Impact of the earthworm Lumbricus terrestris (L.) on As, Cu, Pb and Zn mobility and speciation in contaminated soils

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Abstract

To assess the risks that contaminated soils pose to the environment properly a greater understanding of how soil biota influence the mobility of metal(loid)s in soils is required. Lumbricus terrestris L. were incubated in three soils contaminated with As, Cu, Pb and Zn. The concentration and speciation of metal(loid)s in pore waters and the mobility and partitioning in casts were compared with earthworm-free soil. Generally the concentrations of water extractable metal(loid)s in earthworm casts were greater than in earthworm-free soil. The impact of the earthworms on concentration and speciation in pore waters was soil and metal specific and could be explained either by earthworm induced changes in soil pH or soluble organic carbon. The mobilisation of metal(loid)s in the environment by earthworm activity may allow for leaching or uptake into biota.

Research highlights

► Earthworms increase the mobility and availability of metals and metalloids in soils. ► We incubated L. terrestris in three soils contaminated with As, Cu, Pb and Zn. ► Earthworms increased the mobility of As, Cu, Pb and Zn in their casts. ► The mechanisms for this could be explained by changes in pH or organic carbon.

Introduction

Human activities have resulted in an increase in the concentrations of metals and metalloids in urban and rural soils due to diffuse and point source pollution. These disruptions to the natural biogeochemical cycle of metals and metalloids can lead to toxic effects on flora and fauna. Earthworms are found in soils containing elevated levels of metals and metalloids (Spurgeon and Hopkin, 1996, Langdon et al., 2001, Vijver et al., 2007) and represent a major constituent of soil fauna. Bioavailable- rather than total- concentrations determine metal toxicity in soils (Harmsen, 2007) and this is dependent on mobility and speciation in the living soil environment (Di Toro et al., 2001, Thakali et al., 2006, Arnold et al., 2007). In order to assess properly the risks that metal contamination of soil poses to the environment, a greater understanding of how soil biota influence the mobility, partitioning and speciation of metals and metalloids in contaminated soils is required.

Generally earthworms increase the mobility and availability of metals and metalloids in soils (Sizmur and Hodson, 2009). This can result in greater concentrations of metals leaching out of the soil into ground water (Tomlin et al., 1993) or greater uptake into plants (Ma et al., 2003, Yu et al., 2005, Wang et al., 2006) and soil animals (Currie et al., 2005, Coeurdassier et al., 2007). In addition to this, earthworms may reduce the efficiency of soil remediation by mobilising recalcitrant metals (Udovic et al., 2007). The mechanisms for earthworms increasing metal mobility and availability are unclear, but may involve changes in microbial populations, pH, dissolved organic carbon or metal speciation (Sizmur and Hodson, 2009).

Earthworms burrow in the soil and create casts that are chemically, biologically and physically different from the surrounding soil (Edwards, 2004). Earthworm casts have more active microbial communities than surrounding soil (Scheu, 1987); there is evidence that they have a humifying capacity (Businelli et al., 1984) and contain a higher concentration of soluble organic carbon compared to bulk soil (Daniel and Anderson, 1992). Ireland (1975) extracted more water extractable Zn from earthworm faeces compared with bulk contaminated soil and Devliegher and Verstraete (1996) give evidence that gut associated processes in Lumbricus terrestris (L.) are responsible for increases in metal availability in uncontaminated soils.

Anecic earthworms produce casts on the soil surface (Edwards and Bohlen, 1996) and line their burrows with their own faeces (Binet and Curmi, 1992) leading to the potential for metals and metalloids to be leached out of soils into surface waters or ground waters. Therefore we carried out an experiment with a UK native anecic species (L. terrestris) to determine the impact of soil passage through the earthworm gut on the mobility and partitioning of metals and metalloids in casts and how this impacts on the concentrations and speciation of metals and metalloids in the pore waters of earthworm-inhabited soils compared to earthworm-free soils.

Section snippets

Soil and earthworms

L. terrestris were sourced from Worms Direct, Ulting, UK. Three contaminated soils were used in this study (Table 1). Rookhope (54.780947 -2.121240; WGS84) and Devon Great Consols (DGC) (50.540851 -4.226920; WGS84) soils were collected from a former lead and fluorspar mine and a former copper and arsenic mine, respectively. Wisley soil (51.312975 -0.474771; WGS84) was amended with Pb nitrate and Cu and Zn sulphate salts 15 years ago (Alexander et al., 2006). Soil was collected from the top 30 cm

Results

Earthworm mortality was low in the contaminated soils with 100% survival in Rookhope and Wisley soils and12% mortality in the DGC soil. Earthworms in all three soils lost weight during the test period. L. terrestris fresh weight decreased by 21% (1.1 g, SD = 0.88, n = 25) in Rookhope soil, 11% (0.5 g, SD = 0.48, n = 25) in the Wisley soil and 27% (1.3 g, SD = 1.01, n = 22) in the DGC soil.

Discussion

Earthworms lost weight in all three soils used in this study. This weight loss is most likely due to the absence of food supplied on the surface of the soil. Food was withheld in order to ensure that any changes in metal chemistry that were observed were due to the burrowing activity of the earthworms rather than the effect of mixing the food in with the soil matrix. The greatest weight loss occurred in the DGC soil which was the only soil which had a pH below the recommended range (4.5–7) for

Conclusions

The impact of earthworms on metal mobility, partitioning and speciation in soils and solution is both soil and metal specific and depends on whether earthworm activity increases or decreases pH and the solubility of organic carbon. The speciation (and therefore bioavailability) of metals leached out of contaminated soils to water courses is an important consideration for risk assessment and it is clear that earthworms influence this. In the soil environment the mobilisation of previously

Acknowledgements

This work was funded by a BBSRC studentship, with CASE support from BUFI-BGS. We would like to acknowledge the comments of three anonymous reviewers for improving this manuscript.

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