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

John P. Incardona, Luke D. Gardner, Tiffany L. Linbo, Tanya L. Brown, Andrew J. Esbaugh, Edward M. Mager, John Stieglitz, Barbara L. French, Jana S. Labenia, Cathy A. Laetz, Mark Tagal, Catherine A. Sloan, Abigail Elizur, Daniel D Benetti, Martin Grosell, Barbara A. Block, Nathaniel L. Scholz

Research output: Contribution to journalArticle

189 Citations (Scopus)

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 dosedependent 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.

Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number15
DOIs
StatePublished - Apr 15 2014

Fingerprint

Petroleum
Polycyclic Aromatic Hydrocarbons
Tuna
Fishes
Oils
Embryonic Structures
Ecosystem
Larva
Gulf of Mexico
Water
Disasters
Oceans and Seas
Cardiac Arrhythmias
Edema
Temperature
Mortality

Keywords

  • Damage Assessment
  • Embryology
  • Heart Development
  • Oil Spill

ASJC Scopus subject areas

  • General

Cite this

Deepwater horizon crude oil impacts the developing hearts of large predatory pelagic fish. / Incardona, John P.; Gardner, Luke D.; Linbo, Tiffany L.; Brown, Tanya L.; Esbaugh, Andrew J.; Mager, Edward M.; Stieglitz, John; French, Barbara L.; Labenia, Jana S.; Laetz, Cathy A.; Tagal, Mark; Sloan, Catherine A.; Elizur, Abigail; Benetti, Daniel D; Grosell, Martin; Block, Barbara A.; Scholz, Nathaniel L.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 15, 15.04.2014.

Research output: Contribution to journalArticle

Incardona, JP, Gardner, LD, Linbo, TL, Brown, TL, Esbaugh, AJ, Mager, EM, Stieglitz, J, French, BL, Labenia, JS, Laetz, CA, Tagal, M, Sloan, CA, Elizur, A, Benetti, DD, Grosell, M, Block, BA & Scholz, NL 2014, 'Deepwater horizon crude oil impacts the developing hearts of large predatory pelagic fish', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 15. https://doi.org/10.1073/pnas.1320950111
Incardona, John P. ; Gardner, Luke D. ; Linbo, Tiffany L. ; Brown, Tanya L. ; Esbaugh, Andrew J. ; Mager, Edward M. ; Stieglitz, John ; French, Barbara L. ; Labenia, Jana S. ; Laetz, Cathy A. ; Tagal, Mark ; Sloan, Catherine A. ; Elizur, Abigail ; Benetti, Daniel D ; Grosell, Martin ; Block, Barbara A. ; Scholz, Nathaniel L. / Deepwater horizon crude oil impacts the developing hearts of large predatory pelagic fish. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 15.
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AU - Gardner, Luke D.

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AU - Esbaugh, Andrew J.

AU - Mager, Edward M.

AU - Stieglitz, John

AU - French, Barbara L.

AU - Labenia, Jana S.

AU - Laetz, Cathy A.

AU - Tagal, Mark

AU - Sloan, Catherine A.

AU - Elizur, Abigail

AU - Benetti, Daniel D

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N2 - 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 dosedependent 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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KW - Embryology

KW - Heart Development

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