Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis: Influence of ocean acidification and food type

Antoine Minet; Marc Metian; Angus Taylor; Sophie Gentès; Sabine Azemard; François Oberhänsli; Peter Swarzenski; Paco Bustamante; Thomas Lacoue-Labarthe

doi:10.1016/j.envres.2022.114201

Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis: Influence of ocean acidification and food type

Antoine Minet, Marc Metian, Angus Taylor, Sophie Gentès, Sabine Azemard, François Oberhänsli, Peter Swarzenski, Paco Bustamante, Thomas Lacoue-Labarthe

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

The bioaccumulation of mercury (Hg) in marine organisms through various pathways has not yet been fully explored, particularly in cephalopods. This study utilises radiotracer techniques using the isotope ²⁰³Hg to investigate the toxicokinetics and the organotropism of waterborne inorganic Hg (iHg) and dietary inorganic and organic Hg (methylHg, MeHg) in juvenile common cuttlefish Sepia officinalis. The effect of two contrasting CO₂ partial pressures in seawater (400 and 1600 μatm, equivalent to pH 8.08 and 7.54, respectively) and two types of prey (fish and shrimp) were tested as potential driving factors of Hg bioaccumulation. After 14 days of waterborne exposure, juvenile cuttlefish showed a stable concentration factor of 709 ± 54 and 893 ± 117 at pH 8.08 and 7.54, respectively. The accumulated dissolved i²⁰³Hg was depurated relatively rapidly with a radiotracer biological half-life (Tb_1/2) of 44 ± 12 and 55 ± 16 days at pH 8.08 and 7.54, respectively. During the whole exposure period, approximately half of the i²⁰³Hg was found in the gills, but i²⁰³Hg also increased in the digestive gland. When fed with ²⁰³Hg-radiolabelled prey, cuttlefish assimilated almost all the Hg provided (>95%) independently of the prey type. Nevertheless, the prey type played a major role on the depuration kinetics with Hg Tb_1/2 approaching infinity in fish fed cuttlefish vs. 25 days in shrimp fed cuttlefish. Such a difference is explained by the different proportion of Hg species in the prey, with fish prey containing more than 80% of MeHg vs. only 30% in shrimp. Four days after ingestion of radiolabelled food, iHg was primarily found in the digestive organs while MeHg was transferred towards the muscular tissues. No significant effect of pH/pCO₂ variation was observed during both the waterborne and dietary exposures on the bioaccumulation kinetics and tissue distribution of i²⁰³Hg and Me²⁰³Hg. Dietary exposure is the predominant pathway of Hg bioaccumulation in juvenile cuttlefish.

Original language	English
Article number	114201
Journal	Environmental Research
Volume	215
DOIs	https://doi.org/10.1016/j.envres.2022.114201
State	Published - Dec 2022
Externally published	Yes

Funding

This work is a contribution to the MERCy project funded by la Fondation pour la Recherche sur la Biodiversité and the Ministère de la Transition Ecologique et Solidaire. The Région Nouvelle Aquitaine is acknowledged for its support to the PhD and post-doc grants to AM and SG, respectively, through the EXPO project. The Institut Universitaire de France (IUF) is acknowledged for its support to PB as a Senior Member. AT, SA, FO, MM, and PWS are grateful for the support provided to the Environment Laboratories by the government of the Principality of Monaco. This work benefitted from the French GDR “Aquatic Ecotoxicology” framework which aims at fostering stimulating scientific discussions and collaborations for more integrative approaches. Authors warmly thank Antoine and José Lacoue-Labarthe, Jérôme Fort, Rémy Guilloneau and Fernando Pedraza for their support during field sampling. This work is a contribution to the MERCy project funded by la Fondation pour la Recherche sur la Biodiversité and the Ministère de la Transition Ecologique et Solidaire. The Région Nouvelle Aquitaine is acknowledged for its support to the PhD and post-doc grants to AM and SG, respectively, through the EXPO project. The Institut Universitaire de France (IUF) is acknowledged for its support to PB as a Senior Member. AT, SA, FO, MM, and PWS are grateful for the support provided to the Environment Laboratories by the government of the Principality of Monaco. This work benefitted from the French GDR “Aquatic Ecotoxicology” framework which aims at fostering stimulating scientific discussions and collaborations for more integrative approaches. Authors warmly thank Antoine and José Lacoue-Labarthe, Jérôme Fort, Rémy Guilloneau and Fernando Pedraza for their support during field sampling.

Funders	Funder number
French GDR
Principality of Monaco
Institut universitaire de France
Ministère de la Transition écologique et Solidaire

Keywords

Cephalopod
Kinetics
Methylmercury
Organotropism
Radiotracer
Trophic transfer
Waterborne contamination

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.envres.2022.114201

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@article{67f5f31b78b14ed8bd42452db3be987d,

title = "Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis: Influence of ocean acidification and food type",

abstract = "The bioaccumulation of mercury (Hg) in marine organisms through various pathways has not yet been fully explored, particularly in cephalopods. This study utilises radiotracer techniques using the isotope 203Hg to investigate the toxicokinetics and the organotropism of waterborne inorganic Hg (iHg) and dietary inorganic and organic Hg (methylHg, MeHg) in juvenile common cuttlefish Sepia officinalis. The effect of two contrasting CO2 partial pressures in seawater (400 and 1600 μatm, equivalent to pH 8.08 and 7.54, respectively) and two types of prey (fish and shrimp) were tested as potential driving factors of Hg bioaccumulation. After 14 days of waterborne exposure, juvenile cuttlefish showed a stable concentration factor of 709 ± 54 and 893 ± 117 at pH 8.08 and 7.54, respectively. The accumulated dissolved i203Hg was depurated relatively rapidly with a radiotracer biological half-life (Tb1/2) of 44 ± 12 and 55 ± 16 days at pH 8.08 and 7.54, respectively. During the whole exposure period, approximately half of the i203Hg was found in the gills, but i203Hg also increased in the digestive gland. When fed with 203Hg-radiolabelled prey, cuttlefish assimilated almost all the Hg provided (>95%) independently of the prey type. Nevertheless, the prey type played a major role on the depuration kinetics with Hg Tb1/2 approaching infinity in fish fed cuttlefish vs. 25 days in shrimp fed cuttlefish. Such a difference is explained by the different proportion of Hg species in the prey, with fish prey containing more than 80% of MeHg vs. only 30% in shrimp. Four days after ingestion of radiolabelled food, iHg was primarily found in the digestive organs while MeHg was transferred towards the muscular tissues. No significant effect of pH/pCO2 variation was observed during both the waterborne and dietary exposures on the bioaccumulation kinetics and tissue distribution of i203Hg and Me203Hg. Dietary exposure is the predominant pathway of Hg bioaccumulation in juvenile cuttlefish.",

keywords = "Cephalopod, Kinetics, Methylmercury, Organotropism, Radiotracer, Trophic transfer, Waterborne contamination",

author = "Antoine Minet and Marc Metian and Angus Taylor and Sophie Gent{\`e}s and Sabine Azemard and Fran{\c c}ois Oberh{\"a}nsli and Peter Swarzenski and Paco Bustamante and Thomas Lacoue-Labarthe",

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doi = "10.1016/j.envres.2022.114201",

language = "English",

volume = "215",

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T1 - Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis

T2 - Influence of ocean acidification and food type

AU - Minet, Antoine

AU - Metian, Marc

AU - Taylor, Angus

AU - Gentès, Sophie

AU - Azemard, Sabine

AU - Oberhänsli, François

AU - Swarzenski, Peter

AU - Bustamante, Paco

AU - Lacoue-Labarthe, Thomas

PY - 2022/12

Y1 - 2022/12

N2 - The bioaccumulation of mercury (Hg) in marine organisms through various pathways has not yet been fully explored, particularly in cephalopods. This study utilises radiotracer techniques using the isotope 203Hg to investigate the toxicokinetics and the organotropism of waterborne inorganic Hg (iHg) and dietary inorganic and organic Hg (methylHg, MeHg) in juvenile common cuttlefish Sepia officinalis. The effect of two contrasting CO2 partial pressures in seawater (400 and 1600 μatm, equivalent to pH 8.08 and 7.54, respectively) and two types of prey (fish and shrimp) were tested as potential driving factors of Hg bioaccumulation. After 14 days of waterborne exposure, juvenile cuttlefish showed a stable concentration factor of 709 ± 54 and 893 ± 117 at pH 8.08 and 7.54, respectively. The accumulated dissolved i203Hg was depurated relatively rapidly with a radiotracer biological half-life (Tb1/2) of 44 ± 12 and 55 ± 16 days at pH 8.08 and 7.54, respectively. During the whole exposure period, approximately half of the i203Hg was found in the gills, but i203Hg also increased in the digestive gland. When fed with 203Hg-radiolabelled prey, cuttlefish assimilated almost all the Hg provided (>95%) independently of the prey type. Nevertheless, the prey type played a major role on the depuration kinetics with Hg Tb1/2 approaching infinity in fish fed cuttlefish vs. 25 days in shrimp fed cuttlefish. Such a difference is explained by the different proportion of Hg species in the prey, with fish prey containing more than 80% of MeHg vs. only 30% in shrimp. Four days after ingestion of radiolabelled food, iHg was primarily found in the digestive organs while MeHg was transferred towards the muscular tissues. No significant effect of pH/pCO2 variation was observed during both the waterborne and dietary exposures on the bioaccumulation kinetics and tissue distribution of i203Hg and Me203Hg. Dietary exposure is the predominant pathway of Hg bioaccumulation in juvenile cuttlefish.

AB - The bioaccumulation of mercury (Hg) in marine organisms through various pathways has not yet been fully explored, particularly in cephalopods. This study utilises radiotracer techniques using the isotope 203Hg to investigate the toxicokinetics and the organotropism of waterborne inorganic Hg (iHg) and dietary inorganic and organic Hg (methylHg, MeHg) in juvenile common cuttlefish Sepia officinalis. The effect of two contrasting CO2 partial pressures in seawater (400 and 1600 μatm, equivalent to pH 8.08 and 7.54, respectively) and two types of prey (fish and shrimp) were tested as potential driving factors of Hg bioaccumulation. After 14 days of waterborne exposure, juvenile cuttlefish showed a stable concentration factor of 709 ± 54 and 893 ± 117 at pH 8.08 and 7.54, respectively. The accumulated dissolved i203Hg was depurated relatively rapidly with a radiotracer biological half-life (Tb1/2) of 44 ± 12 and 55 ± 16 days at pH 8.08 and 7.54, respectively. During the whole exposure period, approximately half of the i203Hg was found in the gills, but i203Hg also increased in the digestive gland. When fed with 203Hg-radiolabelled prey, cuttlefish assimilated almost all the Hg provided (>95%) independently of the prey type. Nevertheless, the prey type played a major role on the depuration kinetics with Hg Tb1/2 approaching infinity in fish fed cuttlefish vs. 25 days in shrimp fed cuttlefish. Such a difference is explained by the different proportion of Hg species in the prey, with fish prey containing more than 80% of MeHg vs. only 30% in shrimp. Four days after ingestion of radiolabelled food, iHg was primarily found in the digestive organs while MeHg was transferred towards the muscular tissues. No significant effect of pH/pCO2 variation was observed during both the waterborne and dietary exposures on the bioaccumulation kinetics and tissue distribution of i203Hg and Me203Hg. Dietary exposure is the predominant pathway of Hg bioaccumulation in juvenile cuttlefish.

KW - Cephalopod

KW - Kinetics

KW - Methylmercury

KW - Organotropism

KW - Radiotracer

KW - Trophic transfer

KW - Waterborne contamination

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Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis: Influence of ocean acidification and food type

Abstract

Funding

Keywords

UN SDGs

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