A century of mercury: ecosystem-wide changes drive increasing contamination of a tropical seabird species in the South Atlantic Ocean

Fanny Cusset; Jim Reynolds; Alice Carravieri; David Amouroux; Océane Asensio; Roger Dickey; Jérôme Fort; B. John Hughes; Vitor Paiva; Jaime Ramos; Laura Shearer; Emmanuel Tessier; Colin Wearn; Yves Cherel; Paco Bustamante

doi:10.1016/j.envpol.2023.121187

A century of mercury: ecosystem-wide changes drive increasing contamination of a tropical seabird species in the South Atlantic Ocean

Fanny Cusset^*, Jim Reynolds, Alice Carravieri, David Amouroux, Océane Asensio, Roger Dickey, Jérôme Fort, B. John Hughes, Vitor Paiva, Jaime Ramos, Laura Shearer, Emmanuel Tessier, Colin Wearn, Yves Cherel, Paco Bustamante

^*Corresponding author for this work

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Abstract

Mercury (Hg) is a highly toxic metal that adversely impacts human and wildlife health. The amount of Hg released globally in the environment has increased steadily since the Industrial Revolution, resulting in growing contamination in biota. Seabirds have been extensively studied to monitor Hg contamination in the world's oceans. Multidecadal increases in seabird Hg contamination have been documented in polar, temperate and subtropical regions, whereas in tropical regions they are largely unknown. Since seabirds accumulate Hg mainly from their diet, their trophic ecology is fundamental in understanding their Hg exposure over time. Here, we used the sooty tern (Onychoprion fuscatus), the most abundant tropical seabird, as bioindicator of temporal variations in Hg transfer to marine predators in tropical ecosystems, in response to trophic changes and other potential drivers. Body feathers were sampled from 220 sooty terns, from museum specimens (n = 134) and free-living birds (n = 86) from Ascension Island, in the South Atlantic Ocean, over 145 years (1876–2021). Chemical analyses included (i) total- and methyl-Hg, and (ii) carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes, as proxies of foraging habitat and trophic position, respectively, to investigate the relationship between trophic ecology and Hg contamination over time. Despite current regulations on its global emissions, mean Hg concentrations were 58.9% higher in the 2020s (2.0 μg g⁻¹, n = 34) than in the 1920s (1.2 μg g⁻¹, n = 107). Feather Hg concentrations were negatively and positively associated with δ¹³C and δ¹⁵N values, respectively. The sharp decline of 2.9 ‰ in δ¹³C values over time indicates ecosystem-wide changes (shifting primary productivity) in the tropical South Atlantic Ocean and can help explain the observed increase in terns' feather Hg concentrations. Overall, this study provides invaluable information on how ecosystem-wide changes can increase Hg contamination of tropical marine predators and reinforces the need for long-term regulations of harmful contaminants at the global scale.

Original language	English
Article number	121187
Number of pages	11
Journal	Environmental Pollution
Volume	323
Early online date	31 Jan 2023
DOIs	https://doi.org/10.1016/j.envpol.2023.121187
Publication status	Published - 15 Apr 2023

Bibliographical note

Funding Information:
First, we thank all people involved in the original study of Reynolds et al. (2019), for bird sampling, both in museums and in the field. Funding for sample collections was provided by SJR. We are thankful to the Ascension Island Government for granting research permits to sample live birds in the 2000s, the 2010s and the 2020s. The authors are grateful to Carine Churlaud and Maud Brault-Favrou from the Analyses Elémentaires platform (LIENSs) for their support during Hg analysis and to Gaël Guillou from the Analyses Isotopiques platform (LIENSs) for running the stable isotope analyses. Special thanks are due to Sabrina Tartu and Céline Albert for statistical guidance during data exploration. We are grateful to Lucie Machin for the sooty tern drawing on the graphical abstract. Thanks are due to the CPER (Contrat de Projet Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for funding the AMA and IRMS of 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, that aims to foster stimulating scientific discussions and collaborations for more integrative approaches.

Publisher Copyright:
© 2023 Elsevier Ltd

Keywords

Feathers
Hg
Museum
sooty tern
Stable isotopes
Temporal monitoring

ASJC Scopus subject areas

Toxicology
Pollution
Health, Toxicology and Mutagenesis

UN SDGs

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

Access to Document

10.1016/j.envpol.2023.121187

CussetF2023centuryAccepted author manuscript, 1.13 MBLicence: Creative Commons: Attribution-NonCommercial-NoDerivs (CC BY-NC-ND)

Cite this

Cusset, F., Reynolds, J., Carravieri, A., Amouroux, D., Asensio, O., Dickey, R., Fort, J., Hughes, B. J., Paiva, V., Ramos, J., Shearer, L., Tessier, E., Wearn, C., Cherel, Y., & Bustamante, P. (2023). A century of mercury: ecosystem-wide changes drive increasing contamination of a tropical seabird species in the South Atlantic Ocean. Environmental Pollution, 323, Article 121187. https://doi.org/10.1016/j.envpol.2023.121187

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abstract = "Mercury (Hg) is a highly toxic metal that adversely impacts human and wildlife health. The amount of Hg released globally in the environment has increased steadily since the Industrial Revolution, resulting in growing contamination in biota. Seabirds have been extensively studied to monitor Hg contamination in the world's oceans. Multidecadal increases in seabird Hg contamination have been documented in polar, temperate and subtropical regions, whereas in tropical regions they are largely unknown. Since seabirds accumulate Hg mainly from their diet, their trophic ecology is fundamental in understanding their Hg exposure over time. Here, we used the sooty tern (Onychoprion fuscatus), the most abundant tropical seabird, as bioindicator of temporal variations in Hg transfer to marine predators in tropical ecosystems, in response to trophic changes and other potential drivers. Body feathers were sampled from 220 sooty terns, from museum specimens (n = 134) and free-living birds (n = 86) from Ascension Island, in the South Atlantic Ocean, over 145 years (1876–2021). Chemical analyses included (i) total- and methyl-Hg, and (ii) carbon (δ1³C) and nitrogen (δ15N) stable isotopes, as proxies of foraging habitat and trophic position, respectively, to investigate the relationship between trophic ecology and Hg contamination over time. Despite current regulations on its global emissions, mean Hg concentrations were 58.9\% higher in the 2020s (2.0 μg g−1, n = 34) than in the 1920s (1.2 μg g−1, n = 107). Feather Hg concentrations were negatively and positively associated with δ1³C and δ15N values, respectively. The sharp decline of 2.9 ‰ in δ1³C values over time indicates ecosystem-wide changes (shifting primary productivity) in the tropical South Atlantic Ocean and can help explain the observed increase in terns' feather Hg concentrations. Overall, this study provides invaluable information on how ecosystem-wide changes can increase Hg contamination of tropical marine predators and reinforces the need for long-term regulations of harmful contaminants at the global scale.",

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author = "Fanny Cusset and Jim Reynolds and Alice Carravieri and David Amouroux and Oc{\'e}ane Asensio and Roger Dickey and J{\'e}r{\^o}me Fort and Hughes, \{B. John\} and Vitor Paiva and Jaime Ramos and Laura Shearer and Emmanuel Tessier and Colin Wearn and Yves Cherel and Paco Bustamante",

note = "Funding Information: First, we thank all people involved in the original study of Reynolds et al. (2019), for bird sampling, both in museums and in the field. Funding for sample collections was provided by SJR. We are thankful to the Ascension Island Government for granting research permits to sample live birds in the 2000s, the 2010s and the 2020s. The authors are grateful to Carine Churlaud and Maud Brault-Favrou from the Analyses El{\'e}mentaires platform (LIENSs) for their support during Hg analysis and to Ga{\"e}l Guillou from the Analyses Isotopiques platform (LIENSs) for running the stable isotope analyses. Special thanks are due to Sabrina Tartu and C{\'e}line Albert for statistical guidance during data exploration. We are grateful to Lucie Machin for the sooty tern drawing on the graphical abstract. Thanks are due to the CPER (Contrat de Projet Etat-R{\'e}gion) and the FEDER (Fonds Europ{\'e}en de D{\'e}veloppement R{\'e}gional) for funding the AMA and IRMS of 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, that aims to foster stimulating scientific discussions and collaborations for more integrative approaches. Publisher Copyright: {\textcopyright} 2023 Elsevier Ltd",

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Cusset, F, Reynolds, J, Carravieri, A, Amouroux, D, Asensio, O, Dickey, R, Fort, J, Hughes, BJ, Paiva, V, Ramos, J, Shearer, L, Tessier, E, Wearn, C, Cherel, Y & Bustamante, P 2023, 'A century of mercury: ecosystem-wide changes drive increasing contamination of a tropical seabird species in the South Atlantic Ocean', Environmental Pollution, vol. 323, 121187. https://doi.org/10.1016/j.envpol.2023.121187

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AU - Cusset, Fanny

AU - Reynolds, Jim

AU - Carravieri, Alice

AU - Amouroux, David

AU - Asensio, Océane

AU - Dickey, Roger

AU - Fort, Jérôme

AU - Hughes, B. John

AU - Paiva, Vitor

AU - Ramos, Jaime

AU - Shearer, Laura

AU - Tessier, Emmanuel

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AU - Cherel, Yves

AU - Bustamante, Paco

N1 - Funding Information: First, we thank all people involved in the original study of Reynolds et al. (2019), for bird sampling, both in museums and in the field. Funding for sample collections was provided by SJR. We are thankful to the Ascension Island Government for granting research permits to sample live birds in the 2000s, the 2010s and the 2020s. The authors are grateful to Carine Churlaud and Maud Brault-Favrou from the Analyses Elémentaires platform (LIENSs) for their support during Hg analysis and to Gaël Guillou from the Analyses Isotopiques platform (LIENSs) for running the stable isotope analyses. Special thanks are due to Sabrina Tartu and Céline Albert for statistical guidance during data exploration. We are grateful to Lucie Machin for the sooty tern drawing on the graphical abstract. Thanks are due to the CPER (Contrat de Projet Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for funding the AMA and IRMS of 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, that aims to foster stimulating scientific discussions and collaborations for more integrative approaches. Publisher Copyright: © 2023 Elsevier Ltd

PY - 2023/4/15

Y1 - 2023/4/15

N2 - Mercury (Hg) is a highly toxic metal that adversely impacts human and wildlife health. The amount of Hg released globally in the environment has increased steadily since the Industrial Revolution, resulting in growing contamination in biota. Seabirds have been extensively studied to monitor Hg contamination in the world's oceans. Multidecadal increases in seabird Hg contamination have been documented in polar, temperate and subtropical regions, whereas in tropical regions they are largely unknown. Since seabirds accumulate Hg mainly from their diet, their trophic ecology is fundamental in understanding their Hg exposure over time. Here, we used the sooty tern (Onychoprion fuscatus), the most abundant tropical seabird, as bioindicator of temporal variations in Hg transfer to marine predators in tropical ecosystems, in response to trophic changes and other potential drivers. Body feathers were sampled from 220 sooty terns, from museum specimens (n = 134) and free-living birds (n = 86) from Ascension Island, in the South Atlantic Ocean, over 145 years (1876–2021). Chemical analyses included (i) total- and methyl-Hg, and (ii) carbon (δ1³C) and nitrogen (δ15N) stable isotopes, as proxies of foraging habitat and trophic position, respectively, to investigate the relationship between trophic ecology and Hg contamination over time. Despite current regulations on its global emissions, mean Hg concentrations were 58.9% higher in the 2020s (2.0 μg g−1, n = 34) than in the 1920s (1.2 μg g−1, n = 107). Feather Hg concentrations were negatively and positively associated with δ1³C and δ15N values, respectively. The sharp decline of 2.9 ‰ in δ1³C values over time indicates ecosystem-wide changes (shifting primary productivity) in the tropical South Atlantic Ocean and can help explain the observed increase in terns' feather Hg concentrations. Overall, this study provides invaluable information on how ecosystem-wide changes can increase Hg contamination of tropical marine predators and reinforces the need for long-term regulations of harmful contaminants at the global scale.

AB - Mercury (Hg) is a highly toxic metal that adversely impacts human and wildlife health. The amount of Hg released globally in the environment has increased steadily since the Industrial Revolution, resulting in growing contamination in biota. Seabirds have been extensively studied to monitor Hg contamination in the world's oceans. Multidecadal increases in seabird Hg contamination have been documented in polar, temperate and subtropical regions, whereas in tropical regions they are largely unknown. Since seabirds accumulate Hg mainly from their diet, their trophic ecology is fundamental in understanding their Hg exposure over time. Here, we used the sooty tern (Onychoprion fuscatus), the most abundant tropical seabird, as bioindicator of temporal variations in Hg transfer to marine predators in tropical ecosystems, in response to trophic changes and other potential drivers. Body feathers were sampled from 220 sooty terns, from museum specimens (n = 134) and free-living birds (n = 86) from Ascension Island, in the South Atlantic Ocean, over 145 years (1876–2021). Chemical analyses included (i) total- and methyl-Hg, and (ii) carbon (δ1³C) and nitrogen (δ15N) stable isotopes, as proxies of foraging habitat and trophic position, respectively, to investigate the relationship between trophic ecology and Hg contamination over time. Despite current regulations on its global emissions, mean Hg concentrations were 58.9% higher in the 2020s (2.0 μg g−1, n = 34) than in the 1920s (1.2 μg g−1, n = 107). Feather Hg concentrations were negatively and positively associated with δ1³C and δ15N values, respectively. The sharp decline of 2.9 ‰ in δ1³C values over time indicates ecosystem-wide changes (shifting primary productivity) in the tropical South Atlantic Ocean and can help explain the observed increase in terns' feather Hg concentrations. Overall, this study provides invaluable information on how ecosystem-wide changes can increase Hg contamination of tropical marine predators and reinforces the need for long-term regulations of harmful contaminants at the global scale.

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A century of mercury: ecosystem-wide changes drive increasing contamination of a tropical seabird species in the South Atlantic Ocean

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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