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 100years 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 26year 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.

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.

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. Integr Environ Assess Manag 2011;7:7–27. © 2010 SETAC

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 2–20μgl−1, with a corresponding uptake rate constant of 0.1648±0.0135lg−1d−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±0.0225d−1, respectively) and a corresponding biological half-time of roughly 15d. 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.

Biodynamic modelling has been used to predict bioaccumulated concentrations of Ag, Cd and Zn in the deposit-feeding polychaete Nereis diversicolor from 5 metal-contaminated estuar- ies in SW England and a relatively non-contaminated estuary in SE England. The modelling employed previously measured physiological parameters of bioaccumulation — uptake rate constant, assimilation efficiency (AE) and efflux rate constants after uptake from water and sediment inges- tion — and measured sediment metal concentrations specific for each population. AEs were consid- ered to relate to metals in the organic component of the ingested sediment and ingestion rates were therefore expressed in these terms, with the further assumption that the total sediment metal concen- tration is a proxy for the metal concentration in the sediment organic component. A range of growth rate constants was extracted from the literature, as were concentration ranges of dissolved Ag, Cd and Zn in contaminated coastal waters. The model showed that >99% Cd and >98% Zn accumulated by N. diversicolor is derived from sediment ingestion; more bioaccumulated Ag is derived from solu- tion, the percentage contribution of the dissolved source increasing from 46 to 80% with an increase in Ag dissolved concentration from low to high values for coastal waters. Bioaccumulated metal con- centrations predicted from the model generally showed excellent agreement with independently measured concentrations in field-collected worms, supporting the assumptions made in the model.

Aquatic organisms exposed to atypically high local bioavailabilities of a toxic metal may come under selection for changes in one or more physiological processes, including the rate of metal uptake from an available source of the metal, the rate of efflux and the rate of detoxification of accumulated metal into a relatively metabolically inert form. We investigated parameters of the bioaccumulation kinetics of the toxic metals Ag, Cd and Zn in populations of the estuarine polychaete worm Nereis diversicolor from differentially metal-contaminated sediments of 5 metal-rich estuaries in SW England and a relatively non-contaminated control estuary in SE England. One population (from Restronguet Creek, Cornwall) is known to be tolerant to raised availabilities of Zn and Cu. We compared uptake rate constants from solution (K.) and assimilation efficiencies (AE) from sediment, and subsequent efflux rate constants (K,,) after uptake (from either water or ingested sediment) for each of the 3 metals among all populations. There was some limited interpopulation variation in the biodynamic parameters controlling bioaccumulation (and potential ecotoxicity) of trace metals between populations. There did not, however, appear to be consistent patterns to Such variation. The basis of Zn tolerance in the Restronguet Creek population is not due to a reduction of Zn uptake from either solution or ingested sediment, or increased efflux of Zn accumulated after uptake from either route. The most likely mechanism is, therefore, an increased capacity for storage detoxification of Zn accumulated after regulation of Zn body concentration has broken down.

Diet is an important exposure route for the uptake of trace metals by aquatic invertebrates, with trace metal trophic transfer depending on 2 stages-assimilation and subsequent accumulation by the predator. This study investigated the trophic transfer of trace metals from the sediment-dwelling polychaete worm Nereis diversicolor from metal-rich estuarine sediments in southwestern UK to 2 predators -another polychaete N. virens (Cu, Zn, Pb, Cd, Fe) and the decapod crustacean Palaemonetes varians (Cu, Zn, Pb, Cd, Fe, Ag, As, Mn). N. virens showed net accumulation of Cu, Zn, Pb and Cd from the prey; accumulation increased with increasing prey concentration, but a coefficient of trophic transfer decreased with increasing prey concentration, probably because a higher proportion of accumulated metal in the prey is bound in less trophically available (insoluble) detoxified forms. The trace metal accumulation patterns of P. varians apparently restricted significant net accumulation of metals from the diet of N. diversicolor to just Cd. There was significant mortality of the decapods fed on the diets of metal-rich worms. Metal-rich invertebrates that have accumulated metals from the rich historical store in the sediments of particular SW England estuaries can potentially pass these metals along food chains, with accumulation and total food chain transfer depending on the metal assimilation efficiencies and accumulation patterns of the animal at each trophic level. This trophic transfer may be significant enough to have ecotoxicological effects.

The chemical form of accumulated trace metal in prey is important in controlling the bioavailability of dietary metal to a predator. This study investigated the trophic transfer of radio- labelled Ag, Cd and Zn from the polychaete worm Nereis diversicolor to the decapod crustacean Palaemonetes varians. We used 2 populations of worms with different proportions of accumulated metals in different subcellular fractions as prey, and loaded the worms with radiolabelled metals either from sediment or from solution. Accumulated radiolabelled metals were fractionated into 5 components:metal-rich granules (MRG), cellular debris, organelles, metallothionein-like proteins (MTLP), and other (heat-sensitive) proteins (HSP). Assimilation efficiencies (AE) of the metals by P. varians were measured from the 4 categories of prey (i.e. 2 populations, radiolabelled from sediment or solution). There were significant differences for each metal between the AEs from the different prey categories, confirming that origin of prey and route of uptake of accumulated trace metal will cause intraspecific differences in subsequent metal assimilation. Correlations were sought between AEs and selected fractions or combinations of fractions of metals in the prey-MRG, Trophically Avail- able Metal (TAM = MTLP + HSP + organelles) and total protein (MTLP + HSP). TAM explained 28% of the variance in AEs for Ag, but no consistent relationships emerged between AEs and TAM or total protein when the metals were considered separately. AEs did, however, show significant positive regressions with both TAM and total protein when the 3 metals were considered together, explain- ing only about 21% of the variance in each case. A significant negative relationship was observed between MRG and AE for all metals combined. The predator (P. varians) can assimilate dietary metal from a range of the fractions binding metals in the prey (N. diversicolor), with different assimilation efficiencies summated across these fractions. TAM and/or total protein may represent an approxi- mate minimum for trophic availability but neither of these alone is a fully accurate predictor.

Delineation of metal uptake routes in aquatic invertebrates is critical for characterizing bioaccumulation dynamics and assessing risks associated with metal exposure. Here we demonstrate that Cu stable isotopic ratios can be manipulated in both exposure media and algae to determine the efflux rate constant ( k e ) and to estimate Cu assimilation efficiency (AE) from ingested food in a freshwater bivalve ( Corbicula fluminea ). The Cu AE in Corbicula fed 65 Cu‐spiked Cryptomonas ozolini was 38%. Copper uptake routes had no significant influence on efflux; k e of 0.004 per day characterized the slowest component of efflux following short‐term exposures to 65 Cu in water or in both food and water. Incorporation of the physiological parameters for dietary and dissolved uptake as well as rate constants of loss into a bioaccumulation model allowed for assessing the relative contribution of water and food as Cu sources. At [ 65 Cu 2+ ] of 6.7 μg/L, Corbicula accumulated twice as much Cu from diet as from water. In most freshwater systems, the dietary pathway is likely to act as the major Cu uptake route for Corbicula . Extrapolation of our laboratory results to the San Francisco Bay—Delta (California, USA) indicated that our biodynamic model and the laboratory‐derived parameters for dietary 65 Cu uptake provided a realistic representation of the processes involved in Cu accumulation by the bivalve Corbicula .

This study examined the extent to which dissolved Cd and Zn uptake rates vary in several aquatic insect taxa commonly used as indicators of ecological health. We further attempted to explain the mechanisms underlying observed differences. By comparing dissolved Cd and Zn uptake rates in several aquatic insect species, we demonstrated that species vary widely in these processes. Dissolved uptake rates were not related to gross morphological features such as body size or gill size-features that influence water permeability and therefore have ionoregulatory importance. However, finer morphological features, specifically, the relative numbers of ionoregulatory cells (chloride cells), appeared to be related to dissolved metal uptake rates. This observation was supported by Michaelis-Menten type kinetics experiments, which showed that dissolved Cd uptake rates were driven by the numbers of Cd transporters and not by the affinities of those transporters to Cd. Calcium concentrations in exposure media similarly affected Cd and Zn uptake rates in the caddisfly Hydropsyche californica. Dissolved Cd and Zn uptake rates strongly co-varied among species, suggesting that these metals are transported by similar mechanisms.

We conducted a study with cadmium (Cd) and copper (Cu) in the delta of San Francisco Bay, using nitrogen and carbon stable isotopes to identify trophic position and food web structure. Cadmium is progressively enriched among trophic levels in discrete epiphyte-based food webs composed of macrophyte-dwelling invertebrates (the first link being epiphytic algae) and fishes (the first link being gobies). Cadmium concentrations were biomagnified 15 times within the scope of two trophic links in both food webs. Trophic enrichment in invertebrates was twice that of fishes. No tendency toward trophic-level enrichment was observed for Cu, regardless of whether organisms were sorted by food web or treated on a taxonomic basis within discrete food webs. The greatest toxic effects of Cd are likely to occur with increasing trophic positions, where animals are ingesting Cd-rich prey (or food). In Franks Tract this occurs within discrete food chains composed of macrophyte-dwelling invertebrates or fishes inhabiting submerged aquatic vegetation. Unraveling ecosystem complexity is necessary before species most exposed and at risk can be identified.

Characterization of uptake and loss dynamics is critical to understanding risks associated with contaminant exposure in aquatic animals. Dynamics are especially important in addressing questions such as why coexisting species in nature accumulate different levels of a contaminant. Here we manipulated copper (Cu) stable isotopic ratios (as an alternative to radioisotopes) to describe for the first time Cu dynamics in a freshwater invertebrate, the bivalve Corbicula fluminea. In the laboratory, Corbicula uptake and loss rate constants were determined from an environmentally realistic waterborne exposure to 65Cu (5.7 microg L(-1)). That is, we spiked deionized water with Cu that was 99.4% 65Cu. Net tracer uptake was detectable after 1 day and strongly evident after 4 days. Thus, short-term exposures necessary to determine uptake dynamics are feasible with stable isotopes of Cu. In Corbicula, 65Cu depuration was biphasic. An unusually low rate constant of loss (0.0038 d(-1)) characterized the slow component of efflux, explaining why Corbicula strongly accumulates copper in nature. We incorporated our estimates of rate constants for dissolved 65Cu uptake and physiological efflux into a bioaccumulation model and showed that dietary exposure to Cu is likely an important bioaccumulation pathway for Corbicula.

Chemical contaminants disrupt ecosystems, but specific effects may be under-appreciated when poorly known processes such as uptake mechanisms, uptake via diet, food preferences, and food web dynamics are influential. Here we show that a combination of food web structure and the physiology of trace element accumulation explain why some species in San Francisco Bay are threatened by a relatively low level of selenium contamination and some are not. Bivalves and crustacean zooplankton form the base of two dominant food webs in estuaries. The dominant bivalve Potamocorbula amurensis has a 10-fold slower rate constant of loss for selenium than do common crustaceans such as copepods and the mysid Neomysis mercedis (rate constant of loss, ke = 0.025, 0.155, and 0.25 d(-1), respectively). The result is much higher selenium concentrations in the bivalve than in the crustaceans. Stable isotope analyses show that this difference is propagated up the respective food webs in San Francisco Bay. Several predators of bivalves have tissue concentrations of selenium that exceed thresholds thought to be associated with teratogenesis or reproductive failure (liver Se >15 microg g(-1) dry weight). Deformities typical of selenium-induced teratogenesis were observed in one of these species. Concentrations of selenium in tissues of predators of zooplankton are less than the thresholds. Basic physiological and ecological processes can drive wide differences in exposure and effects among species, but such processes are rarely considered in traditional evaluations of contaminant impacts.

Although the differential responses of stream taxa to metal exposure have been exploited for bioassessment and monitoring, the mechanisms affecting these responses are not well understood. In this study, the subcellular partitioning of metals in operationally defined metal-sensitive and detoxified fractions were analyzed in five insect taxa. Samples were collected in two separate years along an extensive metal contamination gradient in the Clark Fork River (MT, USA) to determine if interspecific differences in the metal concentrations of metal-sensitive fractions and detoxified fractions were linked to the differences in distributions of taxa relative to the gradient. Most of the Cd, Cu, and Zn body burdens were internalized and potentially biologically active in all taxa, although all taxa appeared to detoxify metals (e.g., metal bound to cytosolic metal-binding proteins). Metal concentrations associated with metal-sensitive fractions were highest in the mayflies Epeorus albertae and Serratella tibialis, which were rare or absent from the most contaminated sites but occurred at less contaminated sites. Relatively low concentrations of Cu were common to the tolerant taxa Hydropsyche spp. and Baetis spp., which were widely distributed and dominant in the most contaminated sections of the river. This suggested that distributions of taxa along the contamination gradient were more closely related to the bioaccumulation of Cu than of other metals. Metal bioaccumulation did not appear to explain the spatial distribution of the caddisfly Arctopsyche grandis, considered to be a bioindicator of metal effects in the river. Thus, in this system the presence/ absence of most of these taxa from sites where metal exposure was elevated could be differentiated on the basis of differences in metal bioaccumulation.

Contaminant exposures in natural systems can be highly variable. This variability is superimposed upon cyclic variability in biological processes. Together, these factors can confound determination of contaminant effects. Long term, multidisciplined studies with high frequency sampling can be effective in overcoming such obstacles. While studying trace metal contamination in the tissues of the clam, Potamocorbula amurensis, in the northern reach of San Francisco Bay, an episode of high Ag concentrations was identified (maximum of 5.5 mug g(-1)) at two mid-estuary sites. High concentrations were not seen in clams up-estuary (maximum of 1.92 mug g(-1)) from these sites and were reduced down-estuary (maximum of 2.67 mug g(-1)). Silver is not common naturally in the environment, so its elevated presence is usually indicative of anthropogenic influences such as municipal and industrial discharge. Monthly sampling of reproductive status of clams characterized the reproductive cycle and differences in the patterns of reproductive activity that corresponded to changes in Ag tissue concentrations. The proportion of reproductive clams was less than 60% during periods when tissue concentrations were high (generally >2 mug g(-1)). When tissue concentrations of Ag decreased (less than or equal to1 mug g(-1)), the proportion of reproductive clams was 80 to 100%. A comparison between the annual proportion of reproductive clams and annual Ag tissue concentrations showed a significant negative correlation. No other measured environmental variables were correlated with reproductive impairment. The weight-of-evidence approach strongly supports a cause and effect relationship between Ag contamination and reduced reproductive activity in P. amurensis.

Following the aggressive invasion of the bivalve, Potamocorbula amurensis, in the San Francisco Bay-Delta in 1986, selenium contamination in the benthic food web increased. Concentrations in this dominant (exotic) bivalve in North Bay were three times higher in 1995-1997 than in earlier studies, and 1990 concentrations in benthic predators (sturgeon and diving ducks) were also higher than in 1986. The contamination was widespread, varied seasonally and was greater in P. amurensis than in co-occurring and transplanted species. Selenium concentrations in the water column of the Bay were enriched relative to the Sacramento River but were not as high as observed in many contaminated aquatic environments. Total Se concentrations in the dissolved phase never exceeded 0.3 microg Se per l in 1995 and 1996; Se concentrations on particulate material ranged from 0.5 to 2.0 microg Se per g dry weight (dw) in the Bay. Nevertheless, concentrations in P. amurensis reached as high as 20 microg Se per g dw in October 1996. The enriched concentrations in bivalves (6-20 microg Se per g dw) were widespread throughout North San Francisco Bay in October 1995 and October 1996. Concentrations varied seasonally from 5 to 20 microg Se per g dw, and were highest during the periods of lowest river inflows and lowest after extended high river inflows. Transplanted bivalves (oysters, mussels or clams) were not effective indicators of either the degree of Se contamination in P. amurensis or the seasonal increases in contamination in the resident benthos. Se is a potent environmental toxin that threatens higher trophic level species because of its reproductive toxicity and efficient food web transfer. Bivalves concentrate selenium effectively because they bioaccumulate the element strongly and lose it slowly; and they are a direct link in the exposure of predaceous benthivore species. Biological invasions of estuaries are increasing worldwide. Changes in ecological structure and function are well known in response to invasions. This study shows that changes in processes such as cycling and effects of contaminants can accompany such invasions.

Concentrations of Cu, As, Pb, Zn and Ag (but not Cd, Co, Fe, Mn and Hg) in the tissues of benthic algae (Fucus vesiculosus) correlate significantly with concentrations in sediment. Metals which complex most strongly with algal tissues show the strongest correlations of algal tissue and sediment. Scavenging these metals from particulates may be an important source of uptake by the algae. If so, concentrations of Cu, As, Pb, Zn and Ag in algal tissues may not be good indicators of concentrations of these metals in solution.

Here we ask what types of field studies can best detect interactions among stressors and allow us to separate and rank the relative importance of individual stressors in systems receiving multiple disturbances (natural and/or anthropogenic). If multiple stressor responses are common in nature, then single variable tests, such as analysis of a biomarker in isolation or along a surmised gradient, or studies that exclude variables other than pollutants, could be insensitive to all but the most extreme influences of contamination. Preponderance of evidence approaches will be similarly insensitive if designs are too simplistic. A combination of persistent and intensive study of exposure and response in the field, study of critical ecosystem-specific and organism-specific processes, as well as iteration with experimental studies, are useful (and perhaps necessary) strategies to discern interactions among stressors. As our understanding of the mechanisms responsible for changes at lower levels of organization improves, responses to complex stressors become more predictable. This improved mechanistic understanding could lead to a similar degree of understanding for responses at higher levels of biological organization. Below we discuss three examples where researchers have attempted to identify and quantify the relative importance of individual stressors in systems receiving complex stressors. The firstmore » example demonstrates how intensive field studies identified multiple stressors and how a management plan resulted in mitigation of these stressors. The second example describes a series of field experiments designed to identify the relative importance of water quality and substrate quality on benthic macroinvertebrates in a metal-polluted stream. The final example illustrates the difficulty of sorting out the direct and indirect influences of global climate change on populations.« less