Diet variably affects the trophic transfer of trace elements in the oyster Crassostrea gigas

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Highlights

  • Trophic transfer of Ag, 241Am, Cd, Co, Mn and Zn was assessed in oysters fed on ciliates and diatoms.

  • Assimilation of Ag and 241Am in C. gigas differ in response to the different diets tested.

  • Highest assimilation of Ag and 241Am in C. gigas was observed when it is fed with ciliates.

Abstract

Although it has been shown that trophic transfer of trace elements in oysters can be influenced by the diet, most of the studies investigating the ability of oysters to bioaccumulate trace elements from their diet are based on experiments using phytoplankton alone. Wild oysters feed also on large bacteria, ciliates or detritic organic matter. The present study aimed at examining the influence of food quality on the assimilation efficiency (AE) of trace elements in the Pacific cupped oyster Crassostrea gigas. Oysters were exposed via their food to the radiotracers of essential (57Co, 54Mn and 65Zn) and non-essential (110mAg, 241Am and 109Cd) trace elements under different diets (protozoan ciliates Uronema marinum and diatoms Thalassiosira pseudonana). Significant differences were found only for Ag and 241Am, with lower AEs measured in oysters fed with ciliates than in individuals fed with diatoms (Ag: 54 ± 3% vs. 67 ± 4% and 241Am: 62 ± 4% vs. 76 ± 4%). Interestingly, no significant difference was found among estimated depuration rates (kel) for all trace elements ingested with the two diets tested. These findings indicate that the differences observed are driven by the digestion process, presumably due to difference of bioavailability of trace elements dependent on the quality of the food ingested.

Introduction

The ability of oysters to bioaccumulate trace elements has been studied intensively in laboratory experiments during the last decades. Several studies have indicated that food is generally the main accumulation pathway of trace elements in oysters (e.g., Hédouin et al., 2010b; Metian et al., 2016). Laboratory studies generally showed also that food quality and quantity affect trophic transfer of trace elements in bivalves (e.g., Hédouin et al., 2010a; Metian et al., 2008; Wang and Fisher, 1996). This is likely caused by the adjustment of feeding processes such as filtration rate in response to variations in the feeding environment (Navarro and Iglesias, 1993; Widdows and Donkin, 1992) and the bioavailability of trace elements in the ingested food (e.g., Ng et al., 2005; Wang and Fisher, 1996). An overlook of the literature (see Table 1) indicates that assimilation efficiency (AE) of trace elements was shown to be highly dependent on the food type in seven oyster species. Most studies quantified trace element AE from phytoplankton exclusively (Blackmore and Wang, 2004; Hédouin et al., 2010b, 2010a; Reinfelder et al., 1997) but some also included sediment (Ke and Wang, 2001; Pan and Wang, 2011), whereas other food items were rarely investigated (see Table 1).

Wild oysters are filter-feeders ingesting a variety of food items, including phytoplankton, heterotrophic protists, large bacteria, fungi and detritus (Dupuy et al., 1999; Heral, 1990). For instance, Pacific cupped oyster Crassostrea gigas retains efficiently food particles between 4 and 72 μm of size (Barillé et al., 1993; Dupuy et al., 1999); heterotrophic protists (such as ciliates) can be a major food source for C. gigas and thus act as a trophic link between picoplankton and oysters (Dupuy et al., 1999). Nevertheless, to the best of our knowledge, trophic transfer of trace elements from ciliates to oysters has been poorly investigated. In a recent work, Metian et al. (2020) showed that oysters fed with ciliates Uronema marinum assimilated more efficiently methyl mercury and less efficiently inorganic mercury than oysters fed with diatoms Thalassiosira pseudonana.

In the present study, we investigated the influence of the diet quality on the AE of six essential (Co, Mn and Zn) and non-essential (Ag, 241Am and Cd) trace elements in the Pacific cupped oysters C. gigas, using pulse-chase feeding method and radiolabeled diatom T. pseudonana (2.5–15 μm diameter) and ciliate protozoan U. marinum, 20 μm length). Both protists are components of the oyster natural diet (Le Gall et al., 1997; Dupuy et al., 1999).

Section snippets

Origin and acclimation of organisms

Pacific cupped oysters C. gigas were purchased from a shellfish farm in La Rochelle, France. They were transported to IAEA-EL premises in the Principality of Monaco, and were acclimated to laboratory conditions (constantly aerated, open-circuit aquarium; salinity: 36 ± 1; temperature: 19 ± 1 °C; pH: 8; light/dark cycle: 12h/12h) for 4 weeks. During acclimation, bivalves were fed with Prymnesiophyceae Isochrysis galbana (104 cells mL−1).

Radiotracers and counting

Depuration kinetics of trace elements in oysters were

Results and discussion

During the last three decades, dietary pathway has been increasingly recognized as the main source of trace element bioaccumulation in bivalves (e.g., Hédouin et al., 2010b; Metian et al., 2009; Reinfelder et al., 1998; Wang and Fisher, 1999b; Wang et al., 1996). The assimilation efficiency (AE) is among the critical parameters to assess the dietary uptake of trace elements in aquatic organisms (Pouil et al., 2018; Wang and Fisher, 1999a) and numerous studies have been devoted to determine

CRediT authorship contribution statement

Simon Pouil: Data curation, Investigation, Formal analysis, Visualization, Software, Writing - original draft, Writing - review & editing. Marc Metian: Investigation, Formal analysis, Data curation, Writing - original draft, Writing - review & editing. Christine Dupuy: Investigation, Conceptualization, Resources, Validation. Jean-Louis Teyssié: Methodology, Validation, Resources. Michel Warnau: Conceptualization, Investigation, Project administration, Writing - original draft, Writing - review

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The IAEA is grateful for the support provided to its Environment Laboratories by the Government of the Principality of Monaco. MW is an Honorary Senior Research Associate of the National Fund for Scientific Research (NFSR, Belgium). The IUF (Institut Universitaire de France) is acknowledged for its support to PB as a Senior Member.

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