The distribution and intracellular compartmentation of metals in the endogeic earthworm Aporrectodea caliginosa sampled from an unpolluted and a metal-contaminated site

Abstract

The tissue distribution of Cd, Cu, Pb, Zn and Ca in the endogeic earthworm Aporrectodea caliginosa living in a non-polluted and a heavy metal polluted soil was investigated. The tissues of animals from the contaminated soil contained greater concentrations of Cd, Pb and Zn than the corresponding tissues of animals from the unpolluted soil. The greatest concentrations of Cd, Pb, Zn, and Ca were primarily accumulated within the posterior alimentary canal (PAC), a tissue fraction which contained the greatest proportion of the whole-worm burdens of the respective metals. Cu was distributed fairly evenly in the tissue fractions investigated. The pattern of accumulation for the ‘heavy’ metals is broadly similar to that for epigeic earthworms; in contrast, a different pattern of tissue accumulation was found for Ca. In animals from the uncontaminated site, the major elemental constituents of the chloragosomes were P, Ca, Zn and S. A significant positive correlation exists between P and Ca within the chloragosomal matrix. These intracellular vesicles are major foci for Pb and Zn accumulation within the PAC, with ‘excess’ metals associated with P ligands within the chloragosome matrix. The incorporation of Pb and Zn appears to involve the cationic displacement of Ca. Such compartmentation appears to prevent dissemination of large concentrations of these metals into other earthworm tissues, and may thus represent a detoxification strategy based on accumulative immobilization. No intracellular localization of Cd was identified in the study, although the Cd concentration in the metalliferous soils examined was not exceptionally high. The observations are discussed in the context of a contribution to enhanced understanding of metal ecotoxicology in earthworms by providing baseline data on a little investigated ecophysiological group of earthworms. Comparisons of metal distribution and mechanisms of metal sequestration are made with other ecophysiological groups of earthworms, and the significance of the findings to biomonitoring and toxicity-testing programmes is considered.