Advertisement

Digging Deeper than LC/EC50: Nontraditional Endpoints and Non-model Species in Oil Spill Toxicology

  • Martin GrosellEmail author
  • Robert J. Griffitt
  • Tracy A. Sherwood
  • Dana L. Wetzel
Chapter

Abstract

The response to the 2010 Deepwater Horizon (DWH) oil spill lead to a number of peer-reviewed publications examining the effects of the released oil and dispersant on fish species found in the northern Gulf of Mexico (GoM). Many of these papers, for very good reasons, focused on assessing toxicity by defining lethality through identification of dose-response curves that were specific to a given species, age class, exposure type, oil preparation method, and many other factors. Often those dose-response curves were used to predict LC or EC50 concentrations – amounts of oil that produced an effect on 50% of the exposed organisms. The advantage of this approach is obvious, in that it provides a single point estimate and variance of a concentration required to produce a given effect. This point estimate can then be compared across different exposure regimes to compare susceptibilities. Relevant LC/EC50 data is summarized and discussed in A synthesis of DWH oil, chemical dispersant and chemically dispersed oil aquatic standard laboratory acute and chronic toxicity studies (see Mitchelmore et al. A synthesis of Deepwater Horizon oil, chemical dispersant and chemically dispersed oil aquatic standard laboratory acute and chronic toxicity studies (Chap. 28). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (Eds.) Deep oil spills – facts, fate and effects. Springer; 2020). By constraining toxicity to this point estimate (often of lethality), however, researchers run the risk of missing effects that evince more subtle effects that do not manifest themselves as overt mortality in the short term. In the present chapter, we focus exclusively on fish and explore some of these endpoints, many of which were successfully used in recent years to assess sublethal health impacts on marine fish as part of the response to the DWH spill. We compare what is known about differences in sensitivity, among species, and between age classes within species, examining both organismal and molecular endpoints. Developmental impacts on cardiac health, swim performance, and sensory systems have been widely studied. We discuss what is known about effects on fish immune and endocrine function, the microbiome of the intestine and gill, and intracellular effects such as altered gene expression, oxidative stress, and DNA damage. In conclusion, we attempt to compare the endpoints, assess the sensitivity and utility, and link molecular- and individual-level impacts to larger population and community-level effects.

Keywords

ELS (early life stage) Cardiotoxicity CEWAF (chemically enhanced water accommodated fraction) WAF (water accommodated fraction) Toxicity testing Microbiome Immune function RNA sequencing 

Notes

Acknowledgments

This research was made possible by a grant from The Gulf of Mexico Research Initiative through the C-IMAGE and RECOVER consortia.

References

  1. Ali AO, Hohn C, Allen PJ, Ford L, Dail MB, Pruett S, Petrie-Hanson L (2014) The effects of oil exposure on peripheral blood leukocytes and splenic melano-macrophage centers of Gulf of Mexico fishes. Mar Pollut Bull 79(1–2):87–93CrossRefGoogle Scholar
  2. Arias CR, Koenders K, Larsen AM (2013) Predominant bacteria associated with red snapper from the northern Gulf of Mexico. J Aquat Anim Health 25:281–289CrossRefGoogle Scholar
  3. 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(5):1–21CrossRefGoogle Scholar
  4. 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 36:1763–1766CrossRefGoogle Scholar
  5. Birnie-Gauvin K, Costantini D, Cooke SJ, Willmore WG (2017) A comparative and evolutionary approach to oxidative stress in fish: A review. Fish and Fisheries 18:928–942CrossRefGoogle Scholar
  6. Bosker T, van Balen L, Walsh B, Sepulveda MS, DeGuise S, Perkins C, Griffitt RJ (2017) The combined effect of macondo oil and corexit on sheepshead minnow (Cyprinodon Variegatus) during early development. J Toxicol Environ Health Part A Current Issues 80(9):477–484CrossRefGoogle Scholar
  7. Brette F, Machado B, Cros C, Incardona JP, Scholz NL, Block BA (2014) Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343:772–776CrossRefGoogle Scholar
  8. 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 Toxicol Environ Health Part A 76(21):1198–1209CrossRefGoogle Scholar
  9. 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 (2015) 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 165:197–209CrossRefGoogle Scholar
  10. Cox GK, Crossley DA, Stieglitz JD, Heuer RM, Benetti DD, Grosell M (2017) Oil exposure impairs in situ cardiac function in response to beta-adrenergic stimulation in cobia (Rachycentron canadum). Environ Sci Technol 51:14390–14396CrossRefGoogle Scholar
  11. Dubansky B, Whitehead A, Rice CD, Galvez F (2013) Multi-tissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident Gulf killifish (Fundulus Grandis). Environ Sci Technol 47(10):5074–5082CrossRefGoogle Scholar
  12. Duffy TA, Childress W, Portier R, Chesney EJ (2016) Responses of bay anchovy (Anchoa Mitchilli) larvae under lethal and sublethal scenarios of crude oil exposure. Ecotoxicol Environ Saf 134:264–272CrossRefGoogle Scholar
  13. Edmunds RC, Gill JL, Baldwin DH, Lindo TL, French BL, Brown TL, Esbaugh AJ, Mager EM, Stieglitz J, Hoeing R, Benetti D, Grosell M, Scholz NL, Incardona JP (2015) Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi. Sci Rep 5:17326CrossRefGoogle Scholar
  14. Esbaugh AJ, Mager EM, Stieglitz JD, Hoenig R, Brown TL, , French BL, Lindo 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 543:644–651CrossRefGoogle Scholar
  15. Finch BE, Marzooghi S, Di Toro DM, Stubblefield WA (2017) Phototoxic potential of undispersed and dispersed fresh and weathered Macondo crude oils to Gulf of Mexico marine organisms. Environ Toxicol Chem 36:2640–2650CrossRefGoogle Scholar
  16. Garcia TI, Shen Y, Crawford D, Oleksiak MF, Whitehead A, Walter RB (2012) RNA-seq reveals complex genetic response to Deepwater Horizon oil release in Fundulus grandis. BMC Genomics 13(1):1–9CrossRefGoogle Scholar
  17. 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-Toxicol Pharmacol 133:287–303CrossRefGoogle Scholar
  18. Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, Stringfellow WT, Bill M, Conrad ME, Tom LM, Chavarria KL, Alusi TR, Lamendella R, Joyner DC, Spier C, Baelum J, Auer M, Zemla ML, Chakraborty R, Sonnenthal EL, D’haeseleer P, Holman H-YN, Osman S, Lu Z, Van Nostrand JD, Deng Y, Zhou J, Mason OU (2010) Deep-Sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208CrossRefGoogle Scholar
  19. 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(12):1755–1762CrossRefGoogle Scholar
  20. 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(3):308–321CrossRefGoogle Scholar
  21. Incardona JP, Linbo TL, Scholz NL (2011) Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol 257(2):242–249CrossRefGoogle Scholar
  22. Incardona JP, Garder 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 111(15):E1510–E1518.  https://doi.org/10.1073/pnas.1320950111CrossRefGoogle Scholar
  23. Iwanowicz LR, Blazer VS (2009) An overview of estrogen-associated endocrine disruption in fishes: evidence of effects on reproductive and immune physiology. Conference proceedings of the third bilateral conference between the United States and Russia, pp 266–275Google Scholar
  24. Johansen JL, Esbaugh AJ (2017) Sustained impairment of respiratory function and swim performance following acute oil exposure in a coastal marine fish. Aquat Toxicol 187:82–89CrossRefGoogle Scholar
  25. Johansen JL, Allan BJM, Rummer JL, Esbaugh AJ (2017) Oil exposure disrupts early life-history stages of coral reef fishes. Nat Ecol Evol 1:1146–1152CrossRefGoogle Scholar
  26. Jones ER, Martyniuk CJ, Morris JM, Krasnec MO, Griffitt RJ (2017) Exposure to Deepwater Horizon oil and Corexit 9500 at low concentrations induces transcriptional changes and alters immune transcriptional pathways in sheepshead minnows. Comp Biochem Physiol Part D Genomics Proteomics 23(March):8–16CrossRefGoogle Scholar
  27. Khursigara AJ, Perrichon P, Martinez Bautista N, Burggren WW, Esbaugh AJ (2017) Cardiac function and survival are affected by crude oil in larval red drum, Sciaenops ocellatus. Sci Total Environ 579:797–804CrossRefGoogle Scholar
  28. Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A, Delgardio J, Norton N, Hazen TC, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77:7962–7974CrossRefGoogle Scholar
  29. Larsen AM, Bullard SA, Womble M, Arias CR (2015) Community structure of skin microbiome of Gulf killifish, Fundulus grandis, is driven by seasonality and not exposure to oiled sediments in a Louisiana salt marsh. Microb Ecol 70:534–544CrossRefGoogle Scholar
  30. Lee S, Hong S, Liu X, Kim C, Jung D, Yim UH, Shim WJ, Khim JS, Giesy JP, Choi K (2017) Endocrine disrupting potential of PAHs and their alkylated analogues associated with oil spills. Environ Sci Processes Impacts 19(9):1117–1125CrossRefGoogle Scholar
  31. Mager EM, Esbaugh AJ, Stieglitz JD, Hoenig R, Bodinier C, Incardona JP, Scholz NL, Benetti DD, Grosell M (2014) Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of Mahi-Mahi (Coryphaena hippurus). Environ Sci Technol 48(12):7053–7061CrossRefGoogle Scholar
  32. 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 166:186–191CrossRefGoogle Scholar
  33. Mason OU, Scott NM, Gonzalez A, Robbins-Pianka A, Bælum J, Kimbrel J, Bouskill NJ, Prestat E, Borglin S, Joyner DC, Fortney JL, Jurelevicius D, Stringfellow WT, Alvarez-Cohen L, Hazen TC, Knight R, Gilbert J, Jansson JK (2014) Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill. Int Soc Microbial Ecol J 8:464–475Google Scholar
  34. Mitchelmore CL, Bejarano AC, Wetzel DL (2020) A synthesis of Deepwater Horizon oil, chemical dispersant and chemically dispersed oil aquatic standard laboratory acute and chronic toxicity studies (Chap. 28). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Deep oil spills – facts, fate and effects. SpringerGoogle Scholar
  35. 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(4):1084–1097CrossRefGoogle Scholar
  36. McKim JM (1985) Early life stage toxicity tests. In: Rand GM (ed). (1995) Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment, 2nd edn. CRC press, Boca Raton, pp 974–1010Google Scholar
  37. Nelson D, Heuer RM, Cox GK, Stieglitz JD, Hoenig R, Mager EM, Benetti DD, Grosell M, Crossley D (2016) Effects of crude oil on in situ cardiac function in young adult mahi-mahi (Coryphaena hippurus). Aquat Toxicol 180:274–281CrossRefGoogle Scholar
  38. Nelson D, Stieglitz JD, Cox GK, Heuer RM, Benetti DD, Grosell M, Crossley DA (2017) Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: the impact of crude oil exposure. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 201:58–65CrossRefGoogle Scholar
  39. O’Shaughnessy KA, Forth H, Takeshita R, Chesney EJ (2018) Toxicity of weathered Deepwater Horizon oil to bay anchovy (Anchoa mitchilli) embryos. Ecotoxicol Environ Saf 148:473–479CrossRefGoogle Scholar
  40. Pasparakis C, Mager EM, Stieglitz JD, Benetti D, Grosell M (2016) Effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval Mahi-Mahi (Coryphaena hippurus). Aquat Toxicol 181:113–123CrossRefGoogle Scholar
  41. Pilcher W, Miles S, Tang S, Mayer G, Whitehead A (2014) Genomic and genotoxic responses to controlled weathered-oil exposures confirm and extend field studies on impacts of the Deepwater Horizon oil spill on native killifish. PLoS One 9(9):e106351CrossRefGoogle Scholar
  42. Portnoy DS, 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, effects. Springer, ChamGoogle Scholar
  43. Pulster EL, Main K, Wetzel D, Murawski S (2017) Species-specific metabolism of naphthalene and phenanthrene in 3 species of marine teleosts exposed to Deepwater Horizon crude oil. Environ Toxicol Chem 36(11):3168–3176CrossRefGoogle Scholar
  44. Raimondo S, Hemmer BL, Lilavois CR, Krzykwa J, Almario A, Awkerman JA, Barron MG (2016) Effects of Louisiana crude oil on the sheepshead minnow (Cyprinodon variegatus) during a life-cycle exposure to laboratory oiled sediment. Environ Toxicol 31:1627–1639CrossRefGoogle Scholar
  45. Rauta PR, Nayak B, Das S (2012) Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol Lett 148(1):23–33CrossRefGoogle Scholar
  46. Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77(2):229–238CrossRefGoogle Scholar
  47. Reynaud S, Raveton M, Ravanel P (2008) Interactions between immune and biotransformation systems in fish: a review. Aquat Toxicol 87(3):139–145CrossRefGoogle Scholar
  48. Rowsey LE, Johansen JL, Khursigara AJ, Esbaugh AJ (2019) Oil exposure impairs predator–prey dynamics in larval red drum (Sciaenops ocellatus). Mar Freshw Res. https://doi.org/10.1071/MF18263
  49. 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 242:449–461CrossRefGoogle Scholar
  50. Schirmer K, Fischer BB, Madureira DJ, Pillai S (2010) Transcriptomics in ecotoxicology. Anal Bioanal Chem 397:917–923CrossRefGoogle Scholar
  51. Starostenko LV, Rechkunova NI, Lebedeva NA, Lomzov AA, Koval VV, Lavrik OI (2017) Processing of the abasic sites clustered with the benzo[a]pyrene adducts by the base excision repair enzymes. DNA Repair 50:43–53CrossRefGoogle Scholar
  52. Stieglitz JD, Mager EM, Hoenig RH, Benetti DD, Grosell M (2016) Impacts of Deepwater Horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance. Environ Toxicol Chem 35:2613–2622CrossRefGoogle Scholar
  53. van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149CrossRefGoogle Scholar
  54. Vega-Retter C, Rojas-Hernandez N, Vila I, Espejo R, Loyola DE, Copaja S, Briones M, Nolte AW, Veliz D (2018) Differential gene expression revealed with RNA-Seq and parallel genotype selection of the ornithine decarboxylase gene in fish inhabiting polluted areas. Sci Rep 8(1):4820CrossRefGoogle Scholar
  55. Vignet C, Larcher T, Davail B, Joassard L, Le Menach K, Guionnet T, Lyphout L, Ledevin M, Goubeau M, Budzinski H, Bégout ML, Cousin X (2016) Fish reproduction is disrupted upon lifelong exposure to environmental PAHs fractions revealing different modes of action. Toxics 4(4):26CrossRefGoogle Scholar
  56. 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 109(50):20298–20302CrossRefGoogle Scholar
  57. Xu EG, Mager EM, Grosell M, Pasparakis C, Schlenker LS, Stieglitz JD, Benetti D, Hazard ES, Courtney SM, Diamante G, Freitas J, Hardiman G, Schlenk D (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(14):7842–7851CrossRefGoogle Scholar
  58. Xu EG, Mager EM, Grosell M, Hazard ES, Hardiman G, Schlenk D (2017a) Novel transcriptome assembly and comparative toxicity pathway analysis in mahi-mahi (Coryphaena hippurus) embryos and larvae exposed to Deepwater Horizon oil. Sci Rep 7:44546CrossRefGoogle Scholar
  59. Xu EG, Khursigara AJ, Magnuson J, Hazard ES, Hardiman G, Esbaugh AJ, Roberts AP, Schlenk D (2017b) Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: developmental and transcriptomic consequences. Environ Sci Technol 51:10162–10172CrossRefGoogle Scholar
  60. Xu EG, Magnuson JT, Diamante G, Mager E, Pasparakis C, Grosell M, Roberts AP, Schlenk D (2018) Changes in the global micro-mRNA signatures agree with morphological, physiological and behavioral changes in larval mahi-mahi (Coryphaena hippurus) treated with Deepwater Horizon oil. Environ Sci Technol (Under review)Google Scholar
  61. Xue W, Warshawsky D (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol 206(1):73–93CrossRefGoogle Scholar
  62. Zhang L, Nichols R, Patterson A (2018) The aryl hydrocarbon receptor as a moderator of host- microbiota communication. Current Opinion Toxicology 2:30–35CrossRefGoogle Scholar
  63. Zhang Y, Dong S, Wang H, Tao S, Kiyama R (2016) Biological impact of environmental polycyclic aromatic hydrocarbons (ePAHs) as endocrine disruptors. Environ Pollut 213:809–824CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Martin Grosell
    • 1
    Email author
  • Robert J. Griffitt
    • 2
  • Tracy A. Sherwood
    • 3
  • Dana L. Wetzel
    • 3
  1. 1.Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  2. 2.Division of Coastal Sciences, School of Ocean Science and EngineeringUniversity of Southern MississippiOcean SpringsUSA
  3. 3.Mote Marine LaboratorySarasotaUSA

Personalised recommendations