The common mussel Mytilus edulis as an indicator of pollution by zinc,cadmium, lead and copper. I. Effects of environmental variables on uptake of metals

The net uptake of zinc, cadmium, lead and copper by the common mussel Mytilus edulis (L.) exposed to different conditions was investigated with a view to using this species as an indicator of contamination of the marine environment by these metals. The variables studied were season, position of the mussel in the water column, water salinity, water temperature, and the simultaneous presence of all four metals. Each of these 5 variables affected the net uptake of some or all of the metals studied under some conditions. Seasonal variation in concentrations of zinc, cadmium and copper was found in samples collected at three separate locations. The relationship of seasonal variation to tissue weight and absorption route of the metals is discussed. Near to freshwater inputs of trace metals, the concentrations of zinc, cadmium and lead in mussels were found to vary according to the depth at which the mussels were collected; in summer when freshwater run-off is less, this effect was absent. Low salinities did not affect the net uptake of zinc by mussels, but increased the net uptake of cadmium and decreased that of lead. Low temperatures had no effect on the net uptake of zinc or lead; the net uptake of cadmium was unaffected by low temperatures at high salinities but was decreased by low temperatures at low salinities. The presence of the other metals had no effect on the individual net uptake of either zinc, cadmium or lead. A sampling programme was devised to eliminate the effects of these environmental variables and to allow the use of M. edulis as an indicator of zinc, cadmium and lead in marine and estuarine environments. In contrast to the other metals, the net uptake of copper by the mussel was extremely erratic, and was affected by salinity and temperature changes and by the presence of the other metals and changes in their relative concentrations. The effects of other metals on the net uptake of copper cannot be easily eliminated or allowed for; it is, therefore, suggested that the mussel should not be used as an indicator of copper in the marine environment.     

Effects of salinity on the net uptake of zinc by the common mussel Mytilus edulis

The net uptake of zinc by the common mussel Mytilus edulis (L.) has been investigated under different natural and artificial salinity stresses. The effects of stable and fluctuating salinities on the uptake of zinc by the mussel are discussed in terms of three possible modes of action. Under certain highly-stressful conditions, salinity may affect the uptake of zinc by the mussel. This factor should be considered when the mussel is used as an indicator of environmental pollution by zinc in estuarine areas, or spurious conclusions may result.     

Effects of environmental factors on radiocadmium uptake by four species of marine bivalves

Temperature, salinity, bottom-sediment type, and zinc concentration all influenced Cd uptake by 4 marine bivalves (Mya arenaria, Mytilus edulis, Mulinia lateralis and Nucula proxima) in short-term static assay systems using ¹⁰⁹Cd as a tracer. The experimental system consisted of aquaria containing 20 l of seawater maintained under controlled light and temperature conditions. The water contained either 5 or 20 g/l Cd and tracer. Distribution and kinetics of the metal were monitored in the water column and organisms. The results demonstrate that Cd uptake rates differed widely among the organisms tested. An increase in temperature increased Cd uptake rate by all test organisms. A decrease in salinity increased Cd uptake by all organisms tested. The presence of bottom sediment depresses Cd accumulation in some benthic animals. Zinc in concentrations of 0.5 mg/l substantially decreased Cd uptake by Mytilus edulis and Mulinia lateralis. It is suggested that all important species and environmental variables be considered when studying heavy-metal uptake by marine organisms or when establishing water-quality criteria.     

Bioaccumulation of heavy metals by bivalves from Lim Fjord (North Adriatic Sea)

Trace metal concentrations (Zn, Cd, Pb and Cu) were studied in two different bivalve species of the same age, the mussel Mytilus galloprovincialis, Lmk., and the oyster Ostrea edulis, Linnaeus, which had been grown in the water of Lim Fjord, North West Yugoslavia (Peninsula Istria), i.e. under the same physicochemical conditions. The study offers a realistic view on the metal accumulation ability of oysters and mussels. The distribution of trace metals over the different organs and the edible parts of the mussels and oysters, collected in June 1979, was determined and is discussed in detail. The results are supported by the determination of the trace metal levels in the dissolved state and in the suspended material in the ambient sea water of the bivalves. Concentration factors for zinc, cadmium, lead and copper in the mussels of: 95 000, 9 100, 1 500 and 4 000; and in the oysters of: 95 500, 30 400, 3 400 and 64 500 were found, respectively. The values were evaluated comparing the metal concentration in the bivalve soft part and the dissolved trace metal levels in the adjacent water.     

Metal interaction during accumulation by the mussel Mytilus edulis planulatus

Mytilus edulis planulatus (Lamarck) were collected from Howden, South-east Tasmania in autumn 1981. Interaction effects of cadmium, copper and zinc during accumulation by mussels exposed for ten days to all three metals simultaneously were examined in a series of experiments in which each metal was tested at three concentrations. In general, interaction effects were most evident at the highest concentrations tested (20 g l^-1 Cd; 20 g l^-1 Cu; 200 g l^-1 Zn) and led to a reduction in the accumulation of cadmium and an increase in that of copper and zinc. More specifically, high levels of zinc caused a decrease in cadmium uptake and an increase in copper accumulation. The presence of copper resulted in depressed cadmium accumulation while zinc accumulation increased. Cadmium tended to enhance zinc accumulation, but copper accumulation was only affected to any great extent when zinc was also present.     

The common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters. I. Zinc and cadmium

Concentrations of zinc and cadmium in whole soft parts of mussels, Mytilus edulis (L.), collected from 54 locations in Scandinavian waters were determined. Local variations in concentrations of the two metals found in samples taken close to industrial sources of zinc and cadmium confirmed the ability of the mussel to act as an accurate indicator of pollution by these metals over the entire range of salinities in which this species can exist. In addition, offshore samples remote from industrial discharges revealed higher concentrations of zinc and cadmium in mussels from lowsalinity areas (Gulf of Finland, Southern Bothnian Sea, Baltic proper) than in those from high-salinity areas (Kattegat, Eastern Skagerrak). Major decreases in metal concentrations present in the mussel were apparent in the regions of the Sound and the Great Belt, which are areas of rapid salinity change due to mixing of Baltic water with water from Kattegat. Comparison of these results with those reported for zinc and cadmium in water throughout the study area suggested the existence of a higher biological availability of these metals in regions of low salinity; possible reasons for this are discussed. Data from the present survey are also compared to those reported for mussels taken elsewhere. This comparison reveals the Baltic area to be considerably polluted by trace metals; in contrast, the waters of Kattegat and skagerrak are considered to be relatively unpolluted.     

Variability in dry weight and vertical distributions of decapod larvae in the Irish Sea and North Sea during the spring

Accumulation of waterborne cadmium in Littorina littorea, Mytilus edulis and Carcinus maenas (collected in 1988 and 1989 around the island of Funen, Denmark) was investigated in a matrix of salinities (10 to 30) and calcium concentrations (2.9 to 8.9 mM Ca⁺⁺). Cadmium accumulation rates in soft parts of L. littorina, soft parts and shells of M. edulis and whole bodies and exoskeletons of C. maenas decreased with increasing salinity. Changes in the calcium concentrations accounted for 72% of the salinity effect on cadmium accumulation rates in L. littorina, whereas calcium concentrations had little or no effect on cadmium accumulation in M. edulis. Cadmium accumulation in the whole body of C. maenas was affected equally by calcium concentrations and total salinity, whereas accumulation in the exoskeleton was mainly affected by changes in total salinity. Individual variability in cadmium accumulation in the organs of C. maenas was greater than the variation attributable either to changes in ambient calcium concentrations or total salinity. An appreciable amount of the inter-individual variability in the cadmium accumulation in all three species was correlated with wet:dry weight ratios of the tissues and size of the organisms.     

Toxicity of zinc,cadmium and copper to the shrimp Callianassa australiensis. III. Accumulation of metals

Callianassa australiensis (Dana) that survived 14 d acute lethality studies were analysed to determine the concentrations of zinc, cadmium and copper in the whole shrimp and in various parts of the body. Using regression analysis, the influence of each metal upon the uptake of the others was studied. Zinc and cadmium appeared to enhance the uptake of each other. In a mixture of zinc and copper, the uptake of zinc was enhanced and that of copper was inhibited. In a mixture of cadmium and copper, the uptake of copper was inhibited by the presence of cadmium, but cadmium uptake was unaffected in the presence of copper. In a mixture of all three metals, similar effects were observed except that zinc and copper, occurring together, appeared to have no effect upon cadmium uptake. Additional 14 d experiments with cadmium suggested that accumulation of this metal was a function of metal concentration in the water and of duration of exposure. The whole shrimp cadmium concentration also appeared to be a function of the size of the shrimp. The variation in concentration factors is described and the need for further research on the effects of combinations of metals on various organisms is emphasized.     

Effects of temperature,nutritive and metal stressors on the reproductive biology of Mytilus edulis

Experimental observations suggest that the gametogenic cycle of Mytilus edulis from Swansea Bay, South Wales (U.K.) is adversely modified by the combined effects of temperature, nutritive and sublethal metal-induced stress. During low temperature stress, oogenesis remained in the vegetative stage and vitellogenesis only commenced when temperatures were raised to ambient levels. Copper was the most toxic metal, although its uptake was slowest. A concentration of 0.05 mg l^-1 of this metal proved lethal at ambient temperatures, although at low temperatures there was no mortality. Copper suppressed both the growth of young oocytes and vitellogenesis in larger oocytes. Zinc was less toxic than copper, although this also inhibited oocyte development and resulted in severe lysis of gametes. Cadmium was the least toxic of the three metals studied and suppressed gametogenesis only in the initial stages of gonad development. The low toxicity of cadmium to gametogenesis may be a result of its high solubility and its possible storage in the digestive gland.     

Uptake and cellular distribution of cadmium in Mytilus edulis

Cadmium uptake has been studied in starved and fed Mytilus edulis L. It is suggested that fairly elevated cadmium contents in fed mussels are not due to contaminated food, but to increased pumping rate when food is available. Highest concentration and main body burden are found in the mid-gut gland. Transport via haemolymph, and selective discrimination at the basement lamina of the mid-gut gland tubuli are regarded as mainly responsible for accumulation. Mercury seems to be processed in a similar way as cadmium. In the tubuli, both metals are immobilized in membrane-bound vesicles, which are finally defaecated.This work was financially supported by the German Research Council (DFG) (Sto 75/4 and Th 158/13).     

The common mussel Mytilus edulis as an indicator of pollution by zinc,cadmium, lead and copper. II. Relationship of metals in the mussel to those discharged by industry

Concentrations of zinc, cadmium, lead and copper were determined in whole soft parts of the common mussel Mytilus edulis (L.) sampled in Port Phillip Bay and Western Port Bay, both in Victoria, Australia. The mussels were sampled according to procedures suggested by previous studies in order to eliminate the effects of natural environmental variables. Results of the analytical studies were compared to data on the quantities of trace metals known to be discharged by industry into the catchments of each Bay. This allowed an evaluation of the indicator ability of the mussel without the need for multiple analyses of water samples. The results suggest that the mussel is capable of acting as an efficient time-integrated indicator of zinc, cadmium and lead over a wide variety of environmental conditions. Although additional variables may remain to be investigated, the mussel is recommended as an alternative to the analysis of water and sediments. With further development this organism may also be useful for monitoring industrial effluent characteristics at the discharge site, allowing rapid, reliable and inexpensive control of water quality. In contrast, the mussel is of doubtful use as an indicator of copper; other indicator types such as macroalgae may be better-suited to the study of this element.     

Metallothionein induction inMytilus edulis exposed to cadmium

The exposure of mussels,Mytilus edulis, collected from Whitsand Bay, southwest England, in August 1988, to sublethal concentrations of cadmium (400µg l^–1) for 65 d resulted in the induction of metallothionein (MT) synthesis in the soft tissues. In cadmium-exposed mussels, metallothionein concentrations, measured by differential pulse polarography, increased by a factor of three, from 2 to 3 mg g^–1 to a maximum of 9 mg g^–1 after 30 d. No significant changes could be detected in controls. Cadmium accumulated in the soft tissues of mussels correlated significantly with metallothionein concentrations and can be described by the relationship: MT (mg g^–1)=0.045 Cd (µg g^–1)+3.03 (r=0.803,P<0.001). Gel chromatography of heat-treated cytosolic extracts showed that the accumulated cadmium is bound principally to the newly formed metallothioneins. Copper and zinc were also analysed in the whole soft-tissues and in subcellular fractions of cadmium-exposed mussels. Although copper concentrations were not affected by cadmium-exposure, zinc levels were significantly reduced. The results demonstrate that the induction of metallothioneins inM. edulis is a quantifiable biological response to sublethal levels of cadmium exposure.     

Decrease of net carbon flux in two species of mussels caused by extracts of crude oil

Effects of crude oil and salinity stress on the metabolism of two common filter-feeding animals (Mytilus edulis and Modiolus demissus) have been investigated. Carbon budgets have been calculated for each species under a variety of combinations of oil content and salinity. Both reduced salinity and the presence of crude oil tend to decrease the net carbon flux for each species; stresses from each source interacted in their effects on experimental animals. Although similar responses to oil were shown by each species, Mytilus edulis appeared to be slightly more resistant to oil than Modiolus demissus.     

The effect of copper and zinc on the metabolism of the mussel Mytilus edulis

The effects of copper and zinc on the metabolism of the mussel Mytilus edulis (L.) and its component tissues were studied. 500 ppm copper sodium citrate inhibited oxygen consumption of the whole animal and gill tissue, but no similar effect was observed on digestive gland tissue. 500 ppm zinc sodium citrate exerted no effect upon gill or digestive gland respiration, and neither metal salt affected the respiration of homogenates of gill, digestive gland or gonad. Direct observation of gill tissues during exposure to the metals revealed that 500 ppm copper sodium citrate caused inhibition of ciliary activity; exposure of tissues to 2 ppm Cu for 24 h resulted in only partial inhibition of the cilía. It is suggested that metabolic suppression noted in whole animals and gill tissues is due to the inhibition of an energy-consuming process such as ciliary activity rather than interference with respiratory enzyme systems.     

Accumulation of cadmium and bioenergetics in the mussel Mytilus edulis

Accumulation rates of cadmium, the amount of food ingested and assimilated, the amount of oxygen consumed and changes in dry flesh weight have been measured in Mytilus edulis L. exposed to 0, 10 and 100 ppb cadmium for 17 d in aquaria with seawater flowing continously and at constant algal concentration. The accumulation rates were linear at 10 and 100 ppb, amounting to 0.58 and 8.89 ppm d^-1, respectively. Body loads up to 150 ppm caused no effects on either clearance, ingestion, assimilation, respiration, or growth. High net growth efficiencies between 55–59% were obtained, indicating near optimal experimental conditions. It is suggested that the setup and experimental procedure provide an excellent tool in the study of accumulation and sublethal effects of environmental pollutants in suspension feeding bivalves.     

Experimental analysis of byssus thread production by Mytilus edulis and Modiolus modiolus in sediments

Laboratory experiments have been conducted on byssus thread production by two species of mussel, Mytilus edulis L. and Modiolus modiolus (L.), representing the epibyssate and endobyssate species of the Mytilidae, respectively. Mussels were placed in seven particle sizes of sediment ranging from 50 m to 16 mm for 12 d. The number of byssus threads per mussel, length of threads, number of threads per particle and size of pads were then recorded. Modiolus modiolus (endobyssate) produced more threads than Mytilus edulis (epibyssate). M. edulis produced most threads in the size range 2 to 16 mm and Modiolus modiolus in the size range 500 to 1000 m. M. modiolus produced longer threads than Mytilus edulis. Both species produced longer threads in particle sizes finer than 2 mm. M. edulis produced smaller pads than Modiolus modiolus. Both species produced larger pads in sediments coarser than 1 000 m. Results were also analysed in terms of attachment units (a thread attached to one or more particles, or a particle to which more than one thread is attached). The thread:particle ratio of the attachment units ranged from ca. 1:10 in the finest sediments to ca. 10:1 in the coarsest sediments. Mytilus edulis attached more threads to single particles (72% of attachment units) than Modiolus modiolus (37% of attachment units). M. modiolus had a wider spread of ratios in the finer particle sizes than Mytilus edulis. The significance of our results are discussed in relation to the ecology and palaeoecology of epibyssate and endobysste species.     

The effect of chelating agents on the uptake and accumulation of cadmium by Mytilus edulis

The uptake, storage and excretion of cadmium by the common mussel Mytilus edulis (L.) has been studied at sub-lethal concentrations using the radioactive isotope ^115mCd as a marker. After an initial lag period, the uptake at low concentrations in sea water is linear with time and directly proportional to the sea water concentration, with a maximum concentration factor of 165 at 0.7 g Cd/ml sea water. A decrease occurs at higher concentrations indicating saturation of the available binding capacity. Prior complexation of the cadmium with either EDTA, humic and alginic acids or pectin doubles both the rate of accumulation and the final tissue concentrations (order: kidneyviscera>gillsmantle>muscle) and eliminates the lag period, suggesting that ionic cadmium must first be complexed before uptake can occur. A mechanism for this effect, which may involve thionein, is described. The rate of excretion of cadmium is 18 times slower than that of uptake, with the major route via the kidney but not via the byssal threads as with particulate iron. The need to detoxify and store cadmium by an immobilization mechanism is a consequence of this slower rate of elimination.     

Total body zinc concentration and allometric growth ratios in Mytilus edulis collected from different shore levels

Body zinc concentrations (on a soft parts dry weight basis) in 18 composite collections of mussels (Mytilus edulis) taken from different shore levels within a single mussel bed on the north shore of the Tyne estuary at Tynemouth, on 25 October, 1980, showed highly significant correlations with 4 allometric, size-related factors. A negative correlation was found between body zinc concentration and a flesh condition (FC) index defined as mg dry flesh wt per g dry shell wt. Positive correlations were found between body zinc concentration and width: height ratio, width: length ratio and shell valve inequality index (SVI) defined as the weight of heavier shell valve/weight of lighter shell valve. Unlike earlier observations on a single population taken from a single habitat, this heterogeneous collection showed no significant relationship between body zinc concentration and body size as determined by soft-parts dry weight. Body zinc concentration and allometric ratios were, however, related to position on the shoreline. It is suggested that, where mussels are collected from different habitats, environmental factors probably have a greater influence on body size than age. Therefore, normalization of trace metal concentrations to a standard body weight may not be appropriate where specimens are collected from a variety of habitats. Allometric ratios are related to age, but are independent of absolute size, and may therefore provide a more suitable basis for normalization of trace metal concentration within a monitoring programme.Contribution No. 1222 of the Center for Estuarine and Environmental Studies of the University of Maryland     

Degradation of bacteria by Mytilus edulis

The uptake of several species of bacteria by the common mussel Mytilus edulis (L.) and the subsequent fate of some polymers of the bacteria have been investigated in a study carried out during 1981. Bacteria (Escherichia coli, Micrococcus luteus, M. roseus, Bacillus cereus, Staphylococcus aureus and a marine pseudomonad, 1-1-1) were radiolabelled by growth in medium containing ³H-thymidine and the uptake of bacteria by Mytilus edulis was monitored. Labelled and unlabelled bacteria, at initial concentrations of 0.5 to 1x10⁷ bacteria ml^-1, were cleared at similar, exponential rates with no significant difference in the rates for different bacteria: 90% of bacteria were cleared in a mean time of 1.93±0.12 h (SEM, n=63). Those bacteria with cell walls which were sensitive to M. edulis lysozyme were rapidly degraded by the mussel and ³H-labelled DNA was released in a form not precipitable by 10% trichloroacetic acid. Lysozyme-resistant bacteria (Micrococcus roseus and S. aureus) were cleared from suspension by Mytilus edulis but most were rejected intact. By measuring the rate of release of ³H-thymidine-labelled material from the mussel the rate of degradation of lysozyme-sensitive bacteria by M. edulis was found. For different bacteria the degradation rate varied from approx 2x10⁸ to 27x10⁸ bacteria h^-1 with an overall mean of 10x10⁸ bacteria h^-1. A thymidine- and diaminopimelicacid-requiring auxotroph of E. coli was radiolabelled with ³H-thymidine, ³H-diaminopimelic acid or ¹⁴C-glucose and fed to M. edulis. Bacteria were cleared and degraded by the mussel; ³H-diaminopimelic acid-labelled or ¹⁴C-glucose-labelled polymers were retained, whereas ³H-thymidine-labelled polymers were released into the surrounding water. Extracts of the digestive gland of M. edulis degraded lysozyme-sensitive bacteria to release ³H-thymidine-labelled material, but did not release ³H-thymidine-labelled material from lysozyme-resistant bacteria. It is concluded that M. edulis can select lysozymesensitive bacteria for subsequent processing and discriminate between bacterial polymers to reject DNA. Also, bacteria could provide a substantial fraction of the carbon requirement of the mussel.     

Influence of food quantity on the kinetics of cadmium uptake and loss via food and seawater in Mytilus edulis

The difference between the cadmium uptake via food and seawater in Mytilus edulis has been studied. This was done by labelling algae with Cd-109 and seawater with Cd-115m. Mussels were fed on six different quantities of Isochrysis galbana. Cadmium uptake via algae was more efficient at low food levels, while accumulation from seawater was linearly correlated with food quantities. Cadmium from food contributed only little to the body burden (0.2–0.5%). Half-lives for the elimination of cadmium ranged from 96–190 d and increased with decreasing availability of algae, presumably due to slowed down metabolism. Differences in elimination patterns suggest a release of both isotopes from different storage depots. A computer model shows that the food pathway can only play a significant role if algae are highly contaminated. It also demonstrates the paradox that in long-term studies the highest contribution of food-derived cadmium to the body burden must be expected near maintenance food concentrations.