The objective of our study was to assess the impact of farming systems on soil quality in vegetable fields, focusing on the soil nematode community as an indicator of the soil food-web. We compared nematode communities in vegetable fields with extensively managed grasslands that do not receive any fertilizer and plant protection products.Due to the agricultural intensification under conventional farming, organic farming and extensive grasslands represent a gradient of management intensity, representing high-, moderate- and low-intensive management, respectively. We specifically addressed the following questions: to what extent does management intensity affect the abundance, diversity, community composition and functional guilds of soil nematodes? What accounts for the difference in soil nematode assemblages among conventional vegetable farming, organic vegetable farming and extensive grassland? Are there any nematode taxa that can be used as indicators of a specific management system? A farmer network consisting of 60 fields was established with20 conventional vegetable fields and 20 organic vegetable fields in the Canton of Zurich.
As a standard reference, 20 extensive grassland fields in close location were also selected. The conventional vegetable fields received pesticides and synthetic fertilizers and were managed according to guidelines of the federal office of agriculture. The organic vegetable fields were managed according to the guidelines of the Swiss organic farmers association ,ebb and flow table including no application of synthetic pesticides or synthetic fertilizers. Grasslands were managed according to the Swiss regulations for extensively managed meadows,which do not receive any fertilizer input and are mown at least once per year. In Switzerland, extensively managed meadows are considered as biodiversity promotion areas and farmers are financially compensated by the federal government with biodiversity contributions for the adapted use of their land. Agri-environmental schemes such as the Swiss BPA were introduced in many European countries in the 1990 s to alleviate the loss of biodiversity due to agricultural intensification. Swiss farmers must manage at least 7% of their agricultural land as BPA. The three farming systems are characterized in the Table S1 . The soils of the fields are classified as Cambisol, which is the predominant soil type in this region . The soil samples were collected in the period from 13 to 20 December 2016. At each field, we collected 10 soil cores with a stainless steel auger. These cores were immediately homogenized and placed into a sealing plastic bag. Sub-samples for soil analyses, pesticide analysis and molecular analyses were dried at room temperature, or stored at 4 ◦C or − 20 ◦C . In addition, a soil composite sample of approximately 20 kg of soil and consisting of ten individual soil samples was collected at each site with a shovel for nematode assessment and for the purpose of a greenhouse experiment of another study. In the laboratory, the composite sample for each site was passed through a 5 mm sieve, and visible living plant materials, visible macro-fauna , and stones were removed.
The sieved soil samples were stored in a plastic bag at 4 ◦C until further processing. Effects of farming system on variables including total nematode abundance, abundance per trophic group, nematode diversity indices, maturity indices, food web indices and metabolic footprints of soil nematodes were analyzed using one-way ANOVA with farming system as the fixed factor in R . Before analysis, the normality and the homogeneity of the residuals for data were examined by Shapiro-Wilk test or by Kolmogorov-Smirnov test in the ‘stats’ package. When the assumption of ANOVA of a given variable was violated, the effect of farming system on this variable was examined with non-parametric Kruskal-Wallis test. When the effect of farming system on a given variable was significant, difference between treatments was further compared with a post-hoc test by the Tukey’s Honestly Significant Difference test or the Wilcoxon Signed Rank test at α = 0.05 level. A Pearson correlation analysis was used to evaluate relationships between abiotic soil characteristics and nematode abundance as well as between microbial properties and nematode abundance. Community composition of soil nematodes across the three farming systems were compared with Bray–Curtis similarity using the canonical analysis of principal coordinates and per-mutational multivariate analysis of variance with 999 permutations using the ‘vegan’ packages in R. Finally, we identified potential habitat specialists or indicator taxa for conventional vegetable fields, organic vegetable fields and grasslands, using the indicator species analysis. The indicator species approach identifies a given taxa that tends to be present mostly in a single habitat type and most of the samples from that habitat based on the relative frequency and average abundance, and thus implies the nematode taxa preference for a given environmental condition. Specifically, the clusters were categorized by farming system in the analysis. Indicator species for each cluster were identified using the ‘multipatt’ function in the ‘indicspecies’ package in R . For each of the three farming systems, taxa with a p-value ≤0.05 and IndVal >0.30 were selected as potential indicator species. IndVal analysis was performed on soil nematode dataset.
Although the effect of organic management on soil nematode communities has been explored in previous studies, most of these studies were performed with field-trials.The strength of field-trials is that farming treatments are assessed under a standardized management at one location and with a specific soil type. However, management effects on nematode communities may differ in actual farmlands and thus the results obtained at a single site cannot be generalized. Environmental problems that may be associated with the increase in vegetable production with its intensive management practices is a concern, particularly negative impacts on biodiversity, leaching of nutrients into drinking water, or emissions of greenhouse gases. However, we still have a limited understanding of how soil biota such as nematode respond to vegetable production practices at the farm scale where soil type and nutrient availability are of higher heterogeneity. The present study reports the impact of vegetable management practices on soil nematode communities across many fields at a regional scale analyzing a total of 60 fields. Our results suggest that organic management alters overall community characteristics of soil nematodes. The abundances of herbivores, bacterivores and omnivores were greatly enhanced by organic management in comparison with conventional management . Organic management also enhanced composite footprint and herbivore footprint,indicating that organic farming supports higher herbivore abundance and herbivorous nematode individuals of higher biomass. Moreover, organic farming in vegetable fields resulted in notable shifts in soil nematode community despite of no obvious change in soil food-web index represented by BI, CI, EI and SI, decomposition and nutrient mineralization pathway represented by the Fu/ and primary production represented by Herb/ between conventional vegetable fields and organic vegetable fields . This indicates that there are no significant change in soil ecological processes and functions provided by the nematode communities in organic and conventionally managed fields in Switzerland. However, variation among fields was large and further studies need to verify our observation. The observed higher abundance and biomass of total nematodes in soils under organic farming compared to conventional farming in our study is consistent with an earlier field experiment where organic management supported higher nematode abundance and biomass compared to conventional management in vegetable fields .
We also found that the total nematode abundance in vegetable fields was lower than that in grasslands.This result supports a previous report showing that the land transformation from grassland to agricultural use reduces soil biota . Soil biota in extensive grasslands is generally subjected to fewer disturbances, such as tillage and/or pesticides application compared to arable fields, particularly vegetable fields. Moreover, higher plant diversity and litter coverage in grasslands usually retain higher soil moisture, and thus favour soil nematode colonization and reproduction. Overall, our results suggest a negative impact of land-use intensification on soil nematode abundance. Compared to the conventional farming systems, organic farming systems contained increased population densities of microbivorous and omnivorous nematodes. However, the threat of plant-parasitic nematodes to vegetable production, especially in organic vegetable production should be given attention, and integrated management strategies should be further developed and implemented . In agreement with previous studies , we found a higher abundance of herbivores, bacterivores and omnivores in organic vegetable fields, compared to conventional vegetable fields . Previous studies proposed that the intensive application of mineral fertilizer in conventional farming systems reduced bacteria-feeding nematodes due to direct toxicity of nitrogen solutions.Besides, flood table intensive agriculture may alter the biotic interactions and patterns of resource availability in ecosystems . Such disturbance would further affect nematode abundance by changing the growth and reproductive capacity of nematodes directly and indirectly. As hypothesized, we found that the correlations among edaphic properties, microbial attributes and nematode abundance depended on the trophic group of nematode examined. Interestingly, nematode abundance was found to be positively correlated with NH4+-N in the present study . Note that further work is needed to confirm our observations because we only sampled once and the sampling was conducting at the end of the growing season. Moreover, we sampled to a soil layer in depth of 10 cm while other studies sampled to a depth of 30 cm. This may also affect the nematodes detected. The EI indicates the prevalence of opportunistic species, whereas the metabolic footprint measures the carbon utilization of component taxa . Previous studies report that crop residue retention increases EI and SI . We hypothesized that greater levels for these variables in soils would be observed in organic vegetable fields due to increased residue inputs in organic management compared to conventional management.
Against expectation, we found the EI and SI in soils under organic management were comparable to those under conventional management. However, the composite metabolic footprint and herbivore footprint in soils under organic management was greatly enhanced in comparison to conventional management, implying vegetable fields under organic management supported herbivores with larger body size and higher biomass. The observed comparable level in Shannon-Weaver index between organic management and conventional management in the present study is in disagreement with earlier studies demonstrating that the application of organic manure resulted in a decline in Shannon-Weaver index possibly due to the predominance of r-selected species.One possible reason is that there are greater differences in mulch treatment which has been found to reduce the total number of nematode genera in organic vegetable fields across studies. Another likely explanation is that the effect of organic farming on the richness of nematodes might be time-dependent. A previous study found that organic vegetable farms were more diverse in terms of genera of herbivores than conventional farms at the vegetative and/or reproductive stage . However, in the present study, farmers could not allow us to sample when their fields had fully grown vegetables, and thus herbivores can be difficult to detect due to unfavorable climatic factors and limited food at the harvest of vegetables. Previous study suggested that shifts in community composition of soil organism are usually accompanied by changes in the functioning of soil food webs . The ratio of fungi to bacteria indicates soil microbial shifts, whereas the Fu/, reflects the decomposition and nutrient mineralization pathway due to microbial feeders for a given ecosystem. Small ratios are associated with faster decomposition and nutrient turnover. We observed no difference in the ratio of fungivore to bacterivore. This finding is in line with previous studies suggesting no difference in Fu/ ratio between conventional and organic fields . It is possible that the effects of organic farming on the Fu/ depend on the ecosystem type. The PPI, MI, and PPI/MI are valuable indicators used to evaluate agricultural ecosystems conditions . In the present study, PPI was unaffected by the management intensity whereas MI and PPI/MI ratio were significantly affected. Previous studies also reported mixed results with some studies reporting higher values for both variables under organic farming than conventional farming whereas another study reporting that organic farming increased the PPI, but did not affect the MI and PPI/MI . One likely reason may be that the effect of organic management on MI varies with depending on crop type. However, other factors, such as soil type, plough depth, cover crop type, and the management history might also contribute to the divergent effects of organic farming on nematode assemblage . For example, land transformation from grasslands to arable fields under intensive management results in a reduced the MI of soil nematode community,whereas the conversion from grasslands to vegetable fields did not change MI.