Physiological Responses of Fish to Oil Spills

Literature Cited

1. Alloy M, Baxter D, Stieglitz J, Mager E, Hoenig R et al. 2016. Ultraviolet radiation enhances the toxicity of Deepwater Horizon oil to mahi-mahi (Coryphaena hippurus) embryos. Environ. Sci. Technol. 50:2011–17
   [Google Scholar]
2. Aluru N, Vijayan MM. 2006. Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinology 147:1895–903
   [Google Scholar]
3. Bagby SC, Reddy CM, Aeppli C, Fisher GB, Valentine DL 2017. Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon. . PNAS 114:E9–18
   [Google Scholar]
4. Bautista NM, Burggren WW. 2019. Parental stressor exposure simultaneously conveys both adaptive and maladaptive larval phenotypes through epigenetic inheritance in the zebrafish (Danio rerio). J. Exp. Biol. 222:jeb208918
   [Google Scholar]
5. Bayha KM, Ortell N, Ryan CN, Griffitt KJ, Krasnec M et al. 2017. Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder. PLOS ONE 12:e0176559
   [Google Scholar]
6. Bianchini A, Grosell M, Gregory SM, Wood CM 2002. Acute silver toxicity in aquatic animals is a function of sodium uptake rate. Environ. Sci. Technol. 36:1763–66
   [Google Scholar]
7. Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT 2006. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol. Sci. 92:526–36
   [Google Scholar]
8. Bradshaw JC, Kumai Y, Perry SF 2012. The effects of gill remodeling on transepithelial sodium fluxes and the distribution of presumptive sodium-transporting ionocytes in goldfish (Carassius auratus). J. Comp. Physiol. B 182:351–66
   [Google Scholar]
9. Brauner CJ, Shartau RB, Damsgaard C, Esbaugh AJ, Wilson RW, Grosell M 2019. Acid-base physiology and CO₂ homeostasis: regulation and compensation in response to elevated environmental CO₂. Carbon Dioxide M Grosell, P Munday, AP Farrell, CJ Brauner 69–132 Fish Physiol. 37 Cambridge, MA: Academic
   [Google Scholar]
10. Brette F, Machado B, Cros C, Incardona JP, Scholz NL, Block BA 2014. Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343:772–76
    [Google Scholar]
11. Brette F, Shiels HA, Galli GLJ, Cros C, Incardona JP et al. 2017. A novel cardiotoxic mechanism for a pervasive global pollutant. Sci. Rep. 7:41476
    [Google Scholar]
12. Brown DR, Bailey JM, Oliveri AN, Levin ED, Di Giulio RT 2016a. Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish. Neurotoxicol. Teratol. 53:55–63
    [Google Scholar]
13. Brown DR, Clark BW, Garner LVT, Di Giulio RT 2016b. Embryonic cardiotoxicity of weak aryl hydrocarbon receptor agonists and CYP1A inhibitor fluoranthene in the Atlantic killifish (Fundulus heteroclitus). Comp. Biochem. Physiol. C 188:45–51
    [Google Scholar]
14. Carls MG, Rice SD, Hose JE 1999. 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. Sci. Technol. 18:481–93
    [Google Scholar]
15. Carlson EA, Li Y, Zelikoff JT 2002. Exposure of Japanese medaka (Oryzias latipes) to benzo[a]pyrene suppresses immune function and host resistance against bacterial challenge. Aquat. Toxicol. 56:289–301
    [Google Scholar]
16. Carvalho PSM, Kalil DDCB, Novelli GAA, Bainy ACD, Fraga APM 2008. Effects of naphthalene and phenanthrene on visual and prey capture endpoints during early stages of the dourado Salminus brasiliensis. Mar. Environ. Res 66:205–7
    [Google Scholar]
17. Cave EJ, Kajiura SM. 2018. Effect of Deepwater Horizon crude oil water accommodated fraction on olfactory function in the Atlantic stingray. Hypanus sabinus. Sci. Rep. 8:15786
    [Google Scholar]
18. Claireaux G, Queau P, Marras S, Le Floch S, Farrell AP et al. 2018. Avoidance threshold to oil water-soluble fraction by a juvenile marine teleost fish. Environ. Toxicol. Chem. 37:854–59
    [Google Scholar]
19. Clark BW, Matson CW, Jung D, Di Giulio RT 2010. AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat. Toxicol. 99:232–40
    [Google Scholar]
20. Colavecchia MV, Hodson PV, Parrott JL 2007. The relationships among CYP1A induction, toxicity, and eye pathology in early life stages of fish exposed to oil sands. J. Toxicol. Environ. Health A 70:1542–55
    [Google Scholar]
21. Cox GK, Crossley DA, Stieglitz JD, Heuer RM, Benetti DD, Grosell M 2017. Oil exposure impairs in situ cardiac function in response to β-adrenergic stimulation in cobia (Rachycentron canadum). Environ. Sci. Technol. 51:14390–96
    [Google Scholar]
22. Cox JPL. 2008. Hydrodynamic aspects of fish olfaction. J. R. Soc. Interface 5:575–93
    [Google Scholar]
23. Dange AD. 1986. Branchial Na⁺-K⁺-ATPase inhibition in a fresh-water euryhaline teleost, tilapia (Oreochromis mossambicus), during short-term exposure to toluene or naphthalene: influence of salinity. Environ. Pollut. A 42:273–86
    [Google Scholar]
24. Deepwater Horiz. Nat. Resour. Damage Assess. Trustees 2016. Deepwater Horizon oil spill: final programmatic damage assessment and restoration plan and final programmatic environmental impact statement Rep., Natl. Oceanogr. Atmos. Adm. Silver Spring, MD: Available from http://www.gulfspillrestoration.noaa.gov/restoration-planning/gulf-plan
25. Denison MS, Nagy SR. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. 43:309–34
    [Google Scholar]
26. Di Giulio RT, Clark BW 2015. The Elizabeth River story: a case study in evolutionary toxicology. J. Toxicol. Environ. Health B 18:259–98
    [Google Scholar]
27. Di Toro DM, McGrath JA, Hansen DJ 2000. Technical basis for narcotic chemicals and polycyclic aromatic hydrocarbon criteria. I. Water and tissue. Environ. Toxicol. Chem. 19:1951–70
    [Google Scholar]
28. Dimichele L, Taylor MH. 1978. Histopathological and physiological responses of Fundulus heteroclitus to naphthalene exposure. J. Fish. Res. Board Can. 35:1060–66
    [Google Scholar]
29. Eckle P, Burgherr P, Michax E 2012. Risk of large oil spills: a statistical analysis in the aftermath of Deepwater Horizon. Environ. Sci. Technol. 46:13002–8
    [Google Scholar]
30. Edmunds RC, Gill JA, Baldwin DH, Linbo TL, French BL et al. 2015. Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi. Sci. Rep. 5:17326
    [Google Scholar]
31. Engelhardt FR, Wong MP, Duey ME 1981. Hydromineral balance and gill morphology in rainbow trout Salmo gairdneri, acclimated to fresh and sea water, as affected by petroleum exposure. Aquat. Toxicol. 1:175–86
    [Google Scholar]
32. Esbaugh AJ, Mager EM, Stieglitz JD, Hoenig R, Brown TL et al. 2016. The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages. Sci. Total Environ. 543:644–51
    [Google Scholar]
33. Folkerts EJ, Heuer RM, Flynn S, Stieglitz JD, Benetti DD et al. 2020. Exposure to hydraulic fracturing flowback water impairs mahi-mahi (Coryphaena hippurus) cardiomyocyte contractile function and swimming performance. Environ. Sci. Technol 54:13579–89
    [Google Scholar]
34. Geier MC, Chlebowski AC, Truong L, Simonich SLM, Anderson KA, Tanguay RL 2018a. Comparative developmental toxicity of a comprehensive suite of polycyclic aromatic hydrocarbons. Arch. Toxicol. 92:571–86
    [Google Scholar]
35. Geier MC, Minick DJ, Truong L, Tilton S, Pande P et al. 2018b. Systematic developmental neurotoxicity assessment of a representative PAH Superfund mixture using zebrafish. Toxicol. Appl. Pharmacol. 354:115–25
    [Google Scholar]
36. Girard C, Brodeur JC, Hontela A 1998. Responsiveness of the interrenal tissue of yellow perch (Perca flavescens) from contaminated sites to an ACTH challenge test in vivo. Can. J. Fish. Aquat. Sci. 55:438–50
    [Google Scholar]
37. Gohlke JM, Doke D, Tipre M, Leader M, Fitzgerald T 2011. A review of seafood safety after the Deepwater Horizon blowout. Environ. Health Perspect. 119:1062–69
    [Google Scholar]
38. Gorissen M, Flik G. 2016. The endocrinology of the stress response in fish. Fish Physiol 35:75–111
    [Google Scholar]
39. Greer JB, Pasparakis C, Stieglitz JD, Benetti D, Grosell M, Schlenk D 2019. Effects of Corexit 9500A and Corexit-crude oil mixtures on transcriptomic pathways and developmental toxicity in early life stage mahi-mahi (Coryphaena hippurus). Aquat. Toxicol. 212:233–40
    [Google Scholar]
40. Grosell M. 2011. The role of the gastrointestinal tract in salt and water balance. Fish Physiol 30:135–64
    [Google Scholar]
41. Grosell M, Blanchard J, Brix KV, Gerdes R 2007. Physiology is pivotal for interactions between salinity and acute copper toxicity to fish and invertebrates. Aquat. Toxicol. 84:162–72
    [Google Scholar]
42. Grosell M, De Boeck G, Johannsson O, Wood CM 1999. The effects of silver on intestinal ion and acid-base regulation in the marine teleost fish. Papophrys vetulus. Comp. Biochem. Physiol. C 124:259–70
    [Google Scholar]
43. Grosell M, Jensen FB. 2000. Uptake and effects of nitrite in the marine teleost fish Platichthys flesus. Aquat. Toxicol 50:97–107
    [Google Scholar]
44. Grosell M, McDonald MD, Walsh PJ, Wood CM 2004a. Effects of prolonged copper exposure in the marine gulf toadfish (Opsanus beta). II. Drinking rate, copper accumulation and Na⁺/K⁺-ATPase activity in osmoregulatory tissues. Aquat. Toxicol. 68:263–75
    [Google Scholar]
45. Grosell M, McDonald MD, Wood CM, Walsh PJ 2004b. Effects of prolonged copper exposure in the marine gulf toadfish (Opsanus beta). I. Hydromineral balance and plasma nitrogenous waste products. Aquat. Toxicol. 68:249–62
    [Google Scholar]
46. Grosell M, Nielsen C, Bianchini A 2002. Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp. Biochem. Physiol. C 133:287–303
    [Google Scholar]
47. Grosell M, Wood CM. 2001. Branchial versus intestinal silver toxicity and uptake in the marine teleost Parophrys vetulus. J. Comp. Physiol. B 171:585–94
    [Google Scholar]
48. Gudermann T, Bader M. 2015. Receptors, G proteins, and integration of calcium signalling. J. Mol. Med. 93:937–40
    [Google Scholar]
49. Hahn ME, Karchner SI, Shapiro MA, Perera SA 1997. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. PNAS 94:13743–48
    [Google Scholar]
50. Hamdani EH, Doving KB. 2007. The functional organization of the fish olfactory system. Prog. Neurobiol. 82:80–86
    [Google Scholar]
51. Hawkes JW. 1980. The effects of xenobiotics on fish-tissues: morphological studies. Fed. Proc. 39:3230–36
    [Google Scholar]
52. Hawkes JW, Stehr CM. 1982. Cytopathology of the brain and retina of embryonic surf smelt (Hypomesus pretiosus) exposed to crude oil. Environ. Res. 27:164–78
    [Google Scholar]
53. Heintz RA, Rice SD, Wertheimer AC, Bradshaw RF, Thrower FP et al. 2000. Delayed effects on growth and marine survival of pink salmon Oncorhynchus gorbuscha after exposure to crude oil during embryonic development. Mar. Ecol. Prog. Ser. 208:205–16
    [Google Scholar]
54. Heintz RA, Short JW, Rice SD 1999. Sensitivity of fish embryos to weathered crude oil: part II. Increased mortality of pink salmon (Oncorhynchus gorbuscha) embryos incubating downstream from weathered Exxon Valdez crude oil. Environ. Toxicol. Chem. 18:494–503
    [Google Scholar]
55. Heuer RM, Galli GLJ, Shiels HA, Fieber LA, Cox GK et al. 2019. Impacts of Deepwater Horizon crude oil on mahi-mahi (Coryphaena hippurus) heart cell function. Environ. Sci. Technol. 53:9895–904
    [Google Scholar]
56. Hicken CE, Linbo TL, Baldwin DH, Willis ML, Myers MS et al. 2011. Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. PNAS 108:7086–90
    [Google Scholar]
57. Hogan NS, Thorpe KL, van den Heuvel MR 2018. Opportunistic disease in yellow perch in response to decadal changes in the chemistry of oil sands-affected waters. Environ. Pollut. 234:769–78
    [Google Scholar]
58. Hontela A. 1998. Interrenal dysfunction in fish from contaminated sites: in vivo and in vitro assessment. Environ. Toxicol. Chem. 17:44–48
    [Google Scholar]
59. Hontela A, Rasmussen JB, Audet C, Chevalier G 1992. Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch. Environ. Contam. Toxicol. 22:278–83
    [Google Scholar]
60. Hose JE, Hannah JB, Puffer HW, Landolt ML 1984. Histologic and skeletal abnormalities in benzo(a)pyrene-treated rainbow-trout alevins. Arch. Environ. Contam. Toxicol. 13:675–84
    [Google Scholar]
61. Huang LX, Wang CG, Zhang YY, Wu MF, Zuo ZH 2013. Phenanthrene causes ocular developmental toxicity in zebrafish embryos and the possible mechanisms involved. J. Hazard. Mater. 261:172–80
    [Google Scholar]
62. Huang LX, Zuo ZH, Zhang YY, Wu MF, Lin JJ, Wang CG 2014. Use of toxicogenomics to predict the potential toxic effect of benzo(a)pyrene on zebrafish embryos: ocular developmental toxicity. Chemosphere 108:55–61
    [Google Scholar]
63. Incardona JP. 2017. Molecular mechanisms of crude oil developmental toxicity in fish. Arch. Environ. Contam. Toxicol. 73:19–32
    [Google Scholar]
64. Incardona JP, Carls MG, Day HL, Sloan CA, Bolton JL et al. 2009. Cardiac arrhythmia is the primary response of embryonic Pacific herring (Clupea pallasi) exposed to crude oil during weathering. Environ. Sci. Technol. 43:201–7
    [Google Scholar]
65. Incardona JP, Carls MG, Teraoka H, Sloan CA, Collier TK, Scholz NL 2005. Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ. Health Perspect. 113:1755–62
    [Google Scholar]
66. Incardona JP, Collier TK, Scholz NL 2004. Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 196:191–205
    [Google Scholar]
67. Incardona JP, Day HL, Collier TK, Scholz NL 2006. 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. 217:308–21
    [Google Scholar]
68. Incardona JP, Gardner LD, Linbo TL, Swarts TL, Esbaugh AJ et al. 2014. Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. PNAS 111:E1510–18
    [Google Scholar]
69. Johansen JL, Allan BJM, Rummer JL, Esbaugh AJ 2017. Oil exposure disrupts early life-history stages of coral reef fishes. Nat. Ecol. Evol. 1:1146–52
    [Google Scholar]
70. Johansen JL, Esbaugh AJ. 2017. Sustained impairment of respiratory function and swim performance following acute oil exposure in a coastal marine fish. Aquat. Toxicol. 187:82–89
    [Google Scholar]
71. Katsumiti A, Domingos FXV, Azevedo M, da Silva MD, Damian RC et al. 2009. An assessment of acute biomarker responses in the demersal catfish Cathorops spixii after the Vicuña oil spill in a harbour estuarine area in Southern Brazil. Environ. Monit. Assess. 152:209–22
    [Google Scholar]
72. Kennedy CJ, Farrell AP. 2005. Ion homeostasis and interrenal stress responses in juvenile Pacific herring, Clupea pallasi, exposed to the water-soluble fraction of crude oil. J. Exp. Mar. Biol. Ecol. 323:43–56
    [Google Scholar]
73. Khursigara AJ, Ackerly KL, Esbaugh AJ 2019. Oil toxicity and implications for environmental tolerance in fish. Comp. Biochem. Physiol. C 220:52–61
    [Google Scholar]
74. Khursigara AJ, Perrichon P, Bautista M, Burggren WW, Esbaugh A 2017. Cardiac function and survival are affected by crude oil in larval red drum. Sciaenops ocellatus. Sci. Total Environ. 579:797–804
    [Google Scholar]
75. Kirby AR, Cox GK, Nelson D, Heuer RM, Stieglitz JD et al. 2019. Acute crude oil exposure alters mitochondrial function and ADP affinity in cardiac muscle fibers of young adult mahi-mahi (Coryphaena hippurus). Comp. Biochem. Physiol. C 218:88–95
    [Google Scholar]
76. Kleindienst S, Paul JH, Joye SB 2015a. Using dispersants after oil spills: impacts on the composition and activity of microbial communities. Nat. Rev. Microbiol. 13:388–96
    [Google Scholar]
77. Kleindienst S, Seidel M, Ziervogel K, Grim S, Loftis K et al. 2015b. Chemical dispersants can suppress the activity of natural oil-degrading microorganisms. PNAS 112:14900–5
    [Google Scholar]
78. Knecht AL, Truong L, Marvel SW, Reif DM, Garcia A et al. 2017a. Transgenerational inheritance of neurobehavioral and physiological deficits from developmental exposure to benzo[a]pyrene in zebrafish. Toxicol. Appl. Pharmacol. 329:148–57
    [Google Scholar]
79. Knecht AL, Truong L, Simonich MT, Tanguay RL 2017b. Developmental benzo[a]pyrene (B[a]P) exposure impacts larval behavior and impairs adult learning in zebrafish. Neurotoxicol. Teratol. 59:27–34
    [Google Scholar]
80. Lari E, Abtahi B, Hashtroudi MS, Mohaddes E, Doving KB 2015. The effect of sublethal concentrations of the water-soluble fraction of crude oil on the chemosensory function of Caspian roach, Rutilus caspicus (YAKOVLEV, 1870). Environ. Toxicol. Chem. 34:1826–32
    [Google Scholar]
81. Lari E, Pyle GG. 2017. Rainbow trout (Oncorhynchus mykiss) detection, avoidance, and chemosensory effects of oil sands process-affected water. Environ. Pollut. 225:40–46
    [Google Scholar]
82. Lari E, Steinkey D, Razmara P, Mohaddes E, Pyle GG 2019. Oil sands process-affected water impairs the olfactory system of rainbow trout (Oncorhynchus mykiss). Ecotoxicol. Environ. Saf. 170:62–67
    [Google Scholar]
83. Larsen EH, Deaton LE, Onken H, O'Donnell M, Grosell M et al. 2014. Osmoregulation and excretion. Compr. Physiol. 4:405–573
    [Google Scholar]
84. Lattin CR, Ngai HM, Romero LM 2014. Evaluating the stress response as a bioindicator of sub-lethal effects of crude oil exposure in wild house sparrows (Passer domesticus). PLOS ONE 9:e102106
    [Google Scholar]
85. Leclair LA, MacDonald GZ, Phalen LJ, Kollner B, Hogan NS, van den Heuvel MR 2013. The immunological effects of oil sands surface waters and naphthenic acids on rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 142:185–94
    [Google Scholar]
86. Lie KK, Meier S, Sørhus E, Edvardsen RB, Karlsen O, Olsvik PA 2019. Offshore crude oil disrupts retinoid signaling and eye development in larval Atlantic haddock. Front. Mar. Sci. 6:368
    [Google Scholar]
87. Linden O. 1978. Biological effects of oil on early development of Baltic herring Clupea harengus membras. Mar. Biol 45:273–83
    [Google Scholar]
88. Loughery JR, Kidd KA, Mercer A, Martyniuk CJ 2018. Part A: temporal and dose-dependent transcriptional responses in the liver of fathead minnows following short term exposure to the polycyclic aromatic hydrocarbon phenanthrene. Aquat. Toxicol. 199:90–102
    [Google Scholar]
89. MacDonald GZ, Hogan NS, Kollner B, Thorpe KL, Phalen LJ et al. 2013. Immunotoxic effects of oil sands-derived naphthenic acids to rainbow trout. Aquat. Toxicol. 126:95–103
    [Google Scholar]
90. Mager EM, Esbaugh AJ, Stieglitz JD, Hoenig R, Bodinier C et al. 2014. Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus). Environ. Sci. Technol. 48:7053–61
    [Google Scholar]
91. Mager EM, Pasparakis C, Stieglitz JD, Hoenig R, Morris J et al. 2018. Combined effect of hypoxia or elevated temperature and Deepwater Horizon crude oil exposure on juvenile mahi-mahi swimming performance. Mar. Environ. Res. 139:129–35
    [Google Scholar]
92. Magnuson J, Bautista NM, Ludero J, Lund A, Xu EG et al. 2020. Exposure to crude oil induced retinal apoptosis and impairs visual function in fish. Environ. Sci. Technol. 54:2843–50
    [Google Scholar]
93. Magnuson J, Khursigara AJ, Allmon EB, Esbaugh AJ, Roberts AP 2018. Effects of Deepwater Horizon crude oil on ocular development in two estuarine fish species, red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus). Ecotoxicol. Environ. Saf. 166:186–91
    [Google Scholar]
94. Marty GD, Hose JE, McGurk MD, Brown ED, Hinton DE 1997. Histopathology and cytogenetic evaluation of Pacific herring larvae exposed to petroleum hydrocarbons in the laboratory or in Prince William Sound, Alaska, after the Exxon Valdez oil spill. Can. J. Fish. Aquat. Sci. 54:1846–57
    [Google Scholar]
95. Matsuo AYO, Duarte RM, Val AL 2005. Unidirectional sodium fluxes and gill CYP1A induction in an Amazonian fish (Hyphessobrycon erythrostigma) exposed to a surfactant and to crude oil. Bull. Environ. Contam. Toxicol. 75:851–58
    [Google Scholar]
96. Mauch DH, Nagler K, Schumacher S, Goritz C, Muller EC et al. 2001. CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354–57
    [Google Scholar]
97. McGrath JA, Di Toro DM 2009. Validation of the target lipid model for toxicity assessment of residual petroleum constituents: monocyclic and polycyclic aromatic hydrocarbons. Environ. Toxicol. Chem. 28:1130–48
    [Google Scholar]
98. McGrath JA, Fanelli CJ, Di Toro DM, Parkerton TF, Redman AD et al. 2018. Re-evaluation of target lipid model-derived HC5 predictions for hydrocarbons. Environ. Toxicol. Chem. 37:1579–93
    [Google Scholar]
99. McGruer V, Pasparakis C, Grosell M, Stieglitz JD, Benetti DD et al. 2019. Deepwater Horizon crude oil exposure alters cholesterol biosynthesis with implications for developmental cardiotoxicity in larval mahi-mahi (Coryphaena hippurus). Comp. Biochem. Physiol. C 220:31–35
    [Google Scholar]
100. McKeown BA, March GL. 1978. Acute effect of bunker C oil and an oil dispersant on: 1 serum glucose, serum sodium and gill morphology in both freshwater and seawater acclimated rainbow trout (Salmo gairdneri). Water Res 12:157–63
     [Google Scholar]
101. McNeill SA, Arens CJ, Hogan NS, Kollner B, van den Heuvel MR 2012. Immunological impacts of oil sands-affected waters on rainbow trout evaluated using an in situ exposure. Ecotoxicol. Environ. Saf. 84:254–61
     [Google Scholar]
102. Morrow JE, Gritz RL, Kirton MP 1975. Effects of some components of crude-oil on young coho salmon. Copeia 1975:326–31
     [Google Scholar]
103. Nelson D, Heuer RM, Cox GK, Stieglitz JD, Hoenig R et al. 2016. Effects of crude oil on in situ cardiac function in young adult mahi-mahi (Coryphaena hippurus). Aquat. Toxicol. 180:274–81
     [Google Scholar]
104. Nelson D, Stieglitz JD, Cox GK, Heuer RM, Benetti DD et al. 2017. Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: the impact of crude oil exposure. Comp. Biochem. Physiol. C 201:58–65
     [Google Scholar]
105. Paris CB, Berenshtein I, Trillo ML, Fiallettaz R, Olascoaga MJ et al. 2018. BP Gulf Science Data reveals ineffectual subsea dispersant injection for the Macondo blowout. Front. Mar. Sci. 5:389
     [Google Scholar]
106. Parkinson A. 1995. Biotransformation of xenobiotics. Casarett and Doull's Toxicology CD Klaassen 113–86 New York: McGraw-Hill
     [Google Scholar]
107. Pasparakis C, Esbaugh AJ, Burggren W, Grosell M 2019. Physiological impacts of Deepwater Horizon oil on fish. Comp. Biochem. Physiol. C 224:108558
     [Google Scholar]
108. Pasparakis C, Mager EM, Stieglitz JD, Benetti DD, Grosell M 2016. Combined effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval mahi-mahi (Coryphaena hippurus). Aquat. Toxicol. 181:113–23
     [Google Scholar]
109. Pasparakis C, Sweet LE, Stieglitz JD, Benetti D, Casente CT et al. 2017. Combined effects of oil exposure, temperature and ultraviolet radiation on buoyancy and oxygen consumption of embryonic mahi-mahi. Coryphaena hippurus. Aquat. Toxicol. 191:113–21
     [Google Scholar]
110. Perrichon P, Mager EM, Pasparakis C, Stieglitz JD, Benetti DD et al. 2018. Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi-mahi. Coryphaena hippurus. PLOS ONE 13:e0203949
     [Google Scholar]
111. Phalen LJ, Kollner B, Leclair LA, Hogan NS, van den Heuvel MR 2014. The effects of benzo[a]pyrene on leucocyte distribution and antibody response in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 147:121–28
     [Google Scholar]
112. Prendergast C, Quayle J, Burdyga T, Wray S 2010. Cholesterol depletion alters coronary artery myocyte Ca²⁺ signalling in a stimulus-specific manner. Cell Calcium 47:84–91
     [Google Scholar]
113. Reddam A, Mager EM, Grosell M, McDonald MD 2017. The impact of acute PAH exposure on the toadfish glucocorticoid stress response. Aquat. Toxicol. 192:89–96
     [Google Scholar]
114. Redmond L, Kashani AH, Ghosh A 2002. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34:999–1010
     [Google Scholar]
115. Reichert M, Blunt B, Gabruch T, Zerulla T, Ralph A et al. 2017. Sensory and behavioral responses of a model fish to oil sands process-affected water with and without treatment. Environ. Sci. Technol. 51:7128–37
     [Google Scholar]
116. Reid NM, Proestou DA, Clark BW, Warren WC, Colbourne JK et al. 2016. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354:1305–8
     [Google Scholar]
117. Reid SG, Bernier NJ, Perry SF 1998. The adrenergic stress response in fish: control of catecholamine storage and release. Comp. Biochem. Physiol. C 120:1–27
     [Google Scholar]
118. Roberts A, Alloy MM, Oris JT 2017. A review of the photo-induced toxicity of environmental contaminants. Comp. Biochem. Physiol. A 191:160–67
     [Google Scholar]
119. Rodgers ML, Takeshita R, Griffitt RJ 2018. Deepwater Horizon oil alone and in conjunction with Vibrio anguillarum exposure modulates immune response and growth in red snapper (Lutjanus campechanus). Aquat. Toxicol. 204:91–99
     [Google Scholar]
120. Rowsey LE, Johansen JL, Khursigara AJ, Esbaugh AJ 2020. Oil exposure impairs predator-prey behavior in the larval red drum (Sciaenops ocellatus). Mar. Freshw. Res. 71:99–106
     [Google Scholar]
121. Saliu J, Oluberu S, Akpoke I, Ukwa U 2017. Cortisol stress response and histopathological alteration index in Clarias gariepinus exposed to sublethal concentrations of Qua Iboe crude oil and rig wash. Afr. J. Aquat. Sci. 42:55–64
     [Google Scholar]
122. Sarasquete C, Segner H. 2000. Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Sci. Total Environ. 247:313–32
     [Google Scholar]
123. Schlenker LS, Welch MJ, Mager EM, Stieglitz JD, Benetti DD et al. 2019a. Exposure to crude oil from the Deepwater Horizon oil spill impairs oil avoidance behavior without affecting olfactory physiology in juvenile mahi-mahi (Coryphaena hippurus). Environ. Sci. Technol. 53:14001–9
     [Google Scholar]
124. Schlenker LS, Welch MJ, Meredith TL, Mager EM, Lari E et al. 2019b. Damsels in distress: oil exposure modifies behavior and olfaction in bicolor damselfish (Stegastes partitus). Environ. Sci. Technol. 53:10993–1001
     [Google Scholar]
125. Schreck CB, Tort L. 2016. The concept of stress in fish. Fish Physiol 35:1–34
     [Google Scholar]
126. Schwacke LH, Smith CR, Townsend FI, Wells RS, Hart LB et al. 2014. Health of common bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana, following the Deepwater Horizon oil spill. Environ. Sci. Technol. 48:93–103
     [Google Scholar]
127. Sheng L, Ding XX, Ferguson M, McCallister M, Rhoades R et al. 2010. Prenatal polycyclic aromatic hydrocarbon exposure leads to behavioral deficits and downregulation of receptor tyrosine kinase, MET. Toxicol. Sci. 118:625–34
     [Google Scholar]
128. Short JW, Irvine GV, Mann DH, Maselko JM, Pella JJ et al. 2007. Slightly weathered Exxon Valdez oil persists in Gulf of Alaska beach sediments after 16 years. Environ. Sci. Technol. 41:1245–50
     [Google Scholar]
129. Smith CR, Rowles TK, Hart LB, Townsend FI, Wells RS et al. 2017. Slow recovery of Barataria Bay dolphin health following the Deepwater Horizon oil spill (2013–2014), with evidence of persistent lung disease and impaired stress response. Endanger. Species Res. 33:127–42
     [Google Scholar]
130. Song JY, Nakayama K, Kokushi E, Ito K, Uno S et al. 2012. Effect of heavy oil exposure on antibacterial activity and expression of immune-related genes in Japanese flounder Paralichthys olivaceus. Environ. Toxicol. Chem 31:828–35
     [Google Scholar]
131. Sørhus E, Incardona JP, Furmanek T, Goetz GW, Scholz NL et al. 2017. Novel adverse outcome pathways revealed by chemical genetics in a developing marine fish. eLife 6:e20707
     [Google Scholar]
132. Sørhus E, Incardona JP, Karlsen O, Linbo T, Sorensen L et al. 2016. Crude oil exposures reveal roles for intracellular calcium cycling in haddock craniofacial and cardiac development. Sci. Rep. 6:31058
     [Google Scholar]
133. Souza-Bastos LR, Freire CA. 2011. Osmoregulation of the resident estuarine fish Atherinella brasiliensis was still affected by an oil spill (Vicuña tanker, Paranaguá Bay, Brazil), 7 months after the accident. Sci. Total Environ. 409:1229–34
     [Google Scholar]
134. Stieglitz JD, Mager EM, Hoenig RH, Alloy M, Esbaugh AJ et al. 2016a. A novel system for embryo-larval toxicity testing of pelagic fish: applications for impact assessment of Deepwater Horizon crude oil. Chemosphere 162:261–68
     [Google Scholar]
135. Stieglitz JD, Mager EM, Hoenig RH, Benetti DD, Grosell M 2016b. Impacts of Deepwater Horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance. Environ. Toxicol. Chem. 35:2613–22
     [Google Scholar]
136. Suzuki R, Ferris HA, Chee MJ, Maratos-Flier E, Kahn CR 2013. Reduction of the cholesterol sensor SCAP in the brains of mice causes impaired synaptic transmission and altered cognitive function. PLOS Biol 11:e1001532
     [Google Scholar]
137. Sweet LE, Magnuson J, Garner TR, Alloy MM, Stieglitz JD et al. 2017. Exposure to ultraviolet radiation late in development increases the toxicity of oil to mahi-mahi (Coryphaena hippurus) embryos. Environ. Toxicol. Chem. 36:1592–98
     [Google Scholar]
138. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB 2000. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2:42–49
     [Google Scholar]
139. Thomas RE, Rice SD. 1987. Effect of water-soluble fraction of Cook Inlet crude oil on swimming performance and plasma cortisol in juvenile coho salmon (Oncorhynchus kisutch). Comp. Biochem. Physiol. C 87:177–80
     [Google Scholar]
140. Wang YZ, Thiele C, Huttner WS 2000. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1:952–62
     [Google Scholar]
141. Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE 2000. Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit. Rev. Toxicol. 30:347–570
     [Google Scholar]
142. Wier WG, Balke CW. 1999. Ca²⁺ release mechanisms, Ca²⁺ sparks, and local control of excitation-contraction coupling in normal heart muscle. Circ. Res. 85:770–76
     [Google Scholar]
143. Wilson JM, Vijayan MM, Kennedy CJ, Iwama GK, Moon TW 1998. β-Naphthoflavone abolishes interrenal sensitivity to ACTH stimulation in rainbow trout. J. Endocrinol. 157:63–70
     [Google Scholar]
144. Xu EG, Khursigara AJ, Magnuson J, Hazard ES, Hardiman G et al. 2017a. Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: developmental and transcriptomic consequences. Environ. Sci. Technol. 51:10162–72
     [Google Scholar]
145. Xu EG, Mager EM, Grosell M, Hazard ES, Hardiman G, Schlenk D 2017b. Novel transcriptome assembly and comparative toxicity pathway analysis in mahi-mahi (Coryphaena hippurus) embryos and larvae exposed to Deepwater Horizon oil. Sci. Rep. 7:44546
     [Google Scholar]
146. Xu EG, Mager EM, Grosell M, Pasparakis C, Schlenker LS et al. 2016. Time- and oil-dependent transcriptomic and physiological responses to Deepwater Horizon oil in mahi-mahi (Coryphaena hippurus) embryos and larvae. Environ. Sci. Technol. 50:7842–51
     [Google Scholar]
147. Xu EG, Magnuson JT, Diarnante G, Mager E, Pasparakis C et al. 2018. Changes in microRNA-mRNA signatures agree with morphological, physiological, and behavioral changes in larval mahi-mahi treated with Deepwater Horizon oil. Environ. Sci. Technol. 52:13501–10
     [Google Scholar]
148. Yanase K, Herbert NA, Montgomery JC 2012. Disrupted flow sensing impairs hydrodynamic performance and increases the metabolic cost of swimming in the yellowtail kingfish, Seriola lalandi. J. Exp. Biol. 215:3944–54
     [Google Scholar]
149. Zbanyszek R, Smith LS. 1984. The effect of water-soluble aromatic hydrocarbons on some hematological parameters of rainbow trout, Salmo gairdneri Richardson, during acute exposure. J. Fish Biol. 24:545–52
     [Google Scholar]