Environ. Sci. Technol. 2005, 39, 293-298
Bioaccumulation of Organic Chemicals in Contaminated Soils: Evaluation of Bioassays with Earthworms T J A L L I N G J A G E R , * ,† LEON VAN DER WAL,‡ ROEL H. L. J. FLEUREN,§ ARJAN BARENDREGT,‡ AND JOOP L. M. HERMENS‡ Vrije Universiteit Amsterdam, Department of Theoretical Biology, De Boelelaan 1085, NL-1081 HV, Amsterdam, The Netherlands, Institute for Risk Assessment Sciences (IRAS), Utrecht University, P.O. Box 80176, NL-3508 TD Utrecht, The Netherlands, and National Institute of Public Health and the Environment (RIVM), Laboratory for Ecological Risk assessment (LER), P.O. Box 1, NL-3720 BA Bilthoven, The Netherlands
Earthworms live in close contact with the soil and can thus be considered representative for the bioavailability of chemicals at contaminated sites. Bioavailability can either be assessed by analyzing earthworms from contaminated locations or by exposing laboratory-reared specimens to soil samples from the field (bioassays). In this study, we investigate the relevance of bioassays by using an extended experimental design (to identify signs of depletion of the bioavailable phase by the earthworms) and by using two species of earthworm (the standard test species Eisenia andrei and the field-relevant Aporrectodea caliginosa). Furthermore, bioassay results are compared to body residues of worms collected from the field site: a heavily polluted polder, amended with dredge spoil. We focused on telodrin, dieldrin, hexachlorobenzene, and eight PCBs. With our bioassay design, it was shown that depletion was unlikely, although more subtle effects could have occurred (e.g., changes in sorption during the experiments). E. andrei is a good choice for bioassays because its body residues correlate well to those in A. caliginosa, as well as to those in the field-collected worms. Nevertheless, E. andrei accumulated slightly more than the other species and appeared to be more sensitive to the conditions in soil from one of our sites.
Introduction Most of the seriously polluted soils in The Netherlands originate from practices between 1960 and 1980, including dumping of chemical wastes and disposal of dredge materials from harbors. Risk assessment for these contaminated sites is seriously hampered by a lack of quantitative knowledge about bioavailability of the pollutants. It is generally accepted that the total concentration is a poor measure for predicting * Corresponding author phone: +31 20 444 7134; fax: +31 20 444 7123; e-mail:
[email protected]. † Vrije Universiteit Amsterdam. ‡ Utrecht University. § National Institute of Public Health and the Environment. 10.1021/es035317o CCC: $30.25 Published on Web 11/26/2004
2005 American Chemical Society
accumulation and toxic effects and that bioavailability tends to decrease with increasing contact time between chemical and soil (sequestration) (1). Earthworms are appropriate model organisms for bioavailability as they live in close contact with the soil, have a thin and permeable cuticle, and also consume large amounts of soil. However, bioassays with earthworms have several limitations in providing a general measure of bioavailability. First, bioavailability may depend on the behavior of the organism and may thus differ between species (2); second, assays are generally performed with homogenized and sieved soil samples whereas exposure in the field is more heterogeneous. The capacity of the pore-water pool for hydrophobic chemicals is very small, so desorption from the solid phases is needed to establish the observed body residues (see, e.g., 3). When this desorption is slow, deviating accumulation patterns may result. To illustrate the possible effects of depletion, three extreme cases are shown in Figure 1. When desorption does not occur at all, the worms may deplete the pore-water phase. This will show up as a rapid equilibration in the first accumulation stage and substantially less uptake in the second accumulation stage (reusing the soil from the first accumulation stage with new earthworms). For example, there are indications that uptake of dieldrin was limited by chemical transport in the soil (4) and that the bioavailable phase for PAHs can be depleted (3, 5). Furthermore, the rate constant in the elimination stage in uncontaminated soil will be smaller than the apparent rate constant from the accumulation stages. When desorption is slow and ratelimiting, we should observe a first rapid increase in body residues, followed by a slower rate of increase (governed by desorption). Several authors have reported peak-shaped accumulation curves (3, 5-8), most often for PAHs. The exact cause of this pattern is unknown, but suggested explanations include the induction of active excretion by the worm (6), an increase of sorption in soil (7), or biodegradation coupled to slow desorption from organic matter (8). When there is rapid degradation or sequestration, the bioavailable concentration will decrease during the experiment, leading to peak-shaped uptake curves. When this shape is caused by induced biotransformation in the organism, one can expect that the second accumulation stage will be identical to the first stage (as bioavailability is unaffected). In an attempt to evaluate the relevance and limitations of bioassays, we used an extended experimental setup. As the location, we selected a polder within the city of Rotterdam in The Netherlands that has served as a depot for heavily contaminated dredge spoil from the harbor of Rotterdam in the 1970s. To address potential problems with depletion in laboratory experiments, we follow the accumulation in time, as well as elimination on a reference soil. Furthermore, we reuse the soil from the accumulation assays to assess possible changes in availability or depletion of the bioavailable phase (stage 3 in Figure 1). The resulting patterns can be compared to the predicted curves of Figure 1. Besides depletion, we turn to the more practical problem of whether the standard assays are representative for the field situation and for different species. The standard test species is Eisenia andrei (9, 10), even though its natural habitat is limited to accumulations of organic matter (like compost heaps and manure). Additionally, we therefore use a typical soil-dwelling species (Aporrectodea caliginosa). Furthermore, we collected earthworms from the field site to compare their body residues to those from worms in the laboratory experiments. In the field, the worms may avoid the most polluted spots, and VOL. 39, NO. 1, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Model predictions for body residues against time in a system where the organism is depleting the bioavailable phase (left), uptake is limited by slow desorption (middle), and with rapid degradation or sequestration during the experiment (right). Three stages are shown: (1) accumulation, (2) elimination, and (3) accumulation reusing the soil with fresh worms.
TABLE 1. Soil Characteristics of the Three Locations Sampled (Average of Two Replicates)a soil properties soil property
soil 1
soil 2
soil 3
organic carbon content (Foc) (g OC/gdwt soil) pH (KCl) WHC50 (g water/gdwt soil) clay content e 2 µm
0.044
0.066
0.085
7.7 0.30 na
7.7 0.50 na
7.5 0.53 24.3
chemical
log Kow
soil 1
soil 2
soil 3
telodrin dieldrin HexaCB PCB 95 PCB 110 PCB 149 PCB 153 PCB 179 PCB 138 PCB 174 PCB 180
5.2 5.4 5.73 6.69 6.84 7.3 7.53 7.68 7.45 7.83 8.06
3.6 39 0.9 na 0.3 0.4 0.5 0.7 0.5
