Metal Accumulation and Homeostasis in Antarctic Molluscs

The capability of marine molluscs to tolerate and accumulate metals and other persistent contaminants is well known. Since the 1970s, mussels and oysters have been used extensively around the world as bioaccumulators of contaminants for long-term monitoring of coastal marine waters within the context of"Mussel Watch"programmes (e.g. NAS 1980; Lauenstein et al. 1990). A number of papers have been published on metal accumulation in Antarctic molluscs (e.g. Mauri et al. 1990; Berkman and Nigro 1992; Ahn et al. 1996;

Lohan et al. 2001). These studies have generally revealed that several species of Antarctic molluscs meet most criteria defined in "Mussel Watch" programmes, and that the accumulation pattern of contaminants in their organs and tissues is similar to that in related species from other seas. The main difference between the elemental composition of Antarctic bivalves and that of related species from unpolluted environments in other seas is the huge accumulation of Cd in the digestive gland and kidney of Antarctic molluscs. Nigro et al. (1997) also found a remarkable accumulation of some elements, particularly As (up to 394 |g g-1 dry wt.), in the gills and digestive gland of another Antarctic bivalve (Yoldia eightsi). There are other reports on As accumulation in marine bivalves - Benson and Summons (1981), for instance, measured up to 1,025 |g g-1 dry wt. of As in giant clams from the Greet Barrier Reef.

Among Antarctic molluscs, circumpolar filter-feeding bivalves such as Adamussium colbecki and Laternula elliptica or the Antarctic limpet Nacella concinna (which occurs in intertidal and shallow subtidal zones around the Antarctic Peninsula and adjacent islands) are the species most frequently indicated as useful biomonitors of environmental contaminants in coastal ecosystems. L. elliptica is one of the most studied species (e.g. Ahn et al. 1996; Nigro et al. 1997; Vodopivez and Curtosi 1998; Lohan et al. 2001). In shallow, sheltered areas this deep-burrowing, large-sized bivalve (shell>10 cm long) may occur in dense patches (>100 individuals m-2); it lives for more than 15 years and lays down distinct annual growth bands (Brey and Mackensen 1997). As a part of the biomonitoring campaign linked to the Bahia Paraiso sinking, Kennicutt et al. (1991) found that the total PAH content in L. elliptica samples collected near the wreck was 17,500 ng g-1 dry wt., while that in samples from central Arthur Harbor was 1,200 ng g-1 dry wt. In McMurdo Sound, Kennicutt et al. (1995) found that PCB concentrations in tissues of L. elliptica from Winter Quarters Bay and the sewage outfall (about 400 ng g-1) were 20-80 times higher than in clams from more remote sites. Low concentrations of others POPs such as DDT and its derivatives, HCH, HCB and a-chlordane were also detected in molluscs from more polluted zones. Compared to tissue extracts from clams collected at remote sites of McMurdo Sound, those from L. elliptica in Winter Quarters Bay exhibited higher EROD (P4051A1-depen-dent ethoxyresorufin-O-deethylase) induction activity in rat hepatoma H4IIE cells (McDonald et al. 1994). Additionally, there was an excellent linear correlation between induced EROD activity versus total PCB levels. This result indicated the complementary nature of analytical and bio-analytical data. Furthermore, the assay provided a method for estimating TCDD toxic equivalents in extracts from marine organisms.

For its size, geographical distribution and biomass, the Antarctic scallop A. colbecki is one of the most conspicuous mollusc species in Antarctica. This suspension-feeder species has a wide bathymetric distribution and, in the inner shelf of the Ross Sea, it constitutes an important food source for benthic fish such as Trematomus bernacchii and invertebrate top predators (e.g. the gastropod Neobuccinum eatoni and the nemertine Paraborlasia corrugatus; Vacchi et al. 2000b). There are many studies on the ecophysiology (e.g. Dell 1972; Stockton 1984; Heilmayer et al. 2003) and elemental composition of A. colbecki (e.g. Mauri et al. 1990; Berkman and Nigro 1992; Viarengo et al. 1993; Nigro et al. 1997). Like in other Antarctic organisms, the increase in food availability during the austral summer determines the growth of its digestive gland and other organs, with a consequent "dilution" effect on trace element concentrations. However, there is evidence that Cd accumulates very efficiently in the digestive gland of A. colbecki and that its content does not vary during summer (Nigro et al. 1997). The huge bioaccumulation of Cd and other potentially toxic metals in the digestive gland of molluscs is made possible by several efficient detoxification mechanisms such as compartmentalisation within lysosomes, accumulation of metals into granules and/or membrane-bound vesicles, and binding of metals to specific ligands such as metalloth-ioneins (Viarengo et al. 1993). Metal storage sites also occur in the kidney of A. colbecki. Nigro et al. (1992) found concretions containing Fe, Zn and Cu in the main vacuole of the renal cell; Ag/Se-rich particles and other electron-dense particles containing Fe, Cu and other metals were found in the basal membrane and in amoebocytes. These findings suggest transport of trace elements from uptake to excretion/storage sites.

Metallothioneins are soluble, low-molecular weight, cysteine-rich proteins. Metal ions within cells cause their rapid neosynthesis by enhancing metallothionein gene transcription (Squibb and Cousin 1977). Metalloth-ioneins have been reported not only in molluscs but also in many other Antarctic organisms such as the sea urchin S. neumayeri and several species of fish (e.g. Scudiero et al. 1997; Carginale et al. 1998). The cysteine content in cadmium-induced metallothionein from the digestive gland of A. colbecki (Ponzano et al. 2001) is lower than that in metallothioneins purified from vertebrates and invertebrates in other seas. In addition to metallothioneins, many other biochemical markers can be used as biological indices of exposure to or of the effects of contaminants in molluscs. The enhancement of reactive oxygen species (ROS) has often served as a general pathway of tox-icity induced by pollutants and oxidative stress (Winston 1991). Cells have evolved low-molecular scavengers and antioxidant enzymes for detoxification and removal of ROS and other oxidant molecules. Glutathione is one of the most important antioxidant agents, and variations in the content of glu-tathione and in the activity of glutathione-dependent and antioxidant enzymes are potential biomarkers of contaminant-mediated oxidative stress in several marine organisms (e.g. di Giulio et al. 1989; Viarengo et al. 1990; Regoli and Principato 1995). Cold Antarctic seawater has higher levels of dissolved oxygen, and research has shown that catalase activity and other antioxidants in A. colbecki are enhanced compared to those of the Mediterranean scallop Pecten jacobaeus (Regoli et al. 1997). Further comparative studies with the Arctic scallop Chlamys islandicus (which during summer experiences higher water temperatures than in the Southern Ocean) showed that A. colbecki has the highest scavenging capacity for peroxyl and hydroxyl radicals. These results indicate a possible biochemical adaptation of the Antarctic scallop to high levels of dissolved oxygen in Southern Ocean waters (Regoli et al. 2000).

7.4.2 Antarctic Fish and the Transfer of Contaminants to Higher Vertebrates

Unlike shelf waters in the other continents, the Antarctic shelf is dominated by a single suborder of fish (notothenioids), and most benthic and epibenthic species are notothenioids belonging to the genus Trematomus (e.g. T. bernac-chii, T.pennellii, T.scotti, T.hansoni). These species are usually considered cir-cum-Antarctic benthic feeders, and their diet consists of polychaetes, amphipods, fish eggs, molluscs and other epibenthic organisms, depending on availability (Kiest 1993; Hureau 1994; Vacchi et al. 1994). Epibenthic notothenioids such as T. newnesi and T. loennbergii mainly feed on zooplankton (hyperiids, copepods and euphausiids), fish, benthic polychaetes and gammarids (Gon and Heemstra 1990; Ekau 1991). Nototheniids also include a few pelagic species such as Pleuragramma antarcticum and species living on the undersurface of ice (e.g. Pagothenia borchgrevinki). Besides notothe-nioids, Antarctic waters contain plunderfish, dragonfish and icefish (about 50 species), which are mostly pelagic or semipelagic and prey on crustaceans and fish (Eastman 1993). Icefish, one of the most unusual groups of fish in the world (they lack haemoglobin and are white-blooded) have low concentrations of Fe; in the kidney and liver of the widespread species Chionodraco hamatus, Fe content is three to four times lower than that in the liver and kidney of red-blooded Antarctic fish (Bargagli 2001).

The feeding behaviour of notothenioids at Terra Nova Bay is somewhat reflected in the Cd and Hg concentrations in their organs and tissues. Benthic feeders (T. bernacchii and T. hansoni) have higher body burdens of heavy metals than epibenthic (T. newnesi) or semipelagic fish (C. hamatus). The latter two species mainly feed on copepods and euphausiids, which have lower Cd and Hg concentrations than many species of benthic invertebrates. At Terra Nova Bay A. colbecki and other molluscs are frequently included in the diet of T. bernacchii (Vacchi et al. 2000b), and this helps explain why this species, compared to other notothenioids, has the highest concentration of metals in the liver and accumulates 2-3 times more Hg in the muscle tissue. Minganti et al. (1995) reported Hg concentrations in A. colbecki and T. bernacchii which match those in Fig. 47, and showed that up to 96 % (median 80 %) of total Hg in the muscle of T. bernacchii was MeHg; in the liver, kidney and gonads this percentage was usually less than 50 %. Mercury concentrations in the fish muscle were significantly correlated with body weight. Carginale et al.

Fig. 47. Average trace metal concentrations (|g g-1 dry wt., mean±SD) in different organs and tissues of ben-thic, epibenthic, and semipelagic fish from Terra Nova Bay. (Bar-gagli 2001)

Fig. 47. Average trace metal concentrations (|g g-1 dry wt., mean±SD) in different organs and tissues of ben-thic, epibenthic, and semipelagic fish from Terra Nova Bay. (Bar-gagli 2001)

(1998) found that T. bernacchi contained higher levels of metallothionein than species of white-blooded fish collected in the same marine area. The only low-molecular weight, Zn-binding protein in the liver of icefish was a protein with a low cysteine content and rich in amino acid residues, whereas the predominant metal-binding protein in the red-blooded T. bernacchii was a met-allothionein with molecular characteristics similar to those of rat metalloth-ionein. Santovito et al. (2000) studied the bioaccumulation of Cd, Cu and Zn in different tissues of T. bernacchii and C. hamatus and found that the hepatic content of metallothioneins correlated positively only with Cd concentrations.

Trematomus bernacchii is an ideal bioindicator of local contamination because it not only has metal detoxification and accumulation capabilities, but it also has restricted home ranges and is ubiquitous. Indeed, this species spends much time in restricted areas; for example, some marked individuals released in February 1990 from a coastal site at Terra Nova Bay were recovered at the same site 2 years later. Trematomus bernacchii also has been used as a bioindicator of POPs in marine ecosystems adjacent to scientific stations such as McMurdo (Larsson et al. 1992; Kennicutt et al. 1995), Terra Nova Bay (Focardi et al. 1992a, 1995a; Bargagli et al. 1998d) and Syowa (Subramanian et al. 1983). Comparisons among the results of these studies are difficult because some refer to the whole body content, while others refer to different tissues and/or are expressed on different mass bases. In general, DDTs, PCBs, PAHs and other POPs have always been detected; average concentrations were in the same range as those previously reported for krill and were significantly lower than those usually detected in fish from other seas. Concentrations of three highly toxic non-ortho coplanar PCB congeners (77,126 and 169) were always extremely low (<0.5 pg g-1 wet wt.) in the muscle tissue of T. bernacchi from Terra Nova Bay (Bargagli et al. 1998d). Microsomal CYP4501A-dependent monooxygenase activity was evaluated in the liver of the same samples by EROD, BROD (benzyloxyresorufin-O-deethylase) and BPMO (benzo-a-pyrene) assays; values were slightly higher in samples from a small cove receiving wastewater from the Italian station. Experiments to evaluate the induction of the cytochrome P450 monooxygenase system by PCBs and benzopyrene (Focardi et al. 1992b, 1995b) in T. bernacchi and other species of Antarctic fish showed that, owing to slow metabolic rates, the highest levels of induction occurred after 10 days (i.e. much later than in fish from temperate seas). Miller et al. (1999) measured directly CYP1A mRNA levels (a more sensitive and accurate biomarker than measurements of enzymatic activity) in the liver of T. bernacchi from Winter Quarters Bay and a remote site in McMurdo Sound. They found an average 37-fold increase in CYP1A expression, and two-fold higher levels of naphthalene and phenanthrene in bile samples from fish collected at the polluted site. The extent of CYP1A induction correlated positively with the content of aromatic compounds in bile samples from the same fish. High average concentrations of PAH metabolites were also measured in the bile of Notothenia coriiceps samples collected near Palmer Station and the Bahia Paraiso wreckage (McDonald et al. 1992). The latter species is one of the most abundant fish at depths of 0-450 m along the Antarctic Peninsula, the Scotia Arc, and the South Georgia, Bouvet and Pedro I islands (Kock 1989). Analysis of organochlorine compounds in fish species from the peninsula (Weber and Goerke 1996) showed that HCB concentrations (20 ng g-1 wet wt.) were as high as those in Limanda limanda from the North Sea, and bioaccumulation was attributed to the cold-condensation process. Levels of DDT and PCB congeners (153, 138 and 180) were from one to two orders of magnitude lower than in North Sea fish. However, POPs in samples from the Antarctic Peninsula generally increased between 1987 and 1991.

The Antarctic silverfish (Pleuragramma antarcticum) is the most important circum-Antarctic notothenioid species in terms of both number and biomass. It feeds almost exclusively on euphausiids, copepods and chaetognaths, and P. antarcticum is the only true pelagic species in the water column of most Southern Ocean shelf areas. P. antarcticum therefore plays a prominent role as the main source of food for several species of predatory vertebrates such as the Antarctic cod (Dissostichus mawsoni) and other fish, penguins (gentoo, Adelie and Emperor), South Polar skuas, Antarctic petrels, Weddell seals, crabeater seals and whales (Eastman 1993). Average PCB, HCB, and p,p'-DDE concentrations in adult P. antarcticum samples from the Ross Sea were 348, 4.85 and 2.01 ng g1 wet wt. respectively (Corsolini et al. 2002). The higher PCB content in larvae than in adults was attributed to the affinity of PCBs for suspended particles and to the greater surface:volume ratio in larvae than in adult silverfish.

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