Acute embryonic or juvenile exposure to deepwater horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus)

Environmental Science and Technology

Volumn 48, Issue 12, 2014, Pages 7053-7061

  Mager, Edward M ^a   Esbaugh, Andrew J ^b   Stieglitz, John D ^a   Hoenig, Ronald ^a   Bodinier, Charlotte ^a   Incardona, John P ^c   Scholz, Nathaniel L ^c   Benetti, Daniel D ^a   Grosell, Martin ^a  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c NORTHWEST FISHERIES SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCYCLIC AROMATIC HYDROCARBONS;

CARDIOTOXICITY; CORYPHAENA HIPPURUS; DEEPWATER HORIZONS; EXPOSURE CONCENTRATION; GEOMETRIC MEAN; POLYCYCLIC AROMATIC HYDROCARBONS (PAHS); SWIMMING PERFORMANCE; SWIMMING VELOCITIES;

CRUDE OIL;

PETROLEUM; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE;

CONCENTRATION (COMPOSITION); CRUDE OIL; DOLPHIN; EMBRYO; JUVENILE; POLLUTION EXPOSURE; SWIMMING BEHAVIOR;

ARTICLE; CARDIOTOXICITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORYPHAENA HIPPURUS; EMBRYO; ENVIRONMENTAL EXPOSURE; FISH; GEOMETRY; HEART OUTPUT; HEART RATE; LARVA; METABOLIC RATE; NONHUMAN; RESPIROMETRY; SWIMMING; VELOCITY; YOLK SAC;

AEROBIOSIS; ANIMALS; BASAL METABOLISM; BIOLOGICAL TRANSPORT; CHEMICAL FRACTIONATION; EMBRYO, NONMAMMALIAN; LARVA; PERCIFORMES; PETROLEUM; PETROLEUM POLLUTION; POLYCYCLIC HYDROCARBONS, AROMATIC; SWIMMING; TOXICITY TESTS, ACUTE; WATER POLLUTANTS, CHEMICAL;

EID: 84902590903     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es501628k     Document Type: Article

References (54)

1. Camilli, R.; Di Iorio, D.; Bowen, A.; Reddy, C. M.; Techet, A. H.; Yoerger, D. R.; Whitcomb, L. L.; Seewald, J. S.; Sylva, S. P.; Fenwick, J. Acoustic measurement of the Deepwater Horizon Macondo well flow rate Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (50) 20235-20239
2. Crone, T. J.; Tolstoy, M. Magnitude of the 2010 Gulf of Mexico oil leak Science 2010, 330 (6004) 634
3. McNutt, M.; Camilli, R.; Guthrie, G.; Hsieh, P.; Labson, V.; Lehr, B.; Maclay, D.; Ratzel, A.; Sogge, M. Assessment of flow rate estimates for the Deepwater Horizon/Macondo well oil spill; United States Department of the Interior: Washington, DC, 2011.
4. Block, B. A.; Teo, S. L.; Walli, A.; Boustany, A.; Stokesbury, M. J.; Farwell, C. J.; Weng, K. C.; Dewar, H.; Williams, T. D. Electronic tagging and population structure of Atlantic bluefin tuna Nature 2005, 434 (7037) 1121-1127
5. Muhling, B. A.; Roffer, M. A.; Lamkin, J. T.; Ingram, G. W., Jr.; Upton, M. A.; Gawlikowski, G.; Muller-Karger, F.; Habtes, S.; Richards, W. J. Overlap between Atlantic bluefin tuna spawning grounds and observed Deepwater Horizon surface oil in the northern Gulf of Mexico Mar. Pollut. Bull. 2012, 64 (4) 679-687
6. Gibbs, R. H.; Collette, B. B. On the identification, distribution, and biology of the dolphins, Coryphaena hippurus and C. equiselis Bull. Mar. Sci. 1959, 9, 117-152
7. Palko, B. J.; Beardsley, G. L.; Richards, W. J. Synopsis of the biological data on dolphin-fishes, Coryphaena hippurus Linnaeus and Coryphaena equiselis Linnaeus; United States Department of Commerce: Washington, DC, 1982.
8. Brown-Peterson, N.; Overstreet, R. M.; Lotz, J. M.; Franks, J. S.; Burns, K. M. Reproductive biology of cobia, Rachycentron canadum, from coastal waters of the southern United States Fish. Bull. 2001, 99, 15-28
9. Rooker, J. R.; Kitchens, L. L.; Dance, M. A.; Wells, R. J.; Falterman, B.; Cornic, M. Spatial, temporal, and habitat-related variation in abundance of pelagic fishes in the Gulf of Mexico: Potential implications of the Deepwater Horizon oil spill PLoS One 2013, 8 (10) e76080
10. Rooker, J. R.; Simms, J. R.; Wells, R. J.; Holt, S. A.; Holt, G. J.; Graves, J. E.; Furey, N. B. Distribution and habitat associations of billfish and swordfish larvae across mesoscale features in the Gulf of Mexico PLoS One 2012, 7 (4) e34180
11. Reddy, C. M.; Arey, J. S.; Seewald, J. S.; Sylva, S. P.; Lemkau, K. L.; Nelson, R. K.; Carmichael, C. A.; McIntyre, C. P.; Fenwick, J.; Ventura, G. T.; Van Mooy, B. A.; Camilli, R. Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (50) 20229-20234
12. Ryerson, T. B.; Camilli, R.; Kessler, J. D.; Kujawinski, E. B.; Reddy, C. M.; Valentine, D. L.; Atlas, E.; Blake, D. R.; de Gouw, J.; Meinardi, S.; Parrish, D. D.; Peischl, J.; Seewald, J. S.; Warneke, C. Chemical data quantify Deepwater Horizon hydrocarbon flow rate and environmental distribution Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (50) 20246-20253
13. Peterson, C. H.; Rice, S. D.; Short, J. W.; Esler, D.; Bodkin, J. L.; Ballachey, B. E.; Irons, D. B. Long-term ecosystem response to the Exxon Valdez oil spill Science 2003, 302 (5653) 2082-2086
14. Carls, M. G.; Rice, S. D.; Hose, J. E. Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval Pacific herring (Clupea pallasi) Environ. Toxicol. Chem. 1999, 18, 481-493
15. Fallahtafti, S.; Rantanen, T.; Brown, R. S.; Snieckus, V.; Hodson, P. V. Toxicity of hydroxylated alkyl-phenanthrenes to the early life stages of Japanese medaka (Oryzias latipes) Aquat. Toxicol. 2012, 106-107, 56-64
16. Hicken, C. E.; Linbo, T. L.; Baldwin, D. H.; Willis, M. L.; Myers, M. S.; Holland, L.; Larsen, M.; Stekoll, M. S.; Rice, S. D.; Collier, T. K.; Scholz, N. L.; Incardona, J. P. Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (17) 7086-7090
17. Hodson, P. V.; Qureshi, K.; Noble, C. A.; Akhtar, P.; Brown, R. S. Inhibition of CYP1A enzymes by alpha-naphthoflavone causes both synergism and antagonism of retene toxicity to rainbow trout (Oncorhynchus mykiss) Aquat. Toxicol. 2007, 81 (3) 275-285
18. Incardona, J. P.; Carls, M. G.; Day, H. L.; Sloan, C. A.; Bolton, J. L.; Collier, T. K.; Scholz, N. L. Cardiac arrhythmia is the primary response of embryonic Pacific herring (Clupea pallasi) exposed to crude oil during weathering Environ. Sci. Technol. 2009, 43 (1) 201-207
19. Incardona, J. P.; Carls, M. G.; Teraoka, H.; Sloan, C. A.; Collier, T. K.; Scholz, N. L. Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development Environ. Health Perspect. 2005, 113 (12) 1755-1762
20. Incardona, J. P.; Collier, T. K.; Scholz, N. L. Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons Toxicol. Appl. Pharmacol. 2004, 196 (2) 191-205
21. Incardona, J. P.; Day, H. L.; Collier, T. K.; Scholz, N. L. Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism Toxicol. Appl. Pharmacol. 2006, 217 (3) 308-321
22. Incardona, J. P.; Linbo, T. L.; Scholz, N. L. Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development Toxicol. Appl. Pharmacol. 2011, 257 (2) 242-249
23. Marty, G. D.; Hinton, D. E.; Short, J. W.; Heintz, R. A.; Rice, S. D.; Dambach, D. M.; Willits, N. H.; Stegeman, J. J. Ascites, premature emergence, increased gonadal cell apoptosis, and cytochrome P4501A induction in pink salmon larvae continuously exposed to oil-contaminated gravel during development Can. J. Zool. 1997, 75, 989-1007
24. Scott, J. A.; Incardona, J. P.; Pelkki, K.; Shepardson, S.; Hodson, P. V. AhR2-mediated, CYP1A-independent cardiovascular toxicity in zebrafish (Danio rerio) embryos exposed to retene Aquat. Toxicol. 2011, 101 (1) 165-174
25. Turcotte, D.; Akhtar, P.; Bowerman, M.; Kiparissis, Y.; Brown, R. S.; Hodson, P. V. Measuring the toxicity of alkyl-phenanthrenes to early life stages of medaka (Oryzias latipes) using partition-controlled delivery Environ. Toxicol. Chem. 2011, 30 (2) 487-495
26. Brette, F.; Machado, B.; Cros, C.; Incardona, J. P.; Scholz, N. L.; Block, B. A. Crude oil impairs cardiac excitation-contraction coupling in fish Science 2014, 343 (6172) 772-776
27. Incardona, J. P.; Gardner, L. D.; Linbo, T. L.; Brown, T. L.; Esbaugh, A. J.; Mager, E. M.; Stieglitz, J. D.; French, B. L.; Labenia, J. S.; Laetz, C. A.; Tagal, M.; Sloan, C. A.; Elizur, A.; Benetti, D. D.; Grosell, M.; Block, B. A.; Scholz, N. L. Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish Proc. Natl. Acad. Sci. U. S. A. 2014, 10.1073/pnas.1320950111
28. de Soysa, T. Y.; Ulrich, A.; Friedrich, T.; Pite, D.; Compton, S. L.; Ok, D.; Bernardos, R. L.; Downes, G. B.; Hsieh, S.; Stein, R.; Lagdameo, M. C.; Halvorsen, K.; Kesich, L. R.; Barresi, M. J. Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis BMC Biol. 2012, 10, 40
29. Irie, K.; Kawaguchi, M.; Mizuno, K.; Song, J. Y.; Nakayama, K.; Kitamura, S.; Murakami, Y. Effect of heavy oil on the development of the nervous system of floating and sinking teleost eggs Mar. Pollut. Bull. 2011, 63 (5-12) 297-302
30. Kawaguchi, M.; Song, J. Y.; Irie, K.; Murakami, Y.; Nakayama, K.; Kitamura, S. Disruption of Sema3A expression causes abnormal neural projection in heavy oil exposed Japanese flounder larvae Mar. Pollut. Bull. 2011, 63 (5-12) 356-361
31. Fuiman, L. A.; Rose, K. A.; Cowan, J. H.; Smith, E. P. Survival skills required for predator evasion by fish larvae and their relation to laboratory measures of performance Anim. Behav. 2006, 71, 1389-1399
32. Plaut, I. Critical swimming speed: its ecological relevance Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2001, 131 (1) 41-50
33. Stieglitz, J. D.; Benetti, D. D.; Hoenig, R. H.; Sardenberg, B.; Welch, A. W.; Miralao, S. Environmentally conditioned, year-round volitional spawning of cobia (Rachycentron canadum) in broodstock maturation systems Aquacult. Res. 2012, 43, 1557-1566
34. Benetti, D. D.; Iversen, E. S.; Ostrowski, A. C. Growth rates of captive dolphin, Coryphaena hippurus, in Hawaii Fish. Bull. 1995, 93, 152-157
35. Verdouw, H.; van Echteld, C. J. A.; Dekkers, E. M. J. Ammonia determination based on indophenol formation with sodium salicylate Water Res. 1978, 12, 399-402
36. Blazka, P.; Volf, M.; Cepela, M. A new type of respirometer for the determination of the metabolism of fish in an active state Physiol. Bohemoslov. 1960, 9, 553-558
37. Steffenson, J. F. Some errors in respirometry of aquatic breathers: how to avoid and correct for them Fish. Physiol. Biochem. 1989, 6, 49-59
38. Brett, J. R. The respiratory metabolism and swimming performance of young sockeye salmon J. Fish. Res. Board Can. 1964, 21, 1183-1226
39. Beamish, F. W. H. Swimming Capacity. In Fish Physiology; Hoar, W. S.; Randall, D. J., Eds.; Academic Press: New York, 1978; Vol. VII, pp 101-187.
40. Videler, J. J. Fish swimming; Chapman & Hall: New York, 1993.
41. Couillard, C. M. A microscale test to measure petroleum oil toxicity to mummichog embryos Environ. Toxicol. 2002, 17 (3) 195-202
42. Jung, J. H.; Hicken, C. E.; Boyd, D.; Anulacion, B. F.; Carls, M. G.; Shim, W. J.; Incardona, J. P. Geologically distinct crude oils cause a common cardiotoxicity syndrome in developing zebrafish Chemosphere 2012, 91 (8) 1146-1155
43. Pollino, C. A.; Holdway, D. A. Toxicity testing of crude oil and related compounds using early life stages of the crimson-spotted rainbowfish (Melanotaenia fluviatilis) Ecotoxicol. Environ. Saf. 2002, 52, 180-189
44. Bejarano, A. C.; Levine, E.; Mearns, A. J. Effectiveness and potential ecological effects of offshore surface dispersant use during the Deepwater Horizon oil spill: a retrospective analysis of monitoring data Environ. Monit. Assess. 2013, 185, 10281-10295
45. Diercks, A.-R.; Highsmith, R. C.; Asper, V. L.; Joung, D.; Zhou, Z.; Guo, L.; Shiller, A. M.; Joye, S. B.; Teske, A. P.; Guinasso, N.; Wade, T. L.; Lohrenz, S. E. Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site Geophys. Res. Lett. 2010, 37, L20602
46. Wade, T. L.; Sweet, S. T.; Sericano, J. L.; Guinasso, N. L.; Diercks, A.-R.; Highsmith, R. C.; Asper, V. L.; Joung, D.; Shiller, A. M.; Lohrenz, S. E.; Joye, S. B. Analyses of Water Samples From the Deepwater Horizon Oil Spill: Documentation of the Subsurface Plume; American Geophysical Union: Washington DC, 2011; Vol. 195, p 77-82.
47. Heintz, R. A. Chronic exposure to polynuclear aromatic hydrocarbons in natal habitats leads to decreased equilibrium size, growth, and stability of pink salmon populations Integr. Environ. Assess. Manage. 2007, 3 (3) 351-363
48. Heintz, R. A.; Rice, S. D.; Wertheimer, A. C.; Bradshaw, R. F.; Thrower, F. P.; Joyce, J. E.; Short, J. W. Delayed effects on growth and marine survival of pink salmon Oncorhynchus gorbuscha after exposure to crude oil during embryonic development Mar. Ecol.: Prog. Ser. 2000, 208, 205-216
49. Brett, J. R., Implications and assessments of environmental stress. In The Investigation of Fish-Power Problems; Institute of Fisheries, University of British Columbia: Vancouver, BC, 1958.
50. Farrell, A. P. Cariorespiratory performance during prolonged swimming tests with salmonids: a perspective on temperature effects and potential analytical pitfalls Philos. Trans. R. Soc., B 2007, 362, 2017-2030
51. Jastroch, M.; Divakaruni, A. S.; Mookerjee, S.; Treberg, J. R.; Brand, M. D. Mitochondrial proton and electron leaks Essays Biochem. 2010, 47, 53-67
52. Genova, M. L.; Lenaz, G. Functional role of mitochrondrial respiratory supercomplexes Biochim. Biophys. Acta 2014, 1837 (4) 427-443
53. Lee, C. G.; Farrell, A. P.; Lotto, A.; Hinch, S. G.; Healey, M. C. Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming J. Exp. Biol. 2003, 206, 3253-3260
54. Yanase, K.; Herbert, N. A.; Montgomery, J. C. Disrupted flow sensing impairs hydrodynamic performance and increases the metabolic cost of swimming in the yellowtail kingfish, Seriola lalandi J. Exp. Biol. 2012, 215, 3944-3954