Environ. Sci. Technol. 2003, 37, 81-86
“Nonavailable” Soil Cadmium Is Bioavailable to Snails: Evidence from Isotopic Dilution Experiments RENAUD SCHEIFLER,† CHRISTOPHE SCHWARTZ,‡ GUILLAUME ECHEVARRIA,‡ A N N E T T E D E V A U F L E U R Y , * ,† PIERRE-MARIE BADOT,† AND JEAN-LOUIS MOREL‡ Universite´ de Franche-Comte´, Institut des Sciences et Techniques de l’Environnement, Laboratoire de Biologie et Ecophysiologie, EA 3184 MR USC INRA, Place Leclerc, 25030 Besanc¸ on Cedex, France, and Laboratoire Sols et Environnement, ENSAIA-INPL/INRA UMR 1120, 2 avenue de la Foreˆt de Haye, BP 172, 54505 Vandoeuvre-le`s-Nancy Cedex, France
Isotopic dilution techniques were initially used to evaluate the bioavailability of trace metals contained in soils to plants, i.e., the phytoavailability. Here, we use for the first time an isotopic technique to evaluate the zooavailability of cadmium (Cd), i.e., the bioavailability to an animal organism. A terrestrial invertebrate, the snail Helix aspersa, was exposed for 14 days to a polluted soil that was spiked with 109Cd. Isotopic composition of snail tissues was then determined, allowing the computing of the L value, which can be considered as a biological estimate of the bioavailable Cd pool in the soil. It showed that the bioavailable pool of Cd to H. aspersa represented 58% of the total soil Cd. The E value, a chemical estimate of the soil Cd labile pool, was calculated with short-term isotopic exchange kinetics experiments and a time-dependent model describing the isotopic exchange over time. The E(14 days) value indicated that the labile soil Cd pool represented 49.6% of the total soil Cd. The L value was significantly higher than the E value, showing that snails accessed the nonlabile soil Cd pool, generally considered as nonbioavailable. The nonlabile pool contributed for 16% to the total Cd accumulated by snails. These results showed that the uptake of Cd in the nonlabile pool by soil organisms could be important and should be considered in risk assessment procedures for metal polluted soils.
Introduction Bioavailability of trace metals strongly influences their uptake by soil organisms. The concept of bioavailability is consequently particularly important for many scopes in ecotoxicological studies although it was not clearly defined until recently. It is now well accepted that the bioavailability of metals must be handled as a kinetic process with at least two distinct phases: the environmental availabilitysa physicochemically driven desorption processsand the environ* Corresponding author phone: +33 (0) 381 665 788; fax: +33 (0) 381 665 797; e-mail:
[email protected]. † Universite ´ de Franche-Comte´. ‡ Laboratoire Sols et Environnement, ENSAIA-INPL/INRA UMR 1120. 10.1021/es025677w CCC: $25.00 Published on Web 11/23/2002
2003 American Chemical Society
mental bioavailabilitysa species-specific physiologically driven uptake process (1-3). Numerous techniques and approaches were developed to estimate the bioavailable pools of metals for different soil organisms. The simplest approaches consist of measuring metal concentrations in solutions obtained by chemical extraction (including water-extraction) and to mathematically relate these concentrations to internal concentrations in organisms exposed to the soil. However, despite the large number of extractants used, none of them can satisfactorily describe the bioavailable pools in different soils and for different metals and organisms. This could easily be explained by the huge diversity of soil physicochemical characteristics, metal behavior, exposure routes and uptake mechanisms. Furthermore, even if soil concentrations and organism concentrations are related by a satisfactory relationship, this does not mean that metal ions extracted by the chemicals belong to the same fraction as the bioavailable pool for a particular organism (4). An alternative approach, the so-called pore-water hypothesis or equilibrium partitioning theory (1, 5, 6) was recently developed. This approach is based on the assumption that metal uptake by soil invertebrates is governed by transport via the soil pore-water and that direct uptake from the soil solid phase is negligible. This hypothesis was shown to be valid to characterize the bioavailability of organic chemicals for soft-bodied organisms such as earthworms (7-9). However, due to their complex physicochemical behavior in soils, evidence for the pore-water hypothesis is only circumstantial for metals (5, 10). Moreover, recent studies have found that cadmium (Cd) (11) or copper (Cu) (12) concentrations in Collembolans exposed to contaminated soils were poorly correlated to soil solution concentrations. In agreement with these studies, Oste et al. (13) have recently questioned the pore-water hypothesis for Cd in Lumbricus rubellus earthworms and suggested that uptake of Cd from other sources than the pore-water (as the “intestinal uptake of soil particulates”, for instance) should not be neglected. An unequivocal answer to the above debate is of critical importance for risk assessment in metal polluted areas, and a technique to quantitatively evaluate the pool that is actually bioavailable to soil organisms would greatly improve risk assessment procedures. Isotopic dilution techniques (IDT), initially used to characterize the phytoavailability of some macronutrients (e.g., P and K) (14-18), were successfully used to evaluate the phytoavailable pool of several metallic trace elements (MTE) such as Cd, Ni and Zn (4, 19, 20). However, IDT have never been used to study the zooavailability of MTE. IDT Principle. If a low amount of metal radioisotope (as metal ion in solution) is thoroughly mixed with soil, it is rapidly distributed within the isotopically exchangeable metal pool (21, 22) without modifying the chemical equilibrium of the metal between the solid and the liquid phase of the soil. The isotopically exchangeable metal pool, also called the “soil Cd labile pool”, corresponds to the pool of the element from the soil solid phase that may supply the soil solution during a given period of time. This pool is characterized by its isotopic composition (ratio of the radioisotope to the stable element), from which the E value can be calculated. The E value thus corresponds to a chemical estimate of the labile pool and is expressed in mg.kg-1. By contrast, the nonisotopically exchangeable metal pool, or “soil Cd non-labile pool”, is constituted of Cd strongly bound to the soil solid phase that cannot supply the soil solution during this time VOL. 37, NO. 1, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Physicochemical Characteristics of Soils characteristic
polluted soil
unpolluted soil
clay, g.kg-1 a organic matter, g.kg-1 C/Nb PHH2Oc total CaCO3, g.kg-1 d P2O5, g.kg-1 e CEC, cmol.kg-1 f total Cu, mg.kg-1 total Zn, mg.kg-1 total Ni, mg.kg-1 total Pb, mg.kg-1 total Cd, mg.kg-1
202 42.1 16.8 6.2
