Skip to main content
SpringerLink
Log in

Physiological Effects of Polycyclic Aromatic Hydrocarbons in Fish Organisms

  • REVIEW
  • Published:
Moscow University Biological Sciences Bulletin Aims and scope Submit manuscript

Abstract

Every year, more than 1 million t of oil enter sea waters as a result of accidents during production or transportation; not counting oil products that enter the ocean with wastewater. The carcinogenic effect of oil components (such as benzopyrene) has been known since the middle of the 20th century. However, after a major oil spill from the Exxon Valdez tanker in 1989, it has become obvious that oil and its components have a strong toxic effect on the body of fish, and these effects are to a great extent mediated by polycyclic aromatic hydrocarbons (PAHs), in particular, by phenanthrene. The juvenile fish suffer the most from oil spills; they exhibit developmental anomalies when exposed to oil products. However, the influence of oil components is not limited to teratogenic effects and affects all age groups, causing disturbances in the functioning of nervous and cardiovascular systems (and other systems and organs) in adults. PAHs also change hormonal and osmotic regulation. As a result, the largest oil spills threaten populations of important commercial fish species. This review examines the effects of PAHs on the physiology of the main organ systems of fish, including both dysfunctions and malformations in young fish under the influence of petroleum products. Particular attention is paid to the cardiotoxic effects of di- and tricyclic PAHs, which were discovered recently and potentially both cause the death in animals when PAH enter water bodies and underlie developmental disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

REFERENCES

  1. Eckle, P., Burgherr, P., and Michaux, E., Risk of large oil spills: A statistical analysis in the aftermath of Deepwater Horizon, Environ. Sci. Technol., 2012, vol. 46, no. 23, pp. 13002–13008. https://doi.org/10.1021/es3029523

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Oil in the Sea: Inputs, Fates, and Effects, Washington, D.C.: The National Academies Press, 2002.

  3. Mcgurk, M.D. and Brown, E.D., Egg–larval mortality of Pacific herring in Prince William Sound, Alaska, after the Exxon Valdez oil spill, Can. J. Fish. Aquat. Sci., 1996, vol. 53, no. 10, pp. 2343–2354. https://doi.org/10.1139/f96-172

    Article  Google Scholar 

  4. Hose, J.E., Mcgurk, M.D., Marty, G.D., Hinton, D.E., Brown, E.D., and Baker, T.T., Sublethal effects of the (Exxon Valdez) oil spill on herring embryos and larvae: Morphological, cytogenetic, and histopathological assessments, Can. J. Fish. Aquat. Sci., 1989, vol. 53, no. 10, pp. 2355–2365. https://doi.org/10.1139/f96-174

    Article  Google Scholar 

  5. Norcross, B.L., Hose, J.E., Frandsen, M., and Brown, E.D., Distribution, abundance, morphological condition, and cytogenetic abnormalities of larval herring in Prince William Sound, Alaska, following the (Exxon Valdez) oil spill, Can. J. Fish. Aquat. Sci., 1996, vol. 53, no. 10, pp. 2376–2387. https://doi.org/10.1139/f96-212

    Article  Google Scholar 

  6. Carvan, M.J., Gallagher, E.P., Goksøyr, A., Hahn, M.E., and Joakim Larsson, D.G., Fish models in toxicology, Zebrafish, 2007, vol. 4, no. 1, pp. 9–20. https://doi.org/10.1089/zeb.2006.9998

    Article  PubMed  Google Scholar 

  7. Ernst, V.V., Neff, J.M., and Anderson, J.W., The effects of the water-soluble fractions of no. 2 fuel oil on the early development of the estuarine fish, Fundulus grandis baird and girard, Environ. Pollut., 1977, vol. 14, no. 1, pp. 25–35. https://doi.org/10.1016/0013-9327(77)90085-4

  8. Lindén, O., Biological effects of oil on early development of the Baltic herring Clupea harengus membras, Mar. Biol., 1978, vol. 45, no. 3, pp. 273–283. https://doi.org/10.1007/bf00390611

    Article  Google Scholar 

  9. Wang, Z., Stout, S.A., and Fingas, M., Forensic fingerprinting of biomarkers for oil spill characterization and source identification, Environ. Forensics, 2007, vol. 7, no. 2, pp. 105–146. https://doi.org/10.1080/15275920600667104

    Article  CAS  Google Scholar 

  10. Adeyemo, O.K., Kroll, K.J., and Denslow, N.D., Developmental abnormalities and differential expression of genes induced in oil and dispersant exposed Menidia beryllina embryos, Aquat. Toxicol., 2015, vol. 168, pp. 60–71. https://doi.org/10.1016/j.aquatox.2015.09.012

    Article  CAS  PubMed  Google Scholar 

  11. Incardona, J.P., Carls, M.G., Teraoka, H., Sloan, C.A., Collier, T.K., and Scholz, N.L., Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development, Environ. Health Perspect., 2005, vol. 113, no. 12, pp. 1755–1762. https://doi.org/10.1289/ehp.8230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Jung, J., Hicken, C.E., Boyd, D., Anulacion, B.F., Carls, M.G., Shim, W.J., and Incardona, J.P., Geologically distinct crude oils cause a common cardiotoxicity syndrome in developing zebrafish, Chemosphere, 2013, vol. 91, no. 8, pp. 1146–1155. https://doi.org/10.1016/j.chemosphere.2013.01.019

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Mcintosh, S., King, T., Wu, D., and Hodson, P.V., Toxicity of dispersed weathered crude oil to early life stages of Atlantic herring (Clupea harengus), Environ. Toxicol. Chem., 2010, vol. 29, no. 5, pp. 1160–1167. https://doi.org/10.1002/etc.134

    Article  CAS  PubMed  Google Scholar 

  14. Mu, J., Jin, F., Ma, X., Lin, Z., and Wang, J., Comparative effects of biological and chemical dispersants on the bioavailability and toxicity of crude oil to early life stages of marine medaka (Oryzias melastigma), Environ. Toxicol. Chem., 2014, vol. 33, no. 11, pp. 2576–2583. https://doi.org/10.1002/etc.2721

    Article  CAS  PubMed  Google Scholar 

  15. Pollino, C.A. and Holdway, D.A., Toxicity testing of crude oil and related compounds using early life stages of the crimson-spotted rainbowfish (Melanotaenia fluviatilis), Ecotoxicology Environ. Saf., 2002, vol. 52, no. 3, pp. 180–189. https://doi.org/10.1006/eesa.2002.2190

    Article  CAS  Google Scholar 

  16. Lawal, A.T., Polycyclic aromatic hydrocarbons. A review, Cogent Environ. Sci., 2017, vol. 3, no. 1, p. 1339841. https://doi.org/10.1080/23311843.2017.1339841

    Article  CAS  Google Scholar 

  17. Spromberg, J.A., Baldwin, D.H., Damm, S.E., Mcintyre, J.K., Huff, M., Sloan, C.A., Anulacion, B.F., Davis, J.W., and Scholz, N.L., Coho salmon spawner mortality in western US urban watersheds: Bioinfiltration prevents lethal storm water impacts, J. Appl. Ecol., 2016, vol. 53, no. 2, pp. 398–407. https://doi.org/10.1111/1365-2664.12534

    Article  CAS  PubMed  Google Scholar 

  18. Menzie, C.A., Potocki, B.B., and Santodonato, J., Exposure to carcinogenic PAHs in the environment, Environ. Sci. Technol., 1992, vol. 26, no. 7, pp. 1278–1284. https://doi.org/10.1021/es00031a002

    Article  ADS  CAS  Google Scholar 

  19. Bunton, T.E., Review article: Experimental chemical carcinogenesis in fish, Toxicologic Pathol., 1996, vol. 24, no. 5, pp. 603–618. https://doi.org/10.1177/019262339602400511

    Article  CAS  Google Scholar 

  20. Hose, J.E., Hannaht, J.B., Puffer, H.W., and Landolt, M.L., Histologic and skeletal abnormalities in benzo(a)pyrene-treated rainbow trout alevins, Arch. Environ. Contam. Toxicol., 1984, vol. 13, no. 6, pp. 675–684. https://doi.org/10.1007/bf01055930

    Article  CAS  PubMed  Google Scholar 

  21. Hose, J.E., Hannah, J.B., Dijulio, D., Landolt, M.L., Miller, B.S., Iwaoka, W.T., and Felton, S.P., Effects of benzo(a)pyrene on early development of flatfish, Arch. Environ. Contam. Toxicol., 1982, vol. 11, no. 2, pp. 167–171. https://doi.org/10.1007/bf01054893

    Article  CAS  PubMed  Google Scholar 

  22. Hannah, J.B., Hose, J.E., Landolt, M.L., Miller, B.S., Felton, S.P., and Iwaoka, W.T., Benzo(a)pyrene-induced morphologic and developmental abnormalities in rainbow trout, Arch. Environ. Contam. Toxicol., 1982, vol. 11, no. 6, pp. 727–734. https://doi.org/10.1007/bf01059161

    Article  CAS  PubMed  Google Scholar 

  23. Falk-Petersen, I.-B., Toxic effects of aqueous extracts of ekofisk crude oil, crude oil fractions, and commercial oil products on the development of sea urchin eggs, Sarsia, 1977, vol. 64, no. 3, pp. 161–169. https://doi.org/10.1080/00364827.1979.10411377

    Article  Google Scholar 

  24. Malins, D.C., Alterations in the cellular and subcellular structure of marine teleosts and invertebrates exposed to petroleum in the laboratory and field: A critical review, Can. J. Fish. Aquat. Sci., 1982, vol. 39, no. 6, pp. 877–889. https://doi.org/10.1139/f82-119

    Article  CAS  Google Scholar 

  25. Denison, M.S., Seidel, S.D., Rogers, W.J., Ziccardi, M., Winter, G.M., and Heath-Pagliuso, S., Natural and synthetic ligands for the Ah receptor, Molecular Biology Approaches to Toxicology, Puga, A. and Wallace, K.B., Eds., Philadelphia: Taylor, 1998, pp. 393–410.

    Google Scholar 

  26. Hahn, M.E., Karchner, S.I., Evans, B.R., Franks, D.G., Merson, R.R., and Lapseritis, J.M., Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates: Insights from comparative genomics, J. Exp. Zoology Part A: Comp. Exp. Biol., 2006, vol. 305A, no. 9, pp. 693–706. https://doi.org/10.1002/jez.a.323

    Article  CAS  Google Scholar 

  27. Billiard, S.M., Timme-Laragy, A.R., Wassenberg, D.M., Cockman, C., and Di Giulio, R.T., The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish, Toxicol. Sci., 2006, vol. 92, no. 2, pp. 526–536. https://doi.org/10.1093/toxsci/kfl011

    Article  CAS  PubMed  Google Scholar 

  28. Clark, B.W., Matson, C.W., Jung, D., and Di Giulio, R.T., AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus), Aquat. Toxicol., 2010, vol. 99, no. 2, pp. 232–240. https://doi.org/10.1016/j.aquatox.2010.05.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Prasch, A.L., Teraoka, H., Carney, S.A., Dong, W., Hiraga, T., Stegeman, J.J., Heideman, W., and Peterson, R.E., Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish, Toxicol. Sci., 2003, vol. 76, no. 1, pp. 138–150. https://doi.org/10.1093/toxsci/kfg202

    Article  CAS  PubMed  Google Scholar 

  30. Denison, M.S. and Nagy, S.R., Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals, Annu. Rev. Pharmacol. Toxicol., 2003, vol. 43, no. 1, pp. 309–334. https://doi.org/10.1146/annurev.pharmtox.43.100901.135828

    Article  CAS  PubMed  Google Scholar 

  31. Gohlke, J.M., Doke, D., Tipre, M., Leader, M., and Fitzgerald, T., A review of seafood safety after the Deepwater Horizon blowout, Environ. Health Perspect., 2011, vol. 119, no. 8, pp. 1062–1069. https://doi.org/10.1289/ehp.1103507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Denison, M.S., Fisher, J.M., and Whitlock, J.P., Inducible, receptor-dependent protein-DNA interactions at a dioxin-responsive transcriptional enhancer., Proc. Natl. Acad. Sci., 1988, vol. 85, no. 8, pp. 2528–2532. https://doi.org/10.1073/pnas.85.8.2528

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  33. Korashy, H.M. and El-Kadi, A.O.S., The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular diseases, Drug Metab. Rev., 2006, vol. 38, no. 3, pp. 411–450. https://doi.org/10.1080/03602530600632063

    Article  CAS  PubMed  Google Scholar 

  34. Carney, S.A., Peterson, R.E., and Heideman, W., 2,3,7,8-Tetrachlorodibenzo-p-dioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1A-independent mechanism in zebrafish, Mol. Pharmacol., 2004, vol. 66, no. 3, pp. 512–521.

    CAS  PubMed  Google Scholar 

  35. Carney, S.A., Chen, J., Burns, C.G., Xiong, K.M., Peterson, R.E., and Heideman, W., Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish, Mol. Pharmacol., 2006, vol. 70, no. 2, pp. 549–561. https://doi.org/10.1124/mol.106.025304

    Article  CAS  PubMed  Google Scholar 

  36. Barron, M.G., Heintz, R., and Rice, S.D., Relative potency of PAHs and heterocycles as aryl hydrocarbon receptor agonists in fish, Mar. Environ. Res., 2004, vol. 58, nos. 2–5, pp. 95–100. https://doi.org/10.1016/j.marenvres.2004.03.001

    Article  CAS  PubMed  Google Scholar 

  37. Wang, Z. and Fingas, M.F., Development of oil hydrocarbon fingerprinting and identification techniques, Mar. Pollut. Bull., 2003, vol. 47, nos. 9–12, pp. 423–452. https://doi.org/10.1016/s0025-326x(03)00215-7

    Article  CAS  PubMed  Google Scholar 

  38. Carls, M.G., Rice, S.D., and 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, vol. 18, no. 3, pp. 481–493. https://doi.org/10.1897/1551-5028(1999)018<0481:sofetw>2.3.co;2

    Article  CAS  Google Scholar 

  39. Heintz, R.A., Short, J.W., and Rice, S.D., 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., 1999, vol. 18, no. 3, pp. 494–503. https://doi.org/10.1897/1551-5028(1999)018<0494:sofetw>2.3.co;2

    Article  CAS  Google Scholar 

  40. Marty, G.D., Hinton, D.E., Short, J.W., Heintz, R.A., Rice, S.D., Dambach, D.M., Willits, N.H., and 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. Zoology, 1997, vol. 75, no. 6, pp. 989–1007. https://doi.org/10.1139/z97-120

    Article  CAS  Google Scholar 

  41. Marty, G.D., Hose, J.E., Mcgurk, M.D., Brown, E.D., and Hinton, D.E., 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., 1997, vol. 54, no. 8, pp. 1846–1857. https://doi.org/10.1139/f97-091

    Article  Google Scholar 

  42. Incardona, J.P., Collier, T.K., and Scholz, N.L., Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons, Toxicol. Appl. Pharmacol., 2004, vol. 196, no. 2, pp. 191–205. https://doi.org/10.1016/j.taap.2003.11.026

    Article  CAS  PubMed  Google Scholar 

  43. Xu, K., Zhang, Yi., Zheng, J., Wang, C., and Chen, R., Comparative toxicity of 3–5 ringed polycyclic aromatic hydrocarbons to skeletal development in zebrafish embryos and the possible reason, Bull. Environ. Contam. Toxicol., 2023, vol. 110, no. 1, p. 8. https://doi.org/10.1007/s00128-022-03644-x

    Article  CAS  Google Scholar 

  44. Petersen, G.I. and Kristensen, P., Bioaccumulation of lipophilic substances in fish early life stages, Environ. Toxicol. Chem., 1998, vol. 17, no. 7, pp. 1385–1395. https://doi.org/10.1002/etc.5620170724

    Article  CAS  Google Scholar 

  45. De Pinho, J.V., Lopes, A.P., De Almeida Rodrigues, P., Ferrari, R.G., Hauser-Davis, R.A., and Conte-Junior, C.A., Food safety concerns on polycyclic aromatic hydrocarbon contamination in fish products from estuarine bays throughout the American continent, Sci. Total Environ., 2023, vol. 858, no. 2, p. 159930. https://doi.org/10.1016/j.scitotenv.2022.159930

    Article  ADS  CAS  PubMed  Google Scholar 

  46. Rusni, S., Sassa, M., Takehana, Yu., Kinoshita, M., and Inoue, K., Correlation between cytochrome P450 1A (cyp1a) mRNA expression and ambient phenanthrene and pyrene concentration in Javanese Medaka Oryzias javanicus, Fish. Sci., 2020, vol. 86, no. 4, pp. 605–613. https://doi.org/10.1007/s12562-020-01428-y

    Article  CAS  Google Scholar 

  47. Xie, S., Feng, Yo., Zhou, A., Lu, Z., and Zou, J., Comparative analysis of two new zebrafish models: The cyp1a low-expression line and cyp1a knockout line under PAHs exposure, Gene, 2023, vol. 869, p. 147391. https://doi.org/10.1016/j.gene.2023.147391

    Article  CAS  PubMed  Google Scholar 

  48. Incardona, J.P., Carls, M.G., Day, H.L., Sloan, C.A., Bolton, J.L., Collier, T.K., and 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, vol. 43, no. 1, pp. 201–207. https://doi.org/10.1021/es802270t

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Brette, F., Machado, B., Cros, C., Incardona, J.P., Scholz, N.L., and Block, B.A., Crude oil impairs cardiac excitation-contraction coupling in fish, Science, 2014, vol. 343, no. 6172, pp. 772–776. https://doi.org/10.1126/science.1242747

    Article  ADS  CAS  PubMed  Google Scholar 

  50. Brette, F., Shiels, H.A., Galli, G.L.J., Cros, C., Incardona, J.P., Scholz, N.L., and Block, B.A., A novel cardiotoxic mechanism for a pervasive global pollutant, Sci. Rep., 2017, vol. 7, no. 1, p. 41476. https://doi.org/10.1038/srep41476

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ainerua, M.O., Tinwell, J., Kompella, S.N., Sørhus, E., White, K.N., Van Dongen, B.E., and Shiels, H.A., Understanding the cardiac toxicity of the anthropogenic pollutant phenanthrene on the freshwater indicator species, the brown trout (Salmo trutta): From whole heart to cardiomyocytes, Chemosphere, 2020, vol. 239, p. 124608. https://doi.org/10.1016/j.chemosphere.2019.124608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Abramochkin, D.V., Kompella, S.N., and Shiels, H.A., Phenanthrene alters the electrical activity of atrial and ventricular myocytes of a polar fish, the navaga cod, Aquat. Toxicol., 2021, vol. 235, p. 105823. https://doi.org/10.1016/j.aquatox.2021.105823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Filatova, T.S., Mikhailova, V.B., Guskova, V.O., and Abramochkin, D.V., The effects of phenanthrene on the electrical activity in the heart of shorthorn sculpin Myoxocephalus scorpio, J. Evol. Biochem. Physiol., 2022, vol. 58, no. S1, pp. S44–S51. https://doi.org/10.1134/s0022093022070055

    Article  CAS  Google Scholar 

  54. Vehniäinen, E., Haverinen, J., and Vornanen, M., Polycyclic aromatic hydrocarbons phenanthrene and retene modify the action potential via multiple ion currents in rainbow trout Oncorhynchus mykiss cardiac myocytes, Environ. Toxicol. Chem., 2019, vol. 38, no. 10, pp. 2145–2153. https://doi.org/10.1002/etc.4530

    Article  CAS  PubMed  Google Scholar 

  55. Al-Moubarak, E., Shiels, H.A., Zhang, Yi., Du, C., Hanington, O., Harmer, S.C., Dempsey, C.E., and Hancox, J.C., Inhibition of the hERG potassium channel by phenanthrene: a polycyclic aromatic hydrocarbon pollutant, Cell. Mol. Life Sci., 2021, vol. 78, no. 23, pp. 7899–7914. https://doi.org/10.1007/s00018-021-03967-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sanguinetti, M.C. and Tristani-Firouzi, M., hERG potassium channels and cardiac arrhythmia, Nature, 2006, vol. 440, no. 7083, pp. 463–469. https://doi.org/10.1038/nature04710

    Article  ADS  CAS  PubMed  Google Scholar 

  57. Nelson, D., Heuer, R.M., Cox, G.K., Stieglitz, J.D., Hoenig, R., Mager, E.M., Benetti, D.D., Grosell, M., and Crossley, D.A., Effects of crude oil on in situ cardiac function in young adult mahi–mahi (Coryphaena hippurus), Aquat. Toxicol., 2016, vol. 180, pp. 274–281. https://doi.org/10.1016/j.aquatox.2016.10.012

    Article  CAS  PubMed  Google Scholar 

  58. Hondeghem, L.M., Carlsson, L., and Duker, G., Instability and triangulation of the action potential predict serious proarrhythmia, but action potential duration prolongation is antiarrhythmic, Circulation, 2001, vol. 103, no. 15, pp. 2004–2013. https://doi.org/10.1161/01.cir.103.15.2004

    Article  CAS  PubMed  Google Scholar 

  59. Kompella, S.N., Brette, F., Hancox, J.C., and Shiels, H.A., Phenanthrene impacts zebrafish cardiomyocyte excitability by inhibiting IKr and shortening action potential duration, J. Gen. Physiol., 2021, vol. 153, no. 2. https://doi.org/10.1085/jgp.202012733

  60. Abrajano, T.A., Yan, B., and O’Malley, V., High molecular weight petrogenic and pyrogenic hydrocarbons in aquatic environments, Enviromental Geochemistry, Lollar, B.S., Ed., Elsevier, 2004, vol. 9, pp. 475–509. https://doi.org/10.1016/b978-0-08-095975-7.00913-x

    Book  Google Scholar 

  61. Andersen, Ø., Frantzen, M., Rosland, M., Timmerhaus, G., Skugor, A., and Krasnov, A., Effects of crude oil exposure and elevated temperature on the liver transcriptome of polar cod (Boreogadus saida), Aquat. Toxicol., 2015, vol. 165, pp. 9–18. https://doi.org/10.1016/j.aquatox.2015.04.023

    Article  CAS  PubMed  Google Scholar 

  62. Bender, M.L., Giebichenstein, J., Teisrud, R.N., Laurent, J., Frantzen, M., Meador, J.P., Sørensen, L., Hansen, B.H., Reinardy, H.C., Laurel, B., and Nahrgang, J., Combined effects of crude oil exposure and warming on eggs and larvae of an arctic forage fish, Sci. Rep., 2021, vol. 11, no. 1, p. 8410. https://doi.org/10.1038/s41598-021-87932-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sørhus, E., Incardona, J.P., Furmanek, T., Goetz, G.W., Scholz, N.L., Meier, S., Edvardsen, R.B., and Jentoft, S., Novel adverse outcome pathways revealed by chemical genetics in a developing marine fish, eLife, 2017, vol. 6, p. e20707. https://doi.org/10.7554/elife.20707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Edmunds, R.C., Gill, J.A., Baldwin, D.H., Linbo, T.L., French, B.L., Brown, T.L., Esbaugh, A.J., Mager, E.M., Stieglitz, J., Hoenig, R., Benetti, D., Grosell, M., Scholz, N.L., and Incardona, J.P., Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi, Sci. Rep., 2015, vol. 5, no. 1, p. 17326. https://doi.org/10.1038/srep17326

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sørhus, E., Incardona, J.P., Karlsen, Ø., Linbo, T., Sørensen, L., Nordtug, T., Van Der Meeren, T., Thorsen, A., Thorbjørnsen, M., Jentoft, S., Edvardsen, R.B., and Meier, S., Crude oil exposures reveal roles for intracellular calcium cycling in haddock craniofacial and cardiac development, Sci. Rep., 2016, vol. 6, no. 1, p. 31058. https://doi.org/10.1038/srep31058

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ebert, A.M., Hume, G.L., Warren, K.S., Cook, N.P., Burns, C.G., Mohideen, M.A., Siegal, G., Yelon, D., Fishman, M.C., and Garrity, D.M., Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts, Proc. Natl. Acad. Sci., 2005, vol. 102, no. 49, pp. 17705–17710. https://doi.org/10.1073/pnas.0502683102

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  67. Rottbauer, W., Baker, K., Wo, Z.G., Mohideen, M.P.K., Cantiello, H.F., and Fishman, M.C., Growth and function of the embryonic heart depend upon the cardiac-specific L-type calcium channel α1 subunit, Dev. Cell, 2001, vol. 1, no. 2, pp. 265–275. https://doi.org/10.1016/s1534-5807(01)00023-5

    Article  CAS  PubMed  Google Scholar 

  68. Sørhus, E., Nakken, C.L., Donald, C.E., Ripley, D.M., Shiels, H.A., and Meier, S., Cardiac toxicity of phenanthrene depends on developmental stage in Atlantic cod (Gadus morhua), Sci. Total Environ., 2023, vol. 881, p. 163484. https://doi.org/10.1016/j.scitotenv.2023.163484

    Article  ADS  CAS  PubMed  Google Scholar 

  69. Huang, L., Xi, Z., Wang, C., Zhang, Yo., Yang, Z., Zhang, S., Chen, Yi., and Zuo, Z., Phenanthrene exposure induces cardiac hypertrophy via reducing miR-133a expression by DNA methylation, Sci. Rep., 2016, vol. 6, no. 1, p. 20105. https://doi.org/10.1038/srep20105

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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., and Incar-dona, 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, vol. 108, no. 17, pp. 7086–7090. https://doi.org/10.1073/pnas.1019031108

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  71. Incardona, J.P., Carls, M.G., Holland, L., Linbo, T.L., Baldwin, D.H., Myers, M.S., Peck, K.A., Tagal, M., Rice, S.D., and Scholz, N.L., Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring, Sci. Rep., 2015, vol. 5, no. 1, p. 13499. https://doi.org/10.1038/srep13499

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  72. Anttila, K., Jã¸rgensen, S.M., Casselman, M.T., Timmerhaus, G., Farrell, A.P., and Takle, H., Association between swimming performance, cardiorespiratory morphometry, and thermal tolerance in Atlantic salmon (Salmo salar L.), Front. Mar. Sci., 2014, vol. 1, p. 76. https://doi.org/10.3389/fmars.2014.00076

    Article  Google Scholar 

  73. Heintz, R.A., Rice, S.D., Wertheimer, A.C., Bradshaw, R.F., Thrower, F.P., Joyce, J.E., and 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, vol. 208, pp. 205–216. https://doi.org/10.3354/meps208205

    Article  ADS  Google Scholar 

  74. Incardona, J.P. and Scholz, N.L., The influence of heart developmental anatomy on cardiotoxicity-based adverse outcome pathways in fish, Aquat. Toxicol., 2016, vol. 177, pp. 515–525. https://doi.org/10.1016/j.aquatox.2016.06.016

    Article  CAS  PubMed  Google Scholar 

  75. Gonçalves, R., Scholze, M., Ferreira, A.M., Martins, M., and Correia, A.D., The joint effect of polycyclic aromatic hydrocarbons on fish behavior, Environ. Res., 2008, vol. 108, no. 2, pp. 205–213. https://doi.org/10.1016/j.envres.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  76. Carvalho, P.S.M., Kalil, D.D.C.B., Novelli, G.A.A., Bainy, A.C.D., and Fraga, A.P.M., Effects of naphthalene and phenanthrene on visual and prey capture endpoints during early stages of the dourado Salminus brasiliensis, Mar. Environ. Res., 2008, vol. 66, no. 1, pp. 205–207. https://doi.org/10.1016/j.marenvres.2008.02.059

    Article  CAS  PubMed  Google Scholar 

  77. Johansen, J.L., Allan, B.J.M., Rummer, J.L., and Esbaugh, A.J., Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments, Nat. Ecol. Evol., 2017, vol. 1, no. 8, pp. 1146–1152. https://doi.org/10.1038/s41559-017-0232-5

    Article  PubMed  Google Scholar 

  78. Geier, M.C., James Minick, D., Truong, L., Tilton, S., Pande, P., Anderson, K.A., Teeguardan, J., and Tanguay, R.L., Systematic developmental neurotoxicity assessment of a representative PAH Superfund mixture using zebrafish, Toxicol. Appl. Pharmacol., 2018, vol. 354, pp. 115–125. https://doi.org/10.1016/j.taap.2018.03.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Xu, E.G., Mager, E.M., Grosell, M., Pasparakis, C., Schlenker, L.S., Stieglitz, J.D., Benetti, D., Hazard, E.S., Courtney, S.M., Diamante, G., Freitas, J., Hardiman, G., and Schlenk, D., Time- and oil-dependent transcriptomic and physiological responses to Deepwater Horizon oil in mahi-mahi (Coryphaena hippurus) embryos and larvae, Environ. Sci. Technol., 2016, vol. 50, no. 14, pp. 7842–7851. https://doi.org/10.1021/acs.est.6b02205

    Article  ADS  CAS  PubMed  Google Scholar 

  80. Xu, E.G., Khursigara, A.J., Magnuson, J., Hazard, E.S., Hardiman, G., Esbaugh, A.J., Roberts, A.P., and Schlenk, D., Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: Developmental and transcriptomic consequences, Environ. Sci. Technol., 2017, vol. 51, no. 17, pp. 10162–10172. https://doi.org/10.1021/acs.est.7b02037

    Article  ADS  CAS  PubMed  Google Scholar 

  81. Khursigara, A.J., Ackerly, K.L., and Esbaugh, A.J., Pyrene drives reduced brain size during early life exposure in an estuarine fish, the red drum (Sciaenops ocellatus), Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol., 2022, vol. 259, p. 109397. https://doi.org/10.1016/j.cbpc.2022.109397

    Article  CAS  Google Scholar 

  82. Magnuson, J.T., Bautista, N.M., Lucero, J., Lund, A.K., Xu, E.G., Schlenk, D., Burggren, W.W., and Roberts, A.P., Exposure to crude oil induces retinal apoptosis and impairs visual function in fish, Environ. Sci. Technol., 2020, vol. 54, no. 5, pp. 2843–2850. https://doi.org/10.1021/acs.est.9b07658

    Article  ADS  CAS  PubMed  Google Scholar 

  83. Magnuson, J.T., Khursigara, A.J., Allmon, E.B., Esbaugh, A.J., and Roberts, A.P., Effects of Deepwater Horizon crude oil on ocular development in two estuarine fish species, red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus), Ecotoxicology Environ. Saf., 2018, vol. 166, pp. 186–191. https://doi.org/10.1016/j.ecoenv.2018.09.087

    Article  CAS  Google Scholar 

  84. Cave, E.J. and Kajiura, S.M., Effect of Deepwater Horizon crude oil water accommodated fraction on olfactory function in the Atlantic stingray, Hypanus sabinus, Sci. Rep., 2018, vol. 8, no. 1, p. 15786. https://doi.org/10.1038/s41598-018-34140-0

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  85. Schlenker, L.S., Welch, M.J., Meredith, T.L., Mager, E.M., Lari, E., Babcock, E.A., Pyle, G.G., Munday, P.L., and Grosell, M., Damsels in distress: Oil exposure modifies behavior and olfaction in bicolor damselfish (Stegastes partitus), Environ. Sci. Technol., 2019, vol. 53, no. 18, pp. 10993–11001. https://doi.org/10.1021/acs.est.9b03915

    Article  ADS  CAS  PubMed  Google Scholar 

  86. Lari, E., Steinkey, D., Razmara, P., Mohaddes, E., and Pyle, G.G., Oil sands process-affected water impairs the olfactory system of rainbow trout (Oncorhynchus mykiss), Ecotoxicology Environ. Saf., 2019, vol. 170, pp. 62–67. https://doi.org/10.1016/j.ecoenv.2018.11.105

    Article  CAS  Google Scholar 

  87. Redmond, L., Kashani, A.H., and Ghosh, A., Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription, Neuron, 2002, vol. 34, no. 6, pp. 999–1010. https://doi.org/10.1016/s0896-6273(02)00737-7

    Article  CAS  PubMed  Google Scholar 

  88. Zhang, Ya., Dong, S., Wang, H., Tao, S., and Kiyama, R., Biological impact of environmental polycyclic aromatic hydrocarbons (ePAHs) as endocrine disruptors, Environ. Pollut., 2016, vol. 213, pp. 809–824. https://doi.org/10.1016/j.envpol.2016.03.050

    Article  CAS  PubMed  Google Scholar 

  89. Hayakawa, K., Onoda, Yu., Tachikawa, C., Hosoi, S., Yoshita, M., Chung, S.W., Kizu, R., Toriba, A., Kameda, T., and Tang, N., Estrogenic/antiestrogenic activities of polycyclic aromatic hydrocarbons and their monohydroxylated derivatives by yeast two-hybrid assay, J. Health Sci., 2007, vol. 53, no. 5, pp. 562–570. https://doi.org/10.1248/jhs.53.562

    Article  CAS  Google Scholar 

  90. Colli-Dula, R.C., Fang, X., Moraga-Amador, D., Albornoz-Abud, N., Zamora-Bustillos, R., Conesa, A., Zapata-Perez, O., Moreno, D., and Hernandez-Nuñez, E., Transcriptome analysis reveals novel insights into the response of low-dose benzo(a)pyrene exposure in male tilapia, Aquat. Toxicol., 2018, vol. 201, pp. 162–173. https://doi.org/10.1016/j.aquatox.2018.06.005

    Article  CAS  PubMed  Google Scholar 

  91. Wu, L., Zhong, L., Ru, H., Yao, F., Ni, Z., and Li, Yu., Thyroid disruption and growth inhibition of zebrafish embryos/larvae by phenanthrene treatment at environmentally relevant concentrations, Aquat. Toxicol., 2022, vol. 243, p. 106053. https://doi.org/10.1016/j.aquatox.2021.106053

    Article  CAS  PubMed  Google Scholar 

  92. Mousavi, A., Salamat, N., and Safahieh, A., Phenanthrene disrupting effects on the thyroid system of Arabian seabream, Acanthopagrus arabicus: In situ and in vivo study, Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol., 2022, vol. 252, p. 109226. https://doi.org/10.1016/j.cbpc.2021.109226

    Article  CAS  Google Scholar 

  93. Zhong, L., Wu, L., Ru, H., Wei, N., Yao, F., Zhang, H., Ni, Z., Duan, X., and Li, Yu., Sex-specific thyroid disruption caused by phenanthrene in adult zebrafish (Danio rerio), Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol., 2023, vol. 263, p. 109484. https://doi.org/10.1016/j.cbpc.2022.109484

    Article  CAS  Google Scholar 

  94. Sun, L., Zuo, Z., Chen, M., Chen, Yi., and Wang, C., Reproductive and transgenerational toxicities of phenanthrene on female marine medaka (Oryzias melastigma), Aquat. Toxicol., 2015, vol. 162, pp. 109–116. https://doi.org/10.1016/j.aquatox.2015.03.013

    Article  CAS  PubMed  Google Scholar 

  95. Peng, X., Sun, X., Yu, M., Fu, W., Chen, H., and Chen, J., Chronic exposure to environmental concentrations of phenanthrene impairs zebrafish reproduction, Ecotoxicology Environ. Saf., 2019, vol. 182, p. 109376. https://doi.org/10.1016/j.ecoenv.2019.109376

    Article  CAS  Google Scholar 

  96. Kennedy, C.J. and Farrell, A.P., 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., 2005, vol. 323, no. 1, pp. 43–56. https://doi.org/10.1016/j.jembe.2005.02.021

    Article  CAS  Google Scholar 

  97. Zbanyszek, R. and Smith, L.S., The effect of water-soluble aromatic hydrocarbons on some haematological parameters of rainbow trout, Salmo gairdneri Richardson, during acute exposure, J. Fish Biol., 1984, vol. 24, no. 5, pp. 545–552. https://doi.org/10.1111/j.1095-8649.1984.tb04825.x

    Article  CAS  Google Scholar 

  98. Katsumiti, A., Domingos, F.X.V., Azevedo, M., Da Silva, M.D., Damian, R.C., Almeida, M.I.M., De Assis, H.C.S., Cestari, M.M., Randi, M.A.F., Ribeiro, C.A.O., and Freire, C.A., 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. Monitoring Assess., 2009, vol. 152, nos. 1–4, pp. 209–222. https://doi.org/10.1007/s10661-008-0309-3

    Article  CAS  Google Scholar 

  99. Dangé, A.D., Branchial Na+/K+-ATPase inhibition in a freshwater euryhaline teleost, tilapia (Oreochromis mossambicus), during short-term exposure to toluene or naphthalene: Influence of salinity, Environ. Pollut. Ser. A, Ecol. Biol., 1986, vol. 42, no. 3, pp. 273–286. https://doi.org/10.1016/0143-1471(86)90037-1

    Article  Google Scholar 

  100. Souza-Bastos, L.R. and Freire, C.A., Osmoregulation of the resident estuarine fish Atherinella brasiliensis was still affected by an oil spill (Vicuña tanker, Paranaguá Bay, Brazil), 7months after the accident, Sci. Total Environ., 2011, vol. 409, no. 7, pp. 1229–1234. https://doi.org/10.1016/j.scitotenv.2010.08.035

    Article  ADS  CAS  PubMed  Google Scholar 

  101. Sarasquete, C. and Segner, H., Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies, Sci. Total Environ., 2000, vol. 247, nos. 2–3, pp. 313–332. https://doi.org/10.1016/s0048-9697(99)00500-8

    Article  ADS  CAS  PubMed  Google Scholar 

  102. Meier, S., Karlsen, Ø., Le Goff, J., Sørensen, L., Sørhus, E., Pampanin, D.M., Donald, C.E., Fjelldal, P.G., Dunaevskaya, E., Romano, M., Caliani, I., Casini, S., Bogevik, A.S., Olsvik, P.A., Myers, M., and Grøsvik, B.E., DNA damage and health effects in juvenile haddock (Melanogrammus aeglefinus) exposed to PAHs associated with oil-polluted sediment or produced water, PLoS One, 2020, vol. 15, no. 10, p. e0240307. https://doi.org/10.1371/journal.pone.0240307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Kelly, B.C., Gobas, F.A.P.C., and Mclachlan, M.S., Intestinal absorption and biomagnification of organic contaminants in fish, wildlife, and humans, Environ. Toxicol. Chem., 2004, vol. 23, no. 10, pp. 2324–2336. https://doi.org/10.1897/03-545

    Article  CAS  PubMed  Google Scholar 

  104. De Gelder, S., Sæle, Ø., De Veen, B.T.H., Vos, J., Flik, G., Berntssen, M.H.G., and Klaren, P.H.M., The polycyclic aromatic hydrocarbons benzo[a]pyrene and phenanthrene inhibit intestinal lipase activity in rainbow trout (Oncorhynchus mykiss), Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol., 2017, vol. 198, pp. 1–8. https://doi.org/10.1016/j.cbpc.2017.04.008

    Article  CAS  Google Scholar 

  105. Incardona, J.P. and Scholz, N.L., Case study: The 2010 Deepwater Horizon oil spill and its environmental developmental impacts, Development and Environment, Burggren, W. and Dubansky, B., Eds., Cham: Springer, 2018, pp. 235–283. https://doi.org/10.1007/978-3-319-75935-7_10

    Book  Google Scholar 

Download references

Funding

The research was supported by Russian Science Foundation, project no. 22-14-00075.

Author information

Authors and Affiliations

  1. Department of Human and Animal Physiology, Moscow State University, 119234, Moscow, Russia

    T. S. Filatova & D. V. Abramochkin

Authors
  1. T. S. Filatova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. V. Abramochkin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. S. Filatova.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note.

Allerton Press remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Filatova, T.S., Abramochkin, D.V. Physiological Effects of Polycyclic Aromatic Hydrocarbons in Fish Organisms. Moscow Univ. Biol.Sci. Bull. 78, 115–127 (2023). https://doi.org/10.3103/S0096392523700013

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0096392523700013

Keywords:

Search

Navigation