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Chronic Sub-lethal Effects Observed in Wild-Caught Fishes Following Two Major Oil Spills in the Gulf of Mexico: Deepwater Horizon and Ixtoc 1

  • Erin L. PulsterEmail author
  • Adolfo Gracia
  • Susan M. Snyder
  • Kristina Deak
  • Susan Fogelson
  • Steven A. Murawski
Chapter

Abstract

During and subsequent to major oil spill events, considerable attention focuses on charismatic and economic megafauna – and especially fishes – and visual manifestations of impacts upon them. Beginning with a series of tanker accidents occurring in Europe and the USA in the 1970s–1990s, greater awareness of the potential for both acute and chronic sub-lethal impacts on fish populations has focused on exposure to polycyclic aromatic hydrocarbons (PAHs). The ambiguity of acute impacts observed during the Deepwater Horizon and Ixtoc 1 incidents has promoted considerable new research on alternative toxic endpoints that portend short- and long-term sub-lethal outcomes that influence the overall fitness of exposed populations. Laboratory-based exposure studies have traditionally focused on acute mortality-based endpoints (e.g., lethal concentrations at which 50% of the population dies = LC50) and observed at test concentrations normally exceeding environmentally relevant concentrations in real-world spills. Consequently, using laboratory-based toxicity experiments can be problematic inferring impacts on wild fish populations. In this chapter we review historical and more recent information documenting changes in abundance, recruitment, habitat use, population dynamics, trophic changes, and various physiologically based sub-lethal effects on oil-exposed fishes and especially consider research undertaken following the Deepwater Horizon and Ixtoc 1 spills in the Gulf of Mexico.

Keywords

PAHs Oil-exposed fish Sub-lethal effects Population fitness LC50 

Notes

Acknowledgments

This research was made possible by a grant from The Gulf of Mexico Research Initiative through the Center for the Integrated Modeling and Analysis of the Gulf Ecosystem (C-IMAGE I, II and III). Final data will be publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org. (doi 10.7266/N7PG1PRZ, doi 10.7266/N7T43R3T, doi 10.7266/N7GT5K56, doi 10.7266/N7G73C4N, doi:10.7266/n7-g27a-x012, doi:10.7266/n7-nmsy-tq94, doi:10.7266/n7-460y-rz32, 10.7266/n7-5zt3-8c72, 10.7266/n7-t3g7-sk92, 10.7266/n7-qjz0-bt64, 10.7266/n7-5y5c-9348).

References

  1. Able KW, López-Duarte PC, Fodrie FJ, Jensen OP, Martin CW, Roberts BJ, Valenti J, O’Connor K, Halbert SC (2015) Fish assemblages in Louisiana salt marshes: effects of the Macondo oil spill. Estuar Coasts 38:1385–1398.  https://doi.org/10.1007/s12237-014-9890-6CrossRefGoogle Scholar
  2. Alkindi AYA, Brown JA, Waring CP, Collins JE (1996) Endocrine, osmoregulatory, respiratory and haematological parameters in flounder exposed to the water soluble fraction of crude oil. J Fish Biol 49:1291–1305CrossRefGoogle Scholar
  3. Ameur WB, El Megdiche Y, de Lapuente J, Barhoumi B, Trabelsi S, Ennaceur S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Touil S, Driss MR, Borràs M (2015) Oxidative stress, genotoxicity and histopathology biomarker responses in Mugil cephalus and Dicentrarchus labrax gill exposed to persistent pollutants. A field study in the Bizerte Lagoon: Tunisia. Chemosphere 135:67–74.  https://doi.org/10.1016/j.chemosphere.2015.02.050CrossRefGoogle Scholar
  4. Amezcua-Linares F, Amezcua F, Gil-Manrique B (2015) Effects of the Ixtoc I oil spill on fish assemblages in the Southern Gulf of Mexico. In: Alford JB, Peterson MS, Green CC (eds) Impacts of oil spill disasters on marine habitats and fisheries in North America. CRC Press, Boca Raton, pp 209–236Google Scholar
  5. Anonymous (1980) Informe de los trabajos realizados para el control del pozo IXTOC I, el combate, derrame de petróleo y determinación de sus efectos sobre el ambiente marino. Programa Coordinado de Estudios Ecológicos de la Sonda de Campeche. Instituto Mexicano del Petróleo, México, D.F.Google Scholar
  6. Arvedlund M, Kavanagh K (2009) The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer Netherlands, Dordrecht, pp 135–184.  https://doi.org/10.1007/978-90-481-2406-0_5CrossRefGoogle Scholar
  7. Arvedlund M, Takemura A (2006) The importance of chemical environmental cues for juvenile Lethrinus nebulosus Forsskål (Lethrinidae, Teleostei) when settling into their first benthic habitat. J Exp Mar Biol Ecol 338:112–122.  https://doi.org/10.1016/j.jembe.2006.07.001CrossRefGoogle Scholar
  8. Balfry SK, Iwama GK (2004) Observations on the inherent variability of measuring lysozyme activity in coho salmon (Oncorhynchus kisutch). Comp Biochem Physiol B: Biochem Mol Biol 138:207–211.  https://doi.org/10.1016/j.cbpc.2003.12.010CrossRefGoogle Scholar
  9. Barron MG (2012) Ecological impacts of the Deepwater Horizon oil spill: implications for immunotoxicity. Toxicol Pathol 40:315–320.  https://doi.org/10.1177/0192623311428474CrossRefGoogle Scholar
  10. Bayha KM, Ortell N, Ryan CN, Griffitt KJ, Krasnec M, Sena J, Ramaraj T, Takeshita R, Mayer GD, Schilkey F, Griffitt RJ (2017) Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder. PLoS One 12:e0176559.  https://doi.org/10.1371/journal.pone.0176559CrossRefGoogle Scholar
  11. Benedetti M, Giuliani ME, Regoli F (2015) Oxidative metabolism of chemical pollutants in marine organisms: molecular and biochemical biomarkers in environmental toxicology. Ann NY Acad Sci 1340:8–19.  https://doi.org/10.1111/nyas.12698CrossRefGoogle Scholar
  12. Bentivegna CS, Cooper KR, Olson G, Pena EA, Millemann DR, Portier RJ (2015) Chemical and histological comparisons between Brevoortia sp. (menhaden) collected in fall 2010 from Barataria Bay, LA and Delaware Bay, NJ following the Deepwater Horizon (DWH) oil spill. Mar Environ Res 112(Part A):21–34.  https://doi.org/10.1016/j.marenvres.2015.08.011CrossRefGoogle Scholar
  13. Beyer J, Trannum HC, Bakke T, Hodson PV, Collier TK (2016) Environmental effects of the Deepwater Horizon oil spill: a review. Mar Pollut Bull 110:28–51.  https://doi.org/10.1016/j.marpolbul.2016.06.027CrossRefGoogle Scholar
  14. Brewton RA, Fulford R, Griffitt RJ (2013) Gene expression and growth as indicators of effects of the BP Deepwater Horizon oil spill on spotted seatrout (Cynoscion nebulosus). J Toxic Environ Health A 76:1198–1209.  https://doi.org/10.1080/15287394.2013.848394CrossRefGoogle Scholar
  15. Brian JV, Harris CA, Scholze M, Kortenkamp A, Booy P, Lamoree M, Pojana G, Jonkers N, Marcomini A, Sumpter JP (2007) Evidence of estrogenic mixture effects on the reproductive performance of fish. Environ Sci Technol 41:337–344.  https://doi.org/10.1021/es0617439CrossRefGoogle Scholar
  16. Brown-Peterson NJ, Brewton RA, Griffitt RJ, Fulford RS (2015a) Impacts of the Deepwater Horizon oil spill on the reproductive biology of spotted seatrout (Cynoscion nebulosus). In: Alford JB, Peterson MS, Green CC (eds) Impacts of oil spill disasters on marine habitats and fisheries in North America, CRC marine biology series. CRC Press, Boca Raton, pp 237–252Google Scholar
  17. Brown-Peterson NJ, Krasnec M, Takeshita R, Ryan CN, Griffitt KJ, Lay C, Mayer GD, Bayha KM, Hawkins WE, Lipton I, Morris J, Griffitt RJ (2015b) A multiple endpoint analysis of the effects of chronic exposure to sediment contaminated with Deepwater Horizon oil on juvenile southern flounder and their associated microbiomes. Aquat Toxicol 165:197–209.  https://doi.org/10.1016/j.aquatox.2015.06.001CrossRefGoogle Scholar
  18. Brown-Peterson NJ, Krasnec MO, Lay CR, Morris JM, Griffitt RJ (2017) Responses of juvenile southern flounder exposed to Deepwater Horizon oil-contaminated sediments. Environ Toxicol Chem 36:1067–1076.  https://doi.org/10.1002/etc.3629CrossRefGoogle Scholar
  19. Carr DL, Smith EE, Thiyagarajah A, Cromie M, Crumly C, Davis A, Dong MJ, Garcia C, Heintzman L, Hopper T, Kouth K, Morris K, Ruehlen A, Snodgrass P, Vaughn K, Carr JA (2018) Assessment of gonadal and thyroid histology in Gulf killifish (Fundulus grandis) from Barataria Bay Louisiana one year after the Deepwater Horizon oil spill. Ecotoxicol Environ Saf 154:245–254.  https://doi.org/10.1016/j.ecoenv.2018.01.013CrossRefGoogle Scholar
  20. Chancellor E (2015) Vulnerability of larval fish populations to oil well blowouts in the Northern Gulf of Mexico. M.S. Thesis, College of Marine Science, University of South Florida, Scholar CommonsGoogle Scholar
  21. Chancellor E, Murawski SA, Paris CB, Perruso L, Perlin N (2020) Comparative environmental sensitivity of offshore Gulf of Mexico waters potentially impacted by ultra-deep oil well blowouts. In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Scenarios and responses to future deep oil spills – fighting the next war. Springer, ChamGoogle Scholar
  22. Claireaux G, Queau P, Marras S, Le Floch S, Farrell AP, Nicolas-Kopec A, Lemaire P, Domenici P (2018) Avoidance threshold to oil water-soluble fraction by a juvenile marine teleost fish. Environ Toxicol Chem 37:854–859.  https://doi.org/10.1002/etc.4019CrossRefGoogle Scholar
  23. Dahl KA, Patterson WF, Snyder RA (2016) Experimental assessment of lionfish removals to mitigate reef fish community shifts on northern Gulf of Mexico artificial reefs. Mar Ecol Prog Ser 558:207–221.  https://doi.org/10.3354/meps11898CrossRefGoogle Scholar
  24. Dauble DD, Gray RH, Skalski JR, Lusty EW, Simmons MA (1985) Avoidance of a water-soluble fraction of coal liquid by fathead minnows. Trans Am Fish Soc 114:754–760.  https://doi.org/10.1577/1548-8659(1985)114<754:aoawfo>2.0.co;2CrossRefGoogle Scholar
  25. de Guise S, Levin M, Gebhard E, Jasperse L, Hart LB, Smith CR, Venn-Watson S, Townsend F, Wells R, Balmer B, Zolman E, Rowles T, Schwacke L (2017) Changes in immune functions in bottlenose dolphins in the northern Gulf of Mexico associated with the Deepwater Horizon oil spill. Endanger Species Res 33:290–303.  https://doi.org/10.3354/esr00814CrossRefGoogle Scholar
  26. Deak K, Dishaw L, Murawski S (in prep) Establishment of baseline reference intervals for golden tilefish and red snapper caught throughout the Gulf of MexicoGoogle Scholar
  27. Deak K, Dishaw L, Murawski SA (2017) Gauging Gulf-wide golden tilefish health: how do demersal denizens of De Soto Canyon compare to their Cuban, Mexican, and US neighbors? Presentation at: American Fisheries Society, Tampa, Florida, 2017Google Scholar
  28. Deak K, Dishaw L, Murawski SA (2018) Tracking oil’s toxicological transgressions through tilefish transcriptomics. Presentation at: Gulf of Mexico oil spill and ecosystem science conference, New Orleans, Louisiana, 2018Google Scholar
  29. DeLaune RD, Patrick WH Jr, Buresh RJ (1979) Effect of crude oil on a Louisiana Spartina alterniflora salt marsh. Environ Pollut (1970) 20:21–31.  https://doi.org/10.1016/0013-9327(79)90050-8CrossRefGoogle Scholar
  30. Díaz-Gil C, Cotgrove L, Smee SL, Simón-Otegui D, Hinz H, Grau A, Palmer M, Catalán IA (2017) Anthropogenic chemical cues can alter the swimming behaviour of juvenile stages of a temperate fish. Mar Environ Res 125:34–41.  https://doi.org/10.1016/j.marenvres.2016.11.009CrossRefGoogle Scholar
  31. Dincer Kırman Z, Sericano JL, Wade TL, Bianchi TS, Marcantonio F, Kolker AS (2016) Composition and depth distribution of hydrocarbons in Barataria Bay marsh sediments after the Deepwater Horizon oil spill. Environ Pollut 214:101–113.  https://doi.org/10.1016/j.envpol.2016.03.071CrossRefGoogle Scholar
  32. Dubansky B, Whitehead A, Miller JT, Rice CD, Galvez F (2013) Multitissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident Gulf killifish (Fundulus grandis). Environ Sci Technol 47:5074–5082.  https://doi.org/10.1021/es400458pCrossRefGoogle Scholar
  33. Dubansky B, Rice CD, Barrois LF, Galvez F (2017) Biomarkers of aryl-hydrocarbon receptor activity in Gulf killifish (Fundulus grandis) from northern Gulf of Mexico marshes following the Deepwater Horizon oil spill. Arch Environ Contam Toxicol 73:63–75.  https://doi.org/10.1007/s00244-017-0417-6CrossRefGoogle Scholar
  34. Esbaugh AJ, Mager EM, Stieglitz JD, Hoenig R, Brown TL, French BL, Linbo TL, Lay C, Forth H, Scholz NL, Incardona JP, Morris JM, Benetti DD, Grosell M (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(Part A):644–651.  https://doi.org/10.1016/j.scitotenv.2015.11.068CrossRefGoogle Scholar
  35. Fodrie FJ, Heck KL Jr (2011) Response of coastal fishes to the Gulf of Mexico oil disaster. PLoS One 6(7):1–8.  https://doi.org/10.1371/journal.pone.0021609CrossRefGoogle Scholar
  36. Fonseca VF, França S, Vasconcelos RP, Serafim A, Company R, Lopes B, Bebianno MJ, Cabral HN (2011) Short-term variability of multiple biomarker response in fish from estuaries: influence of environmental dynamics. Mar Environ Res 72:172–178.  https://doi.org/10.1016/j.marenvres.2011.08.001CrossRefGoogle Scholar
  37. Friedrichs KR, Harr KE, Freeman KP, Szladovits B, Walton RM, Barnhart KF, Blanco-Chavez J (2012) ASVCP reference interval guidelines: determination of de novo reference intervals in veterinary species and other related topics. Vet Clin Pathol 41:441–453.  https://doi.org/10.1111/vcp.12006CrossRefGoogle Scholar
  38. Geffré A, Friedrichs K, Harr K, Concordet D, Trumel C, Braun J-P (2009) Reference values: a review. Veterinary Clinical Pathology 38:288–298.  https://doi.org/10.1111/j.1939-165X.2009.00179.xCrossRefGoogle Scholar
  39. Gouraguine A, Díaz-Gil C, Reñones O, Otegui DS, Palmer M, Hinz H, Catalán IA, Smith DJ, Moranta J (2017) Behavioural response to detection of chemical stimuli of predation, feeding and schooling in a temperate juvenile fish. J Exp Mar Biol Ecol 486:140–147.  https://doi.org/10.1016/j.jembe.2016.10.003CrossRefGoogle Scholar
  40. Gracia A, Murawski SA, Alexander-Valdés HM, Snyder S, López-Durán IM, Pulster EL, Ortega-Tenorio P, Frausto-Castillo A (2017) Impact of PAH at fish sub-individual level and resiliency consequences. Presentation at: Gulf of Mexico oil spill & ecosystem science, New Orleans, LA, 2017Google Scholar
  41. Gracia A, Murawski SA, Alexander-Valdés RM, Vázquez-Bader AR, Snyder S, LópezDurán IM, Ortega-Tenorio P, Pulster EL, Frausto-Castillo JA (2018) Fish stock resiliency to environmental PAH. Presentation at: Gulf of Mexico oil spill & ecosystem science conference, New Orleans, LA, February 6–9, 2018Google Scholar
  42. Gracia A, Murawski SA, Vázquez-Bader AR (2020) Impacts of deep spills on fish and fisheries (Chap. 25). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Deep oil spills – facts, fate and effects. Springer, ChamGoogle Scholar
  43. Graham WM, Condon RH, Carmichael RH, D’Ambra I, Patterson HK, Linn LJ, Hernandez FJ (2010) Oil carbon entered the coastal planktonic food web during the Deepwater Horizon oil spill. Environ Res Lett 5.  https://doi.org/10.1088/1748-9326/5/4/045301CrossRefGoogle Scholar
  44. Grosell M, Griffit RJ, Sherwood TA, Wetzel DL (2020) Digging deeper than LC/EC50: non-traditional endpoints and non-model species in oil spill toxicology (Chap. 29). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Deep oil spills – facts, fate and effects. Springer, ChamGoogle Scholar
  45. Guzmán del Próo SA, Chávez EA, Alatriste FM, de la Campa S, De la Cruz G, Gómez L, Guadarrama R, Guerra A, Mille S, Torruco D (1986) The impact of the Ixtoc-1 oil spill on zooplankton. J Plankton Res 8:557–581.  https://doi.org/10.1093/plankt/8.3.557CrossRefGoogle Scholar
  46. Hadfield MG, Paul VJ (2011) Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae. In: McClintock JB (ed) Marine chemical ecology. CRC Press, Boca RatonGoogle Scholar
  47. Hall RA, Zook EG, Meaburn GM (1978) National Marine Fisheries Service survey of trace elements in the fishery resource. NOAA, Washington, DCGoogle Scholar
  48. Hara TJ, Thompson BE (1978) The reaction of whitefish, Coregonus clupeaformis, to the anionic detergent sodium lauryl sulphate and its effects on their olfactory responses. Water Res 12:893–897.  https://doi.org/10.1016/0043-1354(78)90042-8CrossRefGoogle Scholar
  49. Harr KE, Deak K, Murawski SA, Reavill DR, Takeshita RA (2018) Generation of red drum (Sciaenops ocellatus) hematology reference intervals with a focus on identified outliers. Vet Clin Pathol 47:22–28.  https://doi.org/10.1111/vcp.12569CrossRefGoogle Scholar
  50. Harris EK, Boyd JC (1990) On dividing reference data into subgroups to produce separate reference ranges. Clin Chem 36:265–270Google Scholar
  51. Harwell MA, Gentile JH (2006) Ecological significance of residual exposures and effects from the Exxon Valdez oil spill. Integr Environ Assess Manag 2:204–246.  https://doi.org/10.1002/ieam.5630020303CrossRefGoogle Scholar
  52. Havel LN, Fuiman LA (2016) Settlement-size larval red drum (Sciaenops ocellatus) respond to estuarine chemical cues. Estuar Coasts 39:560–570.  https://doi.org/10.1007/s12237-015-0008-6CrossRefGoogle Scholar
  53. Hedgpeth BM, Griffitt RJ (2016) Simultaneous exposure to chronic hypoxia and dissolved polycyclic aromatic hydrocarbons results in reduced egg production and larval survival in the sheepshead minnow (Cyprinodon variegatus). Environ Toxicol Chem 35:645–651.  https://doi.org/10.1002/etc.3207CrossRefGoogle Scholar
  54. Herdter ES, Chambers DP, Stallings CD, Murawski SA (2017) Did the Deepwater Horizon oil spill affect growth of red snapper in the Gulf of Mexico? Fish Res 191:60–68.  https://doi.org/10.1016/j.fishres.2017.03.005CrossRefGoogle Scholar
  55. Hernandez FJ Jr, Filbrun JE, Fang J, Ransom JT (2016) Condition of larval red snapper (Lutjanus campechanus) relative to environmental variability and the Deepwater Horizon oil spill. Environ Res Lett 11:094019CrossRefGoogle Scholar
  56. Hester MW, Mendelssohn IA (2000) Long-term recovery of a Louisiana brackish marsh plant community from oil-spill impact: vegetation response and mitigating effects of marsh surface elevation. Mar Environ Res 49:233–254.  https://doi.org/10.1016/S0141-1136(99)00071-9CrossRefGoogle Scholar
  57. Hidaka H, Tatsukawa R (1989) Avoidance by olfaction in a fish, medaka (Oryzias latipes), to aquatic contaminants. Environ Pollut 56:299–309.  https://doi.org/10.1016/0269-7491(89)90075-4CrossRefGoogle Scholar
  58. Incardona JP, Gardner LD, Linbo TL, Brown TL, Esbaugh AJ, Mager EM, Stieglitz JD, 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. Proc Natl Acad Sci USA 111:E1510–E1518.  https://doi.org/10.1073/pnas.1320950111CrossRefGoogle Scholar
  59. Ishida Y, Kobayashi H (1995) Avoidance behavior of carp to pesticides and decrease of the avoidance threshold by addition of sodium lauryl sulfate. Fish Sci 61:441–446.  https://doi.org/10.2331/fishsci.61.441CrossRefGoogle Scholar
  60. James MO, Kleinow KM (1994) Trophic transfer of chemicals in the aquatic environment. In: Malins DC, Ostrander GK (eds) Aquatic toxicology. Molecular, biochemical and cellular perspectives. Lewis Publishers, Boca Raton, pp 1–36Google Scholar
  61. Javed M, Ahmad MI, Usmani N, Ahmad M (2017) Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water. Sci Rep 7:1675.  https://doi.org/10.1038/s41598-017-01749-6CrossRefGoogle Scholar
  62. Kendall AW Jr, Ahlstrom EH, Moser HG (1983) Early life history stages of fishes and their characters. In: Ontogeny and systematics of fishes. Library of Congress, La JollaGoogle Scholar
  63. Kerambrun E, Sanchez W, Henry F, Amara R (2011) Are biochemical biomarker responses related to physiological performance of juvenile sea bass (Dicentrarchus labrax) and turbot (Scophthalmus maximus) caged in a polluted harbour? Comp Biochem Physiol Part C: Toxicol Pharmacol 154:187–195.  https://doi.org/10.1016/j.cbpc.2011.05.006CrossRefGoogle Scholar
  64. Kerambrun E, Henry F, Courcot L, Gevaert F, Amara R (2012) Biological responses of caged juvenile sea bass (Dicentrarchus labrax) and turbot (Scophthalmus maximus) in a polluted harbour. Ecol Indic 19:161–171.  https://doi.org/10.1016/j.ecolind.2011.06.035CrossRefGoogle Scholar
  65. Khan RA (2003) Health of flatfish from localities in Placentia Bay, Newfoundland, contaminated with petroleum and PCBs. Arch Environ Contam Toxicol 44:485–492.  https://doi.org/10.1007/s00244-002-2063-9CrossRefGoogle Scholar
  66. Kim HN, Park CI, Chae YS, Shim WJ, Kim M, Addison RF, Jung JH (2013) Acute toxic responses of the rockfish (Sebastes schlegelii) to Iranian heavy crude oil: feeding disrupts the biotransformation and innate immune systems. Fish Shellfish Immunol 35:357–365.  https://doi.org/10.1016/j.fsi.2013.04.041CrossRefGoogle Scholar
  67. Klinger DH, Dale JJ, Machado BE, Incardona JP, Farwell CJ, Block BA (2015) Exposure to Deepwater Horizon weathered crude oil increases routine metabolic demand in chub mackerel, Scomber japonicus. Mar Pollut Bull 98:259–266.  https://doi.org/10.1016/j.marpolbul.2015.06.039CrossRefGoogle Scholar
  68. Kwan CK, Sanford E, Long J (2015) Copper pollution increases the relative importance of predation risk in an aquatic food web. PLoS One 10:e0133329.  https://doi.org/10.1371/journal.pone.0133329CrossRefGoogle Scholar
  69. 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.  https://doi.org/10.1016/j.envpol.2017.03.041CrossRefGoogle Scholar
  70. Lecchini D, Dixson DL, Lecellier G, Roux N, Frédérich B, Besson M, Tanaka Y, Banaigs B, Nakamura Y (2017) Habitat selection by marine larvae in changing chemical environments. Mar Pollut Bull 114:210–217.  https://doi.org/10.1016/j.marpolbul.2016.08.083CrossRefGoogle Scholar
  71. Lee EH, Kim M, Moon YS, Yim UH, Ha SY, Jeong CB, Lee JS, Jung JH (2018) Adverse effects and immune dysfunction in response to oral administration of weathered Iranian heavy crude oil in the rockfish Sebastes schlegelii. Aquat Toxicol 200:127–135.  https://doi.org/10.1016/j.aquatox.2018.04.010CrossRefGoogle Scholar
  72. Martin CW (2017) Avoidance of oil contaminated sediments by estuarine fishes. Mar Ecol Prog Ser 576:125–134.  https://doi.org/10.3354/meps12084CrossRefGoogle Scholar
  73. Maynard DJ, Weber DD (1981) Avoidance reactions of juvenile coho salmon (Oncorhynchus kisutch) to monocyclic aromatics. Can J Fish Aquat Sci 38:772–778.  https://doi.org/10.1139/f81-105CrossRefGoogle Scholar
  74. Murawski SA, Hogarth WT, Peebles EB, Barbeiri L (2014) Prevalence of external skin lesions and polycyclic aromatic hydrocarbon concentrations in Gulf of Mexico fishes, Post-Deepwater Horizon. Trans Am Fish Soc 143:1084–1097.  https://doi.org/10.1080/00028487.2014.911205CrossRefGoogle Scholar
  75. Murawski SA, Fleeger JW, Patterson WF, Hu C, Daly K, Romero I, Toro-Farmer GA (2016) How did the Deepwater Horizon oil spill affect coastal and continental shelf ecosystems of the Gulf of Mexico? Oceanography 29:160–173CrossRefGoogle Scholar
  76. Murawski SA, Patterson W II, Campbell M (2018a) Has abundance of continental shelf fish species declined after Deepwater Horizon? Presentation at: Gulf of Mexico Oil Spill & Ecosystem Science Conference, New Orleans, LA, 2018Google Scholar
  77. Murawski SA, Peebles EB, Gracia A, Tunnell JW Jr, Armenteros M (2018b) Comparative abundance, species composition, and demographics of continental shelf fish assemblages throughout the Gulf of Mexico. Mar Coast Fish: Dyn Manag Ecosys Sci 10:325–346CrossRefGoogle Scholar
  78. Naour S, Espinoza BM, Aedo JE, Zuloaga R, Maldonado J, Bastias-Molina M, Silva H, Meneses C, Gallardo-Escarate C, Molina A, Valdes JA (2017) Transcriptomic analysis of the hepatic response to stress in the red cusk-eel (Genypterus chilensis): insights into lipid metabolism, oxidative stress and liver steatosis. Plos One 12.  https://doi.org/10.1371/journal.pone.0176447CrossRefGoogle Scholar
  79. National Research Council (NRC) (2003) Oil in the sea III: inputs, fates, and effects. The National Academies Press, Washington, DC.  https://doi.org/10.17226/10388CrossRefGoogle Scholar
  80. Nixon Z, Zengel S, Baker M, Steinhoff M, Fricano G, Rouhani S, Michel J (2016) Shoreline oiling from the Deepwater Horizon oil spill. Mar Pollut Bull 107:170–178.  https://doi.org/10.1016/j.marpolbul.2016.04.003CrossRefGoogle Scholar
  81. Olson GM, Meyer BM, Portier RJ (2016) Assessment of the toxic potential of polycyclic aromatic hydrocarbons (PAHs) affecting Gulf menhaden (Brevoortia patronus) harvested from waters impacted by the BP Deepwater Horizon Spill. Chemosphere 145:322–328.  https://doi.org/10.1016/j.chemosphere.2015.11.087CrossRefGoogle Scholar
  82. Paris CB, Atema J, Irisson J-O, Kingsford M, Gerlach G, Guigand CM (2013) Reef odor: a wake up call for navigation in reef fish larvae. PLoS One 8:e72808.  https://doi.org/10.1371/journal.pone.0072808CrossRefGoogle Scholar
  83. Patterson WF III, Chanton JP, Barnett B, Joseph H, Tarnecki JH (2020) The utility of stable and radio isotopes in fish tissues as biogeochemical tracers of marine oil spill food web effects. In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Scenarios and responses to future deep oil spills – fighting the next war. Springer, ChamGoogle Scholar
  84. Peterson CH, Rice SD, Short JW, Esler D, Bodkin JL, Ballachey BE, Irons DB (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302(5653):2082–2086.  https://doi.org/10.1126/science.1084282CrossRefGoogle Scholar
  85. Portnoy DA, Fields AT, Greer JB, Schlenk D (2020) Genetics and oil: transcriptomics, epigenetics and population genomics as tools to understand animal responses to exposure across different time scales (Chap. 30). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Deep oil spills – facts, fate and effects. Springer, ChamGoogle Scholar
  86. Pulster EL, Fogelson SB, Carr B, Murawski SA (2018) A spatiotemporal analysis of hepatic polycyclic aromatic hydrocarbon levels and pathological findings in red snapper (Lutjanus campechanus), post-Deepwater Horizon. Presentation at: Gulf of Mexico oil spill & ecosystem science conference, New Orleans, LA, 2018Google Scholar
  87. Quintana-Rizzo E, Torres JJ, Ross SW, Romero I, Watson K, Goddard E, Hollander D (2015) Delta C-13 and delta N-15 in deep-living fishes and shrimps after the Deepwater Horizon oil spill, Gulf of Mexico. Mar Pollut Bull 94:241–250.  https://doi.org/10.1016/j.marpolbul.2015.02.002CrossRefGoogle Scholar
  88. Ransom JT, Filbrun JE, Hernandez FJ Jr (2016) Condition of larval Spanish mackerel Scomberomorus maculatus in relation to the Deepwater Horizon oil spill. Mar Ecol Prog Ser 558:143–152.  https://doi.org/10.3354/meps11880CrossRefGoogle Scholar
  89. Rehberger K, Werner I, Hitzfeld B, Segner H, Baumann L (2017) 20 years of fish immunotoxicology – what we know and where we are. Crit Rev Toxicol 47:516–542.  https://doi.org/10.1080/10408444.2017.1288024CrossRefGoogle Scholar
  90. Reichert M, Blunt B, Gabruch T, Zerulla T, Ralph A, El-Din MG, Sutherland BR, Tierney KB (2017) Sensory and behavioral responses of a model fish to oil sands process-affected water with and without treatment. Environ Sci Technol 51:7128–7137.  https://doi.org/10.1021/acs.est.7b01650CrossRefGoogle Scholar
  91. Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77:229–238.  https://doi.org/10.1016/j.aquatox.2005.10.018CrossRefGoogle Scholar
  92. Rooker JR, Kitchens LL, Dance MA, Wells RJD, Falterman B, Cornic M (2013) 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 8:e76080.  https://doi.org/10.1371/journal.pone.0076080CrossRefGoogle Scholar
  93. Santana MS, Sandrini-Neto L, Filipak Neto F, Oliveira Ribeiro CA, Di Domenico M, Prodocimo MM (2018) Biomarker responses in fish exposed to polycyclic aromatic hydrocarbons (PAHs): systematic review and meta-analysis. Environ Pollut 242:449–461.  https://doi.org/10.1016/j.envpol.2018.07.004CrossRefGoogle Scholar
  94. Schwacke LH, Smith CR, Townsend FI, Wells RS, Hart LB, Balmer BC, Collier TK, De Guise S, Fry MM, Guillette LJ, Lamb SV, Lane SM, McFee WE, Place NJ, Tumlin MC, Ylitalo GM, Zolman ES, Rowles TK (2014) Health of common bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana, following the Deepwater Horizon oil spill. Environ Sci Technol 48:93–103.  https://doi.org/10.1021/es403610fCrossRefGoogle Scholar
  95. Schwaiger J, Wanke R, Adam S, Pawert M, Honnen W, Triebskorn R (1997) The use of histopathological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recover 6:75–86.  https://doi.org/10.1023/a:1008212000208CrossRefGoogle Scholar
  96. Snieszko SF (1974) The effects of environmental stress on outbreaks of infectious diseases of fishes. J Fish Biol 6:197–208.  https://doi.org/10.1111/j.1095-8649.1974.tb04537.xCrossRefGoogle Scholar
  97. Snyder SM, Pulster EL, Wetzel DL, Murawski SA (2015) PAH exposure in Gulf of Mexico demersal fishes, Post-Deepwater Horizon. Environ Sci Technol 49:8786–8795.  https://doi.org/10.1021/acs.est.5b01870CrossRefGoogle Scholar
  98. Snyder SM, Pulster EL, Fogelson SB, Murawski SA (2019) Hepatic accumulation of PAHs and prevalence of hepatic lesions in golden tilefish from the northern Gulf of Mexico. Presentation at: Gulf of Mexico Oil Spill & Ecosystem Science Conference, New Orleans, LA, 2018Google Scholar
  99. Sun S, Hu C, Tunnell JW Jr (2015) Surface oil footprint and trajectory of the Ixtoc-I oil spill determined from Landsat/MSS and CZCS observations. Mar Pollut Bull 101:632–641.  https://doi.org/10.1016/j.marpolbul.2015.10.036CrossRefGoogle Scholar
  100. Tarnecki JH, Patterson WF (2015) Changes in red snapper diet and trophic ecology following the Deepwater Horizon oil spill. Mar Coast Fish 7:135–147.  https://doi.org/10.1080/19425120.2015.1020402CrossRefGoogle Scholar
  101. Teh SJ, Adams SM, Hinton DE (1997) Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat Toxicol 37:51–70.  https://doi.org/10.1016/S0166-445X(96)00808-9CrossRefGoogle Scholar
  102. Tierney KB, Baldwin DH, Hara TJ, Ross PS, Scholz NL, Kennedy CJ (2010) Olfactory toxicity in fishes. Aquat Toxicol 96:2–26.  https://doi.org/10.1016/j.aquatox.2009.09.019CrossRefGoogle Scholar
  103. Tunnell JW Jr (2016) Ixtoc I vs Deepwater Horizon: a different day, a different time, but with similarities. Presentation at: Gulf of Mexico Oil Spill and Ecosystem Science, New Orleans, Louisiana, 2016Google Scholar
  104. Walton RM (2001) Establishing reference intervals: health as a relative concept. Semin Avian Exotic Pet Med 10:66–71.  https://doi.org/10.1053/S1055-937X(01)80026-8CrossRefGoogle Scholar
  105. Wang TH, Secombes CJ (2013) The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 35(6):1703–1718.  https://doi.org/10.1016/j.fsi.2013.08.030CrossRefGoogle Scholar
  106. White ND, Godard-Codding C, Webb SJ, Bossart GD, Fair PA (2017) Immunotoxic effects of in vitro exposure of dolphin lymphocytes to Louisiana sweet crude oil and Corexit. J Appl Toxicol 37(6):676–682.  https://doi.org/10.1002/jat.3414CrossRefGoogle Scholar
  107. Whitehead A, Dubansky B, Bodinier C, Garcia TI, Miles S, Pilley C, Raghunathan V, Roach JL, Walker N, Walter RB, Rice CD, Galvez F (2012) Genomic and physiological footprint of the Deepwater Horizon oil spill on resident marsh fishes. Proc Natl Acad Sci USA 109:20298–20302.  https://doi.org/10.1073/pnas.1109545108CrossRefGoogle Scholar
  108. Wunderlich AC, Silva RJ, Zica ÉOP, Rebelo MF, Parente TEM, Vidal-Martínez VM (2015) The influence of seasonality, fish size and reproductive status on EROD activity in Plagioscion squamosissimus: implications for biomonitoring of tropical/subtropical reservoirs. Ecol Indic 58:267–276.  https://doi.org/10.1016/j.ecolind.2015.05.063CrossRefGoogle Scholar
  109. Yáñez-Arancibia A (1986) Ecología, impacto ambiental y recursos pesqueros: El caso del Ixtoc-1 y los peces. In: Ecología de la Zona Costera Análisis de Siete Tópicos. México, p 180Google Scholar
  110. Yáñez-Arancibia A, Lara-Domínguez AL, Sánchez-Gil P, Álvarez H, Vargas I, Aguirre A (1982) Caracterización Ambient al del Sistema Ecológico y Análisis Comparativo de las Poblaciones de Peces de la Sonda de Campeche y de la LagunadeTérminos antes y Después del Derrame Petrolero del Pozo IXTOC-I (Informe Final). vol 4 partes. PC-EESC/UNAM/ICML(IF)Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Erin L. Pulster
    • 1
    Email author
  • Adolfo Gracia
    • 2
  • Susan M. Snyder
    • 1
  • Kristina Deak
    • 1
    • 3
  • Susan Fogelson
    • 4
  • Steven A. Murawski
    • 1
  1. 1.University of South Florida, College of Marine ScienceSt. PetersburgUSA
  2. 2.Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y LimnologíaMéxico CityMexico
  3. 3.Florida Fish and Wildlife Research InstituteSt. PetersburgUSA
  4. 4.Fishhead LabsStuartUSA

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