Uptake, transfer and distribution of silver and cobalt in tissues of the common cuttlefish Sepia officinalis at different stages of its life cycle

Abstract

Three pathways of exposure (sediment, seawater and food) were examined to determine transfer of 110m Ag and 57 Co in juvenile cuttlefish Sepia officinalis. Additional experiments were conducted on adult cuttlefish and their eggs/embryos in order to assess bioaccumulation patterns at different stages of the organism's life cycle. Eggs, juveniles and adults readily accumulated both Ag and Co from seawater. In eggs, both metals were predominantly adsorbed onto the capsule membrane (≥ 60% for Ag and ≥ 99% for Co), indicating that the latter may act as an effective shield to limit exposure of embryos to soluble metals. Adult cuttlefish incorporated waterborne radiotracers mainly in their muscular tissues (≥ 60% of the whole-body burden); subsequent metal retention was greater for Co (biological half-life, T b ! = 34 d) than for Ag (T b ! = 7 d). Turnover of Co ingested with food was much more rapid in juveniles (T b ! = 5 d) than in adults (T b ! = 990 d), suggesting that the functional maturation of the digestive gland was not complete in the juveniles. With ingested Ag, retention was roughly similar for juveniles and adults (T b ! = 13 and 9 d, respectively). Transfer from sediments was negligible for Co and Ag. Regardless of the exposure pathway, the digestive gland of juveniles and adults contained the major fraction of incorporated metal either following uptake or after depuration. This observation demonstrates that substantial metal transfer takes place from several organs to the digestive gland, and further highlights the major role this organ plays in metal storage and detoxification processes in these cephalopods. KEY WORDS: Metal · Radiotracer · Bioaccumulation · Digestive gland · CephalopodsResale or republication not permitted without written consent of the publisher

Effects of increased <i>p</i>CO<sub>2</sub> and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, <i>Sepia officinalis</i>

“…110m Ag was efficiently accumulated in the cuttlefish embryo, as previously demonstrated (Bustamante et al, 2004;Lacoue-Labarthe et al, 2008a), presumably from the time when the water permeability of the eggshell changed and the perivitelline fluid started to increase in volume. A few hours before hatching, the higher 110m Ag CF values recorded in the perivitelline fluid compared to the other elements highlighted the capacity of Ag to concentrate in the perivitelline space.…”

“…During the embryonic development of cuttlefish, the greatest amounts of the metals, such as Ag, 241 Am, Cd, Co, Hg, Mn, Pb and Zn, remain associated with the eggshell (Bustamante et al, 2002(Bustamante et al, , 2004Lacoue-Labarthe et al 2008a, 2009a. Indeed, the eggshell contains a high proportion of mucin proteins that also have a high content of sulfydrilgroups (Boletzky, 1986) for which Ag, Cd and Zn have a high affinity (e.g., Wedemeyer, 1968;Temara et al, 1997;Bell and Kramer, 1999).…”

“…Exposed to various dissolved trace elements, the cuttlefish eggshell is likely to act as a protective barrier that limits or hinders the incorporation of metals into the embryo during the first developmental stages, with a permeability that is element-specific (Bustamante 2002(Bustamante , 2004Lacoue-Labarthe 2008a). The subsequent incorporation of water into the perivitelline fluid as the egg swells appears to be a key process in metal penetration.…”

Ocean acidification and temperature rise: effects on calcification during early development of the cuttlefish Sepia officinalis

“…PVF is also slightly hypertonic when compared to seawater (de Leersnyder and Lemaire 1972), which enables the characteristic egg swelling process (Cronin and Seymour 2000). In addition, the eggshell was shown to display a trace element selective permeability (Bustamante et al 2002(Bustamante et al , 2004Lacoue-Labarthe et al 2008. Consequently, the embryo grows under abiotic conditions in the PVF that are very different from those that hatchlings and juveniles encounter in the seawater.…”

Interannual patterns of variation in concentrations of trace elements in arms of Octopus vulgaris

“…Miramand and Bentley, 1992;Bustamante, 1998;Bustamante et al, 1998aBustamante et al, ,b, 2000Bustamante et al, , 2002aStorelli and Marcotrigiano, 1999). Among tissues, the digestive gland and branchial hearts appeared to play a major role in bioaccumulation processes of toxic elements such as cadmium and silver, which are detoxified and sequestrated, sometimes over a very long time scale (Bustamante et al, 2002a(Bustamante et al, , 2004Beuerlein et al, 2002). In general, feeding is considered to be the primary pathway for trace element bioaccumulation in cephalopods and second seawater.…”