Advertisement

Russian Journal of Marine Biology

, Volume 43, Issue 2, pp 156–163 | Cite as

The composition and seasonal dynamics of the hemocyte cell population in the clams Corbicula japonica Prime (1864) of the Kievka River (the basin of the Sea of Japan)

  • A. A. Anisimova
  • A. L. Ponomareva
  • A. V. Grinchenko
  • I. A. Kirsanova
  • D. N. Kravchenko
Physiology of Animals
  • 32 Downloads

Abstract

The parameters of a hemocyte cell population were investigated in the bivalve mollusk Corbicula japonica of the Kievka River (the basin of the Sea of Japan) at four seasonal points corresponding to different stages of the reproductive cycle: (1) March (sexual rest); (2) May (gametogenesis); (3) July (spawning); and (4) November (the end of reproductive activity). Using light microscopy, we identified four cell morphotypes in the hemolymph: small and large hyalinocytes, as well as basophilic and eosinophilic granulocytes. Flow cytometry confirmed the structural heterogeneity of the cell population and allowed us to estimate the seasonal variability of the cell composition in C. japonica hemolymph. The total cell count in the mollusk hemolymph did not change significantly during the annual cycle and did not correlate with the average cell size of hemocytes. In March, May, and November, granulocytes dominated in the cell population (74.3 ± 2.9, 77.5 ± 3.5, and 86.7 ± 2.6%, respectively), while in July their relative content was reduced dramatically (37.2 ± 5.1%) causing a significant decrease of both the average cell size and granularity in circulation. Most likely, this is connected with the summer migration of mature eosinophilic granulocytes from the hemolymph to spawning gonads for resorption of the unspent sexual products, as well as to other internal organs for participation in digestion and to provide the immune defense against pathogens.

Keywords

hemocytes hemolymph seasonal dynamics reproductive cycle Corbicula japonica Bivalvia 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Anisimova, A.A., Morphofunctional parameters of hemocytes in the assessment of the physiological status of bivalves, Russ. J. Mar. Biol., 2013, vol. 39, no. 6, pp. 381–391.CrossRefGoogle Scholar
  2. 2.
    Volova, G.N., Macrobenthos of bracking-water bodies of southern Primorye (Sea of Japan), Gidrobiol. Zh., 1974, vol. 10, no. 6, pp. 32–37.Google Scholar
  3. 3.
    Dzyuba, S.M. and Maslennikova, L.A., Reproductive cycle of the bivalve mollusks Anadara broughtoni from the southern part of Peter the Great Bay (Sea of Japan), Biol. Morya (Vladivostok), 1982, no. 3, pp. 34–40.Google Scholar
  4. 4.
    Zavarzin, A.A., Comparative histology of the blood and connective tissue: IV. Inflammatory of connective tissue neoplasms in the mussel (Anodonta anatine L.), in Izbrannye trudy (Selected Research Works), Moscow: Akad. Nauk SSSR, 1953, vol. 2.Google Scholar
  5. 5.
    Rybalkina (Dzyuba), S.M., Maiorova, M.A., Anisimov A.P., and Kravchenko, D.N., The gametogenesis and sexual cycle of the bivalve Corbicula japonica Prime (1864) in the mouth of the Kievka River (Sea of Japan), Russ. J. Mar. Biol., 2013, vol. 39, no. 4, pp. 253–264.CrossRefGoogle Scholar
  6. 6.
    Yavnov, S.V. and Rakov, V.A., Korbikula (Corbicula Species), Vladivostok: TINRO-Center, 2002.Google Scholar
  7. 7.
    Allam, B., Ashton-Alcox, K.A., and Ford, S.E., Flow cytometric comparison of haemocytes from three species of bivalve mollusks, Fish Shellfish Immunol., 2002, vol. 13, pp. 141–158.CrossRefPubMedGoogle Scholar
  8. 8.
    Ashton-Alcox, K.A. and Ford, S.E., Variability in molluscan hemocytes: A flow cytometric study, Tissue Cell, 1998, vol. 30, pp. 195–204.CrossRefPubMedGoogle Scholar
  9. 9.
    Carballal, M.J., López, C., Azevedo C., and Villalba, A., Enzymes involved in defense functions of hemocytes of mussel Mytilus galloprovincialis, J. Invertebr. Pathol., 1997, vol. 70, pp. 96–105.CrossRefPubMedGoogle Scholar
  10. 10.
    Carballal, M.J., López, C., Azevedo, and Villalba, A., In vitro study of phagocytic ability of Mytilus galloprovincialis Lmk. Haemocytes, Fish Shellfish Immunol., 1997, vol. 7, no. 6, pp. 403–416.CrossRefGoogle Scholar
  11. 11.
    Carballal, M.J., Villalba, A., and López, C., Seasonal variation and effects of age, food availability, size, gonadal development, and parasitism on the hemogram of Mytilus galloprovincialis, J. Invertebr. Pathol., 1998, vol. 72, no. 3, pp. 304–312.CrossRefPubMedGoogle Scholar
  12. 12.
    Chang, S.-J., Tseng, S.-M., and Chou, H.-Y., Morphological characterization via light and electron microscopy of the hemocytes of two cultured bivalves: A comparison study between the hard clam (Meretrix lusoria) and Pacific oyster (Crassostrea gigas), Zool. Stud., 2005, vol. 44, no. 1, pp. 144–153.Google Scholar
  13. 13.
    Cheng, T.C., Bivalves, in Invertebrate Blood Cells, London: Academic, 1981, vol. 2, pp. 233–300.Google Scholar
  14. 14.
    Chu, F.L.E. and La Peyre, J.F., Perkinsus marinus susceptibility and defense-related activities in eastern oysters Crassostrea virginica: temperature effects, Dis. Aquat. Org., 1993, vol. 16, pp. 223–234.CrossRefGoogle Scholar
  15. 15.
    Chu, F.L.E., Volety, A.K., and La Peyre, J.F., Annual variation of hemolymph components and Perkinsus marinus infection in oysters sampled from deep water shoal, James River, Virginia, J. Shellfish Res., 1995, vol. 14, p. 263.Google Scholar
  16. 16.
    Delaporte, M., Soudant, P., Lambert, C., et al., Impact of food availability on energy storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle, Aquaculture, 2006, vol. 254, no. 1–4, pp. 571–582.CrossRefGoogle Scholar
  17. 17.
    Donaghy, L., Kim, B.-K., Hong, H.-K., et al., Flow cytometry studies on the populations and immune parameters of the hemocytes of the Suminoe oyster, Crassostrea ariakensis, Fish Shellfish Immunol., 2009, vol. 27, pp. 296–301.CrossRefPubMedGoogle Scholar
  18. 18.
    Donaghy, L., Lambert, C., Choi, K.-S., and Soudant, P., Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): Current knowledge and future prospects, Aquaculture, 2009, vol. 297, pp. 10–24.CrossRefGoogle Scholar
  19. 19.
    Fisher, W.S., Oliver, L.M., and Edwards, P., Hematologic and serologic variability of eastern oysters from Apalachicola Bay, Florida, J. Shellfish Res., 1996, vol. 15, pp. 555–564.Google Scholar
  20. 20.
    Flye-Sainte-Marie, J., Soudant, P., Lambert, C., et al., Variability of the hemocyte parameters of Ruditapes philippinarum in the field during an annual cycle, J. Exp. Mar. Biol. Ecol., 2009, vol. 377, pp. 1–11.CrossRefGoogle Scholar
  21. 21.
    Galimany, E., Place, A.R., Ramón, M., et al., The effects of feeding Karlodinium veneficum (PLY no. 103; Gymnodinium veneficum Ballantine) to the blue mussel Mytilus edulis, Harmful Algae, 2008, vol. 7, no. 1, pp. 91–98.CrossRefGoogle Scholar
  22. 22.
    Garcia-Garcia, E., Prado-Alvarez, M., Novoa, B., et al., Immune responses of mussel hemocyte subpopulations are differentially regulated by enzymes of the PI 3-K, PKC, and ERK kinase families, Dev. Comp. Immunol., 2008, vol. 32, pp. 637–653.CrossRefPubMedGoogle Scholar
  23. 23.
    Goedken, M. and De Guise, S., Flow cytometry as a tool to quantify oyster defence mechanisms, Fish Shellfish Immunol., 2004, vol. 16, pp. 539–552.CrossRefPubMedGoogle Scholar
  24. 24.
    Hine, P.M., The inter-relationships of bivalve haemocytes, Fish Shellfish Immunol., 1999, vol. 9, pp. 367–385.CrossRefGoogle Scholar
  25. 25.
    Liu, S., Jiang, X., Hu, X., et al., Effects of temperature on non-specific immune parameters in two scallop species: Argopecten irradians (Lamarck, 1819) and Chlamys farreri (Jones and Preston, 1904), Aquacult. Res., 2004, vol. 35, pp. 678–682.CrossRefGoogle Scholar
  26. 26.
    López, C., Carballal, M.J., Azevedo, C., et al., Differential phagocytic ability of the circulating haemocyte types of the carpet shell clam Ruditapes decussatus (Mollusca: Bivalvia), Dis. Aquat. Org., 1997, vol. 30, pp. 209–215.CrossRefGoogle Scholar
  27. 27.
    Malagoli, D., Casarini, L., Sacchi, S., et al., Stress and immune response in the mussel Mytilus galloprovincialis, Fish Shellfish Immunol., 2007, vol. 23, pp. 171–177.CrossRefPubMedGoogle Scholar
  28. 28.
    Mix, M.C., A general model for leucocyte cell renewal in bivalve mollusks, Mar. Fish. Rev., 1976, vol. 38, no. 10, pp. 37–41.Google Scholar
  29. 29.
    Monari, M., Matozzo, V., Foschi, J., et al., Effects of high temperatures on functional responses of haemocytes in the clam Chamelea gallina, Fish Shellfish Immunol., 2007, vol. 22, pp. 98–114.CrossRefPubMedGoogle Scholar
  30. 30.
    Ottaviani, E., Franchini, A., Barbieri, D., et al., Comparative and morphofunctional studies on Mytilus galloprovincialis hemocytes: presence of two aging-related hemocyte stages, Ital. J. Zool., 1998, vol. 65, no. 4, pp. 349–354.CrossRefGoogle Scholar
  31. 31.
    Paillard, C., Allam, B., and Oubella, R., Effect of temperature on defense parameters in Manila clam Ruditapes philippinarum challenged with Vibrio tapetis, Dis. Aquat. Org., 2004, vol. 59, pp. 249–262.CrossRefPubMedGoogle Scholar
  32. 32.
    Perrigault, M., Dahl, S.F., Pales Espinosa, E., et al., Effects of temperature on hard clam (Mercenaria mercenaria) immunity and QPX (Quahog Parasite Unknown) disease development, II: Defense parameters, J. Invertebr. Pathol., 2011, vol. 106, pp. 322–332.CrossRefPubMedGoogle Scholar
  33. 33.
    Pipe, R.K., Coles, J.A., Thomas, M.E., et al., Evidence for environmentally derived immunomodulation in mussels from the Venice Lagoon, Aquat. Toxicol., 1995, vol. 32, no. 1, pp. 59–73.CrossRefGoogle Scholar
  34. 34.
    Pipe, R.K., Farley, S.R., and Coles, J.A., The separation and characterization of haemocytes from the mussel Mytilus edulis, Cell Tissue Res., 1997, vol. 289, pp. 537–545.CrossRefPubMedGoogle Scholar
  35. 35.
    Renwrantz, L., Siegmund, E., and Woldmann, M., Variations in hemocyte counts in the mussel, Mytilus edulis: Similar reaction patterns occur in disappearance and return of molluscan hemocytes and vertebrate leukocytes, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2013, vol. 164, pp. 629–637.CrossRefGoogle Scholar
  36. 36.
    Sminia, T. and van der Knaap, W.P.W., Cells and molecules in molluscan immunology, Dev. Comp. Immunol., 1987, vol. 11, pp. 17–28.CrossRefPubMedGoogle Scholar
  37. 37.
    Soudant, P., Paillard, C., Choquet, G., et al., Impact of season and rearing site on the physiological and immunological parameters of the Manila clam Venerupis (=Tapes=Ruditapes) philippinarum, Aquaculture, 2004, vol. 229, pp. 401–418.CrossRefGoogle Scholar
  38. 38.
    Volety, A.K., Winstead, J.T., and Fisher, W.S., Influence of seasonal factors on oyster hemocyte killing of Vibrio parahaemolyticus, J. Shellfish Res., 1999, vol. 18, p. 323.Google Scholar
  39. 39.
    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., 2003, vol. 15, pp. 195–210.CrossRefPubMedGoogle Scholar
  40. 40.
    Wootton, E.C. and Pipe, R.K., Structural and functional characterisation of the blood cells of the bivalve mollusk, Scrobicularia plana, Fish Shellfish Immunol., 2003, vol. 15, pp. 249–262.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • A. A. Anisimova
    • 1
  • A. L. Ponomareva
    • 2
  • A. V. Grinchenko
    • 1
  • I. A. Kirsanova
    • 1
  • D. N. Kravchenko
    • 1
  1. 1.Far Eastern Federal UniversityVladivostokRussia
  2. 2.Somov Institute of Epidemiology and MicrobiologyVladivostokRussia

Personalised recommendations