Skip to main content
SpringerLink
Log in

Leukocytic Indices and Micronucleus in Erythrocytes as Population Markers of the Immune Status of Pelophylax ridibundus (Pallas, 1771) (Amphibia: Ranidae) Living in Various Biotopic Conditions

  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract—A differentiated assessment of blood cells and types of micronuclei in the erythrocytes of marsh frogs (Pelophylax ridibundus) living in reservoirs of the Nizhny Novgorod region was performed. The water reservoirs differ by origin, morphology, and chemical composition. The specific abiotic conditions (a peat bog) and anthropogenic load resulted in the most pronounced change in the leukocyte differential count, corresponding to the neutrophilic type of leukemoid reaction, and in an increased micronucleus fraction in the erythrocytes. A moderate positive correlation between the increase in the number of disintegrated micronuclei and the content (mg/L) of nitrites in the reservoir was found (r = 0.72, p = 0.0179). The complex action of high concentrations of technogenic chemical pollutants (copper, chromium, and oil products) caused the activation of erythropoiesis and humoral immunity, which was confirmed by the nature of the leukemoid reaction of a lymphatic type. The cellular and humoral types of immune reaction aimed at self–foreign molecule differentiation provided stability of the frog ontogenesis under anthropogenic pressure. Integral leukocyte indexes, such as the blood cell indicator, the neutrophil–lymphocyte ratio, the lymphocyte–granulocyte index, and the index of leukocyte shift, which reflect the level of the body’s general reactivity, can be considered as population markers of the immune status of amphibians.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

REFERENCES

  1. Antonini, E. and Brunori, M., Hemoglobin, Annu. Rev. Biochem., 1970, vol. 39, pp. 977–1042.

    Article  CAS  Google Scholar 

  2. Bakka, S.V. and Kiseleva, N.Yu., Osobo okhranyaemye prirodnye territory Nizhegorodsko oblasti (Specially Protected Natural Areas of Nizhny Novgorod Oblast), Nizhny Novgorod, 2008.

    Google Scholar 

  3. Cabagna, M.C., Lajmanovich, R.C., Stringhini, G., Sanchez-Hernandez, J.C., and Peltzer, P.M., Hematological parameters of health status in the common toad Bufo arenarum in agroecosystems of Santa Fe Province, Argentina, Appl. Herpetol., 2005, vol. 2, no. 4, pp. 373–380.

    Article  Google Scholar 

  4. Coico, R., Sunshine, G., and Benjamini, E., Immunology: A Short Course, New York, Wiley, 2003.

    Google Scholar 

  5. Darling, R.C. and Roughton, F.J.W., The effect of methemoglobin on the equilibrium between oxygen and hemoglobin, Am. J. Physiol., 1942, vol. 137, no. 1, pp. 56–68.

    Article  CAS  Google Scholar 

  6. Davis, A.K., Maney, D.L., and Maerz J.C., The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists, Funct. Ecol., 2008, vol. 22, no. 5, pp. 760–772.

    Article  Google Scholar 

  7. Deryagina, V.P. and Reutov, V.P., Ecological aspects of pathophysiology related to nitrate–nitrite pollution of the environment, in Patofiziologiya organov i system: Tipovye patologicheskie protsessy (Pathophysiology of Organs and Systems: Typical Pathological Processes, Abstr. 1st Russian Congress on Pathophysiology), Moscow: Ross. Gos. Med. Univ., 1996, p. 239.

  8. Galaktionov, V.G., Immunologiya (Immunology), Moscow: Akademiya, 2004.

    Google Scholar 

  9. Gelashvili, D.B., Koposov, E.V., and Laptev, L.A., Ekologiya Nizhnego Novgoroda (The Ecology of Nizhny Novgorod), Nizhny Novgorod: 2008.

  10. Glantz, S., Primer of Biostatistics, Moscow: Praktika, 1998.

    Google Scholar 

  11. Jaffe, E.R. and Neumann, G., Hereditary methemoglobinemia, toxic methemoglobinemia and the reduction of methemoglobin, Ann. N.Y. Acad. Sci., 1968, vol. 151, pp. 795–806.

    Article  CAS  Google Scholar 

  12. Johnson, P.T. and La Fonte, B.E., Experimental infection dynamics: Using immunosuppression and in vivo parasite tracking to understand host resistance in an amphibian–trematode system, J. Exp. Biol., 2013, vol. 216, no. 19, pp. 3700–3708.

    Article  Google Scholar 

  13. Kharchenko, E.P., Immune privilege: pathological aspect, Immunologiya, 2009, no. 4, pp. 249–255.

  14. Lebedev, K.A. and Ponyakina, I.D., Immunogramma v klinicheskoi praktike (Immunogram in Clinical Practice), Moscow: Nauka, 1990.

  15. Loginov, V.V., Gelashvili, D.B., Chuprunov, E.V., and Silkin, A.A., Structural-informational analysis of developmental stability in amphibians, Tret’ya konferentsiya gerpetologov Povolzhya: Mat-ly regional’noi konf. (Third Conference of Herpetologists of the Volga Region: Proc. Regional Conf.), Tolyatti: Inst. Ekol. Volzhsk. Basseina, Ross. Akad. Nauk, 2003, pp. 44–47.

  16. Loginov, V.V., Gelashvili, D.B., and Romanova, E.B.,Features of morphometric and morphogenetic indicators in populations of green frogs of the genus Rana in the city Nizhny Novgorod and Nizhni Novgorod oblast, Vestn. Nizhegorod. Univ. im. N.I. Lobachevskogo, 2004, no. 3, pp. 73–79.

  17. Malyutina, T.A., Relationships in the parasite–host system: Biochemical and physiological aspects of adaptation (a retrospective review), Ross. Parazitol. Zh., 2008, no. 1, pp. 24–40.

  18. Manskikh, V.N., On the mechanism of micronuclei formation in somatic cells of tailless amphibians normally and under the effect of N-nitroso-N-methylcarbamide, Bull. Exp. Biol. Med., 2006, vol. 141, no. 2, pp. 254–256.

    Article  CAS  Google Scholar 

  19. Menshikov, V.V., Delektorskaya, L.N., Zolotnitskaya, R.P., Andreeva, Z.M., Ankirskaya, A.S., Balakhovsky, I.S., Belokrinitsky, D.V., Voropaeva, S.D., Garanina, E.N., Lukicheva, T.I., Pletneva, N.G., and Smolyanitsky, A.I., Laboratornye metody issledovaniya v klinike (Laboratory Methods of Research in Clinical Practice), Moscow: Medicina, 1987.

  20. Muravieva, L.V., Tikhomirov, O.A., and Markov, M.V., The formation of aquatic–terrestrial complexes of depleted peat deposits and their classification, Uch. Zap. Kazan. Gos. Univ., Ser. Estestv. Nauki, 2010, vol. 152, no. 4, pp. 102–115.

    Google Scholar 

  21. Mustafina, Zh.G., Kramarenko, Yu.S., and Kobtseva, V.Yu., Integrated hematological indicators in the assessment of immunological reactivity in patients with ophthalmopathology, Klin. Lab. Diagn., 1999, no. 5, pp. 47–48.

  22. Normativy kachestva vody vodnykh ob”ektov rybokhozyaistvennogo znacheniya, v tom chisle normativy predel’no dopustimykh kontsentratsii vrednykh veshchestv v vodnykh ob”ektakh rybokhozyaistvennogo znacheniya (Standards of Water Quality in Fishery Water Bodies, Including Maximum Allowable Concentrations of Harmful Substances. Approved by the Order no. 20 of the Federal Fishery Agency on January 18, 2010), Moscow, 2010.

  23. RD 52.24.643-2002: Metod kompleksnoi otsenki zagryaznennosti poverkhnostnyh vod po gidrokhimicheskim pokazatelyam (RD 52.24.643-2002: Method for Integrated Assessment of the Degree of Impurity of Surface Waters by Hydrochemical Indicators), St. Petersburg: Gidrometeoizdat, 2003.

  24. Romanova, E.B., Fadeeva, G.A., Vershinina, K.S., and Nikolaev, V.Yu., Leukogram changes in marsh frogs (Pelophylax ridibundus Pallas, 1771) with helminthiases, Vestn. Nizhegorod. Univ. im. N.I. Lobachevskogo, 2013, no. 5, pp. 141–147.

  25. Shevkoplyas, V.N. and Lopatin, V.G., The influence of helminthiases on the course of immunological processes in animals, Ross. Parazitol. Zh., 2008, no. 4, pp. 94–101.

  26. Shitikov, V.K. and Rozenberg, G.S., Randomization and Bootstrap: Statistical Analysis in Biology and Ecology Using R, Tolyatti: Kassandra, 2014.

  27. Tkachenko, Ye.A. and Derkho, M.A., Leukocyte indices in mice after experimental cadmium poisoning, Izv. Orenburg. Gos. Agr. Univ., 2014, no. 3, pp. 81–83.

  28. Zhuleva, L.Yu. and Dubinin, N.P., Using the micronuclear test for assessing ecological situation in districts of Astrakhan oblast, Genetika, 1994, vol. 30, no. 7, pp. 999–1004.

    PubMed  Google Scholar 

  29. Zimmerman, L.M., Vogel, L.A., and Bowden, R.M., Understanding the vertebrate immune system: Insights from the reptilian perspective, J. Exp. Biol., 2010, vol. 213, no. 5, pp. 661–671.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lobachevskii State University of Nizhny Novgorod, 603950, Nizhny Novgorod, Russia

    E. B. Romanova, K. V. Shapovalova, E. S. Ryabinina & D. B. Gelashvili

Authors
  1. E. B. Romanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. V. Shapovalova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. S. Ryabinina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. B. Gelashvili
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. B. Romanova.

Ethics declarations

Conflict of interest. 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 I. Shipounova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romanova, E.B., Shapovalova, K.V., Ryabinina, E.S. et al. Leukocytic Indices and Micronucleus in Erythrocytes as Population Markers of the Immune Status of Pelophylax ridibundus (Pallas, 1771) (Amphibia: Ranidae) Living in Various Biotopic Conditions. Biol Bull Russ Acad Sci 46, 1230–1238 (2019). https://doi.org/10.1134/S1062359019100273

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359019100273

Search

Navigation