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Response of soil nematode community composition and diversity to different crop rotations and tillage in the tropics
Applied Soil Ecology 107 (2016) 134–143
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Response of soil nematode community composition and diversity to different crop rotations and tillage in the tropics Zhong Shuanga,b,1,* , Zeng Hui-caic , Jin Zhi-qianga a b c
Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102, China Hainan Key Laboratory of Banana Genetic Improvement, Hainan, Haikou 570102, China Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Science, Haikou 570101, China
A R T I C L E I N F O
Article history: Received 9 February 2016 Received in revised form 13 May 2016 Accepted 19 May 2016 Available online xxx Keywords: Nematodes Community composition Tillage Rotation Monoculture Metabolic footprint
A B S T R A C T
Soil nematode community composition and diversity response to banana-pineapple (BA), bananapapaya (BP), banana-rice (BR) rotations and banana monoculture (CK) (12-year annual crops) under no-tillage (NT) and conventional tillage (CT) were assessed in the Wanzhong Farm in Hainan Island, China. Soil samples were taken at depth of 0–40 cm in 2014–2015. A total of 47 nematode genera with relative abundance over 0.1% were identified. Acrobeloides in BANT and BRCT, Aphelenchus in BANT, BACT, BRNT and BRCT, Helicotylenchus, Rotylenchulus and Meloidogyne in CKNT and CKCT were the dominant genera. In comparison with CK, BA, BP and BR increased the number of bacterivores, fungivores and omnivore–carnivores, and the concentration of bacterial PLFA and fungal PLFA. The no-tillage soils favored bacterivores, fungivores and high colonizer-persister (c-p) value omnivores and carnivores, but reduced plant parasites. Soil food web in the rotation combined with no-tillage systems was highly structured, mature and moderately enriched as indicated by Structure (SI), Maturity (MI) and Enrichment (EI) index values, respectively. Higher number of bacterivores and lower values of Channel index (CI) suggested bacterial-dominated decomposition in no-tillage soil. Soil nematode diversity and functional metabolic footprint were much greater after 12 years of crop rotation. The descriptive indicators were useful to provide insight into the effect of rotation and tillage, and the evaluative indicators were more comprehensive for interpreting the structure and function of the soil food web under different crop rotations and tillage. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction In agroecosystems, agricultural practices such as crop rotation, residue addition and no-tillage or reduced-tillage are beneficial for sustainable crop production due to their positive influences on soil physicochemical properties, microbial activity and biomass, and the composition and function of soil biota (Cunha et al., 2015; Kibet et al., 2016). For example, crop rotation can increase the input of organic C and N into the soil, which enhances soil fertility (Costa and Crusciol, 2016). When high amounts of crop residues are returned to the soil, crop rotation can influence the soil microbial habitat, improve soil structure (Meena et al., 2015), and increase
* Corresponding author at: Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102, China. E-mail address: [email protected] (S. Zhong). 1 Supported by the National Natural Science Foundation of China to S. Zhong (41301277), the Natural Science Foundation of Hainan Province to S. Zhong (310073) and the State Scholarship Fund of China to S. Zhong (201503260016). http://dx.doi.org/10.1016/j.apsoil.2016.05.013 0929-1393/ã 2016 Elsevier B.V. All rights reserved.
biomass and diversity of soil fauna (Zhang et al., 2016). In addition, no-tillage involving surface crop residue application has been adopted as a means to promote soil aggregate stability and fertility, while simultaneously increasing the abundance and viability of soil biota (Ontl et al., 2015). Composition and abundance of nematode fauna in agricultural soils are receiving increased 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 predators-omnivores based on their feeding habits. Each nematode 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 the numbers of these two trophic groups reflects the decomposition of organic matter and mineralization of nitrogen and carbon (Gu et al., 2015). Omnivores-predators are most sensitive to environmental disturbances resulting from changes in land use, which are higher in a natural land than in
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a disturbed agricultural land (Viketoft et al., 2011). Plant parasites attack many field crops and cause serious economical damage (Waweru et al., 2014). Higher population density and diversified structure of nematode communities should be widely used as a powerful ecological tool to assess soil condition as they respond to changes in the soil environment. Considering these indicative functions, many researchers have reported how soil nematodes respond to agricultural practices. For example, Forge et al. (2015) showed that in comparison with conventional tillage, no-tillage or reduced tillage significantly decreased Pratylenchus neglectus populations. Zhang et al. (2015a) showed that the response of nematode trophic diversity was sensitive to the residue and tillage effects. Crop rotation sequences including different crop varieties can also influence nematode abundance, diversity and community structure. Ponge et al. (2013) reported that free-living nematodes were more abundant in a lupin-meadow rotation system than in a continuous meadow system, and Turmel et al. (2015) found that maize monocultures was characterized by plant parasites (especially Pratylenchus and Meloidogyne) and a barley-maize rotation was dominated by bacterivores and fungivores. Banana is the main agricultural crop in South China. Plant pathogenic nematode disease caused by long-term monoculture is recognized as the major factor limiting banana production. Zhong et al. (2015a) reported that crop rotation length and the choice of non-host companion crops in the banana rotation can influence population densities of harmful root-lesion nematodes. Furthermore, no-tillage or reduced-tillage practices that increase soil organic matter near the soil surface, compared to conventional tillage, can improve soil structure and soil biological properties in the banana phase of the crop rotation, and enhance banana yield stability (Zhong et al., 2015b). Until now, most studies on soil nematode communities have been focused either on the effects of different crop rotation or on the effects of tillage practices, with little attention to the interactive influence of both over three years. However, rotation and tillage are two important agricultural practices that are usually applied together in the crop fields of many countries. Therefore, the objectives of our study were to analyze the interactive effect of rotation and tillage on soil nematode and microbial community composition under a longterm experimentation in Hainan Island. 2. Materials and methods 2.1. Site descriptions The experiment was carried out on the Wanzhong Farm in the city of Ledong (18 360 18 380 N, 108 470 108 490 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 2065 mm. The test soil was classified as sandy loam according to the USDA texture classification system with 13.6% clay, 23.3% silt and 63.1% sand. The soil has initial properties of 7.12 g kg1 total organic C, 0.76 g kg1 total N, 0.59 g kg1 total P, 1.21 g kg1, total K and pH 6.53. Soil pH was measured in 1:2.5 soil: KCl 1 M solution.
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The experiment was a split-plot design with four replicates, initiated in 2002 with rotation management as the main plot and tillage system as the sub-plot. Detailed information about the treatments is showed in Table 1. The field experiment was divided into eight plots and the size of each individual plot was 170 m2. Rotation management treatments were banana-pineapple rotation (BA) (three years of banana followed by three years of pineapple), banana-papaya rotation (BP) (three years of banana followed by three years of papaya), banana-rice rotation (BR) (three years of banana followed by three years of rice) and banana monoculture (CK). Tillage systems included a no-tillage (NT) and a conventional tillage (CT) treatment. Chemical N fertilizer (urea), P fertilizer (superphosphate) and K fertilizer (sulphate) were applied at the rates of 129 kg N ha1, 68 kg P ha1 and 292 kg K ha1, respectively to a depth of 0–30 cm after transplanting every year. The manure used was cow manure compost (14.4 t ha1), with 53.3% water content, containing 145 g C kg1, 3.2 g N kg1, 2.5 g P2O5 kg1, 1.6 g K2O kg1 on a dry weight basis, which was basally applied before transplanting (June 25th, 2002–2014) to a depth of 0–30 cm every year. Lime was used (125 kg ha1) together with cow manure compost to increase soil pH. Soil in CT was mouldboard ploughed (40 cm deep) at the end of May and the crops of all treatments were re-sown at the end of June. All aboveground crop residues in CT were incorporated into the soil and residues in NT were left on the surface after crops harvest in the middle of May. 2.2. Soil sampling All soil samples were collected at the same time in the last growing season (2014–2015). After the removal of above-ground plant debris, soil samples were collected using a soil corer (3.0 cm diameter) at a depth of 0–40 cm below the soil surface at the seedling stage (September 16, 2014), jointing stage (December 15, 2014), booting stage (March 17, 2015) and ripening stage (May 19, 2015) within the plant 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 placed in individual plastic bags and then immediately stored at 4 C. A subsample of 100 g soil (fresh weight) was used for nematode extraction. Subsamples were first elutriated and sieved (mesh size 250 and 38 mm) 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 per 100 g dry weight soil. Nematodes were counted using a dissecting microscope and identified using an inverted compound microscope. An average of 150 nematodes (100 nematodes at minimum) per sample were identified at 400 to 1000 magnification to genus or family level within one week of extraction or fixed in 4% formalin until identification. Nematodes were classified into the following trophic groups (Bongers, 1988): bacterivores (BF), fungivores (FF), plant parasites (PP) and omnivores-predators (OP). Phospholipid fatty acids (PLFA) were used as indicators of total, bacterial and fungal biomass in the soil. Lipids were extracted from
Table 1 Description and site history of different treatments in the study area of a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Treatment
Crops
Planting Year
Monoculture (CK) Rotation 1 (BA) Rotation 2 (BP) Rotation 3 (BR)
banana banana and pineapple banana and papaya banana and rice
June 2002–May 2014 Banana: June 2002–May 2005 and June 2008–May 2011; pineapple: June 2005–May 2008 and June 2011–May 2014. Banana: June 2002–May 2005 and June 2008–May 2011; papaya: June 2005–May 2008 and 2011–May 2014. Banana: June 2002–May 2005 and June 2008–May 2011; rice: June 2005–May 2008 and June 2011–May 2014.
Note: In each rotation and monoculture plot, a no-tillage and a conventional tillage treatment were applied.
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8 g of freeze-dried soil using a chloroform–methanol–citrate buffer mixture (1:2:0.8). The polar lipids were separated from neutral lipids and glycolipids on a solid phase extraction column (Supelco Inc., Bellefonte, PA). The phospholipids were trans-esterified with a mild-alkali methanolysis and the resulting fatty acid methyl esters were extracted in hexane and dried under N2. Samples were then dissolved in hexane and analyzed on an Agilent 6850 series Gas Chromatograph with MIDI peak identification software (Version 4.5; MIDI Inc., Newark, DE). The following biomarkers were used: Total PLFAs (sum of all identified PLFAs; from C14 to C20); bacterial
PLFA (iso 15:0, anteiso 15:0, 15:0, iso 16:0, 16:1v5c, iso 17:0, anteiso 17:0, 17:0cy, 17:0 and 19:0cy); fungal PLFA (18:2v, 6 and 9c) (Guckert et al., 1985). 2.3. Statistical analysis Nematode ecological indices were analyzed using the following approaches: Shannon-Weaver diversity (H', Shannon, 1948) was P calculated as H' = Pi (ln Pi), where Pi is the proportion of each of the i genera present. Species richness (SR) was calculated
Table 2 Average contribution (%) of different nematode genera to total soil nematode abundances in rotation and tillage treatments of a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Genus
CK
BA
BP
BR
Guilds
Tillage
RT
Ba1 Ba1 Ba1 Ba1 Ba2 Ba2 Ba2 Ba2 Ba2 Ba2 Ba2 Ba3 Ba3 Ba3 Ba3 Ba3 Ba4
(R) ns 0.045 0.033 <0.01 0.047 ns ns <0.01 ns <0.01 ns ns <0.01 ns ns <0.01 <0.01
(T) ns <0.01 0.018 ns ns ns 0.022 0.048 ns ns ns ns 0.029 ns ns ns <0.01
ns 0.034 ns ns ns ns ns 0.027 ns ns ns ns <0.01 ns ns ns <0.01
22.1 2.9 10.9** 2.4 3.8 2.1
Fu2 Fu2 Fu2 Fu4 Fu4
ns <0.01 ns <0.01 0.039
ns ns ns 0.041 ns
ns ns ns <0.01 ns
23.3 0.3 0.9 2.8 0.0 3.6 1.8 4.3 2.5 2.3 3.6 1.2
24.9 1.4 0.0 0.5 0.3 5.3* 0.7 5.1* 1.0 3.4 5.0* 2.2
Ca4 Ca4 Om4 Om4 Om4 Om4 Ca5 Ca5 Om5 Om5 Om5
ns ns 0.026 ns ns ns ns ns 0.013 <0.01 <0.01
<0.01 0.025 ns ns ns 0.027 ns ns <0.01 <0.01 <0.01
ns ns ns ns ns ns ns ns ns 0.040 0.046
12.7 1.5 3.4 0.9 1.7 0.0 1.3 0.0 0.0 0.0 2.0 0.0 1.9 0.0 0.0
8.1 1.3 1.3 0.6 1.8 0.0 1.1 0.0 0.0 0.0 0.8 0.0 1.2 0.0 0.0
PP2 PP2 PP2 PP2 PP2 PP3 PP3 PP3 PP3 PP3 PP3 PP3 PP3 PP4
ns ns ns ns 0.046 0.023 0.032 <0.01 <0.01 <0.01 <0.01 0.043 <0.01 0.035
ns ns 0.016 ns ns 0.025 ns ns ns 0.011 ns ns 0.020 ns
ns ns ns ns ns ns ns ns ns <0.01 ns ns 0.045 ns
NT
CT
NT
CT
NT
CT
NT
19.4 2.9 4.1 0.0 0.0 0.0 3.7 0.0 4.5 0.0 1.1 0.0 0.0 0.0 0.0 1.9 0.0 1.2
21.3 2.4 3.8 0.0 0.0 0.0 2.6 0.0 5.7* 0.0 0.9 0.0 1.4 0.0 0.0 1.6 0.0 2.9
41.1 1.8 5.2b)* 1.8 2.2 0.6 2.8 2.1 6.1* 0.0 3.4 0.0 0.6 2.4 0.0 2.0 4.6 4.5
42.7 3.4 3.9 2.3 2.1 2.7 1.9 0.0 10.0** 1.3 2.2 0.0 0.7 1.2 0.8 1.8 3.1 5.2*
42.2 2.9 5.8* 0.8 2.4 1.3 2.6 2.7 6.6* 0.0 3.2 0.9 0.0 2.3 1.1 1.0 4.5 4.1
43.6 2.6 4.7 1.8 3.1 0.9 2.2 1.6 6.3* 1.5 2.9 0.0 0.9 3.4 0.9 1.6 3.8 5.4*
43.8 3.7 5.3* 1.6 3.2 0.8 1.7 0.2 10.0** 0.0 2.5 0.9 0.0 3.2 2.4 1.3 2.8 4.2
44.9 2.7 4.2 2.5 1.4 2.5 3.3 3.7 5.9* 2.2 4.1 0.8 1.2 2.1 1.1 0.7 3.3 5.2*
8.5 1.9 3.3 2.6 0.7 0.0
10.4 2.6 4.4 3.4 0.0 0.0
19.0 2.1 10.8** 2.0 2.9 1.2
20.3 2.3 10.2** 3.2 3.5 1.1
16.2 1.8 6.6* 3.9 2.3 1.6
17.4 2.6 5.2* 3.3 3.7 2.4
20.2 1.9 10.5** 3.7 3.3 1.8
Omnivore–carnivores Mononchus Nygolaimus Thonus Eudorylaimus Epidorylaimus Microdorylaimus Prodorylaimus Mesodorylaimus Aporcelaimellus Paractinolaimus Discolaimus
12.6 1.1 0.0 0.0 0.5 4.4 1.7 3.9 1.0 0.0 0.0 0.0
14.9 2.2 0.0 0.0 0.9 4.0 0.0 4.5 0.8 1.0 0.8 0.7
25.1 0.9 0.0 3.2 2.8 4.3 2.6 3.8 0.0 2.1 3.9 1.5
26.8 2.1 0.4 1.8 0.0 5.2* 0.6 5.3* 0.0 3.5 5.1* 2.8
23.4 0.6 1.7 2.0 0.0 4.3 2.8 2.9 0.0 2.5 4.2 2.4
25.5 1.9 0.8 2.3 0.2 5.1* 0.9 2.8 0.0 3.2 5.2* 3.1
Plant parasites Boleodorus Basiria Malenchus Tylenchus Paratylenchus Psilenchus Tylenchorhynchus Helicotylenchus Rotylenchus Rotylenchulus Pratylenchus Hirschmanniella Meloidogyne Dorylaimellus
59.5 1.8 2.6 0.0 3.7 2.3 0.0 0.0 11.8** 5.7* 11.5** 6.3* 0.0 11.2** 2.6
53.4 2.3 2.2 0.8 2.4 2.8 0.0 0.0 10.5** 5.2* 10.1** 5.0* 0.0 10.3** 1.8
14.8 2.2 1.7 0.0 2.1 1.3 0.8 0.0 2.3 3.4 0.0 0.0 0.0 0.0 1.0
10.2 1.7 1.9 0.0 1.3 1.5 0.0 0.0 1.4 1.5 0.0 0.0 0.0 0.0 0.9
18.2 1.8 2.4 1.1 3.9 2.2 0.0 1.7 1.5 0.0 1.1 0.0 1.2 1.4 0.0
13.5 1.4 1.5 0.3 2.6 1.3 0.0 1.3 1.7 0.0 0.0 0.0 2.1 0.9 0.0
Fungivores Ditylenchus Aphelenchus Aphelenchoides Dorylaimoides Tylencholaimus
Effects Rotation
CT Bacterivores Mesorhabditis Protorhabditis Panagrolaimus Monhystera Eucephalobus Heterocephalobus Acrobeles Acrobeloides Cervidellus Plectus Wilsonema Domorganus Chronogaster Leptolaimus Pseudoaulolaimus Prismatolaimus Alaimus
a)
Note: BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. a) Functional guilds of soil nematodes characterized by feeding habits and life-history characters, numbers following the functional guilds indicate the c-p values (Bongers and Bongers, 1998; Ferris et al., 2001); b) ** dominant genus, average contribution (%) of different nematode genera to total soil nematodes is more than 10%; * subdominant genus, average contribution (%) is over 5%.
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according to Ferris et al. (2001). Maturity index (MI) was calculated P as P(i)C(i), where C(i) is the colonizer-persister (c-p) rating of taxon i according to the 1–5 c-p scale of Bongers and Bongers (1998). 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), basal index (BI) and channel index (CI) are indicators for soil food web structure and condition (indicating functional diversity), and were calculated according to the method of Ferris et al. (2001). The colonizerpersister (cp) values for taxa were adopted from Bongers (1990) and Bongers and Bongers (1998). The nematode metabolic footprint (NMF) was calculated as P NMF = (Nt (0.1Wt/mt + 0.273 (W0.75))), where Wt and mt represent the body weight and colonizer-persister (cp) values of genus t, respectively. The enrichment footprint (efoot) is the metabolic footprint of lower trophic levels (cp 1–2) while the structure footprint (sfoot) represents the metabolic footprint with the higher cp value (3–5) (Ferris, 2010). Functional metabolic footprint (FMF) was calculated as (Fs Fe)/2 with complex mg2 units (Ferris, 2010), where Fs is the sum of standardized C labile by structure indicator taxa and Fe is the sum of standardized C labile by enrichment indicator taxa. The magnitudes of C and energy flow through the bacterial, fungal and herbivory channels are represented as bacterial footprints (BFfoot), fungal footprints (FFfoot), and herbivore footprints (PPfoot), the C utilization coefficient, for bacterial-, fungal- and plant-feeding nematodes. Nematode abundances, different trophic metabolic footprints and microbial abundances were ln (x + 1) transformed prior to statistical analysis to obtain normality of data. Repeated measures analysis of variance was used to test the overall effect of rotation, tillage and sampling stage on soil biota. Separate one-way analysis of variance was used to test the effects of rotation and tillage on soil biota at each sampling stage and means were compared by least significant difference. Bivariate correlation analysis was used to test the significance of correlations between soil nematode abundance or ecological index and soil microbial biomass. All statistical analyses were performed by SPSS statistical software
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(SPSS Inc., Chicago, IL, USA). Difference at P < 0.05 level was considered to be statistically significant. 3. Results 3.1. Soil nematode abundance In the eight treatments studied, forty-seven nematode genera were observed, with the highest value in BPNT (40) and lowest in CKCT (25); 36 and 35 genera were found in BANT and BACT, respectively, and 39 and 37 genera in BRNT and BRCT, respectively (Table 2). Among the identified nematode genera, Acrobeloides in BANT and BRCT, Aphelenchus in BANT, BACT, BRNT and BRCT, Helicotylenchus, Rotylenchulus and Meloidogyne in CKNT and CKCT were the dominant genera (relative abundance >10%). Protorhabditis in BACT, BPCT and BRCT, Alaimus, Epidorylaimus and Paractinolaimus in BANT, BPNT and BRNT, Prodorylaimus in BANT and BRNT, Pratylenchus and Rotylenchus in CKNT and CKCT were the subdominant genera (relative abundance >5%, Table 2). The bacterivores including Acrobeloides, Monhystera, Plectus, Chronogaster, Prismatolaimus and Alaimus and fungivores including Aphelenchus and Dorylaimoides were greatly influenced by rotation, with relatively higher abundances in BA, BP and BR than in CK (P < 0.01). Omnivores-predators such as Mononchus, Paractinolaimus, Aporcelaimellus and Discolaimus were strongly affected by tillage, with higher relative abundances in NT and lower in CT (P < 0.01, Table 2). Significant rotation (R), tillage (T) and growth stage (S) effects were observed on the number of total nematodes (P < 0.05, Table 3). During the study period, the total number of nematodes fluctuated obviously among different treatments (Fig. 1), with the highest value (869 individuals 100 g1 dry soil) in BPNT at booting stage, and the lowest (358 individuals 100 g1 dry soil) in CKCT at seedling stage. In rotation systems, the total number of nematodes was on average 37.3%, 41.5% and 39.7% higher in BA, BP and BR, respectively compared with CK. In tillage systems, the total number of nematodes was on average 12.1% higher in the NT compared with the CT.
Table 3 Two-way ANOVA table of P values showing the significance of the effects of different crop rotation and tillage practices on soil biota in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. ANOVA
Rotation (R) P value
Tillage (T) P value
Stage (S) P value
RT P value
RS P value
TS P value
RTS P value
TNEMA BF FF OP PP TP BP FP H' SR MI PPI BI CI EI SI BFfoot FFfoot PPfoot Efoot Sfoot
<0.01 <0.01 <0.01 0.039 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 0.013 <0.01 <0.01 <0.01 <0.01 0.021 <0.01 <0.01 <0.01 <0.01
0.048 0.023 0.036 <0.01 0.042 <0.01 <0.01 <0.01 <0.01 <0.01 0.018 <0.01 <0.01 0.011 <0.01 0.027 <0.01 <0.01 <0.01 <0.01 <0.01
<0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 ns <0.01 <0.01 0.012 ns <0.01 <0.01 ns ns <0.01 <0.01 ns
ns ns ns <0.01 ns <0.01 ns ns <0.01 <0.01 <0.01 <0.01 <0.01 0.019 0.040 <0.01 ns 0.045 <0.01 0.016 <0.01
ns <0.01 <0.01 0.043 <0.01 ns <0.01 <0.01 <0.01 ns <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 ns ns ns ns <0.01
ns ns ns ns ns ns ns ns <0.01 ns 0.036 <0.01 ns <0.01 <0.01 ns ns ns 0.022 0.047 ns
ns ns ns ns ns ns ns ns <0.01 ns <0.01 <0.01 <0.01 0.025 <0.01 <0.01 ns ns ns ns ns
Note: TNEMA, total nematodes; BF, bacterivores; FF, fungivores; OP, omnivore-predators; PP, Plant parasites; TP, total PLFAs; BP, bacterial PLFA; FP, fungal PLFA; H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
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Fig. 1. The abundance of nematodes and phospholipid fatty acids (PLFA) under rotation and tillage treatments at four sampling stages in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. A, total nematodes; B, bacterivores; C, fungivores; D, omnivore-predators; E, plant parasites; F, total PLFAs; G, bacterial PLFA; H, fungal PLFA. Error bars indicate standard error. Different lower case letters in the figure mean significant difference according to Ducan’s multiple range test (P < 0.05).
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Fig. 2. Nematode ecological indices in rotation and tillage treatments at four sampling stages in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
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Significant rotation, tillage and growth stage effects were observed on the numbers of bacterivores, fungivores, omnivore– carnivores and plant parasites (P < 0.05). A significant interaction effect of S R on bacterivores, fungivores and plant parasites and of R T on omnivore–carnivores was observed (P < 0.01). At the booting stage, the numbers of bacterivores, fungivores and plant parasites were higher compared to the other stages. At the jointing, booting and ripening stages, BRNT and BPNT showed higher numbers of omnivore–carnivores, followed by BANT, BRCT and BPCT, while CKNT and CKCT had the lowest numbers. Different kinds of crop rotation increased the numbers of bacterivores, fungivores and omnivore–carnivores, but decreased that of plant parasites (P < 0.01). However, the continuous cropping expanded the number of plant parasites, while it reduced other forms (P < 0.05). In terms of rotation treatments, BA had the highest number of plant parasites and lowest number of bacterivores, fungivores and omnivore–carnivores; BP had the highest number of bacterivores and fungivores; BR had the highest number of omnivore–carnivores and the lowest number of plant parasites. In tillage systems, the numbers of bacterivores, fungivores and omnivore–carnivores were much higher in NT and lower in CT, but the number of plant parasites was much lower in NT than in CT (P < 0.01, Fig. 1).
that of PPfoot was much lower in NT than in CT (P < 0.01, Fig. 2). FMF is the total area of the enrichment and structure footprints as illustrated in Fig. 3. In rotation systems, the FMF was greater in BA, BP and BR than in CK, and in tillage systems it was much higher in NT than in CT. All plots in BANT, BPNT and BRNT were located in quadrat B and almost half of the plots in BACT, BPCT and BRCT were located in quadrat C, whereas all plots in CKNT and CKCT were clustered in quadrat D of the FMF figure. 3.4. Correlations of soil nematode and microbial communities The total number of nematodes, the numbers of bacterivores, fungivores, omnivore–carnivores and the value of H' were positively correlated with the concentrations of total PLFAs, bacterial PLFA and fungal PLFA (P < 0.01, Table 4). However, the number of plant parasites and the values of PPI and PPfoot were negatively correlated with the concentrations of total PLFAs, bacterial PLFA and fungal PLFA (P < 0.01). The values of SR, EI, FFfoot and efoot were positively correlated with the concentrations of bacterial PLFA and fungal PLFA (P < 0.05). 4. Discussion 4.1. Changes of soil nematode and microbial communities
3.2. Soil microbial communities Significant rotation, tillage and growth stage effects were observed on the abundance of specific microbial groups by using indicative PLFA biomarkers (P < 0.01, Table 3). In rotation systems, the concentrations of total PLFAs, bacterial PLFA and fungal PLFA varied in a range of 13.5–46.2, 11.4–37.1 and 2.6–6.3 nmol g1 dry soil, respectively, with the following order: CK < BA < BR < BP. In tillage systems, these PLFA concentrations were on average 18.8%, 17.5% and 13.7%, respectively higher in the NT than in the CT. During the study period, the abundance of microbial functional groups increased with crop maturity. At the booting and ripening stages, the concentrations of total PLFAs, bacterial PLFA and fungal PLFA were higher compared to the seedling and jointing stages. This was true among all treatments (Fig. 1).
Both crop rotation and tillage treatments influenced nematode density and diversity over the 12-year period, although the rotation effect was the main source of data variation. The total nematode abundance was much greater in BA, BP and BR than in CK during the seedling, jointing, booting and ripening stages. The result was consistent with a recent study that compared barley monoculture with sugar beet-barley rotation (Quist et al., 2015).
CKCT
BACT
BPCT
BRCT
CKNT
BANT
BPNT
BRNT
100.0
A
B
D
C
Significant rotation, tillage and growth stage effects were observed on the values of H', SR, MI, PPI, BI, CI, EI and SI (P < 0.01, Table 3). Except SR, interactive effect of R T S was observed for all ecological indices (P < 0.05). The values of almost all ecological indices in rotation and tillage were significantly higher at the booting stage followed by the ripening stage, while the jointing stage and the seedling stage had the lowest values. In the rotation systems, higher H', SR, MI, EI and SI and lower PPI, BI and CI values were obtained in BA, BP and BR compared with CK (P < 0.05). BA had the highest values of PPI, BI and CI and the lowest values of H', SR, MI, EI and SI; BP had the highest values of H' and SR and the lowest values of BI and CI; BR had the highest values of MI, EI and SI and the lowest values of PPI. In tillage systems, the values of H', SR, MI, EI and SI were on average 36.2%, 28.9%, 35.1%, 33.2% and 46.7%, respectively higher in NT compared with CT, whereas those of PPI and CI showed the opposite trend, being 29.3% and 38.4% lower in NT than in CT. At jointing, booting and ripening stages, rotation effect on FFfoot, PPfoot and efoot, tillage effect on FFfoot and sfoot, and effects of the interaction of R T on PPfoot and efoot were all significant (P < 0.05). In the rotation system, greater values of BFfoot, FFfoot, efoot, sfoot and lower PPfoot values were observed in BA, BP and BR than in CK (P < 0.05). In the tillage system, BFfoot, FFfoot, efoot, sfoot were much higher in NT and lower in CT, but
Enrichment Footprint
3.3. Soil nematode ecological indices
50.0
0.0 0.0
50.0
100.0
Structure Footprint Fig. 3. Functional metabolic footprint of nematodes subjected to rotation and tillage effects in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. The vertical axis and horizontal axis of each footprint represent enrichment footprint and structure footprint respectively. The functional metabolic footprint is described by the sequentially joining points: (SI 0.5Fs, EI); (SI, EI + 0.5Fe);05Fe); (SI + 0.5Fs,05Fs, EI); (SI, EI 0.5Fe). Fs and Fe represent structure footprint and enrichment footprint, respectively. The nematode functional metabolic footprint is the total area of the two functional (enrichment and structure) footprints (Ferris 2010).
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Table 4 Pearson’s correlation coefficients between soil nematode and microbial community indicators in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Indicators
Total PLFAs
Bacterial PLFA
Fungal PLFA
Indicators
Total PLFAs
Bacterial PLFA
Fungal PLFA
TNEM BF FF OP PP H' SR MI PPI
0.762** 0.684** 0.686** 0.522** 0.520** 0.426** 0.103 0.163 0.416**
0.742** 0.661** 0.717** 0.501** 0.533** 0.465** 0.212* 0.158 0.378**
0.669** 0.715** 0.593** 0.538** 0.574** 0.506** 0.332* 0.183 0.399**
BI CI EI SI BFfoot FFfoot PPfoot Efoot Sfoot
0.188 0.151 0.105 0.191 0.216* 0.196 0.288* 0.156 0.302*
0.176 0.147 0.211* 0.215* 0.503** 0.231* 0.426** 0.266* 0.113
0.129 0.172 0.234* 0.184 0.424** 0.395* 0.399* 0.347* 0.195
Note: TNEM, number of total nematodes; BF, bacterivores; FF, fungivores; OP, omnivores-predators; PP, plant-parasites; H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
This suggests that the greater variety of organic matter input in crop rotations than in monocultures can increase the abundance and diversity of soil nematodes. In contrast with banana residue, the pineapple, papaya and rice residues included in our study are rich in biodegradable sugars and proteins but poor in cellulose and hemicelluloses (Williams et al., 2014). Thus crop rotations provide the easily-utilizable resource for soil microbes and nematodes. As far as crop rotation was concerned, BP had higher total nematode numbers compared with BA and BR. This could be due to the concentration and type of organic compounds released by the roots of papaya which reduced soil-borne pathogens and maintained higher nutrient levels for nematode development (Daniel et al., 2014). In our study, rotations containing a pineapple, papaya or rice phase significantly reduced populations of plant parasites, which is consistent with Chavez et al. (2014) in a 6-year cotton-clover-cornrye rotation. Initially, the plant parasite taxa constituted 56.5% of the total nematode population under banana monoculture, but after rotation, the proportion of plant parasites declined sharply to 15.9% for pineapple, 12.5% for papaya and only 10.4% for rice (Fig. 1). This suggests that crop rotations, especially rice plots that are flooded (anaerobic, higher soil moisture and lower temperatures), have a suppressive effect on plant parasite populations which associated with suppressed root growth (Song et al., 2016). The abundance of bacterivorous and fungivorous nematodes was markedly higher in the BA, BP and BR than in the CK. As for different rotation treatments, BP had the highest abundance of bacterivores and fungivores, followed by BA and BR. The result is inconsistent with a recent observation that a ley-vegetable rotation did not affect the abundance of bacterivores and fungivores (Ugarte et al., 2013). This suggests that the rotation period in the study of Ugarte et al. (2013) was not long enough to allow recovery of the soil nematodes from the long-term monoculture. Our results showed more abundant microbial populations, effective organic matter decomposition and higher soil fertility in rotation systems compared with monoculture over a long time period, caused by the large input of organic amendments and crop residues (Wang et al., 2015). The differences between pineapple, papaya and rice rotations might be due to the improved soil structure, stabilized microclimate, greater rhizosphere microbial populations and higher root density generally found in banana-papaya rotation compared with banana-pineapple and banana-rice rotation (Qian et al., 2014). The abundance of omnivores-predators was much higher in NT than in CT. Similarly, Zhang et al. (2013) found a greater abundance of omnivores-predators in a maize-soybean residues incorporated no-tillage compared with conventional tillage. This indicated that the positive effects of limiting physical disturbance such as antiabrasion and improvements to soil texture and residue could stir
up increases in the abundance of larger-bodied nematode fauna since they are especially sensitive to soil disruption (Ito et al., 2015a). The recovered omnivores-predators in this study included Mononchus, Epidorylaimus, Paractinolaimus, Aporcelaimellus and Discolaimus which had colonizer-persister (cp) values of cp-4 and cp-5. These values place them in a K-strategist located category in the higher trophic level of the soil food web and thus would be expected to be less prevalent in soils that are disturbed or conventionally-tilled. Our results therefore corroborate earlier reports (Zhao et al., 2015). In rotation systems, the composition of soil microbial communities was altered by the different rotations, with a much higher abundance of bacteria and fungi in BA, BP and BR than in CK, and much higher abundances in BP than in BR and BA. A close association between bacteria, fungi and rotations was also reported by Chen et al. (2014) in a crops-grassland rotation system with a sandy loam texture. They concluded that the crop rotation provides better soil hydrological conditions, effective rhizodepositions and residual fertility which usually stimulate high proportion of soil microorganisms. Yuan et al. (2015) also suggested that the differences in quantity, quality and distribution of papaya residues generally lead to greater concentrations and diversity of organic materials, and thus, to higher soil microbe viability, and accelerated carbon and nutritional cycling compared with pineapple and rice. In tillage systems, the abundance of primary decomposers, such as bacteria and fungi was much greater in NT than in CT, which was instantiated by the higher abundance of bacterivores and fungivores in NT compared with CT (Fig. 1). Mloza-Banda et al. (2016) gained a similar observation in a 5-year tobacco-cotton rotation combined with conservation. They attributed their findings partly to the changes in the soil environment caused by no-tillage, including soil structure and density, soil pH, and nutrient cycles within the soil profile, and partly to the accumulation of crop residues at the surface which produces less soil disturbance, high plant litter quantity, intensive and deep rooting and decreasing percolation water with N nutrients in no-tillage soils. 4.2. Changes of soil nematode ecological indices The ecological indices of H', SR, MI and PPI are often used to assess the soil condition. H' and SR are linked to the diversity of soil nematodes, MI and PPI can reflect the disturbance by human activities due to crop rotations and tillage (Djigal et al., 2012). In this study, the values of H', SR and MI were higher in BA, BP and BR than in CK, which indicates a trend of greater soil nematode biodiversity and a relatively stable environment in banana rotations. We did not find significant seasonal effects on SR which suggests that the soil nematode species richness fluctuated only
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slightly with banana growth. The highest PPI values were observed under banana monoculture in both NT and CT systems. During the growing season, Helicotylenchus, Rotylenchus, Rotylenchulus, Pratylenchus and Meloidogyne with c-p3 were dominant genera in CK and accounted for approximately 40% of total soil nematodes, which probably led to CK exhibiting the highest PPI values (Liu et al., 2016). Weighted indices, such as BI, CI, EI and SI, may provide information about the nematode community structure in stressed, enriched, stable structured and rapidly degraded environments, and indicate the dynamics of soil food webs (Ferris and Tuomisto, 2015). In this study, banana rotations with various residue additions generally contained more bacterivores and fungivores, which resulted in a higher EI, and lower BI compared to banana monoculture with a single residue input. Furthermore, higher EI and SI but lower BI in BP than in BA and BR were also observed, which is in agreement with a recent study that compared wheat monoculture with maize-rice-wheat rotation (Malherbe and Marais, 2015). Papaya has more extensive rooting systems than pineapple and rice, therefore a papaya rotation system may provide greater amounts of plant residues of varying degrees of degradability that would support greater microbial biomass compared to pineapple and rice systems (Silva et al., 2014). The lower values of CI in BA, BP and BR than in CK indicate that the bacterial decomposition pathway was relatively more dominant in banana-based rotations and played a more important role in nutrient cycling and nutrient supply to plants. The fungal decomposition pathway, which was relatively important in monoculture, often reflects lower rates of decomposition (Liu et al., 2015). The extremely high SI values in no-tillage may be due to the enrichment of omnivore–carnivores, which are sensitive to disturbance and need more time to establish than the more rapidly growing bacterivores and fungivores (Dang et al., 2015). Nematode faunal analysis inferred by EI and SI indicate that the soil food webs in NT were less disturbed, more stable and structured due to the increasing of free-living nematodes, while the soil food webs in CT were degraded due to stressed soil surroundings. Roth et al. (2015) also suggested that the soil food web was more complex in organic reduced- and no-tillage systems with high EI and SI values. In this study, nematode metabolic footprints were used to provide information about the structure and function of the soil food web under different agricultural management practices. Higher BFfoot and FFfoot but lower PPfoot were found in rotation and no-tillage systems, suggesting greater flow of resources into the food web through bacterivorous and fungivorous channels than through herbivory channels. In rotation systems, higher efoot and sfoot were found in BA, BP and BR than in CK, as also reported by Zhang et al. (2015b) in a corn-soybean rotation. This shows that a large variety of cover crops is an important determinant of the nature and magnitude of soil food web services and that soil nematodes as significant regulators of food web have decisive influence on residue decomposition and nutrients in ecosystems. In tillage systems, the values of efoot and sfoot were larger in NT than in CT, and significant correlations were found between the numbers of omnivores-predators and the abundance of bacterivores (r = 0.363, P < 0.05) and fungivores (r = 0.516, P < 0.01). The results are consistent with the study of Ito et al. (2015b) in a ricesoybean-maize rotation under different tillage practices. The relatively high efoots in the NT showed the enhancing productivity and turnover rates of the enrichment indicators in this system to maintain metabolic balance. The same variation trend of sfoot indicates an increasing metabolic activity of the predators, which may be related to the increased top-down predation pressure in the no-tillage system relative to the conventional tillage system.
5. Conclusion Our study shows that rotation and no-tillage practices promote the abundance of most nematodes and microbial biomass. Nematode trophic footprints respond more actively to rotation than tillage impacts and offer more information on carbon, nitrogen and energy entering the soil food webs. The application of tillage practices in a rotation system may result in a bacterialdominated decomposition pathway. Nematode community analysis indicates that a banana-based rotation system provides a more diverse residue resource entry into soil food webs, and that a no-tillage system is beneficial for soil ecosystem stability and sustainability. Furthermore, Hainan Island may provide baselines for other tropical situations. This initial inventory could also be used to assess the soil environment in a tropical monsoon climate according to agricultural practices. Acknowledgement This research was supported by the National Natural Science Foundation of China to S. Zhong (41301277), the Natural Science Foundation of Hainan Province to S. Zhong (310073) and the State Scholarship Fund of China to S. Zhong (201503260016). References Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Appl. Soil Ecol. 10, 239–251. Bongers, T., 1988. De Nematoden van Nederland [M]. KNNV Bibliotheekuitgave 46, Pirola, Schrool, Netherlands, 1988, 408pp. Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19. Chavez, H., Taylor, C.R., Rodríguez-Kábana, R., 2014. Population dynamics and interactions between plant parasitic and non-parasitic nematodes: an empirical analysis. Appl. Soil Ecol. 78, 11–17. Chen, X.Y., Daniell, T.J., Neilson, R., O'Flaherty, V., Griffiths, B.S., 2014. Microbial and microfaunal communities in phosphorus limited, grazed grassland change composition but maintain homeostatic nutrient stoichiometry. Soil Biol. Biochem. 75, 94–101. Costa, C.H.M., Crusciol, C.A.C., 2016. Long-term effects of lime and phosphogypsum application on tropical no-till soybean–oat–sorghum rotation and soil chemicalproperties. Eur. J. Agron. 74, 119–132. Cunha, T.P.L., Mingotte, F.L.C., Chiamolera, F.M., Carmeis, A.C.D., Soares, P.L.M., Lemos, L.B., Vendramini, A.R., 2015. Occurrence of nematodes and yield of common bean and maize as a function of cropping systems under no-tillage. Nematropica 45, 34–42. Dang, Y.P., Seymour, N.P., Walker, S.R., Bell, M.J., Freebairn, D.M., 2015. Strategic tillage in no-till farming systems in Australia’s northern grains-growing regions: i. Drivers and implementation. Soil Tillage Res. 152, 104–114. Daniel, M.D., Grandy, A.S., Tiemann, L.K., Weintraub, M.N., 2014. Crop rotation complexity regulates the decomposition of high and low quality residues. Soil Biol. Biochem. 78, 243–254. Djigal, D., Chabrier, C., Duyck, P.F., Achard, R., Quénéhervé, P., Tixier, P., 2012. Cover crops alter the soil nematode food web in banana agroecosystems. Soil Biol. Biochem. 48, 142–150. Ferris, H., Tuomisto, H., 2015. Unearthing the role of biological diversity in soil health. Soil Biol. Biochem. 85, 101–109. 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. Ferris, H., 2010. Form and function: metabolic footprints of nematodes in the soil food web. Eur. J. Soil Biol. 46, 97–104. Forge, T.A., Larney, F.J., Kawchuk, L.M., Pearson, D.C., Koch, C., Blackshaw, R.E., 2015. Crop rotation effects on Pratylenchus neglectus populations in the root zone of irrigated potatoes in southern Alberta. Can. J. Plant. Pathol. 37, 363–368. Gu, Y.F., Zhang, T., Che, H., Lu, X.X., Du, Y.Q., 2015. Influence of returning corn straw to soil on soil nematode communities in winter wheat. Acta Ecol. Sin. 35, 52–56. Guckert, J.B., Antworth, C.P., Nichols, P.D., White, D.C., 1985. Phospholipid, esterlinked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microb. Ecol. 31, 147–158. Ito, T., Araki, M., Komatsuzaki, M., Kaneko, N., Ohta, H., 2015a. Soil nematode community structure affected by tillage systems and cover crop managements in organic soybean production. Appl. Soil Ecol. 86, 137–147. Ito, T., Araki, M., Higashi, T., Komatsuzaki, M., Kaneko, N., Ohta, H., 2015b. Responses of soil nematode community structure to soil carbon changes due to different tillage and cover crop management practices over a nine-year period in Kanto, Japan. Appl. Soil Ecol. 89, 50–58.
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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Response of soil nematode community composition and diversity to different crop rotations and tillage in the tropics Zhong Shuanga,b,1,* , Zeng Hui-caic , Jin Zhi-qianga a b c
Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102, China Hainan Key Laboratory of Banana Genetic Improvement, Hainan, Haikou 570102, China Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Science, Haikou 570101, China
A R T I C L E I N F O
Article history: Received 9 February 2016 Received in revised form 13 May 2016 Accepted 19 May 2016 Available online xxx Keywords: Nematodes Community composition Tillage Rotation Monoculture Metabolic footprint
A B S T R A C T
Soil nematode community composition and diversity response to banana-pineapple (BA), bananapapaya (BP), banana-rice (BR) rotations and banana monoculture (CK) (12-year annual crops) under no-tillage (NT) and conventional tillage (CT) were assessed in the Wanzhong Farm in Hainan Island, China. Soil samples were taken at depth of 0–40 cm in 2014–2015. A total of 47 nematode genera with relative abundance over 0.1% were identified. Acrobeloides in BANT and BRCT, Aphelenchus in BANT, BACT, BRNT and BRCT, Helicotylenchus, Rotylenchulus and Meloidogyne in CKNT and CKCT were the dominant genera. In comparison with CK, BA, BP and BR increased the number of bacterivores, fungivores and omnivore–carnivores, and the concentration of bacterial PLFA and fungal PLFA. The no-tillage soils favored bacterivores, fungivores and high colonizer-persister (c-p) value omnivores and carnivores, but reduced plant parasites. Soil food web in the rotation combined with no-tillage systems was highly structured, mature and moderately enriched as indicated by Structure (SI), Maturity (MI) and Enrichment (EI) index values, respectively. Higher number of bacterivores and lower values of Channel index (CI) suggested bacterial-dominated decomposition in no-tillage soil. Soil nematode diversity and functional metabolic footprint were much greater after 12 years of crop rotation. The descriptive indicators were useful to provide insight into the effect of rotation and tillage, and the evaluative indicators were more comprehensive for interpreting the structure and function of the soil food web under different crop rotations and tillage. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction In agroecosystems, agricultural practices such as crop rotation, residue addition and no-tillage or reduced-tillage are beneficial for sustainable crop production due to their positive influences on soil physicochemical properties, microbial activity and biomass, and the composition and function of soil biota (Cunha et al., 2015; Kibet et al., 2016). For example, crop rotation can increase the input of organic C and N into the soil, which enhances soil fertility (Costa and Crusciol, 2016). When high amounts of crop residues are returned to the soil, crop rotation can influence the soil microbial habitat, improve soil structure (Meena et al., 2015), and increase
* Corresponding author at: Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570102, China. E-mail address: [email protected] (S. Zhong). 1 Supported by the National Natural Science Foundation of China to S. Zhong (41301277), the Natural Science Foundation of Hainan Province to S. Zhong (310073) and the State Scholarship Fund of China to S. Zhong (201503260016). http://dx.doi.org/10.1016/j.apsoil.2016.05.013 0929-1393/ã 2016 Elsevier B.V. All rights reserved.
biomass and diversity of soil fauna (Zhang et al., 2016). In addition, no-tillage involving surface crop residue application has been adopted as a means to promote soil aggregate stability and fertility, while simultaneously increasing the abundance and viability of soil biota (Ontl et al., 2015). Composition and abundance of nematode fauna in agricultural soils are receiving increased 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 predators-omnivores based on their feeding habits. Each nematode 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 the numbers of these two trophic groups reflects the decomposition of organic matter and mineralization of nitrogen and carbon (Gu et al., 2015). Omnivores-predators are most sensitive to environmental disturbances resulting from changes in land use, which are higher in a natural land than in
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a disturbed agricultural land (Viketoft et al., 2011). Plant parasites attack many field crops and cause serious economical damage (Waweru et al., 2014). Higher population density and diversified structure of nematode communities should be widely used as a powerful ecological tool to assess soil condition as they respond to changes in the soil environment. Considering these indicative functions, many researchers have reported how soil nematodes respond to agricultural practices. For example, Forge et al. (2015) showed that in comparison with conventional tillage, no-tillage or reduced tillage significantly decreased Pratylenchus neglectus populations. Zhang et al. (2015a) showed that the response of nematode trophic diversity was sensitive to the residue and tillage effects. Crop rotation sequences including different crop varieties can also influence nematode abundance, diversity and community structure. Ponge et al. (2013) reported that free-living nematodes were more abundant in a lupin-meadow rotation system than in a continuous meadow system, and Turmel et al. (2015) found that maize monocultures was characterized by plant parasites (especially Pratylenchus and Meloidogyne) and a barley-maize rotation was dominated by bacterivores and fungivores. Banana is the main agricultural crop in South China. Plant pathogenic nematode disease caused by long-term monoculture is recognized as the major factor limiting banana production. Zhong et al. (2015a) reported that crop rotation length and the choice of non-host companion crops in the banana rotation can influence population densities of harmful root-lesion nematodes. Furthermore, no-tillage or reduced-tillage practices that increase soil organic matter near the soil surface, compared to conventional tillage, can improve soil structure and soil biological properties in the banana phase of the crop rotation, and enhance banana yield stability (Zhong et al., 2015b). Until now, most studies on soil nematode communities have been focused either on the effects of different crop rotation or on the effects of tillage practices, with little attention to the interactive influence of both over three years. However, rotation and tillage are two important agricultural practices that are usually applied together in the crop fields of many countries. Therefore, the objectives of our study were to analyze the interactive effect of rotation and tillage on soil nematode and microbial community composition under a longterm experimentation in Hainan Island. 2. Materials and methods 2.1. Site descriptions The experiment was carried out on the Wanzhong Farm in the city of Ledong (18 360 18 380 N, 108 470 108 490 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 2065 mm. The test soil was classified as sandy loam according to the USDA texture classification system with 13.6% clay, 23.3% silt and 63.1% sand. The soil has initial properties of 7.12 g kg1 total organic C, 0.76 g kg1 total N, 0.59 g kg1 total P, 1.21 g kg1, total K and pH 6.53. Soil pH was measured in 1:2.5 soil: KCl 1 M solution.
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The experiment was a split-plot design with four replicates, initiated in 2002 with rotation management as the main plot and tillage system as the sub-plot. Detailed information about the treatments is showed in Table 1. The field experiment was divided into eight plots and the size of each individual plot was 170 m2. Rotation management treatments were banana-pineapple rotation (BA) (three years of banana followed by three years of pineapple), banana-papaya rotation (BP) (three years of banana followed by three years of papaya), banana-rice rotation (BR) (three years of banana followed by three years of rice) and banana monoculture (CK). Tillage systems included a no-tillage (NT) and a conventional tillage (CT) treatment. Chemical N fertilizer (urea), P fertilizer (superphosphate) and K fertilizer (sulphate) were applied at the rates of 129 kg N ha1, 68 kg P ha1 and 292 kg K ha1, respectively to a depth of 0–30 cm after transplanting every year. The manure used was cow manure compost (14.4 t ha1), with 53.3% water content, containing 145 g C kg1, 3.2 g N kg1, 2.5 g P2O5 kg1, 1.6 g K2O kg1 on a dry weight basis, which was basally applied before transplanting (June 25th, 2002–2014) to a depth of 0–30 cm every year. Lime was used (125 kg ha1) together with cow manure compost to increase soil pH. Soil in CT was mouldboard ploughed (40 cm deep) at the end of May and the crops of all treatments were re-sown at the end of June. All aboveground crop residues in CT were incorporated into the soil and residues in NT were left on the surface after crops harvest in the middle of May. 2.2. Soil sampling All soil samples were collected at the same time in the last growing season (2014–2015). After the removal of above-ground plant debris, soil samples were collected using a soil corer (3.0 cm diameter) at a depth of 0–40 cm below the soil surface at the seedling stage (September 16, 2014), jointing stage (December 15, 2014), booting stage (March 17, 2015) and ripening stage (May 19, 2015) within the plant 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 placed in individual plastic bags and then immediately stored at 4 C. A subsample of 100 g soil (fresh weight) was used for nematode extraction. Subsamples were first elutriated and sieved (mesh size 250 and 38 mm) 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 per 100 g dry weight soil. Nematodes were counted using a dissecting microscope and identified using an inverted compound microscope. An average of 150 nematodes (100 nematodes at minimum) per sample were identified at 400 to 1000 magnification to genus or family level within one week of extraction or fixed in 4% formalin until identification. Nematodes were classified into the following trophic groups (Bongers, 1988): bacterivores (BF), fungivores (FF), plant parasites (PP) and omnivores-predators (OP). Phospholipid fatty acids (PLFA) were used as indicators of total, bacterial and fungal biomass in the soil. Lipids were extracted from
Table 1 Description and site history of different treatments in the study area of a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Treatment
Crops
Planting Year
Monoculture (CK) Rotation 1 (BA) Rotation 2 (BP) Rotation 3 (BR)
banana banana and pineapple banana and papaya banana and rice
June 2002–May 2014 Banana: June 2002–May 2005 and June 2008–May 2011; pineapple: June 2005–May 2008 and June 2011–May 2014. Banana: June 2002–May 2005 and June 2008–May 2011; papaya: June 2005–May 2008 and 2011–May 2014. Banana: June 2002–May 2005 and June 2008–May 2011; rice: June 2005–May 2008 and June 2011–May 2014.
Note: In each rotation and monoculture plot, a no-tillage and a conventional tillage treatment were applied.
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8 g of freeze-dried soil using a chloroform–methanol–citrate buffer mixture (1:2:0.8). The polar lipids were separated from neutral lipids and glycolipids on a solid phase extraction column (Supelco Inc., Bellefonte, PA). The phospholipids were trans-esterified with a mild-alkali methanolysis and the resulting fatty acid methyl esters were extracted in hexane and dried under N2. Samples were then dissolved in hexane and analyzed on an Agilent 6850 series Gas Chromatograph with MIDI peak identification software (Version 4.5; MIDI Inc., Newark, DE). The following biomarkers were used: Total PLFAs (sum of all identified PLFAs; from C14 to C20); bacterial
PLFA (iso 15:0, anteiso 15:0, 15:0, iso 16:0, 16:1v5c, iso 17:0, anteiso 17:0, 17:0cy, 17:0 and 19:0cy); fungal PLFA (18:2v, 6 and 9c) (Guckert et al., 1985). 2.3. Statistical analysis Nematode ecological indices were analyzed using the following approaches: Shannon-Weaver diversity (H', Shannon, 1948) was P calculated as H' = Pi (ln Pi), where Pi is the proportion of each of the i genera present. Species richness (SR) was calculated
Table 2 Average contribution (%) of different nematode genera to total soil nematode abundances in rotation and tillage treatments of a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Genus
CK
BA
BP
BR
Guilds
Tillage
RT
Ba1 Ba1 Ba1 Ba1 Ba2 Ba2 Ba2 Ba2 Ba2 Ba2 Ba2 Ba3 Ba3 Ba3 Ba3 Ba3 Ba4
(R) ns 0.045 0.033 <0.01 0.047 ns ns <0.01 ns <0.01 ns ns <0.01 ns ns <0.01 <0.01
(T) ns <0.01 0.018 ns ns ns 0.022 0.048 ns ns ns ns 0.029 ns ns ns <0.01
ns 0.034 ns ns ns ns ns 0.027 ns ns ns ns <0.01 ns ns ns <0.01
22.1 2.9 10.9** 2.4 3.8 2.1
Fu2 Fu2 Fu2 Fu4 Fu4
ns <0.01 ns <0.01 0.039
ns ns ns 0.041 ns
ns ns ns <0.01 ns
23.3 0.3 0.9 2.8 0.0 3.6 1.8 4.3 2.5 2.3 3.6 1.2
24.9 1.4 0.0 0.5 0.3 5.3* 0.7 5.1* 1.0 3.4 5.0* 2.2
Ca4 Ca4 Om4 Om4 Om4 Om4 Ca5 Ca5 Om5 Om5 Om5
ns ns 0.026 ns ns ns ns ns 0.013 <0.01 <0.01
<0.01 0.025 ns ns ns 0.027 ns ns <0.01 <0.01 <0.01
ns ns ns ns ns ns ns ns ns 0.040 0.046
12.7 1.5 3.4 0.9 1.7 0.0 1.3 0.0 0.0 0.0 2.0 0.0 1.9 0.0 0.0
8.1 1.3 1.3 0.6 1.8 0.0 1.1 0.0 0.0 0.0 0.8 0.0 1.2 0.0 0.0
PP2 PP2 PP2 PP2 PP2 PP3 PP3 PP3 PP3 PP3 PP3 PP3 PP3 PP4
ns ns ns ns 0.046 0.023 0.032 <0.01 <0.01 <0.01 <0.01 0.043 <0.01 0.035
ns ns 0.016 ns ns 0.025 ns ns ns 0.011 ns ns 0.020 ns
ns ns ns ns ns ns ns ns ns <0.01 ns ns 0.045 ns
NT
CT
NT
CT
NT
CT
NT
19.4 2.9 4.1 0.0 0.0 0.0 3.7 0.0 4.5 0.0 1.1 0.0 0.0 0.0 0.0 1.9 0.0 1.2
21.3 2.4 3.8 0.0 0.0 0.0 2.6 0.0 5.7* 0.0 0.9 0.0 1.4 0.0 0.0 1.6 0.0 2.9
41.1 1.8 5.2b)* 1.8 2.2 0.6 2.8 2.1 6.1* 0.0 3.4 0.0 0.6 2.4 0.0 2.0 4.6 4.5
42.7 3.4 3.9 2.3 2.1 2.7 1.9 0.0 10.0** 1.3 2.2 0.0 0.7 1.2 0.8 1.8 3.1 5.2*
42.2 2.9 5.8* 0.8 2.4 1.3 2.6 2.7 6.6* 0.0 3.2 0.9 0.0 2.3 1.1 1.0 4.5 4.1
43.6 2.6 4.7 1.8 3.1 0.9 2.2 1.6 6.3* 1.5 2.9 0.0 0.9 3.4 0.9 1.6 3.8 5.4*
43.8 3.7 5.3* 1.6 3.2 0.8 1.7 0.2 10.0** 0.0 2.5 0.9 0.0 3.2 2.4 1.3 2.8 4.2
44.9 2.7 4.2 2.5 1.4 2.5 3.3 3.7 5.9* 2.2 4.1 0.8 1.2 2.1 1.1 0.7 3.3 5.2*
8.5 1.9 3.3 2.6 0.7 0.0
10.4 2.6 4.4 3.4 0.0 0.0
19.0 2.1 10.8** 2.0 2.9 1.2
20.3 2.3 10.2** 3.2 3.5 1.1
16.2 1.8 6.6* 3.9 2.3 1.6
17.4 2.6 5.2* 3.3 3.7 2.4
20.2 1.9 10.5** 3.7 3.3 1.8
Omnivore–carnivores Mononchus Nygolaimus Thonus Eudorylaimus Epidorylaimus Microdorylaimus Prodorylaimus Mesodorylaimus Aporcelaimellus Paractinolaimus Discolaimus
12.6 1.1 0.0 0.0 0.5 4.4 1.7 3.9 1.0 0.0 0.0 0.0
14.9 2.2 0.0 0.0 0.9 4.0 0.0 4.5 0.8 1.0 0.8 0.7
25.1 0.9 0.0 3.2 2.8 4.3 2.6 3.8 0.0 2.1 3.9 1.5
26.8 2.1 0.4 1.8 0.0 5.2* 0.6 5.3* 0.0 3.5 5.1* 2.8
23.4 0.6 1.7 2.0 0.0 4.3 2.8 2.9 0.0 2.5 4.2 2.4
25.5 1.9 0.8 2.3 0.2 5.1* 0.9 2.8 0.0 3.2 5.2* 3.1
Plant parasites Boleodorus Basiria Malenchus Tylenchus Paratylenchus Psilenchus Tylenchorhynchus Helicotylenchus Rotylenchus Rotylenchulus Pratylenchus Hirschmanniella Meloidogyne Dorylaimellus
59.5 1.8 2.6 0.0 3.7 2.3 0.0 0.0 11.8** 5.7* 11.5** 6.3* 0.0 11.2** 2.6
53.4 2.3 2.2 0.8 2.4 2.8 0.0 0.0 10.5** 5.2* 10.1** 5.0* 0.0 10.3** 1.8
14.8 2.2 1.7 0.0 2.1 1.3 0.8 0.0 2.3 3.4 0.0 0.0 0.0 0.0 1.0
10.2 1.7 1.9 0.0 1.3 1.5 0.0 0.0 1.4 1.5 0.0 0.0 0.0 0.0 0.9
18.2 1.8 2.4 1.1 3.9 2.2 0.0 1.7 1.5 0.0 1.1 0.0 1.2 1.4 0.0
13.5 1.4 1.5 0.3 2.6 1.3 0.0 1.3 1.7 0.0 0.0 0.0 2.1 0.9 0.0
Fungivores Ditylenchus Aphelenchus Aphelenchoides Dorylaimoides Tylencholaimus
Effects Rotation
CT Bacterivores Mesorhabditis Protorhabditis Panagrolaimus Monhystera Eucephalobus Heterocephalobus Acrobeles Acrobeloides Cervidellus Plectus Wilsonema Domorganus Chronogaster Leptolaimus Pseudoaulolaimus Prismatolaimus Alaimus
a)
Note: BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. a) Functional guilds of soil nematodes characterized by feeding habits and life-history characters, numbers following the functional guilds indicate the c-p values (Bongers and Bongers, 1998; Ferris et al., 2001); b) ** dominant genus, average contribution (%) of different nematode genera to total soil nematodes is more than 10%; * subdominant genus, average contribution (%) is over 5%.
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according to Ferris et al. (2001). Maturity index (MI) was calculated P as P(i)C(i), where C(i) is the colonizer-persister (c-p) rating of taxon i according to the 1–5 c-p scale of Bongers and Bongers (1998). 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), basal index (BI) and channel index (CI) are indicators for soil food web structure and condition (indicating functional diversity), and were calculated according to the method of Ferris et al. (2001). The colonizerpersister (cp) values for taxa were adopted from Bongers (1990) and Bongers and Bongers (1998). The nematode metabolic footprint (NMF) was calculated as P NMF = (Nt (0.1Wt/mt + 0.273 (W0.75))), where Wt and mt represent the body weight and colonizer-persister (cp) values of genus t, respectively. The enrichment footprint (efoot) is the metabolic footprint of lower trophic levels (cp 1–2) while the structure footprint (sfoot) represents the metabolic footprint with the higher cp value (3–5) (Ferris, 2010). Functional metabolic footprint (FMF) was calculated as (Fs Fe)/2 with complex mg2 units (Ferris, 2010), where Fs is the sum of standardized C labile by structure indicator taxa and Fe is the sum of standardized C labile by enrichment indicator taxa. The magnitudes of C and energy flow through the bacterial, fungal and herbivory channels are represented as bacterial footprints (BFfoot), fungal footprints (FFfoot), and herbivore footprints (PPfoot), the C utilization coefficient, for bacterial-, fungal- and plant-feeding nematodes. Nematode abundances, different trophic metabolic footprints and microbial abundances were ln (x + 1) transformed prior to statistical analysis to obtain normality of data. Repeated measures analysis of variance was used to test the overall effect of rotation, tillage and sampling stage on soil biota. Separate one-way analysis of variance was used to test the effects of rotation and tillage on soil biota at each sampling stage and means were compared by least significant difference. Bivariate correlation analysis was used to test the significance of correlations between soil nematode abundance or ecological index and soil microbial biomass. All statistical analyses were performed by SPSS statistical software
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(SPSS Inc., Chicago, IL, USA). Difference at P < 0.05 level was considered to be statistically significant. 3. Results 3.1. Soil nematode abundance In the eight treatments studied, forty-seven nematode genera were observed, with the highest value in BPNT (40) and lowest in CKCT (25); 36 and 35 genera were found in BANT and BACT, respectively, and 39 and 37 genera in BRNT and BRCT, respectively (Table 2). Among the identified nematode genera, Acrobeloides in BANT and BRCT, Aphelenchus in BANT, BACT, BRNT and BRCT, Helicotylenchus, Rotylenchulus and Meloidogyne in CKNT and CKCT were the dominant genera (relative abundance >10%). Protorhabditis in BACT, BPCT and BRCT, Alaimus, Epidorylaimus and Paractinolaimus in BANT, BPNT and BRNT, Prodorylaimus in BANT and BRNT, Pratylenchus and Rotylenchus in CKNT and CKCT were the subdominant genera (relative abundance >5%, Table 2). The bacterivores including Acrobeloides, Monhystera, Plectus, Chronogaster, Prismatolaimus and Alaimus and fungivores including Aphelenchus and Dorylaimoides were greatly influenced by rotation, with relatively higher abundances in BA, BP and BR than in CK (P < 0.01). Omnivores-predators such as Mononchus, Paractinolaimus, Aporcelaimellus and Discolaimus were strongly affected by tillage, with higher relative abundances in NT and lower in CT (P < 0.01, Table 2). Significant rotation (R), tillage (T) and growth stage (S) effects were observed on the number of total nematodes (P < 0.05, Table 3). During the study period, the total number of nematodes fluctuated obviously among different treatments (Fig. 1), with the highest value (869 individuals 100 g1 dry soil) in BPNT at booting stage, and the lowest (358 individuals 100 g1 dry soil) in CKCT at seedling stage. In rotation systems, the total number of nematodes was on average 37.3%, 41.5% and 39.7% higher in BA, BP and BR, respectively compared with CK. In tillage systems, the total number of nematodes was on average 12.1% higher in the NT compared with the CT.
Table 3 Two-way ANOVA table of P values showing the significance of the effects of different crop rotation and tillage practices on soil biota in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. ANOVA
Rotation (R) P value
Tillage (T) P value
Stage (S) P value
RT P value
RS P value
TS P value
RTS P value
TNEMA BF FF OP PP TP BP FP H' SR MI PPI BI CI EI SI BFfoot FFfoot PPfoot Efoot Sfoot
<0.01 <0.01 <0.01 0.039 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 0.013 <0.01 <0.01 <0.01 <0.01 0.021 <0.01 <0.01 <0.01 <0.01
0.048 0.023 0.036 <0.01 0.042 <0.01 <0.01 <0.01 <0.01 <0.01 0.018 <0.01 <0.01 0.011 <0.01 0.027 <0.01 <0.01 <0.01 <0.01 <0.01
<0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 ns <0.01 <0.01 0.012 ns <0.01 <0.01 ns ns <0.01 <0.01 ns
ns ns ns <0.01 ns <0.01 ns ns <0.01 <0.01 <0.01 <0.01 <0.01 0.019 0.040 <0.01 ns 0.045 <0.01 0.016 <0.01
ns <0.01 <0.01 0.043 <0.01 ns <0.01 <0.01 <0.01 ns <0.01 <0.01 <0.01 <0.01 <0.01 <0.01 ns ns ns ns <0.01
ns ns ns ns ns ns ns ns <0.01 ns 0.036 <0.01 ns <0.01 <0.01 ns ns ns 0.022 0.047 ns
ns ns ns ns ns ns ns ns <0.01 ns <0.01 <0.01 <0.01 0.025 <0.01 <0.01 ns ns ns ns ns
Note: TNEMA, total nematodes; BF, bacterivores; FF, fungivores; OP, omnivore-predators; PP, Plant parasites; TP, total PLFAs; BP, bacterial PLFA; FP, fungal PLFA; H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
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Fig. 1. The abundance of nematodes and phospholipid fatty acids (PLFA) under rotation and tillage treatments at four sampling stages in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. A, total nematodes; B, bacterivores; C, fungivores; D, omnivore-predators; E, plant parasites; F, total PLFAs; G, bacterial PLFA; H, fungal PLFA. Error bars indicate standard error. Different lower case letters in the figure mean significant difference according to Ducan’s multiple range test (P < 0.05).
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Fig. 2. Nematode ecological indices in rotation and tillage treatments at four sampling stages in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. BA, banana-pineapple rotation; BP, banana-papaya rotation; BR, banana-rice rotation; CK, banana monoculture; NT, no-tillage; CT, conventional tillage. H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
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Significant rotation, tillage and growth stage effects were observed on the numbers of bacterivores, fungivores, omnivore– carnivores and plant parasites (P < 0.05). A significant interaction effect of S R on bacterivores, fungivores and plant parasites and of R T on omnivore–carnivores was observed (P < 0.01). At the booting stage, the numbers of bacterivores, fungivores and plant parasites were higher compared to the other stages. At the jointing, booting and ripening stages, BRNT and BPNT showed higher numbers of omnivore–carnivores, followed by BANT, BRCT and BPCT, while CKNT and CKCT had the lowest numbers. Different kinds of crop rotation increased the numbers of bacterivores, fungivores and omnivore–carnivores, but decreased that of plant parasites (P < 0.01). However, the continuous cropping expanded the number of plant parasites, while it reduced other forms (P < 0.05). In terms of rotation treatments, BA had the highest number of plant parasites and lowest number of bacterivores, fungivores and omnivore–carnivores; BP had the highest number of bacterivores and fungivores; BR had the highest number of omnivore–carnivores and the lowest number of plant parasites. In tillage systems, the numbers of bacterivores, fungivores and omnivore–carnivores were much higher in NT and lower in CT, but the number of plant parasites was much lower in NT than in CT (P < 0.01, Fig. 1).
that of PPfoot was much lower in NT than in CT (P < 0.01, Fig. 2). FMF is the total area of the enrichment and structure footprints as illustrated in Fig. 3. In rotation systems, the FMF was greater in BA, BP and BR than in CK, and in tillage systems it was much higher in NT than in CT. All plots in BANT, BPNT and BRNT were located in quadrat B and almost half of the plots in BACT, BPCT and BRCT were located in quadrat C, whereas all plots in CKNT and CKCT were clustered in quadrat D of the FMF figure. 3.4. Correlations of soil nematode and microbial communities The total number of nematodes, the numbers of bacterivores, fungivores, omnivore–carnivores and the value of H' were positively correlated with the concentrations of total PLFAs, bacterial PLFA and fungal PLFA (P < 0.01, Table 4). However, the number of plant parasites and the values of PPI and PPfoot were negatively correlated with the concentrations of total PLFAs, bacterial PLFA and fungal PLFA (P < 0.01). The values of SR, EI, FFfoot and efoot were positively correlated with the concentrations of bacterial PLFA and fungal PLFA (P < 0.05). 4. Discussion 4.1. Changes of soil nematode and microbial communities
3.2. Soil microbial communities Significant rotation, tillage and growth stage effects were observed on the abundance of specific microbial groups by using indicative PLFA biomarkers (P < 0.01, Table 3). In rotation systems, the concentrations of total PLFAs, bacterial PLFA and fungal PLFA varied in a range of 13.5–46.2, 11.4–37.1 and 2.6–6.3 nmol g1 dry soil, respectively, with the following order: CK < BA < BR < BP. In tillage systems, these PLFA concentrations were on average 18.8%, 17.5% and 13.7%, respectively higher in the NT than in the CT. During the study period, the abundance of microbial functional groups increased with crop maturity. At the booting and ripening stages, the concentrations of total PLFAs, bacterial PLFA and fungal PLFA were higher compared to the seedling and jointing stages. This was true among all treatments (Fig. 1).
Both crop rotation and tillage treatments influenced nematode density and diversity over the 12-year period, although the rotation effect was the main source of data variation. The total nematode abundance was much greater in BA, BP and BR than in CK during the seedling, jointing, booting and ripening stages. The result was consistent with a recent study that compared barley monoculture with sugar beet-barley rotation (Quist et al., 2015).
CKCT
BACT
BPCT
BRCT
CKNT
BANT
BPNT
BRNT
100.0
A
B
D
C
Significant rotation, tillage and growth stage effects were observed on the values of H', SR, MI, PPI, BI, CI, EI and SI (P < 0.01, Table 3). Except SR, interactive effect of R T S was observed for all ecological indices (P < 0.05). The values of almost all ecological indices in rotation and tillage were significantly higher at the booting stage followed by the ripening stage, while the jointing stage and the seedling stage had the lowest values. In the rotation systems, higher H', SR, MI, EI and SI and lower PPI, BI and CI values were obtained in BA, BP and BR compared with CK (P < 0.05). BA had the highest values of PPI, BI and CI and the lowest values of H', SR, MI, EI and SI; BP had the highest values of H' and SR and the lowest values of BI and CI; BR had the highest values of MI, EI and SI and the lowest values of PPI. In tillage systems, the values of H', SR, MI, EI and SI were on average 36.2%, 28.9%, 35.1%, 33.2% and 46.7%, respectively higher in NT compared with CT, whereas those of PPI and CI showed the opposite trend, being 29.3% and 38.4% lower in NT than in CT. At jointing, booting and ripening stages, rotation effect on FFfoot, PPfoot and efoot, tillage effect on FFfoot and sfoot, and effects of the interaction of R T on PPfoot and efoot were all significant (P < 0.05). In the rotation system, greater values of BFfoot, FFfoot, efoot, sfoot and lower PPfoot values were observed in BA, BP and BR than in CK (P < 0.05). In the tillage system, BFfoot, FFfoot, efoot, sfoot were much higher in NT and lower in CT, but
Enrichment Footprint
3.3. Soil nematode ecological indices
50.0
0.0 0.0
50.0
100.0
Structure Footprint Fig. 3. Functional metabolic footprint of nematodes subjected to rotation and tillage effects in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. The vertical axis and horizontal axis of each footprint represent enrichment footprint and structure footprint respectively. The functional metabolic footprint is described by the sequentially joining points: (SI 0.5Fs, EI); (SI, EI + 0.5Fe);05Fe); (SI + 0.5Fs,05Fs, EI); (SI, EI 0.5Fe). Fs and Fe represent structure footprint and enrichment footprint, respectively. The nematode functional metabolic footprint is the total area of the two functional (enrichment and structure) footprints (Ferris 2010).
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Table 4 Pearson’s correlation coefficients between soil nematode and microbial community indicators in a long-term crop rotation experiment at the Wanzhong Farm in Hainan Island, China. Indicators
Total PLFAs
Bacterial PLFA
Fungal PLFA
Indicators
Total PLFAs
Bacterial PLFA
Fungal PLFA
TNEM BF FF OP PP H' SR MI PPI
0.762** 0.684** 0.686** 0.522** 0.520** 0.426** 0.103 0.163 0.416**
0.742** 0.661** 0.717** 0.501** 0.533** 0.465** 0.212* 0.158 0.378**
0.669** 0.715** 0.593** 0.538** 0.574** 0.506** 0.332* 0.183 0.399**
BI CI EI SI BFfoot FFfoot PPfoot Efoot Sfoot
0.188 0.151 0.105 0.191 0.216* 0.196 0.288* 0.156 0.302*
0.176 0.147 0.211* 0.215* 0.503** 0.231* 0.426** 0.266* 0.113
0.129 0.172 0.234* 0.184 0.424** 0.395* 0.399* 0.347* 0.195
Note: TNEM, number of total nematodes; BF, bacterivores; FF, fungivores; OP, omnivores-predators; PP, plant-parasites; H', diversity; SR, species richness; MI, maturity index; PPI, plant parasite index; BI, basal index; CI, channel index; EI, enrichment index; SI, structure index; BFfoot, bacterial footprint; FFfoot, fungal footprint; PPfoot, herbivore footprint; Efoot, enrichment footprint; Sfoot, structure footprint.
This suggests that the greater variety of organic matter input in crop rotations than in monocultures can increase the abundance and diversity of soil nematodes. In contrast with banana residue, the pineapple, papaya and rice residues included in our study are rich in biodegradable sugars and proteins but poor in cellulose and hemicelluloses (Williams et al., 2014). Thus crop rotations provide the easily-utilizable resource for soil microbes and nematodes. As far as crop rotation was concerned, BP had higher total nematode numbers compared with BA and BR. This could be due to the concentration and type of organic compounds released by the roots of papaya which reduced soil-borne pathogens and maintained higher nutrient levels for nematode development (Daniel et al., 2014). In our study, rotations containing a pineapple, papaya or rice phase significantly reduced populations of plant parasites, which is consistent with Chavez et al. (2014) in a 6-year cotton-clover-cornrye rotation. Initially, the plant parasite taxa constituted 56.5% of the total nematode population under banana monoculture, but after rotation, the proportion of plant parasites declined sharply to 15.9% for pineapple, 12.5% for papaya and only 10.4% for rice (Fig. 1). This suggests that crop rotations, especially rice plots that are flooded (anaerobic, higher soil moisture and lower temperatures), have a suppressive effect on plant parasite populations which associated with suppressed root growth (Song et al., 2016). The abundance of bacterivorous and fungivorous nematodes was markedly higher in the BA, BP and BR than in the CK. As for different rotation treatments, BP had the highest abundance of bacterivores and fungivores, followed by BA and BR. The result is inconsistent with a recent observation that a ley-vegetable rotation did not affect the abundance of bacterivores and fungivores (Ugarte et al., 2013). This suggests that the rotation period in the study of Ugarte et al. (2013) was not long enough to allow recovery of the soil nematodes from the long-term monoculture. Our results showed more abundant microbial populations, effective organic matter decomposition and higher soil fertility in rotation systems compared with monoculture over a long time period, caused by the large input of organic amendments and crop residues (Wang et al., 2015). The differences between pineapple, papaya and rice rotations might be due to the improved soil structure, stabilized microclimate, greater rhizosphere microbial populations and higher root density generally found in banana-papaya rotation compared with banana-pineapple and banana-rice rotation (Qian et al., 2014). The abundance of omnivores-predators was much higher in NT than in CT. Similarly, Zhang et al. (2013) found a greater abundance of omnivores-predators in a maize-soybean residues incorporated no-tillage compared with conventional tillage. This indicated that the positive effects of limiting physical disturbance such as antiabrasion and improvements to soil texture and residue could stir
up increases in the abundance of larger-bodied nematode fauna since they are especially sensitive to soil disruption (Ito et al., 2015a). The recovered omnivores-predators in this study included Mononchus, Epidorylaimus, Paractinolaimus, Aporcelaimellus and Discolaimus which had colonizer-persister (cp) values of cp-4 and cp-5. These values place them in a K-strategist located category in the higher trophic level of the soil food web and thus would be expected to be less prevalent in soils that are disturbed or conventionally-tilled. Our results therefore corroborate earlier reports (Zhao et al., 2015). In rotation systems, the composition of soil microbial communities was altered by the different rotations, with a much higher abundance of bacteria and fungi in BA, BP and BR than in CK, and much higher abundances in BP than in BR and BA. A close association between bacteria, fungi and rotations was also reported by Chen et al. (2014) in a crops-grassland rotation system with a sandy loam texture. They concluded that the crop rotation provides better soil hydrological conditions, effective rhizodepositions and residual fertility which usually stimulate high proportion of soil microorganisms. Yuan et al. (2015) also suggested that the differences in quantity, quality and distribution of papaya residues generally lead to greater concentrations and diversity of organic materials, and thus, to higher soil microbe viability, and accelerated carbon and nutritional cycling compared with pineapple and rice. In tillage systems, the abundance of primary decomposers, such as bacteria and fungi was much greater in NT than in CT, which was instantiated by the higher abundance of bacterivores and fungivores in NT compared with CT (Fig. 1). Mloza-Banda et al. (2016) gained a similar observation in a 5-year tobacco-cotton rotation combined with conservation. They attributed their findings partly to the changes in the soil environment caused by no-tillage, including soil structure and density, soil pH, and nutrient cycles within the soil profile, and partly to the accumulation of crop residues at the surface which produces less soil disturbance, high plant litter quantity, intensive and deep rooting and decreasing percolation water with N nutrients in no-tillage soils. 4.2. Changes of soil nematode ecological indices The ecological indices of H', SR, MI and PPI are often used to assess the soil condition. H' and SR are linked to the diversity of soil nematodes, MI and PPI can reflect the disturbance by human activities due to crop rotations and tillage (Djigal et al., 2012). In this study, the values of H', SR and MI were higher in BA, BP and BR than in CK, which indicates a trend of greater soil nematode biodiversity and a relatively stable environment in banana rotations. We did not find significant seasonal effects on SR which suggests that the soil nematode species richness fluctuated only
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slightly with banana growth. The highest PPI values were observed under banana monoculture in both NT and CT systems. During the growing season, Helicotylenchus, Rotylenchus, Rotylenchulus, Pratylenchus and Meloidogyne with c-p3 were dominant genera in CK and accounted for approximately 40% of total soil nematodes, which probably led to CK exhibiting the highest PPI values (Liu et al., 2016). Weighted indices, such as BI, CI, EI and SI, may provide information about the nematode community structure in stressed, enriched, stable structured and rapidly degraded environments, and indicate the dynamics of soil food webs (Ferris and Tuomisto, 2015). In this study, banana rotations with various residue additions generally contained more bacterivores and fungivores, which resulted in a higher EI, and lower BI compared to banana monoculture with a single residue input. Furthermore, higher EI and SI but lower BI in BP than in BA and BR were also observed, which is in agreement with a recent study that compared wheat monoculture with maize-rice-wheat rotation (Malherbe and Marais, 2015). Papaya has more extensive rooting systems than pineapple and rice, therefore a papaya rotation system may provide greater amounts of plant residues of varying degrees of degradability that would support greater microbial biomass compared to pineapple and rice systems (Silva et al., 2014). The lower values of CI in BA, BP and BR than in CK indicate that the bacterial decomposition pathway was relatively more dominant in banana-based rotations and played a more important role in nutrient cycling and nutrient supply to plants. The fungal decomposition pathway, which was relatively important in monoculture, often reflects lower rates of decomposition (Liu et al., 2015). The extremely high SI values in no-tillage may be due to the enrichment of omnivore–carnivores, which are sensitive to disturbance and need more time to establish than the more rapidly growing bacterivores and fungivores (Dang et al., 2015). Nematode faunal analysis inferred by EI and SI indicate that the soil food webs in NT were less disturbed, more stable and structured due to the increasing of free-living nematodes, while the soil food webs in CT were degraded due to stressed soil surroundings. Roth et al. (2015) also suggested that the soil food web was more complex in organic reduced- and no-tillage systems with high EI and SI values. In this study, nematode metabolic footprints were used to provide information about the structure and function of the soil food web under different agricultural management practices. Higher BFfoot and FFfoot but lower PPfoot were found in rotation and no-tillage systems, suggesting greater flow of resources into the food web through bacterivorous and fungivorous channels than through herbivory channels. In rotation systems, higher efoot and sfoot were found in BA, BP and BR than in CK, as also reported by Zhang et al. (2015b) in a corn-soybean rotation. This shows that a large variety of cover crops is an important determinant of the nature and magnitude of soil food web services and that soil nematodes as significant regulators of food web have decisive influence on residue decomposition and nutrients in ecosystems. In tillage systems, the values of efoot and sfoot were larger in NT than in CT, and significant correlations were found between the numbers of omnivores-predators and the abundance of bacterivores (r = 0.363, P < 0.05) and fungivores (r = 0.516, P < 0.01). The results are consistent with the study of Ito et al. (2015b) in a ricesoybean-maize rotation under different tillage practices. The relatively high efoots in the NT showed the enhancing productivity and turnover rates of the enrichment indicators in this system to maintain metabolic balance. The same variation trend of sfoot indicates an increasing metabolic activity of the predators, which may be related to the increased top-down predation pressure in the no-tillage system relative to the conventional tillage system.
5. Conclusion Our study shows that rotation and no-tillage practices promote the abundance of most nematodes and microbial biomass. Nematode trophic footprints respond more actively to rotation than tillage impacts and offer more information on carbon, nitrogen and energy entering the soil food webs. The application of tillage practices in a rotation system may result in a bacterialdominated decomposition pathway. Nematode community analysis indicates that a banana-based rotation system provides a more diverse residue resource entry into soil food webs, and that a no-tillage system is beneficial for soil ecosystem stability and sustainability. Furthermore, Hainan Island may provide baselines for other tropical situations. This initial inventory could also be used to assess the soil environment in a tropical monsoon climate according to agricultural practices. Acknowledgement This research was supported by the National Natural Science Foundation of China to S. Zhong (41301277), the Natural Science Foundation of Hainan Province to S. Zhong (310073) and the State Scholarship Fund of China to S. Zhong (201503260016). References Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Appl. Soil Ecol. 10, 239–251. Bongers, T., 1988. De Nematoden van Nederland [M]. KNNV Bibliotheekuitgave 46, Pirola, Schrool, Netherlands, 1988, 408pp. Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19. Chavez, H., Taylor, C.R., Rodríguez-Kábana, R., 2014. Population dynamics and interactions between plant parasitic and non-parasitic nematodes: an empirical analysis. Appl. Soil Ecol. 78, 11–17. Chen, X.Y., Daniell, T.J., Neilson, R., O'Flaherty, V., Griffiths, B.S., 2014. Microbial and microfaunal communities in phosphorus limited, grazed grassland change composition but maintain homeostatic nutrient stoichiometry. Soil Biol. Biochem. 75, 94–101. Costa, C.H.M., Crusciol, C.A.C., 2016. Long-term effects of lime and phosphogypsum application on tropical no-till soybean–oat–sorghum rotation and soil chemicalproperties. Eur. J. Agron. 74, 119–132. Cunha, T.P.L., Mingotte, F.L.C., Chiamolera, F.M., Carmeis, A.C.D., Soares, P.L.M., Lemos, L.B., Vendramini, A.R., 2015. Occurrence of nematodes and yield of common bean and maize as a function of cropping systems under no-tillage. Nematropica 45, 34–42. Dang, Y.P., Seymour, N.P., Walker, S.R., Bell, M.J., Freebairn, D.M., 2015. Strategic tillage in no-till farming systems in Australia’s northern grains-growing regions: i. Drivers and implementation. Soil Tillage Res. 152, 104–114. Daniel, M.D., Grandy, A.S., Tiemann, L.K., Weintraub, M.N., 2014. Crop rotation complexity regulates the decomposition of high and low quality residues. Soil Biol. Biochem. 78, 243–254. Djigal, D., Chabrier, C., Duyck, P.F., Achard, R., Quénéhervé, P., Tixier, P., 2012. Cover crops alter the soil nematode food web in banana agroecosystems. Soil Biol. Biochem. 48, 142–150. Ferris, H., Tuomisto, H., 2015. Unearthing the role of biological diversity in soil health. Soil Biol. Biochem. 85, 101–109. 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. Ferris, H., 2010. Form and function: metabolic footprints of nematodes in the soil food web. Eur. J. Soil Biol. 46, 97–104. Forge, T.A., Larney, F.J., Kawchuk, L.M., Pearson, D.C., Koch, C., Blackshaw, R.E., 2015. Crop rotation effects on Pratylenchus neglectus populations in the root zone of irrigated potatoes in southern Alberta. Can. J. Plant. Pathol. 37, 363–368. Gu, Y.F., Zhang, T., Che, H., Lu, X.X., Du, Y.Q., 2015. Influence of returning corn straw to soil on soil nematode communities in winter wheat. Acta Ecol. Sin. 35, 52–56. Guckert, J.B., Antworth, C.P., Nichols, P.D., White, D.C., 1985. Phospholipid, esterlinked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microb. Ecol. 31, 147–158. Ito, T., Araki, M., Komatsuzaki, M., Kaneko, N., Ohta, H., 2015a. Soil nematode community structure affected by tillage systems and cover crop managements in organic soybean production. Appl. Soil Ecol. 86, 137–147. Ito, T., Araki, M., Higashi, T., Komatsuzaki, M., Kaneko, N., Ohta, H., 2015b. Responses of soil nematode community structure to soil carbon changes due to different tillage and cover crop management practices over a nine-year period in Kanto, Japan. Appl. Soil Ecol. 89, 50–58.
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