Skip to main content
Log in

Features of Erythropoiesis of the Mesonephros and Peripheral Blood in Polypterus senegalus (Polypteridae)

  • BICHIRS (POLYPTERIDAE)
  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

The results of determining the concentration of erythropoietin and hemoglobin, morphometric parameters of erythroid elements of the mesonephros and peripheral blood of Polypterus senegalus have been presented. The maturation of erythrocytes in P. senegalus occurs both in the mesonephros and in peripheral blood. The place of synthesis and localization of erythropoietin is the mesonephros. The nuclear-cytoplasmic ratio two times lower compared to teleosts, the volume of cells two times higher and their specific surface area 1.5 times larger, the more pronounced ellipsoidal shape of mature erythrocytes, and the high concentration of hemoglobin indicate that erythrocytes of P. senegalus have a significant potential for gas exchange between the external and internal environment, which is more characteristic of amphibians (Amphibia). The revealed features of erythropoiesis of the mesonephros and peripheral blood of P. senegalus are markers of adaptation to air respiration and periodic terrestrial migrations. These adaptations were formed in the early stages of the evolution of lower vertebrates convergently with lungfish (Dipnoi) and amphibians.

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

Notes

  1. The transportation conditions were in accordance with Directive 2010/63/EU of the European Parliament and of the Council of the European Union of September 22, 2010 “On the protection of animals used for scientific purposes” (https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32-010L0063&from=EN) and Federal Law No. 52-FZ of April 24, 1995 “On the wildlife” (https://docs.cntd.ru/document/9011346).

  2. ARRIVE guidelines (Animal Research: Reporting of in vivo Experiments). https://arriveguidelines.org/

REFERENCES

  1. Allender, M.C. and Fry, M.M., Amphibian hematology, Vet. Clin. North Am. Exot. Anim. Pract., 2008, vol. 11, no. 3, pp. 463–480. https://doi.org/10.1016/j.cvex.2008.03.006

    Article  Google Scholar 

  2. Andreeva, A.Yu., Kukhareva, T.A., and Soldatov, A.A., Proliferative activity of cells of the hematopoietic organs of the sea urchin (Scorpaena porcus L.) during spawning and wintering, Mater. IV nauch.-prakt. molodezhn. konf. “Ekobiologicheskie problemy Azovo-Chernomorskogo regiona i kompleksnoe upravlenie biologicheskimi resursami” (Mater. of the IV Scientific-Practical Youth Conf. “Ecobiological Problems of the Azov-Black Sea Region and Integrated Management of Biological Resources”) (Sevastopol, 2017), Sevastopol: Kolorit, 2018, pp. 76–79.

  3. Andreyeva, A.Y., Kukhareva, T.A., Kladchenko, E.S., and Soldatov, A.A., Comparative characterization of the cellular composition of the black scorpionfish (Scorpaena porcus L.) hematopoietic organs during the spawning season and the period of reproductive inactivity, J. Sib. Fed. Univ. Biol., 2021, vol. 14, no. 2, pp. 195–207. https://doi.org/10.17516/1997-1389-0347

    Article  Google Scholar 

  4. Arikan, H. and Çiçek, K., Haematology of amphibians and reptiles: A review, North-West. J. Zool., 2014, vol. 10, no. 1, pp. 190–209.

    Google Scholar 

  5. Claver, J.A. and Quaglia, A.I.E., Comparative morphology, development, and function of blood cells in nonmammalian vertebrates, J. Exot. Pet Med., 2009, vol. 18, no. 2, pp. 87–97. https://doi.org/10.1053/j.jepm.2009.04.006

    Article  Google Scholar 

  6. Datta, N., Kar, P.K., and Saha, S.K., Circulatory physiology and erythropoiesis in freshwater fish Labeo rohita experimentally parasitized by Argulus bengalensis, J. Appl. Ichthyol., 2022, vol. 38, no. 1, pp. 63–72. https://doi.org/10.1111/jai.14287

    Article  CAS  Google Scholar 

  7. Dantzler, W.H., Transport of Inorganic Ions by Renal Tubules, in Comparative Physiology of the Vertebrate Kidney, New York: Springer, 2016, pp. 81–157. https://doi.org/10.1007/978-1-4939-3734-9_4

  8. de Abreu, Manso P.P., de Brito-Gitirana, L., and Pelajo-Machado, M., Localization of hematopoietic cells in the bullfrog (Lithobates catesbeianus), Cell Tissue Res., 2009, vol. 337, no. 2, pp. 301–312. https://doi.org/10.1007/s00441-009-0803-0

    Article  CAS  Google Scholar 

  9. Delaney, R.G., Shub, C., and Fishman, A.P., Hematologic observations on the aquatic and estivating African lungfish, Protopterus aethiopicus, Copeia, 1976, vol. 1976, no. 3, pp. 423–434. https://doi.org/10.2307/1443355

    Article  Google Scholar 

  10. Du, T.Y., Larsson, H.C.E., and Standen, E.M., Observations of terrestrial locomotion in wild Polypterus senegalus from Lake Albert, Uganda, Afr. J. Aquat. Sci., 2016, vol. 41, no. 1, pp. 67–71. https://doi.org/10.2989/16085914.2015.1125337

    Article  CAS  Google Scholar 

  11. Flerova, E.A., Kletochnaya organizatsiya pochek kostistykh ryb (na primere otryadov Cypriniformes i Perciformes) (Cellular organization of the Kidneys of Teleost Fishes (On the Example of the Orders Cypriniformes and Perciformes)), Yaroslavl: Yaroslav. Gos. Sel’.-Khoz. Akad., 2012.

  12. Gorynya, L.A., Sergeeva, V.V., and Soshina, A.A., A differentiated approach to the diagnosis and treatment of anemia of chronic disease and iron deficiency anemia in the elderly, Vestn. Sev.-Zapad. Gos. Med. Univ., 2012, vol. 4, no. 2, pp. 96–105.

    Google Scholar 

  13. Grushko, M.P., Khvostova, S.M., Kryuchkov, V.N., Features of hematopoiesis in representatives of cartilaginous fish, Vestn. Astrakhan. Gos. Tekhn. Univ. Ser.: Rybn. Khoz-vo, 2012, no. 1, pp. 133–135.

  14. Icardo, J.M., Colvee, E., Kuciel, M., et al., The lungs of Polypterus senegalus and Erpetoichthys calabaricus: Insights into the structure and functional distribution of the pulmonary epithelial cells, J. Morphol., 2017, vol. 278, no. 10, pp. 1321–1332. https://doi.org/10.1002/jmor.20715

    Article  Google Scholar 

  15. Ivanova, N.T., Atlas kletok krovi ryb: sravnitel’naya morfologiya i klassifikatsiya formennykh elementov krovi ryb (Atlas of Fish Blood Cells: Comparative Morphology and Classification of Blood Cells in Fish), Moscow: Leg. i Pishch. Prom-st’, 1983.

  16. Kaufman, Z.S., Embriologiya ryb (Fish Embryology), Moscow: Agropromizdat, 1990.

  17. Kukhareva, T.A. and Soldatov, A.A., Functional morphology of blood erythroid cells in Neogobius melanostomus P. during cell differentiation, J. Evol. Biochem. Physiol., 2016, vol. 52, no. 3, pp. 261–266. https://doi.org/10.1134/S0022093016030091

    Article  Google Scholar 

  18. Kukhareva, T.A., Andreeva, A.Yu., and Soldatov, A.A., Features of the cellular composition of the hematopoietic organs of the scorpionfish (Scorpaena Porcus L.) in winter and summer, Mater. IV nauch.-prakt. molodezhn. konf. “Ekobiologicheskie problemy Azovo-Chernomorskogo regiona i kompleksnoe upravlenie biologicheskimi resursami” (Mater. of the IV Scientific-Practical Youth Conf. “Ecobiological Problems of the Azov-Black Sea Region and Integrated Management of Biological Resources”) (Sevastopol, 2017), Sevastopol: Kolorit, 2018, pp. 108–111.

  19. Lahnsteiner, F., Erythrocyte morphometry in teleost fish – Species-specific, inter-individual and environmental-related differences, Acta Zool., 2021, vol. 102, no. 3, pp. 237–249. https://doi.org/10.1111/azo.12330

    Article  Google Scholar 

  20. Lai, J.C.C., Kakuta, I., Mok, H.O., et al., Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen, J. Exp. Biol., 2006, vol. 209, no. 14, pp. 2734–2738. https://doi.org/10.1242/jeb.02279

    Article  CAS  Google Scholar 

  21. Lutek, K. and Standen, E.M., Increasing viscosity helps explain locomotor control in swimming Polypterus senegalus, Integr. Org. Biol., 2021, vol. 3, no. 1, Article obab024. https://doi.org/10.1093/iob/obab024

    Article  CAS  Google Scholar 

  22. Mineeva, O.V. and Mineev A.K., Features of hematological parameters of the lake frog Rana ridibunda Pallas, 1771 of the Saratov Reservoir, Samarskaya Luka: Probl. Reg. Global. Ekol., 2014, vol. 23, no. 2, pp. 178–184.

    Google Scholar 

  23. Near, T.J., Eytan, R.I., Dornburg, A., et al., Resolution of ray-finned fish phylogeny and timing of diversification, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, no. 34, pp. 13698–13703. https://doi.org/10.1073/pnas.1206625109

    Article  Google Scholar 

  24. Nikinmaa, M., Environmental regulation of the function of circulating erythrocytes via changes in age distribution in teleost fish: Possible mechanisms and significance, Mar. Genomics, 2020, vol. 49, Article 100717. https://doi.org/10.1016/j.margen.2019.100717

    Article  Google Scholar 

  25. Offem, B.O., Ayotunde, E.O., Ikpi, G.U., et al., Influence of seasons on water quality, abundance of fish and plankton species of Ikwori Lake, South-Eastern Nigeria, Fish. Aquac. J., 2011, vol. 2, no. 1, Article FAJ-13.

  26. Roduit N., JMicroVision: Image analysis toolbox for measuring and quantifying components of high-definition images. Version 1.3.1, 2019. https://jmicrovision.github.io. Version 04/2019.

  27. Silkin, Y.A., Silkina, E.N., Chernyaeva, V.N., and Vasilets, V.E., Study of dimensional and morphological characteristics of erythrocytes in some Black Sea fish of different evolution position and ecological specialization, J. Ichthyol., 2019, vol. 59, no. 1, pp. 97–103. https://doi.org/10.1134/S0032945219010168

    Article  Google Scholar 

  28. Silkin, Yu.A., Silkina, E.N., Chernyaeva, V.N., Alekseeva, V.E., Petrova, T.N., Features of hemoglobin content and the number of erythrocytes in blood of Black Sea fish of different evolutionary status and ecological specialization, Sb. tez. nauch.-prakt. shkoly-konf. “Nazemnye i morskie ekosistemy Prichernomor’ya i ikh okhrana” (Coll. of Abstr. of Scientific-Practical School-Conf. “Terrestrial and Marine Ecosystems of the Black Sea Region and Their Protection”) (Novorossiysk, 2018), Sevastopol: Inst. Prirodno-Tekkn. Sist., 2018, pp. 147–148.

    Google Scholar 

  29. Soldatov, A.A., Andreeva, A.Y., Novitskaya, V.N., and Parfenova, I.A., Coupling of membrane and metabolic functions in nucleated erythrocytes of Scorpaena porcus L. under hypoxia in vivo and in vitro, J. Evol. Biochem. Physiol., 2014, vol. 50, no. 5, pp. 409–415. https://doi.org/10.1134/S0022093014050056

    Article  CAS  Google Scholar 

  30. Timakova, T.K., Flerova, E.A., and Zabotkina, E.A., Metody svetovoi i elektronnoi mikroskopii v biologii i veterinarii: uchebno-metodicheskoe posobie (Methods of Light and Electron Microscopy in Biology and Veterinary Science: Study Guide), Yaroslavl: Yaroslavl: Yaroslav. Gos. Sel’.-Khoz. Akad., 2014.

  31. Tusupkaliev, A.B., Dil’magambetov, D.S., Kurmangalieva, S.S., et al., Modul’ “Mochevydelitel’naya sistema”: integrirovannoe uchebnoe posobie (Module “Urinary System”: Integrated Study Guide), Aktobe: Zapadno-Kazakh. Gos. Med. Univ., 2013.

  32. Weber, R.E. and Jensen, F.B., Respiratory Adaptations in Lungfish Blood and Hemoglobin, in The Biology of Lungfishes, Boca Raton: CRC Press, 2010, pp. 283–303. https://doi.org/10.1201/b10357-15

  33. Wright, P.A. and Turko, A.J., Amphibious fishes: Evolution and phenotypic plasticity, J. Exp. Biol., 2016, vol. 219, no. 15, pp. 2245–2259. https://doi.org/10.1242/jeb.126649

    Article  Google Scholar 

  34. Yamaguchi-Yamada, M., Manabe, N., Kiso, M., et al., Dysfunction of erythropoietin-producing interstitial cells in the kidneys of ICR-derived glomerulonephritis (ICGN) mice, J. Vet. Med. Sci., 2005, vol. 67, no. 9, pp. 891–899. https://doi.org/10.1292/jvms.67.891

    Article  Google Scholar 

Download references

Funding

The work was carried out within the framework of the development program of the Yaroslavl State University: P2-GL3-2022 “Molecular genetic research, assessment of the physiological and biochemical status and biotechnological potential of living systems”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. G. Evdokimov.

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 S. Avodkova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Evdokimov, E.G., Flerova, E.A. Features of Erythropoiesis of the Mesonephros and Peripheral Blood in Polypterus senegalus (Polypteridae). J. Ichthyol. 62, 1521–1527 (2022). https://doi.org/10.1134/S003294522206008X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S003294522206008X

Keywords:

Navigation