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A global perspective on the trophic geography of sharks

Nature Ecology & Evolutionvolume 2pages299305 (2018) | Download Citation

Abstract

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.

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Acknowledgements

This research was conducted as part of C.S.B.’s Ph.D dissertation, which was funded by the University of Southampton and NERC (NE/L50161X/1), and through a NERC Grant-in-Kind from the Life Sciences Mass Spectrometry Facility (LSMSF; EK267-03/16). We thank A. Bates, D. Sims, F. Neat, R. McGill and J. Newton for their analytical contributions and comments on the manuscripts.

Author information

Author notes

    • Christopher S. Bird

    Present address: Centre for Environment, Fisheries, & Aquaculture Sciences (CEFAS), Lowestoft, UK

    • Dana M. Bethea

    Present address: NOAA National Marine Fisheries Service, Southeast Regional Office, St. Petersburg, FL, USA

    • Dean L. Courtney

    Present address: National Oceanic and Atmospheric Administration, Southeast Fisheries Science Center, Panama City Laboratory, Delwood Beach Road, Panama City, FL, USA

Affiliations

  1. Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, UK

    • Christopher S. Bird
    • , Sarah Magozzi
    • , Katie Quaeck-Davies
    •  & Clive N. Trueman
  2. CIBIO—Research Center in Biodiversity and Genetic Resources, Vairão, Portugal

    • Ana Veríssimo
  3. Virginia Institute of Marine Science, Gloucester Point, VA, USA

    • Ana Veríssimo
  4. College of Science & Engineering, James Cook University, Cairns, Queensland, Australia

    • Kátya G. Abrantes
    •  & Adam Barnett
  5. IRBio, Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona, Spain

    • Alex Aguilar
    •  & Asuncion Borrell
  6. Department of Biology, College of Science, Sultan Qaboos Univeristy, Muscat, Oman

    • Hassan Al-Reasi
  7. NOAA, National Marine Fisheries Service, Southeast Fisheries Science Center, 3500 Delwood Beach Road, Panama City, FL, USA

    • Dana M. Bethea
  8. Ifremer, Unité Halieutique Gascogne Sud, Laboratoire Ressources Halieutiques de La Rochelle, L’Houmeau, France

    • Gérard Biais
  9. Ifremer, Unité Littoral, Laboratoire Environnement Ressources Provence Azur Corse, La Seyne sur Mer, France

    • Marc Bouchoucha
  10. FishWise, Santa Cruz, CA, USA

    • Mariah Boyle
  11. Shark Research and Conservation Program, Cape Eleuthera Institute, Eleuthera, Bahamas

    • Edward J. Brooks
  12. Gladbachstrasse 60, Zurich, Switzerland

    • Juerg Brunnschweiler
  13. Littoral Environnement et Sociétés (LIENSs), UMR 7266, CNRS-Université de La Rochelle, La Rochelle, France

    • Paco Bustamante
  14. Hopkins Marine Station of Stanford University, Pacific Grove, CA, USA

    • Aaron Carlisle
  15. MARE—Marine and Environmental Sciences Centre, Department of Oceanography and Fisheries, University of the Azores, Azores, Portugal

    • Diana Catarino
    • , Ana Colaço
    •  & Gui M. Menezes
  16. Estación Biológica de Doñana, Consejo Superior de Investigationes Científicas (CSIC), Sevilla, Spain

    • Stéphane Caut
  17. Centre d’Etudes Biologiques de Chizé, UMR 7372, CNRS-Université de La Rochelle, Villiers-en-Bois, France

    • Yves Cherel
  18. Unité Biogéochimie et Écotoxicologie, Laboratoire de Biogéochimie des Contaminants Métalliques, Nantes, France

    • Tiphaine Chouvelon
  19. Marine Sciences Program, School of Environment, Arts and Society, Florida International University, North Miami, FL, USA

    • Diana Churchill
  20. CESIMAR Centro Nacional Patagónico, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Puerto Madryn, Chubut, Argentina

    • Javier Ciancio
  21. Laboratoire de Biologie Marine, Earth and Life Institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgium

    • Julien Claes
  22. College of Fisheries and Ocean Sciences, Juneau Center, University of Alaska Fairbanks, Point Lena Loop Road, Juneau, AK, USA

    • Dean L. Courtney
  23. Ifremer, Unité Halieutique Manche Mer du Nord, Laboratoire Ressources Halieutiques de Boulogne, Boulogne-sur-Mer, France

    • Pierre Cresson
  24. Port Elizabeth Museum at Bayworld, Port Elizabeth, South Africa

    • Ryan Daly
  25. Save Our Seas Foundation—D’Arros Research Centre (SOSF-DRC), Geneva, Switzerland

    • Ryan Daly
  26. University of Cape Town, Department of Biological Sciences, Cape Town, South Africa

    • Leigh de Necker
  27. School of Pharmaceutical Sciences, Health Sciences University of Hokkaido, Hokkaido, Japan

    • Tetsuya Endo
  28. Departamento do Mar IPMA, Lisbon, Portugal

    • Ivone Figueiredo
  29. Reef HQ, Great Barrier Reef Marine Park Authority, Townsville, Queensland, Australia

    • Ashley J. Frisch
  30. Aquatic Biology, Department of Bioscience, Aarhus University, Aarhus C, Denmark

    • Joan Holst Hansen
  31. School of Environment, Arts, and Society, Florida International University, North Miami, FL, USA

    • Michael Heithaus
  32. Biological Sciences, University of Windsor, Windsor, Canada

    • Nigel E. Hussey
  33. Department of Fisheries and Aquatic Sciences, University of Namibia, Henties Bay, Namibia

    • Johannes Iitembu
  34. Department of Biology, University of Victoria, Victoria, British Columbia, Canada

    • Francis Juanes
  35. Ocean Associates, Inc., Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, USA

    • Michael J. Kinney
  36. Marine Sciences Program, Department of Biological Sciences, Florida International University, North Miami, FL, USA

    • Jeremy J. Kiszka
  37. Centro de Investigacion para la Sustentabilidad, Facultad de Ecologia y Recursos Naturales, Universidad Andres Bello, Santiago, Chile

    • Sebastian A. Klarian
  38. Ifremer, Unité Sciences et Techniques Halieutiques, Laboratoire de Technologie et Biologie Halieutique, Lorient, France

    • Dorothée Kopp
  39. Division of Coastal Sciences, University of Southern Mississippi, Ocean Springs, MS, USA

    • Robert Leaf
  40. College of Marine Sciences, Shanghai Ocean University, Shanghai, China

    • Yunkai Li
  41. Institut de Recherche pour le Développement (IRD), R 195 LEMAR, UMR 6539 (UBO, CNRS, IRD, IFREMER), Nouméa, New Caledonia

    • Anne Lorrain
  42. Harvard University Center for the Environment, Harvard University, Cambridge, MA, USA

    • Daniel J. Madigan
  43. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    • Aleksandra Maljković
  44. Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    • Luis Malpica-Cruz
  45. Marine Sciences Program, Florida International University, North Miami, FL, USA

    • Philip Matich
  46. Texas Research Institute for Environmental Studies, Sam Houston State University, Huntsville, TX, USA

    • Philip Matich
  47. Australian Institute of Marine Science, Indian Ocean Marine Research Centre, The University of Western Australia, Perth, Western Australia, Australia

    • Mark G. Meekan
    •  & Conrad W. Speed
  48. Mediterranean Istitute of Oceanography (MIO), Aix Marseille Université, Université de Toulon, CNRS, IRD, 13288 Marseille, France

    • Frédéric Ménard
  49. Australian Rivers Institute, Griffith University, Nathan, Queensland, Australia

    • Samantha E. M. Munroe
  50. Department of Environmental and Aquatic Animal Health, Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, VA, USA

    • Michael C. Newman
  51. Department of Biological Sciences, Florida International University, North Miami, FL, USA

    • Yannis P. Papastamatiou
  52. Scottish Oceans Institute, School of Biology, University of St. Andrews, St. Andrews, UK

    • Yannis P. Papastamatiou
  53. CSIRO Oceans and Atmosphere, Hobart, Tasmania, Australia

    • Heidi Pethybridge
  54. Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, USA

    • Jeffrey D. Plumlee
    •  & R. J. David Wells
  55. Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA

    • Jeffrey D. Plumlee
    •  & R. J. David Wells
  56. Facultad de Ciencias Naturales e Ingeniería, Programa de Biología, Universidad de Bogotá Jorge Tadeo Lozano Marina, Bogotá, Colombia

    • Carlos Polo-Silva
  57. Department of Environmental and Life Sciences, University of Newcastle, Newcastle, New South Wales, Australia

    • Vincent Raoult
  58. Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA, USA

    • Jonathan Reum
  59. Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México (EPOMEX), Universidad Autónoma de Campeche (UAC), Campeche, Campeche, Mexico

    • Yassir Eden Torres-Rojas
  60. Earth to Oceans Group, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    • David S. Shiffman
  61. School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA

    • Oliver N. Shipley
  62. Department of Environmental Conservation, University of Massachusetts Amherst, Amherst, MA, USA

    • Michelle D. Staudinger
  63. Department of the Interior Northeast Climate Science Center, Amherst, MA, USA

    • Michelle D. Staudinger
  64. Department of Biology, University of Victoria, Victoria, British Columbia, Canada

    • Amy K. Teffer
  65. WorldFish Timor-Leste, Dili, Timor-Leste

    • Alexander Tilley
  66. Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Palma, Spain

    • Maria Valls
  67. The Guy Harvey Research Institute, Nova Southeastern University, Dania Beach, FL, USA

    • Jeremy J. Vaudo
  68. State Key Laboratory in Marine Pollution, City University of Hong Kong, Kowloon, Hong Kong, China

    • Tak-Cheung Wai
  69. Department of Chemical Oceanography, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan

    • Alex S. J. Wyatt
  70. National Oceanography Centre Southampton, Southampton, UK

    • Andrew Yool

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Contributions

C.S.B. and C.N.T. contributed the concept and design. C.S.B., C.N.T. and A.V. led the project. C.S.B. and C.N.T. wrote the manuscript. C.S.B., C.N.T., S.M. and A.Y analysed and interpreted the data. C.S.B., C.N.T., A.V., K.G.A., A.A., H.A.-R., A.B., D.M.B., G.B., A.B., M. Bouchoucha, M. Boyle, E.J.B., J.B., P.B., A.C., D.C., J. Ciancio, J. Claes, A.C., D.C., P.C., R.D., L.d.N., T.E., I.F., A.J.F., J.H.H., M.H., N.E.H., J.I., F.J., M.J.K., J.J.K., D.K., R.L., Y.L., S.A.K., A.L., D.M., A.M., L.M.-C., P.M., M.M., F.M., G.M.M., S.M., M.N., Y.P., H.P., J.D.P., C.P.-S., K.Q.-D., V.R., J.R., Y.E.T.-R., D.S.S., O.N.S., C.W.S., M.S., A. Teffer, A. Tilley, M.V., J.J.V., T-C.W., R.J.D.W. and A.S.J.W. provided data and/or samples. All authors have read, provided comments and approved the final manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Christopher S. Bird or Clive N. Trueman.

Supplementary information

  1. Supplementary Information

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  2. Life Sciences Reporting Summary

  3. Supplementary Data

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DOI

https://doi.org/10.1038/s41559-017-0432-z