. b) Mean

the CK at 0–10 cm. The lowest abundance of plant parasites (2.21 individuals g−1 dry soil) and the highest abundance of omnivores-predators (1.25 individuals g−1 dry soil) were both observed in the BB at 20– 30 cm. The abundance of bacterivores, fungivores and omnivores-predators was significantly higher (P <0.01) in the AB and BB than that in the CK at each soil depth (Table II). The abundance of plant parasites was significantly lower (P < 0.01) in the AB and BB than that in the CK at each soil depth. The abundance of bacterivores, fungivores and plant parasites decreased sharply (P < 0.05) with the increase of soil depth under the AB, BB and CK, while those of omnivorespredators increased under the three treatments (Table II). Ecological indices Significant treatment effect was observed on H ′ , λ, MI, PPI, SI, EI and CI (P < 0.01), and significant soil depth effect was observed on λ and MI (P < 0.05, Table III). The values of H ′ , MI, SI and EI were significantly higher (P < 0.01) in the AB and BB than those in the CK at each soil depth. The values of λ, PPI

and CI were significantly lower (P < 0.01) in the AB and BB than in the CK at each soil depth (Table III). The values of H ′ at each soil depth varied in a range of 2.18–2.72, with the following order: CK < AB < BB. The values of λ and PPI at each soil depth varied in a range of 0.08–0.14 and 2.03–2.35, respectively, with the following order: BB < AB < CK. The values of CI in 0–30 cm varied in a range of 26.69–69.03, with the following order: AB < BB < CK. The values of MI, SI and EI at each soil depth varied in a range of 2.01–3.37, 37.47–83.38 and 34.98–71.85, respectively, with the following order: CK < BB < AB (Table III). The values of H ′ , λ, PPI and EI decreased sharply (P < 0.01) with the increase of soil depth under AB, BB and CK, while those of MI, SI and CI increased under the three treatments (Table III). DISCUSSION Changes of soil nematode communities Soil nematode communities showed significantly differences between rotation and monoculture soils. The abundance of total nematode at each soil depth

RESPONSE OF SOIL NEMATODES TO CROP ROTATIONS

849

TABLE III Nematode ecological indices under rotation treatments at three soil depths and the results of two-way analysis of variance (ANOVA) Ecological indexa)

Treatmentb)

Soil depth (cm) 0–10

H′

λ

MI

PPI

SI

EI

CI

AB BB CK AB BB CK AB BB CK AB BB CK AB BB CK AB BB CK AB BB CK

2.61 2.72 2.40 0.12 0.10 0.14 2.86 2.85 2.01 2.20 2.13 2.35 76.59 70.29 37.47 71.85 70.44 44.06 26.69 31.98 55.88

P value 10–20

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.35c) ad) 0.36a 0.34b 0.02b 0.01b 0.02a 0.25a 0.24a 0.19b 0.22b 0.13b 0.26a 7.90a 6.66a 4.71b 7.88a 6.20a 5.25b 6.43b 8.49b 11.66a

2.48 2.69 2.35 0.11 0.09 0.13 3.22 3.10 2.48 2.19 2.09 2.32 79.22 72.32 40.87 69.90 66.81 39.66 30.07 37.29 62.90

20–30 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.34a 0.35a 0.33b 0.01b 0.01b 0.01a 0.31a 0.29a 0.22b 0.21b 0.12b 0.23a 8.03a 7.77a 5.32b 7.04a 5.18a 4.92b 7.21b 8.63b 14.47a

2.44 2.67 2.18 0.09 0.08 0.11 3.37 3.35 2.53 2.13 2.03 2.25 83.38 76.56 43.30 62.23 52.99 34.98 39.54 46.25 69.03

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.33a 0.34a 0.32b 0.01b 0.01b 0.01a 0.39a 0.33a 0.27b 0.16b 0.10b 0.18a 9.34a 8.90a 6.18b 6.24a 4.07a 3.48b 9.34b 10.80b 16.15a

Treatment

Soil depth

Treatment × soil depth

< 0.01

nse)

ns

< 0.01

0.046

ns

< 0.01

0.014

ns

< 0.01

ns

ns

< 0.01

ns

ns

< 0.01

ns

0.037

< 0.01

ns

ns

a) H ′

= Shannon-Weaver diversity; λ = Simpson index; MI = maturity index; PPI = plant parasite index; SI = structural index; EI = enrichment index; CI = channel index. b) AB = banana-pineapple rotation; BB = banana-papaya rotation; CK = banana monoculture. c) Mean ± standard error (n = 3). d) Means followed by the same letter(s), within the same soil depth, are not significantly different (P < 0.05) among different treatments. e) Not significant.

obtained an increase of 9.9%–14.1% on the AB and 4.5%–12.6% on the BB compared with the CK, which was consistent with Matute and Anders (2012) in a 3-year rice-soybean-corn rotation in Arkansas. The increases could have been related to greater root dry matter and higher C and N contents of pineapple and papaya residues (Pan et al., 2012). In this study, rotations containing pineapple or papaya significantly reduced the populations of plant parasites, which was consistent with Briar et al. (2012) in a 10-year wheat-pea-wheat-flax rotation in Glenlea. The aggregate plant parasites constituted 60.3% (a mean at three depths) of the total population under a banana monoculture (CK), but in the rotation treatments, the proportion declined sharply to 46.9% for the AB and 45.8% for the BB. However, pineapple or papaya had no effects on the populations of Boleodors and Ty-

lenchus, perhaps because Tylenchidae could survive well in many hosts (Briar et al., 2011). Populations of Helicotylenchus and Rotylenchus decrease sharply in rotation soils but these species are not an important pathogen of banana (Djigal et al., 2012a). Radopholus similis and Pratylenchus spp. were the most important pathogenic nematodes for banana, but they were not found at all treatments due to the effects of soil temperature, humidity and physicochemical properties. Therefore, the lower abundance of plant parasites in rotation soils may result from the higher level of organic matter-mediated suppressiveness and the predation of nematode pests by omnivores-predators (Stirling et al., 2012). Free-living nematodes (bacterivores, fungivores and omnivores-predators) play very important roles in soil food webs (Ferris and Bongers, 2006), and the

850

higher populations of those nematodes in the AB and BB than in the CK indicated that the food web was more active in rotation soils than in monoculture soils. The abundance of bacterivores and fungivores at each soil depth was markedly higher in the AB and BB than in the CK, which was consistent with the observation by Carter et al. (2009) in a 3-year potato-barley-red clover rotation in Canada. This indicates that more abundant microbial populations, effective organic matter decomposition and higher soil fertility in rotation systems compared with monoculture are caused by the large input of organic amendments and the crop residues (S´anchez-Moreno et al., 2009). Greater abundance of omnivores-predators was observed in the AB and BB than in the CK at each soil depth, which was consistent with Stirling et al. (2010) in a sugarcanemaize-soybean rotation field. The differences were probably associated with tillage (mouldboard ploughed to 30 cm) in monoculture soils and, to a lesser extent, by shallow manual hoeing in rotation soils, which indicated that rotation led to a more stable and undisturbed soil ecosystem than monoculture. Changes of soil nematode ecological indices The ecological indices of H ′ and λ are linked to the diversity of soil nematodes, and MI and PPI can reflect changes in soil environment due to crop rotations (Culman et al., 2010). An increase of 5.5%–22.6% on H ′ and 15.5%–41.7% on λ was observed in rotation soils compared with monoculture soils at each soil depth, which was consistent with the result of Korenko and Schmidt (2006) in a rice-pasture rotation in Uruguay, indicating a trend of greater soil nematode biodiversity and some genera dominated the community in rotation soils, as a result of the long-term presence of the alternative host plant providing a variety of food sources to the nematodes. An increase of 29.8%–42.4% on MI and 5.4%–11.0% on PPI was observed in rotation soils compared with monoculture soils at each soil depth, which was consistent with the result of Zhang et al. (2012) in a maize-wheat rotation in the HuangHuai-Hai Plain, suggesting a relatively stable environment in rotation soils. The result was attributed to the higher proportions of intolerant genera, such as omnivores-predators belonging to long-lived, relative-

S. ZHONG et al.

ly larger sized K-strategists and lower proportion of plant parasites with c-p 3 in rotation soils compared to monoculture soils (Ugarte et al., 2013). The indices of SI, EI and CI may provide information about soil food webs in stressed, enriched, stable structured and decomposition environments (Ferris et al., 2001). The SI and EI values were higher in the AB and BB than those in the CK at each soil depth, which was consistent with the previous studies (Zhang et al., 2013; Wang et al., 2014). The greater SI values in rotation soils demonstrate soil food webs which are more complex and highly structured and contain more top omnivores-predators than those found in monoculture soils. The changes of EI values indicated that rotation soils had a highly enriched soil food web compared with monoculture soils, which could be explained as enrichment-opportunistic bacterivores with short lifecycles (such as Rhabditidae) respond rapidly to organic matter and were more abundant than basal bacterivores (such as Acrobeloides and Cephalobidae) in rotation soils. Basal bacterivores were more abundant in monoculture soils and contributed to the low EI values (Djigal et al., 2012a, b). The CI values were higher than 50 in the AB and BB and lower than 50 in the CK at the three soil depths, which confirmed the result from Stirling et al. (2011) in a sugarcane-soybean rotation, indicating that the soil food web was dominated by a bacterial decomposition pathway in rotation soils, while a fungal decomposition pathway was relatively important in monoculture soils. The reason could be due to organic matter derived from pineapple or papaya residues with low C/N ratios, more easy to decomposition, increasing the ratio of bacterivores to fungivores compared with banana residues (Wang et al., 2014). In conclusion, this study demonstrated that bacterivores, fungivores and omnivores-predators were more abundant in banana rotations, supporting a soil food web with abundant organisms at higher trophic levels. The populations of plant parasites could be controlled successfully through banana rotations, at least below the values that were associated with plant damage. Therefore, nematode faunal analysis has been proposed as a useful tool for assessing crop rotation effects.

RESPONSE OF SOIL NEMATODES TO CROP ROTATIONS

ACKNOWLEGEMENT This research was supported by the National Natural Science Foundation of China (No. 41301277) and the Natural Science Foundation of Hainan Province, China (No. 310073). REFERENCES Bongers T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia. 83: 14–19. Bongers T, Bongers M. 1998. Functional diversity of nematodes. Appl Soil Ecol. 10: 239–251. Briar S S, Barker C, Tenuta M, Entz M H. 2012. Soil nematode responses to crop management and conversion to native grasses. J Nematol. 44: 245–254. Briar S S, Fonte S J, Park I, Six J, Scow K, Ferris H. 2011. The distribution of nematodes and soil microbial communities across soil aggregate fractions and farm management systems. Soil Biol Biochem. 43: 905–914. Carter M R, Noronha C, Peters R D, Kimpinski J. 2009. Influence of conservation tillage and crop rotation on the resilience of an intensive long-term potato cropping system: restoration of soil biological properties after the potato phase. Agr Ecosyst Environ. 133: 32–39. Culman S W, DuPont S T, Glover J D, Buckley D H, Fick G W, Ferris H, Crews T E. 2010. Long-term impacts of high-input annual cropping and unfertilized perennial grass production on soil properties and belowground food webs in Kansas, USA. Agr Ecosyst Environ. 137: 13–24. Damour G, Dorel M, Quoc H T, Meynard C, Ris` ede J M. 2014. A trait-based characterization of cover plants to assess their potential to provide a set of ecological services in banana cropping systems. Eur J Agron. 52: 218–228. De Deyn G B, Raaijmakers C E, Van Ruijven J, Berendse F, Van Der Putten W H. 2004. Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos. 106: 576–586. Djigal D, Chabrier C, Duyck P F, Achard R, Qu´ en´ eherv´ e P, Tixier P. 2012a. Cover crops alter the soil nematode food web in banana agroecosystems. Soil Biol Biochem. 48: 142–150. Djigal D, Saj S, Rabary B, Blanchart E, Villenave C. 2012b. Mulch type affects soil biological functioning and crop yield of conservation agriculture systems in a long-term experiment in Madagascar. Soil Till Res. 118: 11–21. DuPont S T, Beniston J, Glover J D, Hodson A, Culman S W, Lal R, Ferris H. 2014. Root traits and soil properties in harvested perennial grassland, annual wheat, and never-tilled annual wheat. Plant Soil. 381: 405–420. Ferris H, Bongers T. 2006. Nematode indicators of organic enrichment. J Nematol. 38: 3–12. Ferris H, Bongers T, de Goede R G M. 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol. 18: 13–29. Korenko V, Schmidt C. 2006. Effects of agricultural practices in

851

the rice crop system on nematode communities in Uruguay. Nematol Medit. 34: 151–159. Liang W J, Li F P, Li Q, Zhang W D. 2007. Temporal dynamics of soil nematode community structure under invasive Ambrosia trifida and native Chenopodium serotinum. Helminthologia. 44: 29–33. Liang W J, Lou Y L, Li Q, Zhong S, Zhang X K, Wang J K. 2009. Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biol Biochem. 41: 883–890. Matute M M, Anders M. 2012. Influence of rice rotation systems on soil nematode trophic groups in Arkansas. J Agr Sci. 4: 11–20. Neher D A. 2001. Role of nematodes in soil health and their use as indicators. J Nematol. 33: 161–168. Pan F J, McLaughlin N B, Yu Q, Xue A G, Xu Y L, Han X Z, Li C J, Zhao D. 2010. Responses of soil nematode community structure to different long-term fertilizer strategies in the soybean phase of a soybean-wheat-corn rotation. Eur J Soil Biol. 46: 105–111. Pan F J, Xu Y L, McLaughlin N B, Xue A G, Yu Q, Han X Z, Liu W, Zhan L L, Zhao D, Li C J. 2012. Response of soil nematode community structure and diversity to long-term land use in the black soil region in China. Ecol Res. 27: 701–714. Ponge J F, P´ er` es G, Guernion M, Ruiz-Camacho N, Cortet J, Pernin C, Villenave C, Chaussod R, Martin-Laurent F, Bispo A, Cluzeau D. 2013. The impact of agricultural practices on soil biota: a regional study. Soil Biol Biochem. 67: 271–284. Qu´ en´ eherv´ e P, Barri` ere V, Salmon F, Houdin F, Achard R, Gertrude J C, Marie-Luce S, Chabrier C, Duyck P F, Tixier P. 2011. Effect of banana crop mixtures on the plant-feeding nematode community. Appl Soil Ecol. 49: 40–45. S´ anchez-Moreno S, Nicola N L, Ferris H, Zalom F G. 2009. Effects of agricultural management on nematode-mite assemblages: soil food web indices as predictors of mite community composition. Appl Soil Ecol. 41: 107–117. Shannon C E. 1948. A mathematical theory of communication. Bell System Tech J. 27: 379–423. Stirling G R, Halpin N V, Bell M J, Moody P W. 2011. Impact of tillage and residues from rotation crops on the nematode community in soil and surface mulch during the following sugarcane crop. Int Sugar J. 113: 56–64. Stirling G R, Moody P W, Stirling A M. 2010. The impact of an improved sugarcane farming system on chemical, biochemical and biological properties associated with soil health. Appl Soil Ecol. 46: 470–477. Stirling G R, Smith M K, Smith J P, Stirling A M, Hamill S D. 2012. Organic inputs, tillage and rotation practices influence soil health and suppressiveness to soilborne pests and pathogens of ginger. Australas Plant Path. 41: 99–112. Ugarte C M, Zaborski E R, Wander M M. 2013. Nematode indicators as integrative measures of soil condition in organic cropping systems. Soil Biol Biochem. 64: 103–113. Viketoft M, Sohlenius B, Bostr¨ os S, Palmborg C, Bengtsson J, Berg M P, Huss-Danell K. 2011. Temporal dynamics of soil nematode communities in a grassland plant diversity experiment. Soil Biol Biochem. 43: 1063–1070.

852

Wang K H, Radovich T, Pant A, Cheng Z Q. 2014. Integration of cover crops and vermicompost tea for soil and plant health management in a short-term vegetable cropping system. Appl Soil Ecol. 82: 26–37. Waweru B, Turoop L, Kahangi E, Coyne D, Dubois T. 2014. Non-pathogenic Fusarium oxysporum endophytes provide field control of nematodes, improving yield of banana (Musa sp.). Biol Control. 74: 82–88. Yeates G W, Bongers T. 1999. Nematode diversity in agroecosystems. Agr Ecosyst Environ. 74: 113–135. Yeates G W, Bongers T, De Goede R G M, Freckman D W, Georgieva S S. 1993. Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol. 25: 315–331. Zhang X K, Jiang Y, Liang L, Zhao X F, Li Q. 2009. Response of soil nematode communities to long-term application of in-

S. ZHONG et al.

organic fertilizers in the black soil of Northeast China. Front Biol China. 4: 111–116. Zhang S X, Li Q, L¨ u Y, Zhang X P, Liang W J. 2013. Contributions of soil biota to C sequestration varied with aggregate fractions under different tillage systems. Soil Biol Biochem. 62: 147–156. Zhang X K, Li Q, Zhu A N, Liang W J, Zhang J B, Steinberger Y. 2012. Effects of tillage and residue management on soil nematode communities in North China. Ecol Indic. 13: 75–81. Zhong S, Guo G, Zeng H C, Jin Z Q. 2013. Influence of continuous cropping on soil nematode communities in Chinese banana plantation. Res on Crops. 14: 1140–1150. Zhong S, Mo Y, Guo G, Zeng H, Jin Z. 2014. Effect of continuous cropping on soil chemical properties and crop yield in banana plantation. J Agr Sci Tech. 16: 239–250.