Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish

Edited by Karen A. Kidd, University of New Brunwsick, Saint John, BC, Canada, and accepted by the Editorial Board February 24, 2014 (received for review November 6, 2013)
March 24, 2014
111 (15) E1510-E1518

Significance

The 2010 Deepwater Horizon (MC252) disaster in the northern Gulf of Mexico released more than 4 million barrels of crude oil. Oil rose from the ocean floor to the surface where many large pelagic fish spawn. Here we describe the impacts of field-collected oil samples on the rapidly developing embryos of warm-water predators, including bluefin and yellowfin tunas and an amberjack. For each species, environmentally relevant MC252 oil exposures caused serious defects in heart development. Moreover, abnormalities in cardiac function were highly consistent, indicating a broadly conserved developmental crude oil cardiotoxicity. Losses of early life stages were therefore likely for Gulf populations of tunas, amberjack, swordfish, billfish, and other large predators that spawned in oiled surface habitats.

Abstract

The Deepwater Horizon disaster released more than 636 million L of crude oil into the northern Gulf of Mexico. The spill oiled upper surface water spawning habitats for many commercially and ecologically important pelagic fish species. Consequently, the developing spawn (embryos and larvae) of tunas, swordfish, and other large predators were potentially exposed to crude oil-derived polycyclic aromatic hydrocarbons (PAHs). Fish embryos are generally very sensitive to PAH-induced cardiotoxicity, and adverse changes in heart physiology and morphology can cause both acute and delayed mortality. Cardiac function is particularly important for fast-swimming pelagic predators with high aerobic demand. Offspring for these species develop rapidly at relatively high temperatures, and their vulnerability to crude oil toxicity is unknown. We assessed the impacts of field-collected Deepwater Horizon (MC252) oil samples on embryos of three pelagic fish: bluefin tuna, yellowfin tuna, and an amberjack. We show that environmentally realistic exposures (1–15 µg/L total PAH) cause specific dose-dependent defects in cardiac function in all three species, with circulatory disruption culminating in pericardial edema and other secondary malformations. Each species displayed an irregular atrial arrhythmia following oil exposure, indicating a highly conserved response to oil toxicity. A considerable portion of Gulf water samples collected during the spill had PAH concentrations exceeding toxicity thresholds observed here, indicating the potential for losses of pelagic fish larvae. Vulnerability assessments in other ocean habitats, including the Arctic, should focus on the developing heart of resident fish species as an exceptionally sensitive and consistent indicator of crude oil impacts.

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Acknowledgments

The authors thank Adam Miller, Morten Deichmann, and Craig Foster of Cleanseas Tuna for providing bluefin tuna and amberjack embryos, and advice on culture conditions; Erin Bubner and Bob Delaine for facilities access and logistical support at the Lincoln Marine Science Center; Tor Linbo and Robbie Schallert for assistance with bluefin tuna and amberjack embryo exposures; the Inter-American Tropical Tuna Commission members Guillermo Campeán, Richard Deriso, Daniel Margulies, Vernon Scholey, and the staff at the Achotines Laboratory for providing access to the yellowfin tuna broodstock and laboratory facilities; Bernadita Anulacion, Daryle Boyd, and Ron Pearce for assistance with polycyclic aromatic hydrocarbon analyses; and National Oceanic and Atmospheric Administration National Ocean Service staff and contractors for reviewing the experimental design and a draft of the manuscript. M.G. is a Maytag professor of ichthyology. This work was funded as a contributing study to the Deepwater Horizon/MC252 Incident Natural Resource Damage Assessment.

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 111 | No. 15
April 15, 2014
PubMed: 24706825

Classifications

Submission history

Published online: March 24, 2014
Published in issue: April 15, 2014

Keywords

  1. oil spill
  2. damage assessment
  3. heart development
  4. embryology

Acknowledgments

The authors thank Adam Miller, Morten Deichmann, and Craig Foster of Cleanseas Tuna for providing bluefin tuna and amberjack embryos, and advice on culture conditions; Erin Bubner and Bob Delaine for facilities access and logistical support at the Lincoln Marine Science Center; Tor Linbo and Robbie Schallert for assistance with bluefin tuna and amberjack embryo exposures; the Inter-American Tropical Tuna Commission members Guillermo Campeán, Richard Deriso, Daniel Margulies, Vernon Scholey, and the staff at the Achotines Laboratory for providing access to the yellowfin tuna broodstock and laboratory facilities; Bernadita Anulacion, Daryle Boyd, and Ron Pearce for assistance with polycyclic aromatic hydrocarbon analyses; and National Oceanic and Atmospheric Administration National Ocean Service staff and contractors for reviewing the experimental design and a draft of the manuscript. M.G. is a Maytag professor of ichthyology. This work was funded as a contributing study to the Deepwater Horizon/MC252 Incident Natural Resource Damage Assessment.

Notes

This article is a PNAS Direct Submission. K.A.K. is a guest editor invited by the Editorial Board.

Authors

Affiliations

John P. Incardona1 [email protected]
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Luke D. Gardner
Hopkins Marine Station, Department of Biology, Stanford University, Pacific Grove, CA 93950;
Tiffany L. Linbo
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Tanya L. Brown
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Andrew J. Esbaugh
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL 33149-1098; and
Edward M. Mager
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL 33149-1098; and
John D. Stieglitz
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL 33149-1098; and
Barbara L. French
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Jana S. Labenia
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Cathy A. Laetz
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Mark Tagal
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Catherine A. Sloan
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;
Abigail Elizur
Genecology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore DC, QLD 4558, Australia
Daniel D. Benetti
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL 33149-1098; and
Martin Grosell
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL 33149-1098; and
Barbara A. Block
Hopkins Marine Station, Department of Biology, Stanford University, Pacific Grove, CA 93950;
Nathaniel L. Scholz
Ecotoxicology Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, WA 98112;

Notes

1
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: J.P.I., L.D.G., A.J.E., M.G., and B.A.B. designed research; J.P.I., L.D.G., T.L.L., T.L.B., A.J.E., E.M.M., J.D.S., B.L.F., J.S.L., C.A.L., M.T., and C.A.S. performed research; A.E. and D.D.B. contributed new reagents/analytic tools; J.P.I. and C.A.S. analyzed data; J.P.I. and N.L.S. wrote the paper; J.P.I., D.D.B., M.G., B.A.B., and N.L.S. supervised the studies; T.L.L., E.M.M., and J.D.S. handled logistics; and B.L.F. and J.S.L. provided logistical and administrative support.

Competing Interests

The authors declare no conflict of interest.

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    Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish
    Proceedings of the National Academy of Sciences
    • Vol. 111
    • No. 15
    • pp. 5445-5754

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