Earthworms Mitigate Pesticide Effects on Soil Microbial Activities

Abstract

Earthworms act synergistically with microorganisms in soils. They are ecosystem engineers involved in soil organic matter degradation and nutrient cycling, leading to the modulation of resource availability for all soil organisms. Using a soil microcosm approach, we aimed to assess the influence of the earthworm Aporrectodea caliginosa on the response of soil microbial activities against two fungicides, i.e., Cuprafor Micro^® (copper oxychloride, a metal) and Swing^® Gold (epoxiconazole and dimoxystrobin, synthetic organic compounds). The potential nitrification activity (PNA) and soil enzyme activities (glucosidase, phosphatase, arylamidase, and urease) involved in biogeochemical cycling were measured at the end of the incubation period, together with earthworm biomass. Two common indices of the soil biochemistry were used to aggregate the response of the soil microbial functioning: the geometric mean (Gmean) and the Soil Quality Index (SQI). At the end of the experiment, the earthworm biomass was not impacted by the fungicide treatments. Overall, in the earthworm-free soil microcosms, the two fungicides significantly increased several soil enzyme and nitrification activities, leading to a higher GMean index as compared to the non-treated control soils. The microbial activity responses depended on the type of activity (nitrification was the most sensitive one), on the fungicide (Swing^® Gold or Cuprafor Micro^®), and on the doses. The SQI indices revealed higher effects of both fungicides on the soil microbial activity in the absence of earthworms. The presence of earthworms enhanced all soil microbial activities in both the control and fungicide-contaminated soils. Moreover, the magnitude of the fungicide impact, integrated through the SQI index, was mitigated by the presence of earthworms, conferring a higher stability of microbial functional diversity. Our results highlight the importance of biotic interactions in the response of indicators of soil functioning (i.e., microbial activity) to pesticides.

Keywords: Lumbricidae; ecotoxicology; enzyme activity; fungicide; nitrification.

FIGURE 1

Box-plots of (A) the geometric mean (GMean index) and (B) the Mean values (n = 5, ±SD) of the Soil Quality Index (SQI) of microbial activities (β-D-glucosidase, phosphatase, urease and arylamidase, potential nitrification activity) in soils spiked with different Cuprafor Micro^® concentrations (3.33, 10, and 30 times the RD, corresponding to 25.8, 77.5, and 232.5 mg kg⁻¹ of copper, abbreviated Cu3.3, Cu10, and Cu30, respectively), and a control, in the presence or in the absence of earthworms. Different letters mean significant differences between treatments and the results of the two-way ANOVA test are presented as follows: “t” is for treatment effect, “E” for earthworm effect, and “(txE)” for their interaction. “ns” means no significant difference, ^∗p < 0.05 and ^∗∗∗p < 0.001.

FIGURE 2

Box-plots of (A) the geometric mean (GMean index) and (B) the Mean values (n = 5, ±SD) of the Soil Quality Index (SQI) of microbial activities (β-D-glucosidase, phosphatase, urease and arylamidase, potential nitrification activity) in soils spiked with different Swing^® Gold concentrations (0.33, 1, and 3 times the RD abbreviated SG0.33, SG1 and SG3, respectively) and a control soil, in the presence or in the absence of earthworms. Different letters mean significant differences between treatments, and the result of the two-way ANOVA test is presented as follows: “t” is for treatment effect, “E” for earthworm effect, and “(txE)” for their interaction. “ns” means no significant difference, ^∗p < 0.05 and ^∗∗∗p < 0.001.