Russian Journal of Marine Biology

, Volume 44, Issue 6, pp 452–457 | Cite as

Erythroid Elements of Hemolymph in Anadara kagoshimensis (Tokunaga, 1906) under Conditions of the Combined Action of Hypoxia and Hydrogen Sulfide Contamination

  • A. A. SoldatovEmail author
  • T. A. Kukhareva
  • A. Y. Andreeva
  • E. S. Efremova


The effect of the combined action of hypoxia (0.05 mg O2/L) and hydrogen sulfide contamination (4–8 mg S2–/L) on the morphometric characteristics of the bivalve mollusk Anadara kagoshimensis (Tokunaga, 1906) was studied under experimental conditions in vivo; the exposure lasted for 24 hours. A significant increase in the size of granular inclusions in cells was observed. The number of these granular inclusions increased by 72–178%, in comparison with the control values (normoxia). The volume of erythrocytes increased by 15–74% and reached 608.1 ± 15.2 μm3 in some individuals. The cells formed aggregates of different shapes and sizes against the background of pronounced poikilocytosis. A significant increase in the number of erythrocyte shadows became a mass phenomenon. Simultaneously, granular inclusions containing hematin entered into the hemolymph of the mollusk. It is assumed that these granular inclusions reacted with H2S to form Fe2S3 and thus neutralized the toxic effect of hydrogen sulfide.


hypoxia hydrogen sulfide contamination hemolymph erythroid elements hypoxia Anadara kagoshimensis (Tokunaga 1906) 



  1. 1.
    Avtsyn, A.P. and Shakhlamov, V.A., Ul’trastrukturnye osnovy patologii kletki (Ultrastructural Basis of Cell Pathology), Moscow: Meditsina, 1979.Google Scholar
  2. 2.
    Zaika, V.E., Konovalov, S.K., and Sergeeva, N.G., Local and seasonal phenomena of hypoxia at the bottom of Sevastopol bays and their influence on macrobenthos, Morsk. Ekol. Zh., 2011, vol. 10, no. 3, pp. 15–25.Google Scholar
  3. 3.
    Novitskaya, V.N. and Soldatov, A.A., Erythroid elements of the hemolymph Anadara inaequivalvis (Mollusca: Arcidae) under experimental anoxia: functional and morphometric characteristics, Morsk. Ekol. Zh., 2011, vol. 10, no. 1, pp. 56–64.Google Scholar
  4. 4.
    Revkov, N.K. and Shcherban, S.A., Features of biology of the bivalve mollusk Anadara kagoshimensis in the Black Sea, Ekosistemy, 2017, vol. 9, pp. 47–56.Google Scholar
  5. 5.
    Taschke, K.K., Vvedeniye v kolichestvennuyu tsitologicheskuyu morfologiyu (Introduction to Quantitative Cytohistological Morphology), Bucharest, Romania: Akad. Nauk Sots. Resp. Rumynii, 1980.Google Scholar
  6. 6.
    Chizhevskiy, A.L., Strukturnyy analiz dvizhuscheysya krovi (Structural Analysis of Moving Blood), Moscow: Akad. Nauk SSSR, 1959.Google Scholar
  7. 7.
    Arp, A.J., Sulfide binding by the blood of the hydrothermal vent tube worm, Science, 1983, vol. 219, pp. 295−297.CrossRefGoogle Scholar
  8. 8.
    Arp, A.J. and Childress, J.J., Blood function in the hydrothermal vent vestimentiferan tube worm, Science, 1981, vol. 213, pp. 342−344.CrossRefGoogle Scholar
  9. 9.
    Bailly, X. and Vinogradov, S., The sulfide binding function of annelid hemoglobins: relic of an old biosystem?, J. Inorg. Biochem., 2005, no. 99, pp. 142–150.Google Scholar
  10. 10.
    Cortesi, P., Cattani, O., Vitali, G., et al., Physiological and biochemical responses of the bivalve Scapharca inaequivalvis to hypoxia and cadmium exposure: erythrocytes versus other tissues, in Marine coastal eutrophication (Proc. Int. Conf., Bologna, Italy, 21−24 March 1990), 1992, pp. 1041−1054.Google Scholar
  11. 11.
    Cuénot, L., Études sur le sang et les glandes lymphatiques dans la série animale, Arch. Zool. Exp. Gén., 1891, vol. 2, no. 9, pp. 13−19.Google Scholar
  12. 12.
    Girish, V. and Vijayalakshmi, A., Affordable image analysis using NIH Image/Image J., Ind. J. Cancer, 2004, vol. 41, no. 1, pp. 41−47.Google Scholar
  13. 13.
    Glomski, C.A. and Tamburlin, J., The phylogenetic odyssey of the erythrocyte. II. The early or invertebrate prototypes, Histol. Histopathol., 1990, no. 5, pp. 513–525.Google Scholar
  14. 14.
    Grieshaber, M.K., Hardewig, I., Kreutzer, U., and Portner, H.-O., Physiological and metabolic responses to hypoxia in invertebrates, Rev. Physiol. Biochem. Pharmacol., 1994, vol. 125, pp. 44−131.Google Scholar
  15. 15.
    Hochachka, P.W. and Somero, G.N., Biochemical Adaptation: Mechanism and Process in Physiological Evolution, New York: Oxford Univ. Press, 2002.Google Scholar
  16. 16.
    Holden, J.A., Pipe, R.K., Quaglia, A., and Ciani, G., Blood cells of the arcid clam, Scapharca inaequivalvis, J. Mar. Biol. Assoc. U. K., 1994, vol. 74, no. 2, pp. 287−299.CrossRefGoogle Scholar
  17. 17.
    Houchin, D.N., Munn, J.I., and Parnell, B.L., A method for the measurement of red cell dimensions and calculation of mean corpuscular volume and surface area, Blood, 1958, vol. 13, no. 12, pp. 1185–1191.Google Scholar
  18. 18.
    Isani, G., Cattani, O., Tacconi, S., et al., Energy metabolism during anaerobiosis and recovery in the posterior adductor muscle of Scapharca inaequivalvis (Bruguiére), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1989, vol. 93, pp. 193−200.CrossRefGoogle Scholar
  19. 19.
    Miyamoto, Y. and Iwanaga, C., Effects of sulphide on anoxia-driven mortality and anaerobic metabolism in the ark shell Anadara kagoshimensis, J. Mar. Biol. Assoc. U. K., 2017, vol. 97, no. 2, pp. 329−336.Google Scholar
  20. 20.
    Nakano, T., Yamada, K., and Okamura, K., Duration rather than frequency of hypoxia causes mass mortality in ark shells (Anadara kagoshimensis), Mar. Pollut. Bull., 2017, vol. 125, nos. 1–2, pp. 86−91.CrossRefGoogle Scholar
  21. 21.
    Novitskaya, V.N. and Soldatov, A.A., Peculiarities of functional morphology of erythroid elements of hemolymph of the bivalve mollusk Anadara inaequivalvis, the Black Sea, Hydrobiol. J., 2013, vol. 49, no. 6, pp. 64−71.CrossRefGoogle Scholar
  22. 22.
    Powell, E.N., Crenshow, M.A., and Rieger, R.W., Adaptations to sulfide in sulfide-system meiofauna. End products of sulfide detoxification in three turbellarians and a gastrotrich, Mar. Ecol.: Prog. Ser., 1980, vol. 2, pp. 169−177.CrossRefGoogle Scholar
  23. 23.
    Soldatov, A.A., Andreyenko, T.I., Golovina, I.V., and Stolbov, A.Ya., Peculiarities of organization of tissue metabolism in mollusks with different tolerance to external hypoxia, J. Evol. Biochem. Physiol., 2010, vol. 46, no. 4, pp. 341−349.CrossRefGoogle Scholar
  24. 24.
    Soldatov, A.A., Gostyukhina, O.L., Borodina, A.V., and Golovina, I.V., Qualitative composition of carotenoids, catalase and superoxide dismutase activities in tissues of the bivalve mollusc Anadara inaequivalvis (Bruguiere, 1789), J. Evol. Biochem. Physiol., 2013, vol. 49, no. 4, pp. 389−398.CrossRefGoogle Scholar
  25. 25.
    Stewart, F.J. and Cavanaugh, C.M., Bacterial endosymbioses in Solemya (Mollusca: Bivalvia) – model systems for studies of symbiont-host adaptation, Antonie van Leeuwenhoek, 2006, vol. 90, pp. 343−360.CrossRefGoogle Scholar
  26. 26.
    Vismann, B., Hematin and sulfide removal in hemolymph of the hemoglobin-containing bivalve Scapharca inaequivalvis, Mar. Ecol.: Prog. Ser., 1993, vol. 98, pp. 115−122.CrossRefGoogle Scholar
  27. 27.
    Zwaan, A., Cortesi, P., Thillart, G., and Storey, K.B., Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis, Mar. Biol., 1991, vol. 111, no. 3, pp. 343−351.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • A. A. Soldatov
    • 1
    • 2
    Email author
  • T. A. Kukhareva
    • 1
  • A. Y. Andreeva
    • 1
  • E. S. Efremova
    • 1
  1. 1.Kovalevsky Institute of Marine Biological Research, Russian Academy of SciencesSevastopolRussia
  2. 2.Vernadsky Crimean Federal UniversitySimferopolRussia

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