Mercury in the tissues of five cephalopods species: First data on the nervous system

Antoine Minet; Alain Manceau; Anaïs Valada-Mennuni; Maud Brault-Favrou; Carine Churlaud; Jérôme Fort; Thành Nguyen; Jérôme Spitz; Paco Bustamante; Thomas Lacoue-Labarthe

doi:10.1016/j.scitotenv.2020.143907

Mercury in the tissues of five cephalopods species: First data on the nervous system

Antoine Minet, Alain Manceau, Anaïs Valada-Mennuni, Maud Brault-Favrou, Carine Churlaud, Jérôme Fort, Thành Nguyen, Jérôme Spitz, Paco Bustamante, Thomas Lacoue-Labarthe

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

15 Scopus citations

Abstract

Mercury (Hg), one of the elements most toxic to biota, accumulates within organisms throughout their lifespan and biomagnifies along trophic chain. Due to their key role in marine systems, cephalopods constitute a major vector of Hg in predators. Further, they grow rapidly and display complex behaviours, which can be altered by neurotoxic Hg. This study investigated Hg concentrations within 81 cephalopod specimens sampled in the Bay of Biscay, which belonged to five species: Eledone cirrhosa, Sepia officinalis, Loligo vulgaris, Todaropsis eblanae and Illex coindetii. Hg concentrations were measured in the digestive gland, the mantle muscle and the optic lobes of the brain. The digestive gland and the mantle were tissues with the most concentrated Hg among all species considered (up to 1.50 μg.g⁻¹ dw), except E. cirrhosa. This benthic cephalopod had 1.3-fold higher Hg concentrations in the brain (up to 1.89 μg.g⁻¹ dw) than in the mantle, while other species had 2-fold lower concentrations of Hg in the brain than in the mantle. Brain-Hg concentrations can be predicted from muscle-Hg concentrations for a given species, which facilitates the assessment of Hg toxicokinetics in cephalopods. In the most contaminated E. cirrhosa individual, the chemical form of Hg in its digestive gland, mantle muscle and optic lobes, was determined using High energy-Resolution X-ray Absorption Near Edge Structure (HR XANES) spectroscopy. In the digestive gland, 33 ± 11% of total Hg was inorganic Hg speciated as a dicysteinate complex (Hg(Cys)₂), which suggested that the demethylation of dietary MeHg occurs in this organ. All Hg found in the mantle muscle and the optic lobes is methylated and bound to one cysteinyl group (MeHgCys complex), which implies that dietary MeHg is distributed to these tissues via the bloodstream. These results raised the questions regarding interspecific differences observed regarding Hg brain concentrations and the possible effect of Hg on cephalopod functional brain plasticity and behaviour.

Original language	English
Article number	143907
Journal	Science of the Total Environment
Volume	759
DOIs	https://doi.org/10.1016/j.scitotenv.2020.143907
State	Published - Mar 10 2021
Externally published	Yes

Funding

This work is a contribution to the MERCy project funded by the Ministère de la Transition Ecologique et Solidaire et de la Fondation pour la Recherche sur la Biodiversité. The Région Nouvelle Aquitaine is acknowledged for its support to the PhD grant of AM through the EXPO project. We are grateful for the use of the facilities of the Plateforme Analyses Elémentaires of the LIENSs laboratory and to IFREMER for allowing the sampling during the EVHOE cruises (2016-2017). Thanks are due to the CPER (Contrat de Projet Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for funding the AMA of the LIENSs laboratory. The Institut Universitaire de France (IUF) is acknowledged for its support to PB as a Senior Member. This work benefitted from the French GDR “Aquatic Ecotoxicology” framework which aims at fostering stimulating scientific discussions and collaborations for more integrative approaches. The spectroscopic work was supported by the EcoX project funded by the Equipex initiative of the Agence Nationale pour la Recherche (ANR) under grant ANR-10-EQPX-27-01. This work is a contribution to the MERCy project funded by the Ministère de la Transition Ecologique et Solidaire et de la Fondation pour la Recherche sur la Biodiversité . The Région Nouvelle Aquitaine is acknowledged for its support to the PhD grant of AM through the EXPO project. We are grateful for the use of the facilities of the Plateforme Analyses Elémentaires of the LIENSs laboratory and to IFREMER for allowing the sampling during the EVHOE cruises (2016-2017). Thanks are due to the CPER (Contrat de Projet Etat-Région) and the FEDER ( Fonds Européen de Développement Régional ) for funding the AMA of the LIENSs laboratory. The Institut Universitaire de France (IUF) is acknowledged for its support to PB as a Senior Member. This work benefitted from the French GDR “Aquatic Ecotoxicology” framework which aims at fostering stimulating scientific discussions and collaborations for more integrative approaches. The spectroscopic work was supported by the EcoX project funded by the Equipex initiative of the Agence Nationale pour la Recherche (ANR) under grant ANR-10-EQPX-27-01 .

Funders	Funder number
French GDR
Ministère de la Transition Ecologique et Solidaire et de la Fondation pour la Recherche
Agence Nationale de la Recherche	ANR-10-EQPX-27-01
Agence Nationale de la Recherche
Institut universitaire de France
European Regional Development Fund

Keywords

Digestive gland
HR-XANES
Mantle muscle
MethylHg
Optic lobes
Organotropism
Speciation

UN SDGs

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

Access to Document

10.1016/j.scitotenv.2020.143907

Cite this

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title = "Mercury in the tissues of five cephalopods species: First data on the nervous system",

abstract = "Mercury (Hg), one of the elements most toxic to biota, accumulates within organisms throughout their lifespan and biomagnifies along trophic chain. Due to their key role in marine systems, cephalopods constitute a major vector of Hg in predators. Further, they grow rapidly and display complex behaviours, which can be altered by neurotoxic Hg. This study investigated Hg concentrations within 81 cephalopod specimens sampled in the Bay of Biscay, which belonged to five species: Eledone cirrhosa, Sepia officinalis, Loligo vulgaris, Todaropsis eblanae and Illex coindetii. Hg concentrations were measured in the digestive gland, the mantle muscle and the optic lobes of the brain. The digestive gland and the mantle were tissues with the most concentrated Hg among all species considered (up to 1.50 μg.g−1 dw), except E. cirrhosa. This benthic cephalopod had 1.3-fold higher Hg concentrations in the brain (up to 1.89 μg.g−1 dw) than in the mantle, while other species had 2-fold lower concentrations of Hg in the brain than in the mantle. Brain-Hg concentrations can be predicted from muscle-Hg concentrations for a given species, which facilitates the assessment of Hg toxicokinetics in cephalopods. In the most contaminated E. cirrhosa individual, the chemical form of Hg in its digestive gland, mantle muscle and optic lobes, was determined using High energy-Resolution X-ray Absorption Near Edge Structure (HR XANES) spectroscopy. In the digestive gland, 33 ± 11% of total Hg was inorganic Hg speciated as a dicysteinate complex (Hg(Cys)2), which suggested that the demethylation of dietary MeHg occurs in this organ. All Hg found in the mantle muscle and the optic lobes is methylated and bound to one cysteinyl group (MeHgCys complex), which implies that dietary MeHg is distributed to these tissues via the bloodstream. These results raised the questions regarding interspecific differences observed regarding Hg brain concentrations and the possible effect of Hg on cephalopod functional brain plasticity and behaviour.",

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T2 - First data on the nervous system

AU - Minet, Antoine

AU - Manceau, Alain

AU - Valada-Mennuni, Anaïs

AU - Brault-Favrou, Maud

AU - Churlaud, Carine

AU - Fort, Jérôme

AU - Nguyen, Thành

AU - Spitz, Jérôme

AU - Bustamante, Paco

AU - Lacoue-Labarthe, Thomas

PY - 2021/3/10

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N2 - Mercury (Hg), one of the elements most toxic to biota, accumulates within organisms throughout their lifespan and biomagnifies along trophic chain. Due to their key role in marine systems, cephalopods constitute a major vector of Hg in predators. Further, they grow rapidly and display complex behaviours, which can be altered by neurotoxic Hg. This study investigated Hg concentrations within 81 cephalopod specimens sampled in the Bay of Biscay, which belonged to five species: Eledone cirrhosa, Sepia officinalis, Loligo vulgaris, Todaropsis eblanae and Illex coindetii. Hg concentrations were measured in the digestive gland, the mantle muscle and the optic lobes of the brain. The digestive gland and the mantle were tissues with the most concentrated Hg among all species considered (up to 1.50 μg.g−1 dw), except E. cirrhosa. This benthic cephalopod had 1.3-fold higher Hg concentrations in the brain (up to 1.89 μg.g−1 dw) than in the mantle, while other species had 2-fold lower concentrations of Hg in the brain than in the mantle. Brain-Hg concentrations can be predicted from muscle-Hg concentrations for a given species, which facilitates the assessment of Hg toxicokinetics in cephalopods. In the most contaminated E. cirrhosa individual, the chemical form of Hg in its digestive gland, mantle muscle and optic lobes, was determined using High energy-Resolution X-ray Absorption Near Edge Structure (HR XANES) spectroscopy. In the digestive gland, 33 ± 11% of total Hg was inorganic Hg speciated as a dicysteinate complex (Hg(Cys)2), which suggested that the demethylation of dietary MeHg occurs in this organ. All Hg found in the mantle muscle and the optic lobes is methylated and bound to one cysteinyl group (MeHgCys complex), which implies that dietary MeHg is distributed to these tissues via the bloodstream. These results raised the questions regarding interspecific differences observed regarding Hg brain concentrations and the possible effect of Hg on cephalopod functional brain plasticity and behaviour.

AB - Mercury (Hg), one of the elements most toxic to biota, accumulates within organisms throughout their lifespan and biomagnifies along trophic chain. Due to their key role in marine systems, cephalopods constitute a major vector of Hg in predators. Further, they grow rapidly and display complex behaviours, which can be altered by neurotoxic Hg. This study investigated Hg concentrations within 81 cephalopod specimens sampled in the Bay of Biscay, which belonged to five species: Eledone cirrhosa, Sepia officinalis, Loligo vulgaris, Todaropsis eblanae and Illex coindetii. Hg concentrations were measured in the digestive gland, the mantle muscle and the optic lobes of the brain. The digestive gland and the mantle were tissues with the most concentrated Hg among all species considered (up to 1.50 μg.g−1 dw), except E. cirrhosa. This benthic cephalopod had 1.3-fold higher Hg concentrations in the brain (up to 1.89 μg.g−1 dw) than in the mantle, while other species had 2-fold lower concentrations of Hg in the brain than in the mantle. Brain-Hg concentrations can be predicted from muscle-Hg concentrations for a given species, which facilitates the assessment of Hg toxicokinetics in cephalopods. In the most contaminated E. cirrhosa individual, the chemical form of Hg in its digestive gland, mantle muscle and optic lobes, was determined using High energy-Resolution X-ray Absorption Near Edge Structure (HR XANES) spectroscopy. In the digestive gland, 33 ± 11% of total Hg was inorganic Hg speciated as a dicysteinate complex (Hg(Cys)2), which suggested that the demethylation of dietary MeHg occurs in this organ. All Hg found in the mantle muscle and the optic lobes is methylated and bound to one cysteinyl group (MeHgCys complex), which implies that dietary MeHg is distributed to these tissues via the bloodstream. These results raised the questions regarding interspecific differences observed regarding Hg brain concentrations and the possible effect of Hg on cephalopod functional brain plasticity and behaviour.

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KW - Mantle muscle

KW - MethylHg

KW - Optic lobes

KW - Organotropism

KW - Speciation

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Mercury in the tissues of five cephalopods species: First data on the nervous system

Abstract

Funding

Keywords

UN SDGs

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