► Trace metal toxicity is not typically directly related to total accumulated body concentration. ► Trace metal toxicity is related to total rate of trace metal uptake. ► Trace metal toxicity is ...related to a critical concentration of metabolically available metal. ► Critical concentration of metabolically available zinc in a crustacean is estimated as 150
μg
g
−1.
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.
Ecological risks from metal contaminants are difficult to document because responses differ among species, threats differ among metals, and environmental influences are complex. Unifying concepts are ...needed to better tie together such complexities. Here we suggest that a biologically based conceptualization, the biodynamic model, provides the necessary unification for a key aspect in risk: metal bioaccumulation (internal exposure). The model is mechanistically based, but empirically considers geochemical influences, biological differences, and differences among metals. Forecasts from the model agree closely with observations from nature, validating its basic assumptions. The biodynamic metal bioaccumulation model combines targeted, high-quality geochemical analyses from a site of interest with parametrization of key physiological constants for a species from that site. The physiological parameters include metal influx rates from water, influx rates from food, rate constants of loss, and growth rates (when high). We compiled results from 15 publications that forecast species-specific bioaccumulation, and compare the forecasts to bioaccumulation data from the field. These data consider concentrations that cover 7 orders of magnitude. They include 7 metals and 14 species of animals from 3 phyla and 11 marine, estuarine, and freshwater environments. The coefficient of determination (R 2) between forecasts and independently observed bioaccumulation from the field was 0.98. Most forecasts agreed with observations within 2-fold. The agreement suggests that the basic assumptions of the biodynamic model are tenable. A unified explanation of metal bioaccumulation sets the stage for a realistic understanding of toxicity and ecological effects of metals in nature.
Many aspects of metal accumulation in aquatic invertebrates (i.e. toxicity, tolerance and trophic transfer) can be understood by examining the subcellular partitioning of accumulated metal. In this ...paper, we use a compartmentalization approach to interpret the significance of metal, species and size dependence in the subcellular partitioning of Cd and Zn in the bivalvesMacoma balthicaandPotamocorbula amurensis. Of special interest is the compartmentalization of metal as metal-sensitive fractions (MSF) (i.e. organelles and heat-sensitive proteins, termed ‘enzymes’ hereafter) and biologically detoxified metal (BDM) (i.e. metallothioneins MT and metal-rich granules MRG). Clams from San Francisco Bay, CA, were exposed for 14 d to seawater (20‰ salinity) containing 3.5 μg l–1Cd and 20.5 μg l–1Zn, including109Cd and65Zn as radiotracers. Uptake was followed by 21 d of depuration. The subcellular partitioning of metal within clams was examined following exposure and loss.P. amurensisaccumulated ~22× more Cd and ~2× more Zn thanM. balthica. MT played an important role in the storage of Cd inP. amurensis, while organelles were the major site of Zn accumulation. InM. balthica, Cd and Zn partitioned similarly, although the pathway of detoxification was metal-specific (MRG for Cd; MRG and MT for Zn). Upon loss,M. balthicadepurated ~40% of Cd with Zn being retained;P. amurensisretained Cd and depurated Zn (~40%). During efflux, Cd and Zn concentrations in the MSF compartment of both clams declined with metal either being lost from the animal or being transferred to the BDM compartment. Subcellular compartmentalization was also size-dependent, with the importance of BDM increasing with clam size; MSF decreased accordingly. We hypothesized that progressive retention of metal as BDM (i.e. MRG) with age may lead to size dependency of metal concentrations often observed in some populations ofM. balthica.
This paper examines how the subcellular partitioning of Cd and Zn in the bivalvesMacoma balthicaandPotamocorbula amurensismay affect the trophic transfer of metal to predators. Results show that the ...partitioning of metals to organelles, ‘enzymes’ and metallothioneins (MT) comprise a subcellular compartment containing trophically available metal (TAM; i.e. metal trophically available to predators), and that because this partitioning varies with species, animal size and metal, TAM is similarly influenced. Clams from San Francisco Bay, California, were exposed for 14 d to 3.5 μg l–1Cd and 20.5 μg l–1Zn, including109Cd and65Zn as radiotracers, and were used in feeding experiments with grass shrimpPalaemon macrodatylus, or used to investigate the subcellular partitioning of metal. Grass shrimp fed Cd-contaminatedP. amurensisabsorbed ~60% of ingested Cd, which was in accordance with the partitioning of Cd to the bivalve’s TAM compartment (i.e. Cd associated with organelles, ‘enzymes’ and MT); a similar relationship was found in previous studies with grass shrimp fed Cd-contaminated oligochaetes. Thus, TAM may be used as a tool to predict the trophic transfer of at least Cd. Subcellular fractionation revealed that ~34% of both the Cd and Zn accumulated byM. balthicawas associated with TAM, while partitioning to TAM inP. amurensiswas metal-dependent (~60% for TAM-Cd%, ~73% for TAM-Zn%). The greater TAM-Cd% ofP. amurensisthanM. balthicais due to preferential binding of Cd to MT and ‘enzymes’, while enhanced TAM-Zn% ofP. amurensisresults from a greater binding of Zn to organelles. TAM for most species–metal combinations was size-dependent, decreasing with increased clam size. Based on field data, it is estimated that of the 2 bivalves,P. amurensisposes the greater threat of Cd exposure to predators because of higher tissue concentrations and greater partitioning as TAM; exposure of Zn to predators would be similar between these species.
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.
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
μg
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.
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.
► SW England estuaries are contaminated with toxic metals from historical mining. ► High metal concentrations remain in the sediments. ► High metal concentrations still in biomonitors of sediment contamination. ► Mining legacy is sediments rich in metals bioavailable to deposit feeders. ► Bioavailabilities of dissolved metals from historical mining are no longer high.
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 (
k
e
); and the weight-specific growth rate (
g). These four parameters define the trace element trophic transfer potential (TTP=IR·AE/
k
e
+
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
k
e
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.
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.
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 sizefeatures 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.
PDF
