Skip to main content
Log in

Fluorescent in vitro phagocytosis assay differentiates hemocyte activity of the bivalve molluscs Modiolus kurilensis (Bernard, 1983) inhabiting impacted and non-impacted water areas

  • Cell Biology
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract

Hemocyte phagocytosis assay in vitro revealed no significant differences in the average values of phagocytic activity (PA) and phagocytic index (PI) in samples of the molluscs Modiolus kurilensis that inhabit non-impacted water areas (Kievka, Vostok, and Troitsa bays, the Sea of Japan). The only exception was an insignificantly lower value of PI for individuals from Troitsa Bay. The average values of PA for hemocytes of the total population of bivalves from non-impacted water areas were 52.0 ± 1.0%. On the basis of the interannual analysis of PA, the bivalve population from Vostok Bay was chosen as an appropriate reference group that is characterized by relatively stable PA values. In comparison with molluscs from the reference group and other investigated samples, M. kurilensis from the impacted water area (Sportivnaya Gavan, Amursky Bay) had considerably lower values of average PA (36.0 ± 2.0%) and PI (2.1 +- 0.05). The presented cell-mediated immunity assay can serve as an effective method for estimation of the physiological state of the bivalve in natural and aquacultural populations in order to differentiate molluscs from impacted and non-impacted water areas.

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.

Similar content being viewed by others

References

  1. Anisimova, A.A., Flow cytometric and light microscopic identification of hemocyte subpopulations of Modiolus kurilensis (Bernard, 1983) (Bivalvia: Mytilidae), Russ. J. Mar. Biol., 2012, vol. 38, no. 5, pp. 406–415.

    Article  Google Scholar 

  2. Vaschenko, M.A., Almyashova, T.N., and Zhadan, P.M., Long-term and seasonal dynamics of the gonad state in the sea urchin Strongylocentrotus intermedius under anthropogenic pollution (Amursky Bay, the Sea of Japan), Vestnik Dal’nevost. Otd. Ross. Akad. Nauk, 2005, no. 1, pp. 32–42.

    Google Scholar 

  3. Galysheva, Yu.A., Khristoforova, N.K., Chernova, E.N., et al., On ecological parameters of waters and bottom sediments in the Kievka Bay (the Sea of Japan), Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2008, vol. 154, pp. 114–124.

    Google Scholar 

  4. Zhuravel’, E.V., Khristoforova N.K., Drozdovskaya, O.A., et al., The assessment of the state of waters in Vostok Bay (Peter the Great Bay, the Sea of Japan) by hydrochemical and microbiological parameters, Izv. Samar. Nauch. Tsentra, Ross. Akad. Nauk, 2012, vol. 14, no. 1, pp. 2325–2329.

    Google Scholar 

  5. Kolotukhina, N.K. and Semenikhina, O.Ya., Dynamics of abundance of larvae of the Pacific mussel Mytilus trossulus and horse mussel Modiolus kurilensis in plankton of Troitsa Bight (Posiet Bay) and Vostok Bay, the Sea of Japan, Russ. J. Mar. Biol., 1998, vol. 24, no. 2, pp. 127–130.

    Google Scholar 

  6. Korshenko, A.N., Matveichuk I.G., Plotnikova, T.I., et al., Ezhegodnik kachestva morskikh vod po gidrokhimicheskim pokazatelyam (Yaponskoe more) za 2009 god (Yearbook of the Quality of Marine Waters by Hydrochemical Parameters (the Sea of Japan) in 2009), Vladivostok: Primor. Uprav. Gidromet. Sluzhby, 2010.

    Google Scholar 

  7. Markina, Zh.V., Zhuravel’, E.V., and Aizdaicher, N.A., Assessment of the state of waters in Peter the Great Bay (The Sea of Japan) on the basis of hydrochemical indicators and analysis of growth and content chlorophyll A of the microalga Phaeodactylum tricornutum, Izv. Samar. Nauch. Tsentra, Ross. Akad. Nauk, 2011, vol. 13, no. 1, pp. 1460–1463.

    Google Scholar 

  8. Naumov, Yu.A., Antropogenez i ekologicheskoe sostoyanie geosistemy pribrezhno-shelfovoi zony zaliva Petra Velokogo Yaponskogo morya (Anthropogenesis and Ecological State of the Geosystem of the Coastal-Shelf Zone of Peter the Great Bay of the Sea of Japan), Vladivosotok: Dal’nauka, 2006.

    Google Scholar 

  9. Nigmatulina, L.V., Assessment of anthropogenic load of coastal sources of the Amursky Bay (The Sea of Japan), Vestinik Dal’nevost. Otd., Ross. Akad. Nauk, 2007, no. 1, pp. 73–76.

    Google Scholar 

  10. Syasina, I.G. and Shcheblykina, A.V., Morphofunctional characterization of the reproductive system of the gastropods Littorina brevicula, L. mandshurica, and Nucella heyseana from uncontaminated and contaminated areas of Peter the Great Bay, The Sea of Japan, Russ. J. Mar. Biol., 2007, vol. 33, no. 6, pp. 399–404.

    Article  Google Scholar 

  11. Akaishi, F.M., St.-Jean, S.D., Bishay, F., et al., Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater, Aquat. Toxicol., 2007, vol. 82, pp. 1–14.

    Article  CAS  PubMed  Google Scholar 

  12. Barracco, M.A., Medeiros, I.D., and Moreira, F.M., Some haemato-immunological parameters in the mussel Perna perna, Fish Shellfish Immunol., 1999, vol. 9, pp. 387–404.

    Article  Google Scholar 

  13. Beckman, N., Morse, M.P., and Moore, C.M., Comparative study of phagocytosis in normal and diseased hemocytes of the bivalve mollusc Mya areneria, J. Invertebr. Pathol., 1992, vol. 59, pp. 124–132.

    Article  Google Scholar 

  14. Bouilly, K., Gagnaire, B., Bonnard, M., et al., Effects of cadmium on aneuploidy and hemocyte parameters in the Pacific oyster Crassostrea gigas, Aquat. Toxicol., 2006, vol. 78, pp. 149–156.

    Article  CAS  PubMed  Google Scholar 

  15. Cajaraville, M., Olabarrienta, I., and Marigomez, I., In vitro activities in mussel hemocytes as biomarkers of environmental quality: a case study in the Abra Estuary (Biscay Bay), Ecotoxicol. Environ. Saf., 1996, vol. 35, pp. 253–260.

    Article  CAS  PubMed  Google Scholar 

  16. Canesi, L., Ciacci, C., Betti, M., et al., Immunotoxicity of carbon black nanoparticles to blue mussel hemocytes, Environ. Int., 2008, vol. 34, no. 8, pp. 1114–1119.

    Article  CAS  PubMed  Google Scholar 

  17. Canesi, L., Lorusso, L.C., Ciacci, C., et al., Immunomodulation of Mytilus hemocytes by individual estrogenic chemicals and environmentally relevant mixtures of estrogens: in vitro and in vivo studies, Aquat. Toxicol., 2007, vol. 81, pp. 36–44.

    Article  CAS  PubMed  Google Scholar 

  18. Cheng, T.C., Effects of in vivo exposure of Crassostrea virginica to heavy metals on hemocytes viability and activity levels of lysosomal enzymes, in Pathology in Marine Science, San Diego: Academic, 1990, pp. 513–524.

    Chapter  Google Scholar 

  19. Ciacci, C., Fabbri, R., Betti, M., et al., Seasonal changes in functional parameters of the hemolymph of Mytilus galloprovincialis, Invertebrate Survival J., 2009, vol. 6, pp. 44–48.

    Google Scholar 

  20. Coles, J.A., Farley, S.R., and Pipe, R.K., Alteration of the immune response of the common marine mussel Mytilus edulis resulting from exposure to cadmium, Dis. Aquat. Org., 1995, vol. 22, pp. 59–65.

    Article  CAS  Google Scholar 

  21. Coray, C., St.-Jean, S.D., and Bard, S.M., Immunomodulation in blue mussels (Mytilus edulis and Mytilus trossulus) exposed to municipal effluent in Eastern Canada, Water Qual. Res. J., 2007, vol. 42, no. 3, pp. 194–201.

    CAS  Google Scholar 

  22. Dyrynda, E.A., Law, R.J., Dyrynda, P.E.J., et al. Changes in immune parameters of natural Mytilus edulis populations following a major oil spill (Sea Empress, Wales, UK), Mar. Ecol.: Progr. Ser., 2000, vol. 206, pp. 155–170.

    Article  Google Scholar 

  23. Fisher, W.S., Antimicrobial activity of copper and zinc accumulated in eastern oyster amebocytes, J. Shellfish Res., 2004, vol. 23, pp. 321–351.

    Google Scholar 

  24. Gagnaire, B., Gay, M., Huvet, A., et al., Combination of a pesticide exposure and a bacterial challenge: In vivo effects on immune response of Pacific oyster, Crassostrea gigas (Thunberg), Aquat. Toxicol., 2007, vol. 84, pp. 92–102.

    Article  CAS  PubMed  Google Scholar 

  25. Genthner, F.J., Volety, A.K., Oliver, L.M., et al., Factors influencing in vitro killing of bacteria by hemocytes of the eastern oyster (Crassostrea virginica), Appl. Environ. Microbiol., 1999, vol. 65, no. 7, pp. 3015–3020.

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Gillis, P.L., Cumulative impacts of urban runoff and municipal wastewater effluents on wild freshwater mussels (Lasmigona costata), Sci. Total. Environ., 2012, vol. 431, pp. 348–356.

    Article  CAS  PubMed  Google Scholar 

  27. Giron-Perez, M.I., Relationships between innate immunity in bivalve molluscs and environmental pollution, Invertebrate Survival J., 2010, vol. 7, pp. 149–156.

    Google Scholar 

  28. Gomez-Mendikute, A. and Cajaraville, M.P., Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes, Toxicol. In Vitro, 2003, vol. 17, pp. 539–546.

    Article  CAS  PubMed  Google Scholar 

  29. Kolyuchkina, G.A. and Ismailov, A.D., Parameters of extrapallial fluid of bivalves as nonspecific biomarkers of short-term environmental pollution, Oceanology (Engl. Transl.), 2007, vol. 4, no. 2, pp. 213–220.

    Article  Google Scholar 

  30. Mayrand, E., St.-Jean, S.D., and Courtenay, S.C., Haemocyte responses of blue mussels (Mytilus edulis L.) transferred from a contaminated site to a reference site: can the immune system recuperate? Aquacult. Res., 2005, vol. 36, no. 10, pp. 962–971.

    Article  Google Scholar 

  31. Mydlarz, L.D., Jones, L.E., and Harvell, C.D., Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates, Annu. Rev. Ecol. Evol. Syst., 2006, vol. 37, pp. 251–288.

    Article  Google Scholar 

  32. Pipe, R.K. and Coles, J.A., Environmental contaminants influencing immune function in marine bivalve molluscs, Fish Shellfish Immunol., 1995, vol. 5, pp. 581–595.

    Article  Google Scholar 

  33. Pipe, R.K., Coles, J.A., Carissan, F.M., et al., Copper induced immunomodulation in the marine mussel, Mytilus edulis, Aquat. Toxicol., 1999, vol. 46, pp. 43–54.

    Article  CAS  Google Scholar 

  34. Prado-Alvarez, M., Romero, A., Balseiro, P., et al., Morphological characterization and functional immune response of the carpet shell clam (Ruditapes decussates) haemocytes after bacterial stimulation, Fish Shellfish Immunol., 2012, vol. 32, no. 1, pp. 69–78.

    Article  CAS  PubMed  Google Scholar 

  35. Ratcliffe, N.A., Rowley, A.F., Fitzgerald, S.W., et al., Invertebrate immunity: basic concepts and recent advances, Int. Rev. Cytol., 1985, vol. 97, pp. 182–350.

    Google Scholar 

  36. Tunkijjanukij, S. and Olafsen, Jan A., Sialic acid-binding lectin with antibacterial activity from the horse mussel: further characterization and immunolocalization, Dev. Comp. Immunol., 1998, vol. 22, no. 2, pp. 139–150.

    Article  CAS  PubMed  Google Scholar 

  37. Wootton, E.C., Dyrynda, E.A., and Ratcliffe, N.A., Bivalve immunity: comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua), Fish Shellfish Immunol., 2002, vol. 15, pp. 195–210.

    Article  Google Scholar 

  38. Yurchenko, O.V. and Vaschenko, M.A., Morphology of spermatogenic and accessory cells in the mussel Modiolus kurilensis under environmental pollution, Mar. Environ. Res., 2010, vol. 70, no. 2, pp. 171–180.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu. N. Sokolnikova.

Additional information

Original Russian Text © Yu.N. Sokolnikova, E.V. Trubetskaya, I.A. Beleneva, A.V. Grinchenko, V.V. Kumeiko, 2015, published in Biologiya Morya.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sokolnikova, Y.N., Trubetskaya, E.V., Beleneva, I.A. et al. Fluorescent in vitro phagocytosis assay differentiates hemocyte activity of the bivalve molluscs Modiolus kurilensis (Bernard, 1983) inhabiting impacted and non-impacted water areas. Russ J Mar Biol 41, 118–126 (2015). https://doi.org/10.1134/S106307401502011X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106307401502011X

Keywords

Navigation