Modelling the effects of copper on soil organisms and processes using the free ion approach: Towards a multi-species toxicity model
Introduction
Copper is a natural constituent of all soils, and in small quantities is an essential element for all plants and animals. Elevated concentrations of copper in soils can however lead to toxic effects on plants and soil-dwelling animals and hence on ecosystems as a whole (Flemming and Trevors, 1989). For this reason, ecological risk assessment of copper is an important aspect of the management of concentrations of the metal in soils.
Along with other cationic metals such as zinc and cadmium, the influence of soil chemistry on the bioaccumulation and toxicity of copper is well attested (Lexmond, 1980; Cheng and Allen, 2001). There is thus a need to develop approaches to quantify the influence of soil chemical properties on metal toxicity, in order to improve their ecological risk assessment. To date, approaches taken have been both empirical and mechanistic. In the former, endpoints from a single toxicity test, carried out in a variety of soils, are regressed against one or more soil properties believed to impact bioavailability. Such properties include soil solution pH, soil organic matter (OM) content and cation exchange capacity (CEC), and contents of mineral oxides of elements such as Fe and Mn. This type of work has been done for a number of soil organisms including barley and tomato (Rooney et al., 2006), wheat (Warne et al., 2008) and microbial processes (Oorts et al., 2006; Broos et al., 2007) for copper. The mechanistic approach centres on the Biotic Ligand Model (Paquin et al., 2002) which postulates that toxicity results from binding of specific metal species (usually the free metal ion) to a receptor on the organism (the Biotic Ligand), in competition with other solution cations such as H+, Na+ and Ca2+. The concentration of metal bound to the biotic ligand, rather than a measurable or calculable pool of metal in the soil or soil solution, is assumed to correlate with the toxic response. The BLM was originally developed to describe the acute toxic effects of metal accumulation at the gill of fish, but has been applied to toxicity data for a number of other aquatic organisms. Some progress has been made in applying the principles of the BLM to soil-dwelling organisms: acute BLMs have been developed for soil organisms such as the earthworm Aporrectodea caliginosa (Steenbergen et al., 2005) and the enchytraeid Enchytraeus albidus (Lock et al., 2006), and the model has been applied to describe the effects of metals on plants in solution (Lock et al., 2007). Thakali et al., 2006a, Thakali et al., 2006b have developed BLMs to predict the effects of copper on plants, invertebrates and microbial processes, based on testing using a set of European soils of contrasting soil chemistries (Rooney et al., 2006; Oorts et al., 2006; Criel et al., 2008).
An alternative approach to considering bioavailability effects has been taken by Lofts et al. (Lofts et al., 2004; De Vries et al., 2007). Termed the free ion approach, this method considers the toxic effect to depend upon the free metal ion in soil solution, and also on the amounts of other solution cations that ‘protect’ the organism against metal toxicity. The variables considered are thus the same as would be considered by the BLM, but the expression describing the loading of the biotic ligand with toxic metal is replaced with an empirical function, and the ‘biotic ligand’ is not explicitly considered. The free ion approach was used to derive functions giving critical limits (risk threshold concentrations) for copper and other metals in soils directly from existing literature (Lofts et al., 2004; De Vries et al., 2007). Because of the limited nature of the available data, a number of key assumptions were made in the derivation of the critical limit functions. Such assumptions require investigation, either to confirm that they are reasonable, or to allow further refinement of the methodology. In the case of copper, datasets now exist (Rooney et al., 2006; Oorts et al., 2006; Criel et al., 2008) that are suitable for such a purpose. These datasets comprise seven toxicity tests covering a range of species and microbial processes, each carried out in the same set of soils. The soils were chosen to cover a range of key soil properties, thus making the datasets ideal for investigating metal bioavailability effects. The subset of toxicity data from the non-calcareous soils has been previously used to develop terrestrial BLMs (Thakali et al., 2006a,b). The purpose of the work presented here is to extend the free ion approach to these data and to test, for copper, the assumptions previously made in applying the approach.
Section snippets
Theory
The free ion approach is summarised in an empirical expression describing the variation of the effect concentration of a potentially toxic cationic metal in soil solution with the soil solution pH and concentrations of ‘protective’ cations. For copper:Here pHss is the soil solution pH, [Cz+] is the free concentration of a ‘protective’ cation, α, η and γeffect are constants, and [Cu2+]effect is the ‘effect’ concentration of the free copper ion. The
Soils dataset
Nineteen soils from across Europe were used for the toxicity testing and selected soil properties are given in Table 1 (after Oorts et al. (2006)).
Methods for the determination of soil metal and soil solution chemistry in spiked test soils are described in Rooney et al. (2006) and Oorts et al. (2006). Soil solutions were analysed for Cu, major cations (Na, Mg, Al, K, Ca and Fe) and dissolved organic carbon (DOC).
Toxicity testing
The toxicity tests comprised seven endpoints: two plant growth tests, two
Results
Table 3 shows fits to Models 0, 1 and 2 for the individual toxicity tests. Model 2 (Deff = log [Cu2+] − α · pHss) consistently gave a superior fit to the data than Model 1 (Deff = log [Cu2+]). In only three toxicity tests out of seven did Model 1 explain over half the variance in the observations, while Model 2 consistently explained over half the variance in all the tests. It is worth noting that the maize residue mineralisation (MRM) test was relatively insensitive to copper within the range
Discussion
FRIED was successful in describing the variability in copper toxicity across the different soils. In six of the seven tests, FRIED fits were superior to those obtained taking total soil metal as the effective dose. FRIED fitting confirmed a significant effect of pH on Cu2+ toxicity, in agreement with previous work such as that by Steenbergen et al. (2005) on the acute toxicity of Cu to the earthworm A. caliginosa, Thakali et al. (2006a, b) on the non-calcareous soils of this dataset, and the
Acknowledgements
We thank Ed Tipping for discussions and Helen Hooper for comments on an early draft of the manuscript. This work was funded by the International Copper Association. Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
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