Metal toxicity, uptake and bioaccumulation in aquatic invertebrates--modelling zinc in crustaceans.

We use published data on the different patterns of the bioaccumulation of zinc by three crustaceans, the caridean decapod Palaemon elegans, the amphipod Orchestia gammarellus and the barnacle Amphibalanus amphitrite, to construct comparative biodynamic models of the bioaccumulation of zinc into metabolically available and detoxified components of accumulated zinc in each crustacean under both field and laboratory toxicity test conditions. We then link these bioaccumulation models to the onset of toxic effects on exposure of the crustaceans to high dissolved zinc bioavailabilities, using the tenets that toxicity effects are related to the total uptake rate of the toxic metal, and that toxicity is not usually dependent on the total accumulated metal concentration but always on the concentration of accumulated metal that is metabolically available. We dismiss the general concept that there is a critical accumulated body concentration of a metal in an invertebrate at which toxicity ensues, except under specific circumstances involving a rare lack of storage detoxification of accumulated metal. We thus propose a theoretical framework that can be extended to other metals and other aquatic invertebrates (indeed other animals) to explain the variation in the relationship between bioaccumulated body concentrations and toxicity, and subsequently to predict this relationship in many other species for which we have bioaccumulation modelling data.

Have the bioavailabilities of trace metals to a suite of biomonitors changed over three decades in SW England estuaries historically affected by mining?

Many estuaries of southwest England were heavily contaminated with toxic metals associated with the mining of copper and other metals, particularly between 1850 and 1900. The question remains whether the passage of time has brought remediation to these estuaries. In 2003 and 2006 we revisited sites in 5 metal-contaminated estuaries sampled in the 1970s and 1980s - Restronguet Creek, Gannel, West Looe, East Looe and Tavy. We evaluate changes in metal contamination in sediments and in metal bioavailabilities in sediments and water to local organisms employed as biomonitors. We find that the decline in contamination in these estuaries is complex. Differences in bioavailable contamination in the water column were detectable, as were significant detectable changes in at least some estuaries in bioavailable metal contamination originating from sediments. However, in the 100 years since mining activities declined, bioavailable contamination has not declined to the regional baseline in any estuary affected by the mine wastes. The greatest decline in contamination occurred in the one instance (East Looe) where a previous industrial source of (Ag) contamination was considered. We used the macroalgae Fucus vesiculosus and Ascophyllum nodosum as biomonitors of dissolved metal bioavailabilities and the deposit feeders Nereis diversicolor and Scrobicularia plana as biomonitors of bioavailable metal in sediments. We found no systematic decrease in the atypically high Ag, Cu, Pb and Zn concentrations in the estuarine sediments over a 26 year period. Accumulated metal (Ag, As, Cu, Pb, and Zn) concentrations in the deposit feeders are similarly still atypically high in at least one estuary for each metal, and there is no consistent evidence for general decreases in sediment metal bioavailabilities over time. We conclude that the legacy of mining in sheltered estuaries of southwest England is the ongoing presence of sediments rich in metals bioavailable to deposit feeders, while dissolved metal bioavailabilities from this historical source alone are no longer atypically high.

Advancing environmental toxicology through chemical dosimetry: external exposures versus tissue residues.

The tissue residue dose concept has been used, although in a limited manner, in environmental toxicology for more than 100 y. This review outlines the history of this approach and the technical background for organic chemicals and metals. Although the toxicity of both can be explained in tissue residue terms, the relationship between external exposure concentration, body and/or tissues dose surrogates, and the effective internal dose at the sites of toxic action tends to be more complex for metals. Various issues and current limitations related to research and regulatory applications are also examined. It is clear that the tissue residue approach (TRA) should be an integral component in future efforts to enhance the generation, understanding, and utility of toxicity testing data, both in the laboratory and in the field. To accomplish these goals, several key areas need to be addressed: 1) development of a risk-based interpretive framework linking toxicology and ecology at multiple levels of biological organization and incorporating organism-based dose metrics; 2) a broadly applicable, generally accepted classification scheme for modes/mechanisms of toxic action with explicit consideration of residue information to improve both single chemical and mixture toxicity data interpretation and regulatory risk assessment; 3) toxicity testing protocols updated to ensure collection of adequate residue information, along with toxicokinetics and toxicodynamics information, based on explicitly defined toxicological models accompanied by toxicological model validation; 4) continued development of residue-effect databases is needed ensure their ongoing utility; and 5) regulatory guidance incorporating residue-based testing and interpretation approaches, essential in various jurisdictions.

Bioaccumulation of arsenic from water and sediment by a deposit-feeding polychaete (Arenicola marina): a biodynamic modelling approach.

Arsenic bioaccumulation in the deposit-feeding polychaete Arenicola marina has been investigated using biodynamic modelling. Radiotracer techniques were used to determine the rates of uptake of As as arsenate from water and sediment and its subsequent efflux in the laboratory. Lugworms accumulated As from solution linearly at concentrations of 2-20 microg l(-1), with a corresponding uptake rate constant of 0.1648+/-0.0135 l g(-1)d(-1). 7.8+/-0.8% (assimilation efficiency) of the As ingested bound to sediments was retained after egestion of unassimilated metal. Elimination of As followed a two-compartment model, with mean efflux rate constants (from the slow pool) very similar for As accumulated from solution and ingested sediments (0.0449+/-0.0034 and 0.0478+/-0.0225 d(-1), respectively) and a corresponding biological half-time of roughly 15 d. A biodynamic model was constructed and validated through the comparison of biodynamic model predictions against measured bioaccumulated concentrations in lugworms from five UK estuaries. The model accurately predicted bioaccumulated As concentrations in lugworms using mean values of relevant physiological parameters (uptake rate, efflux rate and growth rate constants), a site-specific ingestion rate (calculated according to mean worm size and sediment organic matter content and expressed as the rate of ingestion of the mass of fine sediment), a site-specific sediment concentration measured after HCl extraction, and a standard dissolved As concentration. This combination of parameters showed that sediment ingestion contributed 30-60% of the total As accumulated by lugworms at the studied sites, depending on the different geochemistry at each site. This study showed that it is difficult to predict accurately As bioaccumulation at sites with different chemistries, unless that chemistry is taken into account.

Using biodynamic models to reconcile differences between laboratory toxicity tests and field biomonitoring with aquatic insects.

Aquatic insects often dominate lotic ecosystems, yet these organisms are under-represented in trace metal toxicity databases. Furthermore, toxicity data for aquatic insects do not appear to reflect their actual sensitivities to metals in nature, because the concentrations required to elicit toxicity in the laboratory are considerably higher than those found to impact insect communities in the field. New approaches are therefore needed to better understand how and why insects are differentially susceptible to metal exposures. Biodynamic modeling is a powerful tool for understanding interspecific differences in trace metal bioaccumulation. Because bioaccumulation alone does not necessarily correlate with toxicity, we combined biokinetic parameters associated with dissolved cadmium exposures with studies of the subcellular compartmentalization of accumulated Cd. This combination of physiological traits allowed us to make predictions of susceptibility differences to dissolved Cd in three aquatic insect taxa: Ephemerella excrucians, Rhithrogena morrisoni, and Rhyacophila sp. We compared these predictions with long-term field monitoring data and toxicity tests with closely related taxa: Ephemerella infrequens, Rhithrogena hageni, and Rhyacophila brunea. Kinetic parameters allowed us to estimate steady-state concentrations, the time required to reach steady state, and the concentrations of Cd projected to be in potentially toxic compartments for different species. Species-specific physiological traits identified using biodynamic models provided a means for better understanding why toxicity assays with insects have failed to provide meaningful estimates for metal concentrations that would be expected to be protective in nature.

Influences of dietary uptake and reactive sulfides on metal bioavailability from aquatic sediments.

Understanding how animals are exposed to the large repository of metal pollutants in aquatic sediments is complicated and is important in regulatory decisions. Experiments with four types of invertebrates showed that feeding behavior and dietary uptake control bioaccumulation of cadmium, silver, nickel, and zinc. Metal concentrations in animal tissue correlated with metal concentrations extracted from sediments, but not with metal in porewater, across a range of reactive sulfide concentrations, from 0.5 to 30 micromoles per gram. These results contradict the notion that metal bioavailability in sediments is controlled by geochemical equilibration of metals between porewater and reactive sulfides, a proposed basis for regulatory criteria for metals.

Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach.

The bioaccumulation of trace elements in aquatic organisms can be described with a kinetic model that includes linear expressions for uptake and elimination from dissolved and dietary sources. Within this model, trace element trophic transfer is described by four parameters: the weight-specific ingestion rate (IR); the assimilation efficiency (AE); the physiological loss rate constant (ke); and the weight-specific growth rate (g). These four parameters define the trace element trophic transfer potential (TTP = IR.AE/[ke + g]) which is equal to the ratio of the steady-state trace element concentration in a consumer due to trophic accumulation to that in its prey. Recent work devoted to the quantification of AE and ke for a variety of trace elements in aquatic invertebrates has provided the data needed for comparative studies of trace element trophic transfer among different species and trophic levels and, in at least one group of aquatic consumers (marine bivalves), sensitivity analyses and field tests of kinetic bioaccumulation models. Analysis of the trophic transfer potentials of trace elements for which data are available in zooplankton, bivalves, and fish, suggests that slight variations in assimilation efficiency or elimination rate constant may determine whether or not some trace elements (Cd, Se, and Zn) are biomagnified. A linear, single-compartment model may not be appropriate for fish which, unlike many aquatic invertebrates, have a large mass of tissue in which the concentrations of most trace elements are subject to feedback regulation.

Arsenic in benthic bivalves of San Francisco Bay and the Sacramento/San Joaquin River Delta.

Arsenic concentrations were determined in fine-grained, oxidized, surface sediments and in two benthic bivalves, Corbicula sp. and Macoma balthica, within San Francisco Bay, the Sacramento/San Joaquin River Delta, and selected rivers not influenced by urban or industrial activity. Arsenic concentrations in all samples were characteristic of values reported for uncontaminated estuaries. Small temporal fluctuations and low arsenic concentrations in bivalves and sediments suggest that most inputs of arsenic are likely to be minor and arsenic contamination is not widespread in the Bay.

Temporally intensive study of trace metals in sediments and bivalves from a large river-estuarine system: Suisun Bay/Delta in San Francisco Bay.

Distributions in time and space of Ag, Cd, Cr, Cu, Pb and Zn were determined in fine-grained sediments and in the filter-feeding bivalve Corbicula sp. of Suisun Bay/delta at the mouth of the Sacramento and San Joaquin Rivers in North San Francisco Bay. Samples were collected from seven stations at near-monthly intervals for 3 years. Aggregated data showed little chronic contamination with Ag, Zn and Pb in the river and estuary. Substantial chronic contamination with Cd, Cu and Cr in Suisun Bay/delta occurred, especially in Corbicula, compared with the lower San Joaquin River. Salinity appeared to have secondary effects, if any, on metal concentrations in sediments and metal bioavailability to bivalves. Space/time distributions of Cr were controlled by releases from a local industry. Analyses of time series suggested substantial inputs of Cu might originate from the Sacramento River during high inflows to the Bay, and Cd contamination had both riverine and local sources. Concentrations of metals in sediments correlated with concentrations in Corbicula only in annually or 3-year aggregated data. Condition index for Corbicula was reduced where metal contamination was most severe. The biological availability of Cu and Cd to benthos was greater in Suisun Bay than in many other estuaries. Thus small inputs into this system could have greater impacts than might occur elsewhere; and organisms were generally more sensitive indicators of enrichment than sediments in this system.

The modification of an estuary.

The San Francisco Bay estuary has been rapidly modified by human activity. Diking and filling of most of its wetlands have eliminated habitats for fish and waterfowl; the introduction of exotic species has transformed the composition of its aquatic communities; reduction of freshwater inflow by more than half has changed the dynamics of its plant and animal communities; and wastes have contaminated its sediments and organisms. Continued disposal of toxic wastes, the probable further reduction in freshwater inflow, and the possible synergy between the two provide the potential for further alteration of the estuary's water quality and biotic communities.

Bioavailability of trace metals to aquatic organisms--a review.

The physiological characteristics of the environmental interface of organisms determine the metal forms of highest bioavailability. Studies of metal uptake from solution by aquatic organisms verify the high availability of free metal ions. Metals also are accumulated from food by many aquatic organisms, as indicated by both laboratory and field studies. The quantitative importance of the food vector depends upon biological availability, which differs with the specific type of food being ingested. Uptake from both food and solute vectors may be influenced by interactions among cations, pH, redox, temperature and physiological variables. Separating their relative importance through a basic understanding of these processes will be a necessary prerequisite to understanding metal impacts in natural systems.