Sedimentary metal bioavailability determined by the digestive constraints of marine deposit feeders:gut retention time and dissolved amino acids

Abstract

Contaminant metals bound to sediments are subject to considerable solubilization during passage of the sediments through the digestive systems of deposit feeders. We examined the kinetics of this process, using digestive fluids extracted from deposit feeders Arenicola manna and Parastichopus californicus and then incubated with contaminated sediments. Kinetics are complex, with solubilization followed occasionally by readsorption onto the sediment. In general, solubilization kinetics are biphasic, with an initial rapid step followed by a slower reaction. For many sediment-organism combinations, the reaction will not reach a steady state or equilibrium within the gut retention time (GRT) of the organisms, suggesting that metal bioavailability in sediments is a time-dependent parameter Experiments with commercial protein solutions mimic the kinetic patterns observed with digestive fluids, which corroborates our previous study that complexation by dissolved amino acids (AA) in digestive fluids leads to metal solubilization (Chen & Mayer 1998b, Environ Sci Technol 32:770-378). The relative importance of the fast and slow reactions appears to depend on the ratio of ligands In gut fluids to the amount of bound metal in sediments. High ligand to sohd metal ratios result in more metals released in fast reactions and thus higher lability of sedimentary metals Multiple extractions of a sediment with dgestive fluid of A. marina confirm the potential importance of incomplete reactions within a single deposit-feeding event, and make clear that bioavailabllity to a slngle animal is l~kely different from that to a community of organisms. The con~plex k~netic patterns lead to the counterintuit~ve prediction that toxification of digestive enzymes by solubillzed metals wlll occur more readily in species that dissolve less metals.

Effects of settling organic matter on the bioaccumulation of cadmium and BDE-99 by Baltic Sea benthic invertebrates

“…The dissolution of a contaminated substrate will make the associated contaminant more available for uptake, thereby explaining the higher bioaccumulation of Cd and PBDE in the Tetraselmis treatment. In a situation when ingested OM is incompletely dissolved during gut passage (as probably to a large extent is the case for lignin and sedimentary OM) contaminant dissolution and subsequent bioavailability will depend on a competition between dissolved solubilizing agents in the gut fluid and the binding strength of the particulate ingested substrates (Chen and Mayer, 1999). Thus, a higher affinity of Cd to ingested sediment than to ingested lignin could result in different bioavailability and subsequent bioaccumulation of Cd from these OM sources.…”

“…However, since the contaminants were added in the same OM treatment and with the assumption that the animals have the same feeding behavior in each experimental core, there must be differences in uptake routes and sorption capacities between the organic matter and cadmium and BDE-99. This is possibly an indication of differences in solubilization capacity of Cd and PBDE by Macoma digestive fluid in combination with the binding strength of the substrates (sensu Chen and Mayer, 1999). Moreover, Macoma differs from the other two species in their assimilation of organic matter (Decho and Luoma, 1996) and their ability to sort particles in their gills, where some particles are rejected and excreted as pseudo-feces (Decho and Luoma, 1991).…”

“…For example, a higher ingestion rate of nutritious organic material has been observed to lead to higher bioaccumulation of associated contaminants (Granberg and Forbes, 2006). Furthermore, differences in properties of the digestive fluid, intracellular digestion, gut retention time as well as elimination capacities have all been shown to influence the bioaccumulation of both HOCs and metals (Decho and Luoma, 1996;Chen and Mayer, 1999;Mayer et al, 2001;Griscom et al, 2002a).…”

“…Animal morphology as well as physiological and biochemical properties of the digestive system have also been shown to influence the bioavailability of sediment-associated contaminants (Mayer et al, 1996;Chen and Mayer, 1999;Mayer et al, 2001). …”

Dissolution of particle‐reactive radionuclides in deposit‐feeder digestive fluids

“…Benthic deposit feeders secrete digestive agents such as hydrolytic enzymes and surfactants to hydrolyze and solubilize absorbable food items from sediments (Mayer et al 1997). Digestive fluids of deposit feeders contain high concentrations of various dissolved organic compounds that can serve as ligands for binding and solubilizing metals (Mayer et al 1996;Chen and Mayer 1999;Chen et al 2000).…”