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

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 R2 > 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.

Exotic Earthworms Decrease Cd, Hg, and Pb Pools in Upland Forest Soils of Vermont and New Hampshire USA.

Exotic earthworms are present in the forests of northeastern USA, yet few studies have documented their effects on pollutant metals in soil. The objective of this study was to identify if Cd, Hg, and Pb strong-acid extractable concentrations and pools (bulk inventories) in forest soils decreased with the presence of exotic earthworms. We compared 'Low Earthworm Abundance' (LEA) sites (≤10 g m-2 earthworms, n = 13) and 'High Earthworm Abundance' (HEA) (>10 g m-2 earthworms, n = 17) sites at five watersheds across Vermont and New Hampshire. Organic horizon Cd, Hg, and Pb concentrations were lower at HEA than LEA sites. Organic horizon and total soil pools of Cd and Hg were negatively correlated with earthworm biomass. Soil profile Cd and Hg concentrations were lower at HEA than LEA sites. Our results suggest earthworms are decreasing accumulation of Cd, Hg, and Pb in forest soils, potentially via greater mobilization through organic matter disruption or bioaccumulation.

Forest floor decomposition, metal exchangeability, and metal bioaccumulation by exotic earthworms: Amynthas agrestis and Lumbricus rubellus.

Earthworms have the potential to reduce the retention of pollutant and plant essential metals in the forest floor (organic horizons) by decomposing organic matter and increasing exchangeability of metals. We conducted a laboratory experiment to investigate the effects of two exotic earthworms, Amynthas agrestis and Lumbricus rubellus, on forest floor decomposition, metal exchangeability, and metal bioaccumulation. Eighty-one pots containing homogenized forest floor material were incubated for 20, 40, or 80 days under three treatments: no earthworms, A. agrestis added, or L. rubellus added. For earthworm treatments, A. agrestis and L. rubellus were stocked at densities observed in previous field studies. Pots containing either A. agrestis or L. rubellus had lost more forest floor mass than the control plots after 40 and 80 days of incubation. Forest floor pots containing A. agrestis had significantly lower % C (16 ± 1.5 %) than control pots (21 ± 1.2 %) after 80 days. However, L. rubellus consumed more forest floor and C mass than A. agrestis, when evaluated on a per earthworm biomass basis. Exchangeable (0.1 M KCl + 0.01 M AcOH extractable) and stable (15 M HNO3+ 10 M HCl extractable) concentrations of Al, Ca, Cd, Cu, Mg, Mn, Pb, and Zn in forest floor material were measured. Stable concentrations and % exchangeable metals in forest floor material were similar among treatments. Although exchangeable metal concentrations varied significantly for most metals among treatments (except Mg and Zn), we conclude that earthworms did not increase or decrease the exchangeability of metals. However, earthworms bioaccumulated Cu, Cd, Zn, and Mg and had potentially hazardous tissue concentrations of Al and Pb. This was best illustrated by calculating bioaccumulation factors using exchangeable concentrations rather than total concentrations. Future research is needed to understand the effect of earthworms on metals in other soil types.

Nutrient and pollutant metals within earthworm residues are immobilized in soil during decomposition.

Earthworms are known to bioaccumulate metals, making them a potential vector for metal transport in soils. However, the fate of metals within soil upon death of earthworms has not been characterized. We compared the fate of nutrient (Ca, Mg, Mn) and potentially toxic (Cu, Zn, Pb) metals during decomposition of Amynthas agrestis and Lumbricus rubellus in soil columns. Cumulative leachate pools, exchangeable pools (0.1 M KCl + 0.01 M acetic acid extracted), and stable pools (16 M HNO3 + 12 M HCl extracted) were quantified in the soil columns after 7, 21, and 60 days of decomposition. Soil columns containing A. agrestis and L. rubellus had significantly higher cumulative leachate pools of Ca, Mn, Cu, and Pb than Control soil columns. Exchangeable and stable pools of Cu, Pb, and Zn were greater for A. agrestis and L. rubellus soil columns than Control soil columns. However, we estimated that > 98 % of metals from earthworm residues were immobilized in the soil in an exchangeable or stable form over the 60 days using a mass balance approach. Micro-XRF images of longitudinal thin sections of soil columns after 60 days containing A. agrestis confirm metals immobilization in earthworm residues. Our research demonstrates that nutrient and toxic metals are stabilized in soil within earthworm residues.

Trace Metals and Metalloids in Forest Soils and Exotic Earthworms in Northern New England, USA.

Trace metals and metalloids (TMM) in forest soils and invasive earthworms were studied at 9 uncontaminated sites in northern New England, USA. Essential (Cu, Mo, Ni, Zn, Se) and toxic (As, Cd, Pb, Hg and U) TMM concentrations (mg kg-1) and pools (mg m-2) were quantified for organic horizons (forest floor), mineral soils and earthworm tissues. Essential TMM tissue concentrations were greatest for mineral soil-feeding earthworm Octolasion cyaneum. Toxic TMM tissue concentrations were highest for organic horizon-feeding earthworms Dendobaena octaedra, Aporrectodea rosea and Amynthas agrestis. Most earthworm species had attained tissue concentrations of Pb, Hg and Se potentially hazardous to predators. Bioaccumulation factors were Cd > Se > Hg > Zn > Pb > U > 1.0 > Cu > As > Mo > Ni. Only Cd, Se Hg and Zn were considered strongly bioaccumulated by earthworms because their average bioaccumulation factors were significantly greater than 1.0. Differences in bioaccumulation did not appear to be caused by soil concentrations as earthworm TMM tissue concentrations were poorly correlated with TMM soil concentrations. Instead, TMM bioaccumulation appears to be species and site dependent. The invasive Amynthas agrestis had the greatest tissue TMM pools, due to its large body mass and high abundance at our stands. We observed that TMM tissue pools in earthworms were comparable or exceeded organic horizon TMM pools; earthworm tissue pools of Cd were up 12 times greater than in the organic horizon. Thus, exotic earthworms may represent an unaccounted portion and flux of TMM in forests of the northeastern US. Our results highlight the importance of earthworms in TMM cycling in northern forests and warrant more research into their impact across the region.