Development and validation of an acute biotic ligand model (BLM) predicting cobalt toxicity in soil to the potworm Enchytraeus albidus

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Abstract

An acute Biotic Ligand Model (BLM) was developed to predict the effect of cobalt on the survival of the potworm Enchytraeus albidus, exposed in nutrient solutions added to acid washed, precombusted sand. The extent to which Ca2+, Mg2+ and Na+ ions and pH independently mitigate cobalt toxicity to E. albidus was examined. Higher activities of Ca2+, Mg2+ and H+ linearly increased the 14 d LC50Co2+ (LC50 expressed as Co2+-activity) whereas Na+-activity did not. Stability constants for the binding of Co2+, Ca2+, Mg2+ and H+ to the biotic ligand (BL) were derived, i.e. log KCoBL=5.13, log KCaBL=3.83, log KMgBL=3.95 and log KHBL=6.53. It was calculated that at Co-concentrations corresponding to the 14d-LC50 value, 32% of the BL sites were occupied by cobalt. An initial validation of the applicability of this BLM in true soil exposure systems was performed by comparing observed and model-predicted 14 d LC50 s in a standard artificial soil and a standard field soil. By assuming pore water to be the only route of exposure and assuming equilibrium between pore water Co2+ and solid phase Co, which is predicted by the geochemical WHAM-Model 6, LC50 s (as mg Co kg−1 dry wt of soil) were predicted within an error of less than a factor two. Further validation in true soil exposures, combined with more detailed knowledge of Co binding to soil solid phases is needed, if this model is to be used as a tool for risk assessment and derivation of soil quality criteria for Co.

Introduction

Cobalt is a naturally occurring element and is mainly present in the earth's crust as cobaltite [CoAsS], erythrite [Co3(AsO4)2] and smaltite [CoAs2] (Barceloux, 1999). Cobalt is mainly used as a component of very hard, strong and heat-resistant alloys and in permanent magnets. It is also used as drying agent in paintings, as colour pigment in porcelain, as a catalyst in rubber manufacturing and as an additive in fertilizers and fodders (Barceloux, 1999). Elevated cobalt concentrations in the terrestrial environment may, for example, result from deposition from burning of fossil fuels, wear of cobalt-containing alloys and spreading of sewage sludge and manure (Barceloux, 1999).

Metals such as cobalt may present environmental risk when occurring at elevated concentrations and are being managed through the establishment of environmental quality criteria and standards. Recently it has been recognized by regulators, industry and academic scientists that standard procedures for deriving environmental quality criteria are inadequate to accurately assess the potential impact of metals on the ecological quality of ecosystems (Fairbrother et al., 1999; Janssen et al., 2000). This is because current environmental quality criteria and risk-assessment procedures of metals are predominantly based on total metal concentrations. However, there is extensive evidence that total metal concentrations in soils are not good predictors of metal bioavailability and toxicity. The 14 d LC50 of Zn, Cd, Cu and Pb to Enchytraeus albidus, for example, varied over more than two orders of magnitude depending on the composition of the soil (Lock et al., 2000; Lock and Janssen, 2001a). These differences in metal toxicity were mainly determined by pH and cation exchange capacity of the soil. In addition, metal toxicity is higher in freshly spiked soils compared to historically contaminated field soils (Lock and Janssen, 2001b; Lock and Janssen, 2003).

The dependence of metal toxicity on soil characteristics such as cation exchange capacity, organic matter content and pH indicates the need to develop tools for predicting metal toxicity in soils with distinct properties. Although empirical regression models are promising, the further development of more sophisticated models may provide mechanistic explanations of metal bioavailability in soil. One such approach may be to develop a terrestrial biotic ligand model (BLM). The BLM concept (e.g. Di Toro et al., 2001; De Schamphelaere and Janssen, 2002), originally developed for aquatic metal toxicity, has recently gained increased attention from both academic scientists and regulators and is now considered to be the state-of-the-science metal bioavailability model/concept that might be applicable to regulatory matters concerning metals in the environment.

The main assumption of the BLM is that metal toxicity occurs as the result of free metal ions (or other reactive metal species) reacting with binding sites at the organism–water interface (either physiologically active sites, leading to a direct biological response, or transport sites, leading to metal transport into the cell followed by an indirect biological response), which is represented as the formation of a metal–biotic ligand complexes. The concentration of these metal–biotic ligand complexes directly determines the magnitude of the toxic effect, independent of the chemical characteristics of the test medium. Ca2+, Mg2+, Na+ and H+ ions may compete for binding sites at the organism–water interface (Pagenkopf, 1983; Di Toro et al., 2001; Santore et al., 2001), thus reducing the binding of toxic metal species to the BL and eventually reducing the toxicity of the reactive metal species (Pagenkopf, 1983; Di Toro et al., 2001; Santore et al., 2001; De Schamphelaere and Janssen, 2002). Computationally, a BLM makes use of a speciation model (e.g. Model V or Model VI, Tipping, 1998; Lofts and Tipping, 2002) to calculate the free metal ion activity. The binding of metal ions and competing cations to the BL is then calculated in the same way as any other reaction of a cation with an organic or inorganic ligand, i.e. by stability constants.

Until now, BLMs have mainly been developed to predict metal toxicity to aquatic organisms. Recently, Steenbergen et al. (2005) successfully developed a terrestrial BLM to predict acute Cu toxicity to the earthworm Aporrectodea caliginosa, showing that the BLM concept is also applicable in the terrestrial environment. To our knowledge and according to the review of Niyogi and Wood (2004), no data are available on the effects of competing cations on Co toxicity. However, Richards and Playle (1998) found that increased Ca2+, Na+ and H+ activities reduced short-term cobalt accumulation in rainbow trout (Oncorhynchus mykiss) gills, the primary target of metal toxicity to fish (Paquin et al., 2002).

In this study, it was examined if the BLM concept is applicable to predict acute Co toxicity to the terrestrial invertebrate E. albidus. The hypothesis is that exposure only occurs via the pore water and that interactions between Co2+ and competing cations for the biotic ligand can be described in a similar way as in aquatic BLMs. E. albidus was exposed in nutrient solutions added to acid-washed, precombusted sand for the development of a BLM for cobalt. This approach allowed to control all water characteristics affecting cobalt bioavailability. The aims of the present study were three-fold: (1) to investigate the extent to which calcium, magnesium, sodium and hydrogen ions can individually mitigate cobalt ion toxicity in solution to E. albidus, (2) to use the obtained toxicity data to derive estimates of the parameters necessary to develop a BLM that can predict cobalt toxicity towards E. albidus for a broad range of pore water characteristics and (3) to perform an initial validation of the obtained BLM in a true soil exposure system, using two standard soils spiked with Co.

Section snippets

Test design for BLM development

In order to assess the independent effect of different cations on cobalt toxicity, one cation concentration at a time was varied, while keeping all other cation concentrations low and as constant as possible. Four sets of cobalt bioassays were performed: a Ca-set, a Mg-set, a Na-set and a pH-set (Table 1). Each set consisted of a series of test solutions, added to acid-washed and precombusted sand (see further), in which only the cation under consideration was varied. For each test solution,

Results

The 14 d-LC50Co2+ for E. albidus, expressed as free cobalt ion activity, ranged from 3.7 to 210 μM Co2+, which is a 57-fold difference. The 14 d LC50Co2+ significantly increased with increasing Ca2+ activity (9-fold increase, R2=0.97, p<0.0001) (Fig. 1A), Mg2+ activity (11-fold increase, R2=0.96, p=0.00012) (Fig. 1B) and H+ activity (9-fold increase, R2=0.93, p=0.0019) (Fig. 1D). Calculation of the Ca2+, Mg2+ and H+ stability constants according to De Schamphelaere and Janssen (2002) and using

Discussion

The 14 d LC50Co2+ varied about 57-fold, which clearly demonstrates the limitations of using free ion activity for predicting cobalt toxicity. However, a large part of these differences could be explained by positive linear relations between LC50Co2+ and the activity of Ca2+, Mg2+ and H+. This supports the assumptions of the BLM concept (Eq. (3)) and has often been associated with competitive reactions at biological surfaces of a variety of species (Pagenkopf, 1983; Santore et al., 2001; De

Acknowledgments

Karel De Schamphelaere is a post-doctoral research fellow of the Fund for Scientific Research—Flanders (FWO-Vlaanderen, Belgium). Additional support was provided by the Cobalt Development Association (CDA, United Kingdom). The authors would like to thank Emmy Pequeur and Jill Van Reybrouck for their technical assistance.

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