Abstract
Earthworms are pivotal in soil ecosystems due to their crucial role in shaping soil characteristics through casts and burrow walls. Previous research has predominantly focused on the direct impact of soil pollution on live earthworms, overlooking the subsequent effects on earthworm-mediated soil, such as casts and burrow walls. Using 2D-terraria as incubation containers and the geophagous earthworm species Metaphire guillelmi, this study assessed the change in various properties of earthworm-mediated soil in both uncontaminated soils and Cd- and Pye-contaminated soils. Overall, both Cd and Pye overall improved the ammonium nitrogen (NH4+-N), Olsen's phosphorus (Olsen-P) levels, and invertase and catalase activities while decreasing catalase activities in earthworm-mediated soil. They also fluctuating affected the pH, soil organic matter (SOM) content, soil urease, alkaline phosphatase activities, and microbial functional genes in the cast and burrow walls. These results indicated that earthworms remained crucial “ecosystem engineers” even in polluted soil. Additionally, differences were observed in the responses of properties between casts and burrow walls, showing unequal contributions of transit-through-gut and burrowing processes to soil modification. Specifically, transit-through-gut was found to have a more significant influence on soil NH4+-N and Olsen-P content compared to burrowing behavior. Regarding the pattern of microbial functional genes in earthworm-associated compartments, results revealed that they differed significantly in casts from those in bulk soil and burrow walls under unpolluted conditions, with pollution-enhancing disparities among compartments. Furthermore, NH4+-N and Olsen-P content, urease, and catalase activities in burrow walls and/or casts were identified as potential biomarkers for soil pollution, exhibiting a clear dose-effect relationship. Developing such biomarkers could address ethical concerns related to conventional earthworm biomarkers that require sacrificing earthworms. This study provides insights into the consequences of soil pollution on earthworm-mediated soil components, highlighting the importance of considering the indirect effects of contaminants on soil ecosystems.
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