Synthesis of earthworm trace metal uptake and bioaccumulation data: Role of soil concentration, earthworm ecophysiology, and experimental design. (July 2020)

• Record Type: Journal Article
• Authors: Richardson, J.B.; Görres, J.H.; Sizmur, Tom
• Is Part Of: Environmental pollution. Volume 262(2020)
• Publication Date: 2020-07
• Subjects: Bioconcentration -- Soil pollution -- Toxic metals -- Heavy metals -- Environmental toxicology; Pollution -- Periodicals; Pollution -- Environmental aspects -- Periodicals; Environmental Pollution -- Periodicals; Pollution -- Périodiques; Pollution -- Aspect de l'environnement -- Périodiques; Pollution -- Effets physiologiques -- Périodiques; Pollution; Pollution -- Environmental aspects; Periodicals; Electronic journals; 363.73
• DOI: 10.1016/j.envpol.2020.114126
• Languages: English
• ISSNs: 0269-7491

Abstract

Abstract: Trace metals can be essential for organo-metallic structures and oxidation-reduction in metabolic processes or may cause acute or chronic toxicity at elevated concentrations. The uptake of trace metals by earthworms can cause transfer from immobilized pools in the soil to predators within terrestrial food chains. We report a synthesis and evaluation of uptake and bioaccumulation empirical data across different metals, earthworm genera, ecophysiological groups, soil properties, and experimental conditions (metal source, uptake duration, soil extraction method). Peer-reviewed datasets were extracted from manuscripts published before June 2019. The 56 studies contained 3513 soil-earthworm trace metal concentration paired data sets across 11 trace metals (As, Cd, Cr, Cu, Hg, Mn, Ni, Pb, Sb, U, Zn). Across all field and laboratory experiments studied, the median concentrations of Hg, Pb, and Cd in earthworm tissues that were above concentrations known to be hazardous for consumption by small mammals and avian predators but not for Cu, Zn, Cr, Ni, and As. Power regressions show only Hg and Cd earthworm tissue concentrations were well-correlated with soil concentrations with R 2 > 0.25. However, generalized linear mixed-effect models reveal that earthworm concentrations were significantly correlated with soil concentrations for log-transformed Hg, Cd, Cu, Zn, As, Sb (p < 0.05). Factors that significantly contributed to these relationships included earthworm genera, ecophysiological group, soil pH, and organic matter content. Moreover, spiking soils with metal salts, shortening the duration of exposure, and measuring exchangeable soil concentrations resulted in significantly higher trace metal uptake or greater bioaccumulation factors. Our results highlight that earthworms are able to consistently bioaccumulate toxic metals (Hg and Cd only) across field and laboratory conditions. However, future experiments should incorporate greater suites of trace metals, broader genera of earthworms, and more diverse laboratory and field settings to generate data to devise universal quantitative relationships between soil and earthworm tissue concentrations. Graphical abstract: Image 1 Highlights: The first meta-analysis of trace metals in earthworms, with experimental design considered. Soil concentrations explained variation in earthworm concentrations for only Hg and Cd. Earthworm genera and ecophysiological group, soil pH and organic matter influenced uptake. Source of metal pollution and duration of exposure significantly affected trace metal uptake. Exchangeable soil metal concentrations generate artificially high bioaccumulation factors. Abstract : The meta-analysis revealed that while concentrations affected earthworm Cd and Hg concentrations, earthworm properties, soil properties, and experimental design, source of metal, and exposure duration significantly affected trace metal uptake.