Simon Pouil

Differential bioaccumulation of 134Cs in tropical marine organisms and the relative importance of exposure pathways

Bioaccumulation of (134)Cs was determined in 5 tropical marine species: three bivalves (the oysters Isognomon isognomum and Malleus regula, and the clam Gafrarium pectinatum), one decapod (shrimp Penaeus stylirostris) and one alga (Lobophora variegata). Marine organisms were exposed to the radionuclides via different pathways: seawater (all of them), food (shrimp and bivalves) and sediment (bivalves). Our results indicate that the studied tropical species accumulate Cs similarly than species from temperate regions whereas retention capacities seems to be greater in the tropical species. Bioaccumulation capacities of the two oysters were similar for all the exposure pathways. The alga, and to a lesser extent the shrimp, concentrated dissolved Cs more efficiently than the bivalves (approx. 14 and 7 times higher, respectively). Assimilation efficiencies of Cs in bivalves and shrimp after a single feeding with radiolabelled food were comprised between 7.0 ± 0.4 and 40.7 ± 4.3%, with a variable retention time (half-life -Tb1/2- ranging from 16 ± 3 to 89 ± 55 d). Although the clam lives buried in the sediment, this exposure pathway resulted in low bioaccumulation efficiency for sediment-bound Cs (mean transfer factor: 0.020 ± 0.001) that was lower than the two oyster species, which are not used to live in this media (0.084 ± 0.003 and 0.080 ± 0.005). Nonetheless, Cs accumulated from sediment was similarly absorbed (61.6 ± 9.7 to 79.2 ± 2.3%) and retained (Tb1/2: 37 ± 2 to 58 ± 25 d) for the three bivalves species. Despite the poor transfer efficiency of Cs from food, the use of a global bioaccumulation model indicated that the trophic pathways was the main uptake route of Cs in the bivalves and shrimp. In shelled organisms, shells played a non-negligible role in Cs uptake, and their composition and structure might play a major role in this process. Indeed, most of the Cs taken up from seawater and sediment was principally located on the hard parts of the bivalves and shrimp, with the exception of G. pectinatum, where Cs was mainly distributed in the soft-parts.

Delineation of 134Cs uptake pathways (seawater and food) in the variegated scallop Mimachlamys varia

Among bivalves, scallops have been shown to be good bioindicator species for radionuclide monitoring. The present paper looked at the Cs bioaccumulation capacities of the variegated scallop Mimachlamys varia exposed separately via seawater and food under laboratory conditions. Results were compared with data previously obtained for the king scallop Pecten maximus, the only Pectinid species for which Cs accumulation has been studied in laboratory. Results indicated that M. varia has higher uptake capacity (CF: 1.86 ± 0.08) but lower absorption efficiency (A0l: 33 ± 5%) than P. maximus when exposed to waterborne Cs (CF of P. maximus: 0.94 ± 0.05 and A0l: 45 ± 3%). When scallops were fed radiolabeled phytoplankton, the assimilation efficiency of Cs was similar for the two species (AE: 24 ± 3% for M. varia and 28 ± 4% for P. maximus). Interspecific differences in terms of accumulation and retention, can be explained by physiological factors (including size of individuals) and/or difference in storage mechanisms. Indeed, organotropism differed between the two scallop species, suggesting the occurrence of specific redistribution mechanisms towards the tissues involved in Cs storage, excretion and detoxification. Finally, the present study examined the relative contribution of the different exposure pathways (seawater and food) to global (134)Cs bioaccumulation for M. varia. Results showed that food constitutes the main accumulation pathway, contributing for 77% of the global (134)Cs bioaccumulation.

Trophic transfer of 110mAg in the turbot Scophthalmus maximus through natural prey and compounded feed

Industrial incidents can result in radionuclide release in the environment, among which (110m)Ag. Indeed, under particular circumstances, non-negligible amounts of (110m)Ag have been measured in the marine environment (as observed in Fukushima Dai-ichi incident). This element can therefore be accumulated by aquatic organisms through different pathways including the trophic transfer. The present study aimed at examining the variation of (110m)Ag assimilation efficiency (AE) by turbots, Scophthalmus maximus, when exposed through different feeds. Pulse-chase feeding experiments were carried out in mesocosms, using radiolabelled feeds (natural prey and commercial pellets). Depuration kinetics of (110m)Ag over 21 days were generally fitted by a two-component exponential model; the ingested radioelement was poorly assimilated by turbots regardless of the food item that was used (AE always <3%). Concentration and subcellular distribution of (110m)Ag in prey did not seem to influence its assimilation by turbot. These results suggest that physiological mechanisms could occur in fish that would prevent the transfer of (110m)Ag from gut lumen to internal organs (e.g. (110m)Ag neutralization in the lumen of the stomach, detoxification mechanisms occurring in the gut).

Trophic transfer of essential elements in the clownfish Amphiprion ocellaris in the context of ocean acidification

Little information exists on the effects of ocean acidification (OA) on the digestive and post-digestive processes in marine fish. Here, we investigated OA impacts (Δ pH = 0.5) on the trophic transfer of select trace elements in the clownfish Amphiprion ocellaris using radiotracer techniques. Assimilation efficiencies of three essential elements (Co, Mn and Zn) as well as their other short-term and long-term kinetic parameters in juvenile clownfish were not affected by this experimental pH change. In complement, their stomach pH during digestion were not affected by the variation in seawater pH. Such observations suggest that OA impacts do not affect element assimilation in these fish. This apparent pCO2 tolerance may imply that clownfish have the ability to self-regulate pH shifts in their digestive tract, or that they can metabolically accommodate such shifts. Such results are important to accurately assess future OA impacts on diverse marine biota, as such impacts are highly species specific, complex, and may be modulated by species-specific metabolic processes.

Comparing single‐feeding and multi‐feeding approaches for experimentally assessing trophic transfer of metals in fish

Diet is an important pathway for metal uptake in marine organisms, and assimilation efficiency is one of the most relevant parameters to quantify trophic transfer of metals along aquatic food webs. The most commonly used method to estimate this parameter is pulse-chase feeding using radiolabeled food. This approach is, however, based on several assumptions that are not always tested in an experimental context. The present study aimed to validate the approach by assessing single-feeding and multiple-feeding approaches, using a model species (the turbot Scophthalmus maximus). Using the kinetic data obtained from the single-feeding experiment, the reconstruction of a multi-feeding experiment was tested for consistency with data provided by an actual multi-feeding performed under the same experimental conditions. The results validated the single-feeding approach. Environ Toxicol Chem 2017;36:1227-1234.

The role of salinity in the trophic transfer of 137 Cs in euryhaline fish

In order to better understand the influence of changing salinity conditions on the trophic transfer of 137Cs in marine fish that live in dynamic coastal environments, its depuration kinetics was investigated in controlled aquaria. The juvenile turbot Scophthalmus maximus was acclimated to three distinct salinity conditions (10, 25 and 38) and then single-fed with compounded pellets that were radiolabelled with 137Cs. At the end of a 21-d depuration period, assimilation efficiencies (i.e. AEs = proportion of 137Cs ingested that is actually assimilated by turbots) were determined from observational data acquired over the three weeks. Our results showed that AEs of 137Cs in the turbots acclimated to the highest salinity condition were significantly lower than for the other conditions (p < 0.05). Osmoregulation likely explains the decreasing AE observed at the highest salinity condition. Indeed, observations indicate that fish depurate ingested 137Cs at a higher rate when they increase ion excretion, needed to counterbalance the elevated salinity. Such data confirm that ambient salinity plays an important role in trophic transfer of 137Cs in some fish species. Implications for such findings extend to seafood safety and climate change impact studies, where the salinity of coastal waters may shift in future years in response to changing weather patterns.

The role of marine biotoxins on the trophic transfer of Mn and Zn in fish

Essential nutrients are critical for physiological processes of organisms. In fish, they are obtained primarily from the diet, and their transfer and accumulation are known to be impacted by environmental variables such as water temperature, pH and salinity, as well as by diet composition and matrices. Yet, prey items consumed by fish may also contain toxic compounds such as marine toxins associated with harmful algae. These biotoxins have the potential to affect essential trace element assimilation in fish through chemical interactions such as the formation of trace element-toxin complexes or by affecting general fish physiology as in the modification of ion-specific transport pathways. We assessed the influence of dietary exposure to brevetoxins (PbTxs), ichthyotoxic neurotoxins produced by the dinoflagellate Karenia brevis, on trophic transfer of two essential trace elements, Mn and Zn, in a fish model. Using ecologically relevant concentrations of PbTxs and trace elements in controlled laboratory conditions, juvenile turbots Scophthalmus maximus were given food containing PbTxs before or at the same time as a feeding with radiotracers of the chosen essential elements (54Mn and 65Zn). Treatments included simultaneous exposure (PbTxs + 54Mn + 65Zn) in a single-feeding, 3-week daily pre-exposure to dietary PbTx followed by a single feeding with 54Mn and 65Zn, and a control (54Mn and 65Zn only). After a 21-day depuration period, turbot tissue brevetoxin levels were quantified and assimilation efficiencies of 54Mn and 65Zn were assessed. PbTxs were found in turbot tissues in each exposure treatment, demonstrating dietary trophic transfer of these toxins; yet, no differences in assimilation efficiencies of Mn or Zn were found between treatments or the control (p > 0.05). These results indicate that, in our experimental conditions, PbTx exposure does not significantly affect the trophic transfer of Mn and Zn in fish.

Dietary Zn and the subsequent organotropism in fish: No influence of food quality, frequency of feeding and environmental conditions (pH and temperature)

Trophic transfer of Zn in fish is affected by the type of food and environmental variables such as temperature. However, there is still a lack of knowledge regarding the effects of such factors on Zn organotropism. For this reason, a series of experimental studies have investigated how the distribution and the concentration of Zn is affected by some environmentally-relevant factors (food quality, food availability, water pH, and temperature) in turbot Scophthalmus maximus using radiotracer techniques. In three different experiments, Zn distribution in seven body compartments of juvenile turbot and the calculation of Zn concentration index (IC) for each compartment were compared. Its distribution as well as its concentration in the body compartments of juvenile turbots were not affected by the experimental conditions tested. This apparent consistency in the Zn organotropism can be explained by the ability of the fish to maintain Zn homeostasis at non-toxic Zn concentrations in their diet. These results are important to better understand the trophic transfer of Zn in fish under realistic environmental conditions.

A double-tracer radioisotope approach to assess simultaneous bioaccumulation of caesium in the olive flounder Paralichthys olivaceus

To better understand bioaccumulation of radiocaesium in the commercially important Japanese flatfish, Paralichthys olivaceus, the uptake and depuration kinetics of caesium via both seawater and food were assessed simultaneously using controlled aquaria. The pre-conditioned fish were exposed to radionuclides via the two different pathways (aqueous versus dietary) concurrently using two isotopes of caesium, 137Cs and 134Cs, respectively. Dissolved caesium uptake was linear and did not reach a steady state over the course of the 8-day exposure period. Consumption of 134Cs-labelled food led to higher bioaccumulation rates of radioactive Cs than via seawater exposure of 137Cs during uptake and following depuration, though the model-derived long-lived biological half-lives of both pathways was approximately 66 d. Further development of this method for assessing multiple radiocaesium bioaccumulation pathways simultaneously could lead to a promising new approach for studying Cs contamination in marine organisms.

Allometric relationship in the bioaccumulation of radionuclides (134Cs & 241Am) and delineation of contamination pathways (food and seawater) in bloody cockle Anadara senilis using radiotracer techniques

The uptake and depuration kinetics of 134Cs and 241Am were investigated in the bloody cockle Anadara senilis exposed via seawater and food in controlled conditions, using animals of different weight groups in order to assess how their bioaccumulation is affected by allometry and, hence, the individuals age. This study is one of the few experiments investigating bioaccumulation capacities of radionuclides in a West-African bivalve. Results showed that allometric relationships were mainly dependent on the exposure pathway considered. Significant relationships with body weight of bloody cockles were found during the uptake from dissolved phase for both radionuclides; they followed inverse power functions: smaller cockles concentrated both radionuclides more than larger ones. In contrast, radionuclide absorption and assimilation efficiencies from water and food, respectively, did not show any significant relationship with weight: only slight variation was observed between small and large organisms for the retention of 241Am accumulated from food. A bioaccumulation model was used to assess the contribution of each pathway of exposure (food vs. water) in organisms grouped in small and large individuals. We found that, regardless of the size, 134Cs was mainly bioaccumulated through the dietary pathway. In the case of 241Am, the relative contribution of each pathway is weight-dependent: major contribution of dissolved pathway in smaller organisms and the major dietary contribution in larger organisms.