Impact of earthworms on trace element solubility in contaminated mine soils amended with green waste compost
Graphical abstract
Highlights
► Compost reduced the mobility of Cu, Pb and Zn. ► Compost increased the mobility of As. ► Earthworms decreased water soluble As and Cu but increased Pb and Zn in porewater. ► These effects are explained by the impact of the earthworms and compost on pH and DOC.
Introduction
The combination of large areas of metal or metalloid contaminated soils associated with former mining and smelting activities and the generation of green waste from domestic, agricultural and silvicultural management of vegetation has resulted in the practice of remediating mine contaminated soils with green waste composts and other organic wastes (van Herwijnen et al., 2007b, Pichtel and Bradway, 2008, Farrell et al., 2010). Composts generally increase plant growth which can prevent wind and water erosion of contaminated soils (Tordoff et al., 2000). In addition, cationic metals bind to exchange sites on the surface of organic matter which reduces metal leaching from soils (Soler-Rovira et al., 2010).
Earthworms represent a significant proportion of the soil fauna and are considered ecosystem engineers owing to the role that they play in organic matter degradation, nutrient cycling and hydrology (Jones et al., 1994). For these reasons they have been the subject of innoculation programes during the reclamation of degraded soils (Butt, 1999). Earthworm inoculation therefore has the potential to become a commonly used practice during remediation and revegetation of metal contaminated mine soils. Earthworms are also able to colonise contaminated land if climatic and material (organic matter, texture, pH, contaminant) conditions are suitable (Eijsackers, 2010) and so, when organic amendments are incorporated into contaminated soils, it is likely that earthworms will colonise leading to changes in the chemical, biological and physical properties of the soil.
We reviewed the impact of earthworms on the mobility and availability of metals and found that in the majority of studies earthworms increase the mobility of metals (Sizmur and Hodson, 2009). Recent experiments have identified that this may be due to the impact of earthworms on the degradation of organic matter and subsequent release of organically bound elements and dissolved organic acids that lower the soil pH and lead to further mobilisation of potentially toxic elements (Gomez-Eyles et al., 2011, Sizmur et al., 2011b). In contrast, Beesley and Dickinson (2011) showed in an experiment with an urban soil contaminated with As, Cd, Cu, Pb and Zn, that Lumbricus terrestris reduced dissolved organic carbon in porewater and thereby reduced the solubility of As, Cu and Pb in a compost amended soil.
Different trace elements bind with organic compounds to varying degrees and behave differently to changes in soil pH. Therefore, the impact of compost or earthworm additions on the solubility of trace elements depends not only on the changes in soluble organic carbon and pH, but also on the chemistry of the element in question. Copper and Pb both bind strongly with organic carbon and therefore their solubility is much affected by changes in soluble organic compounds (McBride et al., 1997). Zinc, however, does not bind so strongly with organic carbon and so its solubility is relatively more affected by changes in pH (McBride, 1994). The solublity of Cu, Pb and Zn is increased with decreasing pH because these elements are cationic (McBride et al., 1997), but As solubility is decreased with decreasing pH because As forms an oxy-anion in solution and binds to positively charged soil surfaces such as iron oxyhydroxides (Masscheleyn et al., 1991).
Lukkari et al. (2006) gave evidence that earthworms increase the extractability of Cu and Zn in their faeces, but decrease the overall extractability of metals in the bulk earthworm inhabited soil. This indicates that there are probably at least two separate conflicting mechanisms by which earthworms impact metal mobility. Earthworms burrow and create casts that have elevated concentrations of extractable trace elements (Sizmur et al., 2011a). In addition, they also release mucus into the soil solution which may decrease the solubility of metals (Sizmur et al., 2010). Mucus is produced in greater quantities during copulation (Edwards and Bohlen, 1996) and so this effect would be observed to a greater extent in experiments where two or more earthworms are incubated in each test vessel.
In the current study we used anecic L. terrestris to determine the impact of earthworms on the remediation of contaminated soils with green waste compost. Treatments of either one or two earthworms, with a constant earthworm:soil mass ratio, were applied to determine the impact of earthworm interactions on the solubility, extractability and speciation of As, Cu, Pb and Zn in two highly contaminated mine soils.
Section snippets
Soils and earthworms
L. terrestris (5.1 g, SD = 0.70, n = 150) were sourced from Worms Direct, Ulting, UK. All earthworms were adult, fully clitellate and depurated for 48 h (Arnold and Hodson, 2007) prior to innoculation into the test medium. Rookhope (Pb/Zn) (54.780947 -2.121240; WGS84) and Devon Great Consols (As/Cu) (50.540851 -4.226920; WGS84) soils were collected from a former lead and fluorspar mine (contaminated with Pb and Zn) and a former copper and arsenic mine (contaminated with As and Cu),
Mortality, weight and trace element bioaccumulation in earthworms
Generally, mortality of the earthworms over the test duration was low and the majority of treatments resulted in 0% mortality (Table 2). In treatments containing two earthworms where one earthworm died, the other also died in all cases. The As/Cu soil amended with 20% compost treatment caused the greatest mortality. Earthworms in all treatments lost weight over the test duration, but in both As/Cu and Pb/Zn soils compost addition significantly (p < 0.05) reduced the weight loss (Table 2).
Arsenic
The addition of compost increased the porewater and water soluble concentrations of As in the As/Cu soil (Fig. 1, Fig. 3), as has been previously observed (Beesley et al., 2010). This is due to the increase in soil and porewater pH (Fig. 2, Fig. 4) brought about from the addition of compost with pH 6.8 to a soil with a pH of 4.1 (Table 1). As the pH increases, soil Fe and Mn oxide and oxyhydroxide surfaces become increasingly negatively charged and favour the desorption of arsenic oxyanions (
Conclusions
Generally, the effect of compost increased the solubility of As and decreased the solubility of Cu in As/Cu soil and decreased the solubility of Pb and Zn in Pb/Zn soil. Earthworm addition decreased the solubility of As and Cu in the As/Cu soil and increased the solubility of Pb and Zn in the Pb/Zn soil, apart from when Pb solubility was determined by water soluble Pb and As solubility was determined in porewater. These differences are probably due to the difference in the soil to liquid ratio
Acknowledgements
This work was funded by a BBSRC studentship, with CASE support from BUFI-BGS. We wish to acknowledge the helpful comments of three anonymous reviewers which improved this manuscript.
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