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Circumpolar assessment of mercury contamination: the Adélie penguin as a bioindicator of Antarctic marine ecosystems

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Abstract

Due to its persistence and potential ecological and health impacts, mercury (Hg) is a global pollutant of major concern that may reach high concentrations even in remote polar oceans. In contrast to the Arctic Ocean, studies documenting Hg contamination in the Southern Ocean are spatially restricted and large-scale monitoring is needed. Here, we present the first circumpolar assessment of Hg contamination in Antarctic marine ecosystems. Specifically, the Adélie penguin (Pygoscelis adeliae) was used as a bioindicator species, to examine regional variation across 24 colonies distributed across the entire Antarctic continent. Mercury was measured on body feathers collected from both adults (n = 485) and chicks (n = 48) between 2005 and 2021. Because penguins’ diet represents the dominant source of Hg, feather δ13C and δ15N values were measured as proxies of feeding habitat and trophic position. As expected, chicks had lower Hg concentrations (mean ± SD: 0.22 ± 0.08 μg·g‒1) than adults (0.49 ± 0.23 μg·g‒1), likely because of their shorter bioaccumulation period. In adults, spatial variation in feather Hg concentrations was driven by both trophic ecology and colony location. The highest Hg concentrations were observed in the Ross Sea, possibly because of a higher consumption of fish in the diet compared to other sites (krill-dominated diet). Such large-scale assessments are critical to assess the effectiveness of the Minamata Convention on Mercury. Owing to their circumpolar distribution and their ecological role in Antarctic marine ecosystems, Adélie penguins could be valuable bioindicators for tracking spatial and temporal trends of Hg across Antarctic waters in the future.

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Highlights

  • Adélie penguins are relevant bioindicators of Hg contamination in Antarctic marine ecosystems.

  • Feather Hg concentrations were measured in 24 breeding colonies (adults and chicks).

  • The highest Hg concentrations were found in the Ross Sea.

  • Both trophic ecology and colony location drove feather Hg concentrations.

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Acknowledgements

The authors are thankful to all people involved in fieldwork, sample preparation and shipment in all Antarctic research stations. In addition, we thank the Mawson seabird field team and Casey station expeditioners for collecting samples, and Marcus Salton for organising sample transport. Special thanks are due to Yan Ropert-Coudert for his help in the construction of collaborations in the Antarctic research community and to Frédéric Angelier. The authors are grateful to (i) Maud Brault-Favrou and Carine Churlaud from the Plateforme Analyses Élémentaires of the LIENSs for their support during Hg analyses, as well as (ii) Sandy Pascaud for her support in sample preparation in the laboratory, and to (iii) Julie Charrier for the penguin drawings in the figures. The IUF (Institut Universitaire de France) is acknowledged for its support to Paco Bustamante as a Senior Member. This study is also a contribution to the Excellence Chair in Marine Ecology ECOMM funded by the Région Nouvelle Aquitaine (France). This work/review benefitted from the French GDR Aquatic Ecotoxicology framework which aims at fostering stimulating scientific discussions and collaborations for more integrative approaches.

Funding

This work relied on several national and international existing monitoring programs in Antarctica, implying several funding sources associated with the logistical support to all research stations. (i) The circumpolar monitoring program led by Jean-Baptiste Thiebot was funded by National Geographic Society grant WW-24R-17. (ii) Samples from Mac.Robertson Land (Mawson station), Princess Elizabeth Land (Davis station) and Wilkes Land (Casey station) were collected through Australian Antarctic Division support to AAS 4518. (iii) Sampling in Adélie Land was supported financially and logistically by IPEV (Programmes N°109 ORNITHOECO, C. Barbraud, and N°1091 AMMER, A. Kato and T. Raclot) and WWF-UK. (iv) Sampling in Terra Nova Bay was funded by the Ministry and Research (MUR) and National Research Council Italy (CNR) through project #PNRA2016_004 Penguin ERA. (v) Sampling in Ross Island was funded by the National Science Foundation (OPP Award, #1543498). (vi) Fieldwork in Ardley Island was supported by Instituto Antártico Uruguato (IAU), Ecos Sud Program (project PU20B01/U20B03), Commission for the Conservation of Antarctic Marine Living Ressources (CCAMLR) General Capacity Building Fund and Scientific Scholarship Scheme, Agencia Nacional de Investigación e Innovación’s (ANII) Clemente Estable Fund (project FCE 1 2021 1 166587), National System of Researchers and National Postgraduate Scholarship Programme, and Basic Science Development Programme (PEDECIBA). (vii) The Instituto Antártico Argentino ‒ Dirección Nacional del Antártico (PINST-05) provided financial and logistical support to carry out the Argentine Antarctic campaign. Finally, funding was provided by CPER (Contrat de Plan Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for the AMA and the IRMS of LIENSs laboratory.

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Authors and Affiliations

Authors

Contributions

Conceptualization: FC, PB, JF, YC. Methodology: FC, PB, AC, YC. Software: FC, AC, CB. Investigation: FC, PV. Formal analysis: FC, AC. Visualization: FC, CB. Writing - original draft preparation: FC, PB, AC, YC. Writing - review and editing: FC, PB, AC, CB, RB, IC, MD, LE, GG, TH, MJ, AK, ALM-G, CM, SO, MP, TR, MS, AS, CS, AS, AT, JBT, PT, CW, JF and YC. Project administration: FC. Funding acquisition: PB, Resources: AC, RB, IC, MD, LE, TH, MJ, ALM-G, CM, SO, MP, TR, MS, AS, CS, AS, AT, JBT, PT, CW. Supervision: PB, JF, YC.

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Correspondence to Fanny Cusset.

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The authors declare no competing interests.

Ethics approval

In this work, feather sampling relied on several existing monitoring programs and were carried out at all sites under appropriate permits. More specifically, (i) animal handling and sample collection for Australian stations (Mawson, Davis and Casey stations) were approved by the Australian Antarctic Division animal ethics committee and ATEP environmental approvals. (ii) Fieldwork in Adélie Land was approved by the Conseil des Programmes Scientifiques et Technologies Polaires of the Institut Polaire Français Paul Emile Victor (IPEV), and procedures were approved by the Animal Ethics Committee of IPEV. (iii) Fieldwork in Terra Nova Bay was approved under permission released from the Programma Nazionale di Ricerche in Antartide (PNRA). All sampling followed SCAR’s Code of Conduct for the Use of Animals for Scientific Purposes in Antarctica (https://www.scar.org/policy/scar-codes-of-conduct). (iv) The Instituto Antártico Argentino ‒ Dirección Nacional del Antártico (PINST-05) provided financial and logistical support to carry out the Argentine Antarctic campaign. The field work was carried out under the permit granted by the Dirreción Nacional del Antártico (Environmental Management Office). (v) Animal handling and sample collection at Signy Island was approved by the British Antarctic Survey Animal Welfare and Ethical Review Board, and permission was granted by the British Foreign and Commonwealth Office on behalf of HM Secretary of State, under Sections 12 and 13 of the Antarctic Act, 1994, 2013.

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Cusset, F., Bustamante, P., Carravieri, A. et al. Circumpolar assessment of mercury contamination: the Adélie penguin as a bioindicator of Antarctic marine ecosystems. Ecotoxicology 32, 1024–1049 (2023). https://doi.org/10.1007/s10646-023-02709-9

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  • DOI: https://doi.org/10.1007/s10646-023-02709-9

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