Influence of sediment‐organic matter quality on growth and polychlorobiphenyl bioavailability in Echinodermata (Amphiura filiformis)

Abstract

Abstract-Sediment total organic carbon (TOC) content is considered to be a primary food source for benthic invertebrates and a major factor influencing the partitioning and bioavailability of sediment-associated organic contaminants. Most studies report that both toxicity and uptake of sediment-associated contaminants by benthic organisms are inversely proportional to sediment TOC content. The aim of this study was to determine the importance of the TOC quality for the bioavailability of sediment-associated organic contaminants and the growth of benthic macrofauna. The common infaunal brittle star Amphiura filiformis was exposed to a base sediment covered by a 14 C-polychlorobiphenyl (3,3Ј4,4ЈϪ 14 C-tetrachlorobiphenyl (TCB)) contaminated top layer (0-2 cm), enriched to the same TOC content with 31 g TOC/m 2 of different quality and origin. The following carbon sources, ranging from labile to refractory, were used: (1) green macroalga (Ulva lactuca), (2) brown macroalga (Ascophyllum nodosum), (3) eelgrass (Zostera marina), (4) phytoplankton (Ceratium spp.), and (5) lignins of terrestrial origin. Characterization of the organic matter quality was accomplished by measuring the content of amino acids, lipids, C, N, and polyphenolic compounds. The reactivity of the sedimentary organic matter was assessed by means of respiration and dissolved inorganic nitrogen flux measurements. The experiment was carried out in 1-L glass jars, each containing four brittle stars and the contaminated and enriched sediment. The jars were circulated in a flow-through mode with filtered seawater. Somatic growth (regeneration of a precut arm) and bioaccumulation of 14 C-TCB were measured at 10 sampling occasions during 48 d of exposure. Growth rates, TCB uptake rates, and steady-state concentrations differed significantly between treatments and were correlated to the qualities of the organic substrates. The greatest TCB accumulation and growth were observed in treatments with the most labile organic substrates and the lowest accumulation and growth were seen with the most refractory substrates. Results from this experiment suggest that the bioaccumulation of organic contaminants in benthic infauna is dependent on the nutritional quality of the sedimentary organic matter.

Effects of sediment organic matter quality on bioaccumulation, degradation, and distribution of pyrene in two macrofaunal species and their surrounding sediment

“…Bannister (2004) furthermore report arm regeneration to be highly temperature dependent in A. filiformis, a feature correlating with field measurements of seasonal variations in regeneration rates observed among ophiurids (Sköld, Loo & Rosenberg, 1994, Stancyk, Golde, Papelindstrom & Dobson, 1994. Arm regeneration rates were comparably low in our study (0.13 mm d -1 ) (Nilsson & Sköld, 1996, Gunnarsson et al, 1999a. Consequently, as experiments were performed at low temperatures (+5 °C) in both the present study and in the study by Selck et al (2005), possible treatment effects might not have had sufficient time to develop during the 45 d exposure due to a general slow growth.…”

“…In the present study, we specifically tested the effect of SOM quality by keeping TOC constant and altering nitrogen and amino acid levels through the choice of organic matter sources. Other studies with this design report positive correlations between SOM quality and accumulation of both PCB and cadmium in A. filiformis and of pyrene in the mud snail Hydrobia ulvae (Maloney, 1996, Gunnarsson et al, 1999a, Granberg & Forbes, 2006. The important message supported by all these studies is, however, that during a labile SOM enrichment situation, such as associated with the occurrence and sedimentation of a phytoplankton bloom, accumulation of sediment-associated contaminants increases.…”

“…Arm regeneration has been suggested as a possible screening tool for contaminant exposure filiformis as a function of increased SOM quality while no effects have been observed of either PCB or benzo(a)pyrene , Gunnarsson et al, 1999a, Nilsson, 1999. Carnevali et al (2001b) do however, report hormesis like increased arm regeneration in A. mediterranea after chronic low dose PCB exposure, and pyrene exerted a vague growth stimulation in A. filiformis at low concentrations, while reduced arm regeneration was reported at exposure concentrations exceeding that used in this study (Bannister, 2004).…”

“…Such physiological response due to changes in food value is likely also to affect the absorption, metabolism and general fate of sediment associated contaminants. E xperimental enrichment with high quality SOM has previously been reported to stimulate the accumulation of sediment associated PCBs and PAHs in various marine invertebrates (Gunnarsson, Granberg, Nilsson, Rosenberg & Hellman, 1999a, Gunnarsson, Hollertz & Rosenberg, 1999b, Gunnarsson & Sköld, 1999, Granberg & Forbes, 2006, while effects of SOM quality on contaminant metabolism and toxicity are largely unexplored. Furthermore, the stimulating effect of increased SOM quality on general microbial mineralization is well documented (Graf, Schulz, Peinert & Meyer-Reil, 1983, 6 Meyer-Reil, 1983, while information is scarce on its effects on the microbial degradation of organic contaminants in sediments.…”

“…Amputation of distinct arms separated individuals into four identifiable groups, and 8 only individuals differing in positioning of the cut arm were placed in the same experimental jar. Subsequent to amputation, brittle stars were returned to the sediment in flow through storage aquaria (32 psu, 5 °C) and left to heal and form scars, a procedure proven important for proper measurements of regeneration rates (Gunnarsson et al, 1999a, Selck, Granberg & Forbes, 2005 Tenore, Cammen, Findlay & Phillips, 1982, Mayer, 1989, Gunnarsson et al, 1999a. Tetraselmis sp.…”