Skip to main content
NCBI home page
Helminthologia logoLink to Helminthologia
. 2018 Oct 27;55(4):322–333. doi: 10.2478/helm-2018-0025

Soil Nematode Abundances were Increased by an Incremental Nutrient Input in a Paddy-upland Rotation System

C Hu 1, X G Xia 1, X M Han 2,3,*, Y F Chen 1, Y Qiao 1, D H Liu 1, S L Li 1
PMCID: PMC6662006  PMID: 31662663

Summary

To study the effect of fertilization on soil nematode communities in a paddy-upland rotation system, an ongoing thirty-three years long-term fertilizer experiment is conducted which includes seven treatments; an unfertilized treatment (control), nitrogen (N), phosphorus (P), potassium (K) fertilizer treatments (N, NP, NPK) and organic manure (M) combined with chemical fertilizer treatments (MN, MNP, and MNPK). The soil nematode community structure and crop yields were determined in 2012 and 2013. Overall total nematode abundance was increased by an incremental nutrient input both in the rice and wheat fields. Total number of nematode was 1.25 – 2.37 times greater in the rice field and was 1.08 – 2.97 times greater in wheat field in the fertilization treatments than in the unfertilized treatment. Soil free-living nematode abundances was significantly (P < 0.001) increased in organic manure combined with chemical fertilizer treatments in rice field. Fungi-feeders and plant-feeding nematodes abundances were not significantly different among treatments in rice and wheat fields. Omnivorous and predatory nematodes were the most dominant groups in the present study. Omnivores, predators and Prodorylaimus abundances were significantly (P < 0.05) higher in organic manure combined with NPK fertilizer treatments than in chemical fertilizer alone and unfertilized treatments both in rice and wheat fields. Stepwise regressions revealed that soil free-living nematodes were significant predictors of rice grain yields (R2 = 0.56, P < 0.001) and omnivorous and predatory nematodes were significant predictors of the wheat grain yield (R2 = 0.89, P < 0.001). Therefore, long-term application of organic manure combined with chemical fertilizer could increase nematode abundances and crop yields. Organic manure combined with chemical fertilizer application was recommended in agricultural ecosystem.

Keywords: soil nematode community, trophic group, prodorylaimus, crop yields, long-term fertilizer experiment

Introduction

Maintaining sustainable soil utilization in developing countries is essential to supply the demand for food grain production. However, steady crop yields cannot be maintained without the application of some soil amendments (Gruzdeva et al., 2007). Long-term and large numbers of chemical fertilizer applications have led to the loss of soil fertility, a reduction in soil biodiversity, and polluted farm products (Singh et al., 2016; Ding et al., 2017). Therefore, the application of organic fertilizer has come under consideration. The benefits of long-term manure application to soil include better tilth, improved water-holding capacity and cation exchange capacity, moderated soil temperature, enhanced crop performance, and increased soil organic matter and biological fertility (McSorley & Gallaher, 1997). Accordingly, soil fertility and crop yields are increased and good physical or chemical soil properties and biological communities are maintained. However, the long-term application of chemical fertilizers leads to soil hardening, weak aeration, and weak biological activity (Hopkins & Shiel, 1996).

Paddy rice-upland wheat crop rotation systems are one of the largest agricultural production systems in the world, mainly distributed in southern and eastern Asia (Brar et al., 2013). The 13.5 million hectares were in South Asia, and the other 10.5 million hectares are in South China, widely disseminated throughout the provinces of Jiangsu, Zhejiang, Hubei, Guizhou, Yunnan, Sichuan and Anhui, etc. (Hu et al., 2015). This area accounts for roughly half of the total rice cultivated area in China. Therefore, the protection of the soil environment in the rice-wheat crop system is crucial for the maintenance of sustainable crop yields and to ensure China’s food security (Zhang et al., 2016).

Long-term field experiments are indispensable sources of knowledge and provide a tool for examining soil environment changes (Debreczeni & Körschens, 2003). Furthermore, long-term fertilizer experiments could reflect the influence of fertilizer benefit, crop growth and soil environment due to annual changes in climate (Miao et al., 2011; Wei et al., 2016). Some information could be gained regarding sustainable agriculture and humanity’s influence on the soil fertility, landscape and agricultural environment (Diacono & Montemurro, 2010; Miles & Brown, 2011; Peterson et al., 2012; Geisseler & Scow, 2014).

Soil free-living nematode communities are known to be sensitive to agricultural management practices such as fertilization, irrigation, and tillage (Porazinska et al., 1999; Zhang et al., 2017a). Furthermore, soil nematodes can be placed into at least five functional or trophic groups. They occupy a central position in the soil detrital food web and play a crucial role in soil organic-matter decomposition, plant-nutrient mineralization, and nutrient cycling (Neher, 2001). Therefore, soil nematode diversity, species composition, trophic group, and biomass may be useful bioindicators for monitoring soil environmental changes (Gutiérrez et al., 2016; Scharroba et al., 2016; Zhao et al., 2016; Čerevková et al., 2017). Liang et al. (2009) reported that total nematode abundance responded positively to manure treatments in monoculture maize fields. Hu & Qi (2013) found that long-term application of micro-organic compost could increase nematode abundance in wheat fields. So far, all studies about the effects of fertilization on the nematode community have mainly focused on the upland cropping systems. However, few investigations have reported the effects of long-term application of inorganic and organic fertilizer on soil nematode communities in the paddy-upland rotation system. Therefore, the aims of this study are to (1) determine the impacts of long-term fertilization on the soil nematode community, (2) compare the differences of the nematode communities under organic manure and inorganic fertilizer treatments in the paddy rice-upland wheat rotation systems.

Materials and Methods

Study site

An ongoing long-term (thirty-three years) fertilizer experiment in a rice-wheat rotation system was initiated from rice cultivation in 1981, belonging to the National Fertilizer Experiment Monitoring Network at Nanhu Experimental Station, Hubei Academy of Agricultural Sciences in Wuchang China, located at latitude 30°28′N, longitude 114°25′E and at an altitude of 20 meters in central China. The experimental site lies in a subtropical monsoon zone, which

is characterized by hot summers and severe winters, and occasional snowfall during winter. The mean annual temperature is 13 °C, ranging from a minimum of 3.7 °C in January to a maximum of 28.8 °C in July. The mean annual precipitation is 1300 mm, and the annual non-frost period is 240 days from 1981 to 2013. The soil at the experimental site is yellow-brown soil, belonging to the Albic Luvisol in the FAO classification, which has a clay-loam texture with 15 % sand, 36 % silt, and 49 % clay. Soil physical-chemical properties in October 2012 at an 0 – 20 cm depth were shown in Table 1.

Table 1.

Soil properties (0–20 cm) in different fertilization treatments in October 2012.

Treatment Organic Matter Total N Alkaline N Available P Available K pH
(g kg-1) (g kg-1) (mg kg-1) (mg kg-1) (mg kg-1)
Control 21.69c 1.64c 112.22b 8.21c 105.63bc 7.17ab
N 22.02c 1.79bc 113.88b 8.71c 94.77bc 7.37ab
NP 26.02b 1.86bc 129.51b 18.71c 93.12c 7.57a
NPK 26.54b 1.88b 134.35b 18.33c 117.66bc 7.22ab
MN 36.74a 2.71a 188.98a 130.69b 139.14bc 7.22ab
MNP 34.72a 2.61a 173.51a 136.73b 141.27b 7.30ab
MNPK 34.04a 2.70a 189.01a 151.32a 205.94a 7.03b
Open in a new tab

Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment.

Different letters (a, b, c) in the same column indicate significant differences (P < 0.05) among treatments according to LSD multiple comparison.

Experimental design

The field experiment was constituted of seven treatments and three replicates in a randomized complete block design. Each plot was 40 m2 (5 m width × 8 m length). The seven treatments were as follows: (1) the unfertilized treatment, control; (2) the inorganic N fertilizer treatment, N; (3) the inorganic N and P fertilizer treatment, NP; (4) the inorganic N, P and K fertilizer treatment, NPK; (5) the manure plus inorganic N fertilizer treatment, MN; (6) the manure plus inorganic N and P fertilizer treatment, MNP; and (7) the manure plus inorganic N, P and K fertilizer treatment, MNPK. The chemical fertilizers were applied at an annual rate of 150 kg N ha-1, 75 kg P2O5 ha-1, and 150 kg K2O ha-1 (Zhang et al., 2017b). The N, P, and K fertilizers were applied as urea, ammonium phosphate, and potassium chloride, respectively. 22,500 kg ha-1 of organic fertilizers from pig dung compost was applied to the MN, MNP and MNPK treatments. The pig dung compost contained an average of 282.05 g kg−1 organic C, 15.08 g kg−1 total N, 20.84 g kg−1 P2O5, 13.56 g kg−1 K2O, and 69 % water. 60 % of inorganic fertilizers were applied during the rice growth season and the other 40 % during the wheat growth season, while manure was applied equally (50:50) to the two crops. The N fertilizer was applied three times in the rice growth season. Namely, 40 % of the N fertilizer as basal fertilizer was applied before the cultivating rice, 40 % was applied during the rice tillering stage and 20 % was applied during the rice booting stage. Similarly, the N fertilizer was also applied three times in the wheat growth season. Namely, 50 % of N fertilizer as basal fertilizer was applied before the planting wheat, 25 % during the wheat seedling stage and 25 % was applied during the jointing stage in the wheat growth season. Every year, the P, K fertilizers and manure were applied as basal fertilizer, prior to plough. All basal fertilizers and manure were evenly sprinkled on the soil surface by hand and were incorporated into the plough layer by tillage as soon as possible. Tillage was performed to a depth of 20 cm by a plough, followed by a harrow. The fertilized and unfertilized plots were tilled similarly.

All plots were transplanted with rice seedlings (Oryza sativa L.) in summer and were sown with wheat seeds (Triticum aestivum L.) in winter, which has been done annually since 1981. The rice was transpl anted in June and harvested in October, and the wheat was directly sown in November and harvested in May of the next year. The above-ground crops were harvested with a sickle and removed; thus, no straw returned into the soil in any plot. Nevertheless, rice o r wheat stubble and roots were incorporated into the soil with a plow before the subsequent rice or wheat planting. In addition to the fertilizer treatments, all other agronomic managements were identical in the fertilized and unfertilized plots.

Rice and wheat grains were separated from straws using a plot thresher. Grains and straw were weighed after sun-drying and recorded from the whole plot.

Soil sampling

Soil samples from the upper (0 – 20 cm) soil layer were collected in the rice and wheat maturity stages in October 2012 and in May 2013, respectively. Composite soil samples consisting of ten cores (2.5 cm diameter × 20 cm depth) were collected from each plot. Soil samples were stored in tied and insulated plastic bags to prevent moisture loss. They were transferred to 4 °C storage as soon as possible until they were used to analyze the soil nematode community structure.

Soil physical-chemical properties analysis

Soil samples collected from the 0 – 20 cm were air-dried at room temperature, mixed, sieved through a 1-mm screen, and sub-samples were used to analyze soil physical-chemical properties. The air-dried sub-samples were ground to pass through a 0.25-mm sieve to determine soil organic matter and total N contents. The potassium dichromate external heating method was used to determine soil organic matter content (Blakemore et al., 1972). The Kjeldahl method and the alkaline-hydrolysable diffusion method were used to determine total N and alkaline-hydrolysable N content (Bremner, 1996). Soil available P was extracted with 0.5 mol L-1 NaHCO3 (soil: solution=1:20) and measured with the Olsen method (Olsen et al., 1954). Soil available K was extracted with 1 mol L-1 NH4Ac (soil: solution=1:10) and measured with the flame photometry method (Carson, 1980). Soil pH was measured with 0.01 mol L-1 CaCl2 slurry (soil: solution=1:2.5) using a glass electrode (Lu, 1999).

Nematode analysis

Field moist subsamples (100 g) of each sample were used to extract nematodes with the sugar flotation and centrifugation method (Barker et al., 1985). The nematode populations were expressed as 100 g-1 dry soil. After counting the total number of nematodes using an anatomical lens, two hundred nematodes per sample were randomly selected and identified to genus according to esophageal and morphology characteristics using an inverted compound microscope (Mal & Lyon, 1975; Ying, 1998).

The characteristics of the nematode communities were described using the following approaches: (1) total number of nematodes per 100 g dry soil; (2) the number of soil free-living nematodes per 100 g dry soil; (3) trophic groups: (a) bacterial feeders; (b) fungal feeders; (c) plant feeders; and (d) omnivore-predators (Yeates et al. 1993).

Statistical analysis

One-way variance analysis (one-way ANOVA) was used to detect differences between different treatments. Differences at the P < 0.05 level were considered statistically significant under the least significant difference (LSD) test. All statistical analyses and the stepwise regression were performed using SPSS 18.0 version software package.

Ethical Approval and/or Informed Consent

This article does not contain any studies with human participants or animals by any of the authors.

Results

Soil physical-chemical properties

Soil organic matter, total N, alkaline-hydrolysable N and available P content were significantly (F = 82.892, P < 0.001 in soil organic matter; F = 39.068, P < 0.001 in soil total N; F = 18.383, P < 0.001 in alkaline-hydrolysable N; F = 224.353, P < 0.001 in available P) higher in the manure combined with chemical fertilizer treatment than in the chemical fertilizer alone and unfertilized treatment. Soil available K content were significantly (F = 6.443, P = 0.002) higher in the manure combined with NPK fertilizer treatment than in the other fertilization treatments and unfertilized control (Table 1).

Total nematode abundance

Total number of nematodes had an increasing tendency with soil nutrient input increments in rice and wheat fields (Fig. 1). Total numbe r of nematode was 1.25 – 2.37 times greater in rice field and was 1.08 – 2.97 times greater in wheat field in the fertilization treatments than in the unfertilized treatment. In particular, the increase was significant in the NPK and manure combined with the chemical fertilizer treatments (F = 31.452, P < 0.001 in rice field; F = 5.253, P = 0.005 in wheat field).

Fig. 1.

Fig. 1

Open in a new tab

Total nematode abundance after different fertilization treatments in the rice field (A) and wheat field (B). Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment. Data are means ± SD (n = 3). Different letters (a, b, c) above the column indicate significant differences (P < 0.05) among treatments according to LSD multiple comparison.

Nematode trophic group abundance

Like the total number of nematodes, the number of soil free- living nematodes (bacterial-feeders + fungal-feeders + omnivores + predators) had an increasing tendency with soil nutrient input increments in rice and wheat fields. In particular, the increase was significant (F = 41.455, P < 0.001) in the manure combined with chemical fertilizer treatments in rice field. Moreover, the number of soil free-living nematodes were significantly (F = 9.890, P = 0.005) higher in the NPK treatment than in the NP, N and unfertilized treatments under the rice field (Table 2).

Table 2.

The number of soil nematodes (individuals 100 g-1 dry soil) after different fertilization treatments in rice and wheat fields.

Treatment FN BF FF PF OP Prodorylaimus
Rice Control 262.8d 71.9a 6.9a 110.7a 184.1d 82.3d
field N 270.2d 75.2a 8.4a 195.2a 186.6d 93.6d
NP 339.0d 104.9a 11.6a 181.4a 222.5d 128.7cd
NPK 477.2c 141.2a 6.0a 173.7a 330.0c 197.6c
MN 619.1b 113.2a 7.2a 151.7a 498.7b 446.8b
MNP 704.1ab 66.0a 5.2a 117.0a 633.0a 561.0a
MNPK 772.2a 129.5a 5.9a 111.7a 636.7a 588.7a
Wheat Control 470.2c 65.9bc 10.0a 210.8a 394.3c 178.6d
field N 562.2c 89.0bc 2.5a 173.9a 470.7c 170.0d
NP 578.6c 134.0ab 0.0a 213.0a 444.7c 176.5d
NPK 942.8bc 195.2a 11.2a 202.2a 736.3bc 499.7cd
MN 1238.2b 162.1a 0.0a 232.4a 1076.1b 971.3bc
MNP 1293.0b 58.8c 3.9a 195.2a 1230.2ab 1103.3ab
MNPK 1907.2a 195. 6a 4.0a 115.9a 1707.6a 1591.2a
Open in a new tab

FN: the number of free-living nematodes in soil; BF: bacterial feeders; FF: fungal feeders; PF: plant feeders; OP: omnivores and predators. Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment.

Different letters (a, b, c) in the same column indicate significant differences (P < 0.05) among treatments at the same sampling times according to LSD multiple comparison.

The bacteria-feeding nematode abundance was not significantly different among treatments in rice field; however, the bacteria-feeding nematode abundances were significantly (F = 6.000, P = 0.003) higher in the MNPK, MN, NPK treatments than in the MNP, N and unfertilized treatments in wheat field (Table 2). The fungi-feeding nematode were the least abundant trophic group in this study. Plant-feeding nematodes were the second-most dominant trophic groups. The number of fungi-feeding and plant-feeding nematodes were not significantly different among treatments in rice and wheat fields. The omnivorous and predatory nematodes were the most dominant groups in the present study (Table 2). The number of omnivore-predators was 1.01 – 3.46 times greater in rice field and was 1.19 – 4.33 times greater in wheat field in the fertilization treatments than in the unfertilized treatment. In particular, omnivore and predator abundances were significantly (F = 58.636, P < 0.001) higher in the manure combined with the chemical fertilizer treatments than in the chemical fertilizer alone and the unfertilized treatments in rice field. Omnivore and predator abundances were significantly (F = 5.553, P = 0.013) higher in the MNPK treatment than in the chemical fertilizer alone and unfertilized treatments in wheat field. Omnivore and predator abundances were significantly (F = 9.640, P = 0.005) higher in the NPK treatment than in the NP, N and unfertilized treatments in rice field. A total of 39 nematode taxa were identified in the present study, of which 11 were bacterial feeders, 5 were fungal feeders, 6 were plant feeders, 12 were omnivores and 5 were predators

(Table 3, 4). The number of Prodorylamus were significantly (F = 46.0201, P < 0.05) higher in the manure combined with the chemical fertilizer treatment than in the chemical fertilizer alone and the unfertilized treatments in rice field (Table 2).

Table 3.

The number of soil nematode taxa (individuals 100 g-1 dry soil) for each treatment in rice field.

Genus Guild Control N NP NPK MN MNP MNPK
Protorhabditis Ba1 0.0 0.0 1.9 0.0 0.0 0.0 0.0
Rhabditis Ba1 0.0 0.0 0.0 0.0 0.0 0.0 3.1
Panagrolaimus Ba1 1.3 3.3 3.7 4.0 7.3 2.6 42.4
Cephalobus Ba2 4.2 6.6 1.9 0.0 0.0 2.6 0.0
Eucephalobus Ba2 3.7 1.7 3.4 4.8 4.8 2.6 6.3
Acrobeloides Ba2 3.3 3.8 0.0 0.0 9.6 0.0 3.1
Monhystera Ba2 0.0 0.0 0.0 1.9 2.4 0.0 0.0
Plectus Ba2 3.8 6.7 8.7 17.5 24.8 26.6 13.7
Prismatolaimus Ba3 4.6 4.6 10.0 30.6 14.7 10.6 30.8
Pseudoaulolaimus Ba3 48.9 44.2 73.5 80.3 39.8 18.2 24.7
Amphidelus Ba4 2.0 4.2 1.9 2.0 9.8 2.7 5.2
Aphelenchoides Fu2 0.0 0.0 1.9 0.0 7.2 5.2 5.9
Tylencholaimus Fu4 2.5 0.0 1.9 0.0 0.0 0.0 0.0
Doryllium Fu4 3.1 8.4 7.8 6.0 0.0 0.0 0.0
Leptonchus Fu4 1.3 0.0 0.0 0.0 0.0 0.0 0.0
Malenchus H2 20.8 14.9 20.1 4.3 12.5 5.4 0.0
Basiria H2 43.5 126.4 96.5 98.9 35.3 48.0 39.2
Psilenchus H2 22.9 22.5 22.3 4.8 4.8 0.0 0.0
Tylenchorhynchus H3 0.0 0.0 0.0 0.0 32.5 13.4 11.1
Hirschmanniella H3 22.1 24.8 33.3 56.0 66.6 50.2 61.4
Belondira H5 1.4 6.6 9.3 9.7 0.0 0.0 0.0
Pristionchus Om1 0.0 0.0 0.0 0.0 4.8 2.6 5.6
Lordellonema Om4 0.0 0.0 0.0 0.0 0.0 5.4 0.0
Prodorylaimus Om4 82.3 93.6 128.7 197.6 446.8 561.0 588.7
Mesodorylaimus Om4 26.5 18.4 21.1 45.6 2.4 5.3 6.3
Eudorylaimus Om4 13.9 12.1 0.0 14.2 15.0 15.9 3.1
Thorneella Om4 1.4 0.0 0.0 0.0 0.0 0.0 0.0
Pungentus Om4 2.5 1.3 0.0 0.0 0.0 2.7 0.0
Aporcelaimus Om5 7.1 4.7 3.4 2.0 22.4 13.5 5.4
Sectonema Om5 1.3 0.0 0.0 2.4 0.0 0.0 0.0
Tripyla Ca3 0.0 0.0 0.0 2.4 0.0 0.0 0.0
Iotonchus Ca4 0.0 0.0 0.0 0.0 0.0 2.7 5.4
Mylonchulus Ca4 0.0 1.3 3.1 2.0 2.6 8.0 10.9
Laevides Ca5 49.1 55.2 66.1 63.7 4.8 15.9 11.3
Open in a new tab

Functional guild classifications are made based on the feeding habits and life-cycle characteristics (Ba: bacterivores, Fu: fungivores, Ca: Carnivores, Om: omnivores, H: herbivores) (Yeates, 1993). Suffix numbers are c-p values for the taxon (Bongers & Bongers, 1998). Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment.

Table 4.

The number of soil nematode taxa (individuals 100 g-1 dry soil) for each treatment in wheat field.

Genus Guild Control N NP NPK MN MNP MNPK
Protorhabditis Ba1 0.0 4.8 0.0 0.0 0.0 0.0 0.0
Rhabditis Ba1 0.0 0.0 2.6 0.0 0.0 0.0 0.0
Panagrolaimus Ba1 0.0 11.8 10.5 7.8 23.3 4.0 4.0
Cephalobus Ba2 2.7 2.3 2.7 6.2 4.0 0.0 0.0
Eucephalobus Ba2 0.0 0.0 0.0 0.0 4.0 4.0 0.0
Acrobeloides Ba2 0.0 4.8 2.6 0.0 4.0 0.0 0.0
Monhystera Ba2 4.7 0.0 2.5 3.2 0.0 0.0 13.9
Plectus Ba2 0.0 14.7 28.3 69.8 30.7 22.2 93.9
Prismatolaimus Ba3 9.7 21.1 56.5 32.6 47.3 15.7 54.9
Pseudoaulolaimus Ba3 48.9 29.4 28.3 72.5 49.1 13.0 28.8
Amphidelus Ba4 0.0 0.0 0.0 3.2 0.0 0.0 0.0
Aphelenchoides Fu2 2.3 0.0 0.0 0.0 0.0 0.0 0.0
Ditylenchus Fu2 0.0 0.0 0.0 0.0 0.0 3.9 0.0
Tylencholaimus Fu4 0.0 0.0 0.0 4.8 0.0 0.0 0.0
Doryllium Fu4 7.7 2.5 0.0 6.4 0.0 0.0 4.0
Malenchus H2 0.0 2.3 5.1 14.7 0.0 0.0 0.0
Basiria H2 136.4 115.7 105.2 75.4 106.1 76.6 36.9
Psilenchus H2 5.2 7.3 23.0 12.6 5.7 0.0 0.0
Tylenchorhynchus H3 2.7 0.0 0.0 0.0 34.2 58.3 18.1
Hirschmanniella H3 66.5 43.8 77.0 88.8 86.4 60.3 60.9
Belondira H5 0.0 4.9 2.7 10.7 0.0 0.0 0.0
Pristionchus Om1 6.4 16.9 12.8 3.2 7.9 11.8 13.9
Coomansinema Om4 0.0 0.0 2.7 0.0 4.0 4.0 0.0
Ecumenicus Om4 2.3 0.0 0.0 0.0 0.0 0.0 0.0
Prodorylaimus Om4 178.6 170.0 176.5 499.7 971.3 1103.3 1591.2
Mesodorylaimus Om4 57.8 79.7 65.0 63.4 13.6 23.4 18.1
Eudorylaimus Om4 6.4 0.0 2.5 0.0 0.0 7.9 26.7
Thorneella Om4 7.3 0.0 0.0 0.0 0.0 0.0 0.0
Pungentus Om4 13.5 12.3 15.3 6.4 0.0 7.9 0.0
Aporcelaimus Om5 10.5 7.4 2.7 34.5 24.1 18.3 33.9
Labronema Om4 0.0 7.3 0.0 0.0 0.0 7.9 0.0
Sectonema Om5 5.0 4.8 5.1 0.0 0.0 0.0 0.0
Tripyla Ca3 2.3 0.0 10.5 9.6 8.8 3.9 5.9
Miconchus Ca4 8.0 9.7 12.6 24.1 9.7 16.9 4.0
Iotonchus Ca4 2.3 9.7 0.0 0.0 9.6 10.4 0.0
Laevides Ca5 93.7 152.9 139.1 95.5 27.2 14.3 13.9
Open in a new tab

Functional guild classifications are made based on the feeding habits and life-cycle characteristics (Ba: bacterivores, Fu: fungivores, Ca: carnivores (predators), Om: omnivores, H, plant feeders (herbivores) (Yeates, 1993). Suffix numbers are c-p values for the taxon (Bongers & Bongers, 1998). Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment.

Crop yield

Rice and wheat yields were significantly (F = 3.764, P = 0.019 in rice; F = 91.648, P < 0.001 in wheat) influenced by the different fertilization treatments (Table 5). Rice grain yields were 1.23 – 1.73 times greater in the fertilization treatments than in the unfertilized treatment. In particular, rice grain yields were significantly (F = 5.265, P = 0.015) higher in the MNPK treatment than in the chemical fertilizer alone and the unfertilized treatments. Rice grain yields were significantly (F = 5.415, P = 0.014) higher in the MNPK, MNP, MN treatments than in the N and unfertilized treatments; nevertheless, there were no significant differences between the N and unfertilized treatments.

Table 5.

Crop grain yields after different fertilization treatments.

Treatment Rice grain yield (t/ha) Wheat grain yield (t/ha)
Control 3.79d 2.24c
N 4.66cd 2.32c
NP 5.13bc 3.13b
NPK 5.17bc 3.23b
MN 6.04ab 4.56a
MNP 6.10ab 4.65a
MNPK 6.55a 4.74a
Open in a new tab

Control, the unfertilized treatment; N, the inorganic nitrogen fertilizer treatment; NP, the inorganic nitrogen and phosphorus fertilizer treatment; NPK, the inorganic nitrogen, phosphorus and potassium fertilizer treatment; MN, the manure plus inorganic nitrogen fertilizer treatment; MNP, the manure plus inorganic nitrogen and phosphorus fertilizer treatment; MNPK, the manure plus inorganic nitrogen, phosphorus and potassium fertilizer treatment.

Different letters (a, b, c) in the same column indicate significant differences (P < 0.05) among treatments according to LSD multiple comparison.

Wheat grain yields were 1.04 – 2.12 times greater in the fertilization treatments than in the unfertilized treatment. Wheat grain yields were significantly (F = 91.648, P < 0.001) higher in the manure combined with the chemical fertilizer treatments than in the chemical fertilizer alone and in the unfertilized treatments. Moreover, wheat grain were significantly (F = 19.641, P < 0.001) higher in the NPK, NP treatments than in the N alone and in the unfertilized treatments; nevertheless, there was no significant difference between the N alone and the unfertilized treatments.

Regression analysis

Stepwise regression equations were conducted to evaluate soil nematode community parameters in rice and wheat fields. These parameters were significantly associated with rice and wheat grain yields. The number of soil free-living nematode was found to be a significant (F = 23.968, P < 0.001) predictor of rice grain yields. The number of omnivorous and predatory nematodes was found to be a significant (F = 150.214, P < 0.001) predictor of wheat grain yields (Table 6).

Table 6.

Stepwise regression of grain yields of rice and wheat with the soil nematode community.

Predictor variable Constant Coefficient R2 F P
Rice FN 3.368 0.004 0.558 23.968 < 0.001
Wheat OP 1.613 0.005 0.888 150.214 < 0.001
Open in a new tab

FN: the number of soil free-living nematodes; OP: the number of omnivorous and predatory nematodes.

The values are fitted in the equation: y = a + bx1 + cx2; y = grain yield; x1 and x2 are the independent variables; and a, b and c are coefficients.

Discussion

Compared to the unfertilized treatment, the total number of nematode was increased in rice and wheat fields due to fertilizer application. In particular, there was a significant increase in the NPK and manure combined with the chemical fertilizer treatments. Similarly, increasing total nematode abundances after application of manure were also reported by Villenave et al. (2003), Forge et al. (2005) and Hu & Qi (2013). The increase of nematode populations could possibly be linked directly to higher food resources associated with the input of organic matter (Villenave et al., 2003). Increasing total number of nematodes due to application of chemical fertilizer was also reported by other studies (Li et al., 2016; Hu et al., 2017). Villenave et al. (2010) also observed that soil free-living nematodes were increased due to organic and mineral fertilizer use.

Fungi-feeding and plant-feeding nematode abundances were not significantly different among treatments in the present study. This result is not consistent with previous studies showing that organic materials application resulted in an increase of fungal feeders abundances (Ferris & Matute, 2003; Wang et al., 2006; Villenave et al., 2010) and that plant-feeding nematodes were increased due to compost and chemical fertilizer application in a maize field (Hu & Qi, 2010).

The omnivorous and predatory nematodes were the most dominant groups in the present study. In contrast, bacterial feeders were the most abundant group in paddy field (Ou et al., 2005), in yellow squash field (Wang et al., 2006), and in Horqin sandy land (Jiang et al., 2007; Guan et al., 2015). Plant-feeding nematodes were prevalent in maize and wheat fields (Hu & Qi, 2010, 2013; Zhang et al., 2012), in sorghum field (Villenave et al., 2010), and in millet field (Diakhaté et al., 2013). Compared to the unfertilized treatment, the abundance omnivore-predators was increased in rice and wheat fields due to fertilizer use. A similar study also showed that the application of manure to an agricultural field could increase the abundance of omnivorous nematodes (Villenave et al., 2004). Li et al. (2010) reported that organic fertilizer application increased the relative abundance of omnivore-carnivores, but different levels of applied nitrogen fertilizer decreased their relative abundance under greenhouse conditions. The composition and abundance of omnivores and carnivores were not affected by the soil amendments (Villenave et al., 2010) and the effect of organic amendment on omnivorous and predatory nematodes was minimal (Wang et al., 2006). However, Forge et al. (2005) reported that high amount manure and chemical fertilizer application reduced omnivorous nematode abundance, but predacious nematodes were more abundant in manure-treated soil than in fertilized soil. Abundant omnivorous and predatory nematodes in the manure-treated soils suggested that more complex soil food webs are expected to result in greater biodiversity of the belowground organisms mediating multiple soil ecosystem functions (Ferris et al., 2012). For example, carnivores, through preying on plant-parasitic nematodes, were regarded as having potential for the biological regulation of pest species (Steel & Ferris, 2016). The increase of omnivorous and predacious nematodes were beneficial for soil health because omnivores and predators play an important role in further mineralizing soil nutrients tied up in bacteria-feeders or fungi-feeders, as well as preying on other nematodes including plant-parasitic nematodes (Wang et al., 2006; Khan & Kim, 2007). Prodorylamus were the dominant genera in the present study. However, Helicotylenchus and Scutellonema were predominant in millet field (Diakhaté et al., 2013), Pratylenchus and Tylenchorhynchus were dominant in sorghum field (Villenave et al., 2010) and Tylenchorhynchus, Pratylenchus and Rotylenchus were the dominant genera in wheat field (Hu & Qi, 2013). The number of nematode genera (39) in the present study was lower than in paddy field (45) (Lü et al., 2017), in maize field (48) (Liang et al., 2009), and in banana field (56) (Zhong et al., 2017), but similar to the result in a continuous sorghum field (38) (Villenave et al., 2010), in soybean field (37) (Pan et al., 2016), and in Tibetan plateau grassland (41) (Hu et al., 2017).

The number of soil free-living nematode was a significant predictor of rice grain yields and the number of omnivorous and predatory nematode was a significant predictor of wheat grain yields. Similarly, Mandal et al. (2007) reported that alkaline phosphatase activity was significant (P < 0.001) for predicting the grain yields of wheat at the dough stages of wheat growth. Hu & Qi (2013) observed that soil free-living nematode was a significant (P < 0.05) predictor of wheat grain yields during the jointing stage of wheat growth.

Conclusions

Based on these results, we deduced that long-term application of organic manure and chemical fertilizer modified the soil nematode community structure, increased crop yields. Total nematode abundance had an increasing tendency with soil nutrient input increments in rice and wheat fields. The number of total soil nematode was significantly increased due to organic manure combined with the chemical fertilizer application in rice field. Omnivores and predators and Prodorylaimus were significantly higher in the organic manure combined with NPK fertilizer treatments than in the chemical fertilizer alone and in the unfertilized treatments in rice and wheat fields. Stepwise regressions revealed that the number of soil free-living nematode was a significant predictor of rice grain yields (R2 = 0.56) and the number of omnivorous and predatory nematode was a significant predictor of wheat grain yield (R2 = 0.89). In conclusion, long-term application of organic manure combined with chemical fertilizer could increase nematode abundances and raise crop yields. Organic manure combined with chemical fertilizer application was recommended in agricultural ecosystem.

Acknowledgements

This Project Sponsored by the National Key Research and Development Program of China (2018YFD0200500); the Special Fund for Agro-scientific Research in the Public Interest of China (201203030); the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (2012-940); the Scientific and Technological Key Achievements Cultivation Project of Hubei Academy of Agricultural Sciences (2017CGPY01) and the National Natural Science Foundation of China (31300442).

Footnotes

Conflict of interest

The authors declare there is no conflict of interest.

References

  1. Barker K.R., Carter C.C., Sasser J.N. An Advanced Treatise on Meloidogyne, Methodology. Vol. 2. North Carolina State University Graphics; Raleigh, NC: 1985. p. 223. [Google Scholar]
  2. Blakemore L.C., Searle P.L., Daly B.K. Methods for Chemical Analysis of Soils. Wellington: 1972. New Zealand Soil Bureau Report 10 A. Government Printers. [Google Scholar]
  3. Bongers T., Bongers M.. Functional diversity of nematodes. Appl. Soil Ecol. 1998;10:253. doi: 10.1016/S0929-1393(98)00123-1. –. [DOI] [Google Scholar]
  4. Brar B.S., Singh K., Dheri G.S., Kumar B.. Carbon sequestration and soil carbon pools in a rice-wheat cropping system: Effect of long-term use of inorganic fertilizers and organic manure. Soil Till. Res. 2013;128:30. doi: 10.1016/j.still.2012.10.001. –. [DOI] [Google Scholar]
  5. Bremner J.M. Sparks D.L. Methods of Soil Analysis. Madison: 1996. Nitrogen-Total; pp. 1085–1086. Part 3. Soil Science Society of America Book Series 5. –. [Google Scholar]
  6. Carson P.L. Dahnke WC. Recommended chemical soil test procedures for the North Central Region. Fargo: 1980. Recommended potassium test; pp. 17–18. Bulletin 499. North Dakota Agricultural Experiment Station. –. [Google Scholar]
  7. Čerevková A., Miklisová D., Cagáň L.. Effects of experimental insecticide applications and season on soil nematode communities in a maize field. Crop Prot. 2017;92:1. doi: 10.1016/j.cropro.2016.10.007. –. [DOI] [Google Scholar]
  8. Debreczeni B., Körschens M.. Long-term field experiments of the world. Arch. of Agron. Soil Sci. 2003;49(5):465. doi: 10.1080/03650340310001594754. –. [DOI] [Google Scholar]
  9. Diacono M., Montemurro F.. Long-term effects of organic amendments on soil fertility. A review. Agron. Sustain. Dev. 2010;30(2):401. doi: 10.1051/agro/2009040. –. [DOI] [Google Scholar]
  10. Diakhaté S., Villenave C., Diallo N.H., Ba A.O., Djigal D., Masse D., Sembène P.M., Chapuis-lardy L.. The influence of a shrub-based intercropping system on the soil nematofauna when growing millet in Senegal. Eur. J. Soil Biol. 2013;57:35. doi: 10.1016/j.ejsobi.2013.04.003. –. [DOI] [Google Scholar]
  11. Ding J.L., Jiang X., Guan D.W., Zhao B.S., Ma M.C., Zhou B.K., Cao F.M., Yang X.H., Li L., Li J.. Influence of inorganic fertilizer and organic manure application on fungal communities in a long-term field experiment of Chinese Mollisols. Appl. Soil Ecol. 2017;111:114. doi: 10.1016/j.apsoil.2016.12.003. –. [DOI] [Google Scholar]
  12. Ferris H., Matute M.M.. Structural and functional succession in the nematode fauna of a soil food web. Appl. Soil Ecol. 2003;23(2):93. doi: 10.1016/S0929-1393(03)00044-1. –. [DOI] [Google Scholar]
  13. Ferris H., Pocasangre L.E., Serrano E., Muñoz J., Garcia S., Perichi G., Martinez G.. Diversity and complexity complement apparent competition: Nematode assemblages in banana plantations. Acta Oecol. 2012;40:11. doi: 10.1016/j.act-ao.2012.02.003. –. [DOI] [Google Scholar]
  14. Forge T.A., Bittman S., Kowalenko C.G.. Responses of grassland soil nematodes and protozoa to multi-year and single-year applications of dairy manure slurry and fertilizer. Soil Biol. Biochem. 2005;37(10):1751. doi: 10.1016/j.soilbio.2004.11.013. doi: 10.1016/j.soilbio.2004.11.013. –. Geisseler, D., Scow, K.M. (2014): Long-term effects of mineral fertilizers on soil microorganisms – A review. Soil Biol. Biochem. 75: 54 – 63. Doi. [DOI] [Google Scholar]
  15. Gruzdeva L.I., Matveeva E.M., Kovalenko T.E.. Changes in soil nematode communities under the impact of fertilizers. Eurasian Soil Sci. 2007;40(6):681. doi: 10.1134/S1064229307. –. [DOI] [Google Scholar]
  16. Guan P.T., Zhang X.K., Yu J., Ma N.N., Liang W.J.. Variation of soil nematode community composition with increasing sand-fixation year of Caragana microphylla bioindication for desertification restoration. Ecol. Eng. 2015;81:93. doi: 10.1016/j.ecoleng.2015.04.011. –. [DOI] [Google Scholar]
  17. Gutiérrez C., Fernández C., Escuer M., Campos-herrera R., Rodríguez M.E.B., Carbonell G., Martín J.A.R.. Effect of soil properties, heavy metals and emerging contaminants in the soil nematodes diversity. Environ. Pollut. 2016;213:184. doi: 10.1016/j.envpol.2016.02.012. –. [DOI] [PubMed] [Google Scholar]
  18. Hopkins D.W., Shiel R.S.. Size and activity of soil microbial communities in long-term experimental grassland plots treated with manure and inorganic fertilizers. Biol. Fert. Soils. 1996;22(1-2):66. doi: 10.1007/BF00384434. –. [DOI] [Google Scholar]
  19. Hoschitz M., Kaufmann R.. Nematode community composition in five alpine habitats. Nematology. 2004;6(5):737. doi: 10.1163/1568541042843531. –. [DOI] [Google Scholar]
  20. Hu C., Li S.L., Qiao Y., Liu D.H., Chen Y.F.. Effects of 30 years repeated fertilizer applications on soil properties, microbes and crop yields in rice-wheat cropping systems. Exp. Agr. 2015;51(3):355. doi: 10.1017/S0014479714000350. –. [DOI] [Google Scholar]
  21. Hu C., Qi Y.C.. Effect of compost and chemical fertilizer on soil nematode community in a Chinese maize field. Eur. J. Soil Biol. 2010;46(3–4):230. doi: 10.1016/j.ejsobi.2010.04.002. –. [DOI] [Google Scholar]
  22. Hu C., Qi Y.C.. Effective microorganisms and compost favor nematodes in wheat crops. Agron. Sustain. Dev. 2013;33(3):573. doi: 10.1007/s13593-012-0130-9. –. [DOI] [Google Scholar]
  23. Hu J., Chen G.R., Hassan W.M., Chen H., Li J.Y., Du G.Z.. Fertilization influences the nematode community through changing the plant community in the Tibetan Plateau. Eur. J. Soil Biol. 2017;78:7. doi: 10.1016/j.ejsobi.2016.11.001. –. [DOI] [Google Scholar]
  24. Jiang D.M., Li Q., Liu F.M., Jiang Y., Liang W.J.. Vertical distribution of soil nematodes in an age sequence of Caragana microphylla plantations in the Horqin Sandy Land, Northeast China. Ecol. Res. 2007;22(1):49. doi: 10.1007/s11284-006-0187-5. –. [DOI] [Google Scholar]
  25. Khan Z., Kim Y.H.. A reviews on the role of predatory soil nematodes in the biological control of plant parasitic nematodes. Appl. Soil Ecol. 2007;35(2):370. doi: 10.1016/j.apsoil.2006.07.007. –. [DOI] [Google Scholar]
  26. Li N., Pan F.J., Han X.Z., Zhang B.. Development of soil food web of microbes and nematodes under different agricultural practices during the early stage of pedogenesis of a Mollisol. Soil Biol. Biochem. 2016;98:208. doi: 10.1016/j.soilbio.2016.04.011. doi: 10.1016/j.soilbio.2016.04.011. –. [DOI] [Google Scholar]
  27. Liang W.J., Lou Y.L., Li Q., Zhong S., Zhang X.K., Wang J.K.. Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biol. Biochem. 2009;41(5):883. doi: 10.1016/j.soilbio.2008.06.018. –. [DOI] [Google Scholar]
  28. Lu R. K. Methods of Soil and Agricultural Chemistry. China Agriculture Science and Technology Press; Beijing: 1999. in Chinese. [Google Scholar]
  29. LÜ Y., Bai W., Wang X.F., Cai Q., Liang W.J.. Responses of soil micro-food web to land use change from upland to paddy fields with different years of rice cultivation. Pedosphere. 2017;27(1):155. doi: 10.1016/S1002-0160(15)60102-3. –. [DOI] [Google Scholar]
  30. Mal W.F., Lyon H.H. Pictorial key to genera of pant-parasitic nematodes. Cornell University Press; Ithaca & London: 1975. pp. 1–219. –. [Google Scholar]
  31. Mandal A., Patra A.K., Singh D., Swarup A., Masto R.E.. Effect of long-term application of manure and fertilizer on biological and biochemical activities in soil during crop development stages. Bioresource Technol. 2007;98(18):3585. doi: 10.1016/j.biortech.2006.11.027. –. Doi: 535 10.1016/j. biortech.2006.11.027. [DOI] [PubMed] [Google Scholar]
  32. Mcsorley R., Gallaher R.N.. Effect of compost and maize cultivars on plant-parasitic nematodes. J. Nematol. 1997;29(4S):731–736. [PMC free article] [PubMed] [Google Scholar]
  33. Miao Y.X., Stewart B.A., Zhang F.S.. Long-term experiments for sustainable nutrient management in China. A review. Agron. Sustain. Dev. 2011;31(2):397. doi: 10.1051/agro/2010034. doi: 10.1051/agro/2010034. –. Miles, R.J., Brown, J.R. (2011): The sanborn field experiment: implications for long-term soil organic carbon levels. Agron. J. 103(1): 268 – 278. Doi. [DOI] [Google Scholar]
  34. Neher D.A.. Role of nematodes in soil health and their use as indicators. J Nematol. 2001;33(4):161. –. [PMC free article] [PubMed] [Google Scholar]
  35. Olsen R.S., Cole V.C., Watanabey F.S., Dean L.A.. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. 1954:939. US Department of Agricultural Circulation, pp. [Google Scholar]
  36. Ou W., Liang W.J., Jiang Y., Li Q., Wen D.Z.. Vertical distribution of soil nematodes under different land use types in an aquic brown soil. Pedobiologia. 2005;49(2):139. doi: 10.1016/j.pedobi.2004.10.001. –. [DOI] [Google Scholar]
  37. Pan F.J., Li N., Zou W.X., Han X.Z., Mclaughlin N.B.. Soil nematode community structure and metabolic footprint in the early pedogenesis of a Mollisol. Eur. J. Soil Biol. 2016;77:17. doi: 10.1016/j.ejsobi.2016.09.004. –. [DOI] [Google Scholar]
  38. Peterson G.A., Lyon D.J., Fenster C.R.. Valuing long-term field experiments: quantifying the scientific contribution of a long-term tillage experiment. Soil Sci. Soc. Am. J. 2012;76(3):757. doi: 10.2136/sssaj2011.0413. –. [DOI] [Google Scholar]
  39. Porazinska D.L., Duncan L.W., Mcsorley R., Graham J.H.. Nematode communities as indicators of status and processes of a soil ecosystem influenced by agricultural management practices. Appl. Soil Ecol. 1999;13(1):69. doi: 10.1016/S0929-1393(99)00018-9. –. [DOI] [Google Scholar]
  40. Scharroba A., Kramer S., Kandeler E., Ruess L.. Spatial and temporal variation of resource allocation in an arable soil drives community structure and biomass of nematodes and their role in the micro-food web. Pedobiologia. 2016;59(3):111. doi: 10.1016/j.pedobi.2016.03.005. –. [DOI] [Google Scholar]
  41. Singh J., Brar B.S., Sekhon B.S., Mavi M.S., Singh G., Kaur G.. Impact of long-term phosphorous fertilization on Olsen-P and grain yields in maize-wheat cropping sequence. Nutr. Cycl. Agroecosys. 2016;106(2):157. doi: 10.1007/s10705-016-9796-8. doi: 10.1007/s10705-016-9796-8. –. Steel, H., Ferris, H. (2016): Soil nematode assemblages indicate the potential for biological regulation of pest species. Acta Oecol. 73: 87 – 96. Doi. [DOI] [Google Scholar]
  42. Villenave C., Bongers T., Ekschmitt K., Fernandes P., Oliver R.. Changes in nematode communities after manuring in millet fields in Senegal. Nematology. 2003;5(3):351. doi: 10.1163/156854103769224340. –. [DOI] [Google Scholar]
  43. Villenave C., Ekschmitt K., Nazaret S. & Bongers T.. Interactions between nematodes and microbial communities in a tropical soil following manipulation of the soil food web. Soil Biol Biochem. 2004;36(12):2033. doi: 10.1016/j.soilbio.2004.05.022. doi: 10.1016/j.soilbio.2004.05.022. –. Villenave, C., Saj, S., Pablo, A.L., Sall, S., Djigal, D., Chotte, J.L., Bonzi, M. (2010): Influence of long-term organic and mineral fertilization on soil nematofauna when growing Sorghum bicolor in Burkina Faso. Biol. Fert. Soils 46: 659-670. Doi. [DOI] [Google Scholar]
  44. Wang K.H., Mcsorley R., Marshall A., Gallaher R.N.. Influence of organic Crotalaria juncea hay and ammonium nitrate fertilizers on soil nematode communities. Appl. Soil Ecol. 2006;31(3):186. doi: 10.1016/j.apsoil.2005.06.006. –. [DOI] [Google Scholar]
  45. Wei W.L., Yan Y., Cao J., Christie P., Zhang F.S., Fan M.S.. Effects of combined application of organic amendments and fertilizers on crop yield and soil organic matter: An integrated analysis of long-term experiments. Agr. Ecosysyst. Environ. 2016;225:86. doi: 10.1016/j.agee.2016.04.004. –. [DOI] [Google Scholar]
  46. Yeates G.W., Bongers T., De goede R.G.M., Freckman D.W., Georgieva S.S.. Feeding habits in soil nematode families and genera – an outline for ecologists. J Nematol. 1993;25(3):315. –. Ying, W.Y. (1998): Pictorial keys to soil animals of China Beijing: China Science Press, pp 51 – 89. [PMC free article] [PubMed] [Google Scholar]
  47. Zhang Q., Liang G., Zhou W., Sun J., Wang X., He P.. Fatty-acid profiles and enzyme activities in soil particle-size fractions under long-term fertilization. Soil Sci. Soc. Am. J. 2016;80(1):97. doi: 10.2136/sssaj2015.07.0255. –. [DOI] [Google Scholar]
  48. Zhang X.K., Ferris W., Mitchell J., Liang W.J.. Ecosystem services of the soil food web after long-term application of agricultural management practices. Soil Biol. Biochem. 2017a;111:36. doi: 10.1016/j.soilbio.2017.03.017. –. [DOI] [Google Scholar]
  49. Zhang X.K., Li Q., Zhu A.N., Liang W.J., Zhang J.B., Steinberger Y.. Effects of tillage and residue management on soil nematode communities in North China. Ecol Indic. 2012;13(1):75. doi: 10.1016/j.ecolind.2011.05.009. –. [DOI] [Google Scholar]
  50. Zhao J., Li D.J., Fu S.L., He X.Y., Fu Z.Y., Zhang W., Wang K.L.. Using the biomasses of soil nematode taxa as weighting factors for assessing soil food web conditions. Ecol Indic. 2016;60:310. doi: 10.1016/j.ecolind.2015.06.003. –. [DOI] [Google Scholar]
  51. Zhang Q., Liang G.Q., Myrold D.D., Zhou W.W.. Variable responses of ammonia oxidizers across soil particle-size fractions affect nitrification in a long-term fertilizer experiment. Soil Biol. Biochem. 2017b;105:25. doi: 10.1016/j.soilbio.2016.11.005. –. [DOI] [Google Scholar]
  52. Zhong S., Zeng h.c Jin Z.Q.. Influences of different tillage and residue management systems on soil nematode community composition and diversity in the tropics. Soil Biol. Biochem. 2017;107:234. doi: 10.1016/j.soilbio.2017.01.007. –. [DOI] [Google Scholar]

Articles from Helminthologia are provided here courtesy of De Gruyter

RESOURCES