Skip to main content
Springer Nature Link
Log in

The Cell Composition of the Peripheral Blood and Some Hematopoietic Organs in the Antarctic Starry Skate Amblyraja georgiana (Norman, 1938) (Rajiformes: Rajidae) from the Scotia Sea

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

Abstract—

The composition of leukocytes was studied in the peripheral blood and hematopoietic organs (kidneys and spleen) of the Antarctic starry skate Amblyraja georgiana (Norman, 1938). Cells of several types with different morphofunctional characteristics and structures were found in the blood smears: lymphocytes, monocytes, neutrophils and eosinophils, and blast cells. A leukogram analysis showed that the white blood of A. georgiana is of a lymphoid type. In the kidney and spleen, most cells are blast forms.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Galaktionov, V.G., Evolyutsionnaya immunologiya: uchebnoye posobie (Evolutionary Immunology: A Study Guide), Moscow: Akademkniga, 2005.

  2. Grushko, M.P., Khvostova, S.M., and Kryuchkov, V.N., Specifics of hematopoiesis in members of cartilaginous fishes, Vestn. Astrakhan. Gos. Tekh. Univ., Ser.: Rybn. Khoz., 2012, no. 1, pp. 133–135.

  3. Grushko, M.P. and Khvostova, S.M., Cell composition of hematopoietic organs in cartilaginous fishes, Vestn. Astrakhan. Gos. Tekh. Univ., Ser.: Rybn. Khoz., 2010, no. 2, pp. 98–100.

  4. Gordeev, I.I., Balabanova, L.V., and Suvorova, T.A., Composition of leukocytes in the hematopoietic organs of Antarctic toothfish, Tr. Vseross. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2017, vol. 167, pp. 6–11.

    Google Scholar 

  5. Ivanova, N.T., Atlas kletok krovi ryb (Atlas of Fish Blood Cells), Moscow: Legkaya i Pishchevaya Promyshlennost’, 1983.

  6. Cooper, E.L., Comparative Immunology, Englewood Cliffs, N.J.: Prentice-Hall, 1976.

    Google Scholar 

  7. Zavarzin, A.A., Izbrannye trudy. T. 4. Ocherki evolyutsionnoi gistologii krovi i soedinitel’noi tkani (Selected Works, vol. 4: Essays on Evolutionary Histology of Blood and Connective Tissue), Moscow: Akad. Nauk SSSR, 1953.

  8. Zavarzin, A.A., Osnovy chastnoi tsitologii i sravnitel’noi gistologii mnogokletochnykh zhivotnykh (Basics of Special Cytology and Comparative Histology of Multicellular Animals), Leningrad: Nauka, 1976.

  9. Lakin, G.F., Biometriya (Biometrics), Moscow: Vysshaya Shkola, 1980.

    Google Scholar 

  10. Mikryakov, V.R., Zakonomernosti formirovaniya priobretennogo immuniteta u ryb (Patterns of Formation of Acquired Immunity in Fish), Rybinsk: Inst. Biol. Vnutr. Vod, Ross. Akad. Nauk, 1991.

  11. Roitt, I., Brostoff, J., and Male, D., Immunology, London: Mosby, 1998.

    Google Scholar 

  12. Tochilina, L.V., Leukocyte formula of marine fishes, Gidrobiol. Zh., 1994, vol. 30, no. 3, pp. 50–57.

    Google Scholar 

  13. Fedorov, N.A., Normal’noye krovetvoreniye i ego regulyatsiya (Normal Hematopoiesis and Its Regulation), Moscow: Meditsina, 1976.

  14. Florensov, V.A. and Pestova, I.M., Ocherki evolyutsionnoi immunomorfologii (Essays on Evolutionary Immunomorphology), Irkutsk: Irkutsk. Gos. Univ., 1990.

  15. Dill, D.B., Edwards, H.T., and Florkin, M., Properties of the blood of the skate (Raia oscillata), Biol. Bull., 1932, vol. 62, no. 1, pp. 23–36.

    Article  CAS  Google Scholar 

  16. Ellis, A.E., The leucocytes of fish: A review, J. Fish Biol., 1977, vol. 11, no. 5, pp. 453–491.

    Article  Google Scholar 

  17. Engle, R.L., Woods, K.R., Paulsen, E.C., and Pert, J.N., Plasma cells and serum proteins in marine fish, Proc. Soc. Exp. Biol. Med., 1958, vol. 98, no. 4, pp. 905–909.

    Article  CAS  Google Scholar 

  18. Evans, D.H., Piermarini, P.M., and Choe, K.P., The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste, Physiol. Rev., 2005, vol. 85, no. 1, pp. 97–177.

    Article  CAS  Google Scholar 

  19. Fänge, R., Size relations of lymphomyeloid organs in some cartilaginous fish, Acta Zool., 1977, vol. 58, no. 3, pp. 125–128.

    Article  Google Scholar 

  20. Fange, R.A., A comparative study of limphomyeloid tissue in fish, Dev. Comp. Immunol., 1982, vol. 6, no. 1, suppl. 2, pp. 23–33.

    Article  Google Scholar 

  21. Fänge, R. and Pulsford, A., Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L., Cell Tissue Res., 1983, vol. 230, no. 2, pp. 337–351.

    Article  Google Scholar 

  22. FishBase, World Wide Web Electronic Publication, Froese, R. and Pauly, D., Eds. www.fishbase.org. Accessed March 26, 2018.

  23. Gordeev, I.I., Mikryakov, D., Balabanova, L.V., and Mikryakov, V.R., Composition of leucocytes in peripheral blood of Antarctic toothfish Dissostichus mawsoni (Nototheniidae), J. Ichthyol., 2014, vol. 54, no. 6, pp. 422–425.

    Article  Google Scholar 

  24. Gordeev, I.I., Mikryakov, D.V., Balabanova, L.V., and Mikryakov, V.R., Composition of leucocytes in peripheral blood of Patagonian toothfish (Dissostichus eleginoides Smitt, 1898) (Nototheniidae), Polar Res., 2017, vol. 36, no. 1, art. ID 1374126. https://doi.org/10.1080/17518369.2017.1374126

    Article  Google Scholar 

  25. Gregory, T.R., The bigger the C-value, the larger the cell: Genome size and red blood cell size in vertebrates, Blood Cells, Mol., Dis., 2001, vol. 27, no. 5, pp. 830–843.

    Article  CAS  Google Scholar 

  26. Harris, D.F., On the hæmoglobinometry and hæmacytometry of the blood of the skate, J. Physiol., 1903, vol. 30, nos. 3–4, pp. 319–321.

    Article  CAS  Google Scholar 

  27. Hyder, S.L., Cayer, M.L., and Pettey, C.L., Cell types in peripheral blood of the nurse shark: An approach to structure and function, Tissue Cell, 1983, vol. 15, no. 3, pp. 437–455.

    Article  CAS  Google Scholar 

  28. Jordan, H.E. and Speidel, C.C., Studies on lymphocytes. II. The origin, function, and fate of the lymphocytes in fishes, J. Morphol., 1924, vol. 38, no. 4, pp. 529–549.

    Article  Google Scholar 

  29. Kisch, B., Hemoglobin content, size and amount of erythrocytes in fishes, Exp. Med. Surg., 1949, vol. 7, pp. 118–133.

    CAS  PubMed  Google Scholar 

  30. Kisch, B., Erythrocytes in fishes, Exp. Med. Surg., 1951, vol. 9, pp. 125–137.

    CAS  PubMed  Google Scholar 

  31. Litman, G.W., Frommel, D., Finstad, J., et al., The evolution of the immune response. VIII. Structural studies of the lamprey immunoglobulin, J. Immunol., 1970, vol. 105, pp. 1278–1284.

    CAS  PubMed  Google Scholar 

  32. Main, C.E. and Collins, M.A., Diet of the Antarctic starry skate Amblyraja georgiana (Rajidae, Chondrichthyes) at South Georgia (Southern Ocean), Polar Biol., 2011, vol. 34, no. 3, pp. 389–396.

    Article  Google Scholar 

  33. Maximow, A.A., Bindegewebe und blutbildende Gewebe, in Handbuch der Microscopischen Anatomie des Menschen, Brodersen, J., Maximow, A., and Schaffer, J., Eds., Berlin: Springer-Verlag, 1927, vol. 2/1, pp. 232–538.

    Chapter  Google Scholar 

  34. Malassez, L., De la numération des globules rouges du sang chez les mammiféres, les oiseaux et les poisons, C. R. Acad. Sci.,Paris, 1872, vol. 75, pp. 1528–1531.

    Google Scholar 

  35. Manning, M.J. and Nakanishi, T., The specific immune system: cellular defenses, in The Fish Immune System: Organism, Pathogen and Environment, London: Academic, 1996, vol. 15, ch. 4, pp. 160−206.

    Google Scholar 

  36. Nelson, J.S., Grande, T.C., and Wilson, M.V.H., Fishes of the World, 5th ed., Hoboken, N.J.: Wiley, 2016.

    Book  Google Scholar 

  37. Perey, D.Y., Finstad, J., Pollara, B., and Good, R.A., Evolution of the immune response. VI. First and second set skin homograft rejections in primitive fishes, Lab. Invest., 1968, vol. 19, pp. 591−597.

    CAS  PubMed  Google Scholar 

  38. Saunders, D.C., Elasmobranch blood cells, Copeia, 1966, vol. 1966, no. 2, pp. 348–351.

    Article  Google Scholar 

  39. Saunders, D.C., Differential blood cell counts of 121 species of marine fishes of Puerto Rico, Trans. Am. Microsc. Soc., 1966, vol. 85, no. 3, pp. 427–449.

    Article  Google Scholar 

  40. Sherburne, S.W., Occurrence of both heterophils and neutrophils in the blood of the spiny dogfish, Squalus acanthias,Copeia, 1974, vol. 1974, no. 1, pp. 259–261.

    Article  Google Scholar 

  41. Van Muiswinkel, W.B. and Vervoorn-Van Der Wal, B., The immune system of fish, in Fish Diseases and Disorders, 2nd ed., Wallingford, U.K.: CAB Int., 2006, vol. 1, ch. 18, pp. 678−701.

    Google Scholar 

  42. Voytsytskiy, V.M., Rodionova, N.K., Khyzhniak, S.V., and Manylo, L.G., Hematological characteristics of the Antarctic fish, Hydrobiol. J., 2008, vol. 44, no. 3, pp. 66–74.

    Article  Google Scholar 

  43. Walsh, C.J. and Luer, C.A., Comparative phagocytic and pinocytic activities of leucocytes from peripheral blood and lymphomyeloid tissues of the nurse shark (Ginglymostoma cirratum Bonaterre) and the clearnose skate (Raja eglanteria Bosc), Fish Shellfish Immunol., 1998, vol. 8, no. 3, pp. 197–215.

    Article  Google Scholar 

  44. Walsh, C.J. and Luer, C.A., Elasmobranch hematology: Identification of cell types and practical applications, in The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and Their Relatives, Smith, M., Warmolts, D., Thoney, D., and Hueter, R., Eds., Columbus, Ohio: Ohio Biol. Surv., 2004, pp. 307–323.

    Google Scholar 

  45. Zapata, A., Ultrastructure of elasmobranch lymphoid tissue. 1. Thymus and spleen, Dev. Comp. Immunol., 1980, vol. 4, no. 3, pp. 459–471.

    Article  CAS  Google Scholar 

  46. Zapata, A., Ultrastructure of elasmobranch lymphoid tissue. 2. Leydig’s and epigonal organs, Dev. Comp. Immunol., 1981, vol. 5, no. 1, pp. 43–52.

    Article  CAS  Google Scholar 

  47. Zapata, A. and Carrato, A., Ultrastructure of elasmobranch and teleost erythrocytes, Acta Zool., 1981, vol. 62, no. 2, pp. 129–135.

    Article  Google Scholar 

  48. FAO Species Identification Sheets for Fishery Purposes. Southern Ocean (CCAMLR Convention Area Fishing Areas 48, 58 and 88), Fischer, W. and Hureau, J.-C., Eds., Rome: FAO, 1985, vol. 1, pp. 233–470.

  49. Scientific Observers Manual (Observation Guidelines and Reference Materials), North Hobart, Australia: Comm. Conserv. Antarct. Mar. Living Resour., 2011.

Download references

ACKNOWLEDGMENTS

The authors are grateful to the crew of the R/V Yantar-35 (OOO Orion, Khabarovsk) for their assistance in collection and transportation of material, as well as to A.M. Orlov, Dr. Biol. Sci., from the Russian Federal Research Institute of Fisheries and Oceanography for his valuable advice and assistance in the literature search.

Funding

The study was supported by the Russian Science Foundation (grant no. 17-74-10203) and was conducted in part within the framework of the Governmental Assignment, Federal Agency of Scientific Organizations (FASO) Russia (topic no. AAAA-A18-118012690123-4).

Author information

Authors and Affiliations

  1. Russian Federal Research Institute of Fisheries and Oceanography, 107140, Moscow, Russia

    I. I. Gordeev

  2. Moscow State University, 119991, Moscow, Russia

    I. I. Gordeev

  3. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Russia

    D. V. Mikryakov, L. V. Balabanova & V. R. Mikryakov

Authors
  1. I. I. Gordeev
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. D. V. Mikryakov
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. L. V. Balabanova
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. V. R. Mikryakov
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to I. I. Gordeev.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by E. Shvetsov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gordeev, I.I., Mikryakov, D.V., Balabanova, L.V. et al. The Cell Composition of the Peripheral Blood and Some Hematopoietic Organs in the Antarctic Starry Skate Amblyraja georgiana (Norman, 1938) (Rajiformes: Rajidae) from the Scotia Sea. Russ J Mar Biol 45, 481–485 (2019). https://doi.org/10.1134/S1063074019060038

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1063074019060038

Keywords: