Skip to main content
Log in

Application of biochemical and morphophysiological parameters of round goby Neogobius melanostomus (Pallas, 1814) for assessment of marine ecological state

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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))

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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))

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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))

    Google Scholar 

  • 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))

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Korolyuk MA, Ivanova LI, Mayorova IG, Tokarev VE (1988) Method for assaying catalase activity. Lab Delo 1:16–19 ((in Russian))

    Google Scholar 

  • 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))

    Google Scholar 

  • 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))

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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))

    Article  Google Scholar 

  • 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))

    Google Scholar 

  • 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))

    Google Scholar 

  • 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))

    Google Scholar 

  • 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))

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Powell SR (2000) The antioxidant properties of zinc. J Nutr 130(5):1447–1454. https://doi.org/10.1093/jn/130.5.1447s

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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))

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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))

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

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

Authors

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

Correspondence to Ekaterina Skuratovskaya.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-18962-0

Keywords

Navigation