Earthworms Mitigate Pesticide Effects on Soil Microbial Activities.

Sylvain Bart,Nathalie Cheviron,Virginie Grondin,Alexandre R R Péry,Christian Mougin,Alexandre Barraud,Céline Pelosi,Olivier Crouzet

doi:10.3389/fmicb.2019.01535

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.

Highlights

Earthworms and microorganisms represent the largest part of the living biomass in soils
An earthworm mortality rate of 5% was recorded in the Cu3.33 and the control treatments at the end of the experiment
There was no significant difference in earthworm mortality or weight along the experiment whatever the Cu fungicide concentration tested

Summary

Introduction

Earthworms and microorganisms represent the largest part of the living biomass in soils. Different earthworm species are known to increase soil microbial respiration (Scheu, 1987) or soil enzyme activities related to C, N, and P cycling (Tao et al, 2009; Dempsey et al, 2013), especially in the drilosphere (casts and burrow walls, Loquet et al, 1977; Aira et al, 2003). These works highlight significant effects of earthworms on the abundance of various microbial groups (i.e., ammonifiers, denitrifiers, and proteolytic bacteria). By ingesting microbial biomass, they can decrease the total microbial biomass while increasing the specific activities of its residual component (i.e., extra-cellular enzyme activities, Zhang et al, 2000; Aira et al, 2009)

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Conclusion