Morphological plasticity in metal-sequestering earthworm chloragocytes: morphometric electron microscopy provides a biomarker. of exposure in field populations.

Abstract

Morphometric measurements of the volume fractions (Vv) of two prominent metal-sequestering compartments, chloragosome granules and debris vesicles, were made on transmission electron micrographs of chloragocytes in Dendrodrilus rubidus (Annelida: Oligochaeta: Lumbricidae) from one uncontaminated site and three qualitatively and quantitatively different metalliferous soils associated with disused Pb/Zn mines. We also examined the relative volume fractions of the alimentary wall and attached chloragogenous tissue by light microscopy. Several conclusions relevant to environmental diagnostics were reached: Metal identity and degree of soil pollution exert strong effects on chloragocyte ultrastructure; morphometry by light microscopy indicated that the metal-induced structural effects are characterized by intracellular alterations not accompanied by a significant expansion of the tissue volume; elevated metal burdens can reduce chloragosome Vv and, concomitantly, increase the Vv of their autophagic derivatives, the debris vesicles; the measured cellular alterations were more closely correlated with integrated tissue metal burdens than they were with integrated soil metal burdens; and estimates of tissue metal distribution, derived by combining morphometric data and published whole-worm and chloragosome metal concentrations, suggested that the alimentary wall of earthworms may sequester Pb, Zn, and Cd. Our study shows that cellular changes, directly or indirectly, may yield quantifiable expressions of metal loads bioaccumulated by earthworms. However, the practical use of cellular changes as biomarkers of soil quality probably will require automated light-microscopic morphometry in combination with organelle-specific molecular probes to be cost effective.