Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The Catalase Activity of the Red Alga Ceramium virgatum Roth, 1797 as a Marker of the Quality of the Marine Environment Based on the Example of the Coastal Zone of Southwestern Crimea

  • 5 Accesses


This study determined the range of conditionally normal values of the catalase activity (СA) in the Black Sea red macroalga Ceramium virgatum. The level of CА in the alga corresponded to its conditionally normal functioning (26.79 ± 10.32 μg H2O2/(g wet weight min)). The minimum concentrations of hydrochemical parameters that correspond to the sensitivity threshold of CА in C. virgatum were found; these minimum values are 40 μM/L for organic nitrogen, 0.03 μM/L for nitrites, 0.3 μM/L for nitrates, 0.12 μM/L for inorganic phosphorus, and 0.47 μM/L for organic phosphorus.

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

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.


  1. 1

    Baranov, E.E., Phosphorus compound transformation observation evidence from water ponds of the Volga river basin, Samar. Luka: Probl. Reg. Global’noi Ekol., 2014, vol. 23, no. 3, pp. 160–166.

  2. 2

    Bel’cheva, N.N., Slobodenyuk, A.F., Shul’kin, V.M., et al., Comparative evaluation of antioxidant protection in three populations of mussels from contaminated and clean waters, in Materialy nauchoi konferentsii “Sovremennye problemy fiziologii i biokhimii vodnykh organizmov” (Proc. Sci. Conf. “Modern Problems of the Physiology and Biochemistry of Aquatic Organisms”), September 11–14, 2007, Petrozavodsk, 2007, pp. 20–21.

  3. 3

    Berezov, T.T., Rukovodstvo k laboratornym zanyatiyam po biologicheskoi khimii (Guide to Laboratory Studies in Biological Chemistry), Moscow: Meditsina, 1976, pp. 81–83.

  4. 4

    Vorobeychik, E.L., Environmental regulation: towards a generalizing theory, in Ekologicheskoe normirovanie i upravlenie kachestvom pochv i zemel’ (Environmental Regulation and Quality Management of Soils and Lands), Moscow: NIA-Priroda, 2013, pp. 29–38.

  5. 5

    Gapochka, L.D., Ob adaptatsii vodoroslei (On the Adaptation of Algae), Moscow: Mosk. Gos. Univ., 1981.

  6. 6

    Israel, Yu.A., Ekologiya i kontrol’ sostoyaniya prirodnoi sredy (Ecology and Environmental Monitoring), Leningrad: Gidrometeoizdat, 1979.

  7. 7

    Kutsenko, S.A., Osnovy toksikologii (The Basics of Toxicology), St. Petersburg: Foliant, 2004.

  8. 8

    Lukyanova, O.N., Molecular biomarkers in ecological monitoring of marine ecosystems, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2003, vol. 133, pp. 271–281.

  9. 9

    Makarov, O.A., Ecological rationing of the quality of the environment and soils, in Ekologicheskoe normirovanie i upravlenie kachestvom pochv i zemel’ (Environmental Regulation and Quality Management of Soils and Lands), Moscow: NIA-Priroda, 2013, pp. 82–92.

  10. 10

    Mil’chakova, N.A., Aleksandrov, V.V., Bondareva, L.V., et al., Morskie okhranyaemye akvatorii Kryma: nauchnyi spravochnik (Marine Protected Waters of the Crimea: A Scientific Guide), Simferopol: Nizhnyaya Orianda, 2015.

  11. 11

    Mil’chakova, N.A. and Shakhmatova, O.A., Catalase activity of the widely-distributed macroalgae of the Black Sea by gradient of the sewage pollution, Morsk. Ekol. Zh., 2007, vol. 6, no. 2, pp. 44–57.

  12. 12

    Ovsyany, E.I., Romanov, A.S., Minkovskaya, R.Ya., et al., Main sources of pollution of the marine environment of the Sevastopol region, in Ekologicheskaya bezopasnost’ pribrezhnoi i shel’fovoi zon i kompleksnoe issledovanie resursov shel’fa (Ecological Safety of Coastal and Shelf Zones and a Comprehensive Study of Shelf Resources), Sevastopol: EKOSI-Gidrofizika, 2001, no. 2, pp. 138–152.

  13. 13

    Sapozhnikov, V.V., Metody gidrokhimicheskikh issledovanii osnovnykh biogennykh elementov (Methods of Hydrochemical Studies of the Main Biogenic Elements), Moscow: VNIRO, 1988.

  14. 14

    Smolkin, V.P., Application of ecological standards system for assessment of an ecological development level of an enterprise, Teor. Prakt. Obshchestv. Razvit., Ser.: Ekon. Nauki, 2014, no. 1, pp. 381–383.

  15. 15

    Tkachenko, F.P., Sitnikova, Yu.A., and Kutsin, O.B., Antioxydant system elements of seaweeds from the Black Sea regions with different rate of pollution, Ekol. Morya, 2004, vol. 65, pp. 70–74.

  16. 16

    Fedorov, V.D., Maksimov, V.N., and Sakharov, V.B., A quantitative method for assessing external influences on ecological systems, in Chelovek i Biosfera (Man and the Biosphere), Moscow: Mosk. Gos. Univ., 1980, no. 5, pp. 12–23.

  17. 17

    Shakhmatova, O.A., The activity of the antioxidant system of some Black Sea hydrobionts in the coastal waters of Sevastopol, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Sevastopol, 2004.

  18. 18

    Shakhmatova, O.A., The response of hydrobionts to stress factors of marine ecosystems, in Ekosist., Ikh Optim. Okhr., 2012, no. 7, pp. 98–113.

  19. 19

    Shakhmatova, O.A. and Milchakova, N.A, The influence of environmental conditions on the catalase activity of Black Sea algae mass, Al’gologiya, 2014, vol. 24, no. 4, pp. 461–476.

  20. 20

    Shakhmatova, O.A. and Parchevskaya, D.S., Catalase activity and water quality control, Al’gologiya, 2000, vol. 10, no. 3, pp. 355–361.

  21. 21

    Amano, H. and Noda, H., Effect of nitrogenous fertilizers on the recovery of discoloured fronds of Porphyra yezoensis,Bot. Mar., 1987, vol. 30, no. 6, pp. 467–473.

  22. 22

    Carmona, R., Kraemer, G.P., and Yarish, C., Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish–algal aquaculture system, Aquaculture, 2006, vol. 252, no. 1, pp. 54–65.

  23. 23

    Carocho, M. and Ferreira, I.C.F.R., A review on antioxidants, prooxidants and related controversy: Natural and synthetic compounds, screening and analysis methodologies and future perspectives, Food Chem. Toxicol., 2013, vol. 51, pp. 15–25.

  24. 24

    Dahlhoff, E.P., Biochemical indicators of stress and metabolism: Applications for marine ecological studies, Annu. Rev. Physiol., 2004, vol. 66, pp. 183–207.

  25. 25

    Dondero, F. and Calisi, A., Evaluation of pollution effects in marine organisms: “Old” and “new generation” biomarkers, in Coastal Ecosystems: Experiences and Recommendations for Environmental Monitoring Programs, New York: Nova Science, 2015, pp. 143–192.

  26. 26

    Haines, K.C. and Wheeler, P.A., Ammonium and nitrate uptake rates of the seaweeds Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta), J. Phycol., 1978, vol. 14, no. 3, pp. 319–324.

  27. 27

    Kim, D.I., Matsubara, T., Oh, S.J., et al., Effects of nitrogen and phosphorus sources on the utilization and growth kinetics of the harmful dinoflagellate Cochlodinium polykrikoides isolated from Yatsushiro Sea, Japan, Nippon Suisan Gakkaishi, 2007, vol. 73, no. 4, pp. 711–717.

  28. 28

    Martinez, B. and Rico, J.M., Seasonal variation of P content and major N pools in Palmaria palmata (Rhodophyta), J. Phycol., 2002, vol. 38, no. 6, pp. 1082–1089.

  29. 29

    Mearns, A.J., Reish, D.J., Oshida, P.S., et al., Effects of pollution on marine organisms, Water Environ. Res., 2013, vol. 85, no. 10, pp. 1718–1816.

  30. 30

    Miflin, B.J. and Habash, D.Z., The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops, J. Exp. Bot., 2002, vol. 53, no. 370, pp. 979–987.

  31. 31

    Nausch, M., Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea), Aquat. Microb. Ecol., 1998, vol. 16, pp. 87–94.

  32. 32

    Oh, S.J., Kwon, H.K., Noh, I.H., and Yang, H.-S., Dissolved organic phosphorus utilization and alkaline phosphatase activity of the dinoflagellate Gymnodinium impudicum isolated from the South Sea of Korea, Ocean Sci. J., 2010, vol. 45, no. 3, pp. 171–178.

  33. 33

    Pereira, R., Kraemer, G., Yarish, C., and Sousa-Pinto, I., Nitrogen uptake by gametophytes of Porphyra dioica (Bangiales, Rhodophyta) under controlled-culture conditions, Eur. J. Phycol., 2008, vol. 43, no. 1, pp. 107–118.

  34. 34

    Perez-Garcia, O., Escalante, F.M.E., de-Bashan, L.E., and Bashan, Y., Heterotrophic cultures of microalgae: Metabolism and potential products, Water Res., 2011, vol. 45, no. 1, pp. 11–36.

  35. 35

    Peters, L.D., Porte C., Albaigés, J., and Livingstone, D.R., 7-ethoxyresorufin O-deethylase (EROD) and antioxidant enzyme activities in larvae of sardine (Sardina pilchardus) from the north coast of Spain, Mar. Pollut. Bull., 1994, vol. 28, no. 5, pp. 299–304.

  36. 36

    Schaffelke, B., Surface alkaline phosphatase activities of macroalgae on coral reefs of the central Great Barrier Reef, Australia, Coral Reefs, 2001, vol. 19, no. 4, pp. 310–317.

  37. 37

    Torres, M.A., Barros, M.P., Campos, S.C.G., et al., Biochemical biomarkers in algae and marine pollution: A review, Ecotoxicol. Environ. Saf., 2008, vol. 71, no. 1, pp. 1–15.

  38. 38

    Wang, C., Lei, A., Zhou, K., et al., Growth and nitrogen uptake characteristics reveal outbreak mechanism of the opportunistic macroalga Gracilaria tenuistipitata,PloS One, 2014, vol. 9, no. 10, art. ID e108980. https://doi.org/10.1371/journal.pone.0108980

  39. 39

    Yamaguchi, H., Sakamoto, S., and Yamaguchi, M., Nutrition and growth kinetics in nitrogen- and phosphorus-limited cultures of the novel red tide flagellate Chattonella ovata (Raphidophyceae), Harmful Algae, 2008, vol. 7, pp. 26–32.

Download references


The authors are grateful to N.Yu. Rodionova for the provided data on hydrochemical studies and to D.S. Parchevskaya for her help with mathematical processing and data analysis.


The studies were carried out as part of the state assignment of the Kovalevsky Institute of Marine Biological Research, Russian Academy of Sciences, on the theme Regularities of Formation and Anthropogenic Transformation of Biodiversity and Biological Resources of the Azov-Black Sea Basin and Other Regions of the World Ocean, the State Registration Number AAAA-A18-118020890074-2.

Author information

Correspondence to O. A. Shakhmatova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by I. Barsegova

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shakhmatova, O.A., Kovardakov, S.A. The Catalase Activity of the Red Alga Ceramium virgatum Roth, 1797 as a Marker of the Quality of the Marine Environment Based on the Example of the Coastal Zone of Southwestern Crimea. Russ J Mar Biol 45, 436–442 (2019). https://doi.org/10.1134/S1063074019060087

Download citation


  • The Black Sea
  • Ceramium virgatum
  • catalase activity
  • biomarker
  • hydrochemical parameters
  • sensitivity threshold
  • conditional norm