Skip to main content
SpringerLink
Log in

Determinations of Erythrocyte Sizes in Adult Pelophylax ridibundus (Amphibia: Anura: Ranidae) Inhabiting Industrial Area in Southern Bulgaria

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

In this study, basic erythrocyte sizes in P. ridibundus individuals inhabiting a polluted area (heavy metals, nitrates, nitrites, and ammonium) in southern Bulgaria were evaluated. The erythrocyte cells’ parameters, erythrocyte length (EL), erythrocyte width (EW), length/width ratio (EL/EW), and erythrocyte size (ES), and nuclear parameters, nucleus length (NL), nucleus width (NW), NL/NW ratio, nucleus size (NS) and NS/ES ratio were either measured or calculated. The data obtained were compared with the data from identical measurements made in frogs inhabiting a reference site. In this study, an authentic reduction was established, of the basic erythrocyte-metric cells (EL, EW, EL/EW ratio, and ES) and nuclear (NL, NW, NL/NW, and NS) parameters in P. ridibundus individuals that inhabit the polluted industrial area east of the city of Plovdiv. In those frogs’ blood, oval and spherical erythrocytes circulate. For the erythrocytes from frogs in the polluted site, a significant reduction was found in the nucleus/cytoplasm ratio. Those changes can be seen as adaptations enlarging the contact surface and the oxygen capacity of the erythrocytes in conditions of hypoxia. The results of our research once again emphasize the importance of hematological investigations and specifically of the blood cell morphology as reliable biomarkers in ecotoxicological research in the field.

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

Similar content being viewed by others

Data Availability

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Addy, K., Green, L., & Herron, E. (2004). pH and alkalinity. University of Rhode Island.

  • Adrian, G. J., Czarnoleski, M., & Angilletta, M. J. (2016). Flies evolved small bodies and cells at high or fluctuating temperatures. Ecology and Evolution, 6, 7991–7996. https://doi.org/10.1002/ece3.2534.

    Article  Google Scholar 

  • Allender, M. C., & Fry, M. M. (2008). Amphibian hematology. Veterinary Clinics of North America, 11, 463–480. https://doi.org/10.1016/j.cvex.2008.03.006.

    Article  Google Scholar 

  • Anderson, H. L., Brodsky, I. E., & Mangalmurti, N. S. (2018). The evolving erythrocyte: Red blood cells as modulators of innate immunity. The Journal of Immunology, 201, 1343–1351. https://doi.org/10.4049/jimmunol.1800565.

    Article  CAS  Google Scholar 

  • Arıkan, H., & Cicek, K. (2010). Morphology of peripheral blood cells from various species of Turkish Herpetofauna. Acta Herpetologica, 5(2), 179–198.

    Google Scholar 

  • Arizza, V., Russo, D., Marrone, F., Sacco, F., & Arculeo, M. (2014). Morphological characterization of the blood cells in the endangered Sicilian endemic pond turtle, (Testudines: Emydidae). Italian Journal of Zoology, 81, 344–353.

    Article  Google Scholar 

  • Arserim, S., & Mermer, A. (2008). Hematology of the Uludağ frog Rana macrocnemis Boulenger, 1885 in Uludağ National Park (Bursa, Turkey). Turkish Journal of Fisheries and Aquatic Sciences, 25(1), 39–46.

    Google Scholar 

  • Atatür, M. K., Arikan, H., & Ģevik, İ. E. (1999). Erythrocyte sizes of some anurans from Turkey. Turkish Journal of Zoology, 23, 111–114.

    Google Scholar 

  • Banbura, J., Banbura, M., Kalinski, A., Skwarska, J., Slomczynski, R., Wawrzyniak, J., & Zielinski, P. (2007). Habitat and year-to-year variation in haemoglobin concentration in nestling blue tits Cyanistes caeruleus. Comparative Biochemistry and Physiology - Part A, 148, 572–577. https://doi.org/10.1016/j.cdpa.2007.07.008.

    Article  Google Scholar 

  • Bannikov, A. G., Darevskii, I. S., Ishtenko, V. G., Rustamov, A. K., & Shterbak, N. N. (1977). A Guide to the Amphibians and Reptiles of the USSR. Prosveshtenie Publishing House (In Russian).

  • Baraquet, M., Salas, N. E., & Martino, A. L. (2013). Variation in the erythrocyte size among larvae, juveniles and adults of Hypsiboas cordobae (Anura, Hylidae). Basic and Applied Herpetology, 28, 137–143.

    Google Scholar 

  • Baskurt, O. K., & Meiselman, H. J. (2003). Blood rheology and hemodynamics. Seminars in Thrombosis and Hemostasis, 29, 435–450. https://doi.org/10.1055/s-2003-44551.

    Article  CAS  Google Scholar 

  • Bearhop, S., Griffiths, R., Orr, K., & Furness, R. W. (1999). Mean corpuscular volume (MCV) as a measure of condition in birds. Ecology Letters, 2, 352–356.

    Article  Google Scholar 

  • Bondarieva, A. A., Bibik, Y. S., Samilo, S. M., & Shabanov, D. A. (2012). Erythrocytes cytogenetic characteristics of green frogs from Siversky Donets centre of Pelophylax esculentus complex diversity. JVN Karazin Kharkiv National University, 15(1008), 116–123 (in Russian).

    Google Scholar 

  • Brodeur, J. C., Bahl, M. F., Natale, G. S., & Poliserpi, M. B. (2020). Biomarker and hematological fieldwork with amphibians: is it necessary to sample all night? Environmental Science and Pollution Research, 27, 17152–17161. https://doi.org/10.1007/s11356-020-08313-2.

    Article  CAS  Google Scholar 

  • Cabagna, M. C., Lajmanovich, R. C., Stringhini, G. A., Sanchez-Hermandes, J. C., & Peltzer, P. M. (2005). Hematological parameters of healt status in the common toad Bufo arenarum in the agroecosystems of Santa Fe province, Argentina. Applied Herpetology, 2, 373–380.

    Article  Google Scholar 

  • Cajaraville, M. P., Bebianno, M. J., Blasco, J., Porte, C., Sarasquete, C., & Viarengo, A. (2000). The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Science of the Total Environment, 247(2–3), 295–311. https://doi.org/10.1016/s0048-9697(99)00499-4.

    Article  CAS  Google Scholar 

  • Camargo, J. A., Alonso, A., & Salamanca, A. (2005). Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere, 58, 1255–1267. https://doi.org/10.1016/j.chemosphere.2004.10.044.

    Article  CAS  Google Scholar 

  • Chien, S. (1987). Red cell deformability and its relevance to blood flow. Annual Review of Physiology, 49, 177–192. https://doi.org/10.1146/annurev.ph.49.030187.001141.

    Article  CAS  Google Scholar 

  • Collins, S. J., & Fahrig, L. (2020). Are macroinvertebrate traits reliable indicators of specific agrichemicals? Ecological Indicators, 111(2020), 105965. https://doi.org/10.1016/j.ecolind.2019.105965.

    Article  CAS  Google Scholar 

  • Corduk, N., Hacioglu-Dogru, N., Gul, C., & Tosunoglu, M. (2018). Monitoring of micronuclei and nuclear abnormalities in Pelophylax ridibundus erythrocytes from the Biga Stream (Canakkale, Turkey). Fresenius Environmental Bulletin, 27(1), 147–153. https://doi.org/10.1007/s10646-010-0531-y.

    Article  CAS  Google Scholar 

  • Czech, H. A., & Parsons, K. C. (2002). Agricultural wetlands and water birds: a review. Waterbirds, 25, 56–65.

    Article  Google Scholar 

  • da Costa Araujo, A. P., Lima, V. S., de Andrade Vieira, J. E., Mesak, C., & Malafaia, G. (2019). First report on the mutagenicity and cytotoxicity of ZnO nanoparticles in reptiles. Chemosphere, 235, 556–564. https://doi.org/10.1016/j.chemosphere.2019.06.164.

    Article  CAS  Google Scholar 

  • Davis, A. K., & Maerz, J. C. (2008a). Sex-related diff erences in hematological stress indices of breeding, paedomorphic mole salamanders. Jourmal of Herpetology, 42, 197–201.

    Article  Google Scholar 

  • Davis, A. K., & Maerz, J. C. (2008b). Comparison of hematological stress indicators in recently captured and captive paedomorphic mole salamanders, Ambystoma talpoideum. Copeia, 3, 613–617.

    Article  Google Scholar 

  • Davis, A. K., Maney, D. L., & Maers, J. C. (2008). The use of leukocyte profiles to measure stress in vertebrates: a review for ecologist. Functional Ecology, 22, 760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x.

    Article  Google Scholar 

  • Davis, A. K., Milanovich, J. R., DeVore, J. L., & Maerz, J. C. (2009). An investigation of factors infl uencing erythrocyte morphology of red-backed salamanders ( Plethodon cinereus ). Animal Biology, 59, 201–209. https://doi.org/10.1163/157075609X437718.

    Article  Google Scholar 

  • de Andrade Vieira, J. E., de Oliveira Ferreira, R., Dos Reis Sampaio, D. M., da Costa Araujo, A. P., & Malafaia, G. (2019). An insight on the mutagenicity and cytotoxicity of zinc oxide nanoparticles in Gallus gallus domesticus (Phasianidae). Chemosphere, 231, 10–19. https://doi.org/10.1016/j.chemosphere.2019.05.111.

    Article  CAS  Google Scholar 

  • de Assis, V. R., Titon, S. C. M., & Gomes, F. R. (2018). Acute stress, steroid plasma levels, and innate immunity in Brazilian toads. General and Comparative Endocrinology, 273, 86–97. https://doi.org/10.1016/j.ygcen.2018.05.008.

  • de Oliveira, J. S. P., Vieira, L. G., Carvalho, W. F., de Souza, M. B., de Lima Rodrigues, A. S., Simoes, K., de Melo de Silva, D., dos Santos, M. J., Luz Hirano, L. Q., Quagliatto Santos, A. L., & Malafaia, G. (2020). Mutagenic, genotoxic and morphotoxic potential of different pesticides in the erythrocytes of Podocnemis expansa neonates. Science of the Total Environment, 140304. https://doi.org/10.1016/j.scitotenv.2020.140304.

  • de Wijer, P., Watt, P. J., & Oldham, R. S. (2003). Amphibian decline and aquatic pollution: Effects of nitrogenous fertiliser on survival and development of larvae of the frog Rana temporaria. Applied Herpetology, 1(1-2), 3–12. https://doi.org/10.1163/157075403766451180.

    Article  Google Scholar 

  • Debey, L. B., & Pyenson, N. D. (2013). Osteological correlates and phylogenetic analysis of deep diving in living and extinct pinnipeds: what good are big eyes? Marine Mammal Science, 29(1), 48–83. https://doi.org/10.1111/j.1748-7692.2011.00545.x.

    Article  Google Scholar 

  • Derot, J., Jamoneau, A., Teichert, N., Rosebery, J., Morin, S., & Laplace-Treyture, C. (2020). Response of phytoplankton traits to environmental variables in French lakes: New perspectives for bioindication. Ecological Indicators, 108(2020), 105659. https://doi.org/10.1016/j.ecolind.2019.105659.

    Article  CAS  Google Scholar 

  • Diana, S. G., & Beasley, V. R. (1998). Amphibian toxicology. In M. J. Lannoo (Ed.), Status and Conservation of Midwestern Amphibians (pp. 266–277). University of Iowa.

  • Earl, J. E., & Whiteman, H. H. (2009). Effects of pulsed nitrate exposure on Amphibian development. Environmental Toxicology and Chemistry, 28(6), 1331–1337. https://doi.org/10.1897/08-325.1.

    Article  CAS  Google Scholar 

  • EC. (2000). https://www.eea.europa.eu/data-and-maps/indicators/use-of-freshwater-resources-3.

  • Edens, L. J., & Levy, D. L. (2014). Size scaling of subcellular organelles and structures in Xenopus laevis and Xenopus tropicalis. In M. Kloc & J. Z. Kubiak (Eds.), Xenopus development (pp. 325–345). Wiley.

  • El Idrissi, Y., Baghdad, B., Saufi, H., El Azzouzi, M., Benchrif, A., Elhasni, S., El Mekkaoui, A., & El Azzouzi, E. (2019). Assessment of trace metal contamination in peri-urban soils in the region of Kenitra – Morocco. Mediteranean. Journal of Chemistry, 8(2), 108–114. https://doi.org/10.13171/mjc8219042505mea.

    Article  Google Scholar 

  • Ferrie, G. M., Alford, V. C., Atkinson, J., Baitchman, E., Barber, D., Blaner, W. S., Crawshaw, G., Daneault, A., Dierenfeld, E., Finke, M., Fleming, G., Gagliardo, R., Hoffman, E. A., Karasov, W., Klasing, K., Koutsos, E., Lankton, J., Lavin, S. R., Lentini, A., Livingston, S., Lock, B., Mason, T., McComb, A., Morris, C., Pessier, A. P., Olea-Popelka, F., Probst, T., Rodriguez, C., Schad, K., Semmen, K., Sincage, J., Stamper, M. A., Steinmetz, J., Sullivan, K., Terrell, S., Wertan, N., Wheaton, C. J., Wilson, B., & Valdes, E. V. (2014). Nutrition and health in amphibian husbandry. Zoo Biology, 33(6), 485–501. https://doi.org/10.1002/zoo.21180.

    Article  Google Scholar 

  • Glomski, C. A., Tamburlin, J., Hard, R., & Chainani, M. (1997). The phylogenetic odyssey of the erythrocyte. IV. The amphibians. Histology and Histopathology, 12, 147–170. https://doi.org/10.14670/HH-12.147.

    Article  CAS  Google Scholar 

  • Gonçalves, M. V., de Campos, C. B. M., Godoy, F. R., Gambale, P. G., Nunes, H. F., Nomura, F., Bastos, R. P., da Cruz, A. D., de Melo, E., & Silva, D. (2019). Assessing genotoxicity and mutagenicity of three common Amphibian species inhabiting agroecosysten. Archives of Environmental Contamination and Toxicology, 77(3), 409–420. https://doi.org/10.1007/s00244-019-00647-4.

    Article  CAS  Google Scholar 

  • Gregory, T. R. (2001). The bigger the C-value, the larger the cell: Genome size and red blood cell size in vertebrates. Blood Cell, Molecules, and Diseases, 27, 830–843. https://doi.org/10.1006/bcmd.2001.0457.

    Article  CAS  Google Scholar 

  • Grenat, P. R., Bionda, C. L., Salas, N. E., & Martino, A. L. (2009). Variation in erythrocyte size between juveniles and adults of Odontophrynus americanus. Amphybia-Reptilia, 30, 141–145. https://doi.org/10.1163/156853809787392667.

    Article  Google Scholar 

  • Gül, Ç., Tosunoǧlu, M., Erdoǧan, D., & Özdamar, D. (2011). Changes in the blood composition of some anurans. Acta Herpetologica, 6(2), 137–147. https://doi.org/10.13128/Acta_Herpetol-9137.

    Article  Google Scholar 

  • Haden, R. (1940). Factors affecting the size and shape of the red cell. In F. R. Moulton (Ed.), Blood, heart and circulation (pp. 27–33). Science Press.

  • Hartman, F., & Lessler, M. (1964). Erythrocyte measurements in Fishes, Amphibians and Reptiles. Biology Bulletin, 126, 83–88.

    Article  Google Scholar 

  • Hedrick, M. S., & Duffield, D. A. (1991). Haematological and rheological characteristics of blood in seven marine mammal species: physiological implications for diving behavior. Journal of Zoology, 225(2), 273–283. https://doi.org/10.1111/j.1469-7998.1991.tb03816.x.

    Article  Google Scholar 

  • Hegde, G., Krishnamurthy, S. V., & Berger, G. (2019). Common frogs response to agrochemicals contamination in coffee plantations, Western Ghats, India. Chemistry and Ecology, 35(5), 397–407. https://doi.org/10.1080/02757540.2019.1584613.

    Article  CAS  Google Scholar 

  • Janiga, M., Haas, M., & Kufelová, M. (2017). Age, sex and seasonal variation in the shape and size of erythrocytes of the alpine accentor, Prunella collaris (Passeriformes: Prunellidae). The European Zoological Journal, 84(1), 583–590. https://doi.org/10.1080/24750263.2017.1403656.

    Article  CAS  Google Scholar 

  • Jensen, F. B. (2009). The role of nitrite in nitric oxide homeostasis: a comparative perspective. Biochimica et Biophysica Acta, 1787, 841–848. https://doi.org/10.1016/j.bbabio.2009.02.010.

    Article  CAS  Google Scholar 

  • Kim, D.-H., Li, B., Si, F., Jude, M., Phillip, J. M., Wirtz, D., & Sun, S. X. (2015). Volume regulation and shape bifurcation in the cell nucleus. Journal of Cell Science, 128, 3375–3385. https://doi.org/10.1242/jcs.166330.

    Article  CAS  Google Scholar 

  • Kozłowski, J., Czarnołeski, M., Francois-Krassowska, A., Maciak, S., & Pis, T. (2010). Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals. Biology Letters, 6, 792–796. https://doi.org/10.1098/rsbl.2010.0288.

    Article  Google Scholar 

  • Lay, P. A., & Baldwin, J. (1999). What determines the size of teleost erythrocytes? correlations with oxygen transport and nuclear volume. Fish Physiology and Biochemistry, 20(1), 31–35. https://doi.org/10.1023/A:1007785202280.

    Article  CAS  Google Scholar 

  • Levy, D. L., & Heald, R. (2016). Biological scaling problems and solutions in Amphibians. Cold Spring Harbor Perspectives in Biology, 8(1), a019166. https://doi.org/10.1101/cshperspect.a019166.

    Article  Google Scholar 

  • Macadangdang, B. R., Oberai, A., Spektor, T., Campos, O. A., Sheng, F., Carey, M. F., Vogelauer, M., & Kurdistani, S. K. (2014). Evolution of histone 2A for chromatin compaction in eukaryotes. Elife, 3, e02792. https://doi.org/10.7554/elife.02792.

    Article  Google Scholar 

  • Маnning, М., & Horton, J. (1982). RES structure and function of the Amphibia. The Reticuloendothelial System: a Comprehensive Treatise. Plenum Press.

  • Medina, M. F., Gonzalez, M. E., Klyver, S. M. R., & Aybar Odstrcil, I. M. (2016). Histopathological and biochemical changes in the liver, kidney, and blood of amphibians intoxicated with cadmium. Turkish Journal of Biology, 40, 229–238. https://doi.org/10.3906/biy-1505-72.

    Article  CAS  Google Scholar 

  • Mijošek, T., Marijić, F. V., Dragun, Z., Ivanković, D., Krasnići, N., Erk, M., Gottstein, S., Lajtner, J., Peric, M. C., & Kepčija, R. M. (2019). Comparison of electrochemically determined metallothionein concentrations in wild freshwater salmon fish and gammarids and their relation to total and cytosolic metal levels. Ecological Indicators, 105, 188–198. https://doi.org/10.1016/ecolind.2019.05.069.

    Article  Google Scholar 

  • Mineeva, O. V., & Mineev, A. K. (2010). Morphology defects in peripheral blood erythrocytes of lake frog Rana ridibunda Pallas, 1771. Bulletins University of Nizhny Novgorod, 2(2), 664–667 (in Russian).

    Google Scholar 

  • Monastersky, R. (2014). Biodiversity: Life - a status report. Nature, 516(7530), 158–161. https://doi.org/10.1038/516158a.

    Article  CAS  Google Scholar 

  • Moreira, L. F. B., Knauth, D. S., & Maltchik, L. (2014). Checklist of amphibians in a rice paddy area in the Uruguayan savanna, southern. Brazilian Check List, 10(5), 1014–1019. https://doi.org/10.15560/10.5.1014.

    Article  Google Scholar 

  • Mueller, R. L. (2015). Genome biology and the evolution of cell size diversity. Cold Spring Harbor Perspectives in Biology, 7(11), a019125. https://doi.org/10.1101/cshperspect.a019125.

    Article  Google Scholar 

  • Nadolski, J., Skwarska, J., Kalinski, A., Banbura, M., Sniegula, R., & Banbura, J. (2006). Blood parameters as consistent predictors of nestling performance in great tits (Parus major) in the wild. Comparative Biochemistry and Physiology - Part A, 143(1), 50–54. https://doi.org/10.1016/j.cbpa.2005.10.021.

    Article  CAS  Google Scholar 

  • Navas, C. A., Gomes, F. R., de Domenico, E. A. (2016). Physiological ecology and conservation of anuran amphibians. In Viera de Andrade, R. C., Bevier, J. E. de Carvalho (Eds.), Amphibian and Reptile Adaptations to the Environment: Interplay Between Physiology and Behavior (pp. 155–189). Londin, New York: Denis CRC Press, Taylor & Francis group.

  • Nicol, S. C., Melrose, W., & Stahel, C. D. (1988). Haematology and metabolism of the blood of the little penguin, Eudyptula minor. Comparative Biochemistry and Physiology Part A, 89(3), 383–386. https://doi.org/10.1016/0300-9629(88)91044-4.

    Article  CAS  Google Scholar 

  • Omelykovets, Y. A., & Berezyuk, M. V. (2009). Research of change of morpho-metrical index of red corpuscles tales Amphibious in different periods of ontogenesis. Zoology, 9, 83–88 (In Russian).

    Google Scholar 

  • Otero, M. A., Pollo, F. E., Grenat, P. R., Salas, N. E., & Martino, A. L. (2018). Differential effects on life history traits and body size of two anuran species inhabiting an environment related to fluorite mine. Ecological Indicators, 93, 36–44. https://doi.org/10.1016/j.ecolind.2018.04.065.

    Article  CAS  Google Scholar 

  • Рavlov, D. N., Romanov, M. G., Vasilev, M. K., & Popov, I. C. (1980). Chemical laboratory methods. Medicine & Physical Culture (in Bulgarian).

  • Piatti, L., Souza, F. L., & Filho, P. L. (2010). Anuran assemblage in a rice field agroecosystem in the Pantanal of central Brazil. Journal of Natural History, 44(19), 1215–1224. https://doi.org/10.1080/00222930903499804.

    Article  Google Scholar 

  • Pollo, F. E., Grenat, P. R., Otero, M. A., Salas, N. E., & Martino, A. L. (2016). Assessment in situ of genotoxicity in tadpoles and adults of frog Hypsiboas cordobae (Barrio 1965) inhabiting aquatic ecosystems associated to fluorite mine. Ecotoxicology and Environmental Safety, 133, 466–474. https://doi.org/10.1016/j.ecoenv.2016.08.003.

    Article  CAS  Google Scholar 

  • Pollo, F. E., Grenat, P. R., Otero, M. A., Babini, S., Salas, N. E., & Martino, A. L. (2019). Evaluation in situ of genotoxic and cytotoxic response in the diploid /polyploid complex Odontophrynus (Anura: Odontophrynidae) inhabiting agroecosystems. Chemosphere, 216, 306–312. https://doi.org/10.1016/j.chemosphere.2018.10.149.

    Article  CAS  Google Scholar 

  • Promislow, D. E. L. (1991). The evolution of mammalian blood parameters: patterns and their interpretation. Physiological Zoology, 64(2), 393–431. https://doi.org/10.1086/physzool.64.2.30158183.

    Article  Google Scholar 

  • Reid, A. J., Carlson, A. K., Creed, I. F., Eliason, E. J., Gell, P. A., Johnson, P. T. J., Kidd, K. A., MacCormack, T. J., Olden, J. D., Ormerod, S. J., Smol, J. P., Taylor, W. W., Tockner, K., Vermaire, J. C., Dudgeon, D., & Cooke, S. J. (2018). Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews of the Cambridge Philosophical Society, 94(3), 849–873. https://doi.org/10.1111/bry.12480.

    Article  Google Scholar 

  • Rouse, J. D., Bishop, C. A., & Struger, J. (1999). Nitrogen pollution: An assessment of its threat to amphibian survival. Environmental Health Perspectives, 107, 799–803. https://doi.org/10.1289/ehp.99107799.

    Article  CAS  Google Scholar 

  • Ruiz, G., Rosenmann, M., & Veloso, A. (1989). Altitudinal distribution and blood values in the toad Bufo spinulosus Wiegmann. Comparative Biochemistry and Physiology Part A, 94, 643–646. https://doi.org/10.1016/0300-9629(89)90609-9.

    Article  CAS  Google Scholar 

  • Salamat, M. A., Vaissi, S., Fathipour, F., Sharifi, M., & Parto, P. (2013). Morphological observations on the erythrocyte and erythrocyte size of some Gecko species, Iran. Global Veterinaria, 11, 248–251. https://doi.org/10.5829/idosi.gv.2013.11.2.75100.

    Article  Google Scholar 

  • Salinas, Z. A., Salas, N. E., Baraquet, M., & Martino, A. L. (2015). Biomarcadores hematológicos del sapo común Bufo (Rhinella) arenarum en ecosistemas alterados de la provincia de Córdoba Hematologic biomarkers of the common toad Bufo arenarum in alteredecosystem of Córdoba province. Acta Toxicológica Argentina, 23(1), 25–35 (In Spanish).

    CAS  Google Scholar 

  • Salinas, Z. A., Baraquet, M., Grenat, P. R., Martino, A. L., & Salas, N. E. (2017). Morphology and size of blood cells of Rhinella arenarum (Hensel, 1867) as environmental health assessment in disturbed aquatic ecosystem from central Argentina. Environmental Science and Pollution Research, 24(32), 24907–24915. https://doi.org/10.1007/s11356-017-0107-y.

    Article  CAS  Google Scholar 

  • Scheffer, M., Van Geest, G. J., Zimmer, K., Jeppesen, E., Sondergaard, M., Butler, M. G., Hanson, M. A., Declerck, S., & De Meester, L. (2006). Small habitat size and isolation can promote species richness: secondorder effects on biodiversity in shallow lakes and ponds. Oikos, 112, 227–231.

    Article  Google Scholar 

  • Schuytema, G. S., & Nebeker, A. V. (1999). Comparative toxicity of ammonium and nitrate compounds to Pacific tree frog and African clawed frog tadpoles. Environmental Toxicology and Chemistry, 18, 2251–2257. https://doi.org/10.1002/etc.5620181019.

    Article  CAS  Google Scholar 

  • Selye, H. (1956). The Stress of Life. McGraw-Hill.

  • Statsoft Inc. (2004). Statistica for Windows (Electronic Version 7.0).  Electronic Statistics Textbook, Tulsa.

  • Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S., Fischman, D. L., & Waller, R. W. (2004). Status and trend of amphibians declines and extinctions worldwide. Science, 306(5702), 1783–1786. https://doi.org/10.1126/science.1103538.

    Article  CAS  Google Scholar 

  • Sutherland, W. J. (2000). The Conservation Handbook: Research, Management and Policy. Blackwell Science.

  • Teixeira, P. C., Dias, D. C., Rocha, G. C., Antonucci, A. M., França, F. M., Marcantonio, A. S., Ranzani-Paiva, M. J. T., & Ferreira, C. M. (2012). Profile of cortisol, glycaemia, and blood parameters of American Bullfrog tadpoles Lithobates catesbeianus exposed to density and hypoxia stressors. Pesquisa Veterinaria Brasileira, 32(Supl 1), 91–98. https://doi.org/10.1590/S0100-736X2012001300016.

    Article  Google Scholar 

  • Thrall, M. A., Baker, D. C., & Lassen, E. D. (2004). Veterinary Hematology and Clinical Chemistry. Iowa State University Press.

  • Uca, O., Arikan, H., & Çiçek, K. (2017). Blood cell morphology of turkish gekkonid lizards (Squamata: Sauria: Gekkonidae, Phyllodactylidae). Herpetozoa, 30(1/2), 29–37.

    Google Scholar 

  • Vinogradov, A. E., & Anatskaya, O. V. (2006). Genome size and metabolic intensity in tetrapods: A tale of two lines. Proceedings of the Royal Society B: Biological Sciences, 273, 27–32.

    Article  Google Scholar 

  • Webster, M., Witkin, K. L., & Cohen-Fix, O. (2009). Sizing up the nucleus: Nuclear shape, size and nuclear-envelope assembly. Journal of Cell Science, 122, 1477–1486. https://doi.org/10.1242/jcs.037333.

    Article  CAS  Google Scholar 

  • Wei, J., Li, Y. Y., Wei, L., Ding, G. H., Fan, X. L., & Lin, Z. H. (2015). Evolution of erythrocyte morphology in amphibians (Amphibia: Anura). Zoologia, 32(5), 360–370. https://doi.org/10.1590/S1984-46702015000500005.

    Article  Google Scholar 

  • Wells, R. M. G., & Baldwin, J. (1990). Oxygen transport potential in tropical reef fish with special reference to blood viscosity and haematocrit. Journal of Experimental Marine Biology and Ecology, 141, 131–142.

    Article  Google Scholar 

  • Wickham, L. L., Elsner, R., White, F. C., & Cornell, L. H. (1989). Blood viscosity in phocid seals: possible adaptations to diving. Journal of Comparative Physiology B, 159(2), 153–158. https://doi.org/10.1007/BF00691735.

    Article  CAS  Google Scholar 

  • Wojtaszek, J., & Adamowicz, A. (2003). Haematology of the fire-bellied toad, Bombina bombina L. Comparative Clinical Pathology, 12, 129–134. https://doi.org/10.1007/s00580-003-0482-2.

    Article  Google Scholar 

  • Woodward, G., Gessner, M. O., Giller, P. S., Gulis, V., Hladyz, S., Lecerf, A., Malmqvist, B., Mckie, B. G., Tiegs, S. D., Cariss, H., Dobson, M., Elosegi, A., Ferreira, V., Graça, M. A. S., Fleituch, T., Lacoursière, J. O., Nistorescu, M., Pozo, J., Risnoveanu, G., Schindler, M., Vadineanu, A., Vought, L. B. M., & Chauvet, E. (2012). Continental-Scale Effects of Nutrient Pollution on Stream Ecosystem Functioning. Science, 336, 1438–1440. https://doi.org/10.1126/science.1219534.

    Article  CAS  Google Scholar 

  • Zhelev, Z. M., Angelov, M. V., & Mollov, I. A. (2006). A study of some metric parameters of the erythrocytes in Rana ridibunda (Amphibia: Anura) derived from an area of highly developed chemical industry. Acta Zoologica Bulgarica, 58(2), 235–244.

    Google Scholar 

  • Zhelev, Z. M., Mehterov, N. H., & Popgeorgiev, G. S. (2016). Seasonal changes of basic erythrocyte-metric parameters in Pelophylax ridibundus (Amphibia: Ranidae) from anthropogenically polluted biotopes in Southern Bulgaria and their role as bioindicators. Ecotoxicology and Environmentsl Safety, 124, 406–417. https://doi.org/10.1016/j.ecoenv.2015.11.011.

    Article  CAS  Google Scholar 

  • Zhelev, Z., Popgeorgiev, G., Ivanov, I., & Boyadzhiev, P. (2017). Changes of erythrocyte-metric parameters in Pelophylax ridibundus (Amphibia: Anura: Ranidae) inhabiting water bodies with different types of anthropogenic pollution in Southern Bulgaria. Environmental Science and Pollution Research, 24(21), 17920–17934. https://doi.org/10.1007/s11356-017-9364-z.

    Article  Google Scholar 

  • Zhelev, Z., Tsonev, C., Georgieva, K., & Arnaudova, D. (2018). Health status of Pelophylax ridibundus (Amphibia: Ranidae) in a rice paddy ecosystem in Southern Bulgaria and its importance in assessing environmental state: Haematological parameters. Environmental Science and Pollution Research, 25(8), 7884–7895. https://doi.org/10.1007/s11356-017-1109-5.

    Article  CAS  Google Scholar 

  • Zhelev, Z. M., Arnaudova, D. N., Popgeorgiev, G. S., & Tsonev, S. V. (2020). In situ assessment of health status and heavy metal bioaccumulation of adult Pelophylax ridibundus (Anura: Ranidae) individuals inhabiting polluted area in southern Bulgaria. Ecological Indicators, 115(2020), 106413. https://doi.org/10.1016/j.ecolind.2020.106413.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the. Plovdiv University Project No. FP17-BF-001 “Evaluation of the anthropogenic stress on the wetlands of Southern Bulgaria.”

Funding

This research was supported by the. Plovdiv University Project No. FP17-BF-001 “Evaluation of the anthropogenic stress on the wetlands of Southern Bulgaria.”

Author information

Authors and Affiliations

  1. Faculty of Biology, Department of Human Anatomy and Physiology, Paisii Hilendarski University of Plovdiv, 24 Tsar Asen Str, 4000, Plovdiv, Bulgaria

    Zhivko M. Zhelev

  2. Faculty of Biology, Department of Zoology, Paisii Hilendarski University of Plovdiv, 24 Tzar Asen Str, 4000, Plovdiv, Bulgaria

    Desislava N. Arnaudova

  3. National Museum of Natural History, Bulgarian Academy of Sciences, 1 “Tsar Osvoboditel” Blvd, 1000, Sofia, Bulgaria

    Georgi S. Popgeorgiev

  4. AgroBioInstitute, 8 “Dragan Tsankov” Blvd, 1164, Sofia, Bulgaria

    Stefan V. Tsonev

Authors
  1. Zhivko M. Zhelev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Desislava N. Arnaudova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Georgi S. Popgeorgiev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan V. Tsonev
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Zh. Zhelev is the leading author and team leader who devised and developed the topics. The Fieldwork: catching of amphibians and morphological analysis were performed by Zh. Zhelev and G Popgeorgiev. The laboratory analyses were performed by Zh. Zhelev, D. Arnaudova and S. Tsonev. The statistical analysis and the interpretation of the results: G. Popgeorgiev, S. Tsonev and Zh. Zhelev. Work with the Geographical Information System (GIS): G. Popgeorgiev. Zh. Zhelev wrote the text of the manuscript.

Corresponding author

Correspondence to Stefan V. Tsonev.

Ethics declarations

Ethics Approval and Consent to Participate

According to clause number 42, clause number 41 and appendix 2 to clause number 41 of the Bulgarian Law on Biological Diversity, capture permits for P. ridibundusare not required for the aims of scientific research. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Consent for Publication

Not applicable

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhelev, Z.M., Arnaudova, D.N., Popgeorgiev, G.S. et al. Determinations of Erythrocyte Sizes in Adult Pelophylax ridibundus (Amphibia: Anura: Ranidae) Inhabiting Industrial Area in Southern Bulgaria. Water Air Soil Pollut 232, 125 (2021). https://doi.org/10.1007/s11270-021-05072-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-05072-9

Keywords

Search

Navigation