7.4 marine waters

7.4.1 general

Table 7.2 lists some acute effects of silver nitrate on marine organisms while Table 7.3 lists chronic and sublethal effects of silver on marine organisms.

The life stage, size of the organisms, length of time of exposure, species sensitivity and salinity all contribute to the variation in toxicity reported in the literature. The relative proportion of the free Ag+ ion to the total silver content in the oceans is a function of the salinity. In the ocean, most of the silver at any one time is present as chloride complexes; of these complexes only the mono-chloro complex AgCl is biologically available. The ambient levels of silver in the oceans range from about 0.04 to 2.5 µg/L silver. Thus at a salinity of 250/00 and an ambient level of 2.5 µg/L silver, only 0.16 ng/L of silver would exist as the free ion. This lack of free silver ion is generally not accounted for in the literature where most values are given as total silver and the actual toxic forms of the silver would be a considerably smaller value. This factor accounts for much of the wide variation in toxicity values reported in the literature, for while salinity is generally reported, it is rarely considered as a factor. The total silver measurements reflect the worst case scenario, which should be considered when setting any water quality criteria in order to protect the most sensitive life stages of the most sensitive species. This worst case scenario is particularly important for estuarine environments, where salinity can fluctuate quite dramatically. The criteria set agree closely with the marine criterion of 2.3 µg/L of total recoverable silver, not to be exceeded at any time, set by USEPA in 1980a.

7.4.2 fish

In 1982, Voyer et al. reported on the exposure of embryos of the winter flounder, Pseudopleuronectes americanus, to treatments of silver and silver + cadmium at various salinities (10 to 32) at 8.7C. It was found that silver exerted no toxic effects over the range 0 to 180 µg/L at any salinity. They did note, however, that silver markedly reduced the effects of cadmium toxicity. Contrasting results were reported for an 18 day test, from the 2-celled stage to yolk-sac absorption, for larvae of P. americanus. Silver exposures were from 0 to 386 µg/L and salinity was 27 to 320/00, which resulted in significant abnormal development and larval mortality at levels exceeding 92 µg/L, significant reduction in mean length at yolk-sac absorption, and a chronic no-effect level of 70.5 µg/L with respect to mortality (Klein-Macphee et al. 1984). The marked differences in experimental results is probably due to the stage at which the percent viable larvae were measured: viability at hatching (1) vs. viability at yolk-sac absorption (2). Klein-MacPhee et al. in 1984, noted a 98 percent hatch at 180 µg/L but noted many morphological abnormalities, including abnormal yolk-sacs. The change from an endogenous to an exogenous food source is a critical stage of teleost development, and many of the larvae with abnormal yolk-sacs did not successfully complete absorption. This is the most sensitive stage of development for a chronic toxicity study.

Respiratory response of the cunner, Tautologabrus adspersus, was reported in natural sea water (24, 20C) by Thurberg and Collier in 1977. In a 96-hour assay, significant respiratory depression for exposures of 120 µg/L silver was observed and exposures of >500 µg/L silver were lethal. No change in osmoregulation was observed, which contrasts with observations in bivalves and polychaetes. In 1980a, the USEPA conducted a series of static tests on five marine fish species. The acute toxicity of silver was determined, but no chronic values were determined.
The most sensitive species was the summer flounder larvae, Parlicthys dentatus, with an LC₅₀ of 4.7 µg/L silver, while the least sensitive species was juvenile sheepshead minnow, Cyprinodon variegatus, with an LC₅₀ of 1400 µg/L silver. Larvae were generally much more sensitive than either juveniles or adults.

7.4.3 molluscs

In 1981, Martin et al. reported on the toxicity of ten metals, including silver, to larvae of the crab, Cancer magister, and to embryos of the oyster, Crassostrea virginica, and the mussel, Mytilus edulis. A 96-hour LC₅₀ for silver of 55 ± 20.8 µg/L was obtained for the crab zoeae at a salinity of 340/00. Forty-eight hour EC₅₀'s, percent normal development, for the oyster and the mussel were 22 ± 13.3 µg/L silver and 14 ± 2 µg/L silver respectively, indicating that the mussel embryos were approximately twice as sensitive as the oyster embryos. Silver was the third most toxic element, following copper and mercury.

Another study by Calabrese et al. (1973) subjected C. virginica embryos to silver concentrations from 2.5 to 10 µg/L in synthetic sea water at 25 salinity and 26C for 48 hours in a static bioassay, giving an EC₅₀, percent normal development, of 5.8 µg/L silver. The relative toxicities of various metals was determined to be mercury > silver > copper > zinc. In 1974, Calabrese and Nelson reported the relative toxicity of several metals to the hard clam, Mercenaria mercenaria, in synthetic sea water of 25 salinity at 26C. In a 48-hour assay, an LC₅₀ of 21 µg/L silver, a no observed effect level (NOEL) of 10 µg/L silver, and an LC₁₀₀ of 45 µg/L silver were determined.

A side-by-side study of the oyster, C. virginica, and the clam, M. mercenaria, larvae in natural sea water of 24 ± 2 salinity and 25C, in an 8 to 10-day static bioassay, resulted in an LC₅₀ of 25 µg/L silver and 32.4 µg/L silver for the oyster and the clam, respectively, a NOEL of 14.2 µg/L silver and 18.6 µg/L silver, respectively, and an LC₁₀₀ of 35.7 µg/L silver and 46.2 µg/L silver, respectively (Calabrese et al. 1977). The authors also reported that the growth of the larvae was significantly reduced at the LC₅₀ for both the oyster and the mussel. The relative toxicity of the metals was reported to be mercury > silver > copper > nickel.

In 1982, Coglianese reported the effects of salinity on silver toxicity to the Pacific oyster, Crassostrea gigas. Salinities ranged from 14.5 to 33, the temperature was 20C and the silver exposures were 0 to 18 µg/L. It was determined that salinity had the greatest effect on embryonic survival, salinities below 22.70/00 being highly deleterious to normal development, and that silver toxicity was reduced at higher salinities. Optimum development occurred at salinities between 23 and 330/00 and at <15 µg/L silver.

Embryonic development of the Pacific oyster was also studied. Oysters were subjected to copper and silver, both individually and together, in natural sea water at 33 salinity and 20C. A 48-hour LC₅₀ for silver alone was determined to be 16 to 18 µg/L silver. Silver and copper interacted additively, with copper showing the greatest influence on toxicity. Abnormal embryos exhibited retarded shell growth, reduced size and erratic swimming behavior (Coglianese and Martin 1981).

Development of the surf clam, Spisula solidissima, was monitored following exposure of gametes, embryos and larvae to silver (Eyster and Morse 1984). The NOEL for exposure of eggs (pre-fertilization) was 9.5 µg/L silver; exposure of sperm to silver showed no effect at any of the treatment levels. Post-fertilization exposure of embryos to silver for 48 hours resulted in a significant abnormal development at 16 µg/L silver and 100 percent mortality at 48 hours at 32 µg/L silver. Continuous exposure of eggs and sperm through fertilization and development of embryos for 48 hours resulted in a significant abnormal development at 9.5 µg/L and 100 percent abnormal development and mortality at >9.5 µg/L silver.

The effect of temperature on the toxicity of silver, and mixtures of silver and mercury, to embryos of the American oyster, Crassostrea virginica, was examined by MacInnes and Calabrese in 1977. In natural sea water of 26 salinity, silver was found to be significantly more toxic at 20C than at 25 or 30C, with no significant difference between 25 and 30C. Forty-eight hour EC₅₀'s were 24.2 µg/L, 35.3 µg/L, and 32.2 µg/L silver at 20C, 25C and 30C, respectively. The increased toxicity at 20C may have been due to lower dissolved oxygen levels. Silver and mercury mixtures were significantly less than additive at 20C, but became additive at 30C. probably due to increased solvency with heat, indicating that each metal acted independently.

A 72-hour experiment examined the effects of silver on the oxygen consumption of the mud snail, Nassarius obsoletus (MacInnes and Thurberg 1973). Using synthetic sea water of 25 salinity and 20C, and silver exposures from 0 to 50 µg/L, it was found that oxygen consumption was depressed after exposures 0.5 µg/L silver. The snails appeared distressed at 0.25 µg/L silver and at 2.0 µg/L silver they were fully retracted and no longer consuming oxygen. At exposures exceeding 10.0 µg/L silver, all the snails were dead by the end of the 72-hour period.

In 1990, Metayer et al. reported on the toxicity of silver to the Pacific oyster, Crassostrea gigas, the mussel, Mytilus galloprovincialis, and the scallop, Chlamys varia. No effect was noted at 10 µg/L silver. At 100 µg/L silver the TLm (time to 50 percent mortality) for the scallop, mussel and oyster were 4.8 days, 4.6 days and 8.7 days, respectively; at 1000 µg/L silver the TLm's were <1 day, 3.3 days and 4.5 days, respectively. The availability and accumulation of silver was then determined by addition of silver at 20 µg/L, in the water, in the food (algae linked to silver) or in the water and food. Accumulation in water-exposed, or water-exposed and food-exposed animals, was an order of magnitude higher than for only food-exposed organisms. The oyster and the scallop were found to retain more silver than the mussel based on the ratio of metal available per unit weight of organism. It was also noted that heavy accumulation of silver in the glandular cells of the scallop, which secrete the byssal threads, resulted in >50 percent detachment in those exposed to silver in the water or in the water and food.

Effects of eight metals on the filtering rate of the brown mussel, Perna perna, were reported by Watling and Watling in 1982. An EC₅₀, 50 percent reduction in filtering rate with respect to controls, was determined to be 0.20 µg/L silver. The relative toxicity of the metals was mercury > copper = silver = selenium > nickel = zinc >> lead > cadmium.

7.4.4 worms

Respiration, ion and water balance, and accumulation of silver were measured in two populations of the polychaete, Neanthes virens, a local population from a contaminated area, and a transplanted population from an uncontaminated area (Periera and Kanungo 1981). Silver exposures were 0.5 to 1.0 µg/L in water of 26 salinity and 15C. At 0.8 µg/L silver transplanted worms that had accumulated > 113 µg/g silver dry-weight silver in their whole body soft-tissues showed a significant decrease in oxygen consumption after 48 hours; at 1.0 µg/L silver, transplanted worms showed a significant decrease in oxygen consumption after 24 hours. Local worms showed no effects at any treatment level. In the coelomic fluids of transplanted worms the concentration of K⁺ was found to increase with increasing silver exposure, while the concentration of Ca⁺⁺ was found to decrease with increasing silver exposure in both the local and transplanted worms. Water content significantly decreased in transplanted worms which had accumulated 88 µg/g (dry-weight) silver, but local worms showed no effects. Morphological and behavioural symptoms of distress included agyria of the dorsal surface, tendency to lie on their sides with tail curled towards the ventral surface, edema of the parapodia and uncoordinated movement. Again the local worms appeared to be less affected, indicating that the local worms had developed a tolerance to high environmental levels of silver.

7.4.5 phytoplankton

The effects of salinity on the toxicity of silver to several marine phytoplankton species was determined and measured with respect to growth and yield, as biomass (Sanders and Abbe 1989). In general, yield was a more sensitive measurement of toxicity than growth; EC₅₀ values for yield were, averaging the results of all species, 0.63 % of the value for the growth EC₅₀.
The most sensitive species were the dinoflagellates, Chroomonas, and Prorocentrum mariae-lebouriae; the least sensitive were the diatoms, Skeletonema costatum and Thalassiosira pseudonana. Accumulation of silver at salinities from 7.5 to 300/00 was examined. The data indicated that as salinity was doubled, the uptake of silver by phytoplankton was reduced by 50%; this was most likely due to a decrease in free Ag⁺ and AgCl and increase in AgCl₃^-2 and AgCl₄^-3 as a result of increasing complexing capacity of the sea water.