Interspecies Peculiarities of Biomarkers Response of Marine Fish Embryos to Oil Pollution

Document Type : Original Research Paper

Author

Marine Hydrophysical Institute, 299011 Sevastopol, Kapitanskaya st., 2, Russia

10.22059/poll.2022.345522.1530

Abstract

Shelf areas of the seas and oceans characterizing high productivity are the spawning sites of many aquatic organisms. However, they are strong impacted for anthropogenic pollution, including oil contamination, which negatively influence on marine organisms. The effects of mazut and diesel fuel in the concentrations of 0.05, 0.1 and 0.2 ml/l on the activity of antioxidant enzymes which are recognized as biomarkers of the oxidative stress namely superoxide dismutase (SOD), catalase (CAT), peroxidase (PER) and glutathione reductase (GR) in the developing embryos of two marine blennies Parablennius sanguinolentus and Salaria pavo (Perciformes: Blenniidae) on the V - VI developmental stages were studied. The results demonstrated higher mazut toxicity as compared with diesel fuel. In P. sanguinolentus embryos exposed to mazut the activity of key anti-oxidant  enzymes SOD and CAT were significantly higher (+413% and +100% as  compared with the control, p<0.05), while in the case of diesel fuel the enzymes level varied insignificantly. In the embryos of S. pavo SOD and CAT activities were also increased at mazut incubation (256% and 103% respectively, p<0.05), while the differences between enzymes level in embryos exposed to diesel fuel were lower. In contaminated S. pavo embryos enzyme activities varied less as compared with the embryos of P. sanguinolentus, therefore they are more resistant and adaptive to oil contamination. The possible mechanisms of fish embryos antioxidant system response to oil pollution are discussed.

Keywords


Adams. H., Ojeda-Castillo, V., Guzmán-Osorio, F., Álvarez-Coronel, G. and Domínguez-Rodríguez, V.I.  (2020). Human health risks from fish consumption following a catastrophic gas oil spill in the Chiquito River, Veracruz, Mexico. Environ. Monitor. Ass., 192, Article 83795 https://doi.org/10.1007/s10661-020-08742-zh 
de Andrade Brito, I., Garcia, J.R.E., Salaroli, A.B., Figueira, R.C.L., de Castro Martins, C., Neto, A.C., Gusso-Choueri, P.K., Choueri, R.B., Borges, S., Araujo, L. and de Oliveira Ribeiro, C.A. (2018). Embryo toxicity assay in the fish species Rhamdia quelen (Teleostei, Heptaridae) to assess water  quality in the Upper Iguacu basin (Parana, Brazil). Chemosphere, 208, 207–218. 
 https://doi.org/10. 1016/j.chemosphere.2018.05.009
Beiraoa, J., Baillonc, L., Litt, M.A., Langlois, V. and Purchas, C. (2019). Impact of crude oil and the dispersant Corexit™ EC9500A on capelin (Mallotus villosus) embryo development. Marine Environ. Res., 147, 90–100. https://doi.org/10.1016/j.marenvres.2019.04.004
Bender, M.L., Giebichenstein, V., Teisrud, R.N., Fantzen, M., Meador, J.P., Sørensen, L.,    Hansen, B.H., Reinardy, H.C., Laurel, B. and Nahrgang, J.  (2021). Combined effects of crude oil exposure and  harming on eggs and larvae of an arctic forage. Sci. Rep., 11, Article number 8410 
https://doi.org/10.1038/s41598-021-87932-2 - 7
Beyer, J., Trannum, H.C., Bakke, T., Hodson, P. and Collier, T. (2016). Environmental effects of the Deepwater Horizon oil spill: A review. Mar.  Pollut. Bull. 110 (1), 28-51.      http://creativecommons.org/licenses/by-nc-nd/4.0
Brette, F., Machado, B., Cros, C., Scholz, M.L. and  Block, B.A. (2014). Crude oil impairs cardiac excitation–contraction coupling in fish. Science, 343, 772–776. DOI: 10.1126/science.1242747  
Chesalina, T.L., Rudneva, I.I. and Kuzminova, N.S. (2000). Toxic effects of diesel on the fry of Black Sea  Liza saliens. J. Ichthyol., 40, 429–432. ( in  Russian)
Córdova de la Cruz,   S.E., Martínez‑Bautista, G., Peña‑Marín, E.S., Martínez‑García, R.,  
Núñez‑Nogueir, G.,  Adams, R.H.,  Burggren, W. W. and Alvarez‑González, C.A. (2022).      Morphological and cardiac alterations after crude oil exposure in the early-life stages      of the tropical gar (Atractosteus tropicus). Environ. Sci. Pollut. Res.,29, 22281–22292.  https://doi.org/10.1007/s11356-021-17208
Crower, M., Newton, J.C., Kaltenboeck, B. and  Johnson, C.  (2014). Oxidative stress responses of gulf killifish exposed to hydrocarbons from the deepwater horizon oil spill: potential implications for aquatic food resources. Environ. Toxicol. Chem., 33, 370–374. 
https://doi.org/10.1002/etc.2427 
Dechnik, T.V. (1973). Black Sea Ichthyoplankton. (Kiev: Naukova Dumka). 235 pp. 
Dubansky, B., Whitehead, A., Miller, J.T., Rice, C.D. and Galvez, F.  (2014). Response to comment on “Multitissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident gulf killifish (Fundulus grandis)” Environ. Sci. Tech., 48, 7679–7680. https://doi.org/10.1021/es400458p         
Geraudie, P., Bakkemo, R., Milinkovitch, T. and Thomas-Guyon, H. (2016). First evidence of  marine  diesel effects on  biomarker responses in  the Icelandic scallops, Chlamys islandica.     Environ. Sci,  Pollut. Res., 23, 16504–16512    
Goldberg, D.M. and Sparner, R.J. (1987). Glutathione reductase. (In: Bergmeyer, H.U., Bergmeyer, J., Grab, M.  (Eds) Methods of Enzymatic Analysis.  (pp.258–265). Weinheim; Verlag Chemic.
Halafian, A.A. (2008). Statistica 6. Chapter 8.( Moscow; Binom Publ). pp.133–152.
Incardona, J.P., Linbo, T.L. and Scholz, N.L. (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, 242–249. 
https://doi.org/10.1016/j.taap.2011.09.010
Jiang, M., Li, L., Shen, G. and Shen, X. (2017). Oxidative  stress in shellfish Sinonovacula  constricta  exposed to the water accommodated fraction of zero sulfur diesel oil and pinghu crude oil. Arch. Environ. Contam. Toxicol., 73 ( 2), 294-300.  https://doi.org/10.1007/s00244-017-0391-z
Jin, J., Kurobe, T., Hammock, B.G., Lam, Ch.H., Lim, L. and Ther S. J. (2020). Toxic effects of fluridone on   early developmental stages of Japanese Medaka (Oryzias latipes).  Sci. Total  Environ., 700, Article N 134495 https://doi.org/10.1016/j.scitotenv.2019.134495
Johann, S., Mueller, L. M. and Seiler, Th.-B.  (2019). Differences in biomarker and behavioral responses to native and chemically dispersed crude and refined fossil oils in zebrafish early life tages Sci. Total Environ., 709, Article N 136174  https://doi.org/10.1016/j.scitotenv.2019.136174
Klinger, D.H., Dale, J.J., Machado, B.E., Incardona, J.P., Farwell Ch. J. and Block, B.A. (2015). Exposure to   Deepwater Horizon weathered crude oil increases routine metabolic demand in chub  mackerel, Scomber japonicas. Mar. Pollut. Bull., 98 (1-2), 259-266 
https://doi.org/10.1016/j.marpolbul.2015.06.039
Leonov, A.V. and Fashuk, D.Y. (2006). Biotransformation of oil hydrocarbons in Karkinite Bay in Black Sea: the evaluation as the result of mathematics simulation. Water Res., 33(3), 311– 326. 
Litvin, F.F. (1981). Laboratory manual of physicochemical methods in biology. Moscow: Moscow State University: (in Russian)
Martınez-Gomez, C., Vethaak, A. D., Hylland, K., Burgeot, T, Kohler, A., Lyons, B. P., Thain, J., Gubbins, M. J. and Davies, I.M. (2010). A guide to toxicity assessment and monitoring effects at lower levels of biological organization following marine oil spills in European waters.  ICES J. Mar. Sci.,  67, 1105–1118. https://doi.org/10.1093/icesjms/fsq017  
Mazmanidi, N. (1997).  Black Sea fish  ecology and oil. Batumy; Adsgara, 147 pp. 
Mu, X., Liu, J., Yang, K., Huang, Y., Li, X., Yang, W., Oi, S., Tif, W., Shen, G. and Li, Y. (2018). 0#Diesel water-accommodated fraction induced lipid homeostasis alteration in zebrafish embryos. Environ.  Pollut., 242(4),52–961. https://doi.org/10.1016/j.envpol.2018.07. 055
Muhling, B.A., Roffer, M.A., Lamkin, J.T, .Ingrajr, GW, .Upton, MA, Gawlikowski, G F.Muller-Karger, F., S.Habtes, S. and .Richards, W.J. (2012). Overlap between Atlantic bluefin tuna spawning grounds  and observed Deepwater Horizon surface oil in the northern Gulf of Mexico. Mar. Pollut. Bull., 64, 679–687.  https://doi.org/10.1016/j.marpolbul.2012.01.034
Nishikimi, M, Rao, N.A. and Yagik, K. (1972). The occurrence of superoxide anion in the reaction of reduced phenazine. Biochem. Biophys. Res. Comm., 46(2), 849–854
Pasparakis, C.,  Esbaugh, A.J., Burggren, W. and Crosel, M. (2019). Physiological impacts of Deepwater  Horizon oil on fish. Comp. Biochem. Physiol. Part C. Toxic. Pharmacol., 224, 108558 https://doi.org/10.1016/j.cbpc.2019.06.002
Patin, S.A. (2015). Marine petroleum-gas complex: factors of ecological risk. Security of      the environment in petroleum-oil complex, 4, 5-12.  ( in  Russian). 
Pereira, T.M., Merc, J., Passos, L.S., Coppo, G.C., Lopes, T.O.M., Cabral, D.S., Scherer, R. and Chippari- Gomes, A. (2018). Effects of the water soluble fraction of diesel oil (WSD) on the fertilization  and development of a sea urchin (Echinometra lucunter). Ecotox. Environ.  Safety, 162, 59–62. https://doi.org/10.1016/j.ecoenv.2018.06.0400.
Perrichon, P.,  Le Bihanic, F., Bustamante, P., Le Menach, K., Budzinski, H., Cachot, J.  and Cousin, X. (2014). Influence of sediment composition on PAH toxicity using zebrafish (Danio rerio) and Japanese medaka (Oryzias latipes) embryo-larval assays. Environ. Sci. Pollut. Res., 21,13703– 13719  https://doi.org/10.1007/s11356-014-3502-7
Phan, T.C.T., Manuel, A.V., Tsutsui, N. and Yoshimatsu, T. (2020).  Impacts of short-term salinity and turbidity stress on the embryonic stage of red sea bream Pagrus major. Fish Sci., 86:      119– 125. https://doi.org/10.1007/s12562-019-01368-2.   
Rial, D., Beiras, R., Vázquez, J.A. and Murado, M.A.  (2010). Acute Toxicity of a Shoreline Cleaner,  CytoSol, Mixed With Oil and Ecological Risk Assessment of its Use on the Galician Coast. Arch.  Environ. Contamin. Toxicol., 59, 407–416. 
https://doi.org/10.1007/s00244-010-9492-7 
Rooke, J.R., Kitchens, L., Dance, M.A., Wells, D.R.J., Falterman, B. and 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(10), e76080.   
https://doi.org/10.1371/journal.pone.0076080
Rudneva, I.I. (2014). Biomarkers for stress in fish embryos and larvae. Taylor  & Francis  Group; CRC Press. 206 pp. 
Rudneva, I.I. (2019). Use of fish embryo biomarkers for the evaluation of mazut toxicity in marine environment. Int. Aquatic Res., 11,147–157. https://doi.org/10.1007/s40071-019-0225-x 
Samuelsen, A., Daewe, U. and Wettre, C. (2019). Risk of oil contamination of fish eggs and larvae  under different oceanic and weather conditions. ICES J. Mar. Sci., 76(6),1902–1916. https://doi.org/10.1093/icesjms/fsz035 
Sehonova, P., Plhalova, L., Blahova, J., Doubkova, V., Prokes, M., Tichy, F., Fiorino, E.,  Faggio, C. and Svobodova, Z. (2017). Toxicity of naproxen sodium and its mixture with tramadol   hydrochloride on fish early life stages. Chemosphere. 188: 414-423. 
https://doi.org/10.1016/j.chemosphere.2017.08.151  
Stancova, V., Plhalova, L., Blahova, J., Zivna, D., Bartoskova, M., Siroka, Z., Marsalek, P. and Svobodova, Z.  (2017). Effects of the pharmaceutical contaminants ibuprofen, diclofenac, and 
carbamazepine alone, and in combination, on oxidative stress parameters in early life stages     of tench (Tinca tinca). Veter, Med., 62 (2), 90–96.  doi: 10.17221/125/2016-VETMED  
Velisek, J. and Stara, A. (2018). Effect of thiacloprid on early life stages of common carp yprinus carpio). Chemosphere, 194, 481-487. https://doi.org/10.1016/j.chemosphere.2017.11.176 
Van der Oost, R., Beyer, J. and Vermeulen, N.B.E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol., 13(3),57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Zhang, J.F., Wang, X.R., Guo, H.Y., Wu, C. and Xue, Y.Q. (2004). Effects of water-soluble fractions of   diesel oil on the antioxidant defenses of the goldfish Carassius auratus. Ecotoxicol. Environ.  Safety, 58, 110–116. https://doi.org/10.1016/j.ecoenv.2003.08.025