Trace metal concentrations in aquatic invertebrates: why and so what?

Metallothioneins in aquatic invertebrates : their role in metal detoxification and their use as biomarkers

Indirect effects of contaminants in aquatic ecosystems.

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 (whe...

Why Is Metal Bioaccumulation So Variable? Biodynamics as a Unifying Concept

▪ Abstract Aquatic insects and other benthic invertebrates are the most widely used organisms in freshwater biomonitoring of human impact. Because of the high monetary investment in freshwater management, decisions are often based on biomonitoring results, and a critical and comparative review of different approaches is required. We used 12 criteria that should be fulfilled by an “ideal” biomonitoring tool, addressing the rationale, implementation, and performance of a method. After illustrating how the century-old but still widely used Saprobian system does not meet these criteria, we apply them to nine recent approaches that range from the suborganismal to the ecosystem level. Although significant progress has been made in the field, no recent approach meets all 12 criteria. Given that the use of biomonitoring information has important financial consequences, we suggest that societies and governments prioritize how these criteria should be ranked.

DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING: A Comparative Analysis of Recent Approaches

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 bivalves Macoma balthica and Potamocorbula 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 -1 Cd and 20.5 µg l -1 Zn, including 109 Cd and 65 Zn as radiotracers. Uptake was followed by 21 d of depuration. The subcellular partitioning of metal within clams was examined following exposure and loss. P. amurensis accumulated ~22 × more Cd and ~2 × more Zn than M. balthica. MT played an important role in the storage of Cd in P. amurensis, while organelles were the major site of Zn accu- mulation. In M. 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. balthica depurated ~40% of Cd with Zn being retained; P. amurensis retained 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 of M. balthica.

https://wwwrcamnl.wr.usgs.gov/tracel/references/pdf/MarEcolProgSer_v249p183.pdf

Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM)

This paper examines how the subcellular partitioning of Cd and Zn in the bivalves Macoma balthica and Potamocorbula amurensis may affect the trophic transfer of metal to predators. Results show that the partitioning of metals to organelles, 'enzymes' and metallothioneins (MT) com- prise 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 -1 Cd and 20.5 µg l -1 Zn, including 109 Cd and 65 Zn as radiotracers, and were used in feeding experiments with grass shrimp Palaemon macrodatylus, or used to investigate the subcellular parti- tioning of metal. Grass shrimp fed Cd-contaminated P. amurensis absorbed ~60% of ingested Cd, which was in accordance with the partitioning of Cd to the bivalve's TAM compartment (i.e. Cd asso- ciated 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 by M. balthica was associated with TAM, while partitioning to TAM in P. amurensis was metal-dependent (~60% for TAM-Cd%, ~73% for TAM-Zn%). The greater TAM-Cd% of P. amuren- sis than M. balthica is due to preferential binding of Cd to MT and 'enzymes', while enhanced TAM- Zn% of P. amurensis results 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 esti- mated that of the 2 bivalves, P. amurensis poses 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.

/pdf/subcellular-compartmentalization-of-cd-and-zn-in-two-cuovrjqfjt.pdf

Subcellular compartmentalization of Cd and Zn in two bivalves. II. Significance of trophically available metal (TAM)

It has been demonstrated that the deposit-feeding oligochaete Limnodrilus hoffmeisteri inhabiting Foundry Cove (FC), a severely cadmium (Cd)-contaminated cove located on the Hudson River, New York, USA, has evolved resistance to Cd. In this study we investigate how this resistance influences Cd trophic transfer from this oligochaete to the grass shri.mp Palaernonetes p u g ~ o . Cadmium-resistant worms collected from FC and nonresistant worms collected from an adjacent unpolluted site were investigated for differences in Cd tolerance, accumulation, subcellular distribution and bioavailability to shrimp. FC worms were more tolerant of Cd, surviving twice as long as worms from the unpolluted site during a toxicity bioassay The 7 d concentration factor of Cd-resistant worms was 4 times greater than that of nonresistant worms (2020 vs 577). There were also differences between worm populations with respect to subc~llular Cd distributions. Cd-resistant worms produced metallothionein-like proteins (MT) as well as metal-nch granules (MRG) for Cd storage and detoxification; nonresistant worms only produced MT These differences in subcellular Cd distributions led to large differences in Cd bioavailability to shrimp; shrimp fed Cd-resistant worms absorbed 21 % of the ingested Cd, while those fed nonresistant worms absorbed roughly 4 times that amount (-757:,). These absorption efficiencies were in good agreement with the proportions of Cd bound to the worm's most biologically available subcellular fractions (i e , the cytosol and organelles). Although Cd-resistant worms predominantly stored the toxic metal In biologically unavailable MRG, their increased accumulation of Cd would still result in substantial trophic transfer to shrimp because of the storage of Cd in the biologically available fractions. This work demonstrates that the evolution of Cd resistance can have profound implications for Cd bioavailability and cycling within aquatic ecosystems.

/pdf/cadmium-resistance-in-an-oligochaete-and-its-effect-on-147t6rjyhs.pdf

Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp

/pdf/bioavailability-of-biologically-sequestered-cadmium-and-the-4fh1kihyp4.pdf

Bioavailability of biologically sequestered cadmium and the implications of metal detoxification

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.

/pdf/linking-metal-bioaccumulation-of-aquatic-insects-to-their-sfv8m1l35y.pdf

William G. Wallace

Papers

Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM)

Subcellular compartmentalization of Cd and Zn in two bivalves. II. Significance of trophically available metal (TAM)

Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp

Bioavailability of biologically sequestered cadmium and the implications of metal detoxification

Linking metal bioaccumulation of aquatic insects to their distribution patterns in a mining-impacted river