Quantitative Ultrastructure of Metal-Sequestering Cells Reflects Intersite and Interspecies Differences in Earthworm Metal Burdens

Abstract

Morphometric analysis of transmission electron micrographs was used to compare the effects of metals on the multifunctional, metal-sequestering, chloragocyte cells of two epigeic earthworm species, Dendrodrilus rubidus and Lumbricus rubellus, inhabiting three field soils: a clean circumneutral reference soil (Dinas Powys); an acidic moderately Pb- and Zn-contaminated soil (Cwmystwyth); and a calcareous Cd-, Pb-, and Zn-contaminated soil (Draethen). The main findings were: (1) D. rubidus accumulated significantly higher tissue Cd and Pb and lower Zn concentrations than L. rubellus, especially at Draethen; (2) the volume fraction of chloragosomes was significantly lower and the volume fraction of debris vesicles significantly higher in D. rubidus from Draethen compared with L. rubellus at all sites and with the other two D. rubidus populations; (3) estimated relative toxicity factors, derived from soil metal concentrations and published EC50 data, suggested that the subcellular changes in chloragocytes, particularly in D. rubidus from Draethen, were caused mainly by Zn and Pb exposures; (4) scrutiny of the body burdens of each metal in both worm species across the three sites indicated that Cd was a major contributor to the structural changes observed in Draethen D. rubidus, and its impact was disproportionate to its soil and tissue concentrations in comparison with those of Pb and Zn. The apparent greater susceptibility of D. rubidus cells, compared with L. rubellus cells, to soil metal contaminants is discussed in light of differences in the quality and quantity of the metal body burdens accumulated by the two species. Further histopathalogic and morphometric studies on key organs and tissue of earthworms are required to provide biomarkers of exposure and to underpin linkage of biochemical-level changes and demography.