3.5 bioaccumulation

3.5.1 general

Literature on the bioaccumulation of silver was generally inadequate. Often the ambient concentrations of silver were not reported or measured for field collected organisms. Some studies compare sites as contaminated or uncontaminated, but only assume this to be so. Silver bioaccumulates at low concentrations because most silver compounds are only sparingly soluble in water. Planktonic concentrations are correlated with water levels and benthos concentrations are correlated with sediment levels (Freeman 1977).

3.5.2 marine waters

3.5.2.1-general

Table 3.7 gives some data on the bioaccumulation of silver by marine invertebrates.
The review of silver included ambient water concentrations and speciation, ambient sediment level and complexation with organic compounds and their availability. Ambient ocean concentrations ranged from 0.04 to 2.5 µg/L silver, principally in the form of AgCl₂, while the most bioavailable form is AgCl. Sediment concentrations were usually three to five orders of magnitude greater than concentrations in the the overlying water and ranged from 0.1 to 1.0 µg/g silver.

Silver is tightly bound by sewage sludge and elevated levels of silver are often associated with sewage outfalls with minimal treatment. In the absence of sewage, silver associates with iron oxides and humic substances. The relative bioavailability of either silver-inorganic complexes or silver-organic complexes appears to depend on the individual compounds. Silver-inorganic complexes are probably the most common in the marine environment. Silver-chlorides are generally not bioavailable except for AgCl. Silver-iron oxides or silver-magnesium complexes in sediments increase the availability to bottom feeding organisms.

Silver uptake by the worm Nereis diversicolor , decreased in sediments with high humic content, but increased in sediments with high iron or magnesium concentrations. In an experiment with the clam, Macoma balthica, Harvey et al. 1985) showed that silver uptake increased if silver-iron oxide particles were coated with an extra-cellular polymer produced by bacteria commonly associated with sewage outfall areas. This is important since most high silver tissue levels observed in the field are associated with sewage outfall areas, which are areas of high bacterial activity, and would suggest that some organic complexes increase rather than decrease bioavailability. Evidence from the literature (Nelson 1978, Greig et al. 1975, 1977 and 1983, Gilfillan et al. 1985 and Robinson et al. 1985) is not conclusively in support of this theory.

Accumulation appears to occur mainly as granular deposits in the kidneys or at the basal membranes of tissues and organs and is likely not toxic to the organisms themselves nor subject to either trophic transfer or biomagnification. Although fish, invertebrates and algae can all accumulate silver, there does not appear to be magnification up the trophic food chain to top carnivores.

3.5.2.2-estuaries

In 1992 Bryan and Langston conducted a review on bioavailability of heavy metals in sediments with special reference to the estuaries. They discussed some of the processes which affect the concentrations and bioavailability of metals, such as mobilization of metals to interstitial water and chemical speciation, transformation, control exerted by major sediment components, competition between metals for uptake sites and influence of bioturbation, salinity, redox or pH on the above processes. Synergistic effects of metals were also discussed, and it was found that attributing deleterious effects of a single metal to an organism in the field is rare.

Tolerance and the induction of metal detoxification involving the formation of granules or metal binding proteins may lead to tissue concentrations which are unusually high but without deleterious effects unequivocally attributable to the metal. It was also noted that the only consistent evidence of biomagnification involves methyl mercury.

Young et al. (1981) measured silver in several marine species, commonly used as seafood, near a large municipal sewage outfall in California. It was found that fish species did not accumulate silver significantly with respect to controls. In contrast, benthic invertebrates accumulated three to five times as much silver.
3.5.2.3-molluscs

Cain and Luoma (1985), conducted an in situ study comparing silver accumulation in two populations of clams, Macoma balthica, one resident in a contaminated area, and the other transplanted from a relatively pristine area. Results indicated that accumulation of silver in the hard and soft tissues of the transplanted clams was half that of the resident population; however, the transplanted clams retained 90% of the silver accumulated, whereas in the resident clams the loss of silver from the soft tissue was equivalent to the gain. Shell closure was observed to occur earlier in the transplanted clams. Also noted were seasonal fluctuations in the levels of ambient silver, and an increased bioavailability of silver in the winter months compared to the summer months. Tissue weights changed seasonally for both populations, which was shown to bias measured tissue metal concentrations if not accounted for. This might have lead to spurious conclusions in some of the literature regarding tissue metal concentrations.

The effects of long term silver exposure on growth, bioaccumulation and histopathology of laboratory and field collected blue mussels, Mytilus edulis, were examined. After 12 months, significant accumulation of silver occurred only with laboratory raised mussels exposed to 10 µg/L silver; however, at 18 and 21 months, mussels exposed to 1, 5, and 10 µg/L silver all showed significant accumulation. Significant levels of copper were also accumulated from the ambient levels in the test seawater. In field-collected juvenile and adult mussels, silver accumulation was significant over the first 12 month period but the rate of accumulation was lower for the adults. Growth was inhibited at 6 months, but at 12 months the rate of growth was equal to the controls. Seasonal differences in the rate of accumulation were also noted (Calabrese et al. 1984).
Species related variations of silver bioaccumulation were investigated in a static renewal assay with the Pacific oyster, Crassostrea gigas, the mussel, Mytilus galloprovincialis, and the scallop, Chlamys varia. Exposures to silver occurred through phytoplankton containing 20 µg/g silver, water containing 20 µg/L silver, or food+water containing a total of 20 µg/L silver. Exposure via food only resulted in a rate of uptake of <10 mg/kg, while exposure via the water only or via the water+food resulted in a rate of uptake >100 mg/kg. Uptake via exposure through the food was still considered significant. Heavy accumulation of AgS in the glandular cells, which secrete the byssal threads in the mussel, resulted in a significant percent detachment from the container walls. The scallop and the oyster were observed to retain more silver than the mussel on a quantity of metal available per unit weight of filter feeding organism (Metayer et al. 1990).

In a 28 day study, juvenile Pacific oysters, Crassostrea gigas, were exposed to silver either through 20 µg/L dissolved in solution, or by 59.7 µg/g in the phytoplankton (Majorta et al. 1988). A plateau, where the body burden of silver no longer increased, was reached within 14 days of the study. The major storage of silver was as the sulphide in amoebocytes and basal membranes of tissues and organs. Elimination of the amoebocytes probably resulted in the accumulation plateau. The fact that the major storage of silver occurs as silver sulphide is important as this compound is very stable and unlikely to be a vector for trophic transfer or biomagnification of silver.

Nelson et al. in 1983 reported silver uptake in two succeeding generations of the marine snail, Crepidula fornicata. In the parent generation a very significant uptake of silver was observed for the first six months at all treatment levels. After 12 months only the lowest exposure level, 1µg/L silver, continued to show any significant increase and after 24 months body burdens at all treatment levels were significantly reduced.
Males accumulated silver faster than the females for the first 12 months; in the same period females showed a significant reduction in metal body burden while the males did not. Copper accumulation increased as silver accumulation decreased, which may indicate some competition for binding sites. The F1 progeny also accumulated significant amounts of silver in much the same pattern. Silver was mainly deposited on the basal membranes of cells in tissues and organs, bound primarily to sulfhydryl groups, and therefore probably not toxic.

3.5.2.4-worms

The rates of silver accumulation in two populations of the polychaete, Neanthes virens, one from a local polluted area, and one from a relatively pristine area were compared (Pereira and Kanungo 1981). Transplanted worms accumulated more than twice as much silver in 24 hours of exposure to 1.0 µg/L silver. Increasing levels of the ambient silver and time of exposure increased the levels of silver accumulated. A significant decrease in oxygen consumption was observed in transplanted worms with a metal body burden >113 mg/kg, and a significant decrease in water content was observed in worms with a body burden >88 mg/kg. Worms resident to the contaminated area did not show any adverse effects.

These results are in contrast to those of Bryan and Hummerstone in 1977, which indicated only low levels of silver accumulation in Nereis diversicolor, perhaps indicating that silver accumulation is mainly a function of water, rather than sediment, concentrations; this result may, however, only indicate species variability. Though this study provides evidence of a tolerance of organisms indigenous to a polluted area, it is not clear how this relates to the lowered rate of accumulation of these same animals.
3.5.2.5-crustaceans

The environmental parameters affecting trace metal uptake and toxicity in estuaries were examined in some detail. The complexation of silver in freshwater was discussed as freshwater input to the estuarine environment is often important. In the estuarine environment, silver is likely to be bound to inorganic material due to a high affinity for the chloride ion. Increasing salinity will further decrease silver-organic complexing because calcium and magnesium will compete for chelation sites. In a study with the grass shrimp, Palaemonetes pugio, silver uptake was most closely related to the concentration of silver chloride (r2=0.90) than any other expected silver complex. It was suggested that this was partly due to a potentially greater permeability of silver chloride across cell membranes due to its neutral charge, which generally allows for permeability several orders of magnitude greater than for charged species. Despite this, the rate of uptake of all silver and chloride complexes decreased with the increasing salinity.

In 1985, Cain and Luoma suggested that, because the initial burden of silver in transplanted animals is low, the influx of silver is high, until whatever regulating systems that are utilized in detoxifying metals become accustomed to the change in environmental parameters and are able to operate efficiently. The body burden of silver was measured in the spot prawn, Pandalus platyceros, from two locations in BC waters (Whyte and Boutillier 1991). Levels of silver were measured in the abdomen and the carapace of immature males, mature males and mature females in both areas. In general there was no correlation between size, age or sex of the prawn and silver levels. The greatest accumulation was in the hepatopancreas, 8.27 µg/g silver, followed by the carapace tissue, 1.16 µg/g silver, and the abdomen, 0.80 µg/g silver. Body burdens in the abdomen tissue were the same at both locations, suggesting that the diet was the same.

Carapace levels were significantly different suggesting that silver was incorporated into the carapace due to ambient levels in the surrounding water, rather than deposited through metabolic activity.

3.5.2.6-phytoplankton

In 1989, Sanders and Abbe reported on a study and review on silver transport and impact in estuarine systems, with particular reference to phytoplankton. Uptake of silver was rapid, but was inversely proportional to salinity. Bioavailability, especially at high salinities, appeared to be controlled by the free monovalent silver ion and possibly the silver chloride complex. Accumulation rates were similar in all phytoplankton species monitored.

3.5.3 fresh waters

3.5.3.1-fish

In a six month static bioassay, accumulation of silver in the largemouth bass, Micropterus salmoides, and the bluegill sunfish, Lepomis macrochirus, was measured (Coleman and Cearley 1974). Silver accumulation was significant for the first two months only. By then an equillibrium had developed between the silver levels in the bass tissues and in the water. At 7 µg silver per litre, accumulation in the bass was highest in the gills, 200 times, followed by the internal organs, 12 times, then the whole rest of the body, 9 times. The eventual concentration of silver was greater in the internal organs, 600 µg/kg, than in the gills, 370 µg/kg or the rest of the body, 17 µg/kg. Zinc uptake was observed to decrease as silver uptake increased. The data in this paper should be used with caution since the water contained inordinately high levels of chloride ion which would result in much of the silver being complexed to unavailable forms (Davies and Goettl 1978).

table 3.8

bioconcentration of silver in freshwater fish.

Coleman and Cearley 1974.

The fathead minnow, Pimephales promelas, concentrated silver from the water but less so than Daphnia. It was thought that the fish did not accumulate the silver from the food since the fish had less silver per unit weight; no biomagnification occurred (Terhaar et al. 1977). Bard et al. in 1976 also discussed this lack of biomagnification in fish. Fish in the St Lawrence River had silver levels ranging from 10 to 30 µg/kg fresh weight while the river levels ranged from 1 to 6 µg/L (Tong et al. 1972). Silver levels in Lake Michigan fish muscle, on a wet-weight basis, ranged from 28 µg/kg in yellow perch to 44 µg/kg in brown trout. Whole fish analyses gave 34 µg/kg in alewife and 39 µg/kg in rainbow smelt (Copeland et al. 1973).
3.5.3.2-cladocerans and Algae

A study with Daphnia magna and Euglena, or mixed algal species, with respect to accumulation and biomagnification was reported by Cowgill and Burns in 1975. Algae concentrated silver from water by a factor of 7.5, but D. magna, fed the algae in their diet, did not accumulate silver significantly. In another study by Terhaar et al. in 1977, the alga, Scenedesmus, and the cladoceran, Daphnia magna, absorbed silver from the water. The concentration factor was 26 for the Scenedesmus and 96 for the Daphnia, in water with 500 µg silver per litre.

3.5.3.3-insects

In 1976 Nehring reported on the accumulation of silver by two aquatic insects, the mayfly, Ephemeralla grandi, and the stonefly, Pteronarcys californica. Both accumulated silver by a factor of 100 or greater. The level of silver accumulated appeared to be correlated with the level of exposure, which suggests these species are good indicators of silver contamination.

In 1975 and 1977 Freeman studied silver levels in the sediments and in chironomid and caddis fly larvae in a simple ecosystem where sampling may have affected the distribution of biomass. Sediment and tissue levels were well correlated in 1977 but less so in 1975. In 1975 the silver levels in the sediment, chironomids and caddis flies were 510, 2600 and 400 µg/kg, respectively. The respective levels for 1977 were 290, 560 and 120 µg/kg. The lake water contained 1 µg/L; sediment and both species of insect larvae concentrated silver relative to the water but only the chironomids concentrated silver relative to the sediment. This is to be expected given the differential feeding behaviour and habitat preferences of caddis fly and chironomid larvae. The top predator, cutthroat trout, had silver levels of 3690, 1810 and 290 µg/kg in their bone, liver and muscle, respectively.3.5.3.4-plants

In water with a silver level of 0.4 µg/L, Lemna minor (duckweed) accumulated 33 µg/kg dry-weight (Hutchinson and Czyrska 1975). Nymphaea odorata (waterlily) contained 60 to 2300 µg/kg silver, with a mean of 500. Rhopalosiphum nymphaeae (aphids) feeding on the lilies contained 420 µg/kg. The plants accumulated only twice the level of the substrate. The silver level in the lake water was 12 ng/L. Presumably the silver could not diffuse from the sediment which contained iron sulphide (Cowgill 1973).

In 1985, Jones et al. reported on the levels of silver in three aquatic bryophytes, Scapania undulata, Hygrohypnum luridum and Polytrichum commune, from streams in the lead mining district of Wales. All had higher levels of silver in their tissues than the surrounding water; site specific ambient levels were not reported. S. undulata was considered the best pollution monitor since there were strong correlations between tissue levels of silver and those of lead, zinc, copper and cadmium.

3.5.3.5-microorganisms

Activated sludge organisms bioaccumulate silver at 100 times the concentration in the effluent (Chin 1973).