Trophic transfer of trace metals: subcellular compartmentalization in bivalve prey, assimilation by a gastropod predator and in vitro digestion simulations

Abstract

The uptake of trace metals from the diet is a significant route for their entry into marine animals, and the chemical form of trace metals accumulated by food organisms is one potential factor controlling their assimilation from the diet. Therefore, we investigated relationships between the assimilation efficiencies (AE) of the trace metals Cd, Ag and Zn in the neogastropod mollusc Nassarius festivus and their subcellular compartmentalized fractionation in selected tissues of 4 species of bivalve prey, seeking to identify the relative trophic availabilities of such different fractions. We also sought parallels between the AE of N. festivus and 2 in vitro models of digestion, a generalised invertebrate model and a human digestion model. The bivalves were the scallop Chlamys nobilis, the clam Marcia hiantina, the green mussel Perna viridis and the oyster Saccostrea cucullata, as these show a range of accumulated trace metal concentrations and detoxificatory binding to subcellular compartments. Measured assimilation efficiencies of N. festivus for Cd, Ag and Zn from invertebrate prey tissues are very high in comparison to other marine animals, assimilation occurs from accumulated metal in prey bound in subcellular fractions across the insoluble and soluble spectrum, and assimilation is best modelled in vitro by a human digestion model with low pH (1.3) rather than an invertebrate model (pH 5.6). It is concluded that what is trophically available to one predator (feeding on one prey type) is not necessarily trophically available to another (taxonomically separated) predator even if feeding on the same prey, given the variability between invertebrate digestive systems. Variation in the subcellular distribution of accumulated trace metals within different prey will also add variation in trophic availability even for the same metal.

Assessing abalone growth inhibition risk to cadmium and silver by linking toxicokinetics/toxicodynamics and subcellular partitioning

“…c The risk probability of growth inhibition in water/foodborne Cd and d Ag exposure scenarios. e-g Simulation of biomass of abalone in each life-stage in water/foodborne Cd and h-j Ag exposure scenarios (Cheung and Wang 2005;Rainbow et al 2007;Huang et al 2008;Dubois and Hare 2009;Lapointe et al 2009). This factor may control the metal trophic transfer level.…”

“…Foodborne metal is a significant exposure route affecting the accumulation in marine animals and further in food chains via trophic transfer (Rainbow et al 2007). The interactions among waterborne and foodborne metals and target tissues of aquatic organisms play an important role in the risk assessment of aquatic ecosystems, yet numerous studies only investigated the accumulative capacities in one of these pathways, which is not enough to fully describe the exposure situations for aquatic organisms.…”

Assessment of a subcellular metal partitioning protocol for aquatic invertebrates: preservation, homogenization, and subcellular fractionation

“…For example, the concentration of nonessential metals in heat-stable proteins or granule-like structures is thought to represent metal detoxification, whereas the accumulation of such metals in organelles and some cytosolic enzymes can be a harbinger of metal-induced toxicity (Wallace et al 2003;Campbell and Hare 2009). The subcellular distribution of trace metals in prey items has been shown to influence the facility with which metals are transferred along some aquatic food chains (Wallace and Luoma 2003;Rainbow et al 2007). …”

Differences in trace metal bioaccumulation kinetics among populations of the polychaete Nereis diversicolor from metal-contaminated estuaries

“…We were assisted here by the diverse feeding habits of N. diversicolor, which include oxic sediment ingestion, sediment browsing, carnivory, scavenging and even suspension feeding via a secreted mucus net (Harley 1950). We therefore adapted a method of packaging a food item in gelatin as instigated by Wallace et al (1998) and developed particularly for predatory gastropods (Cheung & Wang 2005, Rainbow et al 2007). For each metal separately, approximately 0.25 g of wet surface (oxic) sediment from the site of collection in the Blackwater estuary was labelled with 2 µCi of radiotracer and left to stand at 4°C for at least 1 mo.…”