Effects of Altitude and Temperature on Erythrocyte Morphology of Emys orbicularis (Linnaeus, 1758) and Mauremys rivulata (Valenciennes, 1833)
Year 2021,
Volume: 5 Issue: 1, 24 - 28, 30.06.2021
Yusuf Bayrakcı
,
Melodi Yenmiş
,
Ahmet Mermer
,
Varol Tok
,
Dinçer Ayaz
Abstract
The decrease in erythrocyte size of animals live at high altitudes yields an evolutionary advantage to survive by providing adaptation to colder temperatures and low partial oxygen pressures. We examined the effect of geographical changes on the erythrocyte morphology of two terrapins, Emys orbicularis and Mauremys rivulata, and analyzed whether such erythrocyte characteristics as size and volume changed at high altitudes and different temperatures. We found out that the erythrocyte characteristics varied both within and between the populations. They varied depending on altitude for E. orbicularis and on temperature for M. rivulata. However, the erythrocyte characteristics were not correlated with the environmental parameters, except between sunshine duration and erythrocyte length, size, and nucleus volume for E. orbicularis.
Supporting Institution
TÜBİTAK
Thanks
This study was supported by TUBITAK (The Scientific and Technical Research Council of Turkey) [Project No: 110T927]. We would like to thank Dr. Hasan Serdar MUTLU and Oğuzkan CUMHURIYET for their contributions to field studies.
References
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- Arizza, V., Russo, D., Marrone, F., Sacco, F., & Arculeo. M. (2014). Morphological characterization of the blood cells in the endangered Sicilian endemic pond turtle, Emys trinacris (Testudines: Emydidae). Italian Journal of Zoology, 1–10. https://doi.org/10.1080/11250003.2014.938371
- Baraquet, M., Grenat, P.R., Salas, N.E., & Martino, A.L. (2013). Intraspecific variation in erythrocyte sizes among populations of Hypsiboas cordobae (Anura, Hylidae). Acta Herpetologica, 8, 93 97. https://doi.org/10.13128/Acta_Herpetol-12954
- Bulté, G., & Blouin-Demers, G. (2010). Estimating the energetic significance of basking behaviour in a temperate-zone turtle. Ecoscience, 17(4), 387-393. https://doi.org/10.2980/17-4-3377
- Çiçek, K., Arıkan, H., & Ayaz, D. (2015). Blood Cells Morphology and Erythrocytes Count of Two Freshwater Turtles, Emys orbicularis and Mauremys rivulata, from Turkey. Ecologia Balkanica, 7(1), 21-27.
- Dessauer, H.C. (1970). Blood chemistry of reptiles: physiological and evolutionary aspects. Biology of the Reptilia, 3, 1 72.
- Hammer, Ø., Harper, D. A., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia electronica, 4(1), 9.
- Hartman, F.A., & Lessler, M.A. (1964). Erythrocyte measurements in fishes amphibia, and reptiles. The Biological Bulletin, 126(1), 83-88.
- Jackson, D.C. (2002). Hibernating without oxygen: physiological adaptations of the painted turtle. Journal of Physiology, 543, 731 737.
- Jacobson, E.R. (2007). Infectious diseases and pathology of reptiles. Boca Raton, Florida, CRC Press, 716 pp.
- Javanbakht, H., Vaissi, S., & Parto, P. (2013). The morphological characterization of the blood cells in the three species of turtle and tortoise in Iran. Research in Zoology, 3, 38 44. https://doi.org/10.5923/j.zoology.20130301.06
- Litzgus, J.D., & Hopkins, W.A., (2003). Effect of temperature on metabolic rate of the mud turtle (Kinosternon subrubrum). Journal of Thermal Biology, 28, 595- 600. https://doi.org/10.1016/j.jtherbio.2003.08.005
- Lu, S., Xin, Y., Tang, X., Yue, F., Wang, H., Bai, Y., & Chen, Q. (2015). Differences in hematological traits between high-and low-altitude lizards (genus Phrynocephalus). PLoS One, 10, e0125751. https://doi.org/10.1371/journal.pone.0125751
- Lutz, P.L., & Kabler, S. (1997). Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Research, 769, 281 286. https://doi.org/10.1016/S0006-8993(97)00719-1
- Metin, K., Türkozan, O., Kargın, F., Basumoglu, Y.K., Taşkavak, E., & Koca, S. (2006). Blood cell morphology and plasma biochemistry of the captive European pond turtle Emys orbicularis. Acta Veterinaria Brno, 75(1), 49-55. https://doi.org/10.2754/avb200675010049
- Moye Jr, R.J., Washburn, K.W., & Huston, T.M. (1969). Effects of environmental temperature on erythrocyte numbers and size. Poultry science, 48(5), 1683-1686. https://doi.org/10.3382/ps.0481683
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- Ruiz, G., Rosenmann, M., & Nuñez, H. (1993). Blood values in South American lizards from high and low altitudes. Comparative Biochemistry & Physiology, 106, 713 718. https://doi.org/10.1016/0300-9629(93)90386-I
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- Setlalekgomo, M.R., Winter, P.E.D., & Els, S.F., (2012). The metabolic adjustments of the angulate tortoise (Chersina angulata) to seasonal changes in temperature and photoperiod. Journal of Applied Sciences Research, 8, 1211-1218.
- Stacy, N.I., Alleman, A.R., & Sayler, K.A. (2011). Diagnostic haematology of reptiles. Clinics in Laboratory Medicine, 31, 87-108. https://doi.org/10.1016/j.cll.2010.10.006
- Storz, J.F., & Moriyama, H. (2008). Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Altitude Medicine & Biology, 9, 148 157. https://doi.org/10.1089/ham.2007.1079
- Storz, J.F., Scott, G.R., & Cheviron, Z.A. (2010). Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. Journal of Experimental Biology, 213, 4125 4136. https://doi.org/10.1242/jeb.048181
- Su, Y., Li, D., Gaur, U., Chen, B., Zhao, X., Wang, Y., & Zhu, Q. (2018). The comparison of blood characteristics in low-and high-altitude chickens. Italian Journal of Animal Science, 17, 195 201. https://doi.org/10.1080/1828051X.2017.1355272
- Tosunoğlu, M., Yılmaz, N., & Gül, C. (2011). Effects of varying ecological conditions on the blood parameters of freshwater turtles in Çanakkale (Turkey). Ekoloji, 20 (78), 7-12. https://doi.org/10.5053/ekoloji.2011.782
- Uca, O., Arıkan, H., & Çiçek, K. (2017). Blood cell morphology of Turkish gekkonid lizards. Herpetozoa, 30, 29 37.
- Vinegar, A., & Hillyard, S.D. (1972). The effects of altitude on oxygen-binding parameters of the blood of the iguanid lizards, Sceloporus jarrovi and Sceloporus occidentalis. Comparative Biochemistry and Physiology Part A: Physiology, 43, 317 320. https://doi.org/10.1016/0300-9629(72)90190-9
- Washburn, K.W., & Huston T.M. (1968). Effect of environmental temperature on iron deficiency anemia in Athens-Canadian randombred. Poultry Science, 47, 1532-1535. https://doi.org/10.3382/ps.0471532
- Weber, R.E. (2007). High-altitude adaptations in vertebrate hemoglobins. Respiratory Physiology & Neurobiology, 158, 132 142. https://doi.org/10.1016/j.resp.2007.05.001
- Yilmaz, N., & Tosunoğlu, M. (2010). Hematology and some plasma biochemistry values of free-living freshwater turtles (Emys orbicularis and Mauremys rivulata) from Turkey. North-Western Journal of Zoology, 6(1), 109-117.
Yükseklik ve Sıcaklığın Emys orbicularis (Linnaeus, 1758) ve Mauremys rivulata (Valenciennes, 1833)’nın Eritrosit Morfolojisi Üzerine Etkisi
Year 2021,
Volume: 5 Issue: 1, 24 - 28, 30.06.2021
Yusuf Bayrakcı
,
Melodi Yenmiş
,
Ahmet Mermer
,
Varol Tok
,
Dinçer Ayaz
Abstract
Yüksek rakımlarda yaşayan hayvanlarda eritrosit boyutlarındaki azalma, düşük sıcaklıklara ve düşük kısmi oksijen basıncına adaptasyon sağlayarak hayatta kalmalarına evrimsel bir avantaj kazandırmaktadır. Coğrafik değişikliklerin eritrosit morfolojisi üzerindeki etkilerini iki tatlısu kaplumbağası türü olan Emys orbicularis ve Mauremys rivulata’da inceledik ve boyut ve hacim gibi eritrosit özelliklerinin yüksek rakım ve farklı sıcaklıklarda değişip değişmediğini analiz ettik. Eritrosit özelliklerinin hem populasyon içerisinde hem de populasyonlar arasında farklılık gösterdiğini belirledik. E. orbicularis için yüksekliğe bağlı olarak, M. rivulata içinse sıcaklığa bağlı olarak değişiklik göstermektedir. Bununla birlikte, E. orbicularis için güneşlenme süresi ile eritrosit uzunluğu, büyüklüğü ve nukleus hacmi arasındaki korelasyon dışında, eritrosit özellikleri ile çevresel parametreler arasında korelasyon görülmemektedir.
References
- Arıkan, H., & Çiçek, K. (2010). Morphology of peripheral blood cells from various species of Turkish Herpetofauna. Acta Herpetologica, 5(2), 179-198. https://doi.org/10.13128/Acta_Herpetol-8526
- Arizza, V., Russo, D., Marrone, F., Sacco, F., & Arculeo. M. (2014). Morphological characterization of the blood cells in the endangered Sicilian endemic pond turtle, Emys trinacris (Testudines: Emydidae). Italian Journal of Zoology, 1–10. https://doi.org/10.1080/11250003.2014.938371
- Baraquet, M., Grenat, P.R., Salas, N.E., & Martino, A.L. (2013). Intraspecific variation in erythrocyte sizes among populations of Hypsiboas cordobae (Anura, Hylidae). Acta Herpetologica, 8, 93 97. https://doi.org/10.13128/Acta_Herpetol-12954
- Bulté, G., & Blouin-Demers, G. (2010). Estimating the energetic significance of basking behaviour in a temperate-zone turtle. Ecoscience, 17(4), 387-393. https://doi.org/10.2980/17-4-3377
- Çiçek, K., Arıkan, H., & Ayaz, D. (2015). Blood Cells Morphology and Erythrocytes Count of Two Freshwater Turtles, Emys orbicularis and Mauremys rivulata, from Turkey. Ecologia Balkanica, 7(1), 21-27.
- Dessauer, H.C. (1970). Blood chemistry of reptiles: physiological and evolutionary aspects. Biology of the Reptilia, 3, 1 72.
- Hammer, Ø., Harper, D. A., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia electronica, 4(1), 9.
- Hartman, F.A., & Lessler, M.A. (1964). Erythrocyte measurements in fishes amphibia, and reptiles. The Biological Bulletin, 126(1), 83-88.
- Jackson, D.C. (2002). Hibernating without oxygen: physiological adaptations of the painted turtle. Journal of Physiology, 543, 731 737.
- Jacobson, E.R. (2007). Infectious diseases and pathology of reptiles. Boca Raton, Florida, CRC Press, 716 pp.
- Javanbakht, H., Vaissi, S., & Parto, P. (2013). The morphological characterization of the blood cells in the three species of turtle and tortoise in Iran. Research in Zoology, 3, 38 44. https://doi.org/10.5923/j.zoology.20130301.06
- Litzgus, J.D., & Hopkins, W.A., (2003). Effect of temperature on metabolic rate of the mud turtle (Kinosternon subrubrum). Journal of Thermal Biology, 28, 595- 600. https://doi.org/10.1016/j.jtherbio.2003.08.005
- Lu, S., Xin, Y., Tang, X., Yue, F., Wang, H., Bai, Y., & Chen, Q. (2015). Differences in hematological traits between high-and low-altitude lizards (genus Phrynocephalus). PLoS One, 10, e0125751. https://doi.org/10.1371/journal.pone.0125751
- Lutz, P.L., & Kabler, S. (1997). Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Research, 769, 281 286. https://doi.org/10.1016/S0006-8993(97)00719-1
- Metin, K., Türkozan, O., Kargın, F., Basumoglu, Y.K., Taşkavak, E., & Koca, S. (2006). Blood cell morphology and plasma biochemistry of the captive European pond turtle Emys orbicularis. Acta Veterinaria Brno, 75(1), 49-55. https://doi.org/10.2754/avb200675010049
- Moye Jr, R.J., Washburn, K.W., & Huston, T.M. (1969). Effects of environmental temperature on erythrocyte numbers and size. Poultry science, 48(5), 1683-1686. https://doi.org/10.3382/ps.0481683
- Ramirez, J.M., Folkow, L.P., & Blix, A.S. (2007), Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annual Review of Physiology, 69, 113 143.
- Ruiz, G., Rosenmann, M., & Nuñez, H. (1993). Blood values in South American lizards from high and low altitudes. Comparative Biochemistry & Physiology, 106, 713 718. https://doi.org/10.1016/0300-9629(93)90386-I
- Samaja, M., Crespi, T., Guazzi, M., & Vandegriff, K.D. (2003). Oxygen transport in blood at high altitude: role of the hemoglobin–oxygen affinity and impact of the phenomena related to hemoglobin allosterism and red cell function. European Journal of Applied Physiology, 90, 351 359. https://doi.org/10.1007/s00421-003-0954-8
- Setlalekgomo, M.R., Winter, P.E.D., & Els, S.F., (2012). The metabolic adjustments of the angulate tortoise (Chersina angulata) to seasonal changes in temperature and photoperiod. Journal of Applied Sciences Research, 8, 1211-1218.
- Stacy, N.I., Alleman, A.R., & Sayler, K.A. (2011). Diagnostic haematology of reptiles. Clinics in Laboratory Medicine, 31, 87-108. https://doi.org/10.1016/j.cll.2010.10.006
- Storz, J.F., & Moriyama, H. (2008). Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Altitude Medicine & Biology, 9, 148 157. https://doi.org/10.1089/ham.2007.1079
- Storz, J.F., Scott, G.R., & Cheviron, Z.A. (2010). Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. Journal of Experimental Biology, 213, 4125 4136. https://doi.org/10.1242/jeb.048181
- Su, Y., Li, D., Gaur, U., Chen, B., Zhao, X., Wang, Y., & Zhu, Q. (2018). The comparison of blood characteristics in low-and high-altitude chickens. Italian Journal of Animal Science, 17, 195 201. https://doi.org/10.1080/1828051X.2017.1355272
- Tosunoğlu, M., Yılmaz, N., & Gül, C. (2011). Effects of varying ecological conditions on the blood parameters of freshwater turtles in Çanakkale (Turkey). Ekoloji, 20 (78), 7-12. https://doi.org/10.5053/ekoloji.2011.782
- Uca, O., Arıkan, H., & Çiçek, K. (2017). Blood cell morphology of Turkish gekkonid lizards. Herpetozoa, 30, 29 37.
- Vinegar, A., & Hillyard, S.D. (1972). The effects of altitude on oxygen-binding parameters of the blood of the iguanid lizards, Sceloporus jarrovi and Sceloporus occidentalis. Comparative Biochemistry and Physiology Part A: Physiology, 43, 317 320. https://doi.org/10.1016/0300-9629(72)90190-9
- Washburn, K.W., & Huston T.M. (1968). Effect of environmental temperature on iron deficiency anemia in Athens-Canadian randombred. Poultry Science, 47, 1532-1535. https://doi.org/10.3382/ps.0471532
- Weber, R.E. (2007). High-altitude adaptations in vertebrate hemoglobins. Respiratory Physiology & Neurobiology, 158, 132 142. https://doi.org/10.1016/j.resp.2007.05.001
- Yilmaz, N., & Tosunoğlu, M. (2010). Hematology and some plasma biochemistry values of free-living freshwater turtles (Emys orbicularis and Mauremys rivulata) from Turkey. North-Western Journal of Zoology, 6(1), 109-117.