Thomas Lacoue-Labarthe

First experiments on the maternal transfer of metals in the cuttlefish Sepia officinalis

The aim of this study was to provide a first insight on the incorporation of eight metals in the eggs of the cuttlefish Sepia officinalis via maternal transfer, using radiotracer techniques ((110m)Ag, (241)Am, (109)Cd, (60)Co, (134)Cs, (54)Mn, (75)Se and (65)Zn). The cuttlefish was fed daily with radiolabelled crabs for two weeks; it then started to spawn every three days. Among the eight tracers, only (110m)Ag, (75)Se and (65)Zn were significantly transferred to the eggs. The radiotracer distribution among the egg compartments showed that (75)Se and (65)Zn were accumulated mainly in the vitellus whereas (110m)Ag was found in similar proportion in the vitellus and the eggshell. During the embryonic development, (75)Se and (65)Zn contained in the vitellus were progressively transferred to the embryo, likely to supply its metabolic needs in these essential elements. Although it has no known biological functions, Ag contained in both vitellus and eggshell was also transferred to the embryo. Overall, our results showed that transfer of Ag, Se, and Zn does actually occur from a female cuttlefish to its eggs, at least during the last two weeks before spawning.

Differential bioaccumulation behaviour of Ag and Cd during the early development of the cuttlefish Sepia officinalis

Cuttlefish eggs were exposed to background concentrations of dissolved Ag and Cd, using the radiotracers (110m)Ag and (109)Cd. At different time of the embryonic development (50 days), some eggs were placed in non-contaminating conditions. During the experiment, the uptake and depuration kinetics, and distribution of these metals among the egg compartments (i.e. eggshell, vitellus, peri-vitelline fluid and embryo) were assessed. In parallel, experiments were conducted with sub-lethal concentrations of stable Ag and Cd (2 and 1 microgl(-1), respectively) to compare the metal behaviour at higher concentrations. From the spawning date up to 1 month of development, both metals were taken up efficiently by the eggs, reaching load/concentration ratio (LCR) of 1059+/-75 and 239+/-22 for (110m)Ag and (109)Cd, respectively. From this time onwards, (110m)Ag activity continued to increase in eggs, whereas (109)Cd kinetics displayed a significant decrease. Whatever the developmental stage, Cd was mainly associated with the eggshell all along the exposure experiment. In addition, both stable Cd concentrations and (109)Cd LCR remained low in the embryo all along the embryonic development, indicating that the eggshell acted as an efficient shield against the penetration of this metal. In contrast, (110m)Ag passed through the eggshell from day 30 onwards and was then accumulated in the embryo, which contained more than 40% of the whole egg metal burden at the end of the exposure period. In depuration conditions, it is noteworthy that Ag continued to accumulate in the embryo indicating translocation processes from the eggshell and a high affinity of the metal for the embryo tissues. Overall our results showed that at day 30 of the embryonic development the cuttlefish eggshell becomes permeable to Ag but not to Cd. Exposure to stable metals confirmed the saturation capacities of the eggshell for Cd and the Ag penetration properties.

Metal and metalloid bioaccumulation in the Pacific blue shrimp Litopenaeus stylirostris (Stimpson) from New Caledonia: Laboratory and field studies

The present work aimed at better understanding metal and metalloid bioaccumulation in the edible Pacific blue shrimp Litopenaeus stylirostris, using both laboratory and field approaches. In the laboratory, the bioaccumulation kinetics of Ag, Cd, Co, Cr, and Zn have been investigated in shrimp exposed via seawater and food, using the corresponding gamma-emitting radiotracers ((110 m)Ag, (109)Cd, (57)Co, (51)Cr, and (65)Zn) and highly sensitive nuclear detection techniques. Results showed that hepatopancreas and intestine concentrated the metals to the highest extent among the blue shrimp organs and tissues. Moulting was found to play a non negligible detoxification role for Co, Cr and, to a lesser extent, Zn. Metal retention by L. stylirostris widely varied (from a few days to several months), according to the element and exposure pathway considered (a given metal was usually less strongly retained when ingested with food than when it was taken up from the dissolved phase). In the field study, Ag, As, Cd, Co, Cr, Cu, Mn, Ni, and Zn were analysed in shrimp collected from a New Caledonian aquaculture pond. Metal concentrations in the shrimp muscles were generally relatively low and results confirmed the role played by the digestive organs and tissues in the bioaccumulation/storage/detoxification of metals in the Pacific blue shrimp. Preliminary risk considerations indicate that consumption of the shrimp farmed in New Caledonia is not of particular concern for human health.

Biokinetics of Hg and Pb accumulation in the encapsulated egg of the common cuttlefish Sepia officinalis: Radiotracer experiments

Uptake and depuration kinetics of dissolved (203)Hg and (210)Pb were determined during the entire embryonic development of the eggs of the cuttlefish, Sepia officinalis (50d at 17 degrees C). (203)Hg and (210)Pb were accumulated continuously by the eggs all along the development time reaching load/concentration ratio (LCR) of 467+/-43 and 1301+/-126g, respectively. During the first month, most of the (203)Hg and (210)Pb remained associated with the eggshell indicating that the latter acted as an efficient shield against metal penetration. From this time onwards, (203)Hg accumulated in the embryo, indicating that it passed through the eggshell, whereas (210)Pb did not cross the chorion during the whole exposure time. It also demonstrated that translocation of Hg associated with the inner layers of the eggshell is a significant source of exposure for the embryo. This study highlighted that the maturing embryo could be subjected to the toxic effects of Hg in the coastal waters where the embryonic development is taking place.

Influence of food on the assimilation of selected metals in tropical bivalves from the New Caledonia lagoon: Qualitative and quantitative aspects

The present study aimed at examining the influence of food quality and quantity on the assimilation efficiency (AE) of metals in two abundant bivalves in the New Caledonia lagoon, the oyster Isognomon isognomon and the clam Gafrarium tumidum. Bivalves were exposed via their food to the radiotracers of three metals of concern in New Caledonia ((54)Mn, (57)Co and (65)Zn) under different feeding conditions (phytoplankton species, cell density, and cell-associated metal concentration). When bivalves were fed Heterocapsa triquetra, Emiliania huxleyi and Isochrysis galbana, AE of Mn, Co and Zn was strongly influenced by the phytoplankton species and by the metal considered. In contrast, when fed one given phytoplankton species previously exposed to different concentrations of Co, phytoplankton-associated Co load had no influence on the AE and on the retention time of the metal in both bivalves. Metals ingested with I. galbana displayed generally the highest AE in both bivalve species, except for Mn in clams for which the highest AE was observed for H. triquetra. Influence of food quantity was investigated by exposing bivalves to different cell densities of I. galbana (5 x 10(3), 10(4) or 5 x 10(4) cell ml(-1)). As for food quality, food quantity was found to influence AE of Mn, Co and Zn, the highest AE being observed when bivalves were fed the lowest cell density. Overall, results indicate that the two bivalve species are able to adjust their feeding strategies according to the food conditions prevailing in their environment.

Comparative bioaccumulation kinetics of trace elements in Mediterranean marine sponges

While marine organisms such as bivalves, seagrasses and macroalgae are commonly used as biomonitors for the environment pollution assessment, widely distributed sponges received little attention as potential helpful species for monitoring programmes. In this study, the trace element and radionuclide bioaccumulation and retention capacities of some marine sponges were estimated in a species-comparative study using radiotracers technique. Six Mediterranean species were exposed to background dissolved concentrations of (110m)Ag, (241)Am, (109)Cd, (60)Co, (134)Cs, (54)Mn, (75)Se and (65)Zn allowing the assessment of the uptake and depuration kinetics for selected elements. Globally, massive demosponges Agelas oroides, Chondrosia reniformis and Ircinia variabilis displayed higher concentration factor (CF) than the erectile ones (Acanthella acuta, Cymbaxinella damicornis, Cymbaxinella verrucosa) at the end of exposure, suggesting that the morphology is a key factor in the metal bioaccumulation efficiency. Considering this observation, two exceptions were noted: (1) A. acuta reached the highest CF for (110m)Ag and strongly retained the accumulated metal without significant Ag loss when placed in depuration conditions and (2) C. reniformis did not accumulate Se as much as A. oroides and I. variabilis. These results suggest that peculiar metal uptake properties in sponges could be driven by specific metabolites or contrasting biosilification processes between species, respectively. This study demonstrated that sponges could be considered as valuable candidate for biomonitoring metal contamination but also that there is a need to experimentally highlight metal-dependant characteristic among species.

Radioisotopes Demonstrate the Contrasting Bioaccumulation Capacities of Heavy Metals in Embryonic Stages of Cephalopod Species

Cephalopods play a key role in many marine trophic food webs and also constitute alternative fishery resources in the context of the ongoing decline in finfish stocks. Most coastal cephalopod species of commercial importance migrate into shallow waters during the breeding season to lay their eggs, and are consequently subjected to coastal contamination. Eggs of common cuttlefish Sepia officinalis, European squid Loligo vulgaris, common octopus Octopus vulgaris and the sepiolid Rossia macrosoma were exposed during embryonic development to dissolved 110mAg, 109Cd, 60Co, 54Mn and 65Zn in order to determine their metal accumulation efficiencies and distribution among different egg compartments. Cuttlefish eggs, in which hard shells enclose the embryos, showed the lowest concentration factor (CF) values despite a longer duration of exposure. In contrast, octopus eggs, which are only protected by the chorionic membrane, accumulated the most metal. Uptake appears to be linked to the selective retention properties of the egg envelopes with respect to each element. The study also demonstrated that the octopus embryo accumulated 110mAg directly from the dissolved phase and also indirectly through assimilation of the contaminated yolk. These results raise questions regarding the potential contrasting vulnerability of early life stages of cephalopods to the metallic contamination of coastal waters.

Metal bioaccumulation and detoxification processes in cephalopods: A review

&NA; In recent decades, cephalopods have been shown to have very high capacities to accumulate most trace elements, regardless of whether they are essential (e.g., Cu and Zn) or non‐essential (e.g., Ag and Cd). Among the different pathways of exposure to trace elements, the trophic pathway appears to be the major route of assimilation for numerous metals, including Cd, Co, Hg and Zn. Once assimilated, trace elements are distributed in the organism, accumulating in storage organs. The digestive gland is the main organ in which many trace elements accumulate, whichever of the exposure pathway. For example, this organ can present Cd concentrations reaching hundreds to thousands of ppm for some species, even though the digestive gland represents only a small proportion of the total mass of the animal. Such a specific organotropism towards the digestive gland of both essential and non‐essential elements, regardless of the exposure pathway, poses the question of the detoxification processes evolved by cephalopods in order to sustain these high concentrations. This paper reviews the current knowledge on the bioaccumulation of trace elements in cephalopods, the differences in pharmaco‐dynamics between organs and tissues, and the detoxification processes they use to counteract trace element toxicity. A peculiar focus has been done on the bioaccumulation within the digestive gland by investigating the subcellular locations of trace elements and their protein ligands. HighlightsThe paper reviews existing knowledge on the metal metabolism in cephalopod.The bioaccumulation pathways, tissue and subcellular distribution are discussed.A peculiar focus is done on Cd and Hg.The paper highlights the gap of knowledge for these organisms of growing interest.

Depletion of Essential Fatty Acids in the Food Source Affects Aerobic Capacities of the Golden Grey Mullet Liza aurata in a Warming Seawater Context

The objective of this study was to evaluate the combined effects of thermal acclimation and n-3 highly unsaturated fatty acids (n-3 HUFA) content of the food source on the aerobic capacities of fish in a thermal changing environment. The model used was the golden grey mullet Liza aurata, a species of high ecological importance in temperate coastal areas. For four months, fish were exposed to two food sources with contrasting n-3 HUFA contents (4.8% ecosapentaenoic acid EPA + docosahexaenoic acid DHA on the dry matter DM basis vs. 0.2% EPA+DHA on DM) combined with two acclimation temperatures (12°C vs. 20°C). The four experimental conditions were LH12, LH20, HH12 and HH20. Each group was then submitted to a thermal challenge consisting of successive exposures to five temperatures (9°C, 12°C, 16°C, 20°C, 24°C). At each temperature, the maximal and minimal metabolic rates, metabolic scope, and the maximum swimming speed were measured. Results showed that the cost of maintenance of basal metabolic activities was particularly higher when n-3 HUFA food content was low. Moreover, fish exposed to high acclimation temperature combined with a low n-3 HUFA dietary level (LH20) exhibited a higher aerobic scope, as well as a greater expenditure of energy to reach the same maximum swimming speed as other groups. This suggested a reduction of the amount of energy available to perform other physiological functions. This study is the first to show that the impact of lowering n-3 HUFA food content is exacerbated for fish previously acclimated to a warmer environment. It raises the question of the consequences of longer and warmer summers that have already been recorded and are still expected in temperate areas, as well as the pertinence of the lowering n-3 HUFA availability in the food web expected with global change, as a factor affecting marine organisms and communities.

Acidified seawater increases accumulation of cobalt but not cesium in manila clam Ruditapes philippinarum

The pH of seawater around the world is expected to continue its decline in the near future in response to ocean acidification that is driven by heightened atmospheric CO2 emissions. Concomitantly, economically-important molluscs that live in coastal waters including estuaries and embayments, may be exposed to a wide assortment of contaminants, including trace metals and radionuclides. Seawater acidification may alter both the chemical speciation of select elements as well as the physiology of organisms, and may thus pose at risk to many shellfish species, including the manila clam Ruditapes philippinarum. The bioconcentration efficiency of two common radionuclides associated with the nuclear fuel cycle, 134Cs and 57Co, were investigated by exposing live clams to dissolved 134Cs and 57Co at control (pH = 8.1) and two lowered pH (pH = 7.8 and 7.5) levels using controlled aquaria. The uptake and depuration kinetics of the two radionuclides in the whole-body clam were followed for 21 and 35 days, respectively. At steady-state equilibrium, the concentration factor (CFss) for 57Co increased as the pH decreased (i.e. 130 ± 5, 194 ± 6, and 258 ± 10 at pH levels 8.1, 7.8 and 7.5, respectively), whereas the 134Cs uptake was not influenced by a change in pH conditions. During depuration, the lowest depuration rate constant of 57Co by the manila clam was observed at the intermediate pH of 7.8. An increase in the accumulation of 57Co at the intermediate pH value was thought to be caused mainly by the aragonitic shell of the clam, as well as the low salinity and alkalinity of seawater used in the experiment. Considering that accumulation consists of uptake and depuration, among the three pH conditions moderately acidified seawater enhanced most the accumulation of 57Co. Accumulation of 134Cs was not strongly influenced by a reduced pH condition, as represented by an analogous uptake constant rate and CFss in each treatment. Such results suggest that future seawater pH values that are projected to be lower in the next decades, may pose a risk for calcium-bearing organisms such as shellfish.