Abstract
The ecological state assessment of the two areas in the Sea of Azov (Temryuk and Yasensky Bays) was carried out using morphophysiological (hepatosomatic and gonadosomatic indices) and biochemical parameters (activity of antioxidant enzymes (superoxide dismutase, catalase), aminotransferases, cholinesterase, level of oxidized proteins, and lipid peroxidation), as well as the toxicological parameters in the liver of round goby Neogobius melanostomus. The results of the biochemical analysis allowed to establish a shift of the prooxidant-antioxidant reactions towards the processes of protein oxidation, also an increase of aminotransferase activities in the fish liver from Temryuk Bay compared to similar indicators in fish from Yasensky Bay. At the same time, the average values of length and weight as well as the gonadosomatic index were found significantly lower, while the hepatosomatic index significantly higher in fish from Temryuk Bay as compared to similar indices of fish from Yasensky Bay. Analysis of the biochemical and morphophysiological parameters of round goby from the two locations demonstrates less favorable ecological state of the Temryuk Bay that fully agrees with the results of the elementary analysis in the fish liver. Studied parameters can be used in the ecological monitoring of the natural surroundings of this species and the areas beyond.
Similar content being viewed by others
Data availability
Not applicable.
References
Abdel-Hameid N-AH (2007) Physiological and histopathological alterations induced by phenol exposure in Oreochromis aureus juveniles. Turkish J Fish Aquat Sci 7(2):131–138. https://www.trjfas.org/uploads/pdf_323.pdf
Al-Ghais SM (2013) Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 74(1):183–186. https://doi.org/10.1016/j.marpolbul.2013.07.005
Bacchetta C, Rossi A, Ale A, Campana M, Parma MJ, Cazenave J (2014) Combined toxicological effects of pesticides: a fish multi-biomarker approach. Ecol Indic 36:532–538. https://doi.org/10.1016/j.ecolind.2013.09.016
Bacevicius E (2004) The new data on ecology of alien fish species and fish metazoan parasites in the Curonian Lagoon and Lithuanian coastal zone. Baltic — the Sea of Aliens. Book of abstracts. Gdynia, Poland, pp 17–18
Bell JG, Cowey CB (1989) Digestibility and bioavailability of dietary selenium from fishmeal, selenite, selenomethionine and selenocystine in Atlantic salmon (Salmo salar). Aquaculture 81(1):61–68. https://doi.org/10.1016/0044-8486(89)90230-5
Biernaczyk M, Opanowski A, Neja Z, Stepanowska K (2010) The emergence of invasive species – round goby Neogobius melanostomus (Pallas, 1811) in Dabie Lake. In: Natural and Anthropological Transformation of Lakes, Proc Nat Conf, Szczecin-Stare Drawsko, pp 10
Bugayov LA, Zinchuk OA, Smir TM, Rudnitskaya OA, Voykina AV (2012) Hematological parameters of round goby (Neogobius melanostomus, Pallas, 1814) from the Sea of Azov. Bull Higher Educ Inst North-Caucasus Reg Nat Sci 1:73–76 ((in Russian))
Bufetova MV (2018) Estimation of heavy metal fluxes (Pb, Cd) in the abiotic components of the Azov Sea ecosystem. Reg Environ Iss 4:70–73. (In Russia) https://doi.org/10.24411/1728-323X-2018-14070
CCAC (2005) Canadian Council on Animal Care guidelines on: the care and use of fish in research, teaching and testing. Canadian Council on Animal Care, Ottawa https://ccac.ca/Documents/Standards/Guidelines/Fish.pdf
Charlebois PM, Marsden JE, Goettel RG, Wolf RK., Jude DJ, Rudnika S (1997) The round goby, Neogobius melanostomus (Pallas): a review of European and North American literature. Illinois Natural History Survey Special Publication 20:1–76. https://archive.org/details/roundgobyneogobi20unse/page/n1/mode/2up?view=theater
Ciepielewski W, Hornatkiewicz-Zbik A (2003) The diversity of ichthyofauna in Lakes Slowinski National Park. Komunikaty Rybackie 2:22–26
Corkum LD, Sapota MR, Skóra KE (2004) The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol Invasions 6(2):173–181. https://doi.org/10.1023/B:BINV.0000022136.43502.db
Diripasko OA, Zabroda TA (2017) Morphometric variability in round goby Neogobius melanostomus (Perciformes: Gobiidae) from the Sea of Azov. Zoosyst Ross 26(2):392–405. https://doi.org/10.31610/zsr/2017.26.2.392
Dubinina EE, Burmistov SO, Khodov DA, Porotov IG (1995) Oxidative modification of human serum proteins. A method of determining it. Vopr Med Khim 1:24–26 ((in Russian))
Fiser B, Jójárt B, Csizmadia IG, Viskolcz B (2013) Glutathione – hydroxyl radical interaction: A theoretical study on radical recognition process. PLoS ONE 8(9):e73652. https://doi.org/10.1371/journal.pone.0073652
Gad NS (2009) Determination of glutathione related enzymes and cholinesterase activities in Oreochromis niloticus and Clarias gariepinus as bioindicator for pollution in Lake Manzala. Glob Vet 3(1):37–44. http://www.idosi.org/gv/gv3(1)09/7.pdf
Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso G (2018) Supplementation of vitamins, minerals, enzymes and antioxidants in fish feeds. In: Feeds for the Aquaculture Sector. Current Situation and Alternative Sources. Springer, Cham, pp 63–103. https://doi.org/10.1007/978-3-319-77941-6_4
Guide for the care and use of laboratory animals (2011) 8th edition. National Academy of Sciences. National Academies Press, Washington, DC
Huang DJ, Zhang YM, Song G, Long J, Liu JH, Ji WH (2007) Contaminants-induced oxidative damage on the carp Cyprinus carpio collected from the Upper Yellow River, China. Environ Monit Assess 128:483–488. https://doi.org/10.1007/s10661-006-9341-3
Jamakala O, Rani UA (2012) Protective role of trace elements against cadmium induced alterations in the selected oxidative stress enzymes in liver and kidney of fresh water teleost, Oreochromis mossambicus (Tilapia). Int J Pharm Pharm Sci 4(suppl. 5):303–310. https://innovareacademics.in/journal/ijpps/Vol4Suppl5/4957.pdf
Jude DJ, Reider RH, Smith GR (1992) Establishment of Gobiidae in the Great Lakes basin. Can J Fish Aquat Sci 49(2):416–421. https://doi.org/10.1139/f92-047
Karapetyan OS, Pavlenko LF, Korotkova LI, Korablina IV, Tsema NI (2012) Influence of accumulation of priority toxicants in the liver of the round goby Neogobius melanostomus from the Sea of Azov on morphometric and molecular biomarkers of this fish species. Modern Problems of Science and Education. Surgery 1. Accessed 3 June 2021 (in Russian) http://www.science-education.ru/101-5429
Karlson AML, Almqvist G, Skora KE, Appelberg M (2007) Indications of competition between non-indigenous round goby and native flounder in the Baltic Sea. ICES J Mar Sci 64(3):479–486. https://doi.org/10.1093/icesjms/fsl049
Kodukhova YuV, Borovikova EA, Ezhova EE, Gushchin AV (2017) Features of the morphology of round goby (Neogobius melanostomus) in the South-Eastern Baltic Sea. Reg Ecol 3:65–74 ((in Russian))
Kornienko GG, Dudkin SI, Sergeeva SG, Ruzhinskaya LP, Tsema NI, Bugaev LA, Voykina AV (2017) Physiological and biochemical characteristics of the Azov and Black Sea fishes undergoing anthropogenic pressure. Vestnik KamchatSTU 40:58–66. https://doi.org/10.17217/2079-0333-2017-40-58-66 ((in Russian))
Kornis MS, Mercado-Silva N, Vander Zander MJ (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80(2):235–285. https://doi.org/10.1111/j.1095-8649.2011.03157.x
Korolyuk MA, Ivanova LI, Mayorova IG, Tokarev VE (1988) Method for assaying catalase activity. Lab Delo 1:16–19 ((in Russian))
Korotaeva SE, Shagalyeva SR (2013) To the characteristics of round goby as invasive species in Votkinsk reservoir. Bull Perm Univ 1:28–31 ((in Russian))
Kovyrshina TB (2017) The Application of Biomarkers of a Round Goby Neogobius melanostomus (Pallas, 1814) for the ecological assessment of coastal waters of the Black Sea and Sea of Azov. Candidate Dissertation, A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS (in Russian)
Kovyrshina TB, Boldirev DA, Omelchenko SO (2012) Studies of long-term changes in the activity of antioxidant enzymes in blood of round-goby from Azov Sea depending on the toxic elements content in the tissues. Vet Med 96:294–296 ((in Russian))
Kovyrshina TB, Rudneva II (2016) The effects of coastal water pollution of the Black Sea on the blood biomarkers of the round goby Neogobius melanostomus Pallas, 1811 (Perciformes: Gobiidae). Russ J Mar Biol 42(1):58–64. https://doi.org/10.1134/S1063074016010132
Kovyrshina TB, Rudneva II (2012) Seasonal dynamics of activity of oxidative modification of proteins and oxidation-inhibiting enzymes in the blood of goby Neogobius melanostomus inhabiting the Black Sea and the Sea of Azov. J Ichthyol 52(4):277–283. https://doi.org/10.1134/S0032945212020099
Kovyrshina TB, Rudneva II (2018) The response of blood biomarkers of the round goby Neogobius melanostomus (Pallas, 1814) (Perciformes: Gobiidae) to chronic coastal pollution in the Sea of Azov. Russ J Mar Biol 44(4):328–333. https://doi.org/10.1134/S1063074018040065
L’avrinčiková M, Kováč V, Katina S (2005) Ontogenetic variability in external morphology of round goby Neogobius melanostomus from Middle Danube. Slovakia J Appl Ichthyol 21(4):328–334. https://doi.org/10.1111/j.1439-0426.2005.00677.x
Lopes DFC, Assis CRD, Sant’Anna MCS, Silva JF, Souza Bezerra R, Frédou FL (2019) Brain acetylcholinesterase of three perciformes: From the characterization to the in vitro effect of metal ions and pesticides. Ecotoxicol Environ Saf 173(1):494–503. https://doi.org/10.1016/j.ecoenv.2019.02.047
Matishov GG, Bufetova MV, Egorov VN (2017) The regulation of heavy metals into the Sea of Azov according to the intensity of sedimentation of water self-purification. Sci South Russia 13(1):44–58. https://doi.org/10.23885/2500-0640-2017-13-1-44-58 ((in Russian))
Mineev AK (2013a) Rejections in haematological parameters of Neogobius melanostomus (Pallas, 1814) of Saratov reservoir. Izvestia Samara Sci Center Russ Acad Sci 15(3):222–228 ((in Russian))
Mineev AK (2013b) Pathologies of some organs of the round goby (Neogobius melanostomus Pallas, 1814) of the Saratov reservoir. Vestnik Lobachevsky Univ Nizhni Novgorod 4(1):153–157 ((in Russian))
Moskalkova КI (1996) Ecological and morpho-physiological prerequisites for the expansion of the range of round goby Neogobius melanostomus in the conditions of anthropogenic pollution of water bodies. J Ichthyol 36(5):615–621 ((in Russian))
Musaev BS, Muradova GR, Rabadanova AI (2009) Influence of cadmium and lead ions on some parameters of lipid metabolism and the antioxidant defense system of carp fingerlings (Cyprinus carpio L.). The South of Russia: Ecology, Development 1:44–54 ((in Russian))
Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochim Biophys Res Commun 46(2):849–854. https://doi.org/10.1016/s0006-291x(72)80218-3
Powell SR (2000) The antioxidant properties of zinc. J Nutr 130(5):1447–1454. https://doi.org/10.1093/jn/130.5.1447s
Pravdin IF (1966) Guide to the fish study. Pischevaya promishlennost, Moscow (in Russian)
Rudneva II, Kovyrshina TB (2015) Comparative study of the cholinesterase activities in tissues of the round goby Neogobius melanostomus (Gobiidae) from different locations of the Black and Azov Seas. J Ichthyol 55(5):734–738. https://doi.org/10.1134/S0032945215050148
Shakirova FM, Severov YuA, Latypova VZ (2015) Modern composition of alien fish species in Kuybyshev reservoir and possible introduction of new representatives into its ecosystem. Russ J Biol Invasions 6(4):278–291. https://doi.org/10.1134/S2075111715040050 ((in Russian))
Skóra KE, Stolarski J (1993) New fish species in the Gulf of Gdansk: Neogobius sp. (cf. Neogobius melanostomus) (Pallas 1811). Bull Sea Fish Inst 1(128):83–84
Skugoreva SG, Ashihmina TYa, Fokina AI, Lyalina EI (2016) Chemical groups of toxic effect of heavy metals (review). Theor Prikl Ekol 14–13. (in Russian) https://doi.org/10.25750/1995-4301-2016-1-014-019
Skuratovskaya EN, Kovyrshina TB, Chesnokova II (2019) Influence of Cryptocotyle spp. metacercariae (Creplin, 1825) on some biochemical parameters of round goby Neogobius melanostomus (Pallas, 1814). Bull Eur Ass Fish Pathol 39(1):24–30. https://eafp.org/download/2019-volume39/issue_1/39-1-024-skuratovskaya.pdf
Skuratovskaya EN, Kovyrshina TB, Rudneva II (2017) A comparative study of long-term pollution effects of marine waters on the blood biomarkers of two benthic fish species: the scorpion fish Scorpaena porcus (Linnaeus, 1758) and the round goby Neogobius melanostomus (Pallas, 1814) from the Black Sea. Russ J Mar Biol 43(3):232–238. https://doi.org/10.1134/S1063074017030105
Stalnaya ID, Garishvili TG (1977) Method for determination of malonic dialdehyde using thiobarbituric acid. In: Orechovich VN (ed) Current Methods in Biochemistry. Medicine Publ, Moscow, pp 66–68 ((in Russian))
Stanic B, Andric N, Zoric S, Grubor-Lajsic G, Kovacevic R (2006) Assessing pollution in the Danube River near Novi Sad (Serbia) using several biomarkers in Sterlet (Acipenser ruthenus L.). Ecotox Environ Safe 65(3):395–402. https://doi.org/10.1016/j.ecoenv.2005.08.005
Suzuki KT, Kuroda T (1994) Direct transfer of copper from metallothionein to superoxide dismutase: a possible mechanism for differential supply of Cu to SOD and ceruloplasmin in LEC rats. Res Commun Mol Pathol Parmacol 86(1):15–23
Tkachenko H, Kurhaluk N, Grudniewska J (2013) Effects of chloramine-T exposure on oxidative stress biomarkers and liver biochemistry of rainbow trout, Oncorhynchus mykiss (Walbaum), brown trout, Salmo trutta (L.), and grayling, Thymallus thymallus (L.). Arch Pol Fish 21(1):41–51. https://doi.org/10.2478/aopf-2013-0005
Udotong JIR (2015) Assessment of diagnostic enzymes as indices of heavy metal pollution in Tilapia fish. IJBB 9(6):670–674. https://doi.org/10.5281/zenodo.1107483
Acknowledgements
The authors are very grateful to the Azov-Black Sea branch of the Russian Federal Research Institute of Fisheries and Oceanography for providing round goby samples.
Funding
This work was conducted under financial support of the Russian Academy of Science research grant № 121030100028–0.
Author information
Authors and Affiliations
Contributions
Tatyana Sigacheva carried out biological, biochemical, and statistical analyzes, analyzed the data, wrote the manuscript, and approved the final version of the manuscript. Ekaterina Skuratovskaya carried out biochemical and statistical analyzes, analyzed the data, wrote the manuscript, and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
All applicable international, national, and/or institutional guidelines for the care and use of animals have been followed. This work does not contain the results of any studies involving people as research objects.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Bruno Nunes
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sigacheva, T., Skuratovskaya, E. Application of biochemical and morphophysiological parameters of round goby Neogobius melanostomus (Pallas, 1814) for assessment of marine ecological state. Environ Sci Pollut Res 29, 39323–39330 (2022). https://doi.org/10.1007/s11356-022-18962-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-18962-0