Bioaccumulation of Polycyclic Aromatic Hydrocarbons by Earthworms: Assessment of Equilibrium Partitioning Theory in in Situ Studies and Water Experiments

Abstract

Abstract-The purpose of this study was to assess the suitability of applying equilibrium partitioning (EqP) theory to predict the bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) by earthworms when these are exposed to contaminated soils in the field. Studies carried out in situ in various contaminated floodplain sites showed the presence of linear relationships with intercept zero between the lipid-normalized concentration of different PAHs in the earthworm Lumbricus rubellus and the organic-matternormalized concentration of the compounds in soil. The demonstration of such an isometric relationship is in agreement with the prediction of EqP theory that the biota-soil accumulation factor (BSAF) should be independent of the octanol/water partition coefficient, log K ow . The average BSAF of PAH compounds in the sampled 20-cm top layer of soil was 0.10 (range, 0.03-0.26). The present study also investigated the route of uptake of PAHs for earthworms in soil. The bioconcentration factor of lowmolecular-weight PAHs, such as phenanthrene, fluoranthene, and pyrene, was derived from bioconcentration kinetic modeling of water-only experiments and found to be of the same order of magnitude as the bioaccumulation factor in the field when the latter was normalized to calculated concentrations in soil pore water. The results indicated that the exposure of earthworms to PAHs in soil is mediated through direct contact of the worms with the dissolved interstitial soil-water phase, further supporting the applicability of EqP theory to PAHs. Our experimental data on the biotransformation of PAHs suggest that earthworms possess some capacity of metabolization, although this does not seem to be a major factor in the total elimination of these compounds. Even though the EqP approach was found to be applicable to low-molecular-weight PAHs with respect to the prediction of bioaccumulation by earthworms in the field, the results were less conclusive for high-molecular-weight compounds, such as benzo [a]pyrene.

The author's reply

“…Dolfing and Bril [1] have made the interesting suggestion that the intersite variation in the biota‐soil accumulation factor (BSAF) for polycyclic aromatic hydrocarbons (PAHs) in earthworms as described in our study [2] can be attributed to variations in clay content (fraction <2 μm) and pH. They hypothesize that clay enhances the bioavailability of PAHs to earthworms by influencing the sorption of these compounds to organic matter or, as another possibility, that PAHs sorbed to clay are more bioavailable.…”

Bioaccumulation factors as a function of soil characteristics

“…The equilibrium partitioning theory [1] states that the biota‐soil accumulation factor (BSAF) of organic chemicals is independent of the octanol/water partitioning coefficient ( K ow ). Ma et al [2] recently presented a valuable dataset that fully supports this theory. In a series of field studies, these authors measured the bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) by earthworms and concluded that “The partitioning of PAHs between the worm lipid phase and soil organic carbon conformed to a linear relationship with intercept zero.…”

“…This suggests that the soil properties of the different sites affected the BSAF. We were surprised, and indeed challenged, by the statement of Ma et al [2] that no significant correlations were present between the BSAF and the soil properties measured, which included pH (KCl), CaCO 3 and soil organic matter (SOM) content, and grain‐size fractions (Table 1). Linear regression on the (log of) the four soil parameters listed in Table 1 indeed did not yield meaningful results (e.g., Fig.…”

“…In a series of field studies, these authors measured the bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) by earthworms and concluded that “The partitioning of PAHs between the worm lipid phase and soil organic carbon conformed to a linear relationship with intercept zero. The presence of such an isometric relationship indicates that the BSAF can be considered a constant for compounds with varying log K ow values” [2].…”

Rhizoremediation of petroleum hydrocarbons: a model system for plant microbiome manipulation

“…Earthworms are typical soil inhabitants making up > 80% of the biomass of soil macrofauna (Yasmin and D'Souza, ), and are frequently found in the rhizosphere environment (Springett and Gray, ). Earthworms can survive in the most highly contaminated soils as only water soluble compounds can be absorbed through their skin (Jager, ), which excludes most toxic PAHs (Ma et al ., ) and PCBs (Beyer and Stafford, ). For instance, Zavala‐Cruz et al .…”