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Widespread Occurrence of Pesticides in Organically Managed Agricultural Soils—the Ghost of a Conventional Agricultural Past?

  • Judith Riedo
    Judith Riedo
    Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
    Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
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    Orcidhttp://orcid.org/0000-0002-6887-7664
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  • Felix E. Wettstein
    Felix E. Wettstein
    Environmental Analytics, Agroscope, Zurich, Switzerland
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  • Andrea Rösch
    Andrea Rösch
    Environmental Analytics, Agroscope, Zurich, Switzerland
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  • Chantal Herzog
    Chantal Herzog
    Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
    Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
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  • Samiran Banerjee
    Samiran Banerjee
    Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
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  • Lucie Büchi
    Lucie Büchi
    Natural Resources Institute, University of Greenwich, Chatham Maritime, United Kingdom
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  • Raphaël Charles
    Raphaël Charles
    Research Institute of Organic Agriculture FiBL, Lausanne, Switzerland
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  • Daniel Wächter
    Daniel Wächter
    Swiss Soil Monitoring Network (NABO), Agroscope, Zurich, Switzerland
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  • Fabrice Martin-Laurent
    Fabrice Martin-Laurent
    Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne, Dijon, France
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  • Thomas D. Bucheli*
    Thomas D. Bucheli
    Environmental Analytics, Agroscope, Zurich, Switzerland
    *Tel. +41 58 468 7342. Email: [email protected]
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    Orcidhttp://orcid.org/0000-0001-9971-3104
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  • Florian Walder*
    Florian Walder
    Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
    *Tel. +41 58 480 8759. Email: [email protected]
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  • , and 
  • Marcel G. A. van der Heijden*
    Marcel G. A. van der Heijden
    Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
    Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    *Tel. ++41 58 468 7278. Email: [email protected]
    More by Marcel G. A. van der Heijden
Cite this: Environ. Sci. Technol. 2021, 55, 5, 2919–2928
Publication Date (Web):February 3, 2021
https://doi.org/10.1021/acs.est.0c06405

Copyright © 2022 American Chemical Society. This publication is licensed under CC-BY-NC-ND.

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Abstract

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Pesticides are applied in large quantities to agroecosystems worldwide. To date, few studies assessed the occurrence of pesticides in organically managed agricultural soils, and it is unresolved whether these pesticide residues affect soil life. We screened 100 fields under organic and conventional management with an analytical method containing 46 pesticides (16 herbicides, 8 herbicide transformation products, 17 fungicides, seven insecticides). Pesticides were found in all sites, including 40 organic fields. The number of pesticide residues was two times and the concentration nine times higher in conventional compared to organic fields. Pesticide number and concentrations significantly decreased with the duration of organic management. Even after 20 years of organic agriculture, up to 16 different pesticide residues were present. Microbial biomass and specifically the abundance of arbuscular mycorrhizal fungi, a widespread group of beneficial plant symbionts, were significantly negatively linked to the amount of pesticide residues in soil. This indicates that pesticide residues, in addition to abiotic factors such as pH, are a key factor determining microbial soil life in agroecosystems. This comprehensive study demonstrates that pesticides are a hidden reality in agricultural soils, and our results suggest that they have harmful effects on beneficial soil life.

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Introduction

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Pesticides constitute an integral part of modern agriculture and contribute to the control of weeds, plant diseases, and pests. Over the past two decades, the use of pesticides has increased over 40%, and currently, over 4.1 million tons are used worldwide each year. (1) Despite their benefits for crop yield, the intensive and widespread use of pesticides raises environmental concerns due to the contamination of natural resources. (2) Depending on their application, only a minor fraction of the applied pesticides reaches their targets, (3) with the rest (30 to 50%) ending up on the soil surface and thereafter getting dispersed through several abiotic processes including volatilization, wind erosion, leaching, or runoff. (4)
The occurrence of pesticide residues in agricultural soils has been reported in a limited number of recent studies. (5−7) To date, it has been poorly investigated whether pesticides are also present in soils where they have not been applied, such as soils under organic management. One study compared residues of currently used pesticides in agricultural soils under conventional and organic management, considering five neonicotinoid insecticides. (8) However, broad scale investigations of various groups of pesticides (e.g., fungicides, herbicides, and insecticides) in organically managed soils are missing. Testing this is of great importance, as pesticide residues of past agricultural management or contamination from conventional fields could especially affect organic agriculture. Organic agriculture relies more on healthy soils that are capable of sustaining ecosystem services than systems under different management practices, such as conventional management where external inputs (e.g., synthetic pesticides and fertilizers) are allowed. (9) It is therefore important to know how long pesticides persist in those organically managed agricultural soils and whether they threaten soil health, which is indispensable for these sustainable systems.
Pesticides, i.e. their active ingredients, and their transformation products (TPs) are known to pollute aquatic environments (10) and to impact aquatic communities. (11) In terrestrial systems they have directly and indirectly been linked to decreasing bird, insect and pollinator populations. (12−15) Studies in model systems with individual pesticides on single organisms further showed that specific pesticides constitute a threat to soil microorganisms, (16) which drive pivotal soil processes such as carbon and nutrient cycling. (17) In the field, studies tested effects of individual pesticides, such as for example the herbicide nicosulfuron, (18) on soil microorganisms. They showed that these individual pesticides negatively affected microbial biomass as well as arbuscular mycorrhizal fungi (AMF) by inhibiting enzyme pathways and eventually stopping protein production. As soil life provides a wide range of ecosystem services and influences ecosystem multifunctionality, (19,20) these deleterious effects of pesticides on beneficial soil life could thus potentially affect soil health, (21) which is crucial for agricultural production. (22) The influence on AMF is of particular interest, as these fungi engage in symbiotic associations with the majority of land plants, including many crops. They provide nutrients and other services to plants in return for carbohydrates. (23,24) Up to 80% of the plant’s phosphorus requirements can be contributed by AMF pointing to their importance for plant nutrition. AMF further provide a number of ecosystem services such as the promotion of soil structure and aggregation and the reduction of nutrient losses through leaching and denitrification. (25) While many studies looked into effects of individual pesticides in model or field studies, those on farm studies that link the occurrence of multiple pesticides to soil life, such as AMF, are missing so far. Therefore, it is still poorly understood whether pesticides in soil act as potential stressors for soil life under farm conditions and how it is affected by the amount of pesticide residues.
Here we provide a comprehensive overview of the presence and abundance of 46 widely applied pesticides (16 herbicides, 8 herbicide TPs, 17 fungicides, and 7 insecticides) in soils of 100 agricultural fields, including 40 under organic management. The following four objectives were addressed: (i) Sixty arable and 40 vegetable fields were compared and it was assessed whether management systems (conventional, conventional without soil tillage (no-till), and organic management) influenced the occurrence of pesticides. (ii) Further, it was investigated whether the duration of organic management affected the occurrence and concentration of pesticides in the soil. (iii) We also evaluated whether soil characteristics influenced the occurrence of pesticide residues and (iv) additionally tested whether the occurrence of pesticide residues detected in this on farm study are linked to indicators of soil life (soil microbial biomass and respiration as well as the abundance of AMF).

Methods

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Study Sites and Soil Sampling

Arable Farming

Soil samples from 60 agricultural sites with different management systems (conventional tillage, conventional without soil tillage, and organic) were sampled in early May 2016 for an on-farm study throughout Switzerland. (26) The farmlands were distributed equally in two sampling areas in the northeast and southwest of Switzerland with 20 sites per management system. The conventional fields implemented soil tillage (20–25 cm depth) and usually applied synthetic fertilizers and pesticides. The no-till cropping systems were managed without soil tillage and with use of synthetic fertilizers and pesticides. Both farming systems followed the ‘Proof of Ecological Performance’ guidelines from the Swiss Federal Office for Agriculture. (27) The organic fields did not apply synthetic pesticides and synthetic fertilizers, applied tillage (20–25 cm depth), and were managed according to the guidelines of the Federation of Swiss Organic Farmers. (28) Winter wheat was seeded in all fields the year before. All soils were characterized as Cambisols and varied in soil texture, elevation, and mean annual temperature. However, none of these parameters differed significantly between farming systems. (26) The median soil characteristics are listed in Table S2 of the Supporting Information (SI).
Details on each farm’s agricultural management were collected directly from the farmers through a questionnaire about management practices applied on the selected field in the last five years (for details see Büchi et al. (26)). Management indices for the degree of plant diversification and soil disturbance as well as amount of mineral fertilizer and organic amendments applied could be deducted from the survey. The farmers further provided an overview of the pesticides applied throughout the year before sampling. (26)
Soil sampling and processing were performed as described by Banerjee et al. (29) and Büchi et al. (26) Twenty soil cores (4 cm diameter) were collected over two transects of 20 m length. To reduce the risk of contamination from neighboring fields a 20 m buffer zone from the field edge was maintained. The 20 cores were mixed and pooled to obtain a representative sample. Due to the high degree of stratification in soils without tillage, the top 5 cm of the soils were sampled representing the most exposed soil layer. Soil samples were processed by removing plant materials, homogenization, and sieving (2 mm). Until further analysis, the samples were stored at −20 °C.

Vegetable Farming

The vegetable farming network consisted of 40 fields (20 under conventional and 20 under organic management) in eastern Switzerland. The soils were also characterized as Cambisol. The organic and conventional systems were managed as described above. The median soil characteristics are listed in SI Table S2. Information on each farm’s agricultural management practices, such as the duration for which the organic sites were managed organically, were collected directly from the farmers through a questionnaire.
Soil samples from the vegetable fields were taken in December of 2016 and were part of a different field study with a slightly different sampling regime. Ten soil cores were randomly collected at each site. The cores were then immediately mixed and pooled to obtain a representative sample for each field. Samples were kept on ice and transported to the laboratory where they were sieved (5 mm) and stored at −20 °C until further analysis. As all vegetable fields were frequently ploughed, a sampling depth of 10 cm has been chosen. Consequently, the sampling depth between arable and vegetable sites differed.

Physicochemical Soil Analyses

The soil physicochemical properties, organic C, texture, pH, and soil nutrients (N, K and P), were determined according to the Swiss reference methods of the Federal Agricultural Research Station. (30) Organic C was determined with the Walkley–Black method. The texture was analyzed with a pipetting method with clay <2 μm, silt 2 to 50 μm, and sand >50 μm as cut-offs, and pH was determined in water. The total nitrogen was determined with the Dumas method. Potassium was extracted with 0.5 M ammonium acetate–EDTA solution at pH 4.65. Total P was extracted by washing the soil sample and using 0.6 M HCl as extractant. Potassium and total P were only measured for the arable fields. (30)

Selection of Analyzed Pesticides

The analyzed synthetic pesticides were selected by the Swiss Soil Monitoring Network taking into account their analytical determinability, (7) the amount and frequency of usage, the expected amounts in soil based on the predicted environmental concentrations, and estimations by experts in the field. All 46 chosen substances, including 38 parent substances and 8 TPs (SI Table S1), are modern pesticides, which are designed to be less persistent and more easily biodegradable than previously used pesticides such as for example organochlorines. (31,32)

Sample Extraction and Analysis with LC-MS/MS

Accelerated Solvent Extraction (Dionex ASE 350, Thermo Scientific) was used to extract the pesticide residues from the soil samples. Soil samples were thawed 2 h before extraction and were subsequently homogenized with a TURBULA (Bühler GmbH) for 15 min. Each 6 g ± 0.01 g of wet soil were weighed into an 11 mL stainless steel extraction cell, which was prefilled with 1 g of sea sand and topped with another 1 g of sea sand. Two glass fiber filters (Whatman GF/F) covered the top and the bottom of the cell. The soil was extracted twice: in a first step, an organic mixture of acetone, methanol, and acetonitrile at a ratio of 65:10:25 (% v/v) was used, and in a second, acidic step, the soils were extracted with a mixture of acetone and 1% phosphoric acid in Millipore water at a ratio of 70:30 (% v/v). Detailed information on extraction parameters such as temperature and pressure are provided in SI Table S3.
Due to the expected large concentration range of the pesticides in the soil samples, two different aliquots of each extract were processed. Two different volumes, 4 mL and 0.4 mL, of extract were evaporated under a gentle stream of compressed air down to 0.4 mL or down to dryness. Subsequently, the extracts were diluted to 1 mL with a mixture of Millipore water and methanol at a ratio of 90:10 (% v/v). A mixture of 23 isotopically labeled internal standards was spiked, and the samples were filtered through 0.20 μm PTFE filters (Fisher Scientific). Lastly, the samples were transferred into HPLC-vials.
Pesticides were analyzed by high-performance liquid chromatography coupled to a triple quadrupole tandem mass spectrometer (HPLC-MS/MS). Chromatographic separation was performed by reversed phase HPLC using water and methanol as mobile phase. The detection was performed after electrospray ionization with a triple quadrupole mass spectrometer (QTrap 5500, Sciex) in positive and negative ionization mode. All detected pesticide concentrations (μg/L) were converted into μg per kg of dry soil. Further details about the analytical method, quantification, and quality control can be found in the SI (Chapter 8. Pesticide analysis in soils).

Root Sampling and Mycorrhizal Colonization

Indicators of microbial soil life were only assessed in the arable sites, as they were sampled when an active agroecosystem with living roots was present (spring). Whereas the vegetable sampling campaign was conducted in wintertime during which not all sampled fields were growing vegetables and therefore had no active rhizosphere. The abundance of AMF in root and soil were determined as described by Banerjee et al. (29) Briefly, the root samples of 10 wheat plants per site were dug out, cut off 5 cm above the roots, and pooled in a plastic bag. Subsequently, the roots were cleaned with water and fine roots (<1 mm) were cut into pieces of about 1 cm and were thoroughly mixed. The mycorrhizal colonization was determined by an estimation of the abundance of arbuscules, hyphae, or vesicles. The abundance of AMF in soil was assessed by PLFA extraction followed by analysis on gas chromatography mass spectrometry. (33) We quantified the abundance of AMF in soil by using the PLFA 16:1ω5, which is well regarded as a biomarker for AMF. (34)

Microbial Biomass and Basal Respiration

For the arable soil samples, microbial biomass carbon and nitrogen estimates by chloroform–fumigation–extraction were carried out according to Vance et al. (35) The extracted organic C was determined by infrared spectrometry after combustion (DIMA-TOC 100, Dimatec), and extracted N was measured by chemo luminescence (TNb, Dimatec). Soil microbial biomass was then calculated according to Joergensen (36) and Joergensen and Mueller. (37) Basal respiration was determined by preincubating soils for 7 days at 50% water holding capacity to stabilize microbial communities. Soils were then incubated in a closed system with a NaOH solution for 24 h and transferred to a new bottle to absorb the emitted CO2 in a NaOH solution over 72 h. The resulting Na2CO3 was precipitated with BaCl2, and the unused NaOH was determined by titration with HCl. (38)

Statistical Analyses

All statistical analyses were performed using R version 3.6.3. (39) Differences between management systems for the occurrence and sum of concentration of pesticide residues were determined by analysis of variance (ANOVA) and subsequent simultaneous multiple comparison of least-squares means (package “lsmeans” (40)). The heatmaps were created using the levelplot function of the lattice package. (41) To describe the relation of numbers of pesticide, as well as pesticide concentrations, with the duration of organic management, the sites were grouped in five-year intervals and the difference was identified with ANOVA. Pairwise correlations between single pesticides and soil properties of the different fields were tested with the cor function based on a Spearman rank correlation coefficient, and p-values were adjusted for multiple comparison with the fdr method. The plot was displayed with the corrplot package. (42)
For arable fields, multimodel inference and random forest analyses were performed to investigate the possible influence of pesticide residues on the soil life parameters, microbial biomass, basal respiration, and abundance of AMF in roots and soil. Due to sample size limitations, insufficient degrees of freedom were available to test the effect of individual pesticide residues on different response variables. Therefore, only the number and the sum of the pesticide concentration were considered. In addition to these indices for the degree of soil pesticide pollution, all physicochemical soil properties, namely soil texture (sand, clay, including the quadratic terms sand2, clay2, and the interaction of sand * clay to account for nonlinear relationships), pH, organic carbon, bulk density, and total N, P, and K were considered as predictors. Further management practices, such as management system, plant diversification, tillage, mineral fertilizer, and organic amendments were also included as predictors. All predictors were tested for collinearity based on Spearman correlation with a threshold level of 0.7 (due to the high correlation of number of pesticide residues and sum of the pesticide concentrations, only the first could be considered). Multimodel inference was applied to assess which predictors across all possible models best predicted the difference in abundance for each of the soil life parameters. Multimodel inference was performed using the package glmulti. (43,44) The unconditional model-averaged parameter estimates and standard errors, z-values, p-values, and the relative importance were extracted with the metaphor package (45) to evaluate the predictors. In addition, random forest analysis was performed to identify the main predictors of abundance for each of the soil life parameters. The importance of each predictor variable was determined by reviewing the increase in the mean square error (MSE). These analyses were conducted using the randomForest package. (46) The significance of the importance of each predictor on multifunctionality was assessed by using the rfPermute package. (47)

Results and Discussion

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Widespread Occurrence of Pesticide Residues

The analysis revealed that pesticide residues were widespread in agricultural soils and that all of the 100 tested sites contained pesticide residues in the top soil layer. The number of detected pesticides per field varied from 3 to 32, with similar numbers in arable and vegetable fields. Soils under conventional management contained about twice as many detected residues (median = 18 different pesticides) compared to soils under organic management (median = 8 different pesticides) (Figure 1A). Arable sites under conventional and no-till management were similar and contained an average of 17 different pesticides. The soil with the highest number of residues (32 different pesticides) was an arable field under no-till management (Figure 1A).

Figure 1

Figure 1. (A) Number of pesticide residues in arable and vegetable fields under conventional management with tillage, conventional management without tillage, or organic management. For each management system 20 fields were analyzed. (B) Sum of the concentrations of pesticides in arable and vegetable fields under conventional, conventional without tillage, or organic management.

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The sum of the concentration of all residues (μg per kilogram of dry soil) also differed significantly between the management systems (see Figure 1B). Conventionally managed vegetable fields contained the highest pesticide loads with concentrations of up to 1170 μg/kg. The median total pesticide concentration in conventionally managed vegetable fields was 79% higher than the median of the conventionally managed arable fields. The median sum of pesticide concentration in organic sites under arable or vegetable production was in both cases 85% lower (arable production: max. 52 μg/kg, vegetable production: max. 90 μg/kg) than the median in conventionally managed sites. However, as the samples were taken from two different soil layers (0–5 cm for the arable fields and 0–10 cm for the vegetable fields) and because the farming systems varied in many aspects including application rate and the formulation of the pesticides being applied (e.g., application rates of pesticides in vegetable systems were much higher), the direct comparisons of residual pesticide concentrations between both systems are difficult. Since both sampling depths lay within the ploughing layer, soils from conventional and organic fields were well mixed, but due to the stratification in the no-till fields, concentrations in the latter are most likely overestimated in comparison to the former management practices. Nonetheless, the sites under no-till management did not differ clearly in their median sum of pesticide concentrations from either conventional or organic managed soils of the arable farming system (Figure 1B). It was expected that the fields under no-till farming would exhibit higher herbicide concentrations, as they are needed to control weeds, which are otherwise removed with tillage. (48) Furthermore, tillage is known to increase catabolic processes, such as oxidation and mineralization, and thus increase the degradation of pesticide residues. (49) However, only three no tillage sites showed high levels of herbicides and thus this hypothesis could not be confirmed.
Out of the 46 analyzed pesticides and transformation products (TPs), 41 were detected in at least one soil, including 12 herbicides, 8 herbicide TPs, 16 fungicides, and 7 insecticides (Figure 2). 2-Hydroxyatrazine, a TP of atrazine (a broad leaf herbicide), was detected most frequently, in 92% of the arable soils and in 100% of the vegetable soils. It further had the highest contribution to the pesticide load in organically managed sites. The herbicide residues atrazine, chloridazon, linuron, napropamide, and terbutylazine; the fungicide residues carbendazim and epoxyconazole; and the insecticide residues clothianidin and imidacloprid were also detected in more than half of the soils of all management systems, and in both arable and vegetable farming systems. The herbicides metamitron, S-metolachlor, and the TP 6-desisopropylatrazine were more abundant in soils from the arable farming system, whereas soils of the vegetable farming systems contained considerable amounts of the fungicides azoxystrobin and metalaxyl, as well as the insecticides pirimicarb and thiamethoxam. The two conventional vegetable sites with the highest loads of pesticide residues contained exceptionally high concentrations of the herbicide linuron and the fungicide azoxystrobin. In the conventional management fields without tillage, the concentrations of the herbicides S-metolachlor, terbutylazine, and its TPs stood out (Figure 2). The occurrence and concentrations of pesticides in agricultural soils can be strongly influenced by the time of sampling and the time of pesticide application. The questionnaires of the arable fields showed for instance that in some fields pesticides were applied in the week before sampling, explaining single high concentrations of epoxiconazole, boscalid, or tebuconazole.

Figure 2

Figure 2. Abundance of 46 pesticides and transformation products (indicated with an asterisk) in the arable and vegetable fields under conventional, no-till, and organic management. Each row represents a pesticide, and each column, one field. The method limits of quantification (MLOQ) ranged between 0.064 μg/kg and 36 μg/kg depending on the substance (SI, Table S8). The color range represents the level of the detected concentrations, whereas empty (white) cells indicate no detects (<MLOQ). The bars on the right show the frequency of occurrence of a specific compound across all samples.

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Pesticide Residues in Organically Managed Fields

The questionnaires additionally gave information about how long the fields were managed organically. The number of pesticide residues as well as the sum of the total pesticide concentration declined significantly with the duration of organic farming by 70% or 90% respectively. However, even after 20 years of organic management, between 3 and 16 different pesticide residues were still detected (Figure 3, Figure S2). The herbicides linuron, napropamide, chloridazon, and atrazine (including TPs), as well as the fungicide carbendazim, were the pesticides that prevailed the longest after conversion to organic farming and were present in the soils, which converted to organic several years ago. As the organically managed fields had not been exposed to direct pesticide application for at least three years, our work suggests that either pesticides persisted in soil far longer than expected or that contamination occurred via an indirect pathway from adjacent conventional fields through particle drift, wind erosion, or runoff. (50)

Figure 3

Figure 3. Decrease of the number of pesticide residues in soils, including both arable and vegetable farms, with the duration of organic management. The duration of organic management is expressed as the number of years since the conversion from conventional to organic. The sites were grouped in five-year time intervals.

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For some of the detected pesticides, such as napropamide, chloridazon, and carbendazim, which are currently applied in many countries including Switzerland, this diffuse contamination via drift is possible. (1) However, for other residues, such as atrazine (and its TPs), which was banned in Switzerland in 2007, (51) an indirect pathway of contamination is not possible anymore. This implies that atrazine residues persist much longer than their half-lives (DT50) of 6–108 days as field studies suggest (52) (SI, Table S1). The half-lives of various other pesticides, such as chloridazon, carbendazim, and linuron, are also low (SI, Table S1), but they were still detected after 20 years of organic management. Older, formerly used pesticides, such as organochlorine pesticides (e.g., DDT), which were last used decades ago, had also been found in soils after conversion to organic management. (53) While the high persistence of compounds of earlier pesticide generations is a known drawback, the presence of pesticides approved in the past 30 years is against expectation, as they are considered less persistent and more rapidly biodegradable. (2) When the pesticides half-lives and their maximal application dosage are taken into account, traces of only five pesticides (boscalid, epoxiconazole, fluopicolid, flusilazole, and an S-metolachlor TP) should still be detectable after ten years. This suggests that, additional input pathways as specified above excluded, these residues remained in the soils even after the conversion from the previous conventional management to organic management and degrade slower than assumed.

Influence of Soil Characteristics on the Occurrence of Pesticide Residues

Additionally, it was tested whether the abundance of pesticide residues or their TPs was linked to specific soil characteristics (soil organic carbon, pH, total nitrogen, texture) (SI Figure S1). The number of pesticides and the sum of concentrations of all pesticide residues were generally not related to the tested soil characteristics. However, the abundance of specific pesticides such as terbutylazine-desethyl (R2 = 0.690, P < 0.001) and fenpropidin (R2 = 0.256, P = 0.014) was positively correlated to soil organic matter content (SI Figure S1). Indications for pH-dependent occurrence of pesticides were observed for individual pesticides including atrazine and its TPs (R2 = 0.228, P < 0.001) as well as fenpropidin (R2 = 0.180, P = 0.044), which showed a negative correlation (SI, Figure S1). This relation suggests that increasing soil pH decreases the biodegradation and mobility of these pesticide residues. This implies that these soil characteristics are at least partly responsible for the high concentrations of atrazine residues, even after many years of organic management. Soil pH is also known to be an important factor that can influence the mobility and degradation of pesticides. (54) For example, higher levels of pesticides were found in soils with a low soil pH, possibly because the ability of such soils to sorb pesticides is higher, resulting in increased persistence. (55) Moreover, microbial activity is reduced at low soil pH, which could impair the breakdown of pesticides (56) and adaptation to pesticide degradation is decreased in acidic soils. (57) In addition, compound properties can play a role in their sorption and degradation. As many of the analyzed pesticides are ionizable, and thus protonate or deprotonate in accordance to their pKA value (SI, Table S1), their sorption is expected to be pH dependent. (58)

Pesticide Residues as a Negative Driver for Microbial Biomass and Arbuscular Mycorrhiza Fungi

For the assessment of the influence pesticide residues on indicators of soil life, we focused on the subset of all 60 arable fields because these were sampled in spring when an active agroecosystem with living roots was present (e.g., for the vegetable fields samples were taken in winter). Furthermore, the arable fields all had the same crop (wheat), which facilitates the comparison, as plant host species has a big impact on AMF root colonization. (24)
Multimodel inference revealed that pH, the number of pesticide residues, and soil texture best predict microbial biomass C and AMF root colonization (Figure 4A and B). Microbial biomass and AMF root colonization were negatively correlated to the number of pesticides residues. This negative correlation was also visible when looking at the direct relationships of the two parameters and when correcting for variation explained by pH, soil organic matter content, and sampling area (Figure 4C–D). The negative correlation between the number of pesticide residues and AMF colonization was most pronounced (Figure 4D).

Figure 4

Figure 4. (A and B) Relative importance of various variables, which explained microbial biomass (A) and AMF root colonization (B) in arable farming using multimodel inference. The bars represent the importance of predictors (see methods for details on individual variables). The colors of the bars indicate the model’s average estimate, where blue implies positive and red negative values. Management (gray bar as this is a categorical variable) is also included in the figure regardless of its rank as a predictor. Asterisks indicate the statistical significance of the variables (*P < 0.05; **P < 0.01; ***P < 0.001). (C) Univariate relationship of microbial biomass C and numbers of pesticide residues corrected for pH, Corg, and sampling area (see methods: Statistical analyses). The colors represent the management systems (dark blue = conventional, light blue = conventional without tillage, green = organic); the solid line indicates the regression line, and the dotted line, the 95% confidence interval. (D) Univariate relationship of AMF and number of pesticide residues corrected for pH, Corg, and sampling area. The relationships between AMF colonization and the number of pesticide residues was also significant without correcting for pH, Corg, and sampling area (SI, Figure S5).

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Further statistical testing with random forest analysis confirmed the multimodel inference and regression analyses and highlighted the importance of the number of pesticides and pH in explaining the abundance of AMF in roots, but not for the microbial biomass (SI, Figure S4). The negative correlation for the abundance of AMF in roots was further confirmed by an AMF specific phospholipid fatty acid (PLFA) biomarker (SI, Figure S3). However, for the AMF biomarker the effect of the pesticide residues was not statistically significant throughout all models (SI, Figure S4). In contrast, for basal respiration, a metric of microbial activity, pesticide residues seem not to be a major driver and no correlation between basal respiration and number of pesticide residues was detected (SI, Figure S3).
We only performed our analysis with all pesticide residues together and not for separate pesticide types (e.g., fungicides, herbicides, and/or insecticides) as it was not possible to assess which type of pesticides was responsible for the observed effects because the occurrence of the types was highly correlated (SI, Figure S1). Furthermore, it was not possible to differentiate between the concentration and number of pesticide residues because these two variables were also highly correlated (SI, Figure S1).
The robust negative association between the number of pesticides and AMF reveals that pesticides in soil are likely a key driver of AMF abundance in the field. It is well established that mineral fertilization reduces the abundance and diversity of AMF and several studies also showed that soil pH influences AMF abundance. (59,60) However, the impact of pesticides on AMF is poorly understood and previous studies were performed under controlled conditions, applying pesticides one by one at rather high application rates, and led to an inconclusive picture. (61) Moreover, so far it has not yet been shown that pesticide residues in soil have such a big impact on AMF abundance in an on-farm study. In our study, the number of pesticide residues was even more important in explaining AMF abundance than mineral fertilization, indicating that the suppression of AMF in many agricultural soils not only is the result of fertilization but also comes from pesticide management. Furthermore, we observed that even though the highest amount of AMF root colonization could be found in organically managed fields and lowest levels in conventionally managed fields, in the statistical analyses pesticide residues and pH best explained AMF abundance and exceeded the effect of management system. Our analysis implies that pesticide management must be considered when explaining the distribution and abundance of AMF in agroecosystems. The mechanisms responsible for the effects of pesticides on AMF remain unclear and need further investigation. Pesticides in soil (e.g., fungicides) could directly impair the growth of fungal hyphae or interfere with specific physiological processes such as uptake and transport of metabolites and nutrients or the signaling between plant and mycorrhizal fungus. These findings are important because AMF, as mentioned above, form symbiotic associations with plants while providing a number of crucial ecosystem services and are thus indispensable for a healthy soil. (23)

Insight and Future Research

The results highlight that the ubiquitous contamination of agricultural soils with a variety of pesticides can have long-term negative effects on soil life. We demonstrate that organically managed sites experience a legacy effect of past conventional management. Moreover, our data indicate that the persistence of both banned and currently used pesticides is underestimated. Even though low concentrations were detected in soils of organically managed fields, the potential effect of this long-term contamination is especially critical, as fields under organic management rely much more on biological soil processes and beneficial soil life such as AMF. Further, the modeled data show that pesticide residues could have a detrimental influence on soil microbial life.
Our work indicates that future studies should not only focus on single pesticides but also consider a wide range of pesticide combinations (e.g., cocktails) and further investigate to what extent these pesticide residues affect soil organisms and consequently soil processes and functions. Additionally, studies should also investigate interactions of pesticide residues with other global change factors such as drought, antibiotics, or microplastic since these abiotic and anthropogenic stressors can synergistically or antagonistically affect soil microbiota and reduce soil functioning. (62)

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c06405.

  • 1.

    Relation between soil characteristics and the occurrence of pesticide residues

    2.

    Decrease of total pesticide concentration with duration of organic management

    3.

    Effects of pesticide residues on basal respiration and PLFA for AMF

    4.

    Results of the random forest analysis

    5.

    Uncorrected univariate relationships

    6.

    Pesticides and pesticide transformation products included in this study

    7.

    Soil characteristics of the selected fields and the test soils used for method validation

    8.

    Pesticide analysis in soils

    8.1.

    Chemicals and reagents

    8.2.

    Accelerated Solvent Extraction and further Sample Preparation

    8.3.

    High-performance Liquid Chromatography coupled to Triple Quadrupole Tandem Mass Spectrometry (HPLC-MS/MS)

    8.4.

    Quantification

    8.5.

    Method Validation

    9.

    Measured concentrations and method limits of quantification

    10.

    Supplementary References

    (PDF)

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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

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  • Corresponding Authors
  • Authors
    • Judith Riedo - Plant-Soil-Interactions, Agroscope, Zurich, Switzerland;  Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland;  Orcidhttp://orcid.org/0000-0002-6887-7664
    • Felix E. Wettstein - Environmental Analytics, Agroscope, Zurich, Switzerland
    • Andrea Rösch - Environmental Analytics, Agroscope, Zurich, Switzerland
    • Chantal Herzog - Plant-Soil-Interactions, Agroscope, Zurich, Switzerland;  Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    • Samiran Banerjee - Plant-Soil-Interactions, Agroscope, Zurich, Switzerland
    • Lucie Büchi - Natural Resources Institute, University of Greenwich, Chatham Maritime, United Kingdom
    • Raphaël Charles - Research Institute of Organic Agriculture FiBL, Lausanne, Switzerland
    • Daniel Wächter - Swiss Soil Monitoring Network (NABO), Agroscope, Zurich, Switzerland
    • Fabrice Martin-Laurent - Agroécologie, AgroSup Dijon, INRAE, Univ. Bourgogne, Dijon, France
  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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We thank the participating farmers and vegetable producers from the farming networks for making this study possible. We would also like to thank Andrea Bonvicini, Susanne Müller, Andrea Corona Ramírez, and Diane Bürge for their support with soil analyses; Andreas Gattinger and Andreas Fliessbach for helping with PLFA analyses; Marc M. Schmid for helpful statistical discussions; and Robert Baur for support and discussion. We would like to thank the Swiss Federal Office for the Environment for funding the development of the analytical methods. Furthermore, we are grateful for the helpful input from Kathrin Fenner (EAWAG). This study was funded by Agroscope (start-up funds), the Swiss National Science Foundation (Grant 31003A 66079), and the National Research Program ‘Sustainable Use of Soil as a Resource’ (NRP 68, Grant 406840-161902).

References

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    Pesticides and earthworms. A review
    Pelosi, Celine; Barot, Sebastien; Capowiez, Yvan; Hedde, Mickael; Vandenbulcke, Franck
    Agronomy for Sustainable Development (2014), 34 (1), 199-228CODEN: ASDGAP; ISSN:1773-0155. (Springer France)
    A review. Earthworms provide key soil functions that favor many pos. ecosystem services. These services are important for agroecosystem sustainability but can be degraded by intensive cultural practices such as use of pesticides. Many literature reports have investigated the effect of pesticides on earthworms. Here, we review those reports to assess the relevance of the indicators of earthworm response to pesticides, to assess their sensitivity to pesticides, and to highlight the remaining knowledge gaps. We focus on European earthworm species and products authorised in Europe, excluding natural compds. and metals. We consider different organization levels: the infra-individual level (gene expression and physiol.), the individual and population levels (life-history traits, population d. and behavior) and the community level: community biomass and d. Our anal. shows that earthworms are impacted by pesticides at all organization levels. For example, pesticides disrupt enzymic activities, increase individual mortality, decrease fecundity and growth, change individual behavior such as feeding rate and decrease the overall community biomass and d. Insecticides and fungicides are the most toxic pesticides impacting survival and reprodn., resp.
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    Karpouzas, D.; Papadopoulou, E.; Ipsilantis, I.; Friedel, I.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Kandeler, E.; Menkissoglu-Spiroudi, U.; Martin-Laurent, F. Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity. Ecol. Indic. 2014, 39, 44– 53,  DOI: 10.1016/j.ecolind.2013.12.004
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    Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity
    Karpouzas, D. G.; Papadopoulou, E.; Ipsilantis, I.; Friedel, I.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Kandeler, E.; Menkissoglu-Spiroudi, U.; Martin-Laurent, F.
    Ecological Indicators (2014), 39 (), 44-53CODEN: EICNBG; ISSN:1470-160X. (Elsevier Ltd.)
    The key role of arbuscular mycorrhizal (AM) fungi in maintaining soil fertility and ecosystem functioning and their general sensitivity to pesticides make them good candidate bioindicators in pesticide soil microbial toxicity assessment. We investigated the impact of the herbicide nicosulfuron on mycorrhizal colonization and community structure of AM fungi via a pot-to-field exptl. approach. This allowed the assessment of nicosulfuron toxicity (i) at extreme exposure schemes (pot expt., Tier I) invoked by the repeated application of a range of dose rates (x0, x10, x100, x1000 the recommended dose) and (ii) under realistic exposure scenarios (x0, x1, x2, x5 the recommended dose) in the field (Tier II). In the pot expt., the x100 and x1000 dose rates significantly reduced plant biomass, mycorrhizal colonization and AM fungal richness as detd. by DGGE. This coincided with the progressive accumulation of herbicide concns. in soil. In contrast, no effects on AM fungi were obsd. at the nicosulfuron dose rates tested in the field. Clone libraries showed that the majority of AM fungi belonged to the Glomus group and were sensitive to the high levels of nicosulfuron accumulated in soil at the latter culture cycles. In contrast, a Paraglomeraceae and a Glomus etunicatum ribotype were present in maize roots in all cycles and dose rates implying a tolerance to nicosulfuron-induced stress. Overall, the deleterious effects of nicosulfuron on AM fungi induced by the highest dose rates in the pot expt. could be attributed either to fungal-driven toxicity or to plant-driven effects which have subsequent implications for mycorrhizal symbiosis. Thus, tiered pot-to-field exptl. approach followed in our study combined with classic and standardized mol. tools could provide a realistic assessment of the toxicity of pesticides onto AM fungi as potential bioindicators.
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    Wagg, C.; Schlaeppi, K.; Banerjee, S.; Kuramae, E. E.; van der Heijden, M. G. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat. Commun. 2019, 10 (1), 1– 10,  DOI: 10.1038/s41467-019-12798-y
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    Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning
    Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran; Kuramae, Eiko E.; van der Heijden, Marcel G. A.
    Nature Communications (2019), 10 (1), 1-10CODEN: NCAOBW; ISSN:2041-1723. (Nature Research)
    The soil microbiome is highly diverse and comprises up to one quarter of Earth's diversity. Yet, how such a diverse and functionally complex microbiome influences ecosystem functioning remains unclear. Here we manipulated the soil microbiome in exptl. grassland ecosystems and obsd. that microbiome diversity and microbial network complexity pos. influenced multiple ecosystem functions related to nutrient cycling (e.g. multifunctionality). Grassland microcosms with poorly developed microbial networks and reduced microbial richness had the lowest multifunctionality due to fewer taxa present that support the same function (redundancy) and lower diversity of taxa that support different functions (reduced functional uniqueness). Moreover, different microbial taxa explained different ecosystem functions pointing to the significance of functional diversity in microbial communities. These findings indicate the importance of microbial interactions within and among fungal and bacterial communities for enhancing ecosystem performance and demonstrate that the extinction of complex ecol. assocns. belowground can impair ecosystem functioning.
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    Delgado-Baquerizo, M.; Maestre, F. T.; Reich, P. B.; Jeffries, T. C.; Gaitan, J. J.; Encinar, D.; Berdugo, M.; Campbell, C. D.; Singh, B. K. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 2016, 7, 10541,  DOI: 10.1038/ncomms10541
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    Microbial diversity drives multifunctionality in terrestrial ecosystems
    Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B.; Jeffries, Thomas C.; Gaitan, Juan J.; Encinar, Daniel; Berdugo, Miguel; Campbell, Colin D.; Singh, Brajesh K.
    Nature Communications (2016), 7 (), 10541CODEN: NCAOBW; ISSN:2041-1723. (Nature Publishing Group)
    Despite the importance of microbial communities for ecosystem services and human welfare, the relationship between microbial diversity and multiple ecosystem functions and services (i.e., multifunctionality) at the global scale has yet to be evaluated. Here we use two independent, large-scale databases with contrasting geog. coverage (from 78 global drylands and from 179 locations across Scotland, resp.), and report that soil microbial diversity pos. relates to multifunctionality in terrestrial ecosystems. The direct pos. effects of microbial diversity were maintained even when accounting simultaneously for multiple multifunctionality drivers (climate, soil abiotic factors and spatial predictors). Our findings provide empirical evidence that any loss in microbial diversity will likely reduce multifunctionality, neg. impacting the provision of services such as climate regulation, soil fertility and food and fiber prodn. by terrestrial ecosystems.
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    Karpouzas, D.; Kandeler, E.; Bru, D.; Friedel, I.; Auer, Y.; Kramer, S.; Vasileiadis, S.; Petric, I.; Udikovic-Kolic, N.; Djuric, S. A tiered assessment approach based on standardized methods to estimate the impact of nicosulfuron on the abundance and function of the soil microbial community. Soil Biol. Biochem. 2014, 75, 282– 291,  DOI: 10.1016/j.soilbio.2014.04.022
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    A tiered assessment approach based on standardized methods to estimate the impact of nicosulfuron on the abundance and function of the soil microbial community
    Karpouzas, D. G.; Kandeler, E.; Bru, D.; Friedel, I.; Auer, Y.; Kramer, S.; Vasileiadis, S.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Martin-Laurent, F.
    Soil Biology & Biochemistry (2014), 75 (), 282-291CODEN: SBIOAH; ISSN:0038-0717. (Elsevier B.V.)
    Pesticides impact soil microorganisms in various ways. Despite the pivotal role of the latter in ecosystem functioning, the assessment of pesticides soil microbial toxicity is lagging behind the recent methodol. advances in microbial ecol. The authors investigated the impact of nicosulfuron, a low dose sulfonylurea herbicide, on the structure, abundance and function of the soil microbial community using standardized methodologies (PLFAs, taxa-specific qPCR and enzyme activities). For this purpose a Tiered approach involving assessment (i) at extreme, long term (five repeated application cycles) exposure schemes in a microcosm expt. conducted under greenhouse conditions (x0, x10, x100 and x1000 the recommended dose, Tier I) and (ii) at realistic field exposure scenarios (x0, x1, x2 and x5, Tier II) was followed. Significant redns. in the abundance of Gram neg. (β-proteobacteria, planctomycetes) and Gram pos. bacteria (actinobacteria) were indicated by both PLFA and qPCR analyses at low soil concns. of nicosulfuron (0.25-1 μg g-1), while a redn. of fungi at equally low levels of nicosulfuron in soil was found only by qPCR anal. C- and P-cycling enzymes were particularly sensitive even at low soil concn. of the herbicide (0-1 μg g-1). In contrast, no inhibitory effects of nicosufluron at field conditions were found. The only exception was cellobiohydrolase which were impaired at herbicide rates higher than the recommended. The authors suggest that the use of a tiered microcosm-to-field experimentation combined with the application of standardized methodologies could provide a comprehensive assessment of the soil microbial toxicity of pesticides.
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    A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment
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    ISME Journal (2016), 10 (2), 389-399CODEN: IJSOCF; ISSN:1751-7362. (Nature Publishing Group)
    Highly diverse microbial assemblages colonize plant roots. It is still poorly understood whether different members of this root microbiome act synergistically by supplying different services (for example, different limiting nutrients) to plants and plant communities. In order to test this, we manipulated the presence of two widespread plant root symbionts, arbuscular mycorrhizal fungi and nitrogen-fixing rhizobia bacteria in model grassland communities established in axenic microcosms. Here, we demonstrate that both symbionts complement each other, resulting in increased plant diversity, enhanced seedling recruitment and improved nutrient acquisition compared with a single symbiont situation. Legume seedlings obtained up to 15-fold higher productivity if they formed an assocn. with both symbionts, opposed to productivity they reached with only one symbiont. Our results reveal the importance of functional diversity of symbionts and demonstrate that different members of the root microbiome can complement each other in acquiring different limiting nutrients and in driving important ecosystem functions.
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    Mycorrhizas and soil structure
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    New Phytologist (2006), 171 (1), 41-53CODEN: NEPHAV; ISSN:0028-646X. (Blackwell Publishing Ltd.)
    A review. In addn. to their well recognized roles in plant nutrition and communities, mycorrhizas can influence the key ecosystem process of soil aggregation. Here, the authors review the contribution of mycorrhizas, mostly focused on arbuscular mycorrhizal fungi (AMF), to soil structure at various hierarchical levels: plant community; individual root; and the soil mycelium. There are a suite of mechanisms by which mycorrhizal fungi can influence soil aggregation at each of these various scales. By extension of these mechanisms to the question of fungal diversity, it is recognized that different species or communities of fungi can promote soil aggregation to different degrees. The authors argue that soil aggregation should be included in a more complete 'multifunctional' perspective of mycorrhizal ecol., and that in-depth understanding of mycorrhizas/soil process relationships will require analyses emphasizing feedbacks between soil structure and mycorrhizas, rather than a unidirectional approach simply addressing mycorrhizal effects on soils. They finish the discussion by highlighting new tools, developments and foci that will probably be crucial in further understanding mycorrhizal contributions to soil structure.
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    Banerjee, S.; Walder, F.; Buchi, L.; Meyer, M.; Held, A. Y.; Gattinger, A.; Keller, T.; Charles, R.; van der Heijden, M. G. A. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019, 13 (7), 1722– 1736,  DOI: 10.1038/s41396-019-0383-2
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    Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots
    Banerjee Samiran; Walder Florian; Meyer Marcel; Held Alain Y; Keller Thomas; van der Heijden Marcel G A; Buchi Lucie; Charles Raphael; Buchi Lucie; Gattinger Andreas; Gattinger Andreas; Keller Thomas; Charles Raphael; van der Heijden Marcel G A
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    Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till, and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harbored a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R(2) = 0.366; P < 0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH, and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.
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    Impact of pesticides on soil microbiological parameters and possible bioremediation strategies
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    Indian Journal of Microbiology (2008), 48 (1), 114-127CODEN: IJMBAC; ISSN:0046-8991. (Springer (India) Private Ltd.)
    A review. Intensive agriculture is spectacularly successful since last couple of decades due to the inputs viz; fertilizers and pesticides along with high yielding varieties. The mandate for agriculture development was to feed and adequate nutrition supply to the expanding population by side the agriculture would be entering to into new area of com. and export orientation. The attention of public health and proper utilization natural resources are also the main issues related with agriculture development. Concern for pesticide contamination in the environment in the current context of pesticide use has assumed great importance. The fate of the pesticides in the soil environment in respect of pest control efficacy, non-target organism exposure and offsite mobility has been given due consideration. Kinetics and pathways of degrdn. depend on abiotic and biotic factors which are specific to a particular pesticide and therefore find preference. Adverse effect of pesticidal chems. on soil microorganisms may affect soil fertility becomes a foreign chems. major issue. Soil microorganisms show an early warning about soil disturbances by foreign chems. than any other parameters. But the fate and behavior of these chems. in soil ecosystem is very important since they are degraded by various factors and have the potential to be in the soil, water etc. So it is indispensable to monitor the persistence, degrdn. of pesticides in soil and is also necessary to study the effect of pesticide on the soil quality or soil health by in depth studies on soil microbial activity. The removal of metabolites or degraded products should be removed from soil and it has now a day's primary concern to the environmentalist. Toxicity or the contamination of pesticides can be reduced by the bioremediation process which involves the uses of microbes or plants. Either they degrade or use the pesticides by various co metabolic processes.
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    Microbial response to exudates in the rhizosphere of young beech trees (Fagus sylvatica L.) after dormancy
    Esperschuetz, J.; Buegger, F.; Winkler, J. B.; Munch, J. C.; Schloter, M.; Gattinger, A.
    Soil Biology & Biochemistry (2009), 41 (9), 1976-1985CODEN: SBIOAH; ISSN:0038-0717. (Elsevier B.V.)
    Plants act as an important link between atm. and soil: CO2 is transformed into carbohydrates by photosynthesis. These assimilates are distributed within the plant and translocated via roots into the rhizosphere and soil microorganisms. In this study, 3 yr old European beech trees (Fagus sylvatica L.) were exposed after the chilling period to an enriched 13C-CO2 atmosphere (δ13C = 60‰ - 80‰) at the time point when leaves development started. Temporal dynamics of assimilated carbon distribution in different plant parts, as well as into dissolved org. carbon and microbial communities in the rhizosphere and bulk soil have been investigated for a 20 days period. Photosynthetically fixed carbon could be traced into plant tissue, dissolved org. carbon and total microbial biomass, where it was utilized by different microbial communities. Due to carbon allocation into the rhizosphere, nutrient stress decreased; exudates were preferentially used by Gram-neg. bacteria and (mycorrhizal) fungi, resulting in an enhanced growth. Other microorganisms, like Gram-pos. bacteria and mainly micro eukaryotes benefited from the exudates via food web development. Overall our results indicate a fast turnover of exudates and the development of initial food web structures. Addnl. a transport of assimilated carbon into bulk soil by (mycrorhizal) fungi was obsd.
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    Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids
    Olsson, P. A.; Francis, R.; Read, D. J.; Soderstrom, B.
    Plant and Soil (1998), 201 (1), 9-16CODEN: PLSOA2; ISSN:0032-079X. (Kluwer Academic Publishers)
    Fatty acid anal. was used for detg. the extent of the development of the external mycelium of AM fungi (mixed inoculum from a sand dune) growing from roots of Festuca rubra and Plantago lanceolata in calcareous dune sand. The plants were raised in chambers specially designed to permit the growth of AM mycelium in root-free compartments. In two sep. expts., growth of external mycelium in the root-free compartments was detected and the amt. of mycelium was estd. using the indicator of AM fungal biomass, phospholipid fatty acid (PLFA) 16:1ω5. The results showed that the PLFA 16:1ω5 was suitable for estg. the mycelium emerging from the mixed inoculum obtained from the field roots of E rubra and P lanceolata. The PLFA 16:1ω5 showed external mycelium to become established in the root-free compartments within a period of 3 wk and the amt. of mycelium to continue to increase at 6 and 9 wk. Increases in neutral lipid fatty acid (NLFA) 16:1ω5 (indicator of storage lipids) over time were inconsistent between the two expts., but appeared to follow patterns of sporulation in each expt. In both expts., the root-free compartment was colonized by saprophytic fungi to a greater extent in the case of non-mycorrhizal than of AM treatment, as indicated by an increase in PLFA 18:2ω6,9 (indicator of saprophytic fungi). The absence of an increase in the case of AM treatment indicates that AM fungal mycelium can neg. affect the growth of saprophytic fungi in this soil type. This result was, however, only weakly supported by measurements of ergosterol content. The anal. of bacteria specific PLFAs showed that bacterial biomass was not affected by the AM mycelium.
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    Soil Biology & Biochemistry (1987), 19 (6), 703-7CODEN: SBIOAH; ISSN:0038-0717.
    The effects of fumigation on org. C extractable by 0.5M K2SO4 were examd. in a contrasting range of soils. Ec (the difference between org. C extd. by 0.5M K2SO4 from fumigated and non-fumigated soil) was about 70% of Fc (the flush of CO2-C caused by fumigation during a 10 day incubation), meaned for 10 soils. There was a close relationship between microbial biomass C, measured by fumigation-incubation (from the relationship biomass-C = Fc/0.45) and Ec, given by the equation: biomass-C = (2.64 ± 0.060) Ec that accounted for 99.2% of the variance in the data. This relationship held over a wide range of soil pH (3.9-8.0). ATP and microbial biomass N concns. were measured in 4 of the soils. The (ATP)/(Ec) ratios were very similar in the 4 soils, suggesting that both ATP and the org. C rendered decomposable by CHCl3 came from the soil microbial biomass. The C:N ratio of the biomass in a strongly acid (pH 4.2) soil was greater (9.4) than in the three less-acid soils (mean C:N ratio 5.1). It is proposed that the org. C rendered extractable to 0.5M K2SO4 after a 24 h CHCl3-fumigation (Ec) comes from the cells of the microbial biomass and can be used to est. soil microbial biomass C in both neutral and acid soils.
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    The fumigation-extn. method was used to investigate the relationship between microbial biomass C and biomass ninhydrin-reactive N (Enin) in a group of 110 soils. This large soil group was used to assess the effects of soil conditions (pH, cation exchange capacity, K2SO4 extractable C, soil org. C and biomass NH4+) or the form of land use (arable, grassland and forest soils) on the relationship between biomass C and Enin and the biomass C-to-Enin ratio. The Enin contents ranged from 1.8 to 139.2 μg N g-1 soil and were significantly correlated with biomass C (r = 0.94). This relationship was affected mainly by the pH but also by the formation of biomass NH4+. In acid soils only small amts. of biomass N were converted to NH4+. The form of land use had no effect on the relationship between biomass C and Enin if the differences in pH were considered. No uniform conversion factor can be proposed for the estn. of microbial biomass C by measuring Enin. Different factors are proposed for two groups differentiated according to the pH: soils pH > 5.0: biomass C = 22.0 × Enin; soils pH < 5.0: biomass C = 35.3 × Enin. For a more precise quantification of the microbial biomass by measuring the Enin content, it would be necessary to det. the specific biomass C-to-Enin ratio for each soil before commencement of an expt.
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    A review. Pesticides are indispensable in modern agricultural prodn.; however, their off-site migration and detrimental effects on surface water and groundwater quality cause concern. Current pesticide usage and trend data show pesticide use is widespread in New Zealand. According to national surveys, concns. of most pesticides in groundwater are usually low, and their occurrence has been attributed to non-point sources of contamination. Although it is well established that the environmental fate of pesticides is governed by complex interactions of many processes such as sorption, degrdn., and transport, our understanding of these basic mechanisms in the vadoze zone is too far from complete to predict quant. the fate of trace residues of pesticides in various soil types within one geog. location. This is mainly due to the vexing issue of the complex nature of soil and its lateral heterogeneity, such as spatial and temporal variability in field-scale. The use of simulation models to predict the environmental fate of pesticides using lab.- and field-derived parameters is discussed. The objective of this overview is to present past and recent environmental fate work on pesticides carried out under New Zealand conditions, to provide a wider perspective on the subject matter, and to give some recommendations for future research directions.
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    Organochlorine pesticides (OCP) are still found in food and feed crops although they were applied about 40 years ago. There is a considerable knowledge gap concerning the extent of soil and crop contamination by OCP. We performed two surveys in 2002 and 2005 to assess the loads of OCP in 41 Swiss horticultural fields under org. and conventional prodn. and corresponding Cucurbitaceae fruits (cucumbers, zucchini, and pumpkin), whereas these fields stay for intensive agricultural prodn. in Europe. In addn., soil org. carbon, texture, and pH were measured also. OCP were detected in 27 out of 41 fields (65.9%). The farming practice had no influence on the contamination or level of OCP in soil. The sum of OCP-loads per field ranged from <0.01 to 1.3 mg kg-1 dry soil and pentachloroaniline (PCA, 2.1 mg kg-1), p,p'-DDT (0.5 mg kg-1), and p,p'-DDE and dieldrin (0.4 mg kg-1) were the most detected pesticides over all investigated soils. PCA (up to 0.02 mg kg-1), dieldrin (up to 0.04 mg kg-1), α-chlordane and cis-heptachloroepoxide (<0.01 mg kg-1) were detected in five cucumber samples out of 41 Cucurbitaceae samples. Statistical anal. revealed no significant influence of the measured soil properties on the OCP-load of soils and cucumbers, although there is evidence that the bioavailability of OCP in soils to Cucurbitaceae plants was influenced by the sorption of the compds. to soil org. matter and by the polarity of the pesticide mols. It is suggested, that OCP contamination is widespread in all European regions with intensive plant prodn. and assocd. pesticide use, and deserves more attention with respect to save food prodn.
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    Scherr, K. E.; Bielská, L.; Kosubová, P.; Dinisová, P.; Hvězdová, M.; Šimek, Z.; Hofman, J. Occurrence of Chlorotriazine herbicides and their transformation products in arable soils. Environ. Pollut. 2017, 222, 283– 293,  DOI: 10.1016/j.envpol.2016.12.043
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    Occurrence of Chlorotriazine herbicides and their transformation products in arable soils
    Scherr, Kerstin E.; Bielska, Lucie; Kosubova, Petra; Dinisova, Petra; Hvezdova, Martina; Simek, Zdenek; Hofman, Jakub
    Environmental Pollution (Oxford, United Kingdom) (2017), 222 (), 283-293CODEN: ENPOEK; ISSN:0269-7491. (Elsevier Ltd.)
    Chlorotriazine herbicides (CTs) are widely used pest control chems. In contrast to groundwater contamination, little attention has been given to the circumstances of residue formation of parent compds. and transformation products in soils. Seventy-five cultivated floodplain topsoils in the Czech Republic were sampled in early spring of 2015, corresponding to a min. of six months (current-use terbuthylazine, TBA) and a up to a decade (banned atrazine, AT and simazine, SIM) after the last herbicide application. Soil residues of parent compds. and nine transformation products were quantified via multiple residue anal. using liq. chromatog. - tandem mass spectrometry of acetonitrile partitioning exts. (QuEChERS). Using principal component anal. (PCA), their relation to soil chem., crops and environmental parameters was detd. Of the parent compds., only TBA was present in more than one sample. In contrast, at least one CT transformation product, particularly hydroxylated CTs, was detected in 89% of the sites, or 54% for banned triazines. Deethylated and bi-dealkylated SIM or AT residues were not detectable. PCA suggests the formation and/or retention of CT hydroxy-metabolite residues to be related to low soil pH, and a direct relation between TBA and soil org. carbon, and between deethyl-TBA and clay or Ca contents, resp., the latter pointing towards distinct sorption mechanisms. The low historic application of simazine contrasted by the high abundance of its residues, and the co-occurrence with AT residues suggests the post-ban application of AT and SIM banned triazines as a permitted impurity of TBA formulations as a recent, secondary source. The present data indicate that topsoils do not contain abundant extractable residues of banned parent chlorotriazines, and are thus likely not the current source for related ground- and surface water contamination. In contrast, topsoils might pose a long-term source of TBA and CT transformation products for ground and surface water contamination.
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    Bending, G. D.; Lincoln, S. D.; Sørensen, S. R.; Morgan, J. A. W.; Aamand, J.; Walker, A. In-field spatial variability in the degradation of the phenyl-urea herbicide isoproturon is the result of interactions between degradative Sphingomonas spp. and soil pH. Appl. Environ. Microbiol. 2003, 69 (2), 827– 834,  DOI: 10.1128/AEM.69.2.827-834.2003
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    In-field spatial variability in the degradation of the phenyl-urea herbicide isoproturon is the result of interactions between degradative Sphingomonas spp. and soil pH
    Bending, Gary D.; Lincoln, Suzanne D.; Sorensen, Sebastian R.; Morgan, J. Alun W.; Aamand, Jens; Walker, Allan
    Applied and Environmental Microbiology (2003), 69 (2), 827-834CODEN: AEMIDF; ISSN:0099-2240. (American Society for Microbiology)
    Substantial spatial variability in the degrdn. rate of the phenylurea herbicide isoproturon (IPU) [3-(4-isopropylphenyl)-1,1-dimethylurea] has been shown to occur within agricultural fields, with implications for the longevity of the compd. in the soil and its movement to ground- and surface water. The microbial mechanisms underlying such spatial variability in degrdn. rate were investigated at Deep Slade field in Warwickshire, United Kingdom. Most-probable-no. anal. showed that rapid degrdn. of IPU was assocd. with proliferation of IPU-degrading organisms. Slow degrdn. of IPU was linked to either a delay in the proliferation of IPU-degrading organisms or apparent cometabolic degrdn. Using enrichment techniques, an IPU-degrading bacterial culture (designated strain F35) was isolated from fast-degrading soil, and partial 16S rRNA sequencing placed it within the Sphingomonas group. Denaturing gradient gel electrophoresis (DGGE) of PCR-amplified bacterial community 16S rRNA revealed two bands that increased in intensity in soil during growth-linked metab. of IPU, and sequencing of the excised bands showed high sequence homol. to the Sphingomonas group. However, while F35 was not closely related to either DGGE band, one of the DGGE bands showed 100% partial 16S rRNA sequence homol. to an IPU-degrading Sphingomonas sp. (strain SRS2) isolated from Deep Slade field in an earlier study (Sorensen, S. R. et al., 2001). Expts. with strains SRS2 and F35 in soil and liq. culture showed that the isolates had a narrow pH optimum (7 to 7.5) for metab. of IPU. The pH requirements of IPU-degrading strains of Sphingomonas spp. could largely account for the spatial variation of IPU degrdn. rates across the field.
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    Houot, S.; Topp, E.; Yassir, A.; Soulas, G. Dependence of accelerated degradation of atrazine on soil pH in French and Canadian soils. Soil Biol. Biochem. 2000, 32 (5), 615– 625,  DOI: 10.1016/S0038-0717(99)00188-1
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    Dependence of accelerated degradation of atrazine on soil pH in French and Canadian soils
    Houot, Sabine; Topp, Edward; Yassir, Abdellah; Soulas, Guy
    Soil Biology & Biochemistry (2000), 32 (5), 615-625CODEN: SBIOAH; ISSN:0038-0717. (Elsevier Science Ltd.)
    A series of agricultural soils varying in their atrazine treatment history were sampled from 12 sites in France and two sites in Canada. The soils varied widely with respect to soil chem., phys. and microbiol. (total microbial biomass, kinetics of C and N mineralization) properties. Soils treated with as few as two successive atrazine field applications mineralized [U-ring-14C]atrazine significantly more rapidly in 35 d lab. incubations than did soils which had never received atrazine. Longer treatment history tended to favor more rapid mineralization in the so-called "adapted" soils. Up to 80% of the initially applied 14C-atrazine was mineralized at the end of the incubations in these adapted soils. Of the properties tested, soil pH was the most significantly related to atrazine mineralized. In soils with pH lower than 6.5, less than 25% of the initial 14C-atrazine was mineralized even after repeated application in field conditions. Atrazine retention in soil did not influence its mineralization rate. Both hydroxylated and dealkylated atrazine metabolites were detected, but no clear pattern of metabolite prodn. could be detd. Large amts. of bound residues were formed in soils that mineralized little atrazine.
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    Kah, M.; Beulke, S.; Brown, C. D. Factors Influencing Degradation of Pesticides in Soil. J. Agric. Food Chem. 2007, 55 (11), 4487– 4492,  DOI: 10.1021/jf0635356
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    Factors Influencing Degradation of Pesticides in Soil
    Kah, Melanie; Beulke, Sabine; Brown, Colin D.
    Journal of Agricultural and Food Chemistry (2007), 55 (11), 4487-4492CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    Degrdn. and sorption of six acidic pesticides (2,4-D, dicamba, fluroxypyr, fluazifop-p, metsulfuron-Me, and flupyrsulfuron-methyl) and four basic pesticides (metribuzin, terbutryn, pirimicarb, and fenpropimorph) were detd. in nine temperate soils. Results were submitted to statistical analyses against a wide range of soil and pesticide properties to (i) identify any commonalities in factors influencing rate of degrdn. and (ii) det. whether there was any link between sorption and degrdn. processes for the compds. and soils studied. There were some marked differences between the soils in their ability to degrade the different pesticides. The parameters selected to explain variations in degrdn. rates depended on the soil-pesticide combination. The lack of consistent behavior renders a global approach to prediction of degrdn. unrealistic. The soil org. carbon content generally had a pos. influence on degrdn. The relationship between pH and degrdn. rates depended on the dominant mode of degrdn. for each pesticide. There were pos. relationships between sorption and rate of degrdn. for metsulfuron-Me, pirimicarb, and all acidic pesticides considered together (all P < 0.001) and for dicamba and all bases considered together (P < 0.05). No relationship between these processes was obsd. for the remaining seven individual pesticides.
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    Van Aarle, I. M.; Olsson, P. A.; Söderström, B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol. 2002, 155 (1), 173– 182,  DOI: 10.1046/j.1469-8137.2002.00439.x
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    Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization
    van Aarle, Ingrid M.; Olsson, Pal Axel; Soderstrom, Bengt
    New Phytologist (2002), 155 (1), 173-182CODEN: NEPHAV; ISSN:0028-646X. (Blackwell Science Ltd.)
    To test the response of arbuscular mycorrhizal (AM) fungi to a difference in soil pH, the extraradical mycelium of Scutellospora calospora or Glomus intraradices, in assocn. with Plantago lanceolata, was exposed to two different pH treatments, while the root substrate pH was left unchanged. Seedlings of P. lanceolata, colonized by one or other of the fungal symbionts, and nonmycorrhizal controls, were grown in mesh bags placed in pots contg. pH-buffered sand (pH around 5 or 6). The systems were harvested at approx. 2-wk intervals between 20 and 80 d. Both fungi formed more extraradical mycelium at the higher pH. Glomus intraradices formed almost no detectable extraradical mycelium at lower pH. The extraradical mycelium of S. calospora had higher acid phosphatase activity than that of G. intraradices. Total AM root colonization decreased for both fungi at the higher pH, and high pH also reduced arbuscule and vesicle formation in G. intraradices. In conclusion, soil pH influences AM root colonization as well as the growth and phosphatase activities of extraradical mycelium, although the two fungi responded differently.
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    Camenzind, T.; Hempel, S.; Homeier, J.; Horn, S.; Velescu, A.; Wilcke, W.; Rillig, M. C. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biology 2014, 20 (12), 3646– 3659,  DOI: 10.1111/gcb.12618
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    Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest
    Camenzind Tessa; Hempel Stefan; Homeier Jurgen; Horn Sebastian; Velescu Andre; Wilcke Wolfgang; Rillig Matthias C
    Global change biology (2014), 20 (12), 3646-59 ISSN:.
    Increased nitrogen (N) depositions expected in the future endanger the diversity and stability of ecosystems primarily limited by N, but also often co-limited by other nutrients like phosphorus (P). In this context a nutrient manipulation experiment (NUMEX) was set up in a tropical montane rainforest in southern Ecuador, an area identified as biodiversity hotspot. We examined impacts of elevated N and P availability on arbuscular mycorrhizal fungi (AMF), a group of obligate biotrophic plant symbionts with an important role in soil nutrient cycles. We tested the hypothesis that increased nutrient availability will reduce AMF abundance, reduce species richness and shift the AMF community toward lineages previously shown to be favored by fertilized conditions. NUMEX was designed as a full factorial randomized block design. Soil cores were taken after 2 years of nutrient additions in plots located at 2000 m above sea level. Roots were extracted and intraradical AMF abundance determined microscopically; the AMF community was analyzed by 454-pyrosequencing targeting the large subunit rDNA. We identified 74 operational taxonomic units (OTUs) with a large proportion of Diversisporales. N additions provoked a significant decrease in intraradical abundance, whereas AMF richness was reduced significantly by N and P additions, with the strongest effect in the combined treatment (39% fewer OTUs), mainly influencing rare species. We identified a differential effect on phylogenetic groups, with Diversisporales richness mainly reduced by N additions in contrast to Glomerales highly significantly affected solely by P. Regarding AMF community structure, we observed a compositional shift when analyzing presence/absence data following P additions. In conclusion, N and P additions in this ecosystem affect AMF abundance, but especially AMF species richness; these changes might influence plant community composition and productivity and by that various ecosystem processes.
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    Hage-Ahmed, K.; Rosner, K.; Steinkellner, S. Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manage. Sci. 2019, 75 (3), 583– 590,  DOI: 10.1002/ps.5220
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    Arbuscular mycorrhizal fungi and their response to pesticides
    Hage-Ahmed, Karin; Rosner, Kathrin; Steinkellner, Siegrid
    Pest Management Science (2019), 75 (3), 583-590CODEN: PMSCFC; ISSN:1526-498X. (John Wiley & Sons Ltd.)
    Arbuscular mycorrhizal fungi (AMF) form symbioses with the majority of plant species and can provide multiple benefits to the host plant. In agro-ecosystems, the abundance and community structure of AMF are affected by agricultural management practices. This review describes and discusses current knowledge on the effects of inorg. and org. chem. pesticides on AMF in the conflicting area between agricultural use and environmental concerns. Variable effects have been reported following chem. pesticide use, ranging from neutral to pos. and neg. Moreover, a species-specific reaction has been documented. The reported effects of pesticides on arbuscular mycorrhizal symbiosis are very diverse, and even when the same substance is investigated, the results are often contradictory. These effects depend on many parameters, such as the active substance, the mode of action, the mode of application and the dosage. In the field, determinants such as the physico-chem. behavior of the active substances, the soil type and other soil microorganisms contribute to the fate of pesticides and thus the amt. of active substances to which AMF are exposed. This review highlights that the fate of AMF following pesticide use needs to be addressed in a broader agro-ecosystem context. © 2018 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chem. Industry.
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    Rillig, M. C.; Ryo, M.; Lehmann, A.; Aguilar-Trigueros, C. A.; Buchert, S.; Wulf, A.; Iwasaki, A.; Roy, J.; Yang, G. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 2019, 366 (6467), 886– 890,  DOI: 10.1126/science.aay2832
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    The role of multiple global change factors in driving soil functions and microbial biodiversity
    Rillig, Matthias C.; Ryo, Masahiro; Lehmann, Anika; Aguilar-Trigueros, Carlos A.; Buchert, Sabine; Wulf, Anja; Iwasaki, Aiko; Roy, Julien; Yang, Gaowen
    Science (Washington, DC, United States) (2019), 366 (6467), 886-890CODEN: SCIEAS; ISSN:1095-9203. (American Association for the Advancement of Science)
    Soils underpin terrestrial ecosystem functions, but they face numerous anthropogenic pressures. Despite their crucial ecol. role, we know little about how soils react to more than two environmental factors at a time. Here, we show exptl. that increasing the no. of simultaneous global change factors (up to 10) caused increasing directional changes in soil properties, soil processes, and microbial communities, though there was greater uncertainty in predicting the magnitude of change. Our study provides a blueprint for addressing multifactor change with an efficient, broadly applicable exptl. design for studying the impacts of global environmental change.
    >> More from SciFinder ®
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  • Abstract

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    Figure 1

    Figure 1. (A) Number of pesticide residues in arable and vegetable fields under conventional management with tillage, conventional management without tillage, or organic management. For each management system 20 fields were analyzed. (B) Sum of the concentrations of pesticides in arable and vegetable fields under conventional, conventional without tillage, or organic management.

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    Figure 2

    Figure 2. Abundance of 46 pesticides and transformation products (indicated with an asterisk) in the arable and vegetable fields under conventional, no-till, and organic management. Each row represents a pesticide, and each column, one field. The method limits of quantification (MLOQ) ranged between 0.064 μg/kg and 36 μg/kg depending on the substance (SI, Table S8). The color range represents the level of the detected concentrations, whereas empty (white) cells indicate no detects (<MLOQ). The bars on the right show the frequency of occurrence of a specific compound across all samples.

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    Figure 3

    Figure 3. Decrease of the number of pesticide residues in soils, including both arable and vegetable farms, with the duration of organic management. The duration of organic management is expressed as the number of years since the conversion from conventional to organic. The sites were grouped in five-year time intervals.

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    Figure 4

    Figure 4. (A and B) Relative importance of various variables, which explained microbial biomass (A) and AMF root colonization (B) in arable farming using multimodel inference. The bars represent the importance of predictors (see methods for details on individual variables). The colors of the bars indicate the model’s average estimate, where blue implies positive and red negative values. Management (gray bar as this is a categorical variable) is also included in the figure regardless of its rank as a predictor. Asterisks indicate the statistical significance of the variables (*P < 0.05; **P < 0.01; ***P < 0.001). (C) Univariate relationship of microbial biomass C and numbers of pesticide residues corrected for pH, Corg, and sampling area (see methods: Statistical analyses). The colors represent the management systems (dark blue = conventional, light blue = conventional without tillage, green = organic); the solid line indicates the regression line, and the dotted line, the 95% confidence interval. (D) Univariate relationship of AMF and number of pesticide residues corrected for pH, Corg, and sampling area. The relationships between AMF colonization and the number of pesticide residues was also significant without correcting for pH, Corg, and sampling area (SI, Figure S5).

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  • References

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      Combined pesticide exposure severely affects individual- and colony-level traits in bees
      Gill, Richard J.; Ramos-Rodriguez, Oscar; Raine, Nigel E.
      Nature (London, United Kingdom) (2012), 491 (7422), 105-108CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)
      Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural prodn. Bees contribute approx. 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations. Recent studies have implicated the role of pesticides in these declines, as exposure to these chems. has been assocd. with changes in bee behavior and redns. in colony queen prodn. However, the key link between changes in individual behavior and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concns. can have subtle or sublethal effects at the individual level, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging, yet the possible combinatorial effects of pesticide exposure have rarely been investigated. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concns. that could approx. field-level exposure impairs natural foraging behavior and increases worker mortality leading to significant redns. in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with obsd. knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.
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      Mitchell, E. A.; Mulhauser, B.; Mulot, M.; Mutabazi, A.; Glauser, G.; Aebi, A. A worldwide survey of neonicotinoids in honey. Science 2017, 358 (6359), 109– 111,  DOI: 10.1126/science.aan3684
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      A worldwide survey of neonicotinoids in honey
      Mitchell, E. A. D.; Mulhauser, B.; Mulot, M.; Mutabazi, A.; Glauser, G.; Aebi, A.
      Science (Washington, DC, United States) (2017), 358 (6359), 109-111CODEN: SCIEAS; ISSN:0036-8075. (American Association for the Advancement of Science)
      Growing evidence for global pollinator decline is causing concern for biodiversity conservation and ecosystem services maintenance. Neonicotinoid pesticides have been identified or suspected as a key factor responsible for this decline. We assessed the global exposure of pollinators to neonicotinoids by analyzing 198 honey samples from across the world. We found at least one of five tested compds. (acetamiprid, clothianidin, imidacloprid, thiacloprid, and thiamethoxam) in 75% of all samples, 45% of samples contained two or more of these compds., and 10% contained four or five. Our results confirm the exposure of bees to neonicotinoids in their food throughout the world. The coexistence of neonicotinoids and other pesticides may increase harm to pollinators. However, the concns. detected are below the max. residue level authorized for human consumption (av. ± std. error for pos. samples: 1.8±0.56 ng per g).
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      Bünemann, E. K.; Schwenke, G.; Van Zwieten, L. Impact of agricultural inputs on soil organisms—a review. Soil Research 2006, 44 (4), 379– 406,  DOI: 10.1071/SR05125
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      Pelosi, C.; Barot, S.; Capowiez, Y.; Hedde, M.; Vandenbulcke, F. Pesticides and earthworms. A review. Agron. Sustainable Dev. 2014, 34 (1), 199– 228,  DOI: 10.1007/s13593-013-0151-z
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      Pesticides and earthworms. A review
      Pelosi, Celine; Barot, Sebastien; Capowiez, Yvan; Hedde, Mickael; Vandenbulcke, Franck
      Agronomy for Sustainable Development (2014), 34 (1), 199-228CODEN: ASDGAP; ISSN:1773-0155. (Springer France)
      A review. Earthworms provide key soil functions that favor many pos. ecosystem services. These services are important for agroecosystem sustainability but can be degraded by intensive cultural practices such as use of pesticides. Many literature reports have investigated the effect of pesticides on earthworms. Here, we review those reports to assess the relevance of the indicators of earthworm response to pesticides, to assess their sensitivity to pesticides, and to highlight the remaining knowledge gaps. We focus on European earthworm species and products authorised in Europe, excluding natural compds. and metals. We consider different organization levels: the infra-individual level (gene expression and physiol.), the individual and population levels (life-history traits, population d. and behavior) and the community level: community biomass and d. Our anal. shows that earthworms are impacted by pesticides at all organization levels. For example, pesticides disrupt enzymic activities, increase individual mortality, decrease fecundity and growth, change individual behavior such as feeding rate and decrease the overall community biomass and d. Insecticides and fungicides are the most toxic pesticides impacting survival and reprodn., resp.
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      Karpouzas, D.; Papadopoulou, E.; Ipsilantis, I.; Friedel, I.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Kandeler, E.; Menkissoglu-Spiroudi, U.; Martin-Laurent, F. Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity. Ecol. Indic. 2014, 39, 44– 53,  DOI: 10.1016/j.ecolind.2013.12.004
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      Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity
      Karpouzas, D. G.; Papadopoulou, E.; Ipsilantis, I.; Friedel, I.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Kandeler, E.; Menkissoglu-Spiroudi, U.; Martin-Laurent, F.
      Ecological Indicators (2014), 39 (), 44-53CODEN: EICNBG; ISSN:1470-160X. (Elsevier Ltd.)
      The key role of arbuscular mycorrhizal (AM) fungi in maintaining soil fertility and ecosystem functioning and their general sensitivity to pesticides make them good candidate bioindicators in pesticide soil microbial toxicity assessment. We investigated the impact of the herbicide nicosulfuron on mycorrhizal colonization and community structure of AM fungi via a pot-to-field exptl. approach. This allowed the assessment of nicosulfuron toxicity (i) at extreme exposure schemes (pot expt., Tier I) invoked by the repeated application of a range of dose rates (x0, x10, x100, x1000 the recommended dose) and (ii) under realistic exposure scenarios (x0, x1, x2, x5 the recommended dose) in the field (Tier II). In the pot expt., the x100 and x1000 dose rates significantly reduced plant biomass, mycorrhizal colonization and AM fungal richness as detd. by DGGE. This coincided with the progressive accumulation of herbicide concns. in soil. In contrast, no effects on AM fungi were obsd. at the nicosulfuron dose rates tested in the field. Clone libraries showed that the majority of AM fungi belonged to the Glomus group and were sensitive to the high levels of nicosulfuron accumulated in soil at the latter culture cycles. In contrast, a Paraglomeraceae and a Glomus etunicatum ribotype were present in maize roots in all cycles and dose rates implying a tolerance to nicosulfuron-induced stress. Overall, the deleterious effects of nicosulfuron on AM fungi induced by the highest dose rates in the pot expt. could be attributed either to fungal-driven toxicity or to plant-driven effects which have subsequent implications for mycorrhizal symbiosis. Thus, tiered pot-to-field exptl. approach followed in our study combined with classic and standardized mol. tools could provide a realistic assessment of the toxicity of pesticides onto AM fungi as potential bioindicators.
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      Wagg, C.; Schlaeppi, K.; Banerjee, S.; Kuramae, E. E.; van der Heijden, M. G. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat. Commun. 2019, 10 (1), 1– 10,  DOI: 10.1038/s41467-019-12798-y
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      Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning
      Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran; Kuramae, Eiko E.; van der Heijden, Marcel G. A.
      Nature Communications (2019), 10 (1), 1-10CODEN: NCAOBW; ISSN:2041-1723. (Nature Research)
      The soil microbiome is highly diverse and comprises up to one quarter of Earth's diversity. Yet, how such a diverse and functionally complex microbiome influences ecosystem functioning remains unclear. Here we manipulated the soil microbiome in exptl. grassland ecosystems and obsd. that microbiome diversity and microbial network complexity pos. influenced multiple ecosystem functions related to nutrient cycling (e.g. multifunctionality). Grassland microcosms with poorly developed microbial networks and reduced microbial richness had the lowest multifunctionality due to fewer taxa present that support the same function (redundancy) and lower diversity of taxa that support different functions (reduced functional uniqueness). Moreover, different microbial taxa explained different ecosystem functions pointing to the significance of functional diversity in microbial communities. These findings indicate the importance of microbial interactions within and among fungal and bacterial communities for enhancing ecosystem performance and demonstrate that the extinction of complex ecol. assocns. belowground can impair ecosystem functioning.
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    20. 20
      Delgado-Baquerizo, M.; Maestre, F. T.; Reich, P. B.; Jeffries, T. C.; Gaitan, J. J.; Encinar, D.; Berdugo, M.; Campbell, C. D.; Singh, B. K. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 2016, 7, 10541,  DOI: 10.1038/ncomms10541
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      Microbial diversity drives multifunctionality in terrestrial ecosystems
      Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B.; Jeffries, Thomas C.; Gaitan, Juan J.; Encinar, Daniel; Berdugo, Miguel; Campbell, Colin D.; Singh, Brajesh K.
      Nature Communications (2016), 7 (), 10541CODEN: NCAOBW; ISSN:2041-1723. (Nature Publishing Group)
      Despite the importance of microbial communities for ecosystem services and human welfare, the relationship between microbial diversity and multiple ecosystem functions and services (i.e., multifunctionality) at the global scale has yet to be evaluated. Here we use two independent, large-scale databases with contrasting geog. coverage (from 78 global drylands and from 179 locations across Scotland, resp.), and report that soil microbial diversity pos. relates to multifunctionality in terrestrial ecosystems. The direct pos. effects of microbial diversity were maintained even when accounting simultaneously for multiple multifunctionality drivers (climate, soil abiotic factors and spatial predictors). Our findings provide empirical evidence that any loss in microbial diversity will likely reduce multifunctionality, neg. impacting the provision of services such as climate regulation, soil fertility and food and fiber prodn. by terrestrial ecosystems.
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      Karpouzas, D.; Kandeler, E.; Bru, D.; Friedel, I.; Auer, Y.; Kramer, S.; Vasileiadis, S.; Petric, I.; Udikovic-Kolic, N.; Djuric, S. A tiered assessment approach based on standardized methods to estimate the impact of nicosulfuron on the abundance and function of the soil microbial community. Soil Biol. Biochem. 2014, 75, 282– 291,  DOI: 10.1016/j.soilbio.2014.04.022
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      A tiered assessment approach based on standardized methods to estimate the impact of nicosulfuron on the abundance and function of the soil microbial community
      Karpouzas, D. G.; Kandeler, E.; Bru, D.; Friedel, I.; Auer, Y.; Kramer, S.; Vasileiadis, S.; Petric, I.; Udikovic-Kolic, N.; Djuric, S.; Martin-Laurent, F.
      Soil Biology & Biochemistry (2014), 75 (), 282-291CODEN: SBIOAH; ISSN:0038-0717. (Elsevier B.V.)
      Pesticides impact soil microorganisms in various ways. Despite the pivotal role of the latter in ecosystem functioning, the assessment of pesticides soil microbial toxicity is lagging behind the recent methodol. advances in microbial ecol. The authors investigated the impact of nicosulfuron, a low dose sulfonylurea herbicide, on the structure, abundance and function of the soil microbial community using standardized methodologies (PLFAs, taxa-specific qPCR and enzyme activities). For this purpose a Tiered approach involving assessment (i) at extreme, long term (five repeated application cycles) exposure schemes in a microcosm expt. conducted under greenhouse conditions (x0, x10, x100 and x1000 the recommended dose, Tier I) and (ii) at realistic field exposure scenarios (x0, x1, x2 and x5, Tier II) was followed. Significant redns. in the abundance of Gram neg. (β-proteobacteria, planctomycetes) and Gram pos. bacteria (actinobacteria) were indicated by both PLFA and qPCR analyses at low soil concns. of nicosulfuron (0.25-1 μg g-1), while a redn. of fungi at equally low levels of nicosulfuron in soil was found only by qPCR anal. C- and P-cycling enzymes were particularly sensitive even at low soil concn. of the herbicide (0-1 μg g-1). In contrast, no inhibitory effects of nicosufluron at field conditions were found. The only exception was cellobiohydrolase which were impaired at herbicide rates higher than the recommended. The authors suggest that the use of a tiered microcosm-to-field experimentation combined with the application of standardized methodologies could provide a comprehensive assessment of the soil microbial toxicity of pesticides.
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      Bünemann, E. K.; Bongiorno, G.; Bai, Z.; Creamer, R. E.; De Deyn, G.; de Goede, R.; Fleskens, L.; Geissen, V.; Kuyper, T. W.; Mäder, P. Soil quality-A critical review. Soil Biol. Biochem. 2018, 120, 105– 125,  DOI: 10.1016/j.soilbio.2018.01.030
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      Van Der Heijden, M. G.; De Bruin, S.; Luckerhoff, L.; Van Logtestijn, R. S.; Schlaeppi, K. A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J. 2016, 10 (2), 389– 399,  DOI: 10.1038/ismej.2015.120
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      A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment
      van der Heijden, Marcel G. A.; de Bruin, Susanne; Luckerhoff, Ludo; van Logtestijn, Richard S. P.; Schlaeppi, Klaus
      ISME Journal (2016), 10 (2), 389-399CODEN: IJSOCF; ISSN:1751-7362. (Nature Publishing Group)
      Highly diverse microbial assemblages colonize plant roots. It is still poorly understood whether different members of this root microbiome act synergistically by supplying different services (for example, different limiting nutrients) to plants and plant communities. In order to test this, we manipulated the presence of two widespread plant root symbionts, arbuscular mycorrhizal fungi and nitrogen-fixing rhizobia bacteria in model grassland communities established in axenic microcosms. Here, we demonstrate that both symbionts complement each other, resulting in increased plant diversity, enhanced seedling recruitment and improved nutrient acquisition compared with a single symbiont situation. Legume seedlings obtained up to 15-fold higher productivity if they formed an assocn. with both symbionts, opposed to productivity they reached with only one symbiont. Our results reveal the importance of functional diversity of symbionts and demonstrate that different members of the root microbiome can complement each other in acquiring different limiting nutrients and in driving important ecosystem functions.
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      Rillig, M. C.; Mummey, D. L. Mycorrhizas and soil structure. New Phytol. 2006, 171 (1), 41– 53,  DOI: 10.1111/j.1469-8137.2006.01750.x
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      Mycorrhizas and soil structure
      Rillig, Matthias C.; Mummey, Daniel L.
      New Phytologist (2006), 171 (1), 41-53CODEN: NEPHAV; ISSN:0028-646X. (Blackwell Publishing Ltd.)
      A review. In addn. to their well recognized roles in plant nutrition and communities, mycorrhizas can influence the key ecosystem process of soil aggregation. Here, the authors review the contribution of mycorrhizas, mostly focused on arbuscular mycorrhizal fungi (AMF), to soil structure at various hierarchical levels: plant community; individual root; and the soil mycelium. There are a suite of mechanisms by which mycorrhizal fungi can influence soil aggregation at each of these various scales. By extension of these mechanisms to the question of fungal diversity, it is recognized that different species or communities of fungi can promote soil aggregation to different degrees. The authors argue that soil aggregation should be included in a more complete 'multifunctional' perspective of mycorrhizal ecol., and that in-depth understanding of mycorrhizas/soil process relationships will require analyses emphasizing feedbacks between soil structure and mycorrhizas, rather than a unidirectional approach simply addressing mycorrhizal effects on soils. They finish the discussion by highlighting new tools, developments and foci that will probably be crucial in further understanding mycorrhizal contributions to soil structure.
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      Büchi, L.; Georges, F.; Walder, F.; Banerjee, S.; Keller, T.; Six, J.; van der Heijden, M. G. A.; Charles, R. Potential of indicators to unveil the hidden side of cropping system classification: Differences and similarities in cropping practices between conventional, no-till and organic systems. Eur. J. Agron. 2019, 109, 125920,  DOI: 10.1016/j.eja.2019.125920
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      Banerjee, S.; Walder, F.; Buchi, L.; Meyer, M.; Held, A. Y.; Gattinger, A.; Keller, T.; Charles, R.; van der Heijden, M. G. A. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019, 13 (7), 1722– 1736,  DOI: 10.1038/s41396-019-0383-2
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      Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots
      Banerjee Samiran; Walder Florian; Meyer Marcel; Held Alain Y; Keller Thomas; van der Heijden Marcel G A; Buchi Lucie; Charles Raphael; Buchi Lucie; Gattinger Andreas; Gattinger Andreas; Keller Thomas; Charles Raphael; van der Heijden Marcel G A
      The ISME journal (2019), 13 (7), 1722-1736 ISSN:.
      Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till, and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harbored a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R(2) = 0.366; P < 0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH, and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.
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      Chowdhury, A.; Pradhan, S.; Saha, M.; Sanyal, N. Impact of pesticides on soil microbiological parameters and possible bioremediation strategies. Indian J. Microbiol. 2008, 48 (1), 114– 27,  DOI: 10.1007/s12088-008-0011-8
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      Impact of pesticides on soil microbiological parameters and possible bioremediation strategies
      Chowdhury, Ashim; Pradhan, Saswati; Saha, Monidipta; Sanyal, Nilanjan
      Indian Journal of Microbiology (2008), 48 (1), 114-127CODEN: IJMBAC; ISSN:0046-8991. (Springer (India) Private Ltd.)
      A review. Intensive agriculture is spectacularly successful since last couple of decades due to the inputs viz; fertilizers and pesticides along with high yielding varieties. The mandate for agriculture development was to feed and adequate nutrition supply to the expanding population by side the agriculture would be entering to into new area of com. and export orientation. The attention of public health and proper utilization natural resources are also the main issues related with agriculture development. Concern for pesticide contamination in the environment in the current context of pesticide use has assumed great importance. The fate of the pesticides in the soil environment in respect of pest control efficacy, non-target organism exposure and offsite mobility has been given due consideration. Kinetics and pathways of degrdn. depend on abiotic and biotic factors which are specific to a particular pesticide and therefore find preference. Adverse effect of pesticidal chems. on soil microorganisms may affect soil fertility becomes a foreign chems. major issue. Soil microorganisms show an early warning about soil disturbances by foreign chems. than any other parameters. But the fate and behavior of these chems. in soil ecosystem is very important since they are degraded by various factors and have the potential to be in the soil, water etc. So it is indispensable to monitor the persistence, degrdn. of pesticides in soil and is also necessary to study the effect of pesticide on the soil quality or soil health by in depth studies on soil microbial activity. The removal of metabolites or degraded products should be removed from soil and it has now a day's primary concern to the environmentalist. Toxicity or the contamination of pesticides can be reduced by the bioremediation process which involves the uses of microbes or plants. Either they degrade or use the pesticides by various co metabolic processes.
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      Ruggirello, R. M.; Hermanson, M. H.; Isaksson, E.; Teixeira, C.; Forsström, S.; Muir, D. C. G.; Pohjola, V.; Van De Wal, R.; Meijer, H. A. J. Current use and legacy pesticide deposition to ice caps on Svalbard, Norway. J. Geophys. Res. 2010, 115, D18,  DOI: 10.1029/2010JD014005
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      Microbial response to exudates in the rhizosphere of young beech trees (Fagus sylvatica L.) after dormancy
      Esperschuetz, J.; Buegger, F.; Winkler, J. B.; Munch, J. C.; Schloter, M.; Gattinger, A.
      Soil Biology & Biochemistry (2009), 41 (9), 1976-1985CODEN: SBIOAH; ISSN:0038-0717. (Elsevier B.V.)
      Plants act as an important link between atm. and soil: CO2 is transformed into carbohydrates by photosynthesis. These assimilates are distributed within the plant and translocated via roots into the rhizosphere and soil microorganisms. In this study, 3 yr old European beech trees (Fagus sylvatica L.) were exposed after the chilling period to an enriched 13C-CO2 atmosphere (δ13C = 60‰ - 80‰) at the time point when leaves development started. Temporal dynamics of assimilated carbon distribution in different plant parts, as well as into dissolved org. carbon and microbial communities in the rhizosphere and bulk soil have been investigated for a 20 days period. Photosynthetically fixed carbon could be traced into plant tissue, dissolved org. carbon and total microbial biomass, where it was utilized by different microbial communities. Due to carbon allocation into the rhizosphere, nutrient stress decreased; exudates were preferentially used by Gram-neg. bacteria and (mycorrhizal) fungi, resulting in an enhanced growth. Other microorganisms, like Gram-pos. bacteria and mainly micro eukaryotes benefited from the exudates via food web development. Overall our results indicate a fast turnover of exudates and the development of initial food web structures. Addnl. a transport of assimilated carbon into bulk soil by (mycrorhizal) fungi was obsd.
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      Olsson, P.; Francis, R.; Read, D.; Söderström, B. Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids. Plant Soil 1998, 201 (1), 9– 16,  DOI: 10.1023/A:1004379404220
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      Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids
      Olsson, P. A.; Francis, R.; Read, D. J.; Soderstrom, B.
      Plant and Soil (1998), 201 (1), 9-16CODEN: PLSOA2; ISSN:0032-079X. (Kluwer Academic Publishers)
      Fatty acid anal. was used for detg. the extent of the development of the external mycelium of AM fungi (mixed inoculum from a sand dune) growing from roots of Festuca rubra and Plantago lanceolata in calcareous dune sand. The plants were raised in chambers specially designed to permit the growth of AM mycelium in root-free compartments. In two sep. expts., growth of external mycelium in the root-free compartments was detected and the amt. of mycelium was estd. using the indicator of AM fungal biomass, phospholipid fatty acid (PLFA) 16:1ω5. The results showed that the PLFA 16:1ω5 was suitable for estg. the mycelium emerging from the mixed inoculum obtained from the field roots of E rubra and P lanceolata. The PLFA 16:1ω5 showed external mycelium to become established in the root-free compartments within a period of 3 wk and the amt. of mycelium to continue to increase at 6 and 9 wk. Increases in neutral lipid fatty acid (NLFA) 16:1ω5 (indicator of storage lipids) over time were inconsistent between the two expts., but appeared to follow patterns of sporulation in each expt. In both expts., the root-free compartment was colonized by saprophytic fungi to a greater extent in the case of non-mycorrhizal than of AM treatment, as indicated by an increase in PLFA 18:2ω6,9 (indicator of saprophytic fungi). The absence of an increase in the case of AM treatment indicates that AM fungal mycelium can neg. affect the growth of saprophytic fungi in this soil type. This result was, however, only weakly supported by measurements of ergosterol content. The anal. of bacteria specific PLFAs showed that bacterial biomass was not affected by the AM mycelium.
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      An extraction method for measuring soil microbial biomass C
      Vance, E. D.; Brookes, P. C.; Jenkinson, D. S.
      Soil Biology & Biochemistry (1987), 19 (6), 703-7CODEN: SBIOAH; ISSN:0038-0717.
      The effects of fumigation on org. C extractable by 0.5M K2SO4 were examd. in a contrasting range of soils. Ec (the difference between org. C extd. by 0.5M K2SO4 from fumigated and non-fumigated soil) was about 70% of Fc (the flush of CO2-C caused by fumigation during a 10 day incubation), meaned for 10 soils. There was a close relationship between microbial biomass C, measured by fumigation-incubation (from the relationship biomass-C = Fc/0.45) and Ec, given by the equation: biomass-C = (2.64 ± 0.060) Ec that accounted for 99.2% of the variance in the data. This relationship held over a wide range of soil pH (3.9-8.0). ATP and microbial biomass N concns. were measured in 4 of the soils. The (ATP)/(Ec) ratios were very similar in the 4 soils, suggesting that both ATP and the org. C rendered decomposable by CHCl3 came from the soil microbial biomass. The C:N ratio of the biomass in a strongly acid (pH 4.2) soil was greater (9.4) than in the three less-acid soils (mean C:N ratio 5.1). It is proposed that the org. C rendered extractable to 0.5M K2SO4 after a 24 h CHCl3-fumigation (Ec) comes from the cells of the microbial biomass and can be used to est. soil microbial biomass C in both neutral and acid soils.
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      Joergensen, R. G. Quantification of the microbial biomass by determining ninhydrin-reactive N. Soil Biol. Biochem. 1996, 28 (3), 301– 306,  DOI: 10.1016/0038-0717(95)00141-7
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      Quantification of the microbial biomass by determining ninhydrin-reactive N
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      The fumigation-extn. method was used to investigate the relationship between microbial biomass C and biomass ninhydrin-reactive N (Enin) in a group of 110 soils. This large soil group was used to assess the effects of soil conditions (pH, cation exchange capacity, K2SO4 extractable C, soil org. C and biomass NH4+) or the form of land use (arable, grassland and forest soils) on the relationship between biomass C and Enin and the biomass C-to-Enin ratio. The Enin contents ranged from 1.8 to 139.2 μg N g-1 soil and were significantly correlated with biomass C (r = 0.94). This relationship was affected mainly by the pH but also by the formation of biomass NH4+. In acid soils only small amts. of biomass N were converted to NH4+. The form of land use had no effect on the relationship between biomass C and Enin if the differences in pH were considered. No uniform conversion factor can be proposed for the estn. of microbial biomass C by measuring Enin. Different factors are proposed for two groups differentiated according to the pH: soils pH > 5.0: biomass C = 22.0 × Enin; soils pH < 5.0: biomass C = 35.3 × Enin. For a more precise quantification of the microbial biomass by measuring the Enin content, it would be necessary to det. the specific biomass C-to-Enin ratio for each soil before commencement of an expt.
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      The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEN value
      Joergensen, Rainer George; Mueller, Torsten
      Soil Biology & Biochemistry (1996), 28 (1), 33-7CODEN: SBIOAH; ISSN:0038-0717. (Elsevier)
      The kEN value (extractable part of microbial biomass N after fumigation) of the fumigation-extn. method was assessed using the C-to-N ratio of the org. matter which was rendered extractable by CHCl3 fumigation. The data for this calibration approach was obtained from 51 arable and 23 grassland soils. The second calibration approach was to compare the relationship between N rendered extractable by CHCl3 fumigation and the C-to-N ratio measured in the flush of the fumigation-incubation method by recalcg. data obtained from the literature. On the basis of these two approaches, we recommend using a kEN value of 0.54 as originally proposed by P. C. Brookers, et al. (1985).
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      A review. Pesticides are indispensable in modern agricultural prodn.; however, their off-site migration and detrimental effects on surface water and groundwater quality cause concern. Current pesticide usage and trend data show pesticide use is widespread in New Zealand. According to national surveys, concns. of most pesticides in groundwater are usually low, and their occurrence has been attributed to non-point sources of contamination. Although it is well established that the environmental fate of pesticides is governed by complex interactions of many processes such as sorption, degrdn., and transport, our understanding of these basic mechanisms in the vadoze zone is too far from complete to predict quant. the fate of trace residues of pesticides in various soil types within one geog. location. This is mainly due to the vexing issue of the complex nature of soil and its lateral heterogeneity, such as spatial and temporal variability in field-scale. The use of simulation models to predict the environmental fate of pesticides using lab.- and field-derived parameters is discussed. The objective of this overview is to present past and recent environmental fate work on pesticides carried out under New Zealand conditions, to provide a wider perspective on the subject matter, and to give some recommendations for future research directions.
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      Hilber, I.; Mäder, P.; Schulin, R.; Wyss, G. S. Survey of organochlorine pesticides in horticultural soils and there grown Cucurbitaceae. Chemosphere 2008, 73 (6), 954– 961,  DOI: 10.1016/j.chemosphere.2008.06.053
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      Chemosphere (2008), 73 (6), 954-961CODEN: CMSHAF; ISSN:0045-6535. (Elsevier Ltd.)
      Organochlorine pesticides (OCP) are still found in food and feed crops although they were applied about 40 years ago. There is a considerable knowledge gap concerning the extent of soil and crop contamination by OCP. We performed two surveys in 2002 and 2005 to assess the loads of OCP in 41 Swiss horticultural fields under org. and conventional prodn. and corresponding Cucurbitaceae fruits (cucumbers, zucchini, and pumpkin), whereas these fields stay for intensive agricultural prodn. in Europe. In addn., soil org. carbon, texture, and pH were measured also. OCP were detected in 27 out of 41 fields (65.9%). The farming practice had no influence on the contamination or level of OCP in soil. The sum of OCP-loads per field ranged from <0.01 to 1.3 mg kg-1 dry soil and pentachloroaniline (PCA, 2.1 mg kg-1), p,p'-DDT (0.5 mg kg-1), and p,p'-DDE and dieldrin (0.4 mg kg-1) were the most detected pesticides over all investigated soils. PCA (up to 0.02 mg kg-1), dieldrin (up to 0.04 mg kg-1), α-chlordane and cis-heptachloroepoxide (<0.01 mg kg-1) were detected in five cucumber samples out of 41 Cucurbitaceae samples. Statistical anal. revealed no significant influence of the measured soil properties on the OCP-load of soils and cucumbers, although there is evidence that the bioavailability of OCP in soils to Cucurbitaceae plants was influenced by the sorption of the compds. to soil org. matter and by the polarity of the pesticide mols. It is suggested, that OCP contamination is widespread in all European regions with intensive plant prodn. and assocd. pesticide use, and deserves more attention with respect to save food prodn.
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      Scherr, K. E.; Bielská, L.; Kosubová, P.; Dinisová, P.; Hvězdová, M.; Šimek, Z.; Hofman, J. Occurrence of Chlorotriazine herbicides and their transformation products in arable soils. Environ. Pollut. 2017, 222, 283– 293,  DOI: 10.1016/j.envpol.2016.12.043
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      Occurrence of Chlorotriazine herbicides and their transformation products in arable soils
      Scherr, Kerstin E.; Bielska, Lucie; Kosubova, Petra; Dinisova, Petra; Hvezdova, Martina; Simek, Zdenek; Hofman, Jakub
      Environmental Pollution (Oxford, United Kingdom) (2017), 222 (), 283-293CODEN: ENPOEK; ISSN:0269-7491. (Elsevier Ltd.)
      Chlorotriazine herbicides (CTs) are widely used pest control chems. In contrast to groundwater contamination, little attention has been given to the circumstances of residue formation of parent compds. and transformation products in soils. Seventy-five cultivated floodplain topsoils in the Czech Republic were sampled in early spring of 2015, corresponding to a min. of six months (current-use terbuthylazine, TBA) and a up to a decade (banned atrazine, AT and simazine, SIM) after the last herbicide application. Soil residues of parent compds. and nine transformation products were quantified via multiple residue anal. using liq. chromatog. - tandem mass spectrometry of acetonitrile partitioning exts. (QuEChERS). Using principal component anal. (PCA), their relation to soil chem., crops and environmental parameters was detd. Of the parent compds., only TBA was present in more than one sample. In contrast, at least one CT transformation product, particularly hydroxylated CTs, was detected in 89% of the sites, or 54% for banned triazines. Deethylated and bi-dealkylated SIM or AT residues were not detectable. PCA suggests the formation and/or retention of CT hydroxy-metabolite residues to be related to low soil pH, and a direct relation between TBA and soil org. carbon, and between deethyl-TBA and clay or Ca contents, resp., the latter pointing towards distinct sorption mechanisms. The low historic application of simazine contrasted by the high abundance of its residues, and the co-occurrence with AT residues suggests the post-ban application of AT and SIM banned triazines as a permitted impurity of TBA formulations as a recent, secondary source. The present data indicate that topsoils do not contain abundant extractable residues of banned parent chlorotriazines, and are thus likely not the current source for related ground- and surface water contamination. In contrast, topsoils might pose a long-term source of TBA and CT transformation products for ground and surface water contamination.
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      Bending, G. D.; Lincoln, S. D.; Sørensen, S. R.; Morgan, J. A. W.; Aamand, J.; Walker, A. In-field spatial variability in the degradation of the phenyl-urea herbicide isoproturon is the result of interactions between degradative Sphingomonas spp. and soil pH. Appl. Environ. Microbiol. 2003, 69 (2), 827– 834,  DOI: 10.1128/AEM.69.2.827-834.2003
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      In-field spatial variability in the degradation of the phenyl-urea herbicide isoproturon is the result of interactions between degradative Sphingomonas spp. and soil pH
      Bending, Gary D.; Lincoln, Suzanne D.; Sorensen, Sebastian R.; Morgan, J. Alun W.; Aamand, Jens; Walker, Allan
      Applied and Environmental Microbiology (2003), 69 (2), 827-834CODEN: AEMIDF; ISSN:0099-2240. (American Society for Microbiology)
      Substantial spatial variability in the degrdn. rate of the phenylurea herbicide isoproturon (IPU) [3-(4-isopropylphenyl)-1,1-dimethylurea] has been shown to occur within agricultural fields, with implications for the longevity of the compd. in the soil and its movement to ground- and surface water. The microbial mechanisms underlying such spatial variability in degrdn. rate were investigated at Deep Slade field in Warwickshire, United Kingdom. Most-probable-no. anal. showed that rapid degrdn. of IPU was assocd. with proliferation of IPU-degrading organisms. Slow degrdn. of IPU was linked to either a delay in the proliferation of IPU-degrading organisms or apparent cometabolic degrdn. Using enrichment techniques, an IPU-degrading bacterial culture (designated strain F35) was isolated from fast-degrading soil, and partial 16S rRNA sequencing placed it within the Sphingomonas group. Denaturing gradient gel electrophoresis (DGGE) of PCR-amplified bacterial community 16S rRNA revealed two bands that increased in intensity in soil during growth-linked metab. of IPU, and sequencing of the excised bands showed high sequence homol. to the Sphingomonas group. However, while F35 was not closely related to either DGGE band, one of the DGGE bands showed 100% partial 16S rRNA sequence homol. to an IPU-degrading Sphingomonas sp. (strain SRS2) isolated from Deep Slade field in an earlier study (Sorensen, S. R. et al., 2001). Expts. with strains SRS2 and F35 in soil and liq. culture showed that the isolates had a narrow pH optimum (7 to 7.5) for metab. of IPU. The pH requirements of IPU-degrading strains of Sphingomonas spp. could largely account for the spatial variation of IPU degrdn. rates across the field.
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      Houot, S.; Topp, E.; Yassir, A.; Soulas, G. Dependence of accelerated degradation of atrazine on soil pH in French and Canadian soils. Soil Biol. Biochem. 2000, 32 (5), 615– 625,  DOI: 10.1016/S0038-0717(99)00188-1
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      Dependence of accelerated degradation of atrazine on soil pH in French and Canadian soils
      Houot, Sabine; Topp, Edward; Yassir, Abdellah; Soulas, Guy
      Soil Biology & Biochemistry (2000), 32 (5), 615-625CODEN: SBIOAH; ISSN:0038-0717. (Elsevier Science Ltd.)
      A series of agricultural soils varying in their atrazine treatment history were sampled from 12 sites in France and two sites in Canada. The soils varied widely with respect to soil chem., phys. and microbiol. (total microbial biomass, kinetics of C and N mineralization) properties. Soils treated with as few as two successive atrazine field applications mineralized [U-ring-14C]atrazine significantly more rapidly in 35 d lab. incubations than did soils which had never received atrazine. Longer treatment history tended to favor more rapid mineralization in the so-called "adapted" soils. Up to 80% of the initially applied 14C-atrazine was mineralized at the end of the incubations in these adapted soils. Of the properties tested, soil pH was the most significantly related to atrazine mineralized. In soils with pH lower than 6.5, less than 25% of the initial 14C-atrazine was mineralized even after repeated application in field conditions. Atrazine retention in soil did not influence its mineralization rate. Both hydroxylated and dealkylated atrazine metabolites were detected, but no clear pattern of metabolite prodn. could be detd. Large amts. of bound residues were formed in soils that mineralized little atrazine.
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      Kah, M.; Beulke, S.; Brown, C. D. Factors Influencing Degradation of Pesticides in Soil. J. Agric. Food Chem. 2007, 55 (11), 4487– 4492,  DOI: 10.1021/jf0635356
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      Factors Influencing Degradation of Pesticides in Soil
      Kah, Melanie; Beulke, Sabine; Brown, Colin D.
      Journal of Agricultural and Food Chemistry (2007), 55 (11), 4487-4492CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      Degrdn. and sorption of six acidic pesticides (2,4-D, dicamba, fluroxypyr, fluazifop-p, metsulfuron-Me, and flupyrsulfuron-methyl) and four basic pesticides (metribuzin, terbutryn, pirimicarb, and fenpropimorph) were detd. in nine temperate soils. Results were submitted to statistical analyses against a wide range of soil and pesticide properties to (i) identify any commonalities in factors influencing rate of degrdn. and (ii) det. whether there was any link between sorption and degrdn. processes for the compds. and soils studied. There were some marked differences between the soils in their ability to degrade the different pesticides. The parameters selected to explain variations in degrdn. rates depended on the soil-pesticide combination. The lack of consistent behavior renders a global approach to prediction of degrdn. unrealistic. The soil org. carbon content generally had a pos. influence on degrdn. The relationship between pH and degrdn. rates depended on the dominant mode of degrdn. for each pesticide. There were pos. relationships between sorption and rate of degrdn. for metsulfuron-Me, pirimicarb, and all acidic pesticides considered together (all P < 0.001) and for dicamba and all bases considered together (P < 0.05). No relationship between these processes was obsd. for the remaining seven individual pesticides.
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      Van Aarle, I. M.; Olsson, P. A.; Söderström, B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol. 2002, 155 (1), 173– 182,  DOI: 10.1046/j.1469-8137.2002.00439.x
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      Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization
      van Aarle, Ingrid M.; Olsson, Pal Axel; Soderstrom, Bengt
      New Phytologist (2002), 155 (1), 173-182CODEN: NEPHAV; ISSN:0028-646X. (Blackwell Science Ltd.)
      To test the response of arbuscular mycorrhizal (AM) fungi to a difference in soil pH, the extraradical mycelium of Scutellospora calospora or Glomus intraradices, in assocn. with Plantago lanceolata, was exposed to two different pH treatments, while the root substrate pH was left unchanged. Seedlings of P. lanceolata, colonized by one or other of the fungal symbionts, and nonmycorrhizal controls, were grown in mesh bags placed in pots contg. pH-buffered sand (pH around 5 or 6). The systems were harvested at approx. 2-wk intervals between 20 and 80 d. Both fungi formed more extraradical mycelium at the higher pH. Glomus intraradices formed almost no detectable extraradical mycelium at lower pH. The extraradical mycelium of S. calospora had higher acid phosphatase activity than that of G. intraradices. Total AM root colonization decreased for both fungi at the higher pH, and high pH also reduced arbuscule and vesicle formation in G. intraradices. In conclusion, soil pH influences AM root colonization as well as the growth and phosphatase activities of extraradical mycelium, although the two fungi responded differently.
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      Camenzind, T.; Hempel, S.; Homeier, J.; Horn, S.; Velescu, A.; Wilcke, W.; Rillig, M. C. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biology 2014, 20 (12), 3646– 3659,  DOI: 10.1111/gcb.12618
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      Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest
      Camenzind Tessa; Hempel Stefan; Homeier Jurgen; Horn Sebastian; Velescu Andre; Wilcke Wolfgang; Rillig Matthias C
      Global change biology (2014), 20 (12), 3646-59 ISSN:.
      Increased nitrogen (N) depositions expected in the future endanger the diversity and stability of ecosystems primarily limited by N, but also often co-limited by other nutrients like phosphorus (P). In this context a nutrient manipulation experiment (NUMEX) was set up in a tropical montane rainforest in southern Ecuador, an area identified as biodiversity hotspot. We examined impacts of elevated N and P availability on arbuscular mycorrhizal fungi (AMF), a group of obligate biotrophic plant symbionts with an important role in soil nutrient cycles. We tested the hypothesis that increased nutrient availability will reduce AMF abundance, reduce species richness and shift the AMF community toward lineages previously shown to be favored by fertilized conditions. NUMEX was designed as a full factorial randomized block design. Soil cores were taken after 2 years of nutrient additions in plots located at 2000 m above sea level. Roots were extracted and intraradical AMF abundance determined microscopically; the AMF community was analyzed by 454-pyrosequencing targeting the large subunit rDNA. We identified 74 operational taxonomic units (OTUs) with a large proportion of Diversisporales. N additions provoked a significant decrease in intraradical abundance, whereas AMF richness was reduced significantly by N and P additions, with the strongest effect in the combined treatment (39% fewer OTUs), mainly influencing rare species. We identified a differential effect on phylogenetic groups, with Diversisporales richness mainly reduced by N additions in contrast to Glomerales highly significantly affected solely by P. Regarding AMF community structure, we observed a compositional shift when analyzing presence/absence data following P additions. In conclusion, N and P additions in this ecosystem affect AMF abundance, but especially AMF species richness; these changes might influence plant community composition and productivity and by that various ecosystem processes.
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      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A280%3ADC%252BC2cnmsFaksw%253D%253D&md5=06061d0b22af98fc233d3ad41c458c45
    61. 61
      Hage-Ahmed, K.; Rosner, K.; Steinkellner, S. Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manage. Sci. 2019, 75 (3), 583– 590,  DOI: 10.1002/ps.5220
      [Crossref], [PubMed], [CAS], Google Scholar
      61
      Arbuscular mycorrhizal fungi and their response to pesticides
      Hage-Ahmed, Karin; Rosner, Kathrin; Steinkellner, Siegrid
      Pest Management Science (2019), 75 (3), 583-590CODEN: PMSCFC; ISSN:1526-498X. (John Wiley & Sons Ltd.)
      Arbuscular mycorrhizal fungi (AMF) form symbioses with the majority of plant species and can provide multiple benefits to the host plant. In agro-ecosystems, the abundance and community structure of AMF are affected by agricultural management practices. This review describes and discusses current knowledge on the effects of inorg. and org. chem. pesticides on AMF in the conflicting area between agricultural use and environmental concerns. Variable effects have been reported following chem. pesticide use, ranging from neutral to pos. and neg. Moreover, a species-specific reaction has been documented. The reported effects of pesticides on arbuscular mycorrhizal symbiosis are very diverse, and even when the same substance is investigated, the results are often contradictory. These effects depend on many parameters, such as the active substance, the mode of action, the mode of application and the dosage. In the field, determinants such as the physico-chem. behavior of the active substances, the soil type and other soil microorganisms contribute to the fate of pesticides and thus the amt. of active substances to which AMF are exposed. This review highlights that the fate of AMF following pesticide use needs to be addressed in a broader agro-ecosystem context. © 2018 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chem. Industry.
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    62. 62
      Rillig, M. C.; Ryo, M.; Lehmann, A.; Aguilar-Trigueros, C. A.; Buchert, S.; Wulf, A.; Iwasaki, A.; Roy, J.; Yang, G. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 2019, 366 (6467), 886– 890,  DOI: 10.1126/science.aay2832
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      62
      The role of multiple global change factors in driving soil functions and microbial biodiversity
      Rillig, Matthias C.; Ryo, Masahiro; Lehmann, Anika; Aguilar-Trigueros, Carlos A.; Buchert, Sabine; Wulf, Anja; Iwasaki, Aiko; Roy, Julien; Yang, Gaowen
      Science (Washington, DC, United States) (2019), 366 (6467), 886-890CODEN: SCIEAS; ISSN:1095-9203. (American Association for the Advancement of Science)
      Soils underpin terrestrial ecosystem functions, but they face numerous anthropogenic pressures. Despite their crucial ecol. role, we know little about how soils react to more than two environmental factors at a time. Here, we show exptl. that increasing the no. of simultaneous global change factors (up to 10) caused increasing directional changes in soil properties, soil processes, and microbial communities, though there was greater uncertainty in predicting the magnitude of change. Our study provides a blueprint for addressing multifactor change with an efficient, broadly applicable exptl. design for studying the impacts of global environmental change.
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  • Supporting Information

    Supporting Information

    ARTICLE SECTIONS
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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c06405.

    • 1.

      Relation between soil characteristics and the occurrence of pesticide residues

      2.

      Decrease of total pesticide concentration with duration of organic management

      3.

      Effects of pesticide residues on basal respiration and PLFA for AMF

      4.

      Results of the random forest analysis

      5.

      Uncorrected univariate relationships

      6.

      Pesticides and pesticide transformation products included in this study

      7.

      Soil characteristics of the selected fields and the test soils used for method validation

      8.

      Pesticide analysis in soils

      8.1.

      Chemicals and reagents

      8.2.

      Accelerated Solvent Extraction and further Sample Preparation

      8.3.

      High-performance Liquid Chromatography coupled to Triple Quadrupole Tandem Mass Spectrometry (HPLC-MS/MS)

      8.4.

      Quantification

      8.5.

      Method Validation

      9.

      Measured concentrations and method limits of quantification

      10.

      Supplementary References

      (PDF)


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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

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