The cytology of heavy metal accumulations in the digestive glands of three marine gastropods

Abstract

In the digestive glands of gastropod molluscs, metals are metabolized in the sense that they are subject to inorganic biochemical processes within the epithelial cells and lumen of the digestive tubules and the pore cells in the intervening connective tissue. These systems have been examined in the tower shell Cerithium vulgatum Bruguieres, a sediment feeder, the top shell Monodonta articulata Lam., a grazing herbivore, and in the whelk Murex trunculus L., a carnivore whose prey includes Cerithium . These animals were taken from a Mediterranean environment polluted by heavy metals. In all three species the metals are compartmentalized within mineralized granules as phosphates and within lysosomal residual bodies in association with sulphur. However, the extent to which a particular metal is accumulated and the relative proportions that are bound within the different compartments are factors that are primarily determined by the species and not the concentration available in the environment. Thus Cerithium accumulates high concentrations of a wide range of metals from the ingested sediment and these are rendered insoluble and non-toxic in the digestive gland. This unavailability is transferred to Murex when it eats Cerithium because Murex does not accumulate the full range of metals from its prey. Indeed, for some metals there appears to be bioreduction rather than bioamplification. The grazing herbivore Monodonta articulata accumulates a third distinct spectrum of metals. The accumulations in each species do not reflect the levels of all the metals in the environment. The presence of metals in the digestive glands is associated with the removal of magnesium from the phosphate granules but also with an increase in the concentration of magnesium in the tissue. It is proposed that metals induce the formation of magnesium phosphate as a source of metal-binding phosphate ions.

Metals and marine food chains

“…The digestible fraction is transferred into a major diverticulum called the hepatopancreas or digestive gland, where digestion and absorption take place; the indigestible fraction continues along the gut via the intestine and hindgut for elimination in faecal pellets. This biphasic process also takes place in gastropod molluscs and is obvious in the sediment-feeder Cerithium vulgatum; particles of silica, clay and calcium carbonate pack the fore-, mid-and hindgut and faecal pellets but the digestive gland contains only organic material that has been separated from the sediment (Nott and Nicolaidou, 1989a) C. vulgatum in polluted situations accumulates levels of zinc approaching 3500 IJ.g g-l dry weight in the viscera (assumed to be similar to digestive gland) compared with levels that are two orders of magnitude less in the muscle tissue Nott, 1989, 1990). The level of zinc in the digestive gland can reach more than 15500 IJ.g g-l (Nott and Nicolaidou, 1989a).…”

“…This biphasic process also takes place in gastropod molluscs and is obvious in the sediment-feeder Cerithium vulgatum; particles of silica, clay and calcium carbonate pack the fore-, mid-and hindgut and faecal pellets but the digestive gland contains only organic material that has been separated from the sediment (Nott and Nicolaidou, 1989a) C. vulgatum in polluted situations accumulates levels of zinc approaching 3500 IJ.g g-l dry weight in the viscera (assumed to be similar to digestive gland) compared with levels that are two orders of magnitude less in the muscle tissue Nott, 1989, 1990). The level of zinc in the digestive gland can reach more than 15500 IJ.g g-l (Nott and Nicolaidou, 1989a). If the weight of the digestive gland is c. 5-10% of the total body weight Nott and Nicolaidou, 1994.…”

“…In the Mediterranean, three species of marine snail living in the same seawater adjacent to a nickel smelting plant accumulate markedly different levels of metals (Nott and Nicolaidou, 1989a). The highest levels occur in the sediment feeder Cerithium vulgatum and the lowest levels in the predator Murex trunculus, which preys on C. vulgatum.…”

Effect of lead and cadmium ions upon the pupariation and morphological changes in Calliphora vicina (Diptera, Calliphoridae)

“…Among soil micro-Arthopoda, assessment has been made of the effect of heavy metals upon Collembola, which are widely used as biological indicators (Huhta et al, 1979;Hagvar, 1982;Faber and Heijmans, 1997;Van Straalen, 1997). The effect of heavy metal pollution has also been well studied for earthworms (Lumbricidae) (Ireland, 1983;Emmerling et al, 1997;Heikens et al, 2001;Nahmani et al, 2003;Tischer, 2009;Kulbachko et al, 2014), gastropods (Gastropoda) (Nott and Nicolaidou, 1989;Greville and Morgan, 1990;Berger and Dallinger, 1993;Presing et al, 1993;Triebskorn and Köhler, 1996), chironomid larvae (Diptera, Chironomidae) (Mackie, 1989;Westcott and Kalff, 1996), and Drosophilidae (Bahadorany and Hilliker, 2009;Safaee et al, 2014). Accumulation of heavy metals in an insect organism can affect its development.…”

Contribution of X-Ray Spectroscopy to Marine Ecotoxicology: Trace Metal Bioaccumulation and Detoxification in Marine Invertebrates

“…In both cases, common cellular structures involved in metal sequestration are requested (Jeantet et al, 1997). Cells have various biological ligands, such as metalloproteins, to which metals can bind, on the one hand, and their organites (ie lysosomes, endoplasmic reticulum) are involved in metal sequestration (Ballan-Dufrançais, 1975;Brown, 1982;Mason & Jenkins, 1995;Nott & Nicolaidou, 1989a;Simkiss & Taylor, 1995;Raimundo et al, 2008;Simkiss & Masson, 1983). Total metal body burden may reflect the presence of inert particles www.intechopen.com Ecotoxicology 2 mineralized (the so-called granules) within tissues and cells which are no longer involved in metabolism.…”