Litter additions reduce the side effects of biocides on soil nematode communities in  forest

Y. Lü; W. F. Xue; P. P. Yan

Détails du journal et du numéro

Helminthologia

Détails du magazine

Format: Magazine
eISSN: 1336-9083
Première parution: 22 Apr 2006
Périodicité: 4 fois par an
Langues: Anglais

Biocides are employed in many parts of the world for protection of crops from pests and diseases. However, biocides may exert toxicity to organisms other than their intended targets (Komárek et al., 2010; Rahmat et al., 2019; Ju et al., 2017). Intensive and repeated biocides inputs can threaten endangered species, reduce biodiversity, inhibited bacterial and fungal growth, and impact on soil quality (Fernández-Calviño et al., 2021). Previous studies have found that biocides adsorption positively correlated with contents of clay and organic matter (Komárek et al., 2010; Chelinho et al., 2011). Although organic matter plays a crucial role in decreasing adverse effects of biocides (Agegnehu et al., 2017), the insights into the degree and consequence of organic matter influence on biocides have not been well studied. Previous studies advocated the use of soil nematode parameters to assess ecological risk ( Yang et al., 2017) and to monitor environmental safety (Wilson 2009), because they can rapidly reflect changes in soil, and provide accurate data to indicate soil quality (Chagnon et al., 2018). Therefore, soil nemaotdes can be used as potential indicators to estimate the influence of organic matter on the effects of biocides on soil ecosystem.

Star anise (fruit of Illicium verum Hook. f.) is an important traditional medicine as well as a commonly used spice in China (Itoigawa et al., 2004). It is also the industrial source of shikimic acid, a major component of drug for the bird flu H5N1 strain of virus (Itoigawa et al., 2004; Wang et al., 2011). Nearly 90 % of star anise production in China is from Guangxi province (Liu 2012). With the development of anise production, the plant diseases and insect pests have attracted more and more attention, and biocides have been applied as an effective method to reduce the pest and disease damage as well as maintain the anise productivity (Liu & Nong 2005). However, our knowledge about the influence of biocides on non-target organisms was limited, especially when they combined with litter additions. The objectives of the present study are to evaluate changes in the soil nematode communities influencing by fungicide and insecticide with and without litter additions, to estimate the litter addition as an alternative management to resist the side effects of chemical biocides.

Materials and Methods

Experimental design

The experiment took place in Nanning, Guangxi province, China (107°45’-108°51’E, 22°13’-23°32’ N). The annual mean temperature and precipitation of this region are 21.6 ˚C and 1304 mm, respectively. The soil is classified as red soil (Udic Ferrosols) according to the Chinese Soil Taxonomy Classification (Gong, 1994). This experiment was arranged as a split-plot with different biocides treatments as main plots, and non-litter added and litter added treatments as subplots. Each plot has three replications. Within each plot, 4 treatments including control, insecticide treatment, fungicide treatment and insecticide × fungicide treatment are randomly distributed. Each treatment was divided into two subplots with or without litter addition. Each subplot (2 m × 2 m) was placed 2 m apart in order to minimize the risk of contamination.

Carbosulfan and benomyl-hymexazol are broad-spectrum biocides, which are often applied to forest pest control. For the insecticide treatment, carbosulfan (granular formulation and 5 % active ingredient) was applied at rate of 250 g/m² in July, it was mixed with soil (non-litter-added subplots) or litter (litter-added subplots) and spread under the crown geometry. For the fungicide treatment, benomyl-hymexazol (6 % of benomyl and 24 % of hymexazol) was applied at rate of 90 g/m² (3 times as recommended dose and diluted 300 times with water when in use). Because the fungicide is liquid, it could not be intercepted by litter layer (about 2 – 3 cm in depth), the fungicide was applied twice in each subplot on the litter layer (litter-added subplots) or bare soil (non-litter-added subplots), in July and August. Control plots received an equivalent volume of water. Insecticide × fungicide treatment applied both insecticide and fungicide as described above. I. verum forests can produce a large amount of litter every year. Shao et al. (2015) found litter provided basal resources for soil microorganisms and connects with soil organism closely in I. verum forest, so it was chosen as a remediator for soil ecosystem disturbance. Litter of I. verum was collected from the previous growth season. Upon collection, litter was oven dried to constant weight at 60 °C and then mechanically chopped to smaller particles (length=2 cm). Litter was completely mixed before adding to each treatment with pH 5.50, total C 483.0 g/kg and total N 15.9 g/kg. In litter-added subplot, 2000 g/m² dry litter was covered uniformly on the soil surface under the crown geometry, a layer of fine soil was sprinkled in order to prevent the litter from being blown away.

Soil sampling and analysis

Soil samples were collected in October. Four random cores (10 cm × 10 cm × 10 cm) were combined to form one composite sample for each treatment. Each composite sample was placed in an individual plastic bag and sealed. All samples were kept at 4 °C for biological and chemical analysis.

Soil organic carbon (SOC) was measured by the dichromate oxidation, and soil total nitrogen (TN) was determined with an ultraviolet spectrophotometer after Kjeldahl digestion (Bao 2000). Total carbon and total nitrogen of plant litter were measured using a Vario MACRO cube Elementary Analyzer (Elementar Analysensysteme Vario MACRO cube, Germany).Microbial biomass carbon (MBC) microbial biomass nitrogen (MBN) were determined using the fumigation extraction method (Wu et al., 2006).

Soil nematode extraction, identification and analysis

Nematodes were extracted from 100 g soil sample (fresh weight) by a modified cotton-wool filter method (Liang et al., 2009). The 100 individuals (or the total number in samples containing less than 100 individuals) of each sample were identified to genus level. The nematodes were assigned to the following trophic groups characterized by feeding habits (1) bacterivores; (2) fungivores; (3) omnivore-predators and (4) herbivores (Yeates et al., 1993).

The following ecological indices were calculated:

(1) Dominance index (λ), $λ = \sum p_{i}^{2},$ $\lambda=\sum p_{i}^{2},$where pi is the proportion of individuals in the i-th taxon (Simpson 1949);

(2) Shannon index (H^ʹ), H^ʹ = -Σp_i(lnp_i), where p_i is the proportion of individuals in the i-th taxon (Shannon & Weaver 1949);

(3) Generic richness GR = (S - 1)/ln(N), where S is the number of taxa and N is the number of total nematodes (Yeates & Bongers 1999);

(4) Nematode channel ratio (NCR), NCR= B/(B+F), where B is the number of bacterivores and F is the number of fungivores (Yeates 2003);

(5) Structure index $S I = 100 \times \sum k_{s} n_{s} / \sum k_{s} n_{s} + \sum k_{b} n_{b}));$ $S I=100 \times\left(\sum k_{s} n_{s} /\left(\sum k_{s} n_{s}+\sum k_{b} n_{b}\right)\right);$

(6) Enrichment index $EI = 100 \times \sum k_{e} n_{e} / \sum k_{e} n_{e} + \sum k_{b} n_{b})),$ $\text { EI }=100 \times\left(\sum k_{e} n_{e} /\left(\sum k_{e} n_{e}+\sum k_{b} n_{b}\right)\right),$

where k_b is the weight assigned to guilds BF₂ and FF₂ and n_b is the abundance of nematodes in guilds BF₂ and FF₂, which indicate basal characteristics of the food web; k_s is the weight assigned to guilds BF₃-BF₅, FF₃-FF₅, and OP₂-OP₅, n_s is the abundance of nematodes in these guilds, which represent the structure condition of the food web; k_e the weight assigned to guilds BF₁ and FF₂, and n_e is the abundance of nematodes in these guilds, which represent an enriched condition of the food web (Ferris et al., 2001). BF_x, FF_x, OP_x, (where x = 1-5) represent the functional guilds of nematodes that are bacterivores, fungivores, predators and omnivores where the guilds have the characters indicated by x on the colonizer-persister (cp) scale (1-5) following Bongers and Bongers (1998).

Plotting EI and SI provides a graphic representation of nematode faunal profile that indicate whether the soil community is basal, enriched, or structured and stable (Ferris et al., 2001). The faunal profile can be divided into four quadrants, quadrant A (SI<50, EI>50) shows that food web is affected by high disturbances and food web condition is disturbed; quadrant B (SI>50, EI>50) means that the disturbance level is low or moderate and food web condition is maturing; quadrant C (SI>50, EI<50) represents an undisturbed and structured food web; quadrant D (SI<50, EI<50) indicates a stressed and degraded food web (Ferris et al., 2001).

Statistical analysis

Data of nematode abundance was ln (x + 1) transformed prior to statistical analysis for normality of data. Three-way ANOVA was applied to assess the effects of litter addition, insecticide treatment, fungicide treatment and their interactions on soil nematodes communities. P-values < 0.05 were considered significant. The relationship between nematode genera and environmental factors was examined based on redundancy analysis (RDA) using the CANOCO software, version 5.0. A Monte Carlo permutation test (499 permutations) was used to test the significance of first and all canonical axes.

Results

Soil nematodes assemblage

In non-litter-added plots, the application of fungicide decreased the abundance of omnivores-predators in comparison with control (CK); while an opposite trend was observed in the treatments with litter additions (Fig.1). Similarly, the decrease in the abundance of herbivores in the insecticide treatments was only observed in the non-litter-added plots. In addition, more bacterivores observed in the treatments with litter addition. The abundance of fungivores only showed response to the fungicide treatments, with higher abundance of fungivores observed in the treatments with litter addition.

Changes of nematode abundance in different treatments (n=3, means + 1SE). Results of Three way-ANOVAs with significant effects of factors (litter, insecticide and fungicide) and their interactions are shown: L, litter addition; I, insecticide treatment; F, fungicide treatment; L×I, interaction between litter addition and insecticide; L×F, interaction between litter addition and fungicide; I×F, interaction between insecticide and fungicide; L×I×F, interaction between litter addition, insecticide and fungicide.*, P < 0.05; **, P < 0.01, ns, non-significant. Different letters (a,b etc.) show significant differences among different treatments with and without litter addition, respectively, as determined by Tukey’s honestly significant difference test, P<0.05.

The interactive effects between insecticide and litter addition significantly influenced nematode ecological indices (P < 0.05). In non-litter-added plots, the application of insecticide decreased the indices of H’, GR and NCR and increased λ. However, in litter-added plots, insecticide did not cause obvious variations in the values of λ and H’ (Table 1). The interactive effects between fungicide and litter addition were only found in GR. In comparison with the control, the application of fungicide increased GR in litter-added plots, but decreased GR in non-litter-added plots.

Table 1

Nematode taxonomic diversity indices and channel ratio in different treatments (means ± SE).

Treatments		λ	H'	GR	NCR
	Non-Litter	0.15 ± 0.03	2.23 ± 0.15	3.36 ± 0.22	0.68 ± 0.08
Control	Litter	0.18 ± 0.01	2.15 ± 0.06	3.34 ± 0.07	0.47 ± 0.10
	Non-Litter	0.40 ± 0.17	1.29 ± 0.35	1.83 ± 0.35	0.30 ± 0.13
Insecticide (I)	Litter	0.20 ± 0.02	2.00 ± 0.12	2.84 ± 0.33	0.57 ± 0.04
Fungicide(F)	Non-Litter	0.14 ± 0.02	2.24 ± 0.10	2.91 ± 0.40	0.56 ± 0.16
	Litter	0.11 ± 0.01	2.42 ± 0.06	3.67 ± 0.23	0.39 ± 0.05
	Non-Litter	0.55 ± 0.22	0.95 ± 0.47	1.14 ± 0.57	0.28 ± 0.17
I×F	Litter	0.13 ± 0.01	2.38 ± 0.10	3.67 ± 0.17	0.55 ± 0.12

Litter (L)		ns	ns	**	ns
Insecticide (I)		**	**	**	ns
Fungicide (F)		ns	ns	ns	ns
L×I		*	**	*	**
L×F		ns	ns	*	ns
I×F		ns	ns	ns	ns
L×I×F		ns	ns	ns	ns

λ, dominance index; H’, diversity index; GR, Generic richness; NCR, nematode channel ratio. *, P < 0.05; **, P < 0.01, ns, non-significant.

Correlations between soil nematode communities and environmental factors

The RDA showed a correlation between soil nematodes and the abiotic factors (Fig. 2). The ordination of nematodes was strongly affected by litter addition and soil abiotic factors. Acrobeloides, Ditylenchus, Plectus, Rhabditidae, Aphelenchus and Panagrellus, associated with litter, SOC and TN positively, Basiria, Heterocephalobus and Rotylenchus associated with insecticide and CK without litter addition positively.

Redundancy analysis (RDA) of the soil nematode communities and soil abiotic variables. Species fit range more than 40% were presented. N, non-litter-added plots; L, litter-added plots. CK, control; I, insecticide application; F, fungicide application; I×F, interaction between insecticide and fungicide.

Soil food web structure and stability

Nematode faunal profiles showed that nematodes from CK and insecticide × fungicide treated soil in litter-added plots were located in quadrant B. Nematodes form single insecticide and fungicide treated soil in litter-added plots and from CK and single fungicide treated soil in non-litter-added plots were located in quadrant C. While nematodes impacted by insecticide and insecticide × fungicide without litter addition were located in quadrant D (Fig. 3).

Changes in the structure and enrichment conditions of soil food web in different treatments (means ± 1SE). N, non-litter-added plots; L, litter-added plots. CK, control; I, insecticide application; F, fungicide application; I×F, interaction between insecticide and fungicide.

Discussion

The effects of litter addition on responses of nematode assemblage to insecticide

Our results showed that non-target soil nematodes were affected adversely by insecticide without litter addition. Neher et al.(2014) also reported soils treated with conventional insecticide contained less complex and successionally mature nematode communities. Insecticide declined nematode diversity via increasing dominant genera abundance (λ) and decreasing rare genera abundance (H’) in non-litter-added plots (Table 1). Both herbivores and bacterivores were impaired by insecticide significantly, and omnivore-predators disappeared in insecticide × fungicide treatment without litter addition (Fig.1). The loss of this high trophic level of the soil micro-food web may cause loss of ecosystem functions (Van der Wurff et al., 2007). Thus, insecticide may decrease the risk of trees disease by killing harmful insect and herbivores, but simultaneously disturb the balance of soil ecosystem by impacting biodiversity.

Litter resources play an important role in shaping nematode community structure and function (Zhao et al., 2021). In our study, the increased soil SOC and TN content correlated with most nematode species positively with litter addition (Fig. 2), which indicated that litter could influence nematode communities by altering soil nutrient content. Litter with high SOC content influences insecticide behavior differently than soil (Puglisi et al., 2012). Singh and Srivastava (2009) suggested clay and organic matter could accelerate adsorption of Carbofuran. Moreover, microarthropods that feed directly on litter and microbes can fragment litter and disperse microbes in the process of feeding (Neher et al., 2012). The increase in microbial carbon and microbial nitrogen confirmed that nematodes could access to more food resource which is conducive to maintaining community stability with litter addition (Supplementary Table 1). Although litter addition could keep nematode away from adverse effects of biocides, it may limit the effectiveness of insecticide via increasing the abundance of herbivores. Litter addition may result in higher soil moisture retention and nutrient content, and then increase abundance of herbivores. Consequently, further studies were needed to evaluate the proper quantity of litter applied in order to match the needs for both keeping insecticide effectively and maintaining soil ecosystem functions.

Supplementary Table 1

Selected properties of soil abiotic factors, microbial carbon and microbial nitrogen in different treatments (means ± SE).

Treatment	SOC (g/kg)		TN (g/kg)		MBC (mg/kg)		MBN (mg/kg)

	Non-Litter	Litter	Non-Litter	Litter	Non-Litter	Litter	Non-Litter	Litter
CK	13.8 ±0.10	17.24 ±0.26	1.54 ±0.05	1.64 ±0.04	132.69 ±7.88	150.10 ±8.81	20.77 ± 0.28	40.15 ±14.56
Insecticide	13.03 ±0.19	15.65 ±0.70	1.37 ±0.06	1.45 ±0.10	106.96 ±8.94	116.69 ±18.83	23.68 ± 9.31	26.80 ± 7.31
Fungicide	12.3 ±0.16	14.21 ±0.41	1.29 ±0.06	1.35 ±0.09	80.09 ± 17.83	115.23 ±27.83	17.27 ±4.38	24.77 ± 7.38
IxF	13.18 ±0.34	15.25 ±0.17	1.33 ±0.07	1.37 ±0.01	83.02 ± 15.46	112.91 ±31.82	24.40 ± 4.03	31.46 ±10.03

Litter	***		ns		**		*
Insecticide	ns		ns		ns		ns
Fungicide	**		**		ns		ns
Lx\|	ns		ns		ns		ns
LxF	ns		ns		ns		ns
IxF	**		*		ns		ns
Lx\|xF	ns		ns		*		ns

*P < 0.05; **, P < 0.01, ns, non-significant.

Unexpectedly, fungivorous seem not to be impaired by insecticide (Fig. 1), one possible reason is that relatively higher microbial carbon content in insecticide treatment can provide more food resources for fungivorous (Supplementary Table 1). Another reason could be that most fungivorous correlated with soil SOC and TN closely (Fig. 2), and those nutrients were not impacted by insecticide (Supplementary Table 1). Additionally, fungivorous are dependent partly on root-derived resources (Kudrin et al., 2021), which help them resist environment stress. Chen et al. (2016) also found some specific microorganisms adapted or improved their tolerance to hexaconazole.

The effects of litter addition on responses of nematode assemblage to fungicide

The effects of fungicide on the nematode appeared not to be relevant in non-litter added plots, our results are in agreement with findings of Neher et al.(2019), in which they found that biocides had no effects on nematode trophic diversity, maturity indices and channel index, and assumed that crop rotation and tillage are main contributors to changes of nematode communities rather than biocides. Wang (2014) reported that soil nematodes showed a clear recovery trend 120 days after fungicide application. Fungicide was applied twice in July and August, and soil samples were collected in October. Therefore, we propose that spaced fungicide application gave nematodes time to recover and adapt to environment. Compensatory mechanisms such as the increase of tolerant nematode were also probably responsible for this phenomenon. For instance, Aphelenchoides which was most abundant in fungicide treatment with litter additions also showed tolerance to benomyl (Schmidt et al., 2000) (Supplementary Table 2).

Supplementary Table 2

Nematode genera identified in this study and their relative abundance (%) in the different treatments.

Genera	Non-litter added plots				Litter added plots
Genera	Control	Insecticide	Fungicide	I×F	Control	Insecticide	Fungicide	I×F
Bacterivores
Prismatolaimus	1.5	3.7	1.1	0.7	4.3	2.4	5.5	11.3
Alaimus	0.5	1.6	0.0	0.7	2.2	2.0	1.0	0.7
Paramphidelus	1.0	0.5	0.0	1.3	0.0	0.4	1.4	1.2
Plectus	0.0	0.0	0.0	0.0	1.5	1.3	0.4	1.5
Drilocephalobus	3.0	2.1	0.0	0.0	0.4	0.0	4.2	1.5
Rhabditidae	0.5	1.0	1.3	0.8	3.3	2.1	0.3	1.5
Acrobeloides	3.0	2.1	1.3	0.8	7.7	13.6	9.9	13.4
Eucephalobus	11.6	9.7	4.9	15.3	4.0	6.1	1.0	2.7
Monhystera	0.0	0.0	0.0	0.0	0.0	0.0	2.0	0.0
Heterocephalobus	6.0	4.0	7.3	3.0	0.0	0.0	0.0	0.0
Panagrellus	0.0	0.0	0.0	0.0	1.4	0.9	0.4	5.0
Fungivores
Tylencholaimus	1.1	3.7	0.0	0.0	1.4	1.3	9.8	7.6
Aphelenchoides	8.6	9.2	59.5	65.8	20.0	11.7	18.9	16.4
Ditylenchus	0.0	0.0	0.0	0.0	9.0	3.4	8.2	4.8
Aphelenchus	2.8	6.0	0.0	0.8	0.0	0.0	0.0	0.0
Filenchus	3.5	3.7	0.0	0.0	2.5	3.8	3.0	7.2
Herbivores
Helicotylenchus	12.3	13.5	8.7	3.4	29.8	36.2	17.6	12.8
Rotylenchus	26.0	28.1	9.9	5.4	6.8	8.1	2.3	1.0
Dolichodoridae	0.0	0.0	0.0	0.0	1.5	0.8	0.0	1.2
Paratylenchus	0.6	0.0	0.0	0.0	0.0	0.0	0.0	0.0
Macroposthonia	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.2
Basiria	6.1	4.6	0.0	2.2	0.0	0.0	0.0	0.0
Malenchus	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0
Rotylenchulus	2.5	0.0	2.4	0.0	0.0	0.0	0.0	0.0
Pratylenchus	0.0	0.0	0.0	0.0	0.4	0.4	0.9	3.6
Lelenchus	1.1	0.0	0.0	0.0	0.0	0.0	0.4	0.0
Dorylaimellus	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.5
Omnivore-predators
Thonus	0.0	0.0	2.4	0.0	0.4	0.4	0.0	1.5
Dorydorella	1.0	1.0	0.0	0.0	0.0	0.4	0.0	0.0
Aporcelaimidae	0.6	1.0	0.0	0.0	0.0	0.0	0.0	0.0
Eudorylaimus	1.5	0.0	0.0	0.0	0.4	1.3	2.3	0.0
Mesodorylaimus	5.4	0.0	1.1	0.0	1.1	1.7	6.3	0.5
Microdorylaimus	0.0	4.6	0.0	0.0	2.1	1.7	3.0	1.0
Mylonchulus	0.0	0.0	0.0	0.0	0.0	0.0	0.4	0.0
Tripyla	0.0	0.0	0.0	0.0	0.0	0.0	0.9	0.0
Seinura	0.0	0.0	0.0	0.0	0.0	0.0	0.0	2.7

I×F, insecticide × fungicide interaction treatment

Liu et al. (2019) reported the accumulation of litter addition may benefit the nematode community. In our study, fungicide increased the abundance of nematode markedly in litter-added plots (Fig.3). Our results were partly in accordance with the findings of Ekelund (1999) who found that fenpropimorph stimulated fungivorous flagellates and ciliates with glucose addition and suggested that the fungicide effect on soil protozoa was not mediated via effects on fungal populations. Hence, the effect of fungicide on fungivores, obviously, may also have no relation to the reduction of their fungal food source in this study.

The effects of litter addition on food web structure condition

Nematode faunal profile derived from EI and SI can provide information about the status of the soil food web (Ferris et al., 2001). In this study, the samples from insecticide and its interaction with fungicide treatments were all located in quadrant D and separated obviously from single fungicide and the control treatments without litter addition (Fig. 3). Therefore, we propose that soil food web length and connections are significantly reduced in insecticide and its interaction with fungicide treatments without litter addition. Our result was in line with Bai et al. (2017) who revealed that soil food web with high level of pesticides addition was stressed and degraded. Neher et al. (2014) also found SI value in insecticide treatment was lower than in non-insecticide treatment, and suggested insecticide shifted ecological succession back to earlier stages. The contributor for this phenomenon is the reduced abundance of high nutrient level nematodes which have ability to regulate soil food web (Fig.1). The normal operation of soil functions depends on the overall cooperation of soil microorganisms (Álvarez-Martín et al., 2016). SI and EI placed nematode communities into quadrant C and quadrant B with litter addition. It can be assumed that litter addition may help to reduce the adverse effects of biocides and maintained the structure and stability of soil food web. Furthermore, lowest SI value was found in insecticide × fungicide treatment (Fig. 3), suggesting that insecticide and fungicide may accumulate their effects and create worse influence on soil food web than single insecticide or fungicide treatment.

The effects of litter addition on soil decomposition pathway

Liu et al. (2019) reported that litter was a limiting food source for the soil food web. Xu et al. (2013) found litter input is a crucial pathway for carbon and nutrient fluxes to the soil. In this study, litter addition changed soil biota community composition, which in turn may affect soil nutrient decomposition and mineralization. In non-litter-added plots, insecticide changed decomposition pathway from bacteria dominant (NCR > 0.5) to fungi dominant (NCR < 0.5) (Table 1). Because fungi have higher C assimilation efficiencies (Rousk & Bååth 2011), fungi dominant pathway could slow down soil nutrient cycling and decrease nutrient availability (Waring et al.,2013). Alternatively, fungal dominant channel maybe one of the defense mechanisms of soil food web that could promote resistance to environment change. Conversely, in litter-added plots, applications of insecticide resulted in bacterial based channels (NCR > 0.5). The present results are in line with the findings of Sauvadet et al. (2016), in which they show that the bacterial channel developed faster with leaf litter addition. Because bacterial based channels can accelerate decomposition rate, nutrient availability in litter-added plots was higher than in non-litter-added plots.

Conclusion

Litter addition could reduce the damage caused by insecticide and its interaction with fungicide to soil nematodes. In non-litter-added plots, nematode abundance was reduced by insecticide applications. Contrarily, insecticide and its interaction with fungicide did not impact nematodes negatively in litter-added plots. Based on our findings, we suggest that litter addition may extenuate the negative effects of biocides, and maintaining an appropriate level of litter addition is crucial to the successful management of soil environment.

Figures et tableaux

Nematode taxonomic diversity indices and channel ratio in different treatments (means ± SE).

Treatments		λ	H'	GR	NCR
	Non-Litter	0.15 ± 0.03	2.23 ± 0.15	3.36 ± 0.22	0.68 ± 0.08
Control	Litter	0.18 ± 0.01	2.15 ± 0.06	3.34 ± 0.07	0.47 ± 0.10
	Non-Litter	0.40 ± 0.17	1.29 ± 0.35	1.83 ± 0.35	0.30 ± 0.13
Insecticide (I)	Litter	0.20 ± 0.02	2.00 ± 0.12	2.84 ± 0.33	0.57 ± 0.04
Fungicide(F)	Non-Litter	0.14 ± 0.02	2.24 ± 0.10	2.91 ± 0.40	0.56 ± 0.16
	Litter	0.11 ± 0.01	2.42 ± 0.06	3.67 ± 0.23	0.39 ± 0.05
	Non-Litter	0.55 ± 0.22	0.95 ± 0.47	1.14 ± 0.57	0.28 ± 0.17
I×F	Litter	0.13 ± 0.01	2.38 ± 0.10	3.67 ± 0.17	0.55 ± 0.12

Litter (L)		ns	ns	**	ns
Insecticide (I)		**	**	**	ns
Fungicide (F)		ns	ns	ns	ns
L×I		*	**	*	**
L×F		ns	ns	*	ns
I×F		ns	ns	ns	ns
L×I×F		ns	ns	ns	ns

Nematode genera identified in this study and their relative abundance (%) in the different treatments.

Genera	Non-litter added plots				Litter added plots
Genera	Control	Insecticide	Fungicide	I×F	Control	Insecticide	Fungicide	I×F
Bacterivores
Prismatolaimus	1.5	3.7	1.1	0.7	4.3	2.4	5.5	11.3
Alaimus	0.5	1.6	0.0	0.7	2.2	2.0	1.0	0.7
Paramphidelus	1.0	0.5	0.0	1.3	0.0	0.4	1.4	1.2
Plectus	0.0	0.0	0.0	0.0	1.5	1.3	0.4	1.5
Drilocephalobus	3.0	2.1	0.0	0.0	0.4	0.0	4.2	1.5
Rhabditidae	0.5	1.0	1.3	0.8	3.3	2.1	0.3	1.5
Acrobeloides	3.0	2.1	1.3	0.8	7.7	13.6	9.9	13.4
Eucephalobus	11.6	9.7	4.9	15.3	4.0	6.1	1.0	2.7
Monhystera	0.0	0.0	0.0	0.0	0.0	0.0	2.0	0.0
Heterocephalobus	6.0	4.0	7.3	3.0	0.0	0.0	0.0	0.0
Panagrellus	0.0	0.0	0.0	0.0	1.4	0.9	0.4	5.0
Fungivores
Tylencholaimus	1.1	3.7	0.0	0.0	1.4	1.3	9.8	7.6
Aphelenchoides	8.6	9.2	59.5	65.8	20.0	11.7	18.9	16.4
Ditylenchus	0.0	0.0	0.0	0.0	9.0	3.4	8.2	4.8
Aphelenchus	2.8	6.0	0.0	0.8	0.0	0.0	0.0	0.0
Filenchus	3.5	3.7	0.0	0.0	2.5	3.8	3.0	7.2
Herbivores
Helicotylenchus	12.3	13.5	8.7	3.4	29.8	36.2	17.6	12.8
Rotylenchus	26.0	28.1	9.9	5.4	6.8	8.1	2.3	1.0
Dolichodoridae	0.0	0.0	0.0	0.0	1.5	0.8	0.0	1.2
Paratylenchus	0.6	0.0	0.0	0.0	0.0	0.0	0.0	0.0
Macroposthonia	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.2
Basiria	6.1	4.6	0.0	2.2	0.0	0.0	0.0	0.0
Malenchus	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0
Rotylenchulus	2.5	0.0	2.4	0.0	0.0	0.0	0.0	0.0
Pratylenchus	0.0	0.0	0.0	0.0	0.4	0.4	0.9	3.6
Lelenchus	1.1	0.0	0.0	0.0	0.0	0.0	0.4	0.0
Dorylaimellus	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.5
Omnivore-predators
Thonus	0.0	0.0	2.4	0.0	0.4	0.4	0.0	1.5
Dorydorella	1.0	1.0	0.0	0.0	0.0	0.4	0.0	0.0
Aporcelaimidae	0.6	1.0	0.0	0.0	0.0	0.0	0.0	0.0
Eudorylaimus	1.5	0.0	0.0	0.0	0.4	1.3	2.3	0.0
Mesodorylaimus	5.4	0.0	1.1	0.0	1.1	1.7	6.3	0.5
Microdorylaimus	0.0	4.6	0.0	0.0	2.1	1.7	3.0	1.0
Mylonchulus	0.0	0.0	0.0	0.0	0.0	0.0	0.4	0.0
Tripyla	0.0	0.0	0.0	0.0	0.0	0.0	0.9	0.0
Seinura	0.0	0.0	0.0	0.0	0.0	0.0	0.0	2.7

Selected properties of soil abiotic factors, microbial carbon and microbial nitrogen in different treatments (means ± SE).

Treatment	SOC (g/kg)		TN (g/kg)		MBC (mg/kg)		MBN (mg/kg)

	Non-Litter	Litter	Non-Litter	Litter	Non-Litter	Litter	Non-Litter	Litter
CK	13.8 ±0.10	17.24 ±0.26	1.54 ±0.05	1.64 ±0.04	132.69 ±7.88	150.10 ±8.81	20.77 ± 0.28	40.15 ±14.56
Insecticide	13.03 ±0.19	15.65 ±0.70	1.37 ±0.06	1.45 ±0.10	106.96 ±8.94	116.69 ±18.83	23.68 ± 9.31	26.80 ± 7.31
Fungicide	12.3 ±0.16	14.21 ±0.41	1.29 ±0.06	1.35 ±0.09	80.09 ± 17.83	115.23 ±27.83	17.27 ±4.38	24.77 ± 7.38
IxF	13.18 ±0.34	15.25 ±0.17	1.33 ±0.07	1.37 ±0.01	83.02 ± 15.46	112.91 ±31.82	24.40 ± 4.03	31.46 ±10.03

Litter	***		ns		**		*
Insecticide	ns		ns		ns		ns
Fungicide	**		**		ns		ns
Lx\|	ns		ns		ns		ns
LxF	ns		ns		ns		ns
IxF	**		*		ns		ns
Lx\|xF	ns		ns		*		ns

Références

Álvarez-Martín, A., Hilton, S.L., Bending, G.D., Rodríguez-Cruz, M.S., Sánchez-Martín, M.J. (2016): Changes in activity and structure of the soil microbial community after application of azoxystrobin or pirimicarb and an organic amendment to an agricultural soil. Appl Soil Ecol, 106: 47–57. DOI: 10.1016/j.apsoil.2016.05.005 Álvarez-Martín A. Hilton S.L. Bending G.D. Rodríguez-Cruz M.S. Sánchez-Martín M.J. 2016 Changes in activity and structure of the soil microbial community after application of azoxystrobin or pirimicarb and an organic amendment to an agricultural soil Appl Soil Ecol 106 47 57 10.1016/j.apsoil.2016.05.005Ouvrir le DOI Search in Google Scholar

Bai, P.H., Liu, Q.Z., Liu, B.S., Feng, Y.R., Liu, C.Y. (2017): Soil nematode community and soil properties in pear orchards as affected by frequent applications of pesticides. J Fruit Sci, 34: 715–722 (In Chinese). DOI: 10.13925/j.cnki.gsxb.20160438 Bai P.H. Liu Q.Z. Liu B.S. Feng Y.R. Liu C.Y. 2017 Soil nematode community and soil properties in pear orchards as affected by frequent applications of pesticides J Fruit Sci 34 715 722 (In Chinese) 10.13925/j.cnki.gsxb.20160438Ouvrir le DOI Search in Google Scholar

Bao, S.D. (2000): Soil Agro-Chemistrical Analysis. Agriculture Press, Beijing, China (In Chinese) Bao S.D. 2000 Soil Agro-Chemistrical Analysis Agriculture Press Beijing, China (In Chinese)Search in Google Scholar

Bongers, T., Bongers, M. (1998): Functional diversity of nematodes. Appl Soil Ecol, 10: 239–251. DOI: 10.1016/S0929-1393(98)00123-1 Bongers T. Bongers M. 1998 Functional diversity of nematodes Appl Soil Ecol 10 239 251 10.1016/S0929-1393(98)00123-1Ouvrir le DOI Search in Google Scholar

Chagnon, P.L., Brown, C., Stotz, G.C., Cahill Jr, J.F. (2018): Soil biotic quality lacks spatial structure and is positively associated with fertility in a northern grassland. J Ecol, 106: 195–206. DOI: 10.1111/1365-2745.12844 Chagnon P.L. Brown C. Stotz G.C. Cahill Jr J.F. 2018 Soil biotic quality lacks spatial structure and is positively associated with fertility in a northern grassland J Ecol 106 195 206 10.1111/1365-2745.12844Ouvrir le DOI Search in Google Scholar

Chelinho, S., Sautter, S.K., Cachada, A., Abrantes, I., Brown, G., Duarte, A.C., Sousa, J.P. (2011): Carbofuran effects in soil nematode communities: Using trait and taxonomic based approaches. Ecotox Environ Safe, 74: 2002–2012. DOI: 10.1016/j. ecoenv.2011.07.015 Chelinho S. Sautter S.K. Cachada A. Abrantes I. Brown G. Duarte A.C. Sousa J.P. 2011 Carbofuran effects in soil nematode communities: Using trait and taxonomic based approaches Ecotox Environ Safe 74 2002 2012 10.1016/j. ecoenv.2011.07.015Ouvrir le DOI Search in Google Scholar

Chen, M.J., Liu, C.S., Chen, P.C., Tong, H., Li, F.B., Qiao, J.T., Qing, L. (2016): Dynamics of the microbial community and Fe(III)-reducing and dechlorinating microorganisms in response to pentachlorophenol transformation in paddy soil. J Hazard Mater, 312: 97–105. DOI: 10.1016/j.jhazmat.2016.03.059 Chen M.J. Liu C.S. Chen P.C. Tong H. Li F.B. Qiao J.T. Qing L. 2016 Dynamics of the microbial community and Fe(III)-reducing and dechlorinating microorganisms in response to pentachlorophenol transformation in paddy soil J Hazard Mater 312 97 105 10.1016/j.jhazmat.2016.03.05927017395Ouvrir le DOI Search in Google Scholar

Ekelund, F. (1999): The impact of the fungicide fenpropimorph (Corbel^®) on bacterivorous and fungivorous protozoa in soil. J Appl Ecol, 36: 233–243. DOI: 10.1046/j.1365-2664.1999.00393.x Ekelund F. 1999 The impact of the fungicide fenpropimorph (Corbel^®) on bacterivorous and fungivorous protozoa in soil J Appl Ecol 36 233 243 10.1046/j.1365-2664.1999.00393.xOuvrir le DOI Search in Google Scholar

Fernández-Calviño, D., Rousk, J., Bååth, E., Bollmann, U.E., Bester, K., Brandt, K.K. (2021): Short-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms. Soil Biol Biochem, 154: 108130. DOI: 10.1016/j.soilbio.2021.108130 Fernández-Calviño D. Rousk J. Bååth E. Bollmann U.E. Bester K. Brandt K.K. 2021 Short-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms Soil Biol Biochem 154 108130 10.1016/j.soilbio.2021.108130Ouvrir le DOI Search in Google Scholar

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. DOI:10.1016/S0929-1393(01)00152-4 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 10.1016/S0929-1393(01)00152-4Ouvrir le DOI Search in Google Scholar

Gong, Z.T. (1994): Chinese soil taxonomic classification (First Proposal). Institute of Soil Science Academia Sinica, Nanjing, China. Itoigawa, M., Ito, C., Tokuda, H., Enjo, F., Nishino, H., Furukawa, H. (2004): Cancer chemopreventive activity of phenylpropanoids and phytoquinoids from Illicium plants. Cancer Lett, 214: 165–169. DOI: 10.1016/j.canlet.2004.05.005 Gong Z.T. 1994 Chinese soil taxonomic classification (First Proposal) Institute of Soil Science Academia Sinica, Nanjing, China. Itoigawa, M., Ito, C., Tokuda, H., Enjo, F., Nishino, H., Furukawa, H. (2004): Cancer chemopreventive activity of phenylpropanoids and phytoquinoids from Illicium plants. Cancer Lett 214 165 169 10.1016/j.canlet.2004.05.00515363542Ouvrir le DOI Search in Google Scholar

Ju, C., Xu, J., Wu, X.H., Dong, F.S., Liu, X.G., Tian, C.Y., Zeng, Y.Q. (2017): Effects of hexaconazole application on soil microbes community and nitrogen transformations in paddy soils. Sci Total Environ, 609: 655–663. DOI: 10.1016/j.scitotenv.2017.07.146 Ju C. Xu J. Wu X.H. Dong F.S. Liu X.G. Tian C.Y. Zeng Y.Q. 2017 Effects of hexaconazole application on soil microbes community and nitrogen transformations in paddy soils Sci Total Environ 609 655 663 10.1016/j.scitotenv.2017.07.14628763662Ouvrir le DOI Search in Google Scholar

Komárek, M., Cadková, E., Chrastný, V., Bordas, F., Bollinger, J.C. (2010): Contamination of vineyard soils with fungicides: A review of environmental and toxicological aspects. Environ Int, 36: 138–151. DOI: 10.1016/j.envint.2009.10.005 Komárek M. Cadková E. Chrastný V. Bordas F. Bollinger J.C. 2010 Contamination of vineyard soils with fungicides: A review of environmental and toxicological aspects Environ Int 36 138 151 10.1016/j.envint.2009.10.00519913914Ouvrir le DOI Search in Google Scholar

Kudrin, A.A., Zuev, A.G., Taskaeva, A.A., Konakova, T.N., Kolesnikova, A.A., Gruzdev, I.V., Gabov, D.N., Yakovleva, E.V., Tiunov, A.V. (2021): Spruce girdling decreases abundance of fungivorous soil nematodes in a boreal forest. Soil Biol Biochem, 155: 108184. DOI: 10.1016/j.soilbio.2021.108184 Kudrin A.A. Zuev A.G. Taskaeva A.A. Konakova T.N. Kolesnikova A.A. Gruzdev I.V. Gabov D.N. Yakovleva E.V. Tiunov A.V. 2021 Spruce girdling decreases abundance of fungivorous soil nematodes in a boreal forest Soil Biol Biochem 155 108184 10.1016/j.soilbio.2021.108184Ouvrir le DOI Search in Google Scholar

Liang, W.J., Lou, Y.L., Li, Q., Zhong, S., Zhang, X.K., Wang, J.K. (2009): Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biol Biochem, 41: 883–890. DOI: 10.1016/j.soilbio.2008.06.018 Liang W.J. Lou Y.L. Li Q. Zhong S. Zhang X.K. Wang J.K. 2009 Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China Soil Biol Biochem 41 883 890 10.1016/j.soilbio.2008.06.018Ouvrir le DOI Search in Google Scholar

Liu, J.S., Chen, Y., Du, C., Liu, X.X., Ma, Q.H., Zhang, X., Wang, D.L. (2019): Interactive effects of nitrogen addition and litter on soil nematodes in grassland. Eur J Soil Sci, 70: 697–706. DOI: 10.1111/ejss.12779 Liu J.S. Chen Y. Du C. Liu X.X. Ma Q.H. Zhang X. Wang D.L. 2019 Interactive effects of nitrogen addition and litter on soil nematodes in grassland Eur J Soil Sci 70 697 706 10.1111/ejss.12779Ouvrir le DOI Search in Google Scholar

Liu, Y.H. (2012): Market status of Chinese Illicium verum export to ASEAN countries and corresponding strategies for industry development. J South Agr, 43: 891–894 (In Chinese) Liu Y.H. 2012 Market status of Chinese Illicium verum export to ASEAN countries and corresponding strategies for industry development J South Agr 43 891 894 (In Chinese)Search in Google Scholar

Liu, Y.H., Nong, W.D. (2005) Anise tree common diseases and their prevention and control countermeasures. Guangxi Trop Agr, 6: 43–44 (In Chinese) Liu Y.H. Nong W.D. 2005 Anise tree common diseases and their prevention and control countermeasures Guangxi Trop Agr 6 43 44 (In Chinese)Search in Google Scholar

Neher, D.A., Muthumbi A.W.N., Dively G.P. (2014) Impact of coleopteran-active Bt corn on non-target nematode communities in soil and decomposing corn roots. Soil Biol Biochem, 76: 127e135. DOI: 10.1016/j.soilbio.2014.05.019 Neher D.A. Muthumbi A.W.N. Dively G.P. 2014 Impact of coleopteran-active Bt corn on non-target nematode communities in soil and decomposing corn roots Soil Biol Biochem 76 127e135 10.1016/j.soilbio.2014.05.019Ouvrir le DOI Search in Google Scholar

Neher, D.A., Weicht, T.R., Barbercheck, M.E. (2012): Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils. Appl Soil Ecol, 54: 14–23. DOI: 10.1016/j. apsoil.2011.12.001 Neher D.A. Weicht T.R. Barbercheck M.E. 2012 Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils Appl Soil Ecol 54 14 23 10.1016/j. apsoil.2011.12.001Ouvrir le DOI Search in Google Scholar

Neher, D.A., Nishanthana, T., Grabaub, Z.J., Chen, S.Y. (2019): Crop rotation and tillage affect nematode communities more than biocides in monoculture soybean. Appl Soil Ecol, 140: 89–97. DOI: 10.1016/j.apsoil.2019.03.016 Neher D.A. Nishanthana T. Grabaub Z.J. Chen S.Y. 2019 Crop rotation and tillage affect nematode communities more than biocides in monoculture soybean Appl Soil Ecol 140 89 97 10.1016/j.apsoil.2019.03.016Ouvrir le DOI Search in Google Scholar

Puglisi, E., Vasileiadis, S., Demiris, K., Basi, D., Karpouzas, D.G., Capri, E., Cocconcelli, P.S., Trevisan, M. (2012): Impact of fungicides on the diversity and function of non-target ammonia-oxidizing microorganisms residing in a litter soil cover. Microb Ecol, 64: 692–701. DOI: 10.1007/s00248-012-0064-4 Puglisi E. Vasileiadis S. Demiris K. Basi D. Karpouzas D.G. Capri E. Cocconcelli P.S. Trevisan M. 2012 Impact of fungicides on the diversity and function of non-target ammonia-oxidizing microorganisms residing in a litter soil cover Microb Ecol 64 692 701 10.1007/s00248-012-0064-422584298Ouvrir le DOI Search in Google Scholar

Rahmat Ullah, M., Dijkstra, F.A. (2019): Fungicide and bactericide effects on carbon and nitrogen cycling in soils: A Meta-Analysis. Soil Syst, 3: 3020023. DOI: 10.3390/soilsystems3020023 Rahmat Ullah M. Dijkstra F.A. 2019 Fungicide and bactericide effects on carbon and nitrogen cycling in soils: A Meta-Analysis Soil Syst 3 3020023 10.3390/soilsystems3020023Ouvrir le DOI Search in Google Scholar

Rousk, J., Bååth, E. (2011): Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol, 78: 17–30. DOI: 10.1111/j.1574-6941.2011.01106.x Rousk J. Bååth E. 2011 Growth of saprotrophic fungi and bacteria in soil FEMS Microbiol Ecol 78 17 30 10.1111/j.1574-6941.2011.01106.x21470255Ouvrir le DOI Search in Google Scholar

Sauvadet, M., Chauvat, M., Cluzeau, D., Maron, P.A., Villenave, C., Bertrand, I. (2016): The dynamics of soil micro-food web structure and functions vary according to litter quality. Soil Biol Biochem, 95: 262–274. DOI: 10.1016/j.soilbio.2016.01.003 Sauvadet M. Chauvat M. Cluzeau D. Maron P.A. Villenave C. Bertrand I. 2016 The dynamics of soil micro-food web structure and functions vary according to litter quality Soil Biol Biochem 95 262 274 10.1016/j.soilbio.2016.01.003Ouvrir le DOI Search in Google Scholar

Schmidt, I.K., Rues, L., Bååth, E., Michelsen, A., Ekelund, F., Jonason, S. (2000): Long-term manipulation of the microbes and microfauna of two subarctic heaths by addition of fungicide, bactericide, carbon and fertilizer. Soil Biol Biochem, 32: 707–720. DOI: 10.1016/S0038-0717(99)00207-2 Schmidt I.K. Rues L. Bååth E. Michelsen A. Ekelund F. Jonason S. 2000 Long-term manipulation of the microbes and microfauna of two subarctic heaths by addition of fungicide, bactericide, carbon and fertilizer Soil Biol Biochem 32 707 720 10.1016/S0038-0717(99)00207-2Ouvrir le DOI Search in Google Scholar

Shannon, C.E., Weaver, W. (1949): The mathematical theory of communication. University of Illinois Press, Urbana and Chicago. Shannon C.E. Weaver W. 1949 The mathematical theory of communication University of Illinois Press Urbana and ChicagoSearch in Google Scholar

Shao, Y.H., Bao, W.K., Chen, D.M., Eisenhauer, N., Zhang, W.X., Pang, X.Y., Xu, G.L., Fu, S.L. (2015): Using structural equation modeling to test established theory and develop novel hypotheses for the structuring forces in soil food webs. Pedobiologia, 58:137–145. DOI: 10.1016/j.pedobi.2015.06.001 Shao Y.H. Bao W.K. Chen D.M. Eisenhauer N. Zhang W.X. Pang X.Y. Xu G.L. Fu S.L. 2015 Using structural equation modeling to test established theory and develop novel hypotheses for the structuring forces in soil food webs Pedobiologia 58137 145 10.1016/j.pedobi.2015.06.001Ouvrir le DOI Search in Google Scholar

Simpson, E.H. (1949): Measurement of diversity. Nature, 163: 668. DOI: 10.1038/163688a0 Simpson E.H. 1949 Measurement of diversity Nature 163 668 10.1038/163688a0Ouvrir le DOI Search in Google Scholar

Singh, R.P., Srivastava, G. (2009): Adsorption and movement of carbofuran in four different soils varying in physical and chemical properties. Adsorpt Sci Technol, 27: 193–203. DOI: 10.1260/026361709789625270 Singh R.P. Srivastava G. 2009 Adsorption and movement of carbofuran in four different soils varying in physical and chemical properties Adsorpt Sci Technol 27 193 203 10.1260/026361709789625270Ouvrir le DOI Search in Google Scholar

Van der Wurff, A.W.G., Kools, S.A.E., Boivin, M.E.Y., Van der Brink, P.J., Van Megen, H.H.M., Riksen, J.A.G., Doroszuk, A., Kammenga, J.E. (2007): Type of disturbance and ecological history determine structural stability. Ecol Appl, 17: 190–202. DOI: 10.1890/1051-0761(2007)017 Van der Wurff A.W.G. Kools S.A.E. Boivin M.E.Y. Van der Brink P.J. Van Megen H.H.M. Riksen J.A.G. Doroszuk A. Kammenga J.E. 2007 Type of disturbance and ecological history determine structural stability Ecol Appl 17 190 202 10.1890/1051-0761(2007)017Ouvrir le DOI Search in Google Scholar

Wang, G.W., Hu, W.T., Huang, B.K., Qin, L.P. (2011): Illicium verum: A review on its botany, traditional use, chemistry and pharmacology. J Ethnopharmacol, 136: 10–20. DOI: 10.1016/j. jep.2011.04.051 Wang G.W. Hu W.T. Huang B.K. Qin L.P. 2011 Illicium verum: A review on its botany, traditional use, chemistry and pharmacology J Ethnopharmacol 136 10 20 10.1016/j. jep.2011.04.051Ouvrir le DOI Search in Google Scholar

Wang, K.H. (2014): Effect of agrochemical application on soil nematode diversity in the reclamation progress of Sanjiang plain. M.S. thesis, China, University of Chinese Academy of Sciences Wang K.H. 2014 Effect of agrochemical application on soil nematode diversity in the reclamation progress of Sanjiang plain. M.S. thesis China University of Chinese Academy of SciencesSearch in Google Scholar

Waring, B.G., Averill, C., Hawkes, C.V., (2013): Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecol Lett, 16: 887–894. DOI: 10.1111/ele.12125 Waring B.G. Averill C. Hawkes C.V. 2013 Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models Ecol Lett 16 887 894 10.1111/ele.1212523692657Ouvrir le DOI Search in Google Scholar

Wu, J.S., Lin,. Q.M., Huang, Q.Y. (2006): Determination method and application of soil microbial biomass carbon soil microbial carbon and nitrogen. Meteorological Press, Beijing,China (In Chinese) Wu J.S. Lin Q.M. Huang Q.Y. 2006 Determination method and application of soil microbial biomass carbon soil microbial carbon and nitrogen Meteorological Press Beijing,China (In Chinese)Search in Google Scholar

Xu, S., Liu, L.L., Sayer, E.J. (2013): Variability of above-ground litter inputs alters soil physicochemical and biological processes: A meta-analysis of litterfall-manipulation experiments. Biogeosciences, 10: 7423–7433. DOI: 10.5194/bg-10-7423-2013 Xu S. Liu L.L. Sayer E.J. 2013 Variability of above-ground litter inputs alters soil physicochemical and biological processes: A meta-analysis of litterfall-manipulation experiments Biogeosciences 10 7423 7433 10.5194/bg-10-7423-2013Ouvrir le DOI Search in Google Scholar

Yang, Y.F., Cheng, Y.H., Liao, C.M. (2017): Nematode-based biomarkers as critical risk indicators on assessing the impact of silver nanoparticles on soil ecosystems. Ecol Indic, 75: 340–351. DOI: 10.1016/j.ecolind.2016.12.051 Yang Y.F. Cheng Y.H. Liao C.M. 2017 Nematode-based biomarkers as critical risk indicators on assessing the impact of silver nanoparticles on soil ecosystems Ecol Indic 75 340 351 10.1016/j.ecolind.2016.12.051Ouvrir le DOI Search in Google Scholar

Yeates, G.W. (2003): Nematodes as soil indicators: Functional and biodiversity aspects. Biol Fert Soils, 37: 199–210. DOI: 10.1007/s00374-003-0586-5 Yeates G.W. 2003 Nematodes as soil indicators: Functional and biodiversity aspects Biol Fert Soils 37 199 210 10.1007/s00374-003-0586-5Ouvrir le DOI Search in Google Scholar

Yeates, G.W., Bongers, T. (1999): Nematode diversity in agroecosystems. Agr Ecosyst Environ, 74: 113–135. DOI: 10.1016/S0167-8809(99)00033-X Yeates G.W. Bongers T. 1999 Nematode diversity in agroecosystems Agr Ecosyst Environ 74 113 135 10.1016/S0167-8809(99)00033-XOuvrir le DOI Search in Google Scholar

Yeates, G.W., Bongers, T., de G oede, R.G.M., Freckman, D.W., Georgieva, S.S. (1993): Feeding habits in soil nematode families and genera - an outline for soil ecologists. J Nematol, 25: 315–331. DOI: 10.1006/jipa.1993.1100 Yeates G.W. Bongers T. de G oede R.G.M. Freckman D.W. Georgieva S.S. 1993 Feeding habits in soil nematode families and genera - an outline for soil ecologists J Nematol 25 315 331 10.1006/jipa.1993.1100Ouvrir le DOI Search in Google Scholar

Zhao, C.C., Guo, E.H., Shao, Y.H., Zhang, W.X., Zhang, C.L., Liu, Y.C., Li, Y., Zou, X.M., Fu, S.L. (2021): Impacts of litter addition and root presence on soil nematode community structure in a young Eucalyptus plantation in southern China. Forest Ecol Manag, 479: 118633. DOI: 10.1016/j.foreco.2020.118633 Zhao C.C. Guo E.H. Shao Y.H. Zhang W.X. Zhang C.L. Liu Y.C. Li Y. Zou X.M. Fu S.L. 2021 Impacts of litter addition and root presence on soil nematode community structure in a young Eucalyptus plantation in southern China Forest Ecol Manag 479 118633 10.1016/j.foreco.2020.118633Ouvrir le DOI Search in Google Scholar

Helminthologia

Litter additions reduce the side effects of biocides on soil nematode communities in Illicium verum forest

Y. Lü,
Y. Lü,
W. F. Xue et
W. F. Xue et
P. P. Yan
P. P. Yan

Publié en ligne: 17 Dec 2022

Volume & Edition: Volume 59 (2022) - Edition 3 (September 2022)

Pages: 301 - 310

Reçu: 10 May 2022

Accepté: 06 Sep 2022

Détails du journal et du numéro

Helminthologia

Aperçu PDF

Article

Fig.1

Fig.2

Fig.3

Figures et tableaux

Fig.1

Fig.2

Fig.3

Nematode taxonomic diversity indices and channel ratio in different treatments (means ± SE).

Nematode genera identified in this study and their relative abundance (%) in the different treatments.

Selected properties of soil abiotic factors, microbial carbon and microbial nitrogen in different treatments (means ± SE).

Références

Articles récents

Planifiez votre conférence à distance avec Sciendo

Helminthologia

Litter additions reduce the side effects of biocides on soil nematode communities in Illicium verum forest

Y. Lü,Y. Lü,W. F. Xue etW. F. Xue etP. P. YanP. P. Yan

Publié en ligne: 17 Dec 2022

Volume & Edition: Volume 59 (2022) - Edition 3 (September 2022)

Pages: 301 - 310

Reçu: 10 May 2022

Accepté: 06 Sep 2022

Détails du journal et du numéro

Helminthologia

Aperçu PDF

Article

Fig.1

Fig.2

Fig.3

Figures et tableaux

Fig.1

Fig.2

Fig.3

Nematode taxonomic diversity indices and channel ratio in different treatments (means ± SE).

Nematode genera identified in this study and their relative abundance (%) in the different treatments.

Selected properties of soil abiotic factors, microbial carbon and microbial nitrogen in different treatments (means ± SE).

Références

Articles récents

Planifiez votre conférence à distance avec Sciendo

Y. Lü,
Y. Lü,
W. F. Xue et
W. F. Xue et
P. P. Yan
P. P. Yan