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Article

The Impact of Different Agricultural Practices on Nematode Biodiversity on Tomato- and Lettuce-Growing Periods Across Two Consecutive Years

Research Centre for Plant Protection and Certification, Council for Agricultural Research and Economics, Via di Lanciola 12A, 51025 Firenze, Italy
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Author to whom correspondence should be addressed.
Diversity 2025, 17(8), 501; https://doi.org/10.3390/d17080501
Submission received: 30 June 2025 / Revised: 18 July 2025 / Accepted: 19 July 2025 / Published: 22 July 2025
(This article belongs to the Special Issue Distribution, Biodiversity, and Ecology of Nematodes)

Abstract

Protecting the soil ecosystem’s functioning is one of the main goals of recent regulations of chemicals. It is important to take soil biodiversity into account when designing cropping systems and measuring their impacts. Our main objective was to evaluate the effects of an organic amendment on soil nematode biodiversity compared to two years of fumigation. The plot-trial was conducted on tomato and lettuce plants under greenhouse, and free-living nematodes were used as bio-indicators of soil health. Treatments included a soil fumigant (applied once or twice over time), water control, and an organic substance. Soil samplings were carried out to determine the Meloidogyne incognita reproduction factor and the soil nematode community analysis using soil biological indicators. Data showed that soil fumigation clearly made the soil increasingly dependent on chemicals. Furthermore, fumigants suppressed pests and pathogens as well as their natural antagonists, causing a lack of biodiversity. While soils treated with organic matter respond slowly to stressors, they are progressively more suppressive thanks to biodiversity enrichment. Nematodes have proven to be useful indicators of the soil biota in response to biotic or abiotic disturbances. Their species richness and functional diversity make them valid bioindicators of soil management impact.

Graphical Abstract

1. Introduction

There is increasing interest in assessing the impact of management practices on soil quality and biodiversity. Soil tillage and application of chemicals are strictly linked to the agroecosystem function’s sustainability [1]. However, these practices can result in soil microbial diversity decline [2]. Biological indicators of environmental quality have been used to monitor and evaluate soil changes [3]. The diversity of soil nematodes and their high sensitivity and ability to reflect the effects of soil management suggest that they are useful bioindicators [4]. Currently, their analysis is mainly based on both species-level taxonomy and trophic-level guilds.
Soils have great biological, biochemical, and chemical complexity, in which nematodes play a key role [5]. Among them, plant-parasitic nematodes (PPNs) cause significant economic losses in agriculture, having a negative impact on plant productivity and quality traits, particularly on tomato (Solanum lycopersicum), the most investigated food crop occupying approximately 4.5 million hectares with an average yield of 243 million tons (FAO, 2020) [6]. This solanaceous crop is mainly threatened by the root-knot nematodes (RKNs) Meloidogyne incognita, M. arenaria, M. hapla, and M. javanica. RKNs cause losses estimated in billions of euros a year [7] and, in particular, M. incognita is responsible for yield losses of 18–65% under field conditions [8], which corresponds to about USD 100 million a year [9]. Generally, the management of PPNs has inevitable effects on the community of free-living nematodes and on their beneficial effects on the agricultural soil’s health. Current trends consider the conservation of indigenous soil nematode communities as a fundamental natural resource. In fact, the natural equilibrium in soil as well as co-evolution and co-speciation of soil taxa are basic processes involved in soil ecosystem services such as nematode regulation.
Damage caused by PPNs is mainly attributable to stunted plant growth and can lead to total harvest loss [10,11]. These losses are significantly aggravated in protected environments, in which sequential cropping systems may also favor pathogen infestations (fungi or bacteria) and consequent synergistic damage [12,13]. In Italy, pest and pathogen control has been carried out for more than 50 years almost exclusively using chemical products (CP), especially soil fumigants (i.e., 1.2 dichloropropane + 1.3 dichloropropene, etc.) [14]. In this context, optimizing the approaches used to manage plant pests and pathogens via environmentally friendly practices represents a current pressing challenge for sustainable agricultural systems.
A European Union report (2024) [15] has set the objective to achieve at least a 50% reduction in CP use by 2030. This downward trend is also necessary due to their unregulated abuse [16]: the efficacy of novel CPs in pest and pathogen management is lower in comparison to the past [17]. Considering the expected increase in world population of 35% by 2050, it will be necessary to promote production by using environmentally friendly resources [18,19], guaranteeing and ensuring food quality. This goal can be achieved through alternative or integrated methods in accordance with environmental and climate change. Among the different strategies proposed, those that have growing support among researchers, specialists, and agricultural operators are undoubtedly solarization [20,21,22], biofumigation [23,24,25,26], and use of plant extracts [27,28,29,30,31], biological agents, in particular fungi and bacteria [32,33,34,35], and organic amendments [36,37,38,39]. In particular, these latter strategies can improve soil ecosystem services and contribute to climate change adaptation, but their efficacy depends on several factors (i.e., soil type, soil management practices, duration of application, climate conditions, etc.) [40]. Often, opposite trends can be observed in their response [41]; for example, an increment of soil nematode population after soil organic amendment treatment has been observed for Pratylenchus penetrans on potato plants and Heterodera trifolii on barley crops [42]. On the other hand, organic matter can change the nematode community composition, reducing PPNs and increasing free-living nematodes [43,44]. Saprophytic nematodes, bacterial and fungal feeders, and their predators play multiple roles in the soil food web and they are also involved in the cycling of carbon, nitrogen, and phosphorous as supporting services [45]. In addition, organic amendments are useful to stimulate a wide range of antagonistic microorganisms [46,47] as well as to promote soil biodiversity and consequently the functioning of ecosystems [48,49,50].
The purpose of this study was to evaluate the impact of different agricultural treatments on soil nematode biodiversity across three consecutive cropping cycles for two years. An organic amendment application was compared with a water-treated control and 1.3D fumigation to provide management advice in the context of the EU Biodiversity Strategy 2030. The experiment was conducted in a cold greenhouse planted with tomato plants as the primary crop, and free-living nematodes were used as bioindicators of soil health.

2. Materials and Methods

2.1. Field Site and Treatments Description

Trials were conducted under a polyethylene greenhouse located in “Terra di lavoro”, Caserta Province, Italy (latitude 41°05′13.0″ N; longitude 13°55′11.7″ E). Tomato, Lycopersicon esculentum cv. Hummer (primary crop) and two cycles of lettuce, Lactuca sativa var. Trocadero, were grown for two consecutive years. The climate of the region is typically Mediterranean because it is located in climatic zones belonging to the Cfa, Cfsa, and Csa categories based on the current Köppen–Geiger classification [51]. Soil of volcanic origin and a pH of 7.6 was severely and uniformly infested by the RKN M. incognita. The greenhouse surface area was 1200 m2 (m 20 × 60), divided into 3 plots, the first plot of 600 m2 (Plot A, m 20 × 30) and the other two of 300 m2 (Plots B and C, m 20 × 15). During the second year, plot A was further divided into two subplots (Plot A1 and A2, 300 m2 each). Fumigation has been used in this area for about 30 years.
During the first season (2022–2023), 3 individual treatment units (plots) received the following soil treatments (carried out on 17 June): (a) Plot A—the fumigant 1.3 dichloropropene (Condorsis EC 2022 B, Dow Europe GMBH) (1.3D) was applied at a dose of 180 L/ha−1 into the soil; (b) Plot B—after soil preparation, pelleted natural manure (Jolly Pellet) (PE) was applied at a dose of 90 q/ha into the soil; (c) Plot C—water-untreated control plot (CTR). Certified tomato seedlings, grown in polystyrene alveolate planting trays, were transplanted at the stage of four true leaves. Plots consisted of twin rows spaced 40 cm apart and an inter-row of 1.40 cm. Tomato (35,000 plants/ha−1) was cropped from 20 July to 11 November. Then, lettuce seedlings were transplanted on 24 November and cropped until 15 February (first cropping cycle). Lettuce (80,000 plants/ha−1) was planted, spaced 25 cm along the row and with 40 cm between the rows. The second cropping cycle was carried out from 3 March to 8 May. In both crops, a few dead seedlings were replaced during the first three days after transplanting.
During the second season (2023–2024), a split-plot experiment was carried out, with 4 individual treatment units. Plot A was divided in A1 and A2 sub-plots. Soil treatments were as follows: (a) Plot A1 was re-fumigated as described above (1.3D T2); (b) Plot A2 was not fumigated (1.3D T1); (c) Plot B was amended as above (PE); and (d) Plot C was an untreated control plot (water) (CTR). The treatment with fumigant was repeated after one year and not two as indicated in the legislative decree, because this trial was developed for experimental purposes and the production was not marketable. In the first season, tomato plants were cropped from 22 July to 8 November, whereas the first cropping cycle of lettuce was from 21 November to 10 February and the second one from 3 March to 3 May.
During both trial seasons, plants received drip irrigation and were fertilized or treated (excluding products with a secondary nematicidal activity) according to the required management procedures. The integrity of each plot was maintained over both seasons.

2.2. Soil Sampling Design

Soil samples were collected for two years of cultivation according to the following schedule: in June (before the tomato crop transplant), in November (after the tomato harvest and before the lettuce transplant), in February (after the harvest of the first lettuce crop and before the second lettuce transplant), and in May (at the end of the second lettuce crop). Soil samples (36 sub-samples/plot) were randomly collected from each plot to a soil depth of 0–20 cm using a small auger. During the first season, a double number of subsamples were collected from Plot A. During both crop seasons, soil samples were collected four days BT and at the end of each tomato- and lettuce-growing period. The composite soil sample was obtained after carefully mixing 36 subsamples/plot and dividing them into 10 samples (10 mL soil each). The nematode reproduction factor was calculated according to the initial (IP) and final (FP) nematode population densities as FP/IP.

2.3. Soil Nematode Community Analysis

Nematodes were isolated from 100 mL of each soil sample using the cotton–wood filter extraction method. Nematodes were extracted at room temperature (~20 °C) for 48 h. Each nematode suspension was sieved through a 25 μm mesh and nematodes were counted under a stereomicroscope (50× magnification). Nematodes were mounted on temporary slides and identified at higher magnification to genus or family level using the keys of Mai and Lyon [52], Bongers [53], Marinari-Palmisano, or Vinciguerra [54]. Taxonomic families were assigned to a trophic grouping based on Yeates et al. [55]; the Tylenchidae family was assigned to the fungivorus trophic group according to Okada et al. [56]. Nematode communities were characterized using (i) absolute abundance of individuals; (ii) richness determined by counting the number of taxa (family level); (iii) biodiversity indices; (iv) the maturity indices (MI) and plant parasitism (PPI) according to Bongers [57]; and the food web indicators (BI, basal index; EI, enrichment index; SI, structure index; CI, channel index) according to Ferris et al. [58].

2.4. Statistical Analysis

A one-way ANOVA was performed to assess the soil nematode assemblage (J2 M. incognita population in the soil and the trophic groups of bacteriophagic, fungivores, and omnivores). A three-way ANOVA was performed to assess the influence of management, year, and season on indicators of nematode biological indicators. When the F-test was significant at p < 0.05, treatment means were compared using the Student–Newman–Keuls test using the CoStat statistical software package (https://www.cohortsoftware.com/costat6451.zip, accessed on 15 January 2025). Additionally, nematode communities were compared using analysis of similarities (ANOSIM), multidimensional scaling (MDS), and SIMPER analysis based on the Bray–Curtis dissimilarity index, and nearest neighbor analysis was provided by the Past analysis package [59] (https://palaeo-electronica.org/2001_1/past/pastprog/Past.exe, accessed on 15 January 2025). Nematode abundance data were transformed using the square root. Bonferroni correction of p-values was applied. Environmental variables (pH, TOC, available P) were added. To evaluate the relationship between environmental variables and soil nematode parameters, a preliminary detrended correspondence analysis (DCA) was applied (Figure S1). Once it was verified that the gradient length on the first axis was >4 standard deviation units, the unimodal method was therefore justified. Canonical correspondence analysis (CCA) was performed to link nematode communities (abundance of nematode taxa and their indicators) and environmental variables (management, year, and season). Only significant environmental axes, represented by vectors, were considered. Statistical significance of the relationship between communities and environmental variables was assessed by permutation tests of both the first ordination axis and the combination of the first and second axes.

3. Results

3.1. Soil Nematode Community Structure and Dynamic

Regarding the plant-parasitic nematode Meloidoyne incognita, during the first season (2022–2023), the results of treatments of PE and 1.3D were statistically significantly different in comparison to the control over time, generally (Figure 1). However, no significant differences were observed between the control (256 ± 8.96 b) and 1.3D (273 ± 6.73 ab) treatments in June, and among all treatments in February because of low temperatures, which are associated with nematode population reduction into the soil. In contrast, differences (SNK’s test: p < 0.05) were detected between PE (294 ± 10.48 b) and 1.3D (249 ± 9.79 c) treatments in May. The highest number in the nematode population was collected in November in all treatments, corresponding to the tomato harvest period and the consecutive transplant of the lettuce.
During the second season (2023–2024), there were several significant differences among all treatments and also between 1.3D 1T and 1.3D 2T (except in June). However, generally the best performance in M. incognita management was found in MA treatment. At the end of the trials (in May), no significant differences were observed between PE (273 ± 7.27 c) and 1.3D 2T (310 ± 31.13 c) treatments. However, these treatments were different (p < 0.05) in comparison to the control (824 ± 5.74 b) and 1.3D 1T (913 ± 34.91 a).
Only seven genera of free-living nematodes were identified in soil samples collected from four different crop managements. As expected, the MDS analysis on taxa nematode abundance showed no separation among different managements before treatments (June 2022) (Figure 2). During the different crop production periods a clear separation was highlighted between 1.3D fumigant (both one and two applications) and the other two managements (PE and CTR). One-way ANOSIM analysis of nematode abundance confirmed this trend: the R value was low only in the pre-treatment (0.34), while it was high and varied from 0.85 to 1 after treatments. SIMPER analysis based on the Bray–Curtis dissimilarity index for family abundance ranged from 7.8% in June 2022 (pre-treatment) to 52.7% in June 2023 (Supplementary Materials, Tables S1–S8). Overall, the differences were mainly due to the high proportion of Rhabditidae and Cephalobidae shifts, followed by Tylenchidae. The breakdown of similarity by family showed that a range of six and seven families accounted for 95% of the similarity in all periods considered.
The proportion of nematodes in the feeding groups was similar for each different treatment: bacterial feeder was the most representative group, while the abundance of fungal feeders and omnivores was low under all regimes (Figure 3). The composition of the trophic group varied more because of seasonal fluctuation than management. Bacterial feeder abundance was strongly influenced by season (low in winter and high in fall). In contrast, fungal feeders and omnivores showed no seasonal trend, and their populations were constant across the two-year trials. However, significant differences were reported among different managements: in fact, bacterial and fungal feeders increased in PE and to a lesser extent in CTR. Omnivores were higher in PE and CTR than fumigated soils.

3.2. Soil Biological Indicators

The mean values of biodiversity indices showed a very low range among the treatments (Table S9). However, the biodiversity in PE was higher than in fumigant treatments. Specifically, Shannon, Brillouin, Menhinick, Margalef, and Fisher α indices were significantly higher in PE than 1.3D T1 and 1.3D T2, while dominance, evenness, equitability, and Berger-Parker showed opposite trends. Significant differences were also found according to year and season. The highest biodiversity was detected during the first crop season (2022–2023), especially in spring.
In general, significant differences were found between management methods for food web indicators (Table 1). MI values ranged from 1.42 to 1.61, showing a very narrow range. In contrast, BI values ranged from 217.6 in PE to 148 in 1.3D T2. EI values were higher than 50% under all management methods, indicating a nitrogen-enriched environment. In contrast, SI values were very low (≥ 15). However, they were higher under more sustainable management methods such as PE and CTR compared to fumigant treatments. Regarding fumigant treatments, 1.3D T1 revealed SI values higher than 1.3D T2. Finally, low CI values suggested the dominance of bacterial decomposers within the free-living soil nematode community in comparison to fungivorus. No differences in ecological indicators were found between the two crop years; in contrast, seasonal values were significantly different. Spring produced the highest MI and CI values and the lowest EI values. BI and SI values increased in fall and winter, respectively.

3.3. Relationship Between Environmental Variables and Community Structure and Nematode Community

CCA analysis conducted comparing the abundance of nematode taxa and environmental variables highlighted that management and season were the main parameters influencing the abundance of nematode taxa (Figure 4A). Axis A was dominated by season (February −0.88; November 0.47), while Axis 2 was dominated by management (1.3D T1 0.42; GM −0.39). In general, the plant-parasitic nematode belonging to the Meloidogynidae family was correlated to the November period and showed an opposite trend compared to free-living nematodes. Dominant families such as Rhabditidae, Cephalobidae, and Tylenchidae were moderately influenced by these parameters. The families of Steinernematidae (entomopathogenic nematodes), Aphelenchidae (fungal nematodes), Plectidae (bacterial nematodes), and Dorylaimidae (omnivores) were correlated with PE and the February period.
The biplot of CCA between soil biological indicators and environmental variables showed that Axis 1 was driven by season (February 0.42; November −0.40), while Axis 2 was dominated by management (1.3D T2 −0.65; PE 0.36) (Figure 4B). The biodiversity indices were scarcely influenced by the environmental gradient. Among food web indicators, only SI varied according to this environmental gradient and was related to the February period, PE, and a lesser extent, CTR.

4. Discussion

4.1. Meloidogyne Incognita Dynamic

Results from M. incognita infestation are a further confirmation that the application of pelleted natural manure to nematode-infested soil can be an effective tool for the management of RKN in horticultural crops, providing nematicidal performance even comparable to that of chemicals (1.3D). The use of pelleted natural manure could be particularly suited to organic crop systems and could also be included in integrated nematode management strategies. Data from the second cropping season trial indicated that these products should be preferred to chemicals, ensuring effective control over time. Soil fumigation with 1.3D was demonstrated to be effective in controlling root-knot nematode infestation, as documented by many other previous studies either on tomato, lettuce, and other horticultural crops [34]. However, although soil treated with 1.3D for two consecutive years maintained a constant nematode population, the nematode numbers increased slightly. This phenomenon is observable in soils increasingly dependent on chemicals. Therefore, it is necessary to increase the doses of the fumigant used to be equally effective. Overall, the use of chemical products reduces soil biodiversity [60,61,62,63]. The decline in soil biodiversity caused by fumigants can be useful against harmful species but also very disadvantageous for the antagonistic species. In fact, their effects are not strictly limited to a target group but apply to more than one group of organisms. In this study, the positive performance of pelleted natural manure was observed both on M. incognita infestation and also on the enrichment in nematode population variability.

4.2. Effects of Different Phytosanitary Management Methods on Soil Nematode Community Structure and Dynamics

In general, long-term intensive vegetable cultivation under greenhouse has led to a decrease in taxa richness. Several authors report that repeated soil applications of pesticides, especially fumigants, may strongly reduce nematode species richness [24,64,65,66,67]. In fact, free-living nematode assemblage was characterized by the dominance of opportunistic bacterial feeders (Rhabditidae and Cephalobidae families) and by the absence of predators. Moreover, a strong reduction in fungivorus and omnivores was found.
ANOSIM analysis highlighted the impact of different treatments on free-living nematodes through the increase in R values between pre- and post-treatments. Moreover, as reported by Grabau et al. [66], MDS analysis showed that the fumigant 1.3D strongly modified the nematode community composition in comparison to control or manure treatments. The trophic group assemblage revealed differences in the composition, according to the treatments and sampling times. The bacterial-feeders population was more adversely affected by fumigation than other trophic groups, especially when 1.3D was applied both years. According to Hodson et al. [68], the fumigant application also reduced fungivore and omnivore populations. As reported by Sanchez-Moreno et al. [65], fungivores were particularly susceptible to one application of 1.3D treatments, but their populations rapidly increased within a year. This evidence demonstrated that the fumigant effect is transitory, and its prolonged application reduced soil biodiversity [64,66,67]. The impact of fumigants on omnivores was more significant. Their abundance was constantly low both in 1.3D T2 and 1.3D T1. In contrast, manure favored all trophic groups as expected. In agreement with Mocali et al. [24], fungal feeders (mainly Aphelenchidae) and omnivores (all belonging to the family Dorylaimidae) increased under organic amended management. Bacterial feeders also increased, especially after the second year of application. Indeed, after two years, the differences compared to the control were still very small. As reported by several authors, only a long period of organic amendment application allows soil nematode structure improvement [69,70].
In general, as reported by Mocali et al. [24], low values in nematode indicators confirmed soil degradation and lack of biodiversity. This was an expected result considering the long period of fumigant application, which caused a negative impact on the soil nematode community. Biodiversity indices showed negligible differences among different management methods; however, this set of indices signaled the potential of organic amendments in improving soil biodiversity. These data should be interpreted within the limits of a short-term context. Several authors have demonstrated that only repeated organic treatments are useful to increase these indices [69,70,71,72].
Ecological indicators, especially MI, EI, BI, and SI, allow further consideration. The low values of MI indicated that the soil was degraded by anthropic activities, whereas the high values of EI highlighted an exponential growth of colonizing species. BI increased after the application of the pellets into the soil, suggesting that organic amendment benefitted the nematode community structure development. Overall, the low SI values indicated a weak ability to regulate soil nematode populations, due to the low abundance of k-strategy individuals, mainly represented by omnivores and predators. The distribution of organic amendments as well as the absence of any treatments favored the increase of this index, indicating an improvement in soil quality and structure stability of the soil nematode community. For this reason, the SI index is the most used to evaluate the impact of chemical fumigation on soil health [24,64,66,68]. Using faunal ordination in the faunal profile reported by Ferris et al. [58], it was possible to confirm that the soil of each treatment was classified in Quadrat A characterized by high disturbance, N-enrichment, bacterial decomposition channels, and disturbed food web conditions. These results describe an “enriched profile” as reported by Ferris and Bongers [73]: the system supported only low abundance of predators and biotic regulation may have been insufficient.
Finally, the temporal trend of these indices suggested that the community composition shifted from an enriched and simple nematode community (high EI and low SI) immediately after treatments to an enriched and more complex nematode community (high EI and SI) at the end of the trial. In accordance with Sanchez-Moreno et al. [65]), this finding confirmed the resilience of the soil food web.

4.3. Environmental Parameters Influencing Soil Nematode Structure

As previously reported, M. incognita causes a strong alteration in the free-living nematode community due to its high exponential growth [24]. This is clearly evident in the CCA biplot. In fact, M. incognita showed an opposite trend in comparison to free-living nematode families. Moreover, the highest M. incognita population was related to the autumn season, when its highest population was found. In contrast, free-living nematodes were related to the winter season, when M. incognita populations were very low. According to other studies, the application of organic matter favored the families of omnivores and fungal feeders as well as entomopathogenic nematodes, useful in the biological control of insect pests [24,65,66,68,70].
Weak correlations were found between nematode community indices and environmental parameters. The most relevant nematode indicator was SI. A positive correlation between the pellet treatment and SI was found. This finding confirmed that the application of soil organic matter to the soil enhances the nematode community structure [24,65,70].

5. Conclusions

By evaluating different pest control management methods—annual and biennial fumigation, and annual organic-amended supplementation—we were able to assess their effects on the soil nematode community. As expected, the pelleted natural manure improved soil nematode structure, especially for fungivores and predators. Further investigation is needed to evaluate the effectiveness of the amendment in controlling M. incognita infestation, although a reduction in the populations of juvenile stages in the soil was reported. In this context, poor in predators, the structure index (SI) appeared to have the greatest potential as an indicator of unhealthy/healthy systems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d17080501/s1, Table S1: SIMPER analysis (1.3D = Fumigant; PE = Pellet; CTR = Control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in June 2022. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S2: SIMPER analysis (1.3D = fumigant; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in November 2022. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S3: SIMPER analysis (1.3D = fumigant; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in February 2023. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S4: SIMPER analysis (1.3D = fumigant; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in May 2023. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S5: SIMPER analysis (1.3D T1 = fumigant one treatment; 1.3D T2 = fumigant two treatments; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in June 2023. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S6: SIMPER analysis (1.3D T1 = fumigant one treatment; 1.3D T2 = fumigant two treatments; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in November 2023. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S7: SIMPER analysis (1.3D T1 = fumigant one treatment; 1.3D T2 = fumigant two treatments; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in February 2024. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S8: SIMPER analysis (1.3D T1 = fumigant one treatment; 1.3D T2 = fumigant two treatments; PE = pellet; CTR = control) on the abundance of nematode taxa (number of nematodes/mL of soil) in Caserta site in May 2024. Av. Diss., average dissimilarity; Contr., cumulative contribution; Table S9: Soil nematode biodiversity indices, 1.3D T1, fumigation applied once; 1.3D fumigation applied twice; PE, pellet; CTR, control during crop year 2022–23 and 2022–24. Mean values with standard errors are reported (±). Letters indicate significant differences between groups (ANOVA p < 0.05). Summary of the significance of the effects of managements (M), year (Y), and season (S) on soil biological indicators and their interactions are reported. Significant p-values are in bold; Figure S1: Detrended correspondence analysis (DCA) for nematode taxa abundance (A) and biological indicators (B).

Author Contributions

Conceptualization, G.d. and S.L.; methodology, G.d.; formal analysis, S.L.; investigation, G.d.; data curation, S.L.; writing—original draft preparation, G.d.; supervision, S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

No ethical approval was required for the sample types collected in this study.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Acknowledgments

We wish to thank Valentina Guardi for her help in the graphical abstract.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effect of soil treatments on tomato- and lettuce-growing periods across two consecutive years. During the first cropping season 2022–2023, the plot experimental design included the following treatments: (a) Plot A, 1.3D—1.3 dichloropropene applied at a dose of 180 L/ha−1 into the soil; (b) Plot B, PE—pelleted natural manure (Jolly Pellet) applied at a dose of 90 q/ha into the soil; and (c) Plot C, water-untreated control plot. During the second cropping season 2023–2024, a split-plot experiment was included and the fumigated plot (Plot A, 1.3D) was divided into two sub-plots: Plot A1 (1.3D 1T) and Plot A2 (1.3D 2T). Treatments included: (a) Plot A1—1.3 dichloropropene application was not repeated; b) Plot A2—1.3 dichloropropene application was repeated; (b) Plot B—PE—pelleted natural manure (Jolly Pellet) applied as above; and (c) Plot C—water-untreated control plot. Soil samplings for the evaluation of initial (IP) and final (FP) nematode population densities were carried out in June (Jun), November (Nov), February (Feb), and May at the end of each cropping season. Means were considered significantly different (p < 0.05) according to Student–Newman–Keuls test. Levels of significance are indicated by asterisks for * p < 0.05, *** p < 0.001.
Figure 1. Effect of soil treatments on tomato- and lettuce-growing periods across two consecutive years. During the first cropping season 2022–2023, the plot experimental design included the following treatments: (a) Plot A, 1.3D—1.3 dichloropropene applied at a dose of 180 L/ha−1 into the soil; (b) Plot B, PE—pelleted natural manure (Jolly Pellet) applied at a dose of 90 q/ha into the soil; and (c) Plot C, water-untreated control plot. During the second cropping season 2023–2024, a split-plot experiment was included and the fumigated plot (Plot A, 1.3D) was divided into two sub-plots: Plot A1 (1.3D 1T) and Plot A2 (1.3D 2T). Treatments included: (a) Plot A1—1.3 dichloropropene application was not repeated; b) Plot A2—1.3 dichloropropene application was repeated; (b) Plot B—PE—pelleted natural manure (Jolly Pellet) applied as above; and (c) Plot C—water-untreated control plot. Soil samplings for the evaluation of initial (IP) and final (FP) nematode population densities were carried out in June (Jun), November (Nov), February (Feb), and May at the end of each cropping season. Means were considered significantly different (p < 0.05) according to Student–Newman–Keuls test. Levels of significance are indicated by asterisks for * p < 0.05, *** p < 0.001.
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Figure 2. MDS analysis based on Bray–Curtis dissimilarity index of nematode community abun-dance from soils sampled; in crop years 2022–2023 and 2023–2024 on Plot A1 (1.3D T1), fumigation applied once; Plot A2 (1.3D T2), fumigation applied twice; Plot B (PE), pellet; Plot C (CTR), control. Symbols represent: Plot A1, fuchsia square; Plot A2, red cross; Plot B, brown rectangle; Plot C, olive green rectangle. Stress values (S) and ANOSIM analysis are reported.
Figure 2. MDS analysis based on Bray–Curtis dissimilarity index of nematode community abun-dance from soils sampled; in crop years 2022–2023 and 2023–2024 on Plot A1 (1.3D T1), fumigation applied once; Plot A2 (1.3D T2), fumigation applied twice; Plot B (PE), pellet; Plot C (CTR), control. Symbols represent: Plot A1, fuchsia square; Plot A2, red cross; Plot B, brown rectangle; Plot C, olive green rectangle. Stress values (S) and ANOSIM analysis are reported.
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Figure 3. Effect of management methods on the abundance of nematode trophic groups (SE) extracted by 100 mL soil. Plot A1 (1.3D T1), fumigation applied once; Plot A2 (1.3D T2), fumigation applied twice; Plot B (PE), pellet; Plot C (CTR), control. Levels of significance are indicated by asterisks for * p < 0.05, ** p < 0.01, *** p < 0.001. (Student–Newman–Keuls test). Data are from the eight sampling dates.
Figure 3. Effect of management methods on the abundance of nematode trophic groups (SE) extracted by 100 mL soil. Plot A1 (1.3D T1), fumigation applied once; Plot A2 (1.3D T2), fumigation applied twice; Plot B (PE), pellet; Plot C (CTR), control. Levels of significance are indicated by asterisks for * p < 0.05, ** p < 0.01, *** p < 0.001. (Student–Newman–Keuls test). Data are from the eight sampling dates.
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Figure 4. Scatter plots of CCA ordination showing relationships between environmental variables and nematode taxa abundance (A) and biological indicators (B). In A, the percentage of variance was 83.43% for axis 1 (p < 0.001) and 10.05% for axis 2 (p < 0.001); in B, the percentage of variance was 72.32% for axis 1 (p < 0.001) and 25.01% for axis 2 (p < 0.001).
Figure 4. Scatter plots of CCA ordination showing relationships between environmental variables and nematode taxa abundance (A) and biological indicators (B). In A, the percentage of variance was 83.43% for axis 1 (p < 0.001) and 10.05% for axis 2 (p < 0.001); in B, the percentage of variance was 72.32% for axis 1 (p < 0.001) and 25.01% for axis 2 (p < 0.001).
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Table 1. Soil nematode ecological indicators, 1.3D T1, fumigation applied once; 1.3D fumigation applied twice; PE, pellet; CTR, control during crop years 2022–2023 and 2022–2024. Mean values with standard errors are reported (±). Letters indicate significant differences between groups (ANOVA p < 0.05). Summary of the significance of the effects of management (M), year (Y), and season (S) on soil biological indicators and their interactions are reported. Significant p-values are in bold.
Table 1. Soil nematode ecological indicators, 1.3D T1, fumigation applied once; 1.3D fumigation applied twice; PE, pellet; CTR, control during crop years 2022–2023 and 2022–2024. Mean values with standard errors are reported (±). Letters indicate significant differences between groups (ANOVA p < 0.05). Summary of the significance of the effects of management (M), year (Y), and season (S) on soil biological indicators and their interactions are reported. Significant p-values are in bold.
MIBIEISICI
Mgmt Method
1.3D T21.42 ± 0.01 b148.00 ± 9.09 c84.99 ± 0.69 a4.64 ± 1.08 b1.37 ± 0.12 c
1.3D T11.61 ± 0.02 a210.40 ± 0.02 a73.73 ± 1.13 b5.62 ± 0.44 b3.14 ± 0.34 a
PE1.44 ± 0.01 b217.56 ± 10.77 a85.40 ± 0.55 a13.22 ± 1.25 a2.83 ± 0.19 ab
CTR1.43 ± 0.01 b194.06 ± 8.61 b85.70 ± 0.61 a13.48 ± 1.25 a2.40 ± 0.28 b
Years
2022–231.42 ± 0.01 b185.23 ± 9.33 b85.04 ± 0.65 a8.83 ± 0.89 b1.96 ± 0.14 b
2023–241.48 ± 0.01 a193.49 ± 7.33 a82.68 ± 0.78 b10.45 ± 1.15 a2.61 ± 0.21 a
Season
June1.51 ± 0.01 a212.91 ± 9.16 b79.98 ± 0.99 b5.70 ± 0.70 b2.76 ± 0.32 a
November1.42 ± 0.01 b242.47 ± 10.53 a84.69 ± 0.64 a6.43 ± 1.00 b1.71 ± 0.19 b
February1.45 ± 0.02 b141.07 ± 6.03 d84.88 ± 1.10 a12.63 ± 1.59 a2.21 ± 0.17 b
May1.44 ± 0.02 b163.34 ± 7.51 c85.22 ± 0.85 a14.26 ± 0.14 a2.65 ± 0.25 a
p value
Main effect
M0.000010.000010.000010.000010.00001
Y0.000010.500.180.00010.025
S0.000010.000010.000010.000010.0005
Interaction
M + Y0.000010.000010.000010.000010.06
M + S0.0020.000010.000010.00140.002
T + S0.000010.000010.000010.00010.22
M + Y + S0.000010.000010.00050.000010.26
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d’Errico, G.; Landi, S. The Impact of Different Agricultural Practices on Nematode Biodiversity on Tomato- and Lettuce-Growing Periods Across Two Consecutive Years. Diversity 2025, 17, 501. https://doi.org/10.3390/d17080501

AMA Style

d’Errico G, Landi S. The Impact of Different Agricultural Practices on Nematode Biodiversity on Tomato- and Lettuce-Growing Periods Across Two Consecutive Years. Diversity. 2025; 17(8):501. https://doi.org/10.3390/d17080501

Chicago/Turabian Style

d’Errico, Giada, and Silvia Landi. 2025. "The Impact of Different Agricultural Practices on Nematode Biodiversity on Tomato- and Lettuce-Growing Periods Across Two Consecutive Years" Diversity 17, no. 8: 501. https://doi.org/10.3390/d17080501

APA Style

d’Errico, G., & Landi, S. (2025). The Impact of Different Agricultural Practices on Nematode Biodiversity on Tomato- and Lettuce-Growing Periods Across Two Consecutive Years. Diversity, 17(8), 501. https://doi.org/10.3390/d17080501

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