Association between cadmium and calcium uptake and distribution during the moult cycle of female shore crabs, Carcinus maenas: an in vivo study
Introduction
The exact mechanism for transepithelial uptake of cadmium in aquatic organisms is still not understood (Wright, 1995). However, evidence exists for an interaction between cadmium and the calcium uptake pathway: The ionic radii of cadmium (0.97 Å) and calcium (0.99 Å) are almost identical and it has been suggested that Cd2+ ions transverse the apical gill epithelium via Ca2+-channels in aquatic animals (Verbost et al., 1989, Lucu and Obersnel, 1996, Pedersen and Bjerregaard, 2000). Cadmium uptake was shown to be inhibited by external lanthanum, an unspecific calcium-channel blocker (Weiss, 1974), in crustacea (Borowitz and McLaughlin, 1992, Pedersen and Bjerregaard, 1995, Pedersen and Bjerregaard, 2000, Lucu and Obersnel, 1996), molluscs (Roesijadi and Unger, 1993, Sidoumou et al., 1997, Vercauteren and Blust, 1999), aquatic insects (Craigh et al., 1999) and fish (Verbost et al., 1987a, Verbost et al., 1989, Perry and Flick, 1988, Block and Pärt, 1992, Wicklund Glynn et al., 1994).
The speciation of cadmium in seawater determines the bioavailability of the metal. Cadmium occurs primarily in the form of chloro-complexes in the seawater (Mantoura et al., 1978). The free hydrated Cd2+ ions are usually considered to be the dissolved form of the metal available for uptake (Sunda et al., 1978, Engel and Fowler, 1979). Changes in salinity of the seawater will therefore change the concentration of bioavailable cadmium by changing the availability of metal-binding ligands (Rainbow, 1997). A reduction in salinity will, however, result in a decrease in external calcium concentration, and therefore a change in the competition between cadmium and calcium for the calcium-channels in the apical gill epithelium cells. In agreement with the above, studies have shown that cadmium uptake by the gills is dependent on the external calcium concentration in intermoult Carcinus maenas (Wright, 1977a, Bjerregaard and Depledge, 1994), intermoult Carcinus mediterranus (Lucu and Obersnel, 1996) the freshwater amphipod Gammarus pulex (Wright, 1980), the marine gastropod Littorina littorea (Bjerregaard and Depledge, 1994), and in the teleost Phoxinus phoxinus (Wicklund Glynn and Runn, 1988).
The calcium uptake rate across the gill epithelium in crustaceans varies between species, with availability of calcium, and with the physiological requirement for calcium (Wheatly, 1996, Wheatly et al., 2002, Ahearn et al., 2004). To allow growth in decapods, the exoskeleton is shed periodically (Passano, 1960). In this process (moult), a large proportion of the total calcium content of the crabs is lost. Marine crabs in the postmoult stages, therefore, markedly increase their branchial uptake of calcium to ensure calcification of the new exoskeleton (Neufeld and Cameron, 1993). This large calcium influx found in postmoult crabs, makes crabs in this stage an advantageous model organism in which to study the possible uptake of cadmium via the calcium pathway. Previous in vivo experiments have demonstrated an increased cadmium accumulation in the tissues of male and female shore crabs C. maenas in the postmoult stages compared to premoult and intermoult crabs, when exposed to cadmium in the seawater (Wright, 1977b, Bondgaard et al., 2000, Nørum et al., 2004). Nørum et al. (2004) demonstrated that the cadmium influx rate was increased across isolated perfused gill epithelia from postmoult C. maenas compared to intermoult crabs. The crabs in the latter study were manipulated into moulting through injections of the moulting hormone 20-hydroxy-ecdysone.
The aim of the present study was to perform an in vivo investigation of the relationship between calcium and cadmium uptake in female postmoult C. maenas, which had moulted naturally. Finally, the differential fates of the metals, subsequent to internalisation at different stages during the moult cycle were studied.
Section snippets
Experimental animals
Adult, female shore crabs C. maenas weighing from 7 to 30 g were caught in August and September 1999, in Kerteminde Harbour, Funen, Denmark, at salinities varying from 10 to 28‰ and ambient water temperatures ranging from 15 to 22 °C. The crabs were kept in the laboratory, at the Research Centre for Aquatic Biology, Kerteminde, in tanks with running seawater, for at least two days under a 12 h light:12 h dark regime before being used in experiments. The female postmoult crabs used in the
Exp 1. Uptake of 109Cd and 45Ca in postmoult and intermoult crabs
The concentration of 45Ca in the haemolymph of postmoult crabs increased after 1 h to significantly higher levels than in intermoult crabs (C3 and C4) (Fig. 1A). Accordingly, the net influx of stable calcium was significantly higher at the postmoult stage than the intermoult stages (C3–C4) (Table 1). During the 24 h of exposure, the C3-crabs continuously accumulated 45Ca in the haemolymph to a higher concentration than C4-crabs (Fig. 1A).
The concentration of 109Cd in the haemolymph of intermoult
Discussion
The present study presents evidence of highly increased cadmium uptake in vivo in female postmoult shore crabs (C. maenas) compared to intermoult crabs. The studies also indicate that cadmium uptake in postmoult crabs occur via calcium-transporting proteins in the apical membrane of gill epithelium cells. When calcium and cadmium were injected, however, large differences in the tissue distribution between the metals were observed. This distribution was, furthermore, shown to change with the
Acknowledgements
We thank Mrs V. Eriksen for technical assistance and Dr. Ulrik Nørum for critical comments to the manuscript. This work was supported by grants from the Danish National Science Research Council.
References (59)
- et al.
Calcium regulation in crustaceans during moult cycle: a review and update
Comp. Biochem. Physiol.
(2004) Interaction between selenium and cadmium in the hemolymph of the shore crab Carcinus maenas (L.)
Aquat. Toxicol.
(1988)- et al.
Uptake of 109Cd by cultured gill epithelial cells from rainbow trout (Oncorhynchus mykiss)
Aquat. Toxicol.
(1992) - et al.
A survey of the fine structure of the integument of the fiddler crab
Tissue Cell.
(1972) Uptake of calcium at the postmoult stage by the marine crabs Callinectes sapidus and Carcinus maenas
Comp. Biochem. Physiol.
(1983)- et al.
The complexation of metals with humic materials in natural waters
Estuar. Coast. Mar. Sci.
(1978) - et al.
The kinetics of zinc and cadmium in the haemolymph of the shore crab Carcinus maenas (L.)
Aquat. Toxicol.
(1998) Molting and its control
- et al.
Calcium and cadmium fluxes across the gills of the shore crab, Carcinus maenas
Mar. Pollut. Bull.
(1995) - et al.
Cadmium influxes and efflux across perfused gills of the shore crab, Carcinus maenas
Aquat. Toxicol.
(2000)
Ionic regulation in the crab Carcinus maenas (L.) in relation to the moulting cycle
Comp. Biochem. Physiol.
Nanomolar concentrations of Cd2+ inhibit Ca2+ transport systems in plasma membranes and intracellular Ca2+ stores in intestinal epithelium
Biochim. Biophys. Acta
Calcium homeostasis in crustaceans: subcellular Ca dynamics
Comp. Biochem. Physiol.
Differences in uptake of inorganic mercury and cadmium in the gills of zebrafish, Brachydanio rerio
Aquat. Toxicol.
Trace metal and major ion interactions in aquatic animals
Mar. Pollut. Bull.
Regulation of blood ions in Carcinus maenas (L.)
Comp. Biochem. Physiol.
Proecdysis, setal development, and molt prediction in the American lobster (Homarus americanus)
J. Fish. Res. Board Can.
Effects of cadmium on hemolymph composition in the shore crab Carcinus maenas
Mar. Ecol. Prog. Ser.
Effects of copper on ion- and osmoregulation in the shore crab Carcinus maenas
Mar. Biol.
Influence of physiological condition on cadmium transport from haemolymph to hepatopancreas in Carcinus maenas
Mar. Biol.
Cadmium accumulation in Littorina littorea, Mytilus edulis and Carcinus maenas: the influence of salinity and calcium ion concentrations
Mar. Biol.
Trace metal concentrations and contents in the tissues of the shore crab Carcinus maenas: effects of size and tissue hydration
Mar. Biol.
Cadmium accumulation in the female shore crab Carcinus maenas during the moult cycle and ovarian maturation
Mar. Biol.
Evidence for calcium channels in brine shrimp: Diltiazem protects shrimp against cadmium
Bull. Environ. Contam. Toxicol.
Experimental evidence for cadmium uptake via calcium channels in the aquatic insect Chironomus staegeri
Aquat. Toxicol.
Mue et cycle d’intermue chez les Crustacés Décapodes
Ann. Inst. Océanogr. Monaco.
Sur la méthode de détermination des stades d’intermue et son application générale aux crustacés
Vie Milieu Ser. A, Biol. Mar.
Factors influencing cadmium accumulation and its toxicity to marine organisms
Environ. Health Perspec.
The biological chemistry of the elements: the inorganic chemistry of life
Cited by (55)
Endocrine disruption in crustaceans: New findings and perspectives
2024, Molecular and Cellular EndocrinologyEndocrinology
2023, Ecophysiology of the European Green Crab (Carcinus Maenas) and Related Species: Mechanisms Behind the Success of a Global InvaderEffects of pile driving sound playbacks and cadmium co-exposure on the early life stage development of the Norway lobster, Nephrops norvegicus
2022, Marine Pollution BulletinCitation Excerpt :If this was the case, it would suggest that chronic exposure led to continued accumulation of cadmium in Nephrops with limited ability to depurate. Permeability to, and absorption of cadmium is also likely greater in recently moulted individuals as seen in the shore crab Carcinus maenas (Bondgaard and Bjerregaard, 2005). Correspondingly, it may be that the process of moulting effectively results in short-term concentration of cadmium in soft tissues, which are known to accumulate metals in Nephrops.
Ecotoxicology of metals-sources, transport, and effects on the ecosystem
2021, Handbook on the Toxicology of Metals: Fifth EditionEffect of size on concentrations and cadmium inducibility of metallothionein in the shore crab Carcinus maenas
2021, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyEcotoxicology of metals-sources, transport, and effects on the ecosystem
2021, Handbook on the Toxicology of Metals: Volume I: General Considerations