Copper toxicity to earthworms: A comprehensive review and meta-analysis.

Copper can accumulate in agricultural topsoil through the use of Cu-based fungicides, which may harm soil organisms such as earthworms. This study aimed at reviewing the effects of copper on earthworms at different levels of biological organization, and to determine critical values of copper toxicity to earthworms using a meta-analysis and accounting for lethal and sub-lethal effects and different earthworm species and exposure conditions. Endpoints at the sub-individual level were more sensitive than at higher levels of organization. At the individual level, the most sensitive endpoints were reproduction and growth (hatching success, hatchling growth). Hormetic growth was clearly recognized at copper concentrations less than 80 mg kg−1 in dry soil. However, effects at the sub-individual level already occurred at lower concentrations. Considering all the exposure conditions, the calculated weighted means were 113 mg Cu kg−1 dry soil (95% CI -356; 582) for the LC50 (lethal concentration for 50% of the exposed individuals), 94.6 mg Cu kg−1 dry soil (95% CI 14.0; 175) for the EC50 reproduction, and 144 mg Cu kg−1 dry soil (95% CI -12.6; 301) for the EC50 growth or weight change. When accounting for the origin of the soil, earthworms were five times more sensitive to copper (LC50) in natural than in artificial soils. The different factors affecting Cu toxicity to earthworms explain the high variability of these values, making it difficult to derive thresholds. However, considering the potential negative effects of copper on earthworms, attention should be given to the more sustainable use of human-contributed copper in agricultural soils.