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The Twilight Zone as a Major Foraging Habitat and Mercury Source for the Great White Shark

  • Gaël Le Croizier*
    Gaël Le Croizier
    UMR Géosciences Environnement Toulouse (GET), Observatoire Midi Pyrénées (OMP), 14 avenue Edouard Belin, 31400 Toulouse, France
    *Email: [email protected]
  • Anne Lorrain
    Anne Lorrain
    Univ Brest, CNRS, Ifremer, LEMAR, 29280 Plouzané, France
    More by Anne Lorrain
  • Jeroen E. Sonke
    Jeroen E. Sonke
    UMR Géosciences Environnement Toulouse (GET), Observatoire Midi Pyrénées (OMP), 14 avenue Edouard Belin, 31400 Toulouse, France
  • E. Mauricio Hoyos-Padilla*
    E. Mauricio Hoyos-Padilla
    Pelagios-Kakunjá A.C., Sinaloa 1540, Col. Las Garzas, 23070 La Paz, Baja California Sur, México
    Fins Attached: Marine Research and Conservation, 19675 Still Glen Drive, Colorado Springs, Colorado 80908, United States
    *Email: [email protected]
  • Felipe Galván-Magaña
    Felipe Galván-Magaña
    Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n., 23096 La Paz, Baja California Sur, México
  • Omar Santana-Morales
    Omar Santana-Morales
    ECOCIMATI A.C., 22800 Ensenada, Baja California, Mexico
  • Marc Aquino-Baleytó
    Marc Aquino-Baleytó
    Pelagios-Kakunjá A.C., Sinaloa 1540, Col. Las Garzas, 23070 La Paz, Baja California Sur, México
    Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n., 23096 La Paz, Baja California Sur, México
  • Edgar E. Becerril-García
    Edgar E. Becerril-García
    Pelagios-Kakunjá A.C., Sinaloa 1540, Col. Las Garzas, 23070 La Paz, Baja California Sur, México
    Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n., 23096 La Paz, Baja California Sur, México
  • Gádor Muntaner-López
    Gádor Muntaner-López
    Pelagios-Kakunjá A.C., Sinaloa 1540, Col. Las Garzas, 23070 La Paz, Baja California Sur, México
    Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n., 23096 La Paz, Baja California Sur, México
  • James Ketchum
    James Ketchum
    Pelagios-Kakunjá A.C., Sinaloa 1540, Col. Las Garzas, 23070 La Paz, Baja California Sur, México
  • Barbara Block
    Barbara Block
    Hopkins Marine Station, Stanford University, Pacific Grove, California 93950, United States
  • Aaron Carlisle
    Aaron Carlisle
    School of Marine Science and Policy, University of Delaware, Lewes, Delaware 19958, United States
  • Salvador J. Jorgensen
    Salvador J. Jorgensen
    Institute of Marine Sciences, University of California, Santa Cruz, Santa Cruz, California 95064, United States
  • Lucien Besnard
    Lucien Besnard
    Univ Brest, CNRS, Ifremer, LEMAR, 29280 Plouzané, France
  • Armelle Jung
    Armelle Jung
    Des Requins et Des Hommes (DRDH), BLP/Technopole Brest-Iroise, 15 rue Dumont d’Urville, Plouzané 29860, France
    More by Armelle Jung
  • Gauthier Schaal
    Gauthier Schaal
    Univ Brest, CNRS, Ifremer, LEMAR, 29280 Plouzané, France
  • , and 
  • David Point
    David Point
    UMR Géosciences Environnement Toulouse (GET), Observatoire Midi Pyrénées (OMP), 14 avenue Edouard Belin, 31400 Toulouse, France
    More by David Point
Cite this: Environ. Sci. Technol. 2020, 54, 24, 15872–15882
Publication Date (Web):November 25, 2020
https://doi.org/10.1021/acs.est.0c05621
Copyright © 2020 American Chemical Society

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    Abstract

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    The twilight zone contains the largest biomass of the world’s ocean. Identifying its role in the trophic supply and contaminant exposure of marine megafauna constitutes a critical challenge in the context of global change. The white shark (Carcharodon carcharias) is a threatened species with some of the highest concentrations of neurotoxin methylmercury (MeHg) among marine top predators. Large white sharks migrate seasonally from coastal habitats, where they primarily forage on pinnipeds, to oceanic offshore habitats. Tagging studies suggest that while offshore, white sharks may forage at depth on mesopelagic species, yet no biochemical evidence exists. Here, we used mercury isotopic composition to assess the dietary origin of MeHg contamination in white sharks from the Northeast Pacific Ocean. We estimated that a minimum of 72% of the MeHg accumulated by white sharks originates from the consumption of mesopelagic prey, while a maximum of 25% derives from pinnipeds. In addition to highlighting the potential of mercury isotopes to decipher the complex ecological cycle of marine predators, our study provides evidence that the twilight zone constitutes a crucial foraging habitat for these large predators, which had been suspected for over a decade. Climate change is predicted to expand the production of mesopelagic MeHg and modify the mesopelagic biomass globally. Considering the pivotal role of the twilight zone is therefore essential to better predict both MeHg exposure and trophic supply to white sharks, and effectively protect these key vulnerable predators.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c05621.

    • Hg isotope signatures in pelagic fish and squids from the foraging habitat of Northeast Pacific white sharks, obtained in previous studies (Figure S1 and Table S2); global data set of the shark and seal samples analyzed in this study (Table S3); and the summary (mean ± 2SD) of δ202Hg and Δ199Hg values measured in certified reference materials (Table S1) (PDF)

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    Cited By

    This article is cited by 20 publications.

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    2. Katherine A. Crichton, Jamie D. Wilson, Andy Ridgwell, Flavia Boscolo-Galazzo, Eleanor H. John, Bridget S. Wade, Paul N. Pearson. What the geological past can tell us about the future of the ocean’s twilight zone. Nature Communications 2023, 14 (1) https://doi.org/10.1038/s41467-023-37781-6
    3. Kiook Baek, Chulyong Park, Joon Sakong. Increase of blood mercury level with shark meat consumption: A repeated-measures study before and after Chuseok, Korean holiday. Chemosphere 2023, 344 , 140317. https://doi.org/10.1016/j.chemosphere.2023.140317
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    11. Gaël Le Croizier, Jeroen E. Sonke, Anne Lorrain, Sandrine Serre, Lucien Besnard, Gauthier Schaal, Felipe Amezcua-Martinez, David Point. Mercury stable isotopes suggest reduced foraging depth in oxygen minimum zones for blue sharks. Marine Pollution Bulletin 2022, 181 , 113892. https://doi.org/10.1016/j.marpolbul.2022.113892
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    13. David Grémillet, Damien Chevallier, Christophe Guinet, . Big data approaches to the spatial ecology and conservation of marine megafauna. ICES Journal of Marine Science 2022, 79 (4) , 975-986. https://doi.org/10.1093/icesjms/fsac059
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